Serogroup-related escape of Yersinia enterocolitica YopE from degradation by the ubiquitin-proteasome pathway

Infection and Immunity

Volumn 75, Issue 9, 2007, Pages 4423-4431

  Hentschke, Moritz ^a   Trülzsch, Konrad ^b   Heesemann, Jürgen ^b   Aepfelbacher, Martin ^a   Ruckdeschel, Klaus ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

POLYUBIQUITIN; PROTEASOME; UBIQUITIN; YERSINIA OUTER PROTEIN E;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; UBIQUITINATION; YERSINIA ENTEROCOLITICA; YERSINIOSIS;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; CELL LINE; ENZYME STABILITY; HUMANS; LYSINE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEASOME ENDOPEPTIDASE COMPLEX; SEROTYPING; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; UBIQUITIN; YERSINIA ENTEROCOLITICA;

EID: 34548481798     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00528-07     Document Type: Article

References (49)

1. Achtman, M., K. Zurth, G. Morelli, G. Torrea, A. Guiyoule, and E. Carniel. 1999. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 96:14043-14048.
2. Aepfelbacher, M., and J. Heesemann. 2001. Modulation of Rho GTPases and the actin cytoskeleton by Yersinia outer proteins (Yops). Int. J. Med. Microbiol. 291:269-276.
3. Balachandran, P., L. Dragone, L. Garrity-Ryan, A. Lemus, A. Weiss, and J. Engel. 2007. The ubiquitin ligase Cbl-b limits Pseudomonas aeruginosa exotoxin T-mediated virulence. J. Clin. Investig. 117:419-427.
4. Black, D. S., and J. B. Bliska. 1997. 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. 16:2730-2744.
5. Black, D. S., and J. B. Bliska. 2000. The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence. Mol. Microbiol. 37:515-527.
6. Bliska, J. B. 2000. Yop effectors of Yersinia spp. and actin rearrangements. Trends Microbiol. 8:205-208.
7. Carniel, E. 2001. The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect. 3:561-569.
8. Carter, P. B., C. F. Varga, and E. E. Keet. 1973. New strain of Yersinia enterocolitica pathogenic for rodents. Appl. Microbiol. 26:1016-1018.
9. Cornelis, G. R. 2002. The Yersinia Ysc-Yop "type III" weaponry. Nat. Rev. Mol. Cell. Biol. 3:742-752.
10. Denecker, G., S. Totemeyer, L. J. Mota, P. Troisfontaines, I. Lambermont, C. Youta, I. Stainier, M. Ackermann, and G. R. Cornelis. 2002. Effect of low-and high-virulence Yersinia enterocolitica strains on the inflammatory response of human umbilical vein endothelial cells. Infect. Immun. 70:3510-3520.
11. Foultier, B., P. Troisfontaines, S. Muller, F. R. Opperdoes, and G. R. Cornelis. 2002. Characterization of the ysa pathogenicity locus in the chromosome of Yersinia enterocolitica and phylogeny analysis of type III secretion systems. J. Mol. Evol. 55:37-51.
12. Glickman, M. H., and A. Ciechanover. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82:373-428.
13. Haase, R., C. J. Kirschning, A. Sing, P. Schröttner, K. Fukase, S. Kusumoto, H. Wagner, J. Heesemann, and K. Ruckdeschel. 2003. A dominant role of Toll-like receptor 4 in the signaling of apoptosis in bacteria-faced macrophages. J. Immunol. 171:4294-4303.
14. Haller, J. C., S. Carlson, K. J. Pederson, and D. E. Pierson. 2000. A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence. Mol. Microbiol. 36:1436-1446.
15. Heesemann, J., U. Gross, N. Schmidt, and R. Laufs. 1986. Immunochemical analysis of plasmid-encoded proteins released by enteropathogenic Yersinia sp. grown in calcium-deficient media. Infect. Immun. 54:561-567.
16. Heesemann, J., C. Keller, R. Morawa, N. Schmidt, H. J. Siemens, and R. Laufs. 1983. Plasmids of human strains of Yersinia enterocolitica: molecular relatedness and possible importance for pathogenesis. J. Infect. Dis. 147: 107-115.
17. Heesemann, J., and R. Laufs. 1983. Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J. Bacteriol. 155:761-767.
18. Heesemann, J., A. Sing, and K. Trülzsch. 2006. Yersinia's stratagem: targeting innate and adaptive immune defense. Curr. Opin. Microbiol. 9:55-61.
19. Howard, S. L., M. W. Gaunt, J. Hinds, A. A. Witney, R. Stabler, and B. W. Wren. 2006. Application of comparative phylogenomics to study the evolution of Yersinia enterocolitica and to identify genetic differences relating to pathogenicity. J. Bacteriol. 188:3645-3653.
20. Iwobi, A., J. Heesemann, E. Garcia, E. Igwe, C. Noelting, and A. Rakin. 2003. Novel virulence-associated type II secretion system unique to high-pathogenicity Yersinia enterocolitica. Infect. Immun. 71:1872-1879.
21. Kloetzel, P. M., and F. Ossendorp. 2004. Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr. Opin. Immunol. 16: 76-81.
22. Kubori, T., and J. E. Galan. 2003. Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115:333-342.
23. Lee, D. H., and A. L. Goldberg. 1998. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell. Biol. 8:397-403.
24. Meng, L., R. Mohan, B. H. Kwok, M. Elofsson, N. Sin, and C. M. Crews. 1999. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo anti-inflammatory activity. Proc. Natl. Acad. Sci. USA 96:10403-10408.
25. Mittal, R., S. Y. Peak-Chew, and H. T. McMahon. 2006. Acetylation of MEK2 and I kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc. Natl. Acad. Sci. USA 103:18574-18579.
26. Mukherjee, S., G. Keitany, Y. Li, Y. Wang, H. L. Ball, E. J. Goldsmith, and K. Orth. 2006. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312:1211-1214.
27. Orth, K. 2002. Function of the Yersinia effector YopJ. Curr. Opin. Microbiol. 5:38-43.
28. Persson, C., N. Carballeira, H. Wolf-Watz, and M. Fallman. 1997. The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J. 16:2307-2318.
29. Pickart, C. M., and R. E. Cohen. 2004. Proteasomes and their kin: proteases in the machine age. Nat. Rev. Mol. Cell. Biol. 5:177-187.
30. Portnoy, D. A., H. Wolf-Watz, I. Bolin, A. B. Beeder, and S. Falkow. 1984. Characterization of common virulence plasmids in Yersinia species and their role in the expression of outer membrane proteins. Infect. Immun. 43:108-114.
31. Prehna, G., M. I. Ivanov, J. B. Bliska, and C. E. Stebbins. 2006. Yersinia virulence depends on mimicry of host Rho-family nucleotide dissociation inhibitors. Cell 126:869-880.
32. Ruckdeschel, K., G. Pfaffinger, K. Trülzsch, G. Zenner, K. Richter, J. Heesemann, and M. Aepfelbacher. 2006. The proteasome pathway destabilizes Yersinia outer protein E and represses its antihost cell activities. J. Immunol. 176:6093-6102.
33. Ruckdeschel, K., K. Richter, O. Mannel, and J. Heesemann. 2001. Arginine-143 of Yersinia enterocolitica YopP crucially determines isotype-related NF-κB suppression and apoptosis induction in macrophages. Infect. Immun. 69:7652-7662.
34. Schubert, S., A. Rakin, and J. Heesemann. 2004. The Yersinia high-pathogenicity island (HPI): evolutionary and functional aspects. Int. J. Med. Microbiol. 294:83-94.
35. Shao, F., P. M. Merritt, Z. Bao, R. W. Innes, and J. E. Dixon. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575-588.
36. Sing, A., D. Reithmeier-Rost, K. Granfors, J. Hill, A. Roggenkamp, and J. Heesemann. 2005. A hypervariable N-terminal region of Yersinia LcrV determines Toll-like receptor 2-mediated IL-10 induction and mouse virulence. Proc. Natl. Acad. Sci. USA 102:16049-16054.
37. Snellings, N. J., M. Popek, and L. E. Lindler. 2001. Complete DNA sequence of Yersinia enterocolitica serotype O:8 low-calcium-response plasmid reveals a new virulence plasmid-associated replicon. Infect. Immun. 69:4627-4638.
38. Sory, M. P., A. Boland, I. Lambermont, and G. R. Cornelis. 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. USA 92:11998-12002.
39. Thrower, J. S., L. Hoffman, M. Rechsteiner, and C. M. Pickart. 2000. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19:94-102.
40. Treier, M., L. M. Staszewski, and D. Bohmann. 1994. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78:787-798.
41. Trülzsch, K., A. Roggenkamp, M. Aepfelbacher, G. Wilharm, K. Ruckdeschel, and J. Heesemann. 2003. Analysis of chaperone-dependent Yop secretion/translocation and effector function using a mini-virulence plasmid of Yersinia enterocolitica. Int. J. Med. Microbiol. 293:167-177.
42. Trülzsch, K., T. Sporleder, E. I. Igwe, H. Rüssmann, and J. Heesemann. 2004. Contribution of the major secreted Yops of Yersinia enterocolitica O:8 to pathogenicity in the mouse infection model. Infect. Immun. 72:5227-5234.
43. Venecia, K., and G. M. Young. 2005. Environmental regulation and virulence attributes of the Ysa type III secretion system of Yersinia enterocolitica biovar 1B. Infect. Immun. 73:5961-5977.
44. Viboud, G. I., and J. B. Bliska. 2001. A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J. 20:5373-5382.
45. Von Pawel-Rammingen, U., M. V. Telepnev, G. Schmidt, K. Aktories, H. Wolf-Watz, and R. Rosqvist. 2000. GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol. Microbiol. 36:737-748.
46. Wilharm, G., V. Lehmann, K. Krauss, B. Lehnert, S. Richter, K. Ruckdeschel, J. Heesemann, and K. Trülzsch. 2004. Yersinia enterocolitica type III secretion depends on the proton motive force but not on the flagellar motor components MotA and MotB. Infect. Immun. 72:4004-4009.
47. Wren, B. W. 2003. The yersiniae - a model genus to study the rapid evolution of bacterial pathogens. Nat. Rev. Microbiol. 1:55-64.
48. Zauberman, A., S. Cohen, E. Mamroud, Y. Flashner, A. Tidhar, R. Ber, E. Elhanany, A. Shafferman, and B. Velan. 2006. Interaction of Yersinia pestis with macrophages: limitations in YopJ-dependent apoptosis. Infect. Immun. 74:3239-3250.
49. Zhang, Y., W. Higashide, S. Dai, D. M. Sherman, and D. Zhou. 2005. Recognition and ubiquitination of Salmonella type III effector SopA by a ubiquitin E3 ligase, HsRMA1. J. Biol. Chem. 280:38682-38688.