Helicobacter pylori disrupts host cell membranes, initiating a repair response and cell proliferation

International Journal of Molecular Sciences

Volumn 13, Issue 8, 2012, Pages 10176-10192

  Lin, Li Ling ^a   Huang, Hsuan Cheng ^b   Ogihara, Satoshi ^c   Wang, Jin Town ^d   Wu, Meng Chuan ^d   McNeil, Paul L ^e   Chen, Chiung Nien ^a,f   Juan, Hsueh Fen ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c OSAKA UNIVERSITY   (Japan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e MEDICAL COLLEGE OF GEORGIA   (United States)

^f NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Annexin A4; Cell proliferation; Helicobacter pylori; Plasma membrane repair

Indexed keywords

CALCIUM ION; LIPOCORTIN 1; LIPOCORTIN 4; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CAGA PROTEIN, HELICOBACTER PYLORI; CALCIUM; MESSENGER RNA; VACA PROTEIN, HELICOBACTER PYLORI;

ARTICLE; CALCIUM TRANSPORT; CANCER CELL CULTURE; CARCINOGENESIS; CELL DAMAGE; CELL MEMBRANE; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; EXPOSURE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN EXPRESSION; STOMACH CANCER; ADENOCARCINOMA; FLOW CYTOMETRY; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH TUMOR; TUMOR CELL CULTURE; WESTERN BLOTTING;

HELICOBACTER PYLORI;

ADENOCARCINOMA; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BLOTTING, WESTERN; CALCIUM; CELL MEMBRANE; CELL PROLIFERATION; FLOW CYTOMETRY; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STOMACH NEOPLASMS; TUMOR CELLS, CULTURED;

EID: 84874058602     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms130810176     Document Type: Article

References (42)

1. Divangahi, M.; Chen, M.; Gan, H.; Desjardins, D.; Hickman, T.T.; Lee, D.M.; Fortune, S.; Behar, S.M.; Remold, H.G. Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat. Immunol. 2009, 10, 899-906.
2. McNeil, P.L.; Kirchhausen, T. An emergency response team for membrane repair. Nat. Rev. Mol. Cell Biol. 2005, 6, 499-505.
3. Roy, D.; Liston, D.R.; Idone, V.J.; Di, A.; Nelson, D.J.; Pujol, C.; Bliska, J.B.; Chakrabarti, S.; Andrews, N.W. A process for controlling intracellular bacterial infections induced by membrane injury. Science 2004, 304, 1515-1518.
4. Bi, G.Q.; Alderton, J.M.; Steinhardt, R.A. Calcium-regulated exocytosis is required for cell membrane resealing. J. Cell Biol. 1995, 131, 1747-1758.
5. McNeil, A.K.; Rescher, U.; Gerke, V.; McNeil, P.L. Requirement for annexin A1 in plasma membrane repair. J. Biol. Chem. 2006, 281, 35202-35207.
6. Babbin, B.A.; Laukoetter, M.G.; Nava, P.; Koch, S.; Lee, W.Y.; Capaldo, C.T.; Peatman, E.; Severson, E.A.; Flower, R.J.; Perretti, M.; et al. Annexin A1 regulates intestinal mucosal injury, inflammation, and repair. J. Immunol. 2008, 181, 5035-5044.
7. Martin, G.R.; Perretti, M.; Flower, R.J.; Wallace, J.L. Annexin-1 modulates repair of gastric mucosal injury. Am. J. Physiol. Gastrointest Liver Physiol. 2008, 294, G764-G769.
8. Bouter, A.; Gounou, C.; Berat, R.; Tan, S.; Gallois, B.; Granier, T.; d'Estaintot, B.L.; Poschl, E.; Brachvogel, B.; Brisson, A.R. Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat. Commun. 2011, 2, doi:10.1038/ncomms1270.
9. Polk, D.B.; Peek, R.M., Jr. Helicobacter pylori: Gastric cancer and beyond. Nat. Rev. Cancer 2010, 10, 403-414.
10. Blaser, M.J. Linking Helicobacter pylori to gastric cancer. Nat. Med. 2000, 6, 376-377.
11. Yamaoka, Y. Mechanisms of disease: Helicobacter pylori virulence factors. Nat. Rev. Gastroenterol. Hepatol. 2010, 7, 629-641.
12. Lai, Y.P.; Yang, J.C.; Lin, T.Z.; Lin, J.T.; Wang, J.T. Helicobacter pylori infection and CagA protein translocation in human primary gastric epithelial cell culture. Helicobacter 2006, 11, 451-459.
13. Beatty, W.L. Lysosome repair enables host cell survival and bacterial persistence following Chlamydia trachomatis infection. Cell. Microbiol. 2007, 9, 2141-2152.
14. McNeil, P.L.; Ito, S. Gastrointestinal cell plasma membrane wounding and resealing in vivo. Gastroenterology 1989, 96, 1238-1248.
15. Theodoropoulos, P.A.; Gravanis, A.; Tsapara, A.; Margioris, A.N.; Papadogiorgaki, E.; Galanopoulos, V.; Stournaras, C. Cytochalasin B may shorten actin filaments by a mechanism independent of barbed end capping. Biochem. Pharmacol. 1994, 47, 1875-1881.
16. Papini, E.; de Bernard, M.; Milia, E.; Bugnoli, M.; Zerial, M.; Rappuoli, R.; Montecucco, C. Cellular vacuoles induced by Helicobacter pylorioriginate from late endosomal compartments. Proc. Natl. Acad. Sci. USA 1994, 91, 9720-9724.
17. Marlink, K.L.; Bacon, K.D.; Sheppard, B.C.; Ashktorab, H.; Smoot, D.T.; Cover, T.L.; Deveney, C.W.; Rutten, M.J. Effects of Helicobacter pylori on intracellular Ca2+ signaling in normal human gastric mucous epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285, G163-G176.
18. Gerke, V.; Creutz, C.E.; Moss, S.E. Annexins: Linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6, 449-461.
19. Draeger, A.; Monastyrskaya, K.; Babiychuk, E.B. Plasma membrane repair and cellular damage control: The annexin survival kit. Biochem. Pharmacol. 2011, 81, 703-712.
20. Lennon, N.J.; Kho, A.; Bacskai, B.J.; Perlmutter, S.L.; Hyman, B.T.; Brown, R.H., Jr. Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing. J. Biol. Chem. 2003, 278, 50466-50473.
21. Lin, L.L.; Chen, C.N.; Lin, W.C.; Lee, P.H.; Chang, K.J.; Lai, Y.P.; Wang, J.T.; Juan, H.F. Annexin A4: A novel molecular marker for gastric cancer with Helicobacter pylori infection using proteomics approach. Proteomics Clin. Appl. 2008, 2, 619-634.
22. Togo, T.; Alderton, J.M.; Bi, G.Q.; Steinhardt, R.A. The mechanism of facilitated cell membrane resealing. J. Cell Sci. 1999, 112, 719-731.
23. Rodriguez, A.; Webster, P.; Ortego, J.; Andrews, N.W. Lysosomes behave as Ca2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 1997, 137, 93-104.
24. Watanabe, T.; Tada, M.; Nagai, H.; Sasaki, S.; Nakao, M. Helicobacter pylori infection induces gastric cancer in mongolian gerbils. Gastroenterology 1998, 115, 642-648.
25. Huynh, C.; Roth, D.; Ward, D.M.; Kaplan, J.; Andrews, N.W. Defective lysosomal exocytosis and plasma membrane repair in Chediak-Higashi/beige cells. Proc. Natl. Acad. Sci. USA 2004, 101, 16795-16800.
26. McNeil, P.L.; Warder, E. Glass beads load macromolecules into living cells. J. Cell Sci. 1987, 88, 669-678.
27. Mellgren, R.L.; Zhang, W.; Miyake, K.; McNeil, P.L. Calpain is required for the rapid, calcium-dependent repair of wounded plasma membrane. J. Biol. Chem. 2007, 282, 2567-2575.
28. McNeil, P.L.; Vogel, S.S.; Miyake, K.; Terasaki, M. Patching plasma membrane disruptions with cytoplasmic membrane. J. Cell Sci. 2000, 113, 1891-1902.
29. Liu, R.; Li, Z.; Bai, S.; Zhang, H.; Tang, M.; Lei, Y.; Chen, L.; Liang, S.; Zhao, Y.L.; Wei, Y.; Huang, C. Mechanism of cancer cell adaptation to metabolic stress: Proteomics identification of a novel thyroid hormone-mediated gastric carcinogenic signaling pathway. Mol. Cell. Proteomics 2009, 8, 70-85.
30. Amieva, M.R.; Vogelmann, R.; Covacci, A.; Tompkins, L.S.; Nelson, W.J.; Falkow, S. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 2003, 300, 1430-1434.
31. Lytton, S.D.; Fischer, W.; Nagel, W.; Haas, R.; Beck, F.X. Production of ammonium by Helicobacter pylori mediates occludin processing and disruption of tight junctions in Caco-2 cells. Microbiology 2005, 151, 3267-3276.
32. Idone, V.; Tam, C.; Goss, J.W.; Toomre, D.; Pypaert, M.; Andrews, N.W. Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis. J. Cell Biol. 2008, 180, 905-914.
33. Monastyrskaya, K.; Babiychuk, E.B.; Draeger, A. The annexins: Spatial and temporal coordination of signaling events during cellular stress. Cell. Mol. Life Sci. 2009, 66, 2623-2642.
34. Duncan, R.; Carpenter, B.; Main, L.C.; Telfer, C.; Murray, G.I. Characterisation and protein expression profiling of annexins in colorectal cancer. Br. J. Cancer 2008, 98, 426-433.
35. Jeon, Y.J.; Kim, D.H.; Jung, H.; Chung, S.J.; Chi, S.W.; Cho, S.; Lee, S.C.; Park, B.C.; Park, S.G.; Bae, K.H. Annexin A4 interacts with the NF-kappaB p50 subunit and modulates NF-kappaB transcriptional activity in a Ca2+-dependent manner. Cell. Mol. Life Sci. 2010, 67, 2271-2281.
36. Xin, W.; Rhodes, D.R.; Ingold, C.; Chinnaiyan, A.M.; Rubin, M.A. Dysregulation of the annexin family protein family is associated with prostate cancer progression. Am. J. Pathol. 2003, 162, 255-261.
37. Zimmermann, U.; Balabanov, S.; Giebel, J.; Teller, S.; Junker, H.; Schmoll, D.; Protzel, C.; Scharf, C.; Kleist, B.; Walther, R. Increased expression and altered location of annexin IV in renal clear cell carcinoma: A possible role in tumour dissemination. Cancer Lett. 2004, 209, 111-118.
38. Shen, J.; Person, M.D.; Zhu, J.; Abbruzzese, J.L.; Li, D. Protein expression profiles in pancreatic adenocarcinoma compared with normal pancreatic tissue and tissue affected by pancreatitis as detected by two-dimensional gel electrophoresis and mass spectrometry. Cancer Res. 2004, 64, 9018-9026.
39. Miao, Y.; Cai, B.; Liu, L.; Yang, Y.; Wan, X. Annexin IV is differentially expressed in clear cell carcinoma of the ovary. Int. J. Gynecol. Cancer Off. J. Int. Gynecol. Cancer Soc. 2009, 19, 1545-1549.
40. Toyama, A.; Suzuki, A.; Shimada, T.; Aoki, C.; Aoki, Y.; Umino, Y.; Nakamura, Y.; Aoki, D.; Sato, T.A. Proteomic characterization of ovarian cancers identifying annexin-A4, phosphoserine aminotransferase, cellular retinoic acid-binding protein 2, and serpin B5 as histology-specific biomarkers. Cancer Sci. 2012, 103, 747-755.
41. Lai, Y.P.; Yang, J.C.; Lin, T.Z.; Wang, J.T.; Lin, J.T. CagA tyrosine phosphorylation in gastric epithelial cells caused by Helicobacter pylori in patients with gastric adenocarcinoma. Helicobacter 2003, 8, 235-243.
42. Tzeng, C.C.; Meng, C.L.; Jin, L.; Hsieh, H.F. Cytogenetic studies of gastric adenocarcinoma. Cancer Genet. Cytogenet. 1991, 55, 67-71.