DOI: 10.1128/jb.00996-08. PilF Is an Outer Membrane Lipoprotein Required for Multimerization and Localization of the<i>Pseudomonas aeruginosa</i>Type IV Pilus Secretin

PilF Is an Outer Membrane Lipoprotein Required for Multimerization and Localization of thePseudomonas aeruginosaType IV Pilus Secretin
10.1128/jb.00996-08
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract
ABSTRACTType IV pili (T4P) are retractile appendages that contribute to the virulence of bacterial pathogens. PilF is aPseudomonas aeruginosalipoprotein that is essential for T4P biogenesis. Phenotypic characterization of apilFmutant confirmed that T4P-mediated functions are abrogated: T4P were no longer present on the cell surface, twitching motility was abolished, and the mutant was resistant to infection by T4P retraction-dependent bacteriophage. The results of cellular fractionation studies indicated that PilF is the outer membrane pilotin required for the localization and multimerization of the secretin, PilQ. Mutation of the putative PilF lipidation site untethered the protein from the outer membrane, causing secretin assembly in both inner and outer membranes. T4P-mediated twitching motility and bacteriophage susceptibility were moderately decreased in the lipidation site mutant, while cell surface piliation was substantially reduced. The tethering of PilF to the outer membrane promotes the correct localization of PilQ and appears to be required for the formation of stable T4P. Our 2.0-Å structure of PilF revealed a superhelical arrangement of six tetratricopeptide protein-protein interaction motifs that may mediate the contacts with PilQ during secretin assembly. An alignment of pseudomonad PilF sequences revealed three highly conserved surfaces that may be involved in PilF function.
Bibliography
Koo, J., Tammam, S., Ku, S.-Y., Sampaleanu, L. M., Burrows, L. L., & Howell, P. L. (2008). PilF Is an Outer Membrane Lipoprotein Required for Multimerization and Localization of thePseudomonas aeruginosaType IV Pilus Secretin. Journal of Bacteriology, 190(21), 6961â6969.
Authors 6
Jason Koo (first)
Stephanie Tammam (additional)
Shao-Yang Ku (additional)
Liliana M. Sampaleanu (additional)
Lori L. Burrows (additional)
P. Lynne Howell (additional)
References 71 Referenced 98
Dates
Type	When
Created	16 years, 11 months ago (Sept. 5, 2008, 8:55 p.m.)
Deposited	1 year, 6 months ago (Feb. 29, 2024, 12:07 p.m.)
Indexed	11 months, 3 weeks ago (Sept. 12, 2024, 9:59 a.m.)
Issued	16 years, 10 months ago (Nov. 1, 2008)
Published	16 years, 10 months ago (Nov. 1, 2008)
Published Print	16 years, 10 months ago (Nov. 1, 2008)
Funders 0
None
BibTeX
@article{Koo_2008, title={PilF Is an Outer Membrane Lipoprotein Required for Multimerization and Localization of thePseudomonas aeruginosaType IV Pilus Secretin}, volume={190}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.00996-08}, DOI={10.1128/jb.00996-08}, number={21}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Koo, Jason and Tammam, Stephanie and Ku, Shao-Yang and Sampaleanu, Liliana M. and Burrows, Lori L. and Howell, P. Lynne}, year={2008}, month=nov, pages={6961–6969} }
JSON
{
  "indexed": {
    "date-parts": [
      [
        2024,
        9,
        12
      ]
    ],
    "date-time": "2024-09-12T13:59:30Z",
    "timestamp": 1726149570885
  },
  "reference-count": 71,
  "publisher": "American Society for Microbiology",
  "issue": "21",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2008,
            11,
            1
          ]
        ],
        "date-time": "2008-11-01T00:00:00Z",
        "timestamp": 1225497600000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "https://journals.asm.org/non-commercial-tdm-license"
    }
  ],
  "content-domain": {
    "domain": [
      "journals.asm.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2008,
        11
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title><jats:p>Type IV pili (T4P) are retractile appendages that contribute to the virulence of bacterial pathogens. PilF is a<jats:italic>Pseudomonas aeruginosa</jats:italic>lipoprotein that is essential for T4P biogenesis. Phenotypic characterization of a<jats:italic>pilF</jats:italic>mutant confirmed that T4P-mediated functions are abrogated: T4P were no longer present on the cell surface, twitching motility was abolished, and the mutant was resistant to infection by T4P retraction-dependent bacteriophage. The results of cellular fractionation studies indicated that PilF is the outer membrane pilotin required for the localization and multimerization of the secretin, PilQ. Mutation of the putative PilF lipidation site untethered the protein from the outer membrane, causing secretin assembly in both inner and outer membranes. T4P-mediated twitching motility and bacteriophage susceptibility were moderately decreased in the lipidation site mutant, while cell surface piliation was substantially reduced. The tethering of PilF to the outer membrane promotes the correct localization of PilQ and appears to be required for the formation of stable T4P. Our 2.0-A\u030a structure of PilF revealed a superhelical arrangement of six tetratricopeptide protein-protein interaction motifs that may mediate the contacts with PilQ during secretin assembly. An alignment of pseudomonad PilF sequences revealed three highly conserved surfaces that may be involved in PilF function.</jats:p>",
  "DOI": "10.1128/jb.00996-08",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2008,
        9,
        6
      ]
    ],
    "date-time": "2008-09-06T00:55:22Z",
    "timestamp": 1220662522000
  },
  "page": "6961-6969",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 98,
  "title": "PilF Is an Outer Membrane Lipoprotein Required for Multimerization and Localization of the<i>Pseudomonas aeruginosa</i>Type IV Pilus Secretin",
  "prefix": "10.1128",
  "volume": "190",
  "author": [
    {
      "given": "Jason",
      "family": "Koo",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Biochemistry, University of Toronto, Ontario, Canada"
        },
        {
          "name": "Program in Molecular Structure and Function, Research Institute, Hospital for Sick Children, Toronto, Ontario, Canada"
        }
      ]
    },
    {
      "given": "Stephanie",
      "family": "Tammam",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry, University of Toronto, Ontario, Canada"
        },
        {
          "name": "Program in Molecular Structure and Function, Research Institute, Hospital for Sick Children, Toronto, Ontario, Canada"
        }
      ]
    },
    {
      "given": "Shao-Yang",
      "family": "Ku",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry, University of Toronto, Ontario, Canada"
        },
        {
          "name": "Program in Molecular Structure and Function, Research Institute, Hospital for Sick Children, Toronto, Ontario, Canada"
        }
      ]
    },
    {
      "given": "Liliana M.",
      "family": "Sampaleanu",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Program in Molecular Structure and Function, Research Institute, Hospital for Sick Children, Toronto, Ontario, Canada"
        }
      ]
    },
    {
      "given": "Lori L.",
      "family": "Burrows",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Program in Molecular Structure and Function, Research Institute, Hospital for Sick Children, Toronto, Ontario, Canada"
        },
        {
          "name": "Michael G. DeGroote Institute for Infectious Diseases Research and Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada"
        }
      ]
    },
    {
      "given": "P. Lynne",
      "family": "Howell",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry, University of Toronto, Ontario, Canada"
        },
        {
          "name": "Program in Molecular Structure and Function, Research Institute, Hospital for Sick Children, Toronto, Ontario, Canada"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.178.13.3809-3817.1996"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "crossref",
      "first-page": "3",
      "DOI": "10.1080/08893118708081678",
      "volume": "1",
      "year": "1987",
      "unstructured": "Blessing, B. H. 1987. Data reduction and error analysis for accurate single crystal diffraction intensities. Crystallogr. Rev. 1 : 3-58.",
      "journal-title": "Crystallogr. Rev."
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-2697(76)90527-3"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "149",
      "DOI": "10.1016/0042-6822(74)90150-0",
      "volume": "58",
      "year": "1974",
      "unstructured": "Bradley, D. E. 1974. The adsorption of Pseudomonas aeruginosa pilus-dependent bacteriophages to a host mutant with nonretractile pili. Virology 58 : 149-163.",
      "journal-title": "Virology"
    },
    {
      "key": "e_1_3_2_6_2",
      "first-page": "905",
      "volume": "54",
      "year": "1998",
      "unstructured": "Brunger, A. T., P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54 : 905-921.",
      "journal-title": "Acta Crystallogr. D"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.186.16.5366-5375.2004"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "crossref",
      "first-page": "878",
      "DOI": "10.1111/j.1365-2958.2005.04703.x",
      "volume": "57",
      "year": "2005",
      "unstructured": "Burrows, L. L. 2005. Weapons of mass retraction. Mol. Microbiol. 57 : 878-888.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "crossref",
      "first-page": "54",
      "DOI": "10.1111/j.1365-2958.2004.04364.x",
      "volume": "55",
      "year": "2005",
      "unstructured": "Carbonnelle, E., S. Helaine, L. Prouvensier, X. Nassif, and V. Pelicic. 2005. Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function. Mol. Microbiol. 55 : 54-64.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "crossref",
      "first-page": "1247",
      "DOI": "10.1099/13500872-141-5-1247",
      "volume": "141",
      "year": "1995",
      "unstructured": "Castric, P. 1995. pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology 141 : 1247-1254.",
      "journal-title": "Microbiology"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.185.7.2374-2378.2003"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "crossref",
      "first-page": "39750",
      "DOI": "10.1074/jbc.M405971200",
      "volume": "279",
      "year": "2004",
      "unstructured": "Collins, R. F., S. A. Frye, A. Kitmitto, R. C. Ford, T. Tonjum, and J. P. Derrick. 2004. Structure of the Neisseria meningitidis outer membrane PilQ secretin complex at 12 A resolution. J. Biol. Chem. 279 : 39750-39756.",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "crossref",
      "first-page": "465",
      "DOI": "10.1046/j.1365-2958.1997.3531727.x",
      "volume": "24",
      "year": "1997",
      "unstructured": "Daefler, S., I. Guilvout, K. R. Hardie, A. P. Pugsley, and M. Russel. 1997. The C-terminal domain of the secretin PulD contains the binding site for its cognate chaperone, PulS, and confers PulS dependence on pIVf1 function. Mol. Microbiol. 24 : 465-475.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "655",
      "DOI": "10.1016/j.tibs.2003.10.007",
      "volume": "28",
      "year": "2003",
      "unstructured": "D'Andrea, L. D., and L. Regan. 2003. TPR proteins: the versatile helix. Trends Biochem. Sci. 28 : 655-662.",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "crossref",
      "first-page": "31",
      "DOI": "10.1111/j.1365-2958.2005.04923.x",
      "volume": "59",
      "year": "2006",
      "unstructured": "Edqvist, P. J., J. E. Broms, H. J. Betts, A. Forsberg, M. J. Pallen, and M. S. Francis. 2006. Tetratricopeptide repeats in the type III secretion chaperone, LcrH: their role in substrate binding and secretion. Mol. Microbiol. 59 : 31-44.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "crossref",
      "first-page": "2126",
      "DOI": "10.1107/S0907444904019158",
      "volume": "60",
      "year": "2004",
      "unstructured": "Emsley, P., and K. Cowtan. 2004. COOT: model-building tools for molecular graphics. Acta Crystallogr. D 60 : 2126-2132.",
      "journal-title": "Acta Crystallogr. D"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.181.5.1623-1629.1999"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "crossref",
      "first-page": "13",
      "DOI": "10.1016/j.jmb.2008.06.055",
      "volume": "382",
      "year": "2008",
      "unstructured": "Guilvout, I., M. Chami, C. Berrier, A. Ghazi, A. Engel, A. P. Pugsley, and N. Bayan. 2008. In vitro multimerization and membrane insertion of bacterial outer membrane secretin PulD. J. Mol. Biol. 382 : 13-23.",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "crossref",
      "first-page": "5241",
      "DOI": "10.1038/sj.emboj.7601402",
      "volume": "25",
      "year": "2006",
      "unstructured": "Guilvout, I., M. Chami, A. Engel, A. P. Pugsley, and N. Bayan. 2006. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J. 25 : 5241-5249.",
      "journal-title": "EMBO J."
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "crossref",
      "first-page": "99",
      "DOI": "10.1016/S0378-1119(97)00116-9",
      "volume": "192",
      "year": "1997",
      "unstructured": "Hahn, H. P. 1997. The type-4 pilus is the major virulence-associated adhesin of Pseudomonas aeruginosa: a review. Gene 192 : 99-108.",
      "journal-title": "Gene"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.136.1.381-390.1978"
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "crossref",
      "first-page": "967",
      "DOI": "10.1046/j.1365-2958.1996.01539.x",
      "volume": "22",
      "year": "1996",
      "unstructured": "Hardie, K. R., A. Seydel, I. Guilvout, and A. P. Pugsley. 1996. The secretin-specific, chaperone-like protein of the general secretory pathway: separation of proteolytic protection and piloting functions. Mol. Microbiol. 22 : 967-976.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "crossref",
      "first-page": "566",
      "DOI": "10.1093/bioinformatics/16.6.566",
      "volume": "16",
      "year": "2000",
      "unstructured": "Holm, L., and J. Park. 2000. DaliLite workbench for protein structure comparison. Bioinformatics 16 : 566-567.",
      "journal-title": "Bioinformatics"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "crossref",
      "first-page": "595",
      "DOI": "10.1126/science.273.5275.595",
      "volume": "273",
      "year": "1996",
      "unstructured": "Holm, L., and C. Sander. 1996. Mapping the protein universe. Science 273 : 595-603.",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "crossref",
      "first-page": "14339",
      "DOI": "10.1073/pnas.2036282100",
      "volume": "100",
      "year": "2003",
      "unstructured": "Jacobs, M. A., A. Alwood, I. Thaipisuttikul, D. Spencer, E. Haugen, S. Ernst, O. Will, R. Kaul, C. Raymond, R. Levy, L. Chun-Rong, D. Guenthner, D. Bovee, M. V. Olson, and C. Manoil. 2003. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 100 : 14339-14344.",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "crossref",
      "first-page": "1001",
      "DOI": "10.1038/nsmb833",
      "volume": "11",
      "year": "2004",
      "unstructured": "Jinek, M., J. Rehwinkel, B. D. Lazarus, E. Izaurralde, J. A. Hanover, and E. Conti. 2004. The superhelical TPR-repeat domain of O-linked GlcNAc transferase exhibits structural similarities to importin alpha. Nat. Struct. Mol. Biol. 11 : 1001-1007.",
      "journal-title": "Nat. Struct. Mol. Biol."
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "crossref",
      "first-page": "800",
      "DOI": "10.1107/S0907444907024353",
      "volume": "63",
      "year": "2007",
      "unstructured": "Kajander, T., A. L. Cortajarena, S. Mochrie, and L. Regan. 2007. Structure and stability of designed TPR protein superhelices: unusual crystal packing and implications for natural TPR proteins. Acta Crystallogr. D 63 : 800-811.",
      "journal-title": "Acta Crystallogr. D"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "crossref",
      "first-page": "1028",
      "DOI": "10.1016/j.bbrc.2005.12.108",
      "volume": "340",
      "year": "2006",
      "unstructured": "Kim, K., J. Oh, D. Han, E. E. Kim, B. Lee, and Y. Kim. 2006. Crystal structure of PilF: functional implication in the type 4 pilus biogenesis in Pseudomonas aeruginosa. Biochem. Biophys. Res. Commun. 340 : 1028-1038.",
      "journal-title": "Biochem. Biophys. Res. Commun."
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.jmb.2007.05.022"
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "crossref",
      "first-page": "899",
      "DOI": "10.1016/S1097-2765(05)00091-2",
      "volume": "6",
      "year": "2000",
      "unstructured": "Lapouge, K., S. J. Smith, P. A. Walker, S. J. Gamblin, S. J. Smerdon, and K. Rittinger. 2000. Structure of the TPR domain of p67phox in complex with Rac.GTP. Mol. Cell 6 : 899-907.",
      "journal-title": "GTP. Mol. Cell"
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/btm404"
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1107/S0021889892009944"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "crossref",
      "first-page": "941",
      "DOI": "10.1016/S0969-2126(01)00656-6",
      "volume": "9",
      "year": "2001",
      "unstructured": "Lee, J. E., K. A. Cornell, M. K. Riscoe, and P. L. Howell. 2001. Structure of E. coli 5\u2032-methylthioadenosine/S-adenosylhomocysteine nucleosidase reveals similarity to the purine nucleoside phosphorylases. Structure 9 : 941-953.",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_2_34_2",
      "doi-asserted-by": "crossref",
      "first-page": "344",
      "DOI": "10.1016/j.mib.2005.04.002",
      "volume": "8",
      "year": "2005",
      "unstructured": "Maier, B. 2005. Using laser tweezers to measure twitching motility in Neisseria. Curr. Opin. Microbiol. 8 : 344-349.",
      "journal-title": "Curr. Opin. Microbiol."
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "DOI": "10.1016/S0969-2126(03)00076-5",
      "volume": "11",
      "year": "2003",
      "unstructured": "Main, E. R., Y. Xiong, M. J. Cocco, L. D'Andrea, and L. Regan. 2003. Design of stable alpha-helical arrays from an idealized TPR motif. Structure 11 : 497-508.",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1146/annurev.micro.56.012302.160938",
      "volume": "56",
      "year": "2002",
      "unstructured": "Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56 : 289-314.",
      "journal-title": "Annu. Rev. Microbiol."
    },
    {
      "key": "e_1_3_2_37_2",
      "doi-asserted-by": "crossref",
      "first-page": "423",
      "DOI": "10.1146/annurev.cellbio.16.1.423",
      "volume": "16",
      "year": "2000",
      "unstructured": "Merz, A. J., and M. So. 2000. Interactions of pathogenic neisseriae with epithelial cell membranes. Annu. Rev. Cell Dev. Biol. 16 : 423-457.",
      "journal-title": "Annu. Rev. Cell Dev. Biol."
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "crossref",
      "first-page": "641",
      "DOI": "10.1016/0022-2836(87)90038-6",
      "volume": "196",
      "year": "1987",
      "unstructured": "Miller, S., J. Janin, A. M. Lesk, and C. Chothia. 1987. Interior and surface of monomeric proteins. J. Mol. Biol. 196 : 641-656.",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "crossref",
      "first-page": "1794",
      "DOI": "10.1093/bioinformatics/btl171",
      "volume": "22",
      "year": "2006",
      "unstructured": "Murakami, Y., and S. Jones. 2006. SHARP2: protein-protein interaction predictions using patch analysis. Bioinformatics 22 : 1794-1795.",
      "journal-title": "Bioinformatics"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "crossref",
      "first-page": "13372",
      "DOI": "10.1074/jbc.M611839200",
      "volume": "282",
      "year": "2007",
      "unstructured": "Narita, S., and H. Tokuda. 2007. Amino acids at positions 3 and 4 determine the membrane specificity of Pseudomonas aeruginosa lipoproteins. J. Biol. Chem. 282 : 13372-13378.",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "crossref",
      "first-page": "3397",
      "DOI": "10.1093/bioinformatics/btm474",
      "volume": "23",
      "year": "2007",
      "unstructured": "Negi, S. S., C. H. Schein, N. Oezguen, T. D. Power, and W. Braun. 2007. InterProSurf: a web server for predicting interacting sites on protein surfaces. Bioinformatics 23 : 3397-3399.",
      "journal-title": "Bioinformatics"
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "crossref",
      "first-page": "125",
      "DOI": "10.1126/science.1112440",
      "volume": "309",
      "year": "2005",
      "unstructured": "Nudleman, E., D. Wall, and D. Kaiser. 2005. Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309 : 125-127.",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_2_43_2",
      "doi-asserted-by": "crossref",
      "first-page": "458",
      "DOI": "10.1038/8263",
      "volume": "6",
      "year": "1999",
      "unstructured": "Perrakis, A., R. Morris, and V. S. Lamzin. 1999. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6 : 458-463.",
      "journal-title": "Nat. Struct. Biol."
    },
    {
      "key": "e_1_3_2_44_2",
      "doi-asserted-by": "crossref",
      "first-page": "1718",
      "DOI": "10.1107/S090744499900935X",
      "volume": "55",
      "year": "1999",
      "unstructured": "Pflugrath, J. W. 1999. The finer things in X-ray diffraction data collection. Acta Crystallogr. D 55 : 1718-1725.",
      "journal-title": "Acta Crystallogr. D"
    },
    {
      "key": "e_1_3_2_45_2",
      "doi-asserted-by": "crossref",
      "first-page": "47",
      "DOI": "10.1002/1097-0134(20001001)41:1<47::AID-PROT80>3.0.CO;2-8",
      "volume": "41",
      "year": "2000",
      "unstructured": "Ponstingl, H., K. Henrick, and J. M. Thornton. 2000. Discriminating between homodimeric and monomeric proteins in the crystalline state. Proteins 41 : 47-57.",
      "journal-title": "Proteins"
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "crossref",
      "first-page": "7803",
      "DOI": "10.1073/pnas.0610098104",
      "volume": "104",
      "year": "2007",
      "unstructured": "Quinaud, M., S. Ple, V. Job, C. Contreras-Martel, J. P. Simorre, I. Attree, and A. Dessen. 2007. Structure of the heterotrimeric complex that regulates type III secretion needle formation. Proc. Natl. Acad. Sci. USA 104 : 7803-7808.",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_47_2",
      "doi-asserted-by": "crossref",
      "first-page": "1871",
      "DOI": "10.1099/00221287-148-6-1871",
      "volume": "148",
      "year": "2002",
      "unstructured": "Rakotoarivonina, H., G. Jubelin, M. Hebraud, B. Gaillard-Martinie, E. Forano, and P. Mosoni. 2002. Adhesion to cellulose of the gram-positive bacterium Ruminococcus albus involves type IV pili. Microbiology 148 : 1871-1880.",
      "journal-title": "Microbiology"
    },
    {
      "key": "e_1_3_2_48_2",
      "doi-asserted-by": "crossref",
      "first-page": "140",
      "DOI": "10.1107/S0108767386099622",
      "volume": "42",
      "year": "1986",
      "unstructured": "Read, R. J. 1986. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr. A 42 : 140-149.",
      "journal-title": "Acta Crystallogr. A"
    },
    {
      "key": "e_1_3_2_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.13.4372-4381.1997"
    },
    {
      "key": "e_1_3_2_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.176.10.2828-2834.1994"
    },
    {
      "key": "e_1_3_2_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)80830-2"
    },
    {
      "key": "e_1_3_2_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.183.24.6991-6998.2001"
    },
    {
      "key": "e_1_3_2_53_2",
      "doi-asserted-by": "crossref",
      "first-page": "2863",
      "DOI": "10.1099/00221287-145-10-2863",
      "volume": "145",
      "year": "1999",
      "unstructured": "Semmler, A. B., C. B. Whitchurch, and J. S. Mattick. 1999. A re-examination of twitching motility in Pseudomonas aeruginosa. Microbiology 145 : 2863-2873.",
      "journal-title": "Microbiology"
    },
    {
      "key": "e_1_3_2_54_2",
      "doi-asserted-by": "crossref",
      "first-page": "3219",
      "DOI": "10.1099/00221287-144-11-3219",
      "volume": "144",
      "year": "1998",
      "unstructured": "Shevchik, V. E., and G. Condemine. 1998. Functional characterization of the Erwinia chrysanthemi OutS protein, an element of a type II secretion system. Microbiology 144 : 3219-3228.",
      "journal-title": "Microbiology"
    },
    {
      "key": "e_1_3_2_55_2",
      "doi-asserted-by": "crossref",
      "first-page": "739",
      "DOI": "10.1093/protein/11.9.739",
      "volume": "11",
      "year": "1998",
      "unstructured": "Shindyalov, I. N., and P. E. Bourne. 1998. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 11 : 739-747.",
      "journal-title": "Protein Eng."
    },
    {
      "key": "e_1_3_2_56_2",
      "doi-asserted-by": "crossref",
      "first-page": "819",
      "DOI": "10.1016/j.jmb.2007.12.067",
      "volume": "377",
      "year": "2008",
      "unstructured": "Sun, P., J. E. Tropea, B. P. Austin, S. Cherry, and D. S. Waugh. 2008. Structural characterization of the Yersinia pestis type III secretion system needle protein YscF in complex with its heterodimeric chaperone YscE/YscG. J. Mol. Biol. 377 : 819-830.",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "e_1_3_2_57_2",
      "doi-asserted-by": "crossref",
      "first-page": "431",
      "DOI": "10.1016/S0969-2126(01)00603-7",
      "volume": "9",
      "year": "2001",
      "unstructured": "Taylor, P., J. Dornan, A. Carrello, R. F. Minchin, T. Ratajczak, and M. D. Walkinshaw. 2001. Two structures of cyclophilin 40: folding and fidelity in the TPR domains. Structure 9 : 431-438.",
      "journal-title": "Structure"
    },
    {
      "key": "e_1_3_2_58_2",
      "doi-asserted-by": "crossref",
      "first-page": "47690",
      "DOI": "10.1074/jbc.M109307200",
      "volume": "276",
      "year": "2001",
      "unstructured": "Terada, M., T. Kuroda, S. I. Matsuyama, and H. Tokuda. 2001. Lipoprotein sorting signals evaluated as the LolA-dependent release of lipoproteins from the cytoplasmic membrane of Escherichia coli. J. Biol. Chem. 276 : 47690-47694.",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_2_59_2",
      "doi-asserted-by": "crossref",
      "first-page": "38",
      "DOI": "10.1107/S0907444902018036",
      "volume": "59",
      "year": "2003",
      "unstructured": "Terwilliger, T. C. 2003. Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr. D 59 : 38-44.",
      "journal-title": "Acta Crystallogr. D"
    },
    {
      "key": "e_1_3_2_60_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.64.7.2853-2856.1996"
    },
    {
      "key": "e_1_3_2_61_2",
      "doi-asserted-by": "crossref",
      "first-page": "29",
      "DOI": "10.1046/j.1462-5822.2002.00167.x",
      "volume": "4",
      "year": "2002",
      "unstructured": "Tobe, T., and C. Sasakawa. 2002. Species-specific cell adhesion of enteropathogenic Escherichia coli is mediated by type IV bundle-forming pili. Cell. Microbiol. 4 : 29-42.",
      "journal-title": "Cell. Microbiol."
    },
    {
      "key": "e_1_3_2_62_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.188.2.370-377.2006"
    },
    {
      "key": "e_1_3_2_63_2",
      "doi-asserted-by": "crossref",
      "first-page": "1031",
      "DOI": "10.1016/j.jmb.2008.03.028",
      "volume": "378",
      "year": "2008",
      "unstructured": "Trindade, M. B., V. Job, C. Contreras-Martel, V. Pelicic, and A. Dessen. 2008. Structure of a widely conserved type IV pilus biogenesis factor that affects the stability of secretin multimers. J. Mol. Biol. 378 : 1031-1039.",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "e_1_3_2_64_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.187.4.1455-1464.2005"
    },
    {
      "key": "e_1_3_2_65_2",
      "doi-asserted-by": "crossref",
      "first-page": "680",
      "DOI": "10.1111/j.1365-2958.2006.05414.x",
      "volume": "62",
      "year": "2006",
      "unstructured": "Varga, J. J., V. Nguyen, D. K. O'Brien, K. Rodgers, R. A. Walker, and S. B. Melville. 2006. Type IV pili-dependent gliding motility in the gram-positive pathogen Clostridium perfringens and other clostridia. Mol. Microbiol. 62 : 680-694.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_66_2",
      "doi-asserted-by": "crossref",
      "first-page": "49",
      "DOI": "10.1016/S0378-1119(96)00403-9",
      "volume": "180",
      "year": "1996",
      "unstructured": "Watson, A. A., R. A. Alm, and J. S. Mattick. 1996. Identification of a gene, pilF, required for type 4 fimbrial biogenesis and twitching motility in Pseudomonas aeruginosa. Gene 180 : 49-56.",
      "journal-title": "Gene"
    },
    {
      "key": "e_1_3_2_67_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.170.6.2592-2598.1988"
    },
    {
      "key": "e_1_3_2_68_2",
      "doi-asserted-by": "crossref",
      "first-page": "8348",
      "DOI": "10.1073/pnas.0305969101",
      "volume": "101",
      "year": "2004",
      "unstructured": "Wu, B., P. Li, Y. Liu, Z. Lou, Y. Ding, C. Shu, S. Ye, M. Bartlam, B. Shen, and Z. Rao. 2004. 3D structure of human FK506-binding protein 52: implications for the assembly of the glucocorticoid receptor/Hsp90/immunophilin heterocomplex. Proc. Natl. Acad. Sci. USA 101 : 8348-8353.",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_69_2",
      "doi-asserted-by": "crossref",
      "first-page": "976",
      "DOI": "10.1107/S0907444905011558",
      "volume": "61",
      "year": "2005",
      "unstructured": "Xu, H., C. M. Weeks, and H. A. Hauptman. 2005. Optimizing statistical Shake-and-Bake for Se-atom substructure determination. Acta Crystallogr. D 61 : 976-981.",
      "journal-title": "Acta Crystallogr. D"
    },
    {
      "key": "e_1_3_2_70_2",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1038/sj.emboj.7600496",
      "volume": "24",
      "year": "2005",
      "unstructured": "Yang, J., S. M. Roe, M. J. Cliff, M. A. Williams, J. E. Ladbury, P. T. Cohen, and D. Barford. 2005. Molecular basis for TPR domain-mediated regulation of protein phosphatase 5. EMBO J. 24 : 1-10.",
      "journal-title": "EMBO J."
    },
    {
      "key": "e_1_3_2_71_2",
      "doi-asserted-by": "crossref",
      "first-page": "2405",
      "DOI": "10.1099/mic.0.2007/007781-0",
      "volume": "153",
      "year": "2007",
      "unstructured": "Zenk, S. F., D. Stabat, J. L. Hodgkinson, A. K. Veenendaal, S. Johnson, and A. J. Blocker. 2007. Identification of minor inner-membrane components of the Shigella type III secretion system \u201cneedle complex.\u201d Microbiology 153 : 2405-2415.",
      "journal-title": "\u201d Microbiology"
    },
    {
      "key": "e_1_3_2_72_2",
      "doi-asserted-by": "crossref",
      "first-page": "18526",
      "DOI": "10.1073/pnas.0706441104",
      "volume": "104",
      "year": "2007",
      "unstructured": "Zhang, Y., and D. C. Chan. 2007. Structural basis for recruitment of mitochondrial fission complexes by Fis1. Proc. Natl. Acad. Sci. USA 104 : 18526-18530.",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    }
  ],
  "container-title": "Journal of Bacteriology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JB.00996-08",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JB.00996-08",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        2,
        29
      ]
    ],
    "date-time": "2024-02-29T17:07:03Z",
    "timestamp": 1709226423000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/JB.00996-08"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2008,
        11
      ]
    ]
  },
  "references-count": 71,
  "journal-issue": {
    "issue": "21",
    "published-print": {
      "date-parts": [
        [
          2008,
          11
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/JB.00996-08"
  ],
  "URL": "http://dx.doi.org/10.1128/JB.00996-08",
  "relation": {},
  "ISSN": [
    "0021-9193",
    "1098-5530"
  ],
  "subject": [],
  "container-title-short": "J Bacteriol",
  "published": {
    "date-parts": [
      [
        2008,
        11
      ]
    ]
  },
  "assertion": [
    {
      "value": "2008-07-18",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2008-08-25",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2020-12-20",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}