DOI: 10.1073/pnas.1407020111. Capsid expansion mechanism of bacteriophage T7 revealed by multistate atomic models derived from cryo-EM reconstructions

Capsid expansion mechanism of bacteriophage T7 revealed by multistate atomic models derived from cryo-EM reconstructions

10.1073/pnas.1407020111

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

Significance T7 phage has been used as a model system to study dsDNA virus capsid assembly and maturation. Yet, atomic capsid models and details of capsid transformations are not elucidated. From our cryo-EM study we have derived near-atomic resolution reconstructions of the DNA-free procapsid, a DNA packaging intermediate, and the DNA-packaged, mature phage capsid. From these structures, we have derived the first near-atomic-level model of T7 capsid maturation. The structural knowledge obtained from this study can serve as a platform for analysis of other dsDNA viruses as well as a platform for the development of molecular tools such as improved phage display systems.

Bibliography

Guo, F., Liu, Z., Fang, P.-A., Zhang, Q., Wright, E. T., Wu, W., Zhang, C., Vago, F., Ren, Y., Jakana, J., Chiu, W., Serwer, P., & Jiang, W. (2014). Capsid expansion mechanism of bacteriophage T7 revealed by multistate atomic models derived from cryo-EM reconstructions. Proceedings of the National Academy of Sciences, 111(43).

Authors 13

Fei Guo (first)
Zheng Liu (additional)
Ping-An Fang (additional)
Qinfen Zhang (additional)
Elena T. Wright (additional)
Weimin Wu (additional)
Ci Zhang (additional)
Frank Vago (additional)
Yue Ren (additional)
Joanita Jakana (additional)
Wah Chiu (additional)
Philip Serwer (additional)
Wen Jiang (additional)

References 68 Referenced 91

DH Chen, , Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc Natl Acad Sci USA 108, 1355–1360 (2011). (10.1073/pnas.1015739108) / Proc Natl Acad Sci USA / Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus by Chen DH (2011)
A Ionel, , Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7. J Biol Chem 286, 234–242 (2011). (10.1074/jbc.M110.187211) / J Biol Chem / Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7 by Ionel A (2011)
W Jiang, , Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Biol 10, 131–135 (2003). (10.1038/nsb891) / Nat Struct Biol / Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions by Jiang W (2003)
ME Cerritelli, JF Conway, N Cheng, BL Trus, AC Steven, Molecular mechanisms in bacteriophage T7 procapsid assembly, maturation, and DNA containment. Adv Protein Chem 64, 301–323 (2003). (10.1016/S0065-3233(03)01008-8) / Adv Protein Chem / Molecular mechanisms in bacteriophage T7 procapsid assembly, maturation, and DNA containment by Cerritelli ME (2003)
JF Conway, , Virus maturation involving large subunit rotations and local refolding. Science 292, 744–748 (2001). (10.1126/science.1058069) / Science / Virus maturation involving large subunit rotations and local refolding by Conway JF (2001)
Y Tao, , Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95, 431–437 (1998). (10.1016/S0092-8674(00)81773-0) / Cell / Assembly of a tailed bacterial virus and its genome release studied in three dimensions by Tao Y (1998)
D Veesler, , Architecture of a dsDNA viral capsid in complex with its maturation protease. Structure 22, 230–237 (2014). (10.1016/j.str.2013.11.007) / Structure / Architecture of a dsDNA viral capsid in complex with its maturation protease by Veesler D (2014)
I Gertsman, , An unexpected twist in viral capsid maturation. Nature 458, 646–650 (2009). (10.1038/nature07686) / Nature / An unexpected twist in viral capsid maturation by Gertsman I (2009)
L Gan, , Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM. Structure 14, 1655–1665 (2006). (10.1016/j.str.2006.09.006) / Structure / Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM by Gan L (2006)
BA Moffatt, JJ Dunn, FW Studier, Nucleotide sequence of the gene for bacteriophage T7 RNA polymerase. J Mol Biol 173, 265–269 (1984). (10.1016/0022-2836(84)90194-3) / J Mol Biol / Nucleotide sequence of the gene for bacteriophage T7 RNA polymerase by Moffatt BA (1984)
A Rosenberg, , T7Select Phage Display System: A powerful new protein display system based on bacteriophage T7. Innovations 6, 1–6 (1996). / Innovations / T7Select Phage Display System: A powerful new protein display system based on bacteriophage T7 by Rosenberg A (1996)
JJ Dunn, FW Studier, Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol 166, 477–535 (1983). (10.1016/S0022-2836(83)80282-4) / J Mol Biol / Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements by Dunn JJ (1983)
A Bertin, M de Frutos, L Letellier, Bacteriophage-host interactions leading to genome internalization. Curr Opin Microbiol 14, 492–496 (2011). (10.1016/j.mib.2011.07.010) / Curr Opin Microbiol / Bacteriophage-host interactions leading to genome internalization by Bertin A (2011)
X Agirrezabala, , Quasi-atomic model of bacteriophage t7 procapsid shell: Insights into the structure and evolution of a basic fold. Structure 15, 461–472 (2007). (10.1016/j.str.2007.03.004) / Structure / Quasi-atomic model of bacteriophage t7 procapsid shell: Insights into the structure and evolution of a basic fold by Agirrezabala X (2007)
ME Cerritelli, FW Studier, Assembly of T7 capsids from independently expressed and purified head protein and scaffolding protein. J Mol Biol 258, 286–298 (1996). (10.1006/jmbi.1996.0250) / J Mol Biol / Assembly of T7 capsids from independently expressed and purified head protein and scaffolding protein by Cerritelli ME (1996)
P Serwer, A metrizamide-impermeable capsid in the DNA packaging pathway of bacteriophage T7. J Mol Biol 138, 65–91 (1980). (10.1016/S0022-2836(80)80005-2) / J Mol Biol / A metrizamide-impermeable capsid in the DNA packaging pathway of bacteriophage T7 by Serwer P (1980)
P Serwer, Buoyant density sedimentation of macromolecules in sodium iothalamate density gradients. J Mol Biol 92, 433–448 (1975). (10.1016/0022-2836(75)90290-9) / J Mol Biol / Buoyant density sedimentation of macromolecules in sodium iothalamate density gradients by Serwer P (1975)
F Guo, , Visualization of uncorrelated, tandem symmetry mismatches in the internal genome packaging apparatus of bacteriophage T7. Proc Natl Acad Sci USA 110, 6811–6816 (2013). (10.1073/pnas.1215563110) / Proc Natl Acad Sci USA / Visualization of uncorrelated, tandem symmetry mismatches in the internal genome packaging apparatus of bacteriophage T7 by Guo F (2013)
H Fujisawa, M Morita, Phage DNA packaging. Genes Cells 2, 537–545 (1997). (10.1046/j.1365-2443.1997.1450343.x) / Genes Cells / Phage DNA packaging by Fujisawa H (1997)
OM Barth, The use of polylysine during negative staining of viral suspensions. J Virol Methods 11, 23–27 (1985). (10.1016/0166-0934(85)90121-1) / J Virol Methods / The use of polylysine during negative staining of viral suspensions by Barth OM (1985)
F Guo, W Jiang, Single particle cryo-electron microscopy and 3-D reconstruction of viruses. Methods Mol Biol 1117, 401–443 (2014). (10.1007/978-1-62703-776-1_19) / Methods Mol Biol / Single particle cryo-electron microscopy and 3-D reconstruction of viruses by Guo F (2014)
SH Scheres, S Chen, Prevention of overfitting in cryo-EM structure determination. Nat Methods 9, 853–854 (2012). (10.1038/nmeth.2115) / Nat Methods / Prevention of overfitting in cryo-EM structure determination by Scheres SH (2012)
R Henderson, , Outcome of the first electron microscopy validation task force meeting. Structure 20, 205–214 (2012). (10.1016/j.str.2011.12.014) / Structure / Outcome of the first electron microscopy validation task force meeting by Henderson R (2012)
PB Rosenthal, R Henderson, Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J Mol Biol 333, 721–745 (2003). (10.1016/j.jmb.2003.07.013) / J Mol Biol / Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy by Rosenthal PB (2003)
LG Trabuco, E Villa, K Mitra, J Frank, K Schulten, Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16, 673–683 (2008). (10.1016/j.str.2008.03.005) / Structure / Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics by Trabuco LG (2008)
MK Pietilä, , Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story. Proc Natl Acad Sci USA 110, 10604–10609 (2013). (10.1073/pnas.1303047110) / Proc Natl Acad Sci USA / Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story by Pietilä MK (2013)
ML Baker, , Validated near-atomic resolution structure of bacteriophage epsilon15 derived from cryo-EM and modeling. Proc Natl Acad Sci USA 110, 12301–6 (2013). (10.1073/pnas.1309947110) / Proc Natl Acad Sci USA / Validated near-atomic resolution structure of bacteriophage epsilon15 derived from cryo-EM and modeling by Baker ML (2013)
C Helgstrand, , The refined structure of a protein catenane: The HK97 bacteriophage capsid at 3.44 A resolution. J Mol Biol 334, 885–899 (2003). (10.1016/j.jmb.2003.09.035) / J Mol Biol / The refined structure of a protein catenane: The HK97 bacteriophage capsid at 3.44 A resolution by Helgstrand C (2003)
WR Wikoff, , Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289, 2129–2133 (2000). (10.1126/science.289.5487.2129) / Science / Topologically linked protein rings in the bacteriophage HK97 capsid by Wikoff WR (2000)
ML Baker, W Jiang, FJ Rixon, W Chiu, Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol 79, 14967–14970 (2005). (10.1128/JVI.79.23.14967-14970.2005) / J Virol / Common ancestry of herpesviruses and tailed DNA bacteriophages by Baker ML (2005)
RK Huang, , The Prohead-I structure of bacteriophage HK97: Implications for scaffold-mediated control of particle assembly and maturation. J Mol Biol 408, 541–554 (2011). (10.1016/j.jmb.2011.01.016) / J Mol Biol / The Prohead-I structure of bacteriophage HK97: Implications for scaffold-mediated control of particle assembly and maturation by Huang RK (2011)
PD Adams, , PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213–221 (2010). (10.1107/S0907444909052925) / Acta Crystallogr D Biol Crystallogr / PHENIX: A comprehensive Python-based system for macromolecular structure solution by Adams PD (2010)
JR Cortines, PR Weigele, EB Gilcrease, SR Casjens, CM Teschke, Decoding bacteriophage P22 assembly: Identification of two charged residues in scaffolding protein responsible for coat protein interaction. Virology 421, 1–11 (2011). (10.1016/j.virol.2011.09.005) / Virology / Decoding bacteriophage P22 assembly: Identification of two charged residues in scaffolding protein responsible for coat protein interaction by Cortines JR (2011)
MC Morais, , Bacteriophage phi29 scaffolding protein gp7 before and after prohead assembly. Nat Struct Biol 10, 572–576 (2003). (10.1038/nsb939) / Nat Struct Biol / Bacteriophage phi29 scaffolding protein gp7 before and after prohead assembly by Morais MC (2003)
Y Sun, , Structure of the coat protein-binding domain of the scaffolding protein from a double-stranded DNA virus. J Mol Biol 297, 1195–1202 (2000). (10.1006/jmbi.2000.3620) / J Mol Biol / Structure of the coat protein-binding domain of the scaffolding protein from a double-stranded DNA virus by Sun Y (2000)
P Serwer, Internal proteins of bacteriophage T7. J Mol Biol 107, 271–291 (1976). (10.1016/S0022-2836(76)80005-8) / J Mol Biol / Internal proteins of bacteriophage T7 by Serwer P (1976)
X Zhang, , A new topology of the HK97-like fold revealed in Bordetella bacteriophage by cryoEM at 3.5 A resolution. eLife 2, e01299 (2013). (10.7554/eLife.01299) / eLife / A new topology of the HK97-like fold revealed in Bordetella bacteriophage by cryoEM at 3.5 A resolution by Zhang X (2013)
G Yu, , Single-step antibody-based affinity cryo-electron microscopy for imaging and structural analysis of macromolecular assemblies. J Struct Biol 187, 1–9 (2014). (10.1016/j.jsb.2014.04.006) / J Struct Biol / Single-step antibody-based affinity cryo-electron microscopy for imaging and structural analysis of macromolecular assemblies by Yu G (2014)
RW Hendrix, RL Duda, Bacteriophage HK97 head assembly: A protein ballet. Adv Virus Res 50, 235–288 (1998). (10.1016/S0065-3527(08)60810-6) / Adv Virus Res / Bacteriophage HK97 head assembly: A protein ballet by Hendrix RW (1998)
S Casjens, J King, P22 morphogenesis. I: Catalytic scaffolding protein in capsid assembly. J Supramol Struct 2, 202–224 (1974). (10.1002/jss.400020215) / J Supramol Struct / P22 morphogenesis. I: Catalytic scaffolding protein in capsid assembly by Casjens S (1974)
AC Steven, AC Bauer, ME Bisher, FA Robey, LW Black, The maturation-dependent conformational change of phage T4 capsid involves the translocation of specific epitopes between the inner and the outer capsid surfaces. J Struct Biol 106, 221–236 (1991). (10.1016/1047-8477(91)90072-5) / J Struct Biol / The maturation-dependent conformational change of phage T4 capsid involves the translocation of specific epitopes between the inner and the outer capsid surfaces by Steven AC (1991)
F Sonntag, S Bleker, B Leuchs, R Fischer, JA Kleinschmidt, Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus. J Virol 80, 11040–11054 (2006). (10.1128/JVI.01056-06) / J Virol / Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus by Sonntag F (2006)
S Kronenberg, B Böttcher, CW von der Lieth, S Bleker, JA Kleinschmidt, A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J Virol 79, 5296–5303 (2005). (10.1128/JVI.79.9.5296-5303.2005) / J Virol / A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini by Kronenberg S (2005)
MA Jiménez-Clavero, E Escribano-Romero, AJ Douglas, V Ley, The N-terminal region of the VP1 protein of swine vesicular disease virus contains a neutralization site that arises upon cell attachment and is involved in viral entry. J Virol 75, 1044–1047 (2001). (10.1128/JVI.75.2.1044-1047.2001) / J Virol / The N-terminal region of the VP1 protein of swine vesicular disease virus contains a neutralization site that arises upon cell attachment and is involved in viral entry by Jiménez-Clavero MA (2001)
L Qin, A Fokine, E O’Donnell, VB Rao, MG Rossmann, Structure of the small outer capsid protein, Soc: A clamp for stabilizing capsids of T4-like phages. J Mol Biol 395, 728–741 (2010). (10.1016/j.jmb.2009.10.007) / J Mol Biol / Structure of the small outer capsid protein, Soc: A clamp for stabilizing capsids of T4-like phages by Qin L (2010)
A Fokine, , Molecular architecture of the prolate head of bacteriophage T4. Proc Natl Acad Sci USA 101, 6003–6008 (2004). (10.1073/pnas.0400444101) / Proc Natl Acad Sci USA / Molecular architecture of the prolate head of bacteriophage T4 by Fokine A (2004)
GC Lander, , Bacteriophage lambda stabilization by auxiliary protein gpD: Timing, location, and mechanism of attachment determined by cryo-EM. Structure 16, 1399–1406 (2008). (10.1016/j.str.2008.05.016) / Structure / Bacteriophage lambda stabilization by auxiliary protein gpD: Timing, location, and mechanism of attachment determined by cryo-EM by Lander GC (2008)
B Koskella, MA Brockhurst, Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 38, 916–931 (2014). (10.1111/1574-6976.12072) / FEMS Microbiol Rev / Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities by Koskella B (2014)
AM Kropinski, , The genome of epsilon15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage. Virology 369, 234–244 (2007). (10.1016/j.virol.2007.07.027) / Virology / The genome of epsilon15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage by Kropinski AM (2007)
ES Miller, , Bacteriophage T4 genome. Microbiol Mol Biol Rev 67, 86–156 (2003). (10.1128/MMBR.67.1.86-156.2003) / Microbiol Mol Biol Rev / Bacteriophage T4 genome by Miller ES (2003)
C Vander Byl, AM Kropinski, Sequence of the genome of Salmonella bacteriophage P22. J Bacteriol 182, 6472–6481 (2000). (10.1128/JB.182.22.6472-6481.2000) / J Bacteriol / Sequence of the genome of Salmonella bacteriophage P22 by Vander Byl C (2000)
RJ Juhala, , Genomic sequences of bacteriophages HK97 and HK022: Pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299, 27–51 (2000). (10.1006/jmbi.2000.3729) / J Mol Biol / Genomic sequences of bacteriophages HK97 and HK022: Pervasive genetic mosaicism in the lambdoid bacteriophages by Juhala RJ (2000)
BA Duerkop KL Palmer MJ Horsburgh Enterococcal bacteriophages and genome defense. Enterococci: From Commensals to Leading Causes of Drug Resistant Infection eds Gilmore MS Clewell DB Ike Y Shankar N (Massachusetts Eye and Ear Infirmary Boston). (2014).
FJ Mojica, C Díez-Villaseñor, E Soria, G Juez, Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol Microbiol 36, 244–246 (2000). (10.1046/j.1365-2958.2000.01838.x) / Mol Microbiol / Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria by Mojica FJ (2000)
RL Duda, , Structure and energetics of encapsidated DNA in bacteriophage HK97 studied by scanning calorimetry and cryo-electron microscopy. J Mol Biol 391, 471–483 (2009). (10.1016/j.jmb.2009.06.035) / J Mol Biol / Structure and energetics of encapsidated DNA in bacteriophage HK97 studied by scanning calorimetry and cryo-electron microscopy by Duda RL (2009)
G Effantin, P Boulanger, E Neumann, L Letellier, JF Conway, Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J Mol Biol 361, 993–1002 (2006). (10.1016/j.jmb.2006.06.081) / J Mol Biol / Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships by Effantin G (2006)
DE Smith, , The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature 413, 748–752 (2001). (10.1038/35099581) / Nature / The bacteriophage straight phi29 portal motor can package DNA against a large internal force by Smith DE (2001)
T Kivioja, J Ravantti, A Verkhovsky, E Ukkonen, D Bamford, Local average intensity-based method for identifying spherical particles in electron micrographs. J Struct Biol 131, 126–134 (2000). (10.1006/jsbi.2000.4279) / J Struct Biol / Local average intensity-based method for identifying spherical particles in electron micrographs by Kivioja T (2000)
SJ Ludtke, PR Baldwin, W Chiu, EMAN: Semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128, 82–97 (1999). (10.1006/jsbi.1999.4174) / J Struct Biol / EMAN: Semiautomated software for high-resolution single-particle reconstructions by Ludtke SJ (1999)
W Jiang, F Guo, Z Liu, A graph theory method for determination of cryo-EM image focuses. J Struct Biol 180, 343–351 (2012). (10.1016/j.jsb.2012.07.005) / J Struct Biol / A graph theory method for determination of cryo-EM image focuses by Jiang W (2012)
C Yang, , Estimating contrast transfer function and associated parameters by constrained non-linear optimization. J Microsc 233, 391–403 (2009). (10.1111/j.1365-2818.2009.03137.x) / J Microsc / Estimating contrast transfer function and associated parameters by constrained non-linear optimization by Yang C (2009)
X Yan, KA Dryden, J Tang, TS Baker, Ab initio random model method facilitates 3D reconstruction of icosahedral particles. J Struct Biol 157, 211–225 (2007). (10.1016/j.jsb.2006.07.013) / J Struct Biol / Ab initio random model method facilitates 3D reconstruction of icosahedral particles by Yan X (2007)
X Liu, W Jiang, J Jakana, W Chiu, Averaging tens to hundreds of icosahedral particle images to resolve protein secondary structure elements using a Multi-Path Simulated Annealing optimization algorithm. J Struct Biol 160, 11–27 (2007). (10.1016/j.jsb.2007.06.009) / J Struct Biol / Averaging tens to hundreds of icosahedral particle images to resolve protein secondary structure elements using a Multi-Path Simulated Annealing optimization algorithm by Liu X (2007)
G Tang, , EMAN2: An extensible image processing suite for electron microscopy. J Struct Biol 157, 38–46 (2007). (10.1016/j.jsb.2006.05.009) / J Struct Biol / EMAN2: An extensible image processing suite for electron microscopy by Tang G (2007)
P Emsley, K Cowtan, Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126–2132 (2004). (10.1107/S0907444904019158) / Acta Crystallogr D Biol Crystallogr / Coot: Model-building tools for molecular graphics by Emsley P (2004)
EF Pettersen, , UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25, 1605–1612 (2004). (10.1002/jcc.20084) / J Comput Chem / UCSF Chimera—a visualization system for exploratory research and analysis by Pettersen EF (2004)
; Collaborative Computational Project, Number 4, The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760–763 (1994). (10.1107/S0907444994003112) / Acta Crystallogr D Biol Crystallogr / The CCP4 suite: Programs for protein crystallography by Collaborative Computational Project, Number 4 (1994)
VB Chen, , MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66, 12–21 (2010). (10.1107/S0907444909042073) / Acta Crystallogr D Biol Crystallogr / MolProbity: All-atom structure validation for macromolecular crystallography by Chen VB (2010)

Dates

Type	When
Created	10 years, 10 months ago (Oct. 14, 2014, midnight)
Deposited	3 years, 3 months ago (June 7, 2022, 7:51 a.m.)
Indexed	55 minutes ago (Sept. 7, 2025, 2:03 p.m.)
Issued	10 years, 10 months ago (Oct. 13, 2014)
Published	10 years, 10 months ago (Oct. 13, 2014)
Published Online	10 years, 10 months ago (Oct. 13, 2014)
Published Print	10 years, 10 months ago (Oct. 28, 2014)

Funders 0

None

BibTeX

@article{Guo_2014, title={Capsid expansion mechanism of bacteriophage T7 revealed by multistate atomic models derived from cryo-EM reconstructions}, volume={111}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1407020111}, DOI={10.1073/pnas.1407020111}, number={43}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Guo, Fei and Liu, Zheng and Fang, Ping-An and Zhang, Qinfen and Wright, Elena T. and Wu, Weimin and Zhang, Ci and Vago, Frank and Ren, Yue and Jakana, Joanita and Chiu, Wah and Serwer, Philip and Jiang, Wen}, year={2014}, month=oct }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        9,
        7
      ]
    ],
    "date-time": "2025-09-07T18:03:14Z",
    "timestamp": 1757268194566
  },
  "reference-count": 68,
  "publisher": "Proceedings of the National Academy of Sciences",
  "issue": "43",
  "content-domain": {
    "domain": [
      "www.pnas.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2014,
        10,
        28
      ]
    ]
  },
  "abstract": "<jats:title>Significance</jats:title>\n          <jats:p>\n            T7 phage has been used as a model system to study dsDNA virus capsid assembly and maturation. Yet, atomic capsid models and details of capsid transformations are not elucidated. From our cryo-EM study we have derived near-atomic resolution\n            <jats:italic>reconstructions</jats:italic>\n            of the DNA-free procapsid, a DNA packaging intermediate, and the DNA-packaged, mature phage capsid. From these structures, we have derived the first near-atomic-level model of T7 capsid maturation. The structural knowledge obtained from this study can serve as a platform for analysis of other dsDNA viruses as well as a platform for the development of molecular tools such as improved phage display systems.\n          </jats:p>",
  "DOI": "10.1073/pnas.1407020111",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2014,
        10,
        14
      ]
    ],
    "date-time": "2014-10-14T04:00:15Z",
    "timestamp": 1413259215000
  },
  "update-policy": "http://dx.doi.org/10.1073/pnas.cm10313",
  "source": "Crossref",
  "is-referenced-by-count": 91,
  "title": "Capsid expansion mechanism of bacteriophage T7 revealed by multistate atomic models derived from cryo-EM reconstructions",
  "prefix": "10.1073",
  "volume": "111",
  "author": [
    {
      "given": "Fei",
      "family": "Guo",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Markey Center for Structural Biology, Department of Biological Sciences, Purdue University, West Lafayette, IN 47907;"
        }
      ]
    },
    {
      "given": "Zheng",
      "family": "Liu",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Markey Center for Structural Biology, Department of Biological Sciences, Purdue University, West Lafayette, IN 47907;"
        }
      ]
    },
    {
      "given": "Ping-An",
      "family": "Fang",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Markey Center for Structural Biology, Department of Biological Sciences, Purdue University, West Lafayette, IN 47907;"
        }
      ]
    },
    {
      "given": "Qinfen",
      "family": "Zhang",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China;"
        },
        {
          "name": "National Center for Macromolecular Imaging, Verna and Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX 77030; and"
        }
      ]
    },
    {
      "given": "Elena T.",
      "family": "Wright",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry, The University of Texas Health Science Center, San Antonio, TX 78229"
        }
      ]
    },
    {
      "given": "Weimin",
      "family": "Wu",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Markey Center for Structural Biology, Department of Biological Sciences, Purdue University, West Lafayette, IN 47907;"
        }
      ]
    },
    {
      "given": "Ci",
      "family": "Zhang",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Markey Center for Structural Biology, Department of Biological Sciences, Purdue University, West Lafayette, IN 47907;"
        }
      ]
    },
    {
      "given": "Frank",
      "family": "Vago",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Markey Center for Structural Biology, Department of Biological Sciences, Purdue University, West Lafayette, IN 47907;"
        }
      ]
    },
    {
      "given": "Yue",
      "family": "Ren",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Markey Center for Structural Biology, Department of Biological Sciences, Purdue University, West Lafayette, IN 47907;"
        }
      ]
    },
    {
      "given": "Joanita",
      "family": "Jakana",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "National Center for Macromolecular Imaging, Verna and Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX 77030; and"
        }
      ]
    },
    {
      "given": "Wah",
      "family": "Chiu",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "National Center for Macromolecular Imaging, Verna and Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX 77030; and"
        }
      ]
    },
    {
      "given": "Philip",
      "family": "Serwer",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry, The University of Texas Health Science Center, San Antonio, TX 78229"
        }
      ]
    },
    {
      "given": "Wen",
      "family": "Jiang",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Markey Center for Structural Biology, Department of Biological Sciences, Purdue University, West Lafayette, IN 47907;"
        }
      ]
    }
  ],
  "member": "341",
  "published-online": {
    "date-parts": [
      [
        2014,
        10,
        13
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_3_4_1_2",
      "doi-asserted-by": "crossref",
      "first-page": "1355",
      "DOI": "10.1073/pnas.1015739108",
      "article-title": "Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus",
      "volume": "108",
      "author": "Chen DH",
      "year": "2011",
      "unstructured": "DH Chen, , Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc Natl Acad Sci USA 108, 1355\u20131360 (2011).",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "e_1_3_4_2_2",
      "doi-asserted-by": "crossref",
      "first-page": "234",
      "DOI": "10.1074/jbc.M110.187211",
      "article-title": "Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7",
      "volume": "286",
      "author": "Ionel A",
      "year": "2011",
      "unstructured": "A Ionel, , Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7. J Biol Chem 286, 234\u2013242 (2011).",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "e_1_3_4_3_2",
      "doi-asserted-by": "crossref",
      "first-page": "131",
      "DOI": "10.1038/nsb891",
      "article-title": "Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions",
      "volume": "10",
      "author": "Jiang W",
      "year": "2003",
      "unstructured": "W Jiang, , Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Biol 10, 131\u2013135 (2003).",
      "journal-title": "Nat Struct Biol"
    },
    {
      "key": "e_1_3_4_4_2",
      "doi-asserted-by": "crossref",
      "first-page": "301",
      "DOI": "10.1016/S0065-3233(03)01008-8",
      "article-title": "Molecular mechanisms in bacteriophage T7 procapsid assembly, maturation, and DNA containment",
      "volume": "64",
      "author": "Cerritelli ME",
      "year": "2003",
      "unstructured": "ME Cerritelli, JF Conway, N Cheng, BL Trus, AC Steven, Molecular mechanisms in bacteriophage T7 procapsid assembly, maturation, and DNA containment. Adv Protein Chem 64, 301\u2013323 (2003).",
      "journal-title": "Adv Protein Chem"
    },
    {
      "key": "e_1_3_4_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "744",
      "DOI": "10.1126/science.1058069",
      "article-title": "Virus maturation involving large subunit rotations and local refolding",
      "volume": "292",
      "author": "Conway JF",
      "year": "2001",
      "unstructured": "JF Conway, , Virus maturation involving large subunit rotations and local refolding. Science 292, 744\u2013748 (2001).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_6_2",
      "doi-asserted-by": "crossref",
      "first-page": "431",
      "DOI": "10.1016/S0092-8674(00)81773-0",
      "article-title": "Assembly of a tailed bacterial virus and its genome release studied in three dimensions",
      "volume": "95",
      "author": "Tao Y",
      "year": "1998",
      "unstructured": "Y Tao, , Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95, 431\u2013437 (1998).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_7_2",
      "doi-asserted-by": "crossref",
      "first-page": "230",
      "DOI": "10.1016/j.str.2013.11.007",
      "article-title": "Architecture of a dsDNA viral capsid in complex with its maturation protease",
      "volume": "22",
      "author": "Veesler D",
      "year": "2014",
      "unstructured": "D Veesler, , Architecture of a dsDNA viral capsid in complex with its maturation protease. Structure 22, 230\u2013237 (2014).",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_4_8_2",
      "doi-asserted-by": "crossref",
      "first-page": "646",
      "DOI": "10.1038/nature07686",
      "article-title": "An unexpected twist in viral capsid maturation",
      "volume": "458",
      "author": "Gertsman I",
      "year": "2009",
      "unstructured": "I Gertsman, , An unexpected twist in viral capsid maturation. Nature 458, 646\u2013650 (2009).",
      "journal-title": "Nature"
    },
    {
      "key": "e_1_3_4_9_2",
      "doi-asserted-by": "crossref",
      "first-page": "1655",
      "DOI": "10.1016/j.str.2006.09.006",
      "article-title": "Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM",
      "volume": "14",
      "author": "Gan L",
      "year": "2006",
      "unstructured": "L Gan, , Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM. Structure 14, 1655\u20131665 (2006).",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_4_10_2",
      "doi-asserted-by": "crossref",
      "first-page": "265",
      "DOI": "10.1016/0022-2836(84)90194-3",
      "article-title": "Nucleotide sequence of the gene for bacteriophage T7 RNA polymerase",
      "volume": "173",
      "author": "Moffatt BA",
      "year": "1984",
      "unstructured": "BA Moffatt, JJ Dunn, FW Studier, Nucleotide sequence of the gene for bacteriophage T7 RNA polymerase. J Mol Biol 173, 265\u2013269 (1984).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_11_2",
      "first-page": "1",
      "article-title": "T7Select Phage Display System: A powerful new protein display system based on bacteriophage T7",
      "volume": "6",
      "author": "Rosenberg A",
      "year": "1996",
      "unstructured": "A Rosenberg, , T7Select Phage Display System: A powerful new protein display system based on bacteriophage T7. Innovations 6, 1\u20136 (1996).",
      "journal-title": "Innovations"
    },
    {
      "key": "e_1_3_4_12_2",
      "doi-asserted-by": "crossref",
      "first-page": "477",
      "DOI": "10.1016/S0022-2836(83)80282-4",
      "article-title": "Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements",
      "volume": "166",
      "author": "Dunn JJ",
      "year": "1983",
      "unstructured": "JJ Dunn, FW Studier, Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol 166, 477\u2013535 (1983).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_13_2",
      "doi-asserted-by": "crossref",
      "first-page": "492",
      "DOI": "10.1016/j.mib.2011.07.010",
      "article-title": "Bacteriophage-host interactions leading to genome internalization",
      "volume": "14",
      "author": "Bertin A",
      "year": "2011",
      "unstructured": "A Bertin, M de Frutos, L Letellier, Bacteriophage-host interactions leading to genome internalization. Curr Opin Microbiol 14, 492\u2013496 (2011).",
      "journal-title": "Curr Opin Microbiol"
    },
    {
      "key": "e_1_3_4_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "461",
      "DOI": "10.1016/j.str.2007.03.004",
      "article-title": "Quasi-atomic model of bacteriophage t7 procapsid shell: Insights into the structure and evolution of a basic fold",
      "volume": "15",
      "author": "Agirrezabala X",
      "year": "2007",
      "unstructured": "X Agirrezabala, , Quasi-atomic model of bacteriophage t7 procapsid shell: Insights into the structure and evolution of a basic fold. Structure 15, 461\u2013472 (2007).",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_4_15_2",
      "doi-asserted-by": "crossref",
      "first-page": "286",
      "DOI": "10.1006/jmbi.1996.0250",
      "article-title": "Assembly of T7 capsids from independently expressed and purified head protein and scaffolding protein",
      "volume": "258",
      "author": "Cerritelli ME",
      "year": "1996",
      "unstructured": "ME Cerritelli, FW Studier, Assembly of T7 capsids from independently expressed and purified head protein and scaffolding protein. J Mol Biol 258, 286\u2013298 (1996).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_16_2",
      "doi-asserted-by": "crossref",
      "first-page": "65",
      "DOI": "10.1016/S0022-2836(80)80005-2",
      "article-title": "A metrizamide-impermeable capsid in the DNA packaging pathway of bacteriophage T7",
      "volume": "138",
      "author": "Serwer P",
      "year": "1980",
      "unstructured": "P Serwer, A metrizamide-impermeable capsid in the DNA packaging pathway of bacteriophage T7. J Mol Biol 138, 65\u201391 (1980).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_17_2",
      "doi-asserted-by": "crossref",
      "first-page": "433",
      "DOI": "10.1016/0022-2836(75)90290-9",
      "article-title": "Buoyant density sedimentation of macromolecules in sodium iothalamate density gradients",
      "volume": "92",
      "author": "Serwer P",
      "year": "1975",
      "unstructured": "P Serwer, Buoyant density sedimentation of macromolecules in sodium iothalamate density gradients. J Mol Biol 92, 433\u2013448 (1975).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_18_2",
      "doi-asserted-by": "crossref",
      "first-page": "6811",
      "DOI": "10.1073/pnas.1215563110",
      "article-title": "Visualization of uncorrelated, tandem symmetry mismatches in the internal genome packaging apparatus of bacteriophage T7",
      "volume": "110",
      "author": "Guo F",
      "year": "2013",
      "unstructured": "F Guo, , Visualization of uncorrelated, tandem symmetry mismatches in the internal genome packaging apparatus of bacteriophage T7. Proc Natl Acad Sci USA 110, 6811\u20136816 (2013).",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "e_1_3_4_19_2",
      "doi-asserted-by": "crossref",
      "first-page": "537",
      "DOI": "10.1046/j.1365-2443.1997.1450343.x",
      "article-title": "Phage DNA packaging",
      "volume": "2",
      "author": "Fujisawa H",
      "year": "1997",
      "unstructured": "H Fujisawa, M Morita, Phage DNA packaging. Genes Cells 2, 537\u2013545 (1997).",
      "journal-title": "Genes Cells"
    },
    {
      "key": "e_1_3_4_20_2",
      "doi-asserted-by": "crossref",
      "first-page": "23",
      "DOI": "10.1016/0166-0934(85)90121-1",
      "article-title": "The use of polylysine during negative staining of viral suspensions",
      "volume": "11",
      "author": "Barth OM",
      "year": "1985",
      "unstructured": "OM Barth, The use of polylysine during negative staining of viral suspensions. J Virol Methods 11, 23\u201327 (1985).",
      "journal-title": "J Virol Methods"
    },
    {
      "key": "e_1_3_4_21_2",
      "doi-asserted-by": "crossref",
      "first-page": "401",
      "DOI": "10.1007/978-1-62703-776-1_19",
      "article-title": "Single particle cryo-electron microscopy and 3-D reconstruction of viruses",
      "volume": "1117",
      "author": "Guo F",
      "year": "2014",
      "unstructured": "F Guo, W Jiang, Single particle cryo-electron microscopy and 3-D reconstruction of viruses. Methods Mol Biol 1117, 401\u2013443 (2014).",
      "journal-title": "Methods Mol Biol"
    },
    {
      "key": "e_1_3_4_22_2",
      "doi-asserted-by": "crossref",
      "first-page": "853",
      "DOI": "10.1038/nmeth.2115",
      "article-title": "Prevention of overfitting in cryo-EM structure determination",
      "volume": "9",
      "author": "Scheres SH",
      "year": "2012",
      "unstructured": "SH Scheres, S Chen, Prevention of overfitting in cryo-EM structure determination. Nat Methods 9, 853\u2013854 (2012).",
      "journal-title": "Nat Methods"
    },
    {
      "key": "e_1_3_4_23_2",
      "doi-asserted-by": "crossref",
      "first-page": "205",
      "DOI": "10.1016/j.str.2011.12.014",
      "article-title": "Outcome of the first electron microscopy validation task force meeting",
      "volume": "20",
      "author": "Henderson R",
      "year": "2012",
      "unstructured": "R Henderson, , Outcome of the first electron microscopy validation task force meeting. Structure 20, 205\u2013214 (2012).",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_4_24_2",
      "doi-asserted-by": "crossref",
      "first-page": "721",
      "DOI": "10.1016/j.jmb.2003.07.013",
      "article-title": "Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy",
      "volume": "333",
      "author": "Rosenthal PB",
      "year": "2003",
      "unstructured": "PB Rosenthal, R Henderson, Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J Mol Biol 333, 721\u2013745 (2003).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_25_2",
      "doi-asserted-by": "crossref",
      "first-page": "673",
      "DOI": "10.1016/j.str.2008.03.005",
      "article-title": "Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics",
      "volume": "16",
      "author": "Trabuco LG",
      "year": "2008",
      "unstructured": "LG Trabuco, E Villa, K Mitra, J Frank, K Schulten, Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16, 673\u2013683 (2008).",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_4_26_2",
      "doi-asserted-by": "crossref",
      "first-page": "10604",
      "DOI": "10.1073/pnas.1303047110",
      "article-title": "Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story",
      "volume": "110",
      "author": "Pietil\u00e4 MK",
      "year": "2013",
      "unstructured": "MK Pietil\u00e4, , Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story. Proc Natl Acad Sci USA 110, 10604\u201310609 (2013).",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "e_1_3_4_27_2",
      "doi-asserted-by": "crossref",
      "first-page": "12301",
      "DOI": "10.1073/pnas.1309947110",
      "article-title": "Validated near-atomic resolution structure of bacteriophage epsilon15 derived from cryo-EM and modeling",
      "volume": "110",
      "author": "Baker ML",
      "year": "2013",
      "unstructured": "ML Baker, , Validated near-atomic resolution structure of bacteriophage epsilon15 derived from cryo-EM and modeling. Proc Natl Acad Sci USA 110, 12301\u20136 (2013).",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "e_1_3_4_28_2",
      "doi-asserted-by": "crossref",
      "first-page": "885",
      "DOI": "10.1016/j.jmb.2003.09.035",
      "article-title": "The refined structure of a protein catenane: The HK97 bacteriophage capsid at 3.44 A resolution",
      "volume": "334",
      "author": "Helgstrand C",
      "year": "2003",
      "unstructured": "C Helgstrand, , The refined structure of a protein catenane: The HK97 bacteriophage capsid at 3.44 A resolution. J Mol Biol 334, 885\u2013899 (2003).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_29_2",
      "doi-asserted-by": "crossref",
      "first-page": "2129",
      "DOI": "10.1126/science.289.5487.2129",
      "article-title": "Topologically linked protein rings in the bacteriophage HK97 capsid",
      "volume": "289",
      "author": "Wikoff WR",
      "year": "2000",
      "unstructured": "WR Wikoff, , Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289, 2129\u20132133 (2000).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_30_2",
      "doi-asserted-by": "crossref",
      "first-page": "14967",
      "DOI": "10.1128/JVI.79.23.14967-14970.2005",
      "article-title": "Common ancestry of herpesviruses and tailed DNA bacteriophages",
      "volume": "79",
      "author": "Baker ML",
      "year": "2005",
      "unstructured": "ML Baker, W Jiang, FJ Rixon, W Chiu, Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol 79, 14967\u201314970 (2005).",
      "journal-title": "J Virol"
    },
    {
      "key": "e_1_3_4_31_2",
      "doi-asserted-by": "crossref",
      "first-page": "541",
      "DOI": "10.1016/j.jmb.2011.01.016",
      "article-title": "The Prohead-I structure of bacteriophage HK97: Implications for scaffold-mediated control of particle assembly and maturation",
      "volume": "408",
      "author": "Huang RK",
      "year": "2011",
      "unstructured": "RK Huang, , The Prohead-I structure of bacteriophage HK97: Implications for scaffold-mediated control of particle assembly and maturation. J Mol Biol 408, 541\u2013554 (2011).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_32_2",
      "doi-asserted-by": "crossref",
      "first-page": "213",
      "DOI": "10.1107/S0907444909052925",
      "article-title": "PHENIX: A comprehensive Python-based system for macromolecular structure solution",
      "volume": "66",
      "author": "Adams PD",
      "year": "2010",
      "unstructured": "PD Adams, , PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213\u2013221 (2010).",
      "journal-title": "Acta Crystallogr D Biol Crystallogr"
    },
    {
      "key": "e_1_3_4_33_2",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/j.virol.2011.09.005",
      "article-title": "Decoding bacteriophage P22 assembly: Identification of two charged residues in scaffolding protein responsible for coat protein interaction",
      "volume": "421",
      "author": "Cortines JR",
      "year": "2011",
      "unstructured": "JR Cortines, PR Weigele, EB Gilcrease, SR Casjens, CM Teschke, Decoding bacteriophage P22 assembly: Identification of two charged residues in scaffolding protein responsible for coat protein interaction. Virology 421, 1\u201311 (2011).",
      "journal-title": "Virology"
    },
    {
      "key": "e_1_3_4_34_2",
      "doi-asserted-by": "crossref",
      "first-page": "572",
      "DOI": "10.1038/nsb939",
      "article-title": "Bacteriophage phi29 scaffolding protein gp7 before and after prohead assembly",
      "volume": "10",
      "author": "Morais MC",
      "year": "2003",
      "unstructured": "MC Morais, , Bacteriophage phi29 scaffolding protein gp7 before and after prohead assembly. Nat Struct Biol 10, 572\u2013576 (2003).",
      "journal-title": "Nat Struct Biol"
    },
    {
      "key": "e_1_3_4_35_2",
      "doi-asserted-by": "crossref",
      "first-page": "1195",
      "DOI": "10.1006/jmbi.2000.3620",
      "article-title": "Structure of the coat protein-binding domain of the scaffolding protein from a double-stranded DNA virus",
      "volume": "297",
      "author": "Sun Y",
      "year": "2000",
      "unstructured": "Y Sun, , Structure of the coat protein-binding domain of the scaffolding protein from a double-stranded DNA virus. J Mol Biol 297, 1195\u20131202 (2000).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_36_2",
      "doi-asserted-by": "crossref",
      "first-page": "271",
      "DOI": "10.1016/S0022-2836(76)80005-8",
      "article-title": "Internal proteins of bacteriophage T7",
      "volume": "107",
      "author": "Serwer P",
      "year": "1976",
      "unstructured": "P Serwer, Internal proteins of bacteriophage T7. J Mol Biol 107, 271\u2013291 (1976).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_37_2",
      "doi-asserted-by": "crossref",
      "first-page": "e01299",
      "DOI": "10.7554/eLife.01299",
      "article-title": "A new topology of the HK97-like fold revealed in Bordetella bacteriophage by cryoEM at 3.5 A resolution",
      "volume": "2",
      "author": "Zhang X",
      "year": "2013",
      "unstructured": "X Zhang, , A new topology of the HK97-like fold revealed in Bordetella bacteriophage by cryoEM at 3.5 A resolution. eLife 2, e01299 (2013).",
      "journal-title": "eLife"
    },
    {
      "key": "e_1_3_4_38_2",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/j.jsb.2014.04.006",
      "article-title": "Single-step antibody-based affinity cryo-electron microscopy for imaging and structural analysis of macromolecular assemblies",
      "volume": "187",
      "author": "Yu G",
      "year": "2014",
      "unstructured": "G Yu, , Single-step antibody-based affinity cryo-electron microscopy for imaging and structural analysis of macromolecular assemblies. J Struct Biol 187, 1\u20139 (2014).",
      "journal-title": "J Struct Biol"
    },
    {
      "key": "e_1_3_4_39_2",
      "doi-asserted-by": "crossref",
      "first-page": "235",
      "DOI": "10.1016/S0065-3527(08)60810-6",
      "article-title": "Bacteriophage HK97 head assembly: A protein ballet",
      "volume": "50",
      "author": "Hendrix RW",
      "year": "1998",
      "unstructured": "RW Hendrix, RL Duda, Bacteriophage HK97 head assembly: A protein ballet. Adv Virus Res 50, 235\u2013288 (1998).",
      "journal-title": "Adv Virus Res"
    },
    {
      "key": "e_1_3_4_40_2",
      "doi-asserted-by": "crossref",
      "first-page": "202",
      "DOI": "10.1002/jss.400020215",
      "article-title": "P22 morphogenesis. I: Catalytic scaffolding protein in capsid assembly",
      "volume": "2",
      "author": "Casjens S",
      "year": "1974",
      "unstructured": "S Casjens, J King, P22 morphogenesis. I: Catalytic scaffolding protein in capsid assembly. J Supramol Struct 2, 202\u2013224 (1974).",
      "journal-title": "J Supramol Struct"
    },
    {
      "key": "e_1_3_4_41_2",
      "doi-asserted-by": "crossref",
      "first-page": "221",
      "DOI": "10.1016/1047-8477(91)90072-5",
      "article-title": "The maturation-dependent conformational change of phage T4 capsid involves the translocation of specific epitopes between the inner and the outer capsid surfaces",
      "volume": "106",
      "author": "Steven AC",
      "year": "1991",
      "unstructured": "AC Steven, AC Bauer, ME Bisher, FA Robey, LW Black, The maturation-dependent conformational change of phage T4 capsid involves the translocation of specific epitopes between the inner and the outer capsid surfaces. J Struct Biol 106, 221\u2013236 (1991).",
      "journal-title": "J Struct Biol"
    },
    {
      "key": "e_1_3_4_42_2",
      "doi-asserted-by": "crossref",
      "first-page": "11040",
      "DOI": "10.1128/JVI.01056-06",
      "article-title": "Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus",
      "volume": "80",
      "author": "Sonntag F",
      "year": "2006",
      "unstructured": "F Sonntag, S Bleker, B Leuchs, R Fischer, JA Kleinschmidt, Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus. J Virol 80, 11040\u201311054 (2006).",
      "journal-title": "J Virol"
    },
    {
      "key": "e_1_3_4_43_2",
      "doi-asserted-by": "crossref",
      "first-page": "5296",
      "DOI": "10.1128/JVI.79.9.5296-5303.2005",
      "article-title": "A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini",
      "volume": "79",
      "author": "Kronenberg S",
      "year": "2005",
      "unstructured": "S Kronenberg, B B\u00f6ttcher, CW von der Lieth, S Bleker, JA Kleinschmidt, A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J Virol 79, 5296\u20135303 (2005).",
      "journal-title": "J Virol"
    },
    {
      "key": "e_1_3_4_44_2",
      "doi-asserted-by": "crossref",
      "first-page": "1044",
      "DOI": "10.1128/JVI.75.2.1044-1047.2001",
      "article-title": "The N-terminal region of the VP1 protein of swine vesicular disease virus contains a neutralization site that arises upon cell attachment and is involved in viral entry",
      "volume": "75",
      "author": "Jim\u00e9nez-Clavero MA",
      "year": "2001",
      "unstructured": "MA Jim\u00e9nez-Clavero, E Escribano-Romero, AJ Douglas, V Ley, The N-terminal region of the VP1 protein of swine vesicular disease virus contains a neutralization site that arises upon cell attachment and is involved in viral entry. J Virol 75, 1044\u20131047 (2001).",
      "journal-title": "J Virol"
    },
    {
      "key": "e_1_3_4_45_2",
      "doi-asserted-by": "crossref",
      "first-page": "728",
      "DOI": "10.1016/j.jmb.2009.10.007",
      "article-title": "Structure of the small outer capsid protein, Soc: A clamp for stabilizing capsids of T4-like phages",
      "volume": "395",
      "author": "Qin L",
      "year": "2010",
      "unstructured": "L Qin, A Fokine, E O\u2019Donnell, VB Rao, MG Rossmann, Structure of the small outer capsid protein, Soc: A clamp for stabilizing capsids of T4-like phages. J Mol Biol 395, 728\u2013741 (2010).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_46_2",
      "doi-asserted-by": "crossref",
      "first-page": "6003",
      "DOI": "10.1073/pnas.0400444101",
      "article-title": "Molecular architecture of the prolate head of bacteriophage T4",
      "volume": "101",
      "author": "Fokine A",
      "year": "2004",
      "unstructured": "A Fokine, , Molecular architecture of the prolate head of bacteriophage T4. Proc Natl Acad Sci USA 101, 6003\u20136008 (2004).",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "e_1_3_4_47_2",
      "doi-asserted-by": "crossref",
      "first-page": "1399",
      "DOI": "10.1016/j.str.2008.05.016",
      "article-title": "Bacteriophage lambda stabilization by auxiliary protein gpD: Timing, location, and mechanism of attachment determined by cryo-EM",
      "volume": "16",
      "author": "Lander GC",
      "year": "2008",
      "unstructured": "GC Lander, , Bacteriophage lambda stabilization by auxiliary protein gpD: Timing, location, and mechanism of attachment determined by cryo-EM. Structure 16, 1399\u20131406 (2008).",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_4_48_2",
      "doi-asserted-by": "crossref",
      "first-page": "916",
      "DOI": "10.1111/1574-6976.12072",
      "article-title": "Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities",
      "volume": "38",
      "author": "Koskella B",
      "year": "2014",
      "unstructured": "B Koskella, MA Brockhurst, Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 38, 916\u2013931 (2014).",
      "journal-title": "FEMS Microbiol Rev"
    },
    {
      "key": "e_1_3_4_49_2",
      "doi-asserted-by": "crossref",
      "first-page": "234",
      "DOI": "10.1016/j.virol.2007.07.027",
      "article-title": "The genome of epsilon15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage",
      "volume": "369",
      "author": "Kropinski AM",
      "year": "2007",
      "unstructured": "AM Kropinski, , The genome of epsilon15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage. Virology 369, 234\u2013244 (2007).",
      "journal-title": "Virology"
    },
    {
      "key": "e_1_3_4_50_2",
      "doi-asserted-by": "crossref",
      "first-page": "86",
      "DOI": "10.1128/MMBR.67.1.86-156.2003",
      "article-title": "Bacteriophage T4 genome",
      "volume": "67",
      "author": "Miller ES",
      "year": "2003",
      "unstructured": "ES Miller, , Bacteriophage T4 genome. Microbiol Mol Biol Rev 67, 86\u2013156 (2003).",
      "journal-title": "Microbiol Mol Biol Rev"
    },
    {
      "key": "e_1_3_4_51_2",
      "doi-asserted-by": "crossref",
      "first-page": "6472",
      "DOI": "10.1128/JB.182.22.6472-6481.2000",
      "article-title": "Sequence of the genome of Salmonella bacteriophage P22",
      "volume": "182",
      "author": "Vander Byl C",
      "year": "2000",
      "unstructured": "C Vander Byl, AM Kropinski, Sequence of the genome of Salmonella bacteriophage P22. J Bacteriol 182, 6472\u20136481 (2000).",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "e_1_3_4_52_2",
      "doi-asserted-by": "crossref",
      "first-page": "27",
      "DOI": "10.1006/jmbi.2000.3729",
      "article-title": "Genomic sequences of bacteriophages HK97 and HK022: Pervasive genetic mosaicism in the lambdoid bacteriophages",
      "volume": "299",
      "author": "Juhala RJ",
      "year": "2000",
      "unstructured": "RJ Juhala, , Genomic sequences of bacteriophages HK97 and HK022: Pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299, 27\u201351 (2000).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_53_2",
      "unstructured": "BA Duerkop KL Palmer MJ Horsburgh Enterococcal bacteriophages and genome defense. Enterococci: From Commensals to Leading Causes of Drug Resistant Infection eds Gilmore MS Clewell DB Ike Y Shankar N (Massachusetts Eye and Ear Infirmary Boston). (2014)."
    },
    {
      "key": "e_1_3_4_54_2",
      "doi-asserted-by": "crossref",
      "first-page": "244",
      "DOI": "10.1046/j.1365-2958.2000.01838.x",
      "article-title": "Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria",
      "volume": "36",
      "author": "Mojica FJ",
      "year": "2000",
      "unstructured": "FJ Mojica, C D\u00edez-Villase\u00f1or, E Soria, G Juez, Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol Microbiol 36, 244\u2013246 (2000).",
      "journal-title": "Mol Microbiol"
    },
    {
      "key": "e_1_3_4_55_2",
      "doi-asserted-by": "crossref",
      "first-page": "471",
      "DOI": "10.1016/j.jmb.2009.06.035",
      "article-title": "Structure and energetics of encapsidated DNA in bacteriophage HK97 studied by scanning calorimetry and cryo-electron microscopy",
      "volume": "391",
      "author": "Duda RL",
      "year": "2009",
      "unstructured": "RL Duda, , Structure and energetics of encapsidated DNA in bacteriophage HK97 studied by scanning calorimetry and cryo-electron microscopy. J Mol Biol 391, 471\u2013483 (2009).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_56_2",
      "doi-asserted-by": "crossref",
      "first-page": "993",
      "DOI": "10.1016/j.jmb.2006.06.081",
      "article-title": "Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships",
      "volume": "361",
      "author": "Effantin G",
      "year": "2006",
      "unstructured": "G Effantin, P Boulanger, E Neumann, L Letellier, JF Conway, Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J Mol Biol 361, 993\u20131002 (2006).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_57_2",
      "doi-asserted-by": "crossref",
      "first-page": "748",
      "DOI": "10.1038/35099581",
      "article-title": "The bacteriophage straight phi29 portal motor can package DNA against a large internal force",
      "volume": "413",
      "author": "Smith DE",
      "year": "2001",
      "unstructured": "DE Smith, , The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature 413, 748\u2013752 (2001).",
      "journal-title": "Nature"
    },
    {
      "key": "e_1_3_4_58_2",
      "doi-asserted-by": "crossref",
      "first-page": "126",
      "DOI": "10.1006/jsbi.2000.4279",
      "article-title": "Local average intensity-based method for identifying spherical particles in electron micrographs",
      "volume": "131",
      "author": "Kivioja T",
      "year": "2000",
      "unstructured": "T Kivioja, J Ravantti, A Verkhovsky, E Ukkonen, D Bamford, Local average intensity-based method for identifying spherical particles in electron micrographs. J Struct Biol 131, 126\u2013134 (2000).",
      "journal-title": "J Struct Biol"
    },
    {
      "key": "e_1_3_4_59_2",
      "doi-asserted-by": "crossref",
      "first-page": "82",
      "DOI": "10.1006/jsbi.1999.4174",
      "article-title": "EMAN: Semiautomated software for high-resolution single-particle reconstructions",
      "volume": "128",
      "author": "Ludtke SJ",
      "year": "1999",
      "unstructured": "SJ Ludtke, PR Baldwin, W Chiu, EMAN: Semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128, 82\u201397 (1999).",
      "journal-title": "J Struct Biol"
    },
    {
      "key": "e_1_3_4_60_2",
      "doi-asserted-by": "crossref",
      "first-page": "343",
      "DOI": "10.1016/j.jsb.2012.07.005",
      "article-title": "A graph theory method for determination of cryo-EM image focuses",
      "volume": "180",
      "author": "Jiang W",
      "year": "2012",
      "unstructured": "W Jiang, F Guo, Z Liu, A graph theory method for determination of cryo-EM image focuses. J Struct Biol 180, 343\u2013351 (2012).",
      "journal-title": "J Struct Biol"
    },
    {
      "key": "e_1_3_4_61_2",
      "doi-asserted-by": "crossref",
      "first-page": "391",
      "DOI": "10.1111/j.1365-2818.2009.03137.x",
      "article-title": "Estimating contrast transfer function and associated parameters by constrained non-linear optimization",
      "volume": "233",
      "author": "Yang C",
      "year": "2009",
      "unstructured": "C Yang, , Estimating contrast transfer function and associated parameters by constrained non-linear optimization. J Microsc 233, 391\u2013403 (2009).",
      "journal-title": "J Microsc"
    },
    {
      "key": "e_1_3_4_62_2",
      "doi-asserted-by": "crossref",
      "first-page": "211",
      "DOI": "10.1016/j.jsb.2006.07.013",
      "article-title": "Ab initio random model method facilitates 3D reconstruction of icosahedral particles",
      "volume": "157",
      "author": "Yan X",
      "year": "2007",
      "unstructured": "X Yan, KA Dryden, J Tang, TS Baker, Ab initio random model method facilitates 3D reconstruction of icosahedral particles. J Struct Biol 157, 211\u2013225 (2007).",
      "journal-title": "J Struct Biol"
    },
    {
      "key": "e_1_3_4_63_2",
      "doi-asserted-by": "crossref",
      "first-page": "11",
      "DOI": "10.1016/j.jsb.2007.06.009",
      "article-title": "Averaging tens to hundreds of icosahedral particle images to resolve protein secondary structure elements using a Multi-Path Simulated Annealing optimization algorithm",
      "volume": "160",
      "author": "Liu X",
      "year": "2007",
      "unstructured": "X Liu, W Jiang, J Jakana, W Chiu, Averaging tens to hundreds of icosahedral particle images to resolve protein secondary structure elements using a Multi-Path Simulated Annealing optimization algorithm. J Struct Biol 160, 11\u201327 (2007).",
      "journal-title": "J Struct Biol"
    },
    {
      "key": "e_1_3_4_64_2",
      "doi-asserted-by": "crossref",
      "first-page": "38",
      "DOI": "10.1016/j.jsb.2006.05.009",
      "article-title": "EMAN2: An extensible image processing suite for electron microscopy",
      "volume": "157",
      "author": "Tang G",
      "year": "2007",
      "unstructured": "G Tang, , EMAN2: An extensible image processing suite for electron microscopy. J Struct Biol 157, 38\u201346 (2007).",
      "journal-title": "J Struct Biol"
    },
    {
      "key": "e_1_3_4_65_2",
      "doi-asserted-by": "crossref",
      "first-page": "2126",
      "DOI": "10.1107/S0907444904019158",
      "article-title": "Coot: Model-building tools for molecular graphics",
      "volume": "60",
      "author": "Emsley P",
      "year": "2004",
      "unstructured": "P Emsley, K Cowtan, Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126\u20132132 (2004).",
      "journal-title": "Acta Crystallogr D Biol Crystallogr"
    },
    {
      "key": "e_1_3_4_66_2",
      "doi-asserted-by": "crossref",
      "first-page": "1605",
      "DOI": "10.1002/jcc.20084",
      "article-title": "UCSF Chimera\u2014a visualization system for exploratory research and analysis",
      "volume": "25",
      "author": "Pettersen EF",
      "year": "2004",
      "unstructured": "EF Pettersen, , UCSF Chimera\u2014a visualization system for exploratory research and analysis. J Comput Chem 25, 1605\u20131612 (2004).",
      "journal-title": "J Comput Chem"
    },
    {
      "key": "e_1_3_4_67_2",
      "doi-asserted-by": "crossref",
      "first-page": "760",
      "DOI": "10.1107/S0907444994003112",
      "article-title": "The CCP4 suite: Programs for protein crystallography",
      "volume": "50",
      "author": "Collaborative Computational Project, Number 4",
      "year": "1994",
      "unstructured": "; Collaborative Computational Project, Number 4, The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760\u2013763 (1994).",
      "journal-title": "Acta Crystallogr D Biol Crystallogr"
    },
    {
      "key": "e_1_3_4_68_2",
      "doi-asserted-by": "crossref",
      "first-page": "12",
      "DOI": "10.1107/S0907444909042073",
      "article-title": "MolProbity: All-atom structure validation for macromolecular crystallography",
      "volume": "66",
      "author": "Chen VB",
      "year": "2010",
      "unstructured": "VB Chen, , MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66, 12\u201321 (2010).",
      "journal-title": "Acta Crystallogr D Biol Crystallogr"
    }
  ],
  "container-title": "Proceedings of the National Academy of Sciences",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://pnas.org/doi/pdf/10.1073/pnas.1407020111",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        6,
        7
      ]
    ],
    "date-time": "2022-06-07T11:51:45Z",
    "timestamp": 1654602705000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://pnas.org/doi/full/10.1073/pnas.1407020111"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2014,
        10,
        13
      ]
    ]
  },
  "references-count": 68,
  "journal-issue": {
    "issue": "43",
    "published-print": {
      "date-parts": [
        [
          2014,
          10,
          28
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1073/pnas.1407020111"
  ],
  "URL": "http://dx.doi.org/10.1073/pnas.1407020111",
  "relation": {},
  "ISSN": [
    "0027-8424",
    "1091-6490"
  ],
  "subject": [],
  "container-title-short": "Proc. Natl. Acad. Sci. U.S.A.",
  "published": {
    "date-parts": [
      [
        2014,
        10,
        13
      ]
    ]
  },
  "assertion": [
    {
      "value": "2014-10-13",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}