A new means to identify type 3 secreted effectors: Functionally interchangeable class IB chaperones recognize a conserved sequence

mBio

Volumn 3, Issue 1, 2012, Pages 1-10

  Costa, Sonia C P ^a   Schmitz, Alexa M ^a   Jahufar, Fathima F ^a   Boyd, Justin D ^b   Cho, Min Y ^a   Glicksman, Marcie A ^b   Lesser, Cammie F ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; BACTERIAL PROTEIN;

ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL SECRETION SYSTEM; CONTROLLED STUDY; ENDOSYMBIONT; GENE SEQUENCE; GENETIC CONSERVATION; GRAM NEGATIVE BACTERIUM; HOST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEUS; SALMONELLA; SHIGELLA; YERSINIA; BIOLOGY; ENTEROBACTERIACEAE; ENZYME SPECIFICITY; HELA CELL; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM; SITE DIRECTED MUTAGENESIS; SPECIES DIFFERENCE; SYMBIOSIS;

BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; SHIGELLA; SODALIS GLOSSINIDIUS;

ALGORITHMS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; ENTEROBACTERIACEAE; HELA CELLS; HUMANS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM; SHIGELLA; SPECIES SPECIFICITY; SUBSTRATE SPECIFICITY; SYMBIOSIS;

EID: 84857874120     PISSN: None     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00243-11     Document Type: Article

References (45)

1. Troisfontaines P, Cornelis GR. 2005. Type III secretion: more systems than you think. Physiology (Bethesda) 20:326-339.
2. Schesser K, Frithz-Lindsten E, Wolf-Watz H. 1996. Delineation and mutational analysis of the Yersinia pseudotuberculosis YopE domains which mediate translocation across bacterial and eukaryotic cellular membranes. J. Bacteriol. 178:7227-7233.
3. Sory MP, Boland A, Lambermont I, Cornelis GR. 1995. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc. Natl. Acad. Sci. U. S. A. 92:11998-12002.
4. Buchko GW, et al. 2010. A multi-pronged search for a common structural motif in the secretion signal ofSalmonella enterica serovar Typhimu-rium type III effector proteins. Mol. Biosyst. 6:2448-2458.
5. Arnold R, et al. 2009. Sequence-based prediction of type III secreted proteins. PLoS Pathog. 5:e1000376.
6. Löwer M, Schneider G. 2009. Prediction of type III secretion signals in genomes of gram-negative bacteria. PLoS One 4:e5917.
7. Samudrala R, Heffron F, McDermott JE. 2009. Accurate prediction of secreted substrates and identification of a conserved putative secretion signal for type III secretion systems. PLoS Pathog. 5:e1000375.
8. Parsot C, Hamiaux C, Page AL. 2003. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6:7-14.
9. van Eerde A, Hamiaux C, Pérez J, Parsot C, Dijkstra BW. 2004. Structure of Spa15, a type III secretion chaperone from Shigella flexneri with broad specificity. EMBO Rep. 5:477-483.
10. Birtalan SC, Phillips RM, Ghosh P. 2002. Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol. Cell 9:971-980.
11. Lilic M, Vujanac M, Stebbins CE. 2006. A common structural motif in the binding of virulence factors to bacterial secretion chaperones. Mol. Cell 21:653-664.
12. Schubot FD, et al. 2005. Three-dimensional structure of a macromolec-ular assembly that regulates type III secretion in Yersinia pestis. J. Mol. Biol. 346:1147-1161.
13. Stebbins CE, Galán JE. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414:77-81.
14. Hachani A, et al. 2008. IpgB1 and IpgB2, two homologous effectors secreted via the Mxi-Spa type III secretion apparatus, cooperate to mediate polarized cell invasion and inflammatory potential of Shigella flexneri. Microbes Infect. 10:260-268.
15. Page AL, Sansonetti P, Parsot C. 2002. Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol. Microbiol. 43: 1533-1542.
16. Schmitz AM, Morrison MF, Agunwamba AO, Nibert ML, Lesser CF. 2009. Protein interaction platforms: visualization of interacting proteins in yeast. Nat. Methods 6:500-502.
17. Ehrbar K, Friebel A, Miller SI, Hardt WD. 2003. Role of the Salmonella pathogenicity island 1 (SPI-1) protein InvB in type III secretion of SopE and SopE2, two Salmonella effector proteins encoded outside of SPI-1. J. Bacteriol. 185:6950-6967.
18. Ghosh P. 2004. Process of protein transport by the type III secretion system. Microbiol. Mol. Biol. Rev. 68:771-795.
19. Kenny B, Warawa J. 2001. Enteropathogenic Escherichia coli (EPEC) Tir receptor molecule does not undergo full modification when introduced into host cells by EPEC-independent mechanisms. Infect. Immun. 69: 1444-1453.
20. Rosqvist R, Håkansson S, Forsberg A, Wolf-Watz H. 1995. Functional conservation of the secretion and translocation machinery for virulence proteins of yersiniae, salmonellae and shigellae. EMBO J. 14:4187-4195.
21. de Groot JC, et al. 2011. Structural basis for complex formation between human IRSp53 and the translocated intimin receptor tir of enterohemor-rhagic E. coli. Structure 19:1294-1306.
22. Bronstein PA, Miao EA, Miller SI. 2000. InvB is a type III secretion chaperone specific for SspA. J. Bacteriol. 182:6638-6644.
23. Ehrbar K, Hapfelmeier S, Stecher B, Hardt WD. 2004. InvB is required for type III-dependent secretion of SopA in Salmonella enterica serovar Typhimurium. J. Bacteriol. 186:1215-1219.
24. Weiss DS, Chen JC, Ghigo JM, Boyd D, Beckwith J. 1999. Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J. Bacteriol. 181:508-520.
25. Estojak J, Brent R, Golemis EA. 1995. Correlation of two-hybrid affinity data with in vitro measurements. Mol. Cell. Biol. 15:5820-5829.
26. Alto NM, et al. 2006. Identification of a bacterial type III effector family with G protein mimicry functions. Cell 124:133-145.
27. Cooper CA, et al. 2010. Structural and biochemical characterization of SrcA, a multi-cargo type III secretion chaperone in Salmonella required for pathogenic association with a host. PLoS Pathog. 6:e1000751.
28. Thomas NA, et al. 2005. CesT is a multi-effector chaperone and recruitment factor required for the efficient type III secretion of both LEE- and non-LEE-encoded effectors ofenteropathogenicEscherichia coli. Mol. Mi-crobiol. 57:1762-1779.
29. Pearson MM, Mobley HL. 2007. The type III secretion system of Proteus mirabilis HI4320 does not contribute to virulence in the mouse model of ascending urinary tract infection. J. Med. Microbiol. 56:1277-1283.
30. Stevens MP, et al. 2002. An Inv/Mxi-Spa-like type III protein secretion system in Burkholderia pseudomallei modulates intracellular behaviour of the pathogen. Mol. Microbiol. 46:649-659.
31. Haller JC, Carlson S, Pederson KJ, Pierson DE. 2000. A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence. Mol. Microbiol. 36:1436-1446.
32. Dale C, Jones T, Pontes M. 2005. Degenerative evolution and functional diversification of type-III secretion systems in the insect endosymbiont Sodalis glossinidius. Mol. Biol. Evol. 22:758-766.
33. Toh H, et al. 2006. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 16:149-156.
34. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA. 2009. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc. Natl. Acad. Sci. U. S. A. 106:9063-9068.
35. Charpentier X, Oswald E. 2004. Identification of the secretion and trans-location domain of the enteropathogenic and enterohemorrhagic Esche-richia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J. Bacteriol. 186:5486-5495.
36. Biegert A, Mayer C, Remmert M, Söding J, Lupas AN. 2006. The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res. 34:W335-W339.
37. Schuch R, Sandlin RC, Maurelli AT. 1999. A system for identifying post-invasion functions of invasion genes: requirements for the Mxi-Spa type III secretion pathway of Shigella flexneri in intercellular dissemination. Mol. Microbiol. 34:675-689.
38. McDermott JE, et al. 2011. Computational prediction of type III and IV secreted effectors in gram-negative bacteria. Infect. Immun. 79:23-32.
39. Rodgers L, Mukerjea R, Birtalan S, Friedberg D, Ghosh P. 2010. A solvent-exposed patch in chaperone-bound YopE is required for translo-cation by the type III secretion system. J. Bacteriol. 192:3114-3122.
40. Akeda Y, Galán JE. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437:911-915.
41. Slagowski NL, Kramer RW, Morrison MF, LaBaer J, Lesser CF. 2008. A functional genomic yeast screen to identify pathogenic bacterial proteins. PLoS Pathog. 4:e9.
42. Alberti S, Gitler AD, Lindquist S. 2007. A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24:913-919.
43. Goehring NW, Gonzalez MD, Beckwith J. 2006. Premature targeting of cell division proteins to midcell reveals hierarchies of protein interactions involved in divisome assembly. Mol. Microbiol. 61:33-45.
44. Pavlidis P, Noble WS. 2003. Matrix2png: a utility for visualizing matrix data. Bioinformatics 19:295-296.
45. Lesser CF, Miller SI. 2001. Expression of microbial virulence proteins in Saccharomyces cerevisiae models mammalian infection. EMBO J. 20: 1840-1849.