Structure of the filamentous phage pIV multimer by cryo-electron microscopy

Journal of Molecular Biology

Volumn 325, Issue 3, 2003, Pages 461-470

  Opalka, Natacha ^a   Beckmann, Roland ^b   Boisset, Nicolas ^c   Simon, Martha N ^d   Russel, Marjorie ^a   Darst, Seth A ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^d BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Cryo electron microscopy; Filamentous phage; Membrane protein; pIV; Secretin

Indexed keywords

CYSTEINE; OUTER MEMBRANE PROTEIN; POLYMER; PROTEIN PIV; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE; CHANNEL GATING; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; IMAGE ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; THREE DIMENSIONAL IMAGING;

ESCHERICHIA COLI; HOMO;

EID: 0037225318     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01246-9     Document Type: Article

References (42)

1. Russel, M. (1991). Filamentous phage assembly. Mol. Microbiol. 5, 1607-1613.
2. Russel, M. (1993). Protein-protein interactions during filamentous phage assembly. J. Mol. Biol. 231, 689-697.
3. Feng, J-N., Model, P. & Russel, M. (1999). A trans-envelope protein complex needed for filamentous phage assembly and export. Mol. Microbiol. 34, 745-755.
4. Lopez, J. & Webster, R. E. (1985). Assembly site of bacteriophage f1 corresponds to adhesion zones between the inner and outer membranes of the host cell. J. Bacteriol. 163, 1270-1274.
5. Feng, J-N., Russel, M. & Model, P. (1997). A permeabilized cell system that assembles filamentous bacteriophage. Proc. Natl. Acad. Sci. USA, 94, 4068-4073.
6. Rapoza, M. P. & Webster, R. E. (1995). The products of gene I and the overlapping in-frame gene XI are required for filamentous phage assembly. J. Mol. Biol. 248, 627-638.
7. Kazmierczak, B., Mielke, D. L., Russel, M. & Model, P. (1994). Filamentous phage pIV forms a multimer that mediates phage export across the bacterial cell. J. Mol. Biol. 238, 187-198.
8. Brissette, J. L. & Russel, M. (1990). Secretion and membrane integration of a filamentous phage-encoded morphogenic protein. J. Mol. Biol. 211, 565-580.
9. Russel, M. & Kazmierczak, B. (1993). Analysis of the structure and subcellular location of filamentous phage pIV. J. Bacteriol. 175, 3998-4007.
10. Linderoth, N. A., Simon, M. N. & Russel, M. (1997). The filamentous phage pIV multimer visualized by scanning transmission electron microscopy. Science, 278, 1635-1638.
11. Pugsley, A. P. (1993). The complete general secretary pathway in Gram-negative bacteria. Microbiol. Rev. 57 , 50-108.
12. Russel, M. (1998). Macromolecular assembly and secretion across the bacterial cell envelope: Type II protein secretion systems. J. Mol. Biol. 279, 485-499.
13. Stathopoulos, C., Hendrixson, D. R., Thanassi, D. G., Hultgren, S. J., St Geme, J. W. & Curtiss, R. (2000). Secretion of virulence determinants by the general secretory pathway in gram-negative pathogens: An evolving story. Microbes Infect. 2, 1061-1072.
14. Galan, J. E. & Collmer, A. (1999). Type III secretion machines: Bacterial devices for protein delivery into host cells. Science, 284, 1322-1328.
15. Hardie, K. R., Lory, S. & Pugsley, A. P. (1996). Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 15, 978-988.
16. Bitter, W., Koster, M., Latijnhouwers, M., De Cock, H. & Tommassen, J. (1998). Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. Mol. Microbiol. 27, 209-219.
17. Koster, M., Bitter, W., de Cock, H., Allaoui, A., Cornelis, G. R. & Tommassen, J. (1997). The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Mol. Microbiol. 26, 789-797.
18. Crago, A. & Koronalds, V. (1998). Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization. Mol. Microbiol. 30, 47-56.
19. Nouwen, N., Ranson, N., Saibil, H., Wolpensinger, B., Engel, A., Ghazi, A. & Pugsley, A. P. (1999). Secretin PulD: Association with pilot PulS, structure, and ion-conducting channel formation. Proc. Natl. Acad. Sci. USA, 96, 8173-8177.
20. Russel, M., Linderoth, N. A. & Sali, A. (1997). Filamentous phage assembly: Variation on a protein export theme. Gene, 192, 23-32.
21. Marciano, D. K., Russel, M. & Simon, S. M. (1999). An aqueous channel for filamentous phage export. Science, 284, 1516-1519.
22. Marciano, D. K., Russel, M. & Simon, S. M. (2001). Assembling filamentous phage occlude pIV channels. Proc. Natl. Acad. Sci. USA, 98, 9359-9364.
23. C-hemocyanins)of Helix pomatia from frozen-hydrated specimens. J. Mol. Biol. 248, 431-448.
24. Nouwen, N., Stahlberg, H., Pugsley, A. P. & Engel, A. (2000). Domain structure of secretin PulD revealed by limited proteolysis and electron microscopy. EMBO. J. 19, 2229-2236.
25. Daefler, S., Russel, M. & Model, P. (1997). Module swaps between related translocator proteins pIV(f1), pIV(IKe) and PulD: Identification of a specificity domain. J. Mol. Biol. 266, 978-992.
26. Ferguson, A. D., Hofmann, E., Coulton, J. W., Diederichs, K. & Welte, W. (1998). Siderophore-mediated iron transport: Crystal structure of FhuA with bound lipopolysaccharide. Science, 282, 2215-2220.
27. Locher, K. P., Rees, B., Koebnik, R., Mitschler, A., Mouliner, L., Rosenbush, J. P. & Moras, D. (1998). Transmembrane signalling across the ligand-gated FhuA receptor: Crystal structures of free and ferri-chrome-bound states reveal allosteric changes. Cell, 95 , 771-778.
28. Buchanan, S. K., Smith, B. S., Venkatramani, L., Xia, D., Esser, L., Palnitkar, M. et al. (1999). Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nature Struct. Biol. 6, 56-63.
29. Ferguson, A. D., Chakraborty, R., Smith, B. S., Esser, L., van der Helm, D. & Deisenhofer, J. (2002). Structural basis of gating by the outer membrane transporter FecA. Science, 295, 1715-1719.
30. Larsen, R. A., Thomas, M. G. & Postle (1999). Proton-motive force, ExbB and ligand-bound FepA drive conformational changes in TonB. Mol. Microbiol. 31, 1809-1824.
31. Russel, M. (1994). Mutants at conserved positions in gene IV, a gene required for assembly and secretion of filamentous phage. Mol. Microbiol. 14, 357-369.
32. Hottenrott, S., Schumann, T., Plückthun, A., Fischer, G. & Rahfeld, J-U. (1997). The Escherichia coli SlyD is a metal ion-regulated peptidylprolyl cis/transisomerase. J. Biol. Chem. 272, 15697-15701.
33. Roof, W. D., Horne, S. M., Young, K. D. & Young, R. (1994). slyD, a host gene required for fXl74 lysis, is related to the FK506-binding protein family of pepti-dyl-prolyl cis-trans isomerases. J. Biol. Chem. 269, 2902-2910.
34. Gottesman, S. & Stout, V. (1991). Regulation of capsular polysaccharide synthesis in Escherichia coli K-12. Mol. Microbiol. 5, 1599-1606.
35. Torres-Cabassa, A. S. & Gottesman, S. (1987). Capsule synthesis in Escherichia coli K-12 is regulated by proteolysis. J. Bacteriol. 169, 981-989.
36. Lessl, M., Balzer, D., Lurz, R., Waters, V. L., Guiney, D. G. & Lanka, E. (1992). Dissection of IncP conjugative plasmid transfer: Definition of the transfer region Tra2 by mobilization of the Tra1 region in trans. J. Bacteriol. 174, 2493-2500.
37. Han, J. C. & Han, G. Y. (1994). A procedure for quantitative determination of tris(2-carboxyethyl)-phosphine, an odorless reducing agent more stable and effective than dithithreitol. Anal. Biochem. 220, 5-10.
38. . Wall, J. S. (1979). Introduction to Analytical Electron Microscopy (Hren, J. J., Goldstein, J. I. & Joy, D. C., eds), pp. 333-342, Plenum Publishing Corporation, New York.
39. Wall, J. S. & Hainfeld, J. F. (1986). Mass mapping with the scanning transmission electron microscope. Annu. Rev. Biophys. Biophys. Chem. 15, 355-376.
40. Wall, J. S., Hainfeld, J. F. & Simon, M. N. (1998). Scanning transmission electron microscopy (STEM) of nuclear structures. In Methods in Cell Biology, Nuclear Structure and Function (Berrios, M., ed.), pp. 139-166, Academic press, New York.
41. Crowther, R. A. & Amos, L. A. (1971). Harmonic analysis of electron microscope images with rotational symmetry. J. Mol. Biol. 60, 123-130.
42. Boisset, N., Penczek, P. A., Taveau, J-C., You, V., de Haas, F. & Lamy, J. (1998). Overabundant single-particle electron microscope views induce a three-dimensional reconstruction artifact. Ultramicroscopy, 74 , 201-207.