Cholesterol glucosylation promotes immune evasion by Helicobacter pylori

Nature Medicine

Volumn 12, Issue 9, 2006, Pages 1030-1038

  Wunder, Christian ^a,e   Churin, Yuri ^a   Winau, Florian ^a   Warnecke, Dirk ^b   Vieth, Michael ^c,e,f   Lindner, Buko ^d   Zähringer, Ulrich ^d   Mollenkopf, Hans Joachim ^a   Heinz, Ernst ^b   Meyer, Thomas F ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d RESEARCH CENTER BORSTEL   (Germany)

^e EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^f INSTITUTE OF PATHOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; GLUCOSYLTRANSFERASE;

ARTICLE; CELL ACTIVATION; CELL MEMBRANE; DENDRITIC CELL; EPITHELIUM CELL; GLYCOSYLATION; HELICOBACTER PYLORI; HUMAN; IN VIVO STUDY; KNOCKOUT GENE; MACROPHAGE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; CELL MEMBRANE; CHOLESTEROL; CYTOKINES; EPITHELIAL CELLS; GASTRIC MUCOSA; GLUCOSE; GLUCOSYLTRANSFERASES; GLYCOSYLATION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; IMMUNITY, INNATE; IMMUNITY, NATURAL; MACROPHAGES; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; PHAGOCYTOSIS; STOMACH NEOPLASMS; T-LYMPHOCYTES, HELPER-INDUCER; TUMOR CELLS, CULTURED;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

EID: 33748462851     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm1480     Document Type: Article

References (47)

1. Falush, D. et al. Traces of human migrations in Helicobacter pylori populations. Science 299, 1582-1585 (2003).
2. Marshall, B.J., Armstrong, J.A., McGechie, D.B. & Glancy, R.J. Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med. J. Aust. 142, 436-439 (1985).
3. Peek, R.M., Jr. & Blaser, M.J. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2, 28-37 (2002).
4. Simons, K. & Vaz, W.L. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33, 269-295 (2004).
5. Dixon, M.F., Genta, R.M., Yardley, J.H. & Correa, P. Histological classification of gastritis and Helicobacter pylori infection: an agreement at last? The International Workshop on the Histopathology of Gastritis. Helicobacter. 2 (Suppl. 1), S17-S24 (1997).
6. Hirai, Y. et al. Unique cholesteryl glucosides in Helicobacter pylori: composition and structural analysis. J. Bacteriol. 177, 5327-5333 (1995).
7. Kawakubo, M. et al. Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection. Science 305, 1003-1006 (2004).
8. Testerman, T.L., McGee, D.J. & Mobley, H.L. Helicobacter pylori growth and urease detection in the chemically defined medium Ham's F-12 nutrient mixture. J. Clin. Microbiol. 39, 3842-3850 (2001).
9. O'Toole, P.W., Kostrzynska, M. & Trust, T.J. Non-motile mutants of Helicobacter pylori and Helicobacter mustelae defective in flagellar hook production. Mol. Microbiol. 14, 691-703 (1994).
10. Schreiber, S. et al. The spatial orientation of Helicobacter pylori in the gastric mucus. Proc. Natl. Acad. Sci. USA 101, 5024-5029 (2004).
11. Song, K.S. et al. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J. Biol. Chem. 271, 9690-9697 (1996).
12. Foster, L.J., De Hoog, C.L. & Mann, M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. USA 100, 5813-5818 (2003).
13. Harder, T., Scheiffele, P., Verkade, P. & Simons, K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929-942 (1998).
14. Legler, D.F. et al. Differential insertion of GPI-anchored GFPs into lipid rafts of live cells. FASEB J. 19, 73-75 (2005).
15. Amieva, M.R. et al. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300, 1430-1434 (2003).
16. Censini, S. et al. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93, 14648-14653 (1996).
17. Hatakeyama, M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat. Rev. Cancer 4, 688-694 (2004).
18. Montecucco, C. & Rappuoli, R. Living dangerously: how Helicobacter pylori survives in the human stomach. Nat. Rev. Mol. Cell Biol. 2, 457-466 (2001).
19. Smart, E.J., Ying, Y.S., Conrad, P.A. & Anderson, R.G. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127, 1185-1197 (1994).
20. Allen, L.A., Schlesinger, L.S. & Kang, B. Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J. Exp. Med. 191, 115-128 (2000).
21. Odenbreit, S., Gebert, B., Puls, J., Fischer, W. & Haas, R. Interaction of Helicobacter pylori with professional phagocytes: role of the cag pathogenicity island and translocation, phosphorylation and processing of CagA. Cell. Microbiol. 3, 21-31 (2001).
22. Haque, M., Hirai, Y., Yokota, K. & Oguma, K. Steryl glycosides: a characteristic feature of the Helicobacter spp.? J. Bacteriol. 177, 5334-5337 (1995).
23. Kanehisa, M. & Goto, S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27-30 (2000).
24. Gomez-Duarte, O.G. et al. Protection of mice against gastric colonization by Helicobacter pylori by single oral dose immunization with attenuated Salmonella typhimurium producing urease subunits A and B. Vaccine 16, 460-471 (1998).
25. Mombaerts, P. et al. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68, 869-877 (1992).
26. Haque, M., Hirai, Y., Yokota, K. & Oguma, K. Lipid profiles of Helicobacter pylori and Helicobacter mustelae grown in serum-supplemented and serum-free media. Acta Med. Okayama 49, 205-211 (1995).
27. Lebrun, A.H. et al. Cloning of a cholesterol-α-glucosyltransferase from Helicobacter pylori. J. Biol. Chem., published online 14 July 2006.
28. Oku, M. et al. Peroxisome degradation requires catalytically active sterol glucosyltransferase with a GRAM domain. EMBO J. 22, 3231-3241 (2003).
29. Raggers, R.J., Pomorski, T., Holthuis, J.C., Kalin, N. & van Meer, G. Lipid traffic: the ABC of transbilayer movement. Traffic 1, 226-234 (2000).
30. Simons, K. & Toomre, D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39 (2000).
31. Schaller, H. New aspects of sterol biosynthesis in growth and development of higher plants. Plant Physiol. Biochem. 42, 465-476 (2004).
32. Parks, L.W. & Casey, W.M. Physiological implications of sterol biosynthesis in yeast. Annu. Rev. Microbiol. 49, 95-116 (1995).
33. Mayberry, W.R. & Smith, P.F. Structures and properties of acyl diglucosylcholesterol and galactofuranosyl diacylglycerol from Acholeplasma axanthum. Biochim. Biophys. Acta 752, 434-443 (1983).
34. Smith, P.F. Biosynthesis of cholesteryl glucoside by Mycoplasma gallinarum. J. Bacteriol. 108, 986-991 (1971).
35. Livermore, B.P., Bey, R.F. & Johnson, R.C. Lipid metabolism of Borrelia hermsi. Infect. Immun. 20, 215-220 (1978).
36. Peng, L., Kawagoe, Y., Hogan, P. & Delmer, D. Sitosterol-β- glucoside as primer for cellulose synthesis in plants. Science 295, 147-150 (2002).
37. Ben Menachem, G., Kubler-Kielb, J., Coxon, B., Yergey, A. & Schneerson, R. A newly discovered cholesteryl galactoside from Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 100, 7913-7918 (2003).
38. Shimomura, H., Hayashi, S., Yokota, K., Oguma, K. & Hirai, Y. Alteration in the composition of cholesteryl glucosides and other lipids in Helicobacter pylori undergoing morphological change from spiral to coccoid form. FEMS Microbiol. Lett. 237, 407-413 (2004).
39. Tannaes, T. & Bukholm, G. Cholesteryl-6-O-acyl-α-D- glucopyranoside of Helicobacter pylori relate to relative lysophospholipid content. FEMS Microbiol. Lett. 244, 117-120 (2005).
40. Burger, K., Gimpl, G. & Fahrenholz, F. Regulation of receptor function by cholesterol. Cell. Mol. Life Sci. 57, 1577-1592 (2000).
41. Li, J. et al. Impaired phagocytosis in caveolin-1 deficient macrophages. Cell Cycle 4, 1599-1607 (2005).
42. Wang, Y., Thiele, C. & Huttner, W.B. Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 1, 952-962 (2000).
43. Guillemin, K., Salama, N.R., Tompkins, L.S. & Falkow, S. Cag pathogenicity island-specific responses of gastric epithelial cells to Helicobacter pylori infection. Proc. Natl. Acad. Sci. USA 99, 15136-15141 (2002).
44. Slonczewski, J.L., McGee, D.J., Phillips, J., Kirkpatrick, C. & Mobley, H.L. pH-dependent protein profiles of Helicobacter pylori analyzed by two-dimensional gels. Helicobacter 5, 240-247 (2000).
45. Heuermann, D. & Haas, R. A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol. Gen. Genet. 257, 519-528 (1998).
46. Schaible, U.E. et al. Parasitophorous vacuoles of Leishmania mexicana acquire macromolecules from the host cell cytosol via two independent routes. J. Cell Sci. 112, 681-693 (1999).
47. Barrett, T. et al. NCBI GEO: mining millions of expression profiles-database and tools. Nucleic Acids Res. 33, D562-D566 (2005).