Translocated effectors of Yersinia

Current Opinion in Microbiology

Volumn 12, Issue 1, 2009, Pages 94-100

  Matsumoto, Hiroyuki ^a   Young, Glenn M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; GENES, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; PLASMIDS; VIRULENCE FACTORS; YERSINIA;

YERSINIA; YERSINIA ENTEROCOLITICA;

EID: 59849097108     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2008.12.005     Document Type: Review

References (45)

1. Stenseth N.C., Atshabar B.B., Begon M., Belmain S.R., Bertherat E., Carniel E., Gage K.L., Leirs H., and Rahalison L. Plague: past, present, and future. PLoS Med 5 (2008) e3
2. Bottone E.J. Yersinia enterocolitica: overview and epidemiologic correlates. Microbes Infect 1 (1999) 323-333
3. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 449 (2007) 819-826
4. Shao F. Biochemical functions of Yersinia type III effectors. Curr Opin Microbiol 11 (2008) 21-29
5. Viboud G.I., and Bliska J.B. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59 (2005) 69-89
6. Trosky J.E., Liverman A.D., and Orth K. Yersinia outer proteins: Yops. Cell Microbiol 10 (2008) 557-565
7. Orth K. Function of Yersinia effector YopJ. Curr Opin Microbiol 5 (2002) 38-43
8. ••].
9. Mittal R., Peak-Chew S.Y., and McMahon H.T. Acetylation of MEK2 and I kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc Natl Acad Sci U S A 103 (2006) 18574-18579. These two studies convincingly demonstrated that acetyltransferase activity of YopJ/P, which sheds light on a new biochemical modification that affects cellular processes. This biochemical modification may have broader implications on understanding how mammalian signal transduction pathways are regulated.
10. Hao Y.H., Wang Y., Burdette D., Mukherjee S., Keitany G., Goldsmith E., and Orth K. Structural requirements for Yersinia YopJ inhibition of MAP kinase pathways. PLoS ONE 3 (2008) e1375. A genetic screen to isolate mutants in the yeast MKK, Pbs2, that suppress YopJ inhibition. Corresponding mutants in human MKKs were similarly affected suggesting a conserved binding site for YopJ/P found on the superfamily of MAPK kinases.
11. Barbieri J.T., Riese M.J., and Aktories K. Bacterial toxins that modify the actin cytoskeleton. Annu Rev Cell Dev Biol 18 (2002) 315-344
12. Aepfelbacher M. Modulation of Rho GTPases by type III secretion system translocated effectors of Yersinia. Rev Physiol Biochem Pharmacol 152 (2004) 65-77
13. Viboud G.I., Mejia E., and Bliska J.B. Comparison of YopE and YopT activities in counteracting host signalling responses to Yersinia pseudotuberculosis infection. Cell Microbiol 8 (2006) 1504-1515. YopE was shown to be a potent inhibitor of infection-induced signalling cascades, and YopT can only partially compensate for the loss of YopE. These data helped to demonstrate that there is some but not complete overlap in the contribution that each of these effectors plays in pathogenesis.
14. Sorg I., Hoffmann C., Dumbach J., Aktories K., and Schmidt G. The C terminus of YopT is crucial for activity and the N terminus is crucial for substrate binding. Infect Immun 71 (2003) 4623-4632
15. Shao F., Merritt P.M., Bao Z., Innes R.W., and Dixon J.E. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109 (2002) 575-588
16. Aepfelbacher M., Trasak C., Wilharm G., Wiedemann A., Trulzsch K., Krauss K., Gierschik P., and Heesemann J. Characterization of YopT effects on Rho GTPases in Yersinia enterocolitica-infected cells. J Biol Chem 278 (2003) 33217-33223
17. Prehna G., Ivanov M.I., Bliska J.B., and Stebbins C.E. Yersinia virulence depends on mimicry of host Rho-family nucleotide dissociation inhibitors. Cell 126 (2006) 869-880. These authors utilized structural analysis in combination with biochemical approaches to demonstrate that the C-terminus of YpkA/YopO binds RhoA and Rac1 in a manner that mimics RhoGDI. This provides a mechanistic model that supports previous observations of kinase-independent functions for YpkA/YopO.
18. Galyov E.E., Hakansson S., Forsberg A., and Wolf-Watz H. A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Nature 361 (1993) 730-732
19. Navarro L., Koller A., Nordfelth R., Wolf-Watz H., Taylor S., and Dixon J.E. Identification of a molecular target for the Yersinia protein kinase A. Mol Cell 26 (2007) 465-477. This kinase substrate for YpkA/YopO eluded investigators for many years. This elegant study revealed Gαq to be phosphorylated by YpkA at a residue in the diphosphate-binding loop that is necessary for nucleotide exchange. This implicates trimeric G proteins in controlling key signaling pathways that affect the outcome of an infection.
20. Persson C., Carbelleira N., Wolf-Watz H., and Fallman M. The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130cas and FAK, and the associated accumulation of the proteins in peripheral focal adhesion. EMBO J 16 (1997) 2307-2318
21. Persson C., Nordfelth R., Andersson K., Forsberg A., Wolf-Watz H., and Fallman M. Localization of the Yersinia PTPase to focal complexes is an important virulence mechanism. Mol Microbiol 33 (1999) 828-838
22. Black D.S., and Bliska J.B. Identification of p130Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO J 16 (1997) 2730-2744
23. Black D.S., Montagna L.G., Zitsmann S., and Bliska J.B. Identification of an amino-terminal substrate-binding domain in the Yersinia tyrosine phosphatase that is required for efficient recognition of focal adhesion targets. Mol Microbiol 29 (1998) 1263-1274
24. Fallman M., Andersson K., Hakansson S., Magnusson K.E., Stendahl O., and Wolf-Watz H. Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect Immun 63 (1995) 3117-3124
25. Ruckdeschel K., Roggenkamp A., Schubert S., and Heesemann J. Differential contribution of Yersinia enterocolitica virulence factors to evasion of microbicidal action of neutrophils. Infect Immun 64 (1996) 724-733
26. Kerschen E.J., Cohen D.A., Kaplan A.M., and Straley S.C. The plague virulence protein YopM targets the innate immune response by causing a global depletion of NK cells. Infect Immun 72 (2004) 4589-4602
27. Foultier B., Troisfontaines P., Vertommen D., Marenne M.-N., Rider M., Persot C., and Cornelis GR. Identification of substrates and chaperone from the Yersinia enterocolitica 1B Ysa type III secretion system. Infect Immun 71 (2003) 242-253
28. Haller J.C., Carlson S., Pederson K.J., and Pierson D.E. A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence. Mol Microbiol 36 (2000) 1436-1446
29. Young G.M. The Ysa type 3 secretion system of Yersinia enterocolitica biovar 1B. Adv Exp Med Biol 603 (2007) 286-297
30. Thomson N.R., Howard S., Wren B.W., Holden M.T., Crossman L., Challis G.L., Churcher C., Mungall K., Brooks K., Chillingworth T., et al. The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet 2 (2006) e206. The complete genome analysis of Y. enterocolitica revealed numerous insights on the evolution of this genus. Among the new insights was the plasticity zone, a genomic region containing numerous virulence factors such as the Ysa T3SS, YAPI pilus and Yst-1 T2SS system.
31. Venecia K., and Young G.M. Environmental regulation and virulence attributes of the Ysa type III secretion system of Yersinia enterocolitica biovar 1B. Infect Immun 73 (2005) 5961-5977
32. Young B.M., and Young G.M. Evidence for targeting of Yop effectors by the chromosomally encoded Ysa type III secretion system of Yersinia enterocolitica. J Bacteriol 184 (2002) 5563-5571
33. Matsumoto H., and Young G.M. Proteomic and functional analysis of the suite of Ysp proteins exported by the Ysa type III secretion system of Yersinia enterocolitica Biovar 1B. Mol Microbiol 59 (2006) 689-706. The study revealed a completely new set of Yersinia effectors that affect the outcome of a gastrointestinal infection. This information helped to clarify that the Ysa T3S system was needed for the infection of a mammalian host.
34. Kim D.W., Lenzen G., Page A.L., Legrain P., Sansonetti P.J., and Parsot C. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci U S A 102 (2005) 14046-14051. This study has important implications on understanding the function of YspK, which is 91% identical to OspG. A series of elegant biochemical approaches and the use of a mouse model of infection revealed that OspG interacts with ubiquitin-cojugating enzymes to direct suppression of the proinflammatory pathways and affect disease pathology.
35. Witowski S.E., Walker K.A., and Miller V.L. YspM, a newly identified Ysa type III secreted protein of Yersinia enterocolitica. J Bacteriol 190 (2008) 7315-7325. This work described the identification of Ysa T3SS effector YspM produced by a subset of Y. enterocolitica strains. YspM is homologous to proteins classified as GDSL bacterial lipases and resulted in growth inhibition when expressed in Saccharomyces cerevisiae.
36. Holbourn K.P., Shone C.C., and Acharya K.R. A family of killer toxins. Exploring the mechanism of ADP-ribosylating toxins. FEBS J 273 (2006) 4579-4593
37. Chain P.S., Carniel E., Larimer F.W., Lamerdin J., Stoutland P.O., Regala W.M., Georgescu A.M., Vergez L.M., Land M.L., Motin V.L., et al. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 101 (2004) 13826-13831
38. Parkhill J., Wren B.W., Thomson N.R., Titball R.W., Holden M.T., Prentice M.B., Sebaihia M., James K.D., Churcher C., Mungall K.L., et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413 (2001) 523-527
39. Troisfontaines P., and Cornelis G.R. Type III secretion: more systems than you think. Physiology (Bethesda) 20 (2005) 326-339
40. Golubov A., Heesemann J., and Rakin A. Uncovering genomic differences in human pathogenic Yersinia enterocolitica. FEMS Immunol Med Microbiol 38 (2003) 107111
41. Gendlina I., Held K.G., Bartra S.S., Gallis B.M., Doneanu C.E., Goodlett D.R., Plano G.V., and Collins C.M. Identification and type III-dependent secretion of the Yersinia pestis insecticidal-like proteins. Mol Microbiol 64 (2007) 1214-1227
42. Hares M.C., Hinchliffe S.J., Strong P.C., Eleftherianos I., Dowling A.J., Ffrench-Constant R.H., and Waterfield N. The Yersinia pseudotuberculosis and Yersinia pestis toxin complex is active against cultured mammalian cells. Microbiology 154 (2008) 3503-3517. In this study, the authors demonstrated that insecticidal toxins are extracellularly secreted. Thus, it was proposed that these proteins are not likely to be translocated effectors as originally hypothesized by others.
43. Bingle L.E., Bailey C.M., and Pallen M.J. Type VI secretion: a beginner's guide. Curr Opin Microbiol 11 (2008) 3-8
44. Yen Y.T., Bhattacharya M., and Stathopoulos C. Genome-wide in silico mapping of the secretome in pathogenic Yersinia pestis KIM. FEMS Microbiol Lett 279 (2008) 56-63
45. Eppinger M., Rosovitz M.J., Fricke W.F., Rasko D.A., Kokorina G., Fayolle C., Lindler L.E., Carniel E., and Ravel J. The complete genome sequence of Yersinia pseudotuberculosis IP31758, the causative agent of Far East scarlet-like fever. PLoS Genet 3 (2007) e142