Helicobacter pylori cholesteryl glucosides interfere with host membrane phase and affect type IV secretion system function during infection in AGS cells

Molecular Microbiology

Volumn 83, Issue 1, 2012, Pages 67-84

  Wang, Hung Jung ^a   Cheng, Wen Chi ^a   Cheng, Hsin Hung ^a   Lai, Chih Ho ^a,b   Wang, Wen Ching ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CAGA PROTEIN; CHOLESTEROL ALPHA GLUCOSYLTRANSFERASE; CHOLESTEROL ESTERASE; GLUCOSIDE; GLUCOSYLTRANSFERASE; INTERLEUKIN 8; SPHINGOLIPID ACTIVATOR PROTEIN 1; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIUM ADHERENCE; CULTURE MEDIUM; CYTOKINE PRODUCTION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETIC COMPLEMENTATION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOST PATHOGEN INTERACTION; LIPID RAFT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THIN LAYER CHROMATOGRAPHY; TYPE IV SECRETION SYSTEM; WESTERN BLOTTING;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL LINE, TUMOR; CELL MEMBRANE; CHOLESTEROL; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

EID: 84155167763     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07910.x     Document Type: Article

References (54)

1. Alm, R.A., Ling, L.S., Moir, D.T., King, B.L., Brown, E.D., Doig, P.C., etal. (1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176-180.
2. Amieva, M.R., and El-Omar, E.M. (2008) Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134: 306-323.
3. Backert, S., Schwarz, T., Miehlke, S., Kirsch, C., Sommer, C., Kwok, T., etal. (2004) Functional analysis of the cag pathogenicity island in Helicobacter pylori isolates from patients with gastritis, peptic ulcer, and gastric cancer. Infect Immun 72: 1043-1056.
4. Brandt, S., Kwok, T., Hartig, R., Konig, W., and Backert, S. (2005) NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc Natl Acad Sci USA 102: 9300-9305.
5. Censini, S., Lange, C., Xiang, Z., Crabtree, J.E., Ghiara, P., Borodovsky, M., etal. (1996) cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 93: 14648-14653.
6. Crabtree, J.E. (1996) Immune and inflammatory responses to Helicobacter pylori infection. Scand J Gastroenterol Suppl 215: 3-10.
7. Crabtree, J.E., Peichl, P., Wyatt, J.I., Stachl, U., and Lindley, I.J. (1993) Gastric interleukin-8 and IgA IL-8 autoantibodies in Helicobacter pylori infection. Scand J Immunol 37: 65-70.
8. Folch, J., Lees, M., and Sloane Stanley, G.H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
9. Fujioka, T., Honda, S., and Tokieda, M. (2000) Helicobacter pylori infection and gastric carcinoma in animal models. J Gastroenterol Hepatol 15 (Suppl.): D55-D59.
10. Hatakeyama, M. (2009) Helicobacter pylori and gastric carcinogenesis. J Gastroenterol 44: 239-248.
11. Higashi, H., Tsutsumi, R., Muto, S., Sugiyama, T., Azuma, T., Asaka, M., and Hatakeyama, M. (2002) SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295: 683-686.
12. Higashi, H., Yokoyama, K., Fujii, Y., Ren, S., Yuasa, H., Saadat, I., etal. (2005) EPIYA motif is a membrane-targeting signal of Helicobacter pylori virulence factor CagA in mammalian cells. J Biol Chem 280: 23130-23137.
13. Hirai, Y., Haque, M., Yoshida, T., Yokota, K., Yasuda, T., and Oguma, K. (1995) Unique cholesteryl glucosides in Helicobacter pylori: composition and structural analysis. J Bacteriol 177: 5327-5333.
14. Hutton, M.L., Kaparakis-Liaskos, M., Turner, L., Cardona, A., Kwok, T., and Ferrero, R.L. (2010) Helicobacter pylori exploits cholesterol-rich microdomains for induction of NF-kappaB-dependent responses and peptidoglycan delivery in epithelial cells. Infect Immun 78: 4523-4531.
15. Ikonen, E. (2001) Roles of lipid rafts in membrane transport. Curr Opin Cell Biol 13: 470-477.
16. Johnson, J.K., and Somerson, N.L. (1980) Cholesterol as a limiting factor in the growth of Mycoplasma pneumoniae. Appl Environ Microbiol 40: 391-399.
17. Kenworthy, A.K. (2007) Fluorescence recovery after photobleaching studies of lipid rafts. Methods Mol Biol 398: 179-192.
18. Kenworthy, A.K., Nichols, B.J., Remmert, C.L., Hendrix, G.M., Kumar, M., Zimmerberg, J., and Lippincott-Schwartz, J. (2004) Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol 165: 735-746.
19. Kuo, C.H., Poon, S.K., Su, Y.C., Su, R., Chang, C.S., and Wang, W.C. (1999) Heterogeneous Helicobacter pylori isolates from H. pylori-infected couples in Taiwan. J Infect Dis 180: 2064-2068.
20. Kusumi, A., and Sako, Y. (1996) Cell surface organization by the membrane skeleton. Curr Opin Cell Biol 8: 566-574.
21. Kwok, T., Zabler, D., Urman, S., Rohde, M., Hartig, R., Wessler, S., etal. (2007) Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449: 862-866.
22. Lai, C.H., Kuo, C.H., Chen, P.Y., Poon, S.K., Chang, C.S., and Wang, W.C. (2006) Association of antibiotic resistance and higher internalization activity in resistant Helicobacter pylori isolates. J Antimicrob Chemother 57: 466-471.
23. Lai, C.H., Chang, Y.C., Du, S.Y., Wang, H.J., Kuo, C.H., Fang, S.H., etal. (2008) Cholesterol depletion reduces Helicobacter pylori CagA translocation and CagA-induced responses in AGS cells. Infect Immun 76: 3293-3303.
24. Lebrun, A.H., Wunder, C., Hildebrand, J., Churin, Y., Zahringer, U., Lindner, B., etal. (2006) Cloning of a cholesterol-alpha-glucosyltransferase from Helicobacter pylori. J Biol Chem 281: 27765-27772.
25. Lingwood, D., Kaiser, H.J., Levental, I., and Simons, K. (2009) Lipid rafts as functional heterogeneity in cell membranes. Biochem Soc Trans 37: 955-960.
26. Lippincott-Schwartz, J., Snapp, E., and Kenworthy, A. (2001) Studying protein dynamics in living cells. Nat Rev Mol Cell Biol 2: 444-456.
27. Lommerse, P.H., Blab, G.A., Cognet, L., Harms, G.S., Snaar-Jagalska, B.E., Spaink, H.P., and Schmidt, T. (2004) Single-molecule imaging of the H-ras membrane-anchor reveals domains in the cytoplasmic leaflet of the cell membrane. Biophys J 86: 609-616.
28. Marshall, B. (2002) Helicobacter pylori: 20 years on. Clin Med 2: 147-152.
29. Nakayama, M., Hisatsune, J., Yamasaki, E., Nishi, Y., Wada, A., Kurazono, H., etal. (2006) Clustering of Helicobacter pylori VacA in lipid rafts, mediated by its receptor, receptor-like protein tyrosine phosphatase beta, is required for intoxication in AZ-521 Cells. Infect Immun 74: 6571-6580.
30. Odenbreit, S., Puls, 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.
31. Ohnishi, N., Yuasa, H., Tanaka, S., Sawa, H., Miura, M., Matsui, A., etal. (2008) Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci USA 105: 1003-1008.
32. Peek, R.M., Jr, and Blaser, M.J. (2002) Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2: 28-37.
33. Phair, R.D., Gorski, S.A., and Misteli, T. (2004) Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol 375: 393-414.
34. Reits, E.A., and Neefjes, J.J. (2001) From fixed to FRAP: measuring protein mobility and activity in living cells. Nat Cell Biol 3: E145-E147.
35. Ritter, B., Kilian, P., Reboll, M.R., Resch, K., DiStefano, J.K., Frank, R., etal. (2011) Differential effects of multiplicity of infection on Helicobacter pylori-induced signaling pathways and interleukin-8 gene transcription. J Clin Immunol 31: 60-68.
36. Schraw, W., Li, Y., McClain, M.S., van der Goot, F.G., and Cover, T.L. (2002) Association of Helicobacter pylori vacuolating toxin (VacA) with lipid rafts. J Biol Chem 277: 34642-34650.
37. Segal, E.D., Lange, C., Covacci, A., Tompkins, L.S., and Falkow, S. (1997) Induction of host signal transduction pathways by Helicobacter pylori. Proc Natl Acad Sci USA 94: 7595-7599.
38. Segal, E.D., Cha, J., Lo, J., Falkow, S., and Tompkins, L.S. (1999) Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci USA 96: 14559-14564.
39. Selbach, M., Moese, S., Hauck, C.R., Meyer, T.F., and Backert, S. (2002) Src is the kinase of the Helicobacter pylori CagA protein in vitro and in vivo. J Biol Chem 277: 6775-6778.
40. Selbach, M., Moese, S., Hurwitz, R., Hauck, C.R., Meyer, T.F., and Backert, S. (2003) The Helicobacter pylori CagA protein induces cortactin dephosphorylation and actin rearrangement by c-Src inactivation. EMBO J 22: 515-528.
41. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387: 569-572.
42. Suerbaum, S., and Michetti, P. (2002) Helicobacter pylori infection. N Engl J Med 347: 1175-1186.
43. Taylor, D.E. (1999) Helicobacter pylori and its genome: lessons from the treasure map. Can J Gastroenterol 13: 218-223.
44. Tomb, J.F., White, O., Kerlavage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., etal. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
45. Tsutsumi, R., Higashi, H., Higuchi, M., Okada, M., and Hatakeyama, M. (2003) Attenuation of Helicobacter pylori CagA x SHP-2 signaling by interaction between CagA and C-terminal Src kinase. J Biol Chem 278: 3664-3670.
46. Tsutsumi, R., Takahashi, A., Azuma, T., Higashi, H., and Hatakeyama, M. (2006) Focal adhesion kinase is a substrate and downstream effector of SHP-2 complexed with Helicobacter pylori CagA. Mol Cell Biol 26: 261-276.
47. Varma, R., and Mayor, S. (1998) GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394: 798-801.
48. Viala, J., Chaput, C., Boneca, I.G., Cardona, A., Girardin, S.E., Moran, A.P., etal. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5: 1166-1174.
49. Wang, Y., and Taylor, D.E. (1990) Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94: 23-28.
50. Wang, Y., Roos, K.P., and Taylor, D.E. (1993) Transformation of Helicobacter pylori by chromosomal metronidazole resistance and by a plasmid with a selectable chloramphenicol resistance marker. J Gen Microbiol 139: 2485-2493.
51. Watanabe, T., Tada, M., Nagai, H., Sasaki, S., and Nakao, M. (1998) Helicobacter pylori infection induces gastric cancer in Mongolian gerbils. Gastroenterology 115: 642-648.
52. WHO (1994) IARC monographs on the evaluation of carcinogenic risks to humans, Vol. 61: Schistosomes, liver flukes and Helicobacter pylori, pp. 177-241.
53. Willingham, M.C., Hanover, J.A., Dickson, R.B., and Pastan, I. (1984) Morphologic characterization of the pathway of transferrin endocytosis and recycling in human KB cells. Proc Natl Acad Sci USA 81: 175-179.
54. Wunder, C., Churin, Y., Winau, F., Warnecke, D., Vieth, M., Lindner, B., etal. (2006) Cholesterol glucosylation promotes immune evasion by Helicobacter pylori. Nat Med 12: 1030-1038.