Cytotoxic necrotizing factor-Y boosts yersinia effector translocation by activating Rac protein

Journal of Biological Chemistry

Volumn 288, Issue 32, 2013, Pages 23543-23553

  Wolters, Manuel ^a   Boyle, Erin C ^a   Lardong, Kerstin ^a   Trülzsch, Konrad ^b   Steffen, Anika ^c   Rottner, Klemens ^c,d   Ruckdeschel, Klaus ^e   Aepfelbacher, Martin ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^e Labor Schottdorf MVZ GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC; GTP-BINDING PROTEINS; HOST CELLS; IMMUNE DEFENSE; PATHOGENIC YERSINIAE;

BIOCHEMISTRY; BIOLOGY;

PROTEINS;

BACTERIAL PROTEIN; BACTERIAL TOXIN; CYTOTOXIC NECROTIZING FACTOR Y; GUANINE NUCLEOTIDE BINDING PROTEIN; MUTANT PROTEIN; PROTEIN CDC42; PROTEIN YOP; PROTEIN YOPO; PROTEIN YOPT; RAC PROTEIN; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; RHOC GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN E;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; GENE INACTIVATION; GENE SILENCING; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; YERSINIA; YERSINIA ENTEROCOLITICA;

CDC42; CNF-Y; CYTOTOXIC NECROTIZING FACTOR-Y; RAC; RHO; RHO GTPASES; TOXINS; TYPE III SECRETION SYSTEM; YERSINIA ENTEROCOLITICA;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL TOXINS; CDC42 GTP-BINDING PROTEIN; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; NEUROPEPTIDES; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; RAS PROTEINS; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; RHOB GTP-BINDING PROTEIN; YERSINIA ENTEROCOLITICA; YERSINIA INFECTIONS;

EID: 84881469450     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.448662     Document Type: Article

References (69)

1. Prentice, M. B., and Rahalison, L. (2007) Plague. Lancet 369, 1196-1207
2. 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
3. Trülzsch, K., Oellerich, M. F., and Heesemann, J. (2007) Invasion and dissemination of Yersinia enterocolitica in the mouse infection model. Adv. Exp. Med. Biol. 603, 279-285
4. Heesemann, J., Sing, A., and Trülzsch, K. (2006) Yersinia's stratagem: targeting innate and adaptive immune defense. Curr. Opin. Microbiol. 9, 55-61
5. Navarro, L., Alto, N. M., and Dixon, J. E. (2005) Functions of the Yersinia effector proteins in inhibiting host immune responses. Curr. Opin. Microbiol. 8, 21-27
6. Cornelis, G. R. (2002) The Yersinia Ysc-Yop 'type III' weaponry. Nat. Rev. Mol. Cell Biol. 3, 742-752
7. Cornelis, G. R., and Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23, 861-867
8. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K. E., and Wolf-Watz, H. (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273, 1231-1233
9. 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
10. Dewoody, R., Merritt, P. M., Houppert, A. S., and Marketon, M. M. (2011) YopK regulates the Yersinia pestis type III secretion system from within host cells. Mol. Microbiol. 79, 1445-1461
11. Gaus, K., Hentschke, M., Czymmeck, N., Novikova, L., Trülzsch, K., Valentin-Weigand, P., Aepfelbacher, M., and Ruckdeschel, K. (2011) Destabilization of YopE by the ubiquitin-proteasome pathway fine-tunes Yop delivery into host cells and facilitates systemic spread of Yersinia enterocolitica in host lymphoid tissue. Infection Immunity 79, 1166-1175
12. Aepfelbacher, M., Trasak, C., and Ruckdeschel, K. (2007) Effector functions of pathogenic Yersinia species. Thromb. Haemost. 98, 521-529
13. Black, D. S., and Bliska, J. B. (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
14. Persson, C., Carballeira, N., Wolf-Watz, H., and FAllman, M. (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
15. Alonso, A., Bottini, N., Bruckner, S., Rahmouni, S., Williams, S., Schoenberger, S. P., and Mustelin, T. (2004) Lck dephosphorylation at Tyr-394 and inhibition of T cell antigen receptor signaling by Yersinia phosphatase YopH. J. Biol. Chem. 279, 4922-4928
16. Gerke, C., Falkow, S., and Chien, Y. H. (2005) The adaptor molecules LAT and SLP-76 are specifically targeted by Yersinia to inhibit T cell activation. J. Exp. Med. 201, 361-371
17. Yao, T., Mecsas, J., Healy, J. I., Falkow, S., and Chien, Y. (1999) Suppression of T and B lymphocyte activation by a Yersinia pseudotuberculosis virulence factor, yopH. J. Exp. Med. 190, 1343-1350
18. Mukherjee, S., Keitany, G., Li, Y., Wang, Y., Ball, H. L., Goldsmith, E. J., and Orth, K. (2006) Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312, 1211-1214
19. Mukherjee, S., and Orth, K. (2008) In vitro signaling by MAPK and NF-B pathways inhibited by Yersinia YopJ. Methods Enzymol. 438, 343-353
20. Mittal, R., Peak-Chew, S. Y., and McMahon, H. T. (2006) Acetylation of MEK2 and I-B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc. Natl. Acad. Sci. U.S.A. 103, 18574-18579
21. Hentschke, M., Berneking, L., Belmar Campos, C., Buck, F., Ruckdeschel, K., and Aepfelbacher, M. (2010) Yersinia virulence factor YopM induces sustained RSK activation by interfering with dephosphorylation. PLoS One 5, e13165
22. McPhee, J. B., Mena, P., and Bliska, J. B. (2010) Delineation of regions of the Yersinia YopM protein required for interaction with the RSK1 and PRK2 host kinases and their requirement for interleukin-10 production and virulence. Infection Immunity 78, 3529-3539
23. McCoy, M. W., Marré, M. L., Lesser, C. F., and Mecsas, J. (2010) The C-terminal tail of Yersinia pseudotuberculosis YopM is critical for interacting with RSK1 and for virulence. Infection Immunity 78, 2584-2598
24. 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
25. Evdokimov, A. G., Anderson, D. E., Routzahn, K. M., and Waugh, D. S. (2001) Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: a leucine-rich repeat protein with the shortest repeating unit. J. Mol. Biol. 312, 807-821
26. Peters, K. N., and Anderson, D. M. (2012) Modulation of host cell death pathways by Yersinia species and the type III effector YopK. Adv. Exp. Med. Biol. 954, 229-236
27. Holmström, A., Petterson, J., Rosqvist, R., HAkansson, S., Tafazoli, F., FAllman, M., Magnusson, K. E., Wolf-Watz, H., and Forsberg, A. (1997) YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane. Mol. Microbiol. 24, 73-91
28. Holmström, A., Rosqvist, R., Wolf-Watz, H., and Forsberg, A. (1995) YopK, a novel virulence determinant of Yersinia pseudotuberculosis. Contrib. Microbiol. Immunol. 13, 239-243
29. Brodsky, I. E., Palm, N. W., Sadanand, S., Ryndak, M. B., Sutterwala, F. S., Flavell, R. A., Bliska, J. B., and Medzhitov, R. (2010) A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe. 7, 376-387
30. Jaffe, A. B., and Hall, A. (2005) Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269
31. Heasman, S. J., and Ridley, A. J. (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690-701
32. Prehna, G., Ivanov, M. I., Bliska, J. B., and Stebbins, C. E. (2006) Yersinia virulence depends on mimicry of host Rho-family nucleotide dissociation inhibitors. Cell 126, 869-880
33. Juris, S. J., Rudolph, A. E., Huddler, D., Orth, K., and Dixon, J. E. (2000) A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. Proc. Natl. Acad. Sci. U.S.A. 97, 9431-9436
34. Trasak, C., Zenner, G., Vogel, A., Yüksekdag, G., Rost, R., Haase, I., Fischer, M., Israel, L., Imhof, A., Linder, S., Schleicher, M., and Aepfelbacher, M. (2007) Yersinia protein kinase YopO is activated by a novel G-actin binding process. J. Biol. Chem. 282, 2268-2277
35. Groves, E., Rittinger, K., Amstutz, M., Berry, S., Holden, D. W., Cornelis, G. R., and Caron, E. (2010) Sequestering of Rac by the Yersinia effector YopO blocks Fcreceptor-mediated phagocytosis. J. Biol. Chem. 285, 4087-4098
36. Aepfelbacher, M., Roppenser, B., Hentschke, M., and Ruckdeschel, K. (2011) Activity modulation of the bacterial Rho GAP YopE: an inspiration for the investigation of mammalian Rho GAPs. Eur. J. Cell Biol. 90, 951-954
37. Aili, M., Isaksson, E. L., Hallberg, B., Wolf-Watz, H., and Rosqvist, R. (2006) Functional analysis of the YopE GTPase-activating protein (GAP) activity of Yersinia pseudotuberculosis. Cell. Microbiol. 8, 1020-1033
38. Schmidt, G. (2011) Yersinia enterocolitica outer protein T (YopT). Eur. J. Cell Biol. 90, 955-958
39. Schotte, P., Denecker, G., Van Den Broeke, A., Vandenabeele, P., Cornelis, G. R., and Beyaert, R. (2004) Targeting Rac1 by the Yersinia effector protein YopE inhibits caspase-1-mediated maturation and release of interleukin-1. J. Biol. Chem. 279, 25134-25142
40. Viboud, G. I., Mejía, 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
41. Aktories, K. (2011) Bacterial protein toxins that modify host regulatory GTPases. Nat. Rev. Microbiol. 9, 487-498
42. Mejía, 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
43. 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
44. Köberle, M., Klein-Günther, A., Schütz, M., Fritz, M., Berchtold, S., Tolosa, E., Autenrieth, I. B., and Bohn, E. (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
45. Aktories, K., and Schmidt, G. (2003) A new turn in Rho GTPase activation by Escherichia coli cytotoxic necrotizing factors. Trends Microbiol. 11, 152-155
46. Lockman, H. A., Gillespie, R. A., Baker, B. D., and Shakhnovich, E. (2002) Yersinia pseudotuberculosis produces a cytotoxic necrotizing factor. Infection Immunity 70, 2708-2714
47. Flatau, G., Lemichez, E., Gauthier, M., Chardin, P., Paris, S., Fiorentini, C., and Boquet, P. (1997) Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387, 729-733
48. Schmidt, G., Sehr, P., Wilm, M., Selzer, J., Mann, M., and Aktories, K. (1997) Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387, 725-729
49. Hoffmann, C., Pop, M., Leemhuis, J., Schirmer, J., Aktories, K., and Schmidt, G. (2004) The Yersinia pseudotuberculosis cytotoxic necrotizing factor (CNFY) selectively activates RhoA. J. Biol. Chem. 279, 16026-16032
50. Trülzsch, K., Sporleder, T., Igwe, E. I., Rüssmann, H., and Heesemann, J. (2004) Contribution of the major secreted yops of Yersinia enterocolitica O:8 to pathogenicity in the mouse infection model. Infection Immunity 72, 5227-5234
51. Essler, M., Linder, S., Schell, B., Hüfner, K., Wiedemann, A., Randhahn, K., Staddon, J. M., and Aepfelbacher, M. (2003) Cytotoxic necrotizing factor 1 of Escherichia coli stimulates Rho/Rho-kinase-dependent myosin lightchain phosphorylation without inactivating myosin light-chain phosphatase in endothelial cells. Infection Immunity 71, 5188-5193
52. Chrostek, A., Wu, X., Quondamatteo, F., Hu, R., Sanecka, A., Niemann, C., Langbein, L., Haase, I., and Brakebusch, C. (2006) Rac1 is crucial for hair follicle integrity but is not essential for maintenance of the epidermis. Mol. Cell. Biol. 26, 6957-6970
53. Nordfelth, R., and Wolf-Watz, H. (2001) YopB of Yersinia enterocolitica is essential for YopE translocation. Infection Immunity 69, 3516-3518
54. Charpentier, X., and Oswald, E. (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1-lactamase as a new fluorescence-based reporter. J. Bacteriol. 186, 5486-5495
55. Mills, E., Baruch, K., Charpentier, X., Kobi, S., and Rosenshine, I. (2008) Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe 3, 104-113
56. Melendez, J., Stengel, K., Zhou, X., Chauhan, B. K., Debidda, M., Andreassen, P., Lang, R. A., and Zheng, Y. (2011) RhoA GTPase is dispensable for actomyosin regulation but is essential for mitosis in primary mouse embryonic fibroblasts. J. Biol. Chem. 286, 15132-15137
57. Wong, K. W., and Isberg, R. R. (2005) Yersinia pseudotuberculosis spatially controls activation and misregulation of host cell Rac1. PLoS Pathog. 1, e16
58. Aepfelbacher, M., Trasak, C., Wilharm, G., Wiedemann, A., Trülzsch, K., Krauss, K., Gierschik, P., and Heesemann, J. (2003) Characterization of YopT effects on Rho GTPases in Yersinia enterocolitica-infected cells. J. Biol. Chem. 278, 33217-33223
59. Andor, A., Trülzsch, K., Essler, M., Roggenkamp, A., Wiedemann, A., Heesemann, J., and Aepfelbacher, M. (2001) YopE of Yersinia, a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells. Cell. Microbiol. 3, 301-310
60. Doye, A., Boyer, L., Mettouchi, A., and Lemichez, E. (2006) Ubiquitinmediated proteasomal degradation of Rho proteins by the CNF1 toxin. Methods Enzymol. 406, 447-456
61. Lerm, M., Pop, M., Fritz, G., Aktories, K., and Schmidt, G. (2002) Proteasomal degradation of cytotoxic necrotizing factor 1-activated Rac. Infection Immunity 70, 4053-4058
62. Humphreys, D., Davidson, A., Hume, P. J., and Koronakis, V. (2012) Salmonella virulence effector SopE and Host GEF ARNO cooperate to recruit and activate WAVE to trigger bacterial invasion. Cell Host Microbe 11, 129-139
63. Koronakis, V., Hume, P. J., Humphreys, D., Liu, T., Hørning, O., Jensen, O. N., and McGhie, E. J. (2011) WAVE regulatory complex activation by cooperating GTPases Arf and Rac1. Proc. Natl. Acad. Sci. U.S.A. 108, 14449-14454
64. Steffen, A., Rottner, K., Ehinger, J., Innocenti, M., Scita, G., Wehland, J., and Stradal, T. E. (2004) Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J. 23, 749-759
65. Harris, K. P., and Tepass, U. (2010) Cdc42 and vesicle trafficking in polarized cells. Traffic 11, 1272-1279
66. Heesemann, J., and Laufs, R. (1983) Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J. Bacteriol. 155, 761-767
67. 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
68. Bölin, I., Norlander, L., and Wolf-Watz, H. (1982) Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infection Immunity 37, 506-512
69. Gemski, P., Lazere, J. R., Casey, T., and Wohlhieter, J. A. (1980) Presence of a virulence-associated plasmid in Yersinia pseudotuberculosis. Infection Immunity 28, 1044-1047