DOI: 10.1126/science.278.5343.1635. The Filamentous Phage pIV Multimer Visualized by Scanning Transmission Electron Microscopy

The Filamentous Phage pIV Multimer Visualized by Scanning Transmission Electron Microscopy

10.1126/science.278.5343.1635

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

A family of homomultimeric outer-membrane proteins termed secretins mediates the secretion of large macromolecules such as enzymes and filamentous bacteriophages across bacterial outer membranes to the extracellular milieu. The secretin encoded by filamentous phage f1 was purified. Mass determination of individual molecules by scanning transmission electron microscopy revealed two forms, a unit multimer composed of about 14 subunits and a multimer dimer. The secretin is roughly cylindrical and has an internal diameter of about 80 angstroms, which is large enough to accommodate filamentous phage (diameter of 65 angstroms).

Bibliography

Linderoth, N. A., Simon, M. N., & Russel, M. (1997). The Filamentous Phage pIV Multimer Visualized by Scanning Transmission Electron Microscopy. Science, 278(5343), 1635â1638.

Authors 3

Nora A. Linderoth (first)
Martha N. Simon (additional)
Marjorie Russel (additional)

References 33 Referenced 112

Hobbs M., Mattick J. S., Mol. Microbiol. 10, 233 (1993); (10.1111/j.1365-2958.1993.tb01949.x) / Mol. Microbiol. by Hobbs M. (1993)
Pugsley A. P., Microbiol. Rev. 57, 50 (1993); (10.1128/mr.57.1.50-108.1993) / Microbiol. Rev. by Pugsley A. P. (1993)
Salmond G., Reeves P., Trends Biochem. Sci. 18, 7 (1993); (10.1016/0968-0004(93)90080-7) / Trends Biochem. Sci. by Salmond G. (1993)
Genin S., Boucher C. A., Mol. Gen. Genet. 243, 112 (1994); (10.1007/BF00283883) / Mol. Gen. Genet. by Genin S. (1994)
Lee C. A., Trends Microbiol. 5, 148 (1997). (10.1016/S0966-842X(97)01029-9) / Trends Microbiol. by Lee C. A. (1997)
Russel M., Science 265, 612 (1994). (10.1126/science.8036510) / Science by Russel M. (1994)
Waldor M. K., Mekalanos J. J., ibid. 272, 1910 (1996). / ibid. by Waldor M. K. (1996)
P. Model and M. Russel Bacteriophages 2 375 (1988); (10.1007/978-1-4684-5490-1_6)
Russel M., Mol. Microbiol. 5, 1607 (1991); (10.1111/j.1365-2958.1991.tb01907.x) / Mol. Microbiol. by Russel M. (1991)
Endemann H., Model P., J. Mol. Biol. 250, 496 (1995) ; (10.1006/jmbi.1995.0393) / J. Mol. Biol. by Endemann H. (1995)
Russel M., Trends Microbiol. 3, 223 (1995). (10.1016/S0966-842X(00)88929-5) / Trends Microbiol. by Russel M. (1995)
Kazmierczak B. I., Mielke D. L., Russel M., Model P., J. Mol. Biol. 238, 187 (1994). (10.1006/jmbi.1994.1280) / J. Mol. Biol. by Kazmierczak B. I. (1994)
Chen L.-Y., Chen D.-Y., Miaw J., Hu N.-T., J. Biol. Chem. 271, 2703 (1996). (10.1074/jbc.271.5.2703) / J. Biol. Chem. by Chen L.-Y. (1996)
Hardie K. R., Lory S., Pugsley A. P., EMBO J. 15, 978 (1996). (10.1002/j.1460-2075.1996.tb00434.x) / EMBO J. by Hardie K. R. (1996)
Shevchik V. E., Robert-Badouy J., Condemine G., ibid. 16, 3007 (1997). / ibid. by Shevchik V. E. (1997)
Newhalv W. J., Wilde C. E., Sawyer W. D., Haak R. A., Infect. Immun. 27, 475 (1980). (10.1128/iai.27.2.475-482.1980) / Infect. Immun. by Newhalv W. J. (1980)
Drake S. L., Koomey M., Mol. Microbiol. 18, 975 (1995). (10.1111/j.1365-2958.1995.18050975.x) / Mol. Microbiol. by Drake S. L. (1995)
Linderoth N. A., Model P., Russel M., J. Bacteriol. 178, 1962 (1996). (10.1128/jb.178.7.1962-1970.1996) / J. Bacteriol. by Linderoth N. A. (1996)
Daefler S., Russel M., Model P., J. Mol. Biol. 266, 978 (1997). (10.1006/jmbi.1996.0866) / J. Mol. Biol. by Daefler S. (1997)
Liu J., Rutz J. M., Feix J. B., Klebba P. E., Proc. Natl. Acad. Sci. U.S.A. 90, 10653 (1993); (10.1073/pnas.90.22.10653) / Proc. Natl. Acad. Sci. U.S.A. by Liu J. (1993)
Nikaido H.J. Biol. Chem.26919943905. 14. (10.1016/S0021-9258(17)41716-9) / J. Biol. Chem. by Nikaido H. (1994)
Russel M., Linderoth N. A., Sali A., Gene 192, 23 (1997). (10.1016/S0378-1119(96)00801-3) / Gene by Russel M. (1997)
N. A. Linderoth M. Russel P. Model unpublished results.
In brief His-tagged pIV with His(×7) inserted after Ala 308 and Ser 318 → Ile (11) was expressed from plasmid pPMR132. Cells were lysed after incubation with lysozyme and treated with ribonuclease A and deoxyribonuclease I and the membranes were isolated by centrifugation and suspended in buffer containing the nonionic detergent octyl-poly-oxyethylene (4%). Solubilized material was bound to Ni-Sepharose beads washed with buffer containing 1% CHAPS and eluted with imidazole in the same buffer. The pIV-containing fractions were pooled concentrated and chromatographed on Bio-Gel A5M (Bio-Rad Hercules CA) also in buffer containing 1% CHAPS. Peak fractions were used for the STEM.
Lindeberg M., Salmond G. P. C., Collmer A., Mol. Microbiol. 20, 175 (1996). (10.1111/j.1365-2958.1996.tb02499.x) / Mol. Microbiol. by Lindeberg M. (1996)
N. A. Linderoth M. N. Simon M. Russel data not shown.
Laver W. G., Valentine R. C., Virology 38, 105 (1969). (10.1016/0042-6822(69)90132-9) / Virology by Laver W. G. (1969)
10.1038/358727a0
10.1126/science.7824948
J. S. Wall in Introduction to Analytical Electron Microscopy J. J. Hren J. I. Goldstein D. C. Joy Eds. (Plenum New York 1979) pp. 333-342 (10.1007/978-1-4757-5581-7_12)
J. S. Wall J. F. Hainfeld K. D. Chung in Proceedings of the 43rd Annual Meeting of the Electron Microscopy Society of America G. W. Bailey Ed. (San Francisco Press San Francisco CA 1985) pp. 716-717; (10.1017/S0424820100120278)
10.1146/annurev.bb.15.060186.002035
We thank P. Model for suggestions interest encouragement and criticism of the manuscript; B. Lin for STEM specimen preparation; and J. Wall for helpful discussions about the data analysis. Supported by NSF grant MCB93-16625 (M.R.). The Brookhaven National Laboratory STEM is an NIH Supported Resource Center (NIH grant P41-RR01777) with additional support provided by the U.S. Department of Energy Office of Health and Environmental Research.

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 5:45 a.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 11:49 p.m.)
Indexed	1 year, 1 month ago (July 27, 2024, 11:49 a.m.)
Issued	27 years, 8 months ago (Nov. 28, 1997)
Published	27 years, 8 months ago (Nov. 28, 1997)
Published Print	27 years, 8 months ago (Nov. 28, 1997)

Funders 0

None

BibTeX

@article{Linderoth_1997, title={The Filamentous Phage pIV Multimer Visualized by Scanning Transmission Electron Microscopy}, volume={278}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.278.5343.1635}, DOI={10.1126/science.278.5343.1635}, number={5343}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Linderoth, Nora A. and Simon, Martha N. and Russel, Marjorie}, year={1997}, month=nov, pages={1635–1638} }

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