Role of predicted transmembrane domains for Type III translocation, pore formation, and signaling by the Yersinia pseudotuberculosis YopB protein

Infection and Immunity

Volumn 73, Issue 4, 2005, Pages 2433-2443

  Ryndak, Michelle B ^a   Chung, Hachung ^a   London, Erwin ^a   Bliska, James B ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; PROTEIN YOPB; UNCLASSIFIED DRUG; OUTER MEMBRANE PROTEIN; YOPB PROTEIN, YERSINIA; YOPD PROTEIN, YERSINIA; YOPE PROTEIN, YERSINIA;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL TRANSLOCATION; CELL MEMBRANE; CHANNEL GATING; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS; ANIMAL; CHEMISTRY; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CELL MEMBRANE; MICE; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; YERSINIA PSEUDOTUBERCULOSIS;

EID: 16244414595     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.4.2433-2443.2005     Document Type: Article

References (60)

1. Aepfelbacher, M., R. Zumbihl, K. Ruckdeschel, C. A. Jacobi, C. Barz, and J. Heesemann. 1999. The tranquilizing injection of Yersinia proteins: a pathogen's strategy to resist host defense. Biol. Chem. 380:795-802.
2. Armulik, A., I. Nilsson, G. von Heijne, and S. Johansson. 1999. Determination of the border between the transmembrane and cytoplasmic domains of human integrin subunits. J. Biol. Chem. 274:37030-37034.
3. Beel, B. D., and G. L. Hazelbauer. 2001. Signalling substitutions in the periplasmic domain of chemoreceptor Trg induce or reduce helical sliding in the transmembrane domain. Mol. Microbiol. 40:824-834.
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. Black, D. S., A. Marie-Cardine, B. Schraven, and J. B. Bliska. 2000. The Yersinia tyrosine phosphatase YopH targets a novel adhesion-regulated signalling complex in macrophages. Cell. Microbiol. 2:401-414.
7. Bliska, J. B., M. C. Copass, and S. Falkow. 1993. The Yersinia pseudotuberculosis adhesin YadA mediates intimate bacterial attachment to and entry into HEp-2 cells. Infect. Immun. 61:3914-3921.
8. Blocker, A., K. Komoriya, and S. Aizawa. 2003. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl. Acad. Sci. USA 100:3027-3030.
9. Bolin, I., L. Norlander, and H. Wolf-Watz. 1982. Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect. Immun. 37:506-512.
10. 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.
11. Buttner, D., and U. Bonas. 2002. Port of entry-the type III secretion translocon. Trends Microbiol. 10:186-192.
12. Caputo, G. A., and E. London. 2003. Cumulative effects of amino acid substitutions and hydrophobic mismatch upon the transmembrane stability and conformation of hydrophobic alpha-helices. Biochemistry 42:3275-3285.
13. Chervitz, S. A., and J. J. Falke. 1995. Lock on/off disulfides identify the transmembrane signaling helix of the aspartate receptor. J. Biol. Chem. 270:24043-24053.
14. Cornelis, G. R. 2002. Yersinia type III secretion: send in the effectors. J. Cell Biol. 158:401-408.
15. Cornelis, G. R. 2002. The Yersinia Ysc-Yop "type III" weaponry. Nat. Rev. Mol. Cell. Biol. 3:742-752.
16. Cornelis, G. R., and F. Van Gijsegem. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
17. Falke, J. J., and G. L. Hazelbauer. 2001. Transmembrane signaling in bacterial chemoreceptorsa. Trends Biochem. Sci. 26:257-265.
18. Fields, K. A., M. L. Nilles, C. Cowan, and S. C. Straley. 1999. Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect. Immun. 67: 5395-5408.
19. Fields, K. A., and S. C. Straley. 1999. LcrV of Yersinia pestis enters infected eukaryotic cells by a virulence plasmid-independent mechanism. Infect. Immun. 67:4801-4813.
20. Francis, M. S., H. Wolf-Watz, and A. Forsberg. 2002. Regulation of type III secretion systems. Curr. Opin. Microbiol. 5:166-172.
21. Hakansson, S., T. Bergman, J. Vanooteghem, G. Cornelis, and H. Wolf-Watz. 1993. YopB and YopD constitute a novel class of Yersinia Yop proteins. Infect Immun. 61:71-80.
22. Hakansson, S., K. Schesser, C. Persson, E. E. Galyov, R. Rosqvist, F. Homble, and H. Wolf-Watz. 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.
23. Hamid, N., K. Gustavsson, K. Andersen, K. McGee, C. Persson, C. E. Rudd, and M. Fallman. 1999. YopH dephosphorylates Cas and Fyn-binding protein in macrophages. Microb. Pathog. 27:231-242.
24. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
25. Holmstrom, A., J. Olsson, P. Cherepanov, E. Maier, R. Nordfelth, J. Pettersson, R. Benz, H. Wolf-Watz, and A. Forsberg. 2001. LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol. Microbiol. 39:620-632.
26. Holmstrom, A., J. Pettersson, R. Rosqvist, S. Hakansson, F. Tafazoli, M. Fallman, K.-E. Magnusson, H. Wolf-Watz, and A. Forsberg. 1997. YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane. Mol. Microbiol. 24:73-91.
27. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
28. Hughson, A. G., and G. L. Hazelbauer. 1996. Detecting the conformational change of transmembrane signaling in a bacterial chemoreceptor by measuring effects on disulfide cross-linking in vivo. Proc. Natl. Acad. Sci. USA 93:11546-11551.
29. Hume, P. J., E. J. McGhie, R. D. Hayward, and V. Koronakis. 2003. The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology. Mol. Microbiol. 49:425-439.
30. Juris, S. J., F. Shao, and J. E. Dixon. 2002. Yersinia effectors target mammalian signalling pathways. Cell. Microbiol. 4:201-211.
31. Lee, V. T., and O. Schneewind. 1999. Type III machines of pathogenic yersiniae secrete virulence factors into the extracellular milieu. Mol. Microbiol. 31:1619-1629.
32. Lee, V. T., C. Tam, and O. Schneewind. 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.
33. Marenne, M. N., L. Journet, L. J. Mota, and G. R. Cornelis. 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.
34. McGhie, E. J., P. J. Hume, R. D. Hayward, J. Torres, and V. Koronakis. 2002. Topology of the Salmonella invasion protein SipB in a model bilayer. Mol. Microbiol. 44:1309-1321.
35. Miller, A. S., and J. J. Falke. 2004. Side chains at the membrane-water interface modulate the signaling state of a transmembrane receptor. Biochemistry 43:1763-1770.
36. Monack, D. M., J. Mecsas, N. Ghori, and S. Falkow. 1997. Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc. Natl. Acad. Sci. USA 94:10385-10390.
37. Monne, M., I. Nilsson, A. Elofsson, and G. von Heijne. 1999. Turns in transmembrane helices: determination of the minimal length of a "helical hairpin" and derivation of a fine-grained turn propensity scale. J. Mol. Biol. 293:807-814.
38. Neyt, C., and G. Cornelis. 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.
39. Neyt, C., and G. Cornelis. 1999. Role of SycD, the chaperone of the Yersinia Yop translocators YopB and YopD. Mol. Microbiol. 31:143-156.
40. Nilles, M. L., K. A. Fields, and S. C. Straley. 1998. The V antigen of Yersinia pestis regulates Yop vectorial targeting as well as Yop secretion through its effects on YopB and LcrG. J. Bacteriol. 180:3410-3420.
41. Nordfelth, R., and H. Wolf-Watz. 2001. YopB of Yersinia enterocolitica is essential for YopE translocation. Infect. Immun. 69:3516-3518.
42. Orth, K. 2002. Function of the Yersinia effector YopJ. Curr. Opin. Microbiol. 5:38-43.
43. Pallen, M. J., G. Dougan, and G. Frankel. 1997. Coiled-coiled domains in proteins secreted by type III secretion systems. Mol. Microbiol. 25:423-425.
44. Palmer, L. E., S. Hobbie, J. E. Galan, and J. B. Bliska. 1998. YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNFα production and the downregulation of the MAP kinases p38 and JNK. Mol. Microbiol. 27:953-965.
45. Palmer, L. E., A. R. Pancetti, S. Greenberg, and J. B. Bliska. 1999. YopJ of Yersinia spp. is sufficient to cause downregulation of multiple mitogen-activated protein kinases in eukaryotic cells. Infect. Immun. 67:708-716.
46. 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.
47. Pettersson, J., A. Holmstrom, J. Hill, S. Leary, E. Frithz-Lindsten, A. von Euler-Matell, E. Carlsson, R. Titball, A. Forsberg, and H. Wolf-Watz. 1999. The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol. Microbiol. 32:961-976.
48. Plano, G. V., J. B. Day, and F. Ferracci. 2001. Type III export: new uses for an old pathway. Mol. Microbiol. 40:284-293.
49. Ramamurthi, K. S., and O. Schneewind. 2002. Type III protein secretion in Yersinia species. Annu. Rev. Cell. Dev. Biol. 18:107-133.
50. Rosqvist, R., K.-E. Magnusson, and H. Wolf-Watz. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13:964-972.
51. Ruckdeschel, K., S. Harb, A. Roggenkamp, M. Hornef, R. Zumbihl, S. Kohler, J. Heesemann, and B. Rouot. 1998. Yersinia enterocolitica impairs activation of transcription factor NF-κB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor α production. J. Exp. Med. 187:1069-1079.
52. Shao, F., P. O. Vacratsis, Z. Bao, K. E. Bowers, C. A. Fierke, and J. E. Dixon. 2003. Biochemical characterization of the Yersinia YopT protease: cleavage site and recognition elements in Rho GTPases. Proc. Natl. Acad. Sci. USA 100:904-909.
53. Sing, A., D. Rost, N. Tvardovskaia, A. Roggenkamp, A. Wiedemann, C. J. Kirschning, M. Aepfelbacher, and J. Heesemann. 2002. Yersinia V-antigen exploits toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196:1017-1024.
54. Skoudy, A., J. Mounier, A. Aruffo, H. Ohayon, P. Gounon, P. Sansonetti, and G. Tran Van Nhieu. 2000. CD44 binds to the Shigella IpaB protein and participates in bacterial invasion of epithelial cells. Cell. Microbiol. 2:19-33.
55. Smith, S. O., C. S. Smith, and B. J. Bormann. 1996. Strong hydrogen bonding interactions involving a buried glutamic acid in the transmembrane sequence of the neu/erbB-2 receptor. Nat. Struct. Biol. 3:252-258.
56. Tardy, F., F. Homble, C. Neyt, R. Wattiez, G. R. Cornelis, J. M. Ruysschaert, and V. Cabiaux. 1999. Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J. 18:6793-6799.
57. 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.
58. Viboud, G. I., S. S. So, M. B. Ryndak, and J. B. Bliska. 2003. Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis. Mol. Microbiol. 47:1305-1315.
59. 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.
60. Williams, A. W., and S. C. Straley. 1998. YopD of Yersinia pestis plays a role in negative regulation of the low-calcium response in addition to its role in translocation of Yops. J. Bacteriol. 180:350-358.