PKC-dependent endocytosis of the Helicobacter pylori vacuolating cytotoxin in primary T lymphocytes

Cellular Microbiology

Volumn 13, Issue 3, 2011, Pages 482-496

  Sewald, Xaver ^a   Jiménez Soto, Luisa ^a   Haas, Rainer ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA2 INTEGRIN; CD18 ANTIGEN; CYTOTOXIN; PROTEIN CDC42; PROTEIN KINASE C; PROTEIN SUBUNIT; RAC1 PROTEIN; THREONINE; UNCLASSIFIED DRUG; VACOULATING CYTOTOXIN;

ARTICLE; CELL PROLIFERATION; ENDOCYTOSIS; ENZYME ACTIVATION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE;

HELICOBACTER PYLORI;

EID: 79951487830     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01551.x     Document Type: Article

References (60)

1. Algood, H.M., Torres, V.J., Unutmaz, D., and Cover, T.L. (2007) Resistance of primary murine CD4+ T cells to Helicobacter pylori vacuolating cytotoxin. Infect Immun 75: 334-341.
2. Atherton, J.C., Cao, P., Peek, R.M., Tummuru, M.K.R., Blaser, M.J., and Cover, T.L. (1995) Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. J Biol Chem 270: 17771-17777.
3. Blaser, M.J., Perez-Perez, G.I., Kleanthous, H., Cover, T.L., Peek, R.M., Chyou, P.H., etal. (1995) Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55: 2111-2115.
4. Boncristiano, M., Paccani, S.R., Barone, S., Ulivieri, C., Patrussi, L., Ilver, D., etal. (2003) The Helicobacter pylori Vacuolating Toxin Inhibits T Cell Activation by Two Independent Mechanisms. J Exp Med 198: 1887-1897.
5. Caswell, P.T., and Norman, J.C. (2006) Integrin trafficking and the control of cell migration. Traffic 7: 14-21.
6. Chianale, F., Rainero, E., Cianflone, C., Bettio, V., Pighini, A., Porporato, P.E., etal. (2010) Diacylglycerol kinase alpha mediates HGF-induced Rac activation and membrane ruffling by regulating atypical PKC and RhoGDI. Proc Natl Acad Sci USA 107: 4182-4187.
7. Cover, T.L., and Blanke, S.R. (2005) Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol 3: 320-332.
8. Eichholtz, T., de Bont, D.B., de Widt, J., Liskamp, R.M., and Ploegh, H.L. (1993) A myristoylated pseudosubstrate peptide, a novel protein kinase C inhibitor. J Biol Chem 268: 1982-1986.
9. Fabbri, M., Fumagalli, L., Bossi, G., Bianchi, E., Bender, J.R., and Pardi, R. (1999) A tyrosine-based sorting signal in the beta2 integrin cytoplasmic domain mediates its recycling to the plasma membrane and is required for ligand-supported migration. EMBO J 18: 4915-4925.
10. Fabbri, M., Di Meglio, S., Gagliani, M.C., Consonni, E., Molteni, R., Bender, J.R., etal. (2005) Dynamic partitioning into lipid rafts controls the endo-exocytic cycle of the alphaL/beta2 integrin, LFA-1, during leukocyte chemotaxis. Mol Biol Cell 16: 5793-5803.
11. Fagerholm, S., Morrice, N., Gahmberg, C.G., and Cohen, P. (2002) Phosphorylation of the cytoplasmic domain of the integrin CD18 chain by protein kinase C isoforms in leukocytes. J Biol Chem 277: 1728-1738.
12. Fiory, F., Oriente, F., Miele, C., Romano, C., Trencia, A., Alberobello, A.T., etal. (2004) Protein kinase C-zeta and protein kinase B regulate distinct steps of insulin endocytosis and intracellular sorting. J Biol Chem 279: 11137-11145.
13. Fischer, W., Buhrdorf, R., Gerland, E., and Haas, R. (2001) Outer membrane targeting of passenger proteins by the vacuolating cytotoxin autotransporter of Helicobacter pylori. Infect Immun 69: 6769-6775.
14. Gahmberg, C.G., Fagerholm, S.C., Nurmi, S.M., Chavakis, T., Marchesan, S., and Gronholm, M. (2009) Regulation of integrin activity and signalling. Biochim Biophys Acta 1790: 431-444.
15. Gangwer, K.A., Mushrush, D.J., Stauff, D.L., Spiller, B., McClain, M.S., Cover, T.L., etal. (2007) Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain. Proc Natl Acad Sci USA 104: 16293-16298.
16. Garner, J.A., and Cover, T.L. (1996) Binding and internalization of the Helicobacter pylori vacuolating cytotoxin by epithelial cells. Infect Immun 64: 4197-4203.
17. Gauthier, N.C., Monzo, P., Kaddai, V., Doye, A., Ricci, V., and Boquet, P. (2005) Helicobacter pylori VacA cytotoxin: a probe for a clathrin-independent and Cdc42-dependent pinocytic pathway routed to late endosomes. Mol Biol Cell 16: 4852-4866.
18. Gauthier, N.C., Monzo, P., Gonzalez, T., Doye, A., Oldani, A., Gounon, P., etal. (2007) Early endosomes associated with dynamic F-actin structures are required for late trafficking of H. pylori VacA toxin. J Cell Biol 177 343-354
19. Gebert, B., Fischer, W., Weiss, E., Hoffmann, R., and Haas, R. (2003) Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301: 1099-1102.
20. Gupta, V.R., Patel, H.K., Kostolansky, S.S., Ballivian, R.A., Eichberg, J., and Blanke, S.R. (2008) Sphingomyelin functions as a novel receptor for Helicobacter pylori VacA. PLoS Pathog 4: e1000073.
21. Gusarova, G.A., Dada, L.A., Kelly, A.M., Brodie, C., Witters, L.A., Chandel, N.S., etal. (2009) Alpha1-AMP-activated protein kinase regulates hypoxia-induced Na, K-ATPase endocytosis via direct phosphorylation of protein kinase C zeta. Mol Cell Biol 29: 3455-3464.
22. Hilden, T.J., Valmu, L., Karkkainen, S., and Gahmberg, C.G. (2003) Threonine phosphorylation sites in the beta 2 and beta 7 leukocyte integrin polypeptides. J Immunol 170: 4170-4177.
23. House, C., and Kemp, B.E. (1987) Protein kinase C contains a pseudosubstrate prototope in its regulatory domain. Science 238: 1726-1728.
24. Ivaska, J., Vuoriluoto, K., Huovinen, T., Izawa, I., Inagaki, M., and Parker, P.J. (2005) PKCepsilon-mediated phosphorylation of vimentin controls integrin recycling and motility. EMBO J 24: 3834-3845.
25. Iwamoto, H., Czajkowsky, D.M., Cover, T.L., Szabo, G., and Shao, Z. (1999) VacA from Helicobacter pylori: a hexameric chloride channel. FEBS Lett 450: 101-104.
26. Kim, S.K. (2000) Cell polarity: new PARtners for Cdc42 and Rac. Nat Cell Biol 2: E143-E145.
27. Kishikawa, K., Chalfant, C.E., Perry, D.K., Bielawska, A., and Hannun, Y.A. (1999) Phosphatidic acid is a potent and selective inhibitor of protein phosphatase 1 and an inhibitor of ceramide-mediated responses. J Biol Chem 274: 21335-21341.
28. Laudanna, C. (2005) Integrin activation under flow: a local affair. Nat Immunol 6: 429-430.
29. Laudanna, C., Mochly-Rosen, D., Liron, T., Constantin, G., and Butcher, E.C. (1998) Evidence of zeta protein kinase C involvement in polymorphonuclear neutrophil integrin-dependent adhesion and chemotaxis. J Biol Chem 273: 30306-30315.
30. Lehel, C., Olah, Z., Jakab, G., and Anderson, W.B. (1995) Protein kinase C epsilon is localized to the Golgi via its zinc-finger domain and modulates Golgi function. Proc Natl Acad Sci USA 92: 1406-1410.
31. Limatola, C., Schaap, D., Moolenaar, W.H., and van Blitterswijk, W.J. (1994) Phosphatidic acid activation of protein kinase C-zeta overexpressed in COS cells: comparison with other protein kinase C isotypes and other acidic lipids. Biochem J 304: 1001-1008.
32. Luo, B., Prescott, S.M., and Topham, M.K. (2003) Protein kinase C alpha phosphorylates and negatively regulates diacylglycerol kinase zeta. J Biol Chem 278: 39542-39547.
33. Moser, M., Legate, K.R., Zent, R., and Fassler, R. (2009) The tail of integrins, talin, and kindlins. Science 324: 895-899.
34. Nurmi, S.M., Gahmberg, C.G., and Fagerholm, S.C. (2006) 14-3-3 proteins bind both filamin and alphaLbeta2 integrin in activated T cells. Ann NY Acad Sci 1090: 318-325.
35. Nurmi, S.M., Autero, M., Raunio, A.K., Gahmberg, C.G., and Fagerholm, S.C. (2007) Phosphorylation of the LFA-1 integrin beta2-chain on Thr-758 leads to adhesion, Rac-1/Cdc42 activation, and stimulation of CD69 expression in human T cells. J Biol Chem 282: 968-975.
36. Odenbreit, S., Püls, J., Sedlmaier, B., Gerland, E., Fischer, W., and Haas, R. (2000) Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287: 1497-1500.
37. Papini, E., Gottardi, E., Satin, B., Debernard, M., Massari, P., Telford, J., etal. (1996) The vacuolar ATPase proton pump is present on intracellular vacuoles induced by Helicobacter pylori. J Med Microbiol 45: 84-89.
38. Papini, E., Satin, B., Bucci, C., Debernard, M., Telford, J.L., Manetti, R., etal. (1997) The small GTP-binding protein Rab7 is essential for cellular vacuolation induced by Helicobacter pylori cytotoxin. EMBO J 16: 15-24.
39. Pelish, H.E., Peterson, J.R., Salvarezza, S.B., Rodriguez-Boulan, E., Chen, J.L., Stamnes, M., etal. (2006) Secramine inhibits Cdc42-dependent functions in cells and Cdc42 activation in vitro. Nat Chem Biol 2: 39-46.
40. Pelkmans, L., Fava, E., Grabner, H., Hannus, M., Habermann, B., Krausz, E., etal. (2005) Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436: 78-86.
41. Petit, I., Goichberg, P., Spiegel, A., Peled, A., Brodie, C., Seger, R., etal. (2005) Atypical PKC-zeta regulates SDF-1-mediated migration and development of human CD34+ progenitor cells. J Clin Invest 115: 168-176.
42. Reyrat, J.M., Lanzavecchia, S., Lupetti, P., de Bernard, M., Pagliaccia, C., Pelicic, V., etal. (1999) 3D imaging of the 58 kDa cell binding subunit of the Helicobacter pylori cytotoxin. J Mol Biol 290 459-470.
43. Rhead, J.L., Letley, D.P., Mohammadi, M., Hussein, N., Mohagheghi, M.A., Eshagh, H.M., etal. (2007) A new Helicobacter pylori vacuolating cytotoxin determinant, the intermediate region, is associated with gastric cancer. Gastroenterology 133: 926-936.
44. Ricci, V., Galmiche, A., Doye, A., Necchi, V., Solcia, E., and Boquet, P. (2000) High cell sensitivity to Helicobacter pylori VacA toxin depends on a GPI-anchored protein and is not blocked by inhibition of the clathrin-mediated pathway of endocytosis. Mol Biol Cell 11: 3897-3909.
45. Sewald, X., Gebert-Vogl, B., Prassl, S., Barwig, I., Weiss, E., Fabbri, M., etal. (2008) Integrin subunit CD18 Is the T-lymphocyte receptor for the Helicobacter pylori vacuolating cytotoxin. Cell Host & Microbe 3: 20-29.
46. Shamri, R., Grabovsky, V., Gauguet, J.M., Feigelson, S., Manevich, E., Kolanus, W., etal. (2005) Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat Immunol 6: 497-506.
47. Sharlow, E.R., Giridhar, K.V., LaValle, C.R., Chen, J., Leimgruber, S., Barrett, R., etal. (2008) Potent and selective disruption of protein kinase D functionality by a benzoxoloazepinolone. J Biol Chem 283: 33516-33526.
48. Stasek, J.E., Jr, Natarajan, V., and Garcia, J.G. (1993) Phosphatidic acid directly activates endothelial cell protein kinase C. Biochem Biophys Res Commun 191: 134-141.
49. Steinberg, S.F. (2008) Structural basis of protein kinase C isoform function. Physiol Rev 88: 1341-1378.
50. Suerbaum, S., and Michetti, P. (2002) Helicobacter pylori infection. N Engl J Med 347: 1175-1186.
51. Sundrud, M.S., Torres, V.J., Unutmaz, D., and Cover, T.L. (2004) Inhibition of primary human T cell proliferation by Helicobacter pylori vacuolating toxin (VacA) is independent of VacA effects on IL-2 secretion. Proc Natl Acad Sci USA 101: 7727-7732.
52. Szabo, I., Brutsche, S., Tombola, F., Moschioni, M., Satin, B., Telford, J.L., etal. (1999) Formation of anion-selective channels in the cell plasma membrane by the toxin VacA of Helicobacter pylori is required for its biological activity. EMBO J 18: 5517-5527.
53. Takala, H., Nurminen, E., Nurmi, S.M., Aatonen, M., Strandin, T., Takatalo, M., etal. (2008) Beta2 integrin phosphorylation on Thr758 acts as a molecular switch to regulate 14-3-3 and filamin binding. Blood 112: 1853-1862.
54. Tracy, S., van der Geer, P., and Hunter, T. (1995) The receptor-like protein-tyrosine phosphatase, RPTP alpha, is phosphorylated by protein kinase C on two serines close to the inner face of the plasma membrane. J Biol Chem 270: 10587-10594.
55. Weber, K.S., York, M.R., Springer, T.A., and Klickstein, L.B. (1997) Characterization of lymphocyte function-associated antigen 1 (LFA-1)-deficient T cell lines: the alphaL and beta2 subunits are interdependent for cell surface expression. J Immunol 158: 273-279.
56. Woods, A.J., White, D.P., Caswell, P.T., and Norman, J.C. (2004) PKD1/PKCmu promotes alphavbeta3 integrin recycling and delivery to nascent focal adhesions. EMBO J 23: 2531-2543.
57. Yahiro, K., Niidome, T., Kimura, M., Hatakeyama, T., Aoyagi, H., Kurazono, H., etal. (1999) Activation of Helicobacter pylori VacA toxin by alkaline or acid conditions increases its binding to a 250-kDa receptor protein-tyrosine phosphatase beta. J Biol Chem 274: 36693-36699.
58. Yahiro, K., Wada, A., Nakayama, M., Kimura, T., Ogushi, K.I., Niidome, T., etal. (2003) Protein-tyrosine phosphatase α, RPTPα, is a Helicobacter pylori VacA receptor. J Biol Chem 278: 19183-19189.
59. Yahiro, K., Wada, A., Yamasaki, E., Nakayama, M., Nishi, Y., Hisatsune, J., etal. (2004) Essential domain of receptor tyrosine phosphatase beta (RPTPbeta) for interaction with Helicobacter pylori vacuolating cytotoxin. J Biol Chem 279: 51013-51021.
60. Yang, C., and Kazanietz, M.G. (2003) Divergence and complexities in DAG signaling: looking beyond PKC. Trends Pharmacol Sci 24: 602-608.