YopK regulates the Yersinia pestis type III secretion system from within host cells

Molecular Microbiology

Volumn 79, Issue 6, 2011, Pages 1445-1461

  Dewoody, Rebecca ^a   Merritt, Peter M ^a   Houppert, Andrew S ^a   Marketon, Melanie M ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA LACTAMASE; PROTEIN YOPK; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN E; YERSINIA OUTER PROTEIN K;

ARTICLE; BACTERIAL STRAIN; CHO CELL; CONTROLLED STUDY; CYTOSOL; HOST CELL; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; REGULATORY MECHANISM; TISSUE CULTURE; TYPE III SECRETION SYSTEM; YERSINIA PESTIS;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CHO CELLS; CRICETINAE; CRICETULUS; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; PLAGUE; PROTEIN TRANSPORT; YERSINIA PESTIS;

BACTERIA (MICROORGANISMS); MAMMALIA; YERSINIA; YERSINIA PESTIS;

EID: 79952455347     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07534.x     Document Type: Article

References (54)

1. Aili, M., Hallberg, B., Wolf-Watz, H., and Rosqvist, R. (2002) GAP activity of Yersinia YopE. Methods Enzymol 358: 359-370.
2. Aili, M., Isaksson, E.L., Carlsson, S.E., Wolf-Watz, H., Rosqvist, R., and Francis, M.S. (2008) Regulation of Yersinia Yop-effector delivery by translocated YopE. Int J Med Microbiol 298: 183-192.
3. Ben-Gurion, R., and Shafferman, A. (1981) Essential virulence determinants of different Yersinia species are carried on a common plasmid. Plasmid 5: 183-187.
4. Black, D.S., and Bliska, J.B. (2000) The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence. Mol Microbiol 37: 515-527.
5. Boland, A., Havaux, S., and Cornelis, G.R. (1998) Heterogeneity of the Yersinia YopM protein. Microb Pathog 25: 343-348.
6. Brodsky, I.E., Palm, N.W., Sadanand, S., Ryndak, M.B., Sutterwala, F.S., Flavell, R.A., etal. (2010) A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 7: 376-387.
7. Brubaker, R.R. (1969) Mutation rate to nonpigmentation in Pasteurella pestis. J Bacteriol 98: 1404-1406.
8. Brubaker, R.R. (2003) Interleukin-10 and inhibition of innate immunity to Yersiniae: roles of Yops and LcrV (V antigen). Infect Immun 71: 3673-3681.
9. Cambronne, E.D., Sorg, J.A., and Schneewind, O. (2004) Binding of SycH chaperone to YscM1 and YscM2 activates effector Yop expression in Yersinia enterocolitica. J Bacteriol 186: 829-841.
10. Cheng, L.W., Anderson, D.M., and Schneewind, O. (1997) Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica. Mol Microbiol 24: 757-765.
11. Cherepanov, P., and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158: 9-14.
12. Choi, K., Gaynor, J.B., White, K.G., Lopez, C., Bosio, C.M., Karkhoff-Schweizer, R.R., and Schweizer, H.P. (2005) A Tn7-based broad-range bacterial cloning and expression system. Nat Methods 2: 443-448.
13. Cornelis, G. (2002a) The Yersinia Ysc-Yop virulence apparatus. Int J Med Microbiol 291: 455-462.
14. Cornelis, G. (2002b) Yersinia type III secretion: send in the effectors. J Cell Biol 158: 401-408.
15. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
16. Dennis, D.T., Gage, K., Gratz, N., Poand, J., and Tikhomirov, E. (1999) Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: World Health Organization.
17. Garcia, J.T., Ferracci, F., Jackson, M.W., Joseph, S.S., Pattis, I., Plano, L.R.W., etal. (2006) Measurement of effector protein injection by type III and type IV secretion systems by using a 13-residue phosphorylatable glycogen synthase kinase tag. Infect Immun 74: 5645-5657.
18. Guan, K.L., and Dixon, J.E. (1990) Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249: 553-556.
19. Hakansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homble, F., and Wolf-Watz, H. (1996) The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J 15: 5812-5823.
20. Holmstrom, A., Rosqvist, R., Wolf-Watz, H., and Forsberg, A. (1995a) Virulence plasmid-encoded YopK is essential for Yersinia pseudotuberculosis to cause systemic infection in mice. Infect Immun 63: 2269-2276.
21. Holmstrom, A., Rosqvist, R., Wolf-Watz, H., and Forsberg, A. (1995b) YopK, a novel virulence determinant of Yersinia pseudotuberculosis. Contrib Microbiol Immunol 13: 239-243.
22. Holmstrom, A., Pettersson, J., Rosqvist, R., Hakansson, S., Tafazoli, F., Fallman, M., etal. (1997) YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane. Mol Microbiol 24: 73-91.
23. Kerschen, E.J., Cohen, D.A., Kaplan, A.M., and Straley, S.C. (2004) The plague virulence protein YopM targets the innate immune response by causing a global depletion of NK cells. Infect Immun 72: 4589-4602.
24. Köberle, M., Klein-Günther, A., Schütz, M., Fritz, M., Berchtold, S., Tolosa, E., etal. (2009) Yersinia enterocolitica targets cells of the innate and adaptive immune system by injection of Yops in a mouse infection model. PLoS Pathog 5: e1000551.
25. Kogure, T., Kawano, H., Abe, Y., and Miyawaki, A. (2008) Fluorescence imaging using a fluorescent protein with a large Stokes shift. Methods 45: 223-226.
26. Lathem, W.W., Price, P.A., Miller, V.L., and Goldman, W.E. (2007) A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315: 509-513.
27. Lee, V.T., Anderson, D.M., and Schneewind, O. (1998) Targeting of Yersinia Yop proteins into the cytosol of HeLa cells: one-step translocation of YopE across bacterial and eukaryotic membranes is dependent on SycE chaperone. Mol Microbiol 28: 593-601.
28. Lee, V.T., Tam, C., and Schneewind, O. (2000) LcrV, a substrate for Yersinia enterocolitica type III secretion, is required for toxin targeting into the cytosol of HeLa cells. J Biol Chem 275: 36869-36875.
29. Leung, K.A., Reisner, B.S., and Straley, S.C. (1990) YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice. Infect Immun 58: 3262-3271.
30. McDonald, C., Vacratsis, P.O., Bliska, J.B., and Dixon, J.E. (2003) The Yersinia virulence factor YopM forms a novel protein complex with two cellular kinases. J Biol Chem 278: 18514-18523.
31. Marenne, M.N., Journet, L., Mota, L.J., and Cornelis, G.R. (2003) Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb Pathog 35: 243-258.
32. Marketon, M.M., DePaolo, R.W., DeBord, K.L., Jabri, B., and Schneewind, O. (2005) Plague bacteria target immune cells during infection. Science 309: 1739-1741.
33. Mejia, E., Bliska, J.B., and Viboud, G.I. (2008) Yersinia controls type III effector delivery into host cells by modulating Rho activity. PLoS Pathog 4: e3.
34. Mulder, B., Michiels, T., Simonet, M., Sory, M.P., and Cornelis, G. (1989) Identification of additional virulence determinants on the pYV plasmid of Yersinia enterocolitica W227. Infect Immun 57: 2534-2541.
35. Nakajima, R., Motin, V.L., and Brubaker, R.R. (1995) Suppression of cytokines in mice by protein A-V antigen fusion peptide and restoration of synthesis by active immunization. Infect Immun 63: 3021-3029.
36. Nedialkov, Y.A., Motin, V.L., and Brubaker, R.R. (1997) Resistance to lipopolysaccharide mediated by the Yersinia pestis V antigen-polyhistidine fusion peptide: amplification of interleukin-10. Infect Immun 65: 1196-1203.
37. Neyt, C., and Cornelis, G.R. (1999) Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol 33: 971-981.
38. Orth, K. (2002) Function of the Yersinia effector YopJ. Curr Opin Microbiol 5: 38-43.
39. von Pawel-Rammingen, U., Telepnev, M.V., Schmidt, G., Aktories, K., Wolf-Watz, H., and Rosqvist, R. (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.
40. Persson, C., Nordfelth, R., Holmstrom, A., Hakansson, S., Rosqvist, R., and Wolf-Watz, H. (1995) Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell. Mol Microbiol 18: 135-150.
41. Pettersson, J., Holmstrom, A., Hill, J., Leary, S., Frithz-Lindsten, E., von Euler-Matell, A., etal. (1999) The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol Microbiol 32: 961-976.
42. Ramsby, M., and Makowski, G. (2005) Differential detergent fractionation of eukaryotic cells. In The Proteomics Protocols Handbook. Walker, J. (ed.). Totowa, NJ: Humana Press, pp. 37-48.
43. Ruckdeschel, K., Pfaffinger, G., Trulzsch, K., Zenner, G., Richter, K., Heesemann, J., and Aepfelbacher, M. (2006) The proteasome pathway destabilizes Yersinia outer protein E and represses its antihost cell activities. J Immunol 176: 6093-6102.
44. Skrzypek, E., Cowan, C., and Straley, S.C. (1998) Targeting of the Yersinia pestis YopM protein into HeLa cells and intracellular trafficking to the nucleus. Mol Microbiol 30: 1051-1065.
45. Sorg, J.A., Blaylock, B., and Schneewind, O. (2006) Secretion signal recognition by YscN, the Yersinia type III secretion ATPase. Proc Natl Acad Sci USA 103: 16490-16495.
46. Straley, S.C., and Bowmer, W.S. (1986) Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun 51: 445-454.
47. Straley, S.C., and Cibull, M.L. (1989) Differential clearance and host-pathogen interactions of YopE- and YopK- YopL-Yersinia pestis in BALB/c mice. Infect Immun 57: 1200-1210.
48. Tabrizi, S., and Robins-Browne, R. (1993) Elimination of extracellular bacteria by antibiotics in quantitative assays of bacterial ingestion and killing by phagocytes. J Immunol Methods 158: 201-206.
49. Takeshita, S., Sato, M., Toba, M., Masahashi, W., and Hashimoto-Gotoh, T. (1987) High-copy-number and low-copy-number plasmid vectors for lacZ alpha-complementation and chloramphenicol- or kanamycin-resistance selection. Gene 61: 63-74.
50. Viboud, G.I., and Bliska, J.B. (2001) A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J 20: 5373-5382.
51. Viboud, G.I., and Bliska, J.B. (2005) Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59: 69-89.
52. Viboud, G.I., Mejia, E., and Bliska, J.B. (2006) Comparison of YopE and YopT activities in counteracting host signalling responses to Yersinia pseudotuberculosis infection. Cell Microbiol 8: 1504-1515.
53. Wattiau, P., and Cornells, G.R. (1993) SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol Microbiol 8: 123-131.
54. Zumbihl, R., Aepfelbacher, M., Andor, A., Jacobi, C.A., Ruckdeschel, K., Rouot, B., and Heesemann, J. (1999) The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J Biol Chem 274: 29289-29293.