Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA

Gastroenterology

Volumn 141, Issue 5, 2011, Pages 1696-1708.e2

  Chaturvedi, Rupesh ^a,c   Asim, Mohammad ^a,c   Romero Gallo, Judith ^a   Barry, Daniel P ^a,c   Hoge, Svea ^a,d   De Sablet, Thibaut ^a,c   Delgado, Alberto G ^a   Wroblewski, Lydia E ^a   Piazuelo, M Blanca ^a   Yan, Fang ^a   Israel, Dawn A ^a   Casero Jr , Robert A ^e   Correa, Pelayo ^a   Gobert, Alain P ^a,c,f   Polk, D Brent ^a,g   Peek Jr , Richard M ^a,b,c   Wilson, Keith T ^a,b,c  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f CEMAGREF   (France)

^g UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

DNA Damage; Epithelial Cells; Polyamines

Indexed keywords

CAGA PROTEIN; DNA; OXIDOREDUCTASE; SMALL INTERFERING RNA; SPERMINE OXIDASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER RISK; CONTROLLED STUDY; DNA DAMAGE; DYSPLASIA; ENZYME ACTIVITY; EPITHELIUM CELL; FLOW CYTOMETRY; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH BIOPSY; STOMACH CANCER; STOMACH EPITHELIUM;

EID: 80054859726     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2011.07.045     Document Type: Article

References (40)

1. Parsonnet J, Friedman GD, Vandersteen DP, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 1991;325:1127-1131.
2. Parkin DM, Bray FI, Devesa SS. Cancer burden in the year 2000. The global picture. Eur J Cancer 2001;37(Suppl 8):S4-S66.
3. Peek RM Jr, Fiske C, Wilson KT. Role of innate immunity in Helicobacter pylori-induced gastric malignancy. Physiol Rev 2010;90:831-858.
4. Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010;23:713-739.
5. Moss SF, Calam J, Agarwal B, et al. Induction of gastric epithelial apoptosis by Helicobacter pylori. Gut 1996;38:498-501. (Pubitemid 26111366)
6. Wagner S, Beil W, Westermann J, et al. Regulation of gastric epithelial cell growth by Helicobacter pylori: offdence for a major role of apoptosis. Gastroenterology 1997;113:1836-1847. (Pubitemid 27512142)
7. Yan F, Cao H, Chaturvedi R, et al. Epidermal growth factor receptor activation protects gastric epithelial cells from Helicobacter pyloriinduced apoptosis. Gastroenterology 2009;136:1297-1307.
8. Chaturvedi R, Cheng Y, Asim M, et al. Induction of polyamine oxidase 1 by Helicobacter pylori causes macrophage apoptosis by hydrogen peroxide release and mitochondrial membrane depolarization. J Biol Chem 2004;279:40161-40173. (Pubitemid 39258292)
9. Xu H, Chaturvedi R, Cheng Y, et al. Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res 2004;64:8521-8525. (Pubitemid 39552063)
10. Bagchi D, Bhattacharya G, Stohs SJ. Production of reactive oxygen species by gastric cells in association with Helicobacter pylori. Free Radic Res 1996;24:439-450. (Pubitemid 26188962)
11. Farinati F, Cardin R, Degan P, et al. Oxidative DNA damage accumulation in gastric carcinogenesis. Gut 1998;42:351-356. (Pubitemid 28197023)
12. Touati E, Michel V, Thiberge JM, et al. Chronic Helicobacter pylori infections induce gastric mutations in mice. Gastroenterology 2003;124:1408-1419. (Pubitemid 36531814)
13. Wei J, Nagy TA, Vilgelm A, et al. Regulation of p53 tumor suppressor by Helicobacter pylori in gastric epithelial cells. Gastroenterology 2010;139:1333-1343.
14. Amieva MR, Vogelmann R, Covacci A, et al. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 2003;300:1430-1434. (Pubitemid 36638162)
15. Odenbreit S, Puls J, Sedlmaier B, et al. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 2000;287:1497-1500. (Pubitemid 30127145)
16. Kuipers EJ, Perez-Perez GI, Meuwissen SG, et al. Helicobacter pylori and atrophic gastritis: importance of the cagA status. J Natl Cancer Inst 1995;87:1777-1780.
17. Parsonnet J, Friedman GD, Orentreich N, et al. Risk for gastric cancer in people with CagA positive or CagA negative Helicobacter pylori infection. Gut 1997;40:297-301. (Pubitemid 27145639)
18. Blaser MJ, Perez-Perez GI, Kleanthous H, et al. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 1995;55:2111-2115.
19. Ohnishi N, Yuasa H, Tanaka S, et al. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci U S A 2008;105:1003-1008. (Pubitemid 351282071)
20. Franco AT, Israel DA, Washington MK, et al. Activation of betacatenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci U S A 2005;102:10646-10651. (Pubitemid 41061608)
21. Peek RM Jr, Blaser MJ, Mays DJ, et al. Helicobacter pylori strainspecific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res 1999;59:6124-6131. (Pubitemid 30035632)
22. Arnold I, Lee JY, Amieva MR, et al. Tolerance rather than immunity protects from Helicobacter pylori-induced gastric preneoplasia. Gastroenterology 2011;140:199-209.
23. Whitehead RH, VanEeden PE, Noble MD, et al. Establishment of conditionally immortalized epithelial cell lines from both colon and small intestine of adult H-2Kb-tsA58 transgenic mice. Proc Natl Acad Sci U S A 1993;90:587-591. (Pubitemid 23028908)
24. Franco AT, Johnston E, Krishna U, et al. Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res 2008;68:379-387. (Pubitemid 351380064)
25. Hong SK, Chaturvedi R, Piazuelo MB, et al. Increased expression and cellular localization of spermine oxidase in ulcerative colitis and relationship to disease activity. Inflamm Bowel Dis 2010;16:1557-1566.
26. Davies GR, Simmonds NJ, Stevens TR, et al. Helicobacter pylori stimulates antral mucosal reactive oxygen metabolite production in vivo. Gut 1994;35:179-185. (Pubitemid 24092862)
27. Murray-Stewart T, Wang Y, Goodwin A, et al. Nuclear localization of human spermine oxidase isoforms-possible implications in drug response and disease etiology. FEBS J 2008;275:2795-2806. (Pubitemid 351678666)
28. Shirin H, Sordillo EM, Oh SH, et al. Helicobacter pylori inhibits the G1 to S transition in AGS gastric epithelial cells. Cancer Res 1999;59:2277-2281. (Pubitemid 29242267)
29. Peek RM Jr, Moss SF, Tham KT, et al. Helicobacter pylori cagA+ strains and dissociation of gastric epithelial cell proliferation from apoptosis. J Natl Cancer Inst 1997;89:863-868. (Pubitemid 27268451)
30. Cover TL, Krishna US, Israel DA, et al. Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res 2003;63:951-957. (Pubitemid 36278424)
31. Oldani A, Cormont M, Hofman V, et al. Helicobacter pylori counteracts the apoptotic action of its VacA toxin by injecting the CagA protein into gastric epithelial cells. PLoS Pathog 2009;5:e1000603.
32. Bussiere FI, Chaturvedi R, Asim M, et al. Low multiplicity of infection of Helicobacter pylori suppresses apoptosis of B lymphocytes. Cancer Res 2006;66:6834-6842. (Pubitemid 44085644)
33. Tsutsumi R, Higashi H, Higuchi M, et al. Attenuation of Helicobacter pylori CagA·SHP-2 signaling by interaction between CagA and C-terminal Src kinase. J Biol Chem 2003;278:3664-3670. (Pubitemid 36801090)
34. Ladeira MS, Rodrigues MA, Salvadori DM, et al. Relationships between cagA, vacA, and iceA genotypes of Helicobacter pylori and DNA damage in the gastric mucosa. Environ Mol Mutagen 2004;44:91-98. (Pubitemid 39063337)
35. Mimuro H, Suzuki T, Nagai S, et al. Helicobacter pylori dampens gut epithelial self-renewal by inhibiting apoptosis, a bacterial strategy to enhance colonization of the stomach. Cell Host Microbe 2007;2:250-263. (Pubitemid 47500824)
36. Matsumoto Y, Marusawa H, Kinoshita K, et al. Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nat Med 2007;13:470-476. (Pubitemid 46559833)
37. Quante M, Tu SP, Tomita H, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011;19:257-272.
38. Qiao XT, Ziel JW, McKimpson W, et al. Prospective identification of a multilineage progenitor in murine stomach epithelium. Gastroenterology 2007;133:1989-1998.
39. Houghton J, Stoicov C, Nomura S, et al. Gastric cancer originating from bone marrow-derived cells. Science 2004;306:1568-1571. (Pubitemid 39564955)
40. Chaturvedi R, Asim M, Hoge S, et al. Polyamines impair immunity to Helicobacter pylori by inhibiting L-arginine uptake required for nitric oxide production. Gastroenterology 2010;139:1686-1698.