Reactive oxygen species-induced autophagic degradation of helicobacter pylori CagA is specifically suppressed in cancer stem-like cells

Cell Host and Microbe

Volumn 12, Issue 6, 2012, Pages 764-777

  Tsugawa, Hitoshi ^a   Suzuki, Hidekazu ^a   Saya, Hideyuki ^a   Hatakeyama, Masanori ^b   Hirayama, Toshiya ^c   Hirata, Kenro ^a   Nagano, Osamu ^a   Matsuzaki, Juntaro ^a   Hibi, Toshifumi ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CAGA PROTEIN; GLUTATHIONE; HERMES ANTIGEN; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE;

ARTICLE; AUTOPHAGY; CANCER STEM CELL; CONTROLLED STUDY; ENZYME ACTIVATION; HELICOBACTER PYLORI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PYLORUS; STOMACH CANCER;

ANTIGENS, BACTERIAL; ANTIGENS, CD44; AUTOPHAGY; BACTERIAL PROTEINS; CELL LINE, TUMOR; EPITHELIAL CELLS; HELICOBACTER PYLORI; HUMANS; PROTEOLYSIS; REACTIVE OXYGEN SPECIES; VIRULENCE FACTORS;

HELICOBACTER PYLORI;

EID: 84870999066     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2012.10.014     Document Type: Article

References (39)

1. K.R. Atkuri, J.J. Mantovani, L.A. Herzenberg, and L.A. Herzenberg N-Acetylcysteine - a safe antidote for cysteine/glutathione deficiency Curr. Opin. Pharmacol. 7 2007 355 359
2. D. Basso, C.F. Zambon, D.P. Letley, A. Stranges, A. Marchet, J.L. Rhead, S. Schiavon, G. Guariso, M. Ceroti, and D. Nitti Clinical relevance of Helicobacter pylori cagA and vacA gene polymorphisms Gastroenterology 135 2008 91 99
3. M.J. Blaser, G.I. Perez-Perez, H. Kleanthous, T.L. Cover, R.M. Peek, P.H. Chyou, G.N. Stemmermann, and A. Nomura Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach Cancer Res. 55 1995 2111 2115
4. T.L. Cover, and S.R. Blanke Helicobacter pylori VacA, a paradigm for toxin multifunctionality Nat. Rev. Microbiol. 3 2005 320 332
5. P. Dalerba, S.J. Dylla, I.K. Park, R. Liu, X. Wang, R.W. Cho, T. Hoey, A. Gurney, E.H. Huang, and D.M. Simeone Phenotypic characterization of human colorectal cancer stem cells Proc. Natl. Acad. Sci. USA 104 2007 10158 10163
6. V. Deretic, and B. Levine Autophagy, immunity, and microbial adaptations Cell Host Microbe 5 2009 527 549
7. S.Z. Ding, Y. Minohara, X.J. Fan, J. Wang, V.E. Reyes, J. Patel, B. Dirden-Kramer, I. Boldogh, P.B. Ernst, and S.E. Crowe Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells Infect. Immun. 75 2007 4030 4039
8. S. Dong-Yun, D. Yu-Ru, L. Shan-Lin, Z. Ya-Dong, and W. Lian Redox stress regulates cell proliferation and apoptosis of human hepatoma through Akt protein phosphorylation FEBS Lett. 542 2003 60 64
9. X. Fan, A. Long, M. Goggins, X. Fan, P.W. Keeling, and D. Kelleher Expression of CD44 and its variants on gastric epithelial cells of patients with Helicobacter pylori colonisation Gut 38 1996 507 512
10. M. Hatakeyama Oncogenic mechanisms of the Helicobacter pylori CagA protein Nat. Rev. Cancer 4 2004 688 694
11. J.Q. Huang, G.F. Zheng, K. Sumanac, E.J. Irvine, and R.H. Hunt Meta-analysis of the relationship between cagA seropositivity and gastric cancer Gastroenterology 125 2003 1636 1644
12. J. Huang, V. Canadien, G.Y. Lam, B.E. Steinberg, M.C. Dinauer, M.A. Magalhaes, M. Glogauer, S. Grinstein, and J.H. Brumell Activation of antibacterial autophagy by NADPH oxidases Proc. Natl. Acad. Sci. USA 106 2009 6226 6231
13. S. Ishikawa, T. Ohta, and M. Hatakeyama Stability of Helicobacter pylori CagA oncoprotein in human gastric epithelial cells FEBS Lett. 583 2009 2414 2418
14. T. Ishimoto, H. Oshima, M. Oshima, K. Kai, R. Torii, T. Masuko, H. Baba, H. Saya, and O. Nagano CD44+ slow-cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis Cancer Sci. 101 2010 673 678
15. T. Ishimoto, O. Nagano, T. Yae, M. Tamada, T. Motohara, H. Oshima, M. Oshima, T. Ikeda, R. Asaba, and H. Yagi CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth Cancer Cell 19 2011 387 400
16. D.G. Marshall, S.O. Hynes, D.C. Coleman, C.A. O'Morain, C.J. Smyth, and A.P. Moran Lack of a relationship between Lewis antigen expression and cagA, CagA, vacA and VacA status of Irish Helicobacter pylori isolates FEMS Immunol. Med. Microbiol. 24 1999 79 90
17. B. Mayer, K.W. Jauch, U. Günthert, C.G. Figdor, F.W. Schildberg, I. Funke, and J.P. Johnson De-novo expression of CD44 and survival in gastric cancer Lancet 342 1993 1019 1022
18. S. Miehlke, C. Kirsch, K. Agha-Amiri, T. Günther, N. Lehn, P. Malfertheiner, M. Stolte, G. Ehninger, and E. Bayerdörffer The Helicobacter pylori vacA s1, m1 genotype and cagA is associated with gastric carcinoma in Germany Int. J. Cancer 87 2000 322 327
19. Y. Ogawara, S. Kishishita, T. Obata, Y. Isazawa, T. Suzuki, K. Tanaka, N. Masuyama, and Y. Gotoh Akt enhances Mdm2-mediated ubiquitination and degradation of p53 J. Biol. Chem. 277 2002 21843 21850
20. N. Ohnishi, H. Yuasa, S. Tanaka, H. Sawa, M. Miura, A. Matsui, H. Higashi, M. Musashi, K. Iwabuchi, and M. Suzuki Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse Proc. Natl. Acad. Sci. USA 105 2008 1003 1008
21. S.A. Patel, B.A. Warren, J.F. Rhoderick, and R.J. Bridges Differentiation of substrate and non-substrate inhibitors of transport system xc(-): an obligate exchanger of L-glutamate and L-cystine Neuropharmacology 46 2004 273 284
22. D. Raju, S. Hussey, M. Ang, M.R. Terebiznik, M. Sibony, E. Galindo-Mata, V. Gupta, S.R. Blanke, A. Delgado, and J. Romero-Gallo Vacuolating cytotoxin and variants in Atg16L1 that disrupt autophagy promote Helicobacter pylori infection in humans Gastroenterology 142 2012 1160 1171
23. Y. Saito, N. Murata-Kamiya, T. Hirayama, Y. Ohba, and M. Hatakeyama Conversion of Helicobacter pylori CagA from senescence inducer to oncogenic driver through polarity-dependent regulation of p21 J. Exp. Med. 207 2010 2157 2174
24. R. Scherz-Shouval, and Z. Elazar ROS, mitochondria and the regulation of autophagy Trends Cell Biol. 17 2007 422 427
25. H. Suzuki, M. Suematsu, H. Ishii, S. Kato, H. Miki, M. Mori, Y. Ishimura, T. Nishino, and M. Tsuchiya Prostaglandin E1 abrogates early reductive stress and zone-specific paradoxical oxidative injury in hypoperfused rat liver J. Clin. Invest. 93 1994 155 164
26. H. Suzuki, E. Iwasaki, and T. Hibi Helicobacter pylori and gastric cancer Gastric Cancer 12 2009 79 87
27. S. Takaishi, T. Okumura, S. Tu, S.S. Wang, W. Shibata, R. Vigneshwaran, S.A. Gordon, Y. Shimada, and T.C. Wang Identification of gastric cancer stem cells using the cell surface marker CD44 Stem Cells 27 2009 1006 1020
28. M. Tamada, O. Nagano, S. Tateyama, M. Ohmura, T. Yae, T. Ishimoto, E. Sugihara, N. Onishi, T. Yamamoto, and H. Yanagawa Modulation of glucose metabolism by CD44 contributes to antioxidant status and drug resistance in cancer cells Cancer Res. 72 2012 1438 1448
29. M.R. Terebiznik, D. Raju, C.L. Vázquez, K. Torbricki, R. Kulkarni, S.R. Blanke, T. Yoshimori, M.I. Colombo, and N.L. Jones Effect of Helicobacter pylori's vacuolating cytotoxin on the autophagy pathway in gastric epithelial cells Autophagy 5 2009 370 379
30. N. Uemura, S. Okamoto, S. Yamamoto, N. Matsumura, S. Yamaguchi, M. Yamakido, K. Taniyama, N. Sasaki, and R.J. Schlemper Helicobacter pylori infection and the development of gastric cancer N. Engl. J. Med. 345 2001 784 789
31. H.J. Wang, C.H. Kuo, A.A. Yeh, P.C. Chang, and W.C. Wang Vacuolating toxin production in clinical isolates of Helicobacter pylori with different vacA genotypes J. Infect. Dis. 178 1998 207 212
32. J. Wei, T.A. Nagy, A. Vilgelm, E. Zaika, S.R. Ogden, J. Romero-Gallo, M.B. Piazuelo, P. Correa, M.K. Washington, and W. El-Rifai Regulation of p53 tumor suppressor by Helicobacter pylori in gastric epithelial cells Gastroenterology 139 2010 1333 1343
33. T. Yae, K. Tsuchihashi, T. Ishimoto, T. Motohara, M. Yoshikawa, G.J. Yoshida, T. Wada, T. Masuko, K. Mogushi, and H. Tanaka Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell Nat Commun. 3 2012 883
34. K. Yahiro, T. Niidome, M. Kimura, T. Hatakeyama, H. Aoyagi, H. Kurazono, K. Imagawa, A. Wada, J. Moss, and T. Hirayama 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 1999 36693 36699
35. K. Yahiro, M. Satoh, M. Nakano, J. Hisatsune, H. Isomoto, J. Sap, H. Suzuki, F. Nomura, M. Noda, J. Moss, and T. Hirayama Low-density lipoprotein receptor-related protein-1 (LRP1) mediates autophagy and apoptosis caused by Helicobacter pylori VacA J. Biol. Chem. 287 2012 31104 31115
36. Y. Yamaoka, T. Kodama, M. Kita, J. Imanishi, K. Kashima, and D.Y. Graham Relationship of vacA genotypes of Helicobacter pylori to cagA status, cytotoxin production, and clinical outcome Helicobacter 3 1998 241 253
37. S. Yamazaki, A. Yamakawa, Y. Ito, M. Ohtani, H. Higashi, M. Hatakeyama, and T. Azuma The CagA protein of Helicobacter pylori is translocated into epithelial cells and binds to SHP-2 in human gastric mucosa J. Infect. Dis. 187 2003 334 337
38. K. Yokoyama, H. Higashi, S. Ishikawa, Y. Fujii, S. Kondo, H. Kato, T. Azuma, A. Wada, T. Hirayama, H. Aburatani, and M. Hatakeyama Functional antagonism between Helicobacter pylori CagA and vacuolating toxin VacA in control of the NFAT signaling pathway in gastric epithelial cells Proc. Natl. Acad. Sci. USA 102 2005 9661 9666
39. B.P. Zhou, Y. Liao, W. Xia, Y. Zou, B. Spohn, and M.C. Hung HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation Nat. Cell Biol. 3 2001 973 982