Proton pump inhibitors suppress iNOS-dependent DNA damage in Barrett's esophagus by increasing Mn-SOD expression

Biochemical and Biophysical Research Communications

Volumn 421, Issue 2, 2012, Pages 280-285

  Thanan, Raynoo ^a,b   Ma, Ning ^a   Iijima, Katsunori ^c   Abe, Yasuhiko ^c   Koike, Tomoyuki ^c   Shimosegawa, Tooru ^c   Pinlaor, Somchai ^d   Hiraku, Yusuke ^b   Oikawa, Shinji ^b   Murata, Mariko ^b   Kawanishi, Shosuke ^a  

^a SUZUKA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^b MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TOHOKU UNIVERSITY HOSPITAL   (Japan)

^d KHON KAEN UNIVERSITY   (Thailand)

Author keywords

8 Nitroguanine; Antioxidants; Barrett's esophagus; Oxidative stress; Proton pump inhibitors

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; 8 NITROGUANINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; LANSOPRAZOLE; MANGANESE SUPEROXIDE DISMUTASE; PROTON PUMP INHIBITOR; RABEPRAZOLE; TRANSCRIPTION FACTOR NRF2;

ADULT; AGED; ARTICLE; BARRETT ESOPHAGUS; CLINICAL ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFICACY; DRUG MECHANISM; ESOPHAGEAL ADENOCARCINOMA; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGED; BARRETT ESOPHAGUS; DEOXYGUANOSINE; DNA DAMAGE; ESOPHAGUS; GUANINE; HUMANS; MALE; NF-E2-RELATED FACTOR 2; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; PROTON PUMP INHIBITORS; SUPEROXIDE DISMUTASE;

EID: 84860465926     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.03.152     Document Type: Article

References (41)

1. Cameron A.J. Barrett's esophagus: does the incidence of adenocarcinoma matter?. Am. J. Gastroenterol. 1997, 92:193-194.
2. Shields H.M., Nardone G., Zhao J., Wang W., Xing Z., Fang D., Jacobson B.C., Romero Y., Dvorak K., Goldman A., Pellegrini C.A., Wiley E.L., Peura D.A., Tatum R.P., Schnell T.G. Barrett's esophagus: prevalence and incidence of adenocarcinomas. Ann. N. Y. Acad. Sci. 2011, 1232:230-247.
3. Barbera M., Fitzgerald R.C. Cellular mechanisms of Barrett's esophagus development. Surg. Oncol. Clin. N. Am. 2009, 18:393-410.
4. Wild C.P., Hardie L.J. Reflux, Barrett's oesophagus and adenocarcinoma: burning questions. Nat. Rev. Cancer 2003, 3:676-684.
5. Hutchinson L., Stenstrom B., Chen D., Piperdi B., Levey S., Lyle S., Wang T., Houghton J.M. Human Barrett's adenocarcinoma of the esophagus, associated myofibroblasts and endothelium can arise from bone marrow derived cells after allogeneic stem cell transplant. Stem Cells Dev 2011, 20:11-17.
6. Yoshida N., Yoshikawa T., Tanaka Y., Fujita N., Kassai K., Naito Y., Kondo M. A new mechanism for anti-inflammatory actions of proton pump inhibitors-inhibitory effects on neutrophil-endothelial cell interactions. Aliment Pharmacol. Ther. 2000, 14(Suppl. 1):74-81.
7. Hashioka S., Klegeris A., McGeer P.L. Proton pump inhibitors exert anti-inflammatory effects and decrease human microglial and monocytic THP-1 cell neurotoxicity. Exp. Neurol. 2009, 217:177-183.
8. Sachs G., Shin J.M., Vagin O., Lambrecht N., Yakubov I., Munson K. The gastric H, K ATPase as a drug target: past, present, and future. J. Clin. Gastroenterol. 2007, 41(Suppl 2):S226-S242.
9. El-Serag H.B., Aguirre T.V., Davis S., Kuebeler M., Bhattacharyya A., Sampliner R.E. Proton pump inhibitors are associated with reduced incidence of dysplasia in Barrett's esophagus. Am. J. Gastroenterol. 2004, 99:1877-1883.
10. Hillman L.C., Chiragakis L., Shadbolt B., Kaye G.L., Clarke A.C. Proton-pump inhibitor therapy and the development of dysplasia in patients with Barrett's oesophagus. Med. J. Aust. 2004, 180:387-391.
11. Curvers W.L., ten Kate F.J., Krishnadath K.K., Visser M., Elzer B., Baak L.C., Bohmer C., Mallant-Hent R.C., van Oijen A., Naber A.H., Scholten P., Busch O.R., Blaauwgeers H.G., Meijer G.A., Bergman J.J. Low-grade dysplasia in Barrett's esophagus: overdiagnosed and underestimated. Am. J. Gastroenterol. 2010, 105:1523-1530.
12. Nguyen D.M., El-Serag H.B., Henderson L., Stein D., Bhattacharyya A., Sampliner R.E. Medication usage and the risk of neoplasia in patients with Barrett's esophagus. Clin. Gastroenterol. Hepatol. 2009, 7:1299-1304.
13. Nguyen D.M., Richardson P., El-Serag H.B. Medications (NSAIDs, statins, proton pump inhibitors) and the risk of esophageal adenocarcinoma in patients with Barrett's esophagus. Gastroenterology 2010, 138:2260-2266.
14. Abdel-Latif M.M., Duggan S., Reynolds J.V., Kelleher D. Inflammation and esophageal carcinogenesis. Curr. Opin. Pharmacol. 2009, 9:396-404.
15. Kawanishi S., Hiraku Y., Pinlaor S., Ma N. Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol. Chem. 2006, 387:365-372.
16. Hiraku Y. Formation of 8-nitroguanine, a nitrative DNA lesion, in inflammation-related carcinogenesis and its significance. Environ. Health Prev. Med. 2010, 15:63-72.
17. Murata M., Thanan R., Ma N., Kawanishi S. Role of nitrative and oxidative DNA damage in inflammation-related carcinogenesis. J. Biomed. Biotechnol. 2012, 2012:623019.
18. Olliver J.R., Hardie L.J., Dexter S., Chalmers D., Wild C.P. DNA damage levels are raised in Barrett's oesophageal mucosa relative to the squamous epithelium of the oesophagus. Biomarkers 2003, 8:509-521.
19. Pinlaor S., Hiraku Y., Ma N., Yongvanit P., Semba R., Oikawa S., Murata M., Sripa B., Sithithaworn P., Kawanishi S. Mechanism of NO-mediated oxidative and nitrative DNA damage in hamsters infected with Opisthorchis viverrini: a model of inflammation-mediated carcinogenesis. Nitric Oxide 2004, 11:175-183.
20. Kawanishi S., Hiraku Y. Oxidative and nitrative DNA damage as biomarker for carcinogenesis with special reference to inflammation. Antioxid. Redox Signal. 2006, 8:1047-1058.
21. Loeb L.A., Preston B.D. Mutagenesis by apurinic/apyrimidinic sites. Annu. Rev. Genet. 1986, 20:201-230.
22. Yermilov V., Rubio J., Becchi M., Friesen M.D., Pignatelli B., Ohshima H. Formation of 8-nitroguanine by the reaction of guanine with peroxynitrite in vitro. Carcinogenesis 1995, 16:2045-2050.
23. Wu X., Takenaka K., Sonoda E., Hochegger H., Kawanishi S., Kawamoto T., Takeda S., Yamazoe M. Critical roles for polymerase ζ in cellular tolerance to nitric oxide-induced DNA damage. Cancer Res. 2006, 66:748-754.
24. Bruner S.D., Norman D.P., Verdine G.L. Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature 2000, 403:859-866.
25. Shibutani S., Takeshita M., Grollman A.P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 1991, 349:431-434.
26. Ditsworth D., Zong W.X. NF-κB: key mediator of inflammation-associated cancer. Cancer Biol. Ther. 2004, 3:1214-1216.
27. Pikarsky E., Porat R.M., Stein I., Abramovitch R., Amit S., Kasem S., Gutkovich-Pyest E., Urieli-Shoval S., Galun E., Ben-Neriah Y. NF-κB functions as a tumour promoter in inflammation-associated cancer. Nature 2004, 431:461-466.
28. Tak P.P., Firestein G.S. NF-κB: a key role in inflammatory diseases. J. Clin. Invest. 2001, 107:7-11.
29. Fridovich I. Superoxide dismutases. Annu. Rev. Biochem. 1975, 44:147-159.
30. Hermann B., Li Y., Ray M.B., Wo J.M., Martin R.C. Association of manganese superoxide dismutase expression with progression of carcinogenesis in Barrett esophagus. Arch. Surg. 2005, 140:1204-1209. discussion 1209.
31. S.C. Schiffman, Y. Li, D. Xiao, X. Li, H.S. Aiyer, R.C. Martin, The resistance of esophageal adenocarcinoma to bile salt insult is associated with manganese superoxide dismutase expression, J. Surg. Res. (2010).
32. Dreger H., Westphal K., Weller A., Baumann G., Stangl V., Meiners S., Stangl K. Nrf2-dependent upregulation of antioxidative enzymes: a novel pathway for proteasome inhibitor-mediated cardioprotection. Cardiovasc. Res. 2009, 83:354-361.
33. Na H.K., Kim E.H., Jung J.H., Lee H.H., Hyun J.W., Surh Y.J. (-)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells. Arch. Biochem. Biophys. 2008, 476:171-177.
34. Lee I.K., Kang K.A., Zhang R., Kim B.J., Kang S.S., Hyun J.W. Mitochondria protection of baicalein against oxidative damage via induction of manganese superoxide dismutase. Environ. Toxicol. Pharmacol. 2011, 31:233-241.
35. Khor T.O., Huang M.T., Prawan A., Liu Y., Hao X., Yu S., Cheung W.K., Chan J.Y., Reddy B.S., Yang C.S., Kong A.N. Increased susceptibility of Nrf2 knockout mice to colitis-associated colorectal cancer. Cancer Prev. Res. (Phila.) 2008, 1:187-191.
36. Kim J., Cha Y.N., Surh Y.J. A protective role of nuclear factor-erythroid 2-related factor-2 (Nrf2) in inflammatory disorders. Mutat. Res. 2010, 690:12-23.
37. Kundu J.K., Surh Y.J. Nrf2-Keap1 signaling as a potential target for chemoprevention of inflammation-associated carcinogenesis. Pharm. Res. 2010, 27:999-1013.
38. Zhang D.D. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab. Rev. 2006, 38:769-789.
39. Taguchi K., Motohashi H., Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 2011, 16:123-140.
40. Takagi T., Naito Y., Okada H., Ishii T., Mizushima K., Akagiri S., Adachi S., Handa O., Kokura S., Ichikawa H., Itoh K., Yamamoto M., Matsui H., Yoshikawa T. Lansoprazole, a proton pump inhibitor, mediates anti-inflammatory effect in gastric mucosal cells through the induction of heme oxygenase-1 via activation of NF-E2-related factor 2 and oxidation of kelch-like ECH-associating protein 1. J. Pharmacol. Exp. Ther. 2009, 331:255-264.
41. Morii M., Takata H., Takeguchi N. Acid activation of omeprazole in isolated gastric vesicles, oxyntic cells, and gastric glands. Gastroenterology 1989, 96:1453-1461.