Importance of conserved residues of the serine protease autotransporter β-domain in passenger domain processing and β-barrel assembly

Infection and Immunity

Volumn 78, Issue 8, 2010, Pages 3516-3528

  Yen, Yihfen T ^a   Tsang, Casey ^a   Cameron, Todd A ^a   Ankrah, Dennis O ^a   Rodou, Athina ^a   Stathopoulos, Christos ^a  

^a CALIFORNIA STATE POLYTECHNIC UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN SPATE; SERINE PROTEINASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; ESCHERICHIA COLI PROTEIN; ESPP PROTEIN, E COLI; MUTANT PROTEIN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL OUTER MEMBRANE; CELL FRACTIONATION; ENTEROBACTERIACEAE; GENE INSERTION; GENE MUTATION; IMMUNOCHEMISTRY; INTRACELLULAR SPACE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; SITE DIRECTED MUTAGENESIS;

AMINO ACID SUBSTITUTION; CONSERVED SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IMMUNOCHEMISTRY; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROTEIN FOLDING; SERINE ENDOPEPTIDASES; VIRULENCE FACTORS;

EID: 77955292666     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00390-10     Document Type: Article

References (45)

1. Barnard, T. J., N. Dautin, P. Lukacik, H. D. Bernstein, and S. K. Buchanan. 2007. Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat. Struct. Mol. Biol. 14:1214-1220.
2. Brandon, L. D., and M. B. Goldberg. 2001. Periplasmic transit and disulfide bond formation of the autotransported Shigella protein IcsA. J. Bacteriol. 183:951-958.
3. Dautin, N., T. J. Barnard, D. E. Anderson, and H. D. Bernstein. 2007. Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism. EMBO J. 26:1942-1952. (Pubitemid 46624049)
4. Dautin, N., and H. D. Bernstein. 2007. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 61:89-112.
5. Egile, C., H. d'Hauteville, C. Parsot, and P. J. Sansonetti. 1997. SopA, the outer membrane protease responsible for polar localization of IcsA in Shigella flexneri. Mol. Microbiol. 23:1063-1073.
6. Henderson, I. R., F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, and D. Ala'Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
7. Henderson, I. R., F. Navarro-Garcia, and J. P. Nataro. 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:370-378. (Pubitemid 28473198)
8. Hendrixson, D. R., M. L. de la Morena, C. Stathopoulos, and J. W. St. Geme III. 1997. Structural determinants of processing and secretion of the Haemophilus influenzae Hap protein. Mol. Microbiol. 26:505-518.
9. Hennecke, G., J. Nolte, R. Volkmer-Engert, J. Schneider-Mergener, and S. Behrens. 2005. The periplasmic chaperone SurA exploits two features characteristic of integral outer membrane proteins for selective substrate recognition. J. Biol. Chem. 280:23540-23548.
10. Hodak, H., and F. Jacob-Dubuisson. 2007. Current challenges in autotransport and two-partner protein secretion pathways. Res. Microbiol. 158:631-637.
11. Ieva, R., and H. D. Bernstein. 2009. Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. U. S. A. 106:19120-19125.
12. Ieva, R., K. M. Skillman, and H. D. Bernstein. 2008. Incorporation of a polypeptide segment into the beta-domain pore during the assembly of a bacterial autotransporter. Mol. Microbiol. 67:188-201.
13. Jackups, R., Jr., and J. Liang. 2005. Interstrand pairing patterns in betabarrel membrane proteins: the positive-outside rule, aromatic rescue, and strand registration prediction. J. Mol. Biol. 354:979-993.
14. Jacob-Dubuisson, F., R. Fernandez, and L. Coutte. 2004. Protein secretion through autotransporter and two-partner pathways. Biochim. Biophys. Acta 1694:235-257.
15. Jain, S., and M. B. Goldberg. 2007. Requirement for YaeT in the outer membrane assembly of autotransporter proteins. J. Bacteriol. 189:5393-5398. (Pubitemid 47076086)
16. Jong, W. S., C. M. ten Hagen-Jongman, T. den Blaauwen, D. Jan Slotboom, J. R. Tame, D. Wickstrom, J. W. de Gier, B. R. Otto, and J. Luirink. 2007. Limited tolerance towards folded elements during secretion of the autotransporter Hbp. Mol. Microbiol. 63:1524-1536.
17. Kostakioti, M., and C. Stathopoulos. 2004. Functional analysis of the Tsh autotransporter from an avian pathogenic Escherichia coli strain. Infect. Immun. 72:5548-5554.
18. Kostakioti, M., and C. Stathopoulos. 2006. Role of the alpha-helical linker of the C-terminal translocator in the biogenesis of the serine protease sub-family of autotransporters. Infect. Immun. 74:4961-4969.
19. Lazar, S. W., and R. Kolter. 1996. SurA assists the folding of Escherichia coli outer membrane proteins. J. Bacteriol. 178:1770-1773. (Pubitemid 26085629)
20. Newman, C. L., and C. Stathopoulos. 2004. Autotransporter and two-partner secretion: delivery of large-size virulence factors by gram-negative bacterial pathogens. Crit. Rev. Microbiol. 30:275-286.
21. Nikaido, H., and M. Vaara. 1987. Outer membrane, p. 7-22. In F. Neidhardt (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol. 1. ASM Press, Washington, DC.
22. Oomen, C. J., P. van Ulsen, P. van Gelder, M. Feijen, J. Tommassen, and P. Gros. 2004. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23:1257-1266.
23. Pohlner, J., R. Halter, K. Beyreuther, and T. F. Meyer. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458-462. (Pubitemid 17056417)
24. Provence, D. L., and R. Curtiss III. 1994. Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect. Immun. 62:1369-1380.
25. Purdy, G. E., C. R. Fisher, and S. M. Payne. 2007. IcsA surface presentation in Shigella flexneri requires the periplasmic chaperones DegP, Skp, and SurA. J. Bacteriol. 189:5566-5573.
26. Rasband, W. S. 1997-2008. ImageJ. National Institutes of Health, Bethesda, MD.
27. Robert, V., E. B. Volokhina, F. Senf, M. P. Bos, P. Van Gelder, and J. Tommassen. 2006. Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol. 4:e377.
28. Ruiz-Perez, F., I. R. Henderson, D. L. Leyton, A. E. Rossiter, Y. Zhang, and J. P. Nataro. 2009. Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J. Bacteriol. 191: 6571-6583.
29. Rutherford, N., M. E. Charbonneau, F. Berthiaume, J. M. Betton, and M. Mourez. 2006. The periplasmic folding of a cysteineless autotransporter passenger domain interferes with its outer membrane translocation. J. Bacteriol. 188:4111-4116. (Pubitemid 43825414)
30. Schnaitman, C. A. 1970. Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli. J. Bacteriol. 104:890-901.
31. Shere, K. D., S. Sallustio, A. Manessis, T. G. D'Aversa, and M. B. Goldberg. 1997. Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility. Mol. Microbiol. 25:451-462.
32. Skillman, K. M., T. J. Barnard, J. H. Peterson, R. Ghirlando, and H. D. Bernstein. 2005. Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol. Microbiol. 58:945-958.
33. Soto, G. E., K. W. Dodson, D. Ogg, C. Liu, J. Heuser, S. Knight, J. Kihlberg, C. H. Jones, and S. J. Hultgren. 1998. Periplasmic chaperone recognition motif of subunits mediates quaternary interactions in the pilus. EMBO J. 17:6155-6167.
34. Stathopoulos, C., D. L. Provence, and R. Curtiss III. 1999. Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect. Immun. 67:772-781.
35. Strauch, K. L., K. Johnson, and J. Beckwith. 1989. Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J. Bacteriol. 171:2689-2696.
36. Struyve, M., M. Moons, and J. Tommassen. 1991. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J. Mol. Biol. 218:141-148.
37. Voulhoux, R., M. P. Bos, J. Geurtsen, M. Mols, and J. Tommassen. 2003. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299:262-265. (Pubitemid 36125214)
38. Voulhoux, R., and J. Tommassen. 2004. Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res. Microbiol. 155:129-135.
39. Walsh, N. P., B. M. Alba, B. Bose, C. A. Gross, and R. T. Sauer. 2003. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113:61-71.
40. Wang, R. F., and S. R. Kushner. 1991. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
41. Wu, T., J. Malinverni, N. Ruiz, S. Kim, T. J. Silhavy, and D. Kahne. 2005. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235-245. (Pubitemid 40546391)
42. Xu, X., S. Wang, Y. X. Hu, and D. B. McKay. 2007. The periplasmic bacterial molecular chaperone SurA adapts its structure to bind peptides in different conformations to assert a sequence preference for aromatic residues. J. Mol. Biol. 373:367-381.
43. Yen, Y. T., A. Karkal, M. Bhattacharya, R. C. Fernandez, and C. Stathopoulos. 2007. Identification and characterization of autotransporter proteins of Yersinia pestis KIM. Mol. Membr. Biol. 24:28-40.
44. Yen, Y. T., M. Kostakioti, I. R. Henderson, and C. Stathopoulos. 2008. Common themes and variations in serine protease autotransporters. Trends Microbiol. 16:370-379.
45. Yen, Y. T., and C. Stathopoulos. 2007. Identification of autotransporter proteins secreted by type v secretion systems in gram-negative bacteria. Methods Mol. Biol. 390:33-46.