Helicobacter pylori exploits host membrane phosphatidylserine for delivery, localization, and pathophysiological action of the CagA oncoprotein

Cell Host and Microbe

Volumn 7, Issue 5, 2010, Pages 399-411

  Murata Kamiya, Naoko ^a   Kikuchi, Kenji ^a,b   Hayashi, Takeru ^a,c   Higashi, Hideaki ^c   Hatakeyama, Masanori ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CAGA PROTEIN; ONCOPROTEIN; PHOSPHATIDYLSERINE; PROTEIN KINASE; PROTEIN PARTITIONING DEFECTIVE 1; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CAGA PROTEIN, HELICOBACTER PYLORI; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CELL MEMBRANE; CELL POLARITY; CONTROLLED STUDY; ENDOSOME; EPITHELIUM CELL; HELICOBACTER PYLORI; HOST CELL; HUMAN; HUMAN CELL; MEMBRANE LEAFLET; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; TRANSPORT KINETICS; ANIMAL; CELL LINE; DOG; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE; CELL MEMBRANE; DOGS; EPITHELIAL CELLS; HELICOBACTER PYLORI; ONCOGENE PROTEINS; PHOSPHATIDYLSERINES; PROTEIN TRANSPORT; VIRULENCE FACTORS;

EID: 77955292149     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2010.04.005     Document Type: Article

References (47)

1. Amieva, M. R., Vogelmann, R., Covacci, A., Tompkins, L. S., Nelson, W. J., and Falkow, S. (2003). Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300, 1430-1434.
2. Asahi, M., Azuma, T., Ito, S., Ito, Y., Suto, H., Nagai, Y., Tsubokawa, M., Tohyama, Y., Maeda, S., Omata, M., et al. (2000). Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J. Exp. Med. 191, 593-602.
3. Backert, S., Ziska, E., Brinkmann, V., Zimny-Arndt, U., Fauconnier, A., Jungblut, P. R., Naumann, M., and Meyer, T. F. (2000). Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell. Microbiol. 2, 155-164.
4. Backert, S., Feller, S. M., and Wessler, S. (2008). Emerging roles of Abl family tyrosine kinases in microbial pathogenesis. Trends Biochem. Sci. 33, 80-90.
5. Bagnoli, F., Buti, L., Tompkins, L., Covacci, A., and Amieva, M. R. (2005). Helicobacter pylori CagA induces a transition from polarized to invasive phenotypes in MDCK cells. Proc. Natl. Acad. Sci. USA 102, 16339-16344.
6. Bevers, E. M., Comfurius, P., and Zwaal, R. F. (1983). Changes in membrane phospholipid distribution during platelet activation. Biochim. Biophys. Acta 736, 57-66.
7. Bouchier-Hayes, L., Muñoz-Pinedo, C., Connell, S., and Green, D. R. (2008). Measuring apoptosis at the single cell level. Methods 44, 222-228.
8. Christie, P. J., Atmakuri, K., Krishnamoorthy, V., Jakubowski, S., and Cascales, E. (2005). Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59, 451-485. (Pubitemid 41507439)
9. Churin, Y., Al-Ghoul, L., Kepp, O., Meyer, T. F., Birchmeier, W., and Naumann, M. (2003). Helicobacter pylori CagA protein targets the c-Met receptor and enhances the motogenic response. J. Cell Biol. 161, 249-255.
10. Daleke, D. L., and Lyles, J. V. (2000). Identification and purification of aminophospholipid flippases. Biochim. Biophys. Acta 1486, 108-127.
11. Doherty, G. J., and McMahon, H. T. (2009). Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857-902.
12. Fischer, W., Püls, J., Buhrdorf, R., Gebert, B., Odenbreit, S., and Haas, R. (2001). Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42, 1337-1348.
13. Fronzes, R., Schäfer, E., Wang, L., Saibil, H. R., Orlova, E. V., and Waksman, G. (2009). Structure of a type IV secretion system core complex. Science 323, 266-268.
14. Gautier, I., Coppey, J., and Durieux, C. (2003). Early apoptosis-related changes triggered by HSV-1 in individual neuronlike cells. Exp. Cell Res. 289, 174-183.
15. Goth, S. R., and Stephens, R. S. (2001). Rapid, transient phosphatidylserine externalization induced in host cells by infection with Chlamydia spp. Infect. Immun. 69, 1109-1119.
16. Haas, R., Meyer, T. F., and van Putten, J. P. (1993). Aflagellated mutants of Helicobacter pylori generated by genetic transformation of naturally competent strains using transposon shuttle mutagenesis. Mol. Microbiol. 8, 753-760.
17. Hatakeyama, M. (2004). Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat. Rev. Cancer 4, 688-694. (Pubitemid 39215067)
18. Hatakeyama, M. (2008). SagA of CagA in Helicobacter pylori pathogenesis. Curr. Opin. Microbiol. 11, 30-37.
19. 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. (Pubitemid 34111828)
20. Higashi, H., Nakaya, A., Tsutsumi, R., Yokoyama, K., Fujii, Y., Ishikawa, S., Higuchi, M., Takahashi, A., Kurashima, Y., Teishikata, Y., et al. (2004). Helicobacter pylori CagA induces Ras-independent morphogenetic response through SHP-2 recruitment and activation. J. Biol. Chem. 279, 17205-17216.
21. Higashi, H., Yokoyama, K., Fujii, Y., Ren, S., Yuasa, H., Saadat, I., Murata-Kamiya, N., Azuma, T., and Hatakeyama, M. (2005). EPIYA motif is a membrane-targeting signal of Helicobacter pylori virulence factor CagA in mammalian cells. J. Biol. Chem. 280, 23130-23137.
22. Isberg, R. R., Hamburger, Z., and Dersch, P. (2000). Signaling and invasinpromoted uptake via integrin receptors. Microbes Infect. 2, 793-801.
23. Juhas, M., Crook, D. W., and Hood, D. W. (2008). Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell. Microbiol. 10, 2377-2386.
24. Kenis, H., van Genderen, H., Bennaghmouch, A., Rinia, H. A., Frederik, P., Narula, J., Hofstra, L., and Reutelingsperger, C. P. M. (2004). Cell surface-expressed phosphatidylserine and annexin A5 open a novel portal of cell entry. J. Biol. Chem. 279, 52623-52629.
25. Kierbel, A., Gassama-Diagne, A., Rocha, C., Radoshevich, L., Olson, J., Mostov, K., and Engel, J. (2007). Pseudomonas aeruginosa exploits a PIP3-dependent pathway to transform apical into basolateral membrane. J. Cell Biol. 177, 21-27.
26. Kwok, T., Zabler, D., Urman, S., Rohde, M., Hartig, R., Wessler, S., Misselwitz, R., Berger, J., Sewald, N., König, W., and Backert, S. (2007). Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449, 862-866.
27. Lai, C. H., Chang, Y. C., Du, S. Y., Wang, H. J., Kuo, C. H., Fang, S. H., Fu, H. W., Lin, H. H., Chiang, A. S., and Wang, W. C. (2008). Cholesterol depletion reduces Helicobacter pylori CagA translocation and CagA-induced responses in AGS cells. Infect. Immun. 76, 3293-3303.
28. Lemmon, M. A. (2008). Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111.
29. Mayor, S., and Pagano, R. E. (2007). Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8, 603-612.
30. Meier, O., Boucke, K., Hammer, S. V., Keller, S., Stidwill, R. P., Hemmi, S., and Greber, U. F. (2002). Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 158, 1119-1131.
31. Mercer, J., and Helenius, A. (2008). Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320, 531-535.
32. Mimuro, H., Suzuki, T., Tanaka, J., Asahi, M., Haas, R., and Sasakawa, C. (2002). Grb2 is a key mediator of helicobacter pylori CagA protein activities. Mol. Cell 10, 745-755.
33. 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.
34. Ohnishi, N., Yuasa, H., Tanaka, S., Sawa, H., Miura, M., Matsui, A., Higashi, H., Musashi, M., Iwabuchi, K., Suzuki, M., et al. (2008). Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc. Natl. Acad. Sci. USA 105, 1003-1008.
35. Peek, R. M., Jr. (2005). Orchestration of aberrant epithelial signaling by Helicobacter pylori CagA. Sci. STKE 2005, pe14.
36. Peek, R. M., Jr., and Blaser, M. J. (2002). Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2, 28-37.
37. Rohde, M., Püls, J., Buhrdorf, R., Fischer, W., and Haas, R. (2003). A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system. Mol. Microbiol. 49, 219-234.
38. Saadat, I., Higashi, H., Obuse, C., Umeda, M., Murata-Kamiya, N., Saito, Y., Lu, H., Ohnishi, N., Azuma, T., Suzuki, A., et al. (2007). Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature 447, 330-333.
39. 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.
40. Soares, M. M., King, S. W., and Thorpe, P. E. (2008). Targeting inside-out phosphatidylserine as a therapeutic strategy for viral diseases. Nat. Med. 14, 1357-1362.
41. Stein, M., Rappuoli, R., and Covacci, A. (2000). Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc. Natl. Acad. Sci. USA 97, 1263-1268.
42. Suzuki, M., Mimuro, H., Suzuki, T., Park, M., Yamamoto, T., and Sasakawa, C. (2005). Interaction of CagA with Crk plays an important role in Helicobacter pylori-induced loss of gastric epithelial cell adhesion. J. Exp. Med. 202, 1235-1247.
43. Tréhin, R., and Merkle, H. P. (2004). Chances and pitfalls of cell penetrating peptides for cellular drug delivery. Eur. J. Pharm. Biopharm. 58, 209-223.
44. 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.
45. Wen, W., Liu, W., Yan, J., and Zhang, M. (2008). Structure basis and unconventional lipid membrane binding properties of the PH-C1 tandem of Rho kinases. J. Biol. Chem. 283, 26263-26273.
46. Yeung, T., Gilbert, G. E., Shi, J., Silvius, J., Kapus, A., and Grinstein, S. (2008). Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210-213.
47. Zwaal, R. F. A., Comfurius, P., and Bevers, E. M. (2005). Surface exposure of phosphatidylserine in pathological cells. Cell. Mol. Life Sci. 62, 971-988.