Nox enzymes and oxidative stress in the immunopathology of the gastrointestinal tract

Seminars in Immunopathology

Volumn 30, Issue 3, 2008, Pages 315-327

  Rokutan, Kazuhito ^a   Kawahara, Tsukasa ^a   Kuwano, Yuki ^a   Tominaga, Kumiko ^a   Nishida, Keisei ^a   Teshima Kondo, Shigetada ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Carcinogenesis; Duox2; Inflammation; Innate immunity; Nox1; Nox2

Indexed keywords

ADENOSINE DERIVATIVE; DUAL OXIDASE 1; DUAL OXIDASE 2; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE 3; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE 5; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4;

CARCINOGENESIS; CHEMICAL INTERACTION; DIGESTIVE SYSTEM CANCER; DISEASE COURSE; ENTERITIS; ENZYME ANALYSIS; GASTROINTESTINAL TRACT; GENE EXPRESSION; HELICOBACTER PYLORI; HUMAN; IMMUNOPATHOLOGY; INNATE IMMUNITY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SEQUENCE HOMOLOGY; STOMACH CANCER;

ANIMALS; DIGESTIVE SYSTEM DISEASES; GASTROINTESTINAL TRACT; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; NADPH OXIDASE; OXIDATIVE STRESS;

EID: 47149085967     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-008-0124-5     Document Type: Review

References (119)

1. Abreu MT, Fukata M, Arditi M (2005) TLR signaling in the gut in health and disease. J Immunol 174:4453-4460, Medline
2. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783-801
3. Allen L-AH (2000) Modulating phagocyte activation: the pros and cons of Helicobacter pylori virulence factors. J Exp Med 191:1451-1454, Medline DOI 10.1084/jem.191.9.1451
4. Allen L-AH (2007) Phagocytosis and persistence of Helicobacter pylori. Cell Microbiol 9:817-828, Medline DOI 10.1111/j.1462-5822.2007.00906.x
5. Allen L-AH, Beecher BR, Lynch JT, Rohner OV, Wittine LM (2005) Helicobacter pylori disrupts NADPH oxidase targeting in human neutrophils to induce extracellular superoxide release. J Immunol 174:3658-3667, Medline
6. Ambasta RK, Kumar P, Griendling KK, Schmidt HHHW, Busse R, Brandes RP (2004) Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH Oxidase. J Biol Chem 279:45935-45941, Medline DOI 10.1074/jbc.M406486200
7. 2-generating activity. J Biol Chem 280:30046-30054, Medline DOI 10.1074/jbc.M500516200
8. Amieva MR, El-Omar EM (2008) Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134:306-323, Medline DOI 10.1053/j.gastro. 2007.11.009
9. Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, Cohen C, Moses M, Kilroy S, Arnold RS, Lambeth JD (2002) Reactive oxygen generated by Nox1 triggers the angiogenic switch. PNAS 99:715-720, Medline DOI 10.1073/pnas.022630199
10. Arnold RS, Shi J, Murad E, Whalen AM, Sun CQ, Polavarapu R, Parthasarathy S, Petros JA, Lambeth JD (2001) Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. PNAS 98:5550-5555, Medline DOI 10.1073/pnas.101505898
11. Aspholm-Hurtig M, Dailide G, Lahmann M, Kalia A, Ilver D, Roche N, Vikstrom S, Sjostrom R, Linden S, Backstrom A, Lundberg C, Arnqvist A, Mahdavi J, Nilsson UJ, Velapatino B, Gilman RH, Gerhard M, Alarcon T, Lopez-Brea M, Nakazawa T, Fox JG, Correa P, Dominguez-Bello MG, Perez-Perez GI, Blaser MJ, Normark S, Carlstedt I, Oscarson S, Teneberg S, Berg DE, Boren T (2004) Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305:519-522, Medline DOI 10.1126/science.1098801
12. Augusto AC, Miguel F, Mendonca S, Pedrazzoli Jr J, Gurgueira SA (2007) Oxidative stress expression status associated to Helicobacter pylori virulence in gastric diseases. Clin Biochem 40:615-622, Medline DOI 10.1016/j.clinbiochem. 2007.03.014
13. Baik S-C, Youn H-S, Chung M-H, Lee W-K, Cho M-J, Ko G-H, Park C-K, Kasai H, Rhee K-H (1996) Increased oxidative DNA damage in Helicobacter pylori-infected human gastric mucosa. Cancer Res 56:1279-1282, Medline
14. Baillon M-LA, van Vliet AHM, Ketley JM, Constantinidou C, Penn CW (1999) An iron-regulated alkyl hydroperoxide reductase (AhpC) confers arotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J Bacteriol 181:4798-4804, Medline
15. Banfi B, Clark RA, Steger K, Krause K-H (2003) Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J Biol Chem 278:3510-3513, Medline DOI 10.1074/jbc.C200613200
16. + channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science 287:138-142, Medline DOI 10.1126/science.287.5450.138
17. 2+ -activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem 276:37594-37601, Medline DOI 10.1074/jbc.M103034200
18. Bedard K, Krause K-H (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313, Medline DOI 10.1152/physrev.00044.2005
19. Blaser MJ, Atherton JC (2004) Helicobacter pylori persistence: biology and disease. J Clin Invest 113:321-333, Medline
20. Brewer AC, Sparks EC, Shah AM (2006) Transcriptional regulation of the NADPH oxidase isoform, Nox1, in colon epithelial cells: role of GATA-binding factor(s). Free Radic Biol Med 40:260-274, Medline DOI 10.1016/j.freeradbiomed. 2005.08.022
21. Brown JR, Goldblatt D, Buddle J, Morton L, Thrasher AJ (2003) Diminished production of anti-inflammatory mediators during neutrophil apoptosis and macrophage phagocytosis in chronic granulomatous disease (CGD). J Leukoc Biol 73:591-599, Medline DOI 10.1189/jlb.1202599
22. Brown SJ, Mayer L (2007) The immune response in inflammatory bowel disease. Am J Gastroenterol 102:2058-2069, Medline DOI 10.1111/j.1572-0241.2007. 01343.x
23. Bryk R, Griffin P, Nathan C (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211-215, Medline DOI 10.1038/35025109
24. Cheng G, Cao Z, Xu X, Meir EGV, Lambeth JD (2001) Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269:131-140, Medline DOI 10.1016/S0378-1119(01)00449-8
25. Cheng G, Diebold BA, Hughes Y, Lambeth JD (2006) Nox1-dependent reactive oxygen generation is regulated by Rac1. J Biol Chem 281:17718-17726, Medline DOI 10.1074/jbc.M512751200
26. Cheng G, Lambeth JD (2004) NOXO1, Regulation of lipid binding, localization, and activation of Nox1 by the phox homology (PX) domain. J Biol Chem 279:4737-4742, Medline DOI 10.1074/jbc.M305968200
27. Correa P (1992) Human gastric carcinogenesis: a multistep and multifactorial process-First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 52:6735-6740, Medline
28. Correa P, Houghton J (2007) Carcinogenesis of Helicobacter pylori. Gastroenterology 133:659-672, Medline DOI 10.1053/j.gastro.2007.06.026
29. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860-867, Medline DOI 10.1038/nature01322
30. Covacci A, Telford JL, Giudice GD, Parsonnet J, Rappuoli R (1999) Helicobacter pylori virulence and genetic geography. Science 284:1328-1333, Medline DOI 10.1126/science.284.35418.1328
31. de Carvalho DD, Sadok A, Bourgarel-Rey V, Gattacceca F, Penel C, Lehmann M, Kovacic H. (2008) Nox1 downstream of 12-lipoxygenase controls cell proliferation but not cell spreading of colon cancer cells. Int J Cancer 122:1757-1764
32. Davies GR, Simmonds NJ, Stevens TR, Sheaff MT, Banatvala N, Laurenson IF, Blake DR, Rampton DS (1994) Helicobacter pylori stimulates antral mucosal reactive oxygen metabolite production in vivo. Gut 35:179-185, Medline DOI 10.1136/gut.35.2.179
33. De Deken X, Wang D, Many M-C, Costagliola S, Libert F, Vassart G, Dumont JE, Miot F (2000) Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family. J Biol Chem 275:23227-23233, Medline DOI 10.1074/jbc.M000916200
34. Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47-95, Medline
35. Dupuy C, Pomerance M, Ohayon R, Noel-Hudson M-S, Deme D, Chaaraoui M, Francon J, Virion A (2000) Thyroid oxidase (THOX2) gene expression in the rat thyroid cell Line FRTL-5. Biochem Biophys Res Commun 277:287-292, Medline DOI 10.1006/bbrc.2000.3671
36. El-Omar EM, Rabkin CS, Gammon MD, Vaughan TL, Risch HA, Schoenberg JB, Stanford JL, Mayne ST, Goedert J, Blot WJ, Fraumeni JF Jr, Chow WH (2003) Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 124:1193-1201, Medline DOI 10.1016/S0016-5085(03)00157-4
37. El Hassani RA, Benfares N, Caillou B, Talbot M, Sabourin J-C, Belotte V, Morand S, Gnidehou S, Agnandji D, Ohayon R, Kaniewski J, Noel-Hudson M-S, Bidart J-M, Schlumberger M, Virion A, Dupuy C (2005) Dual oxidase2 is expressed all along the digestive tract. Am J Physiol Gastrointest Liver Physiol 288:G933-G942, Medline DOI 10.1152/ajpgi.00198.2004
38. Evans DJ Jr, Evans DG, Takemura T, Nakano H, Lampert HC, Graham DY, Granger DN, Kvietys PR (1995) Characterization of a Helicobacter pylori neutrophil-activating protein. Infect Immun 63:2213-2220, Medline
39. Farinati F, Cardin R, Degan P, Rugge M, Di Mario F, Bonvicini P, Naccarato R (1998) Oxidative DNA damage accumulation in gastric carcinogenesis. Gut 42:351-356, Medline
40. Figueiredo C, Machado JC, Pharoah P, Seruca R, Sousa S, Carvalho R, Capelinha AF, Quint W, Caldas C, van Doorn L-J, Carneiro F, Sobrinho-Simoes M (2002) Helicobacter pylori and interleukin 1 genotyping: an opportunity to identify high-risk individuals for gastric carcinoma. J Natl Cancer Inst 94:1680-1687, Medline
41. Fox JG, Wang TC (2001) Helicobacter pylori-not a good bug after all!. N Engl J Med 345:829-832, Medline DOI 10.1056/NEJM200109133451111
42. Fukata M, Abreu MT (2008) Role of Toll-like receptors in gastrointestinal malignancies. Oncogene 27:234-243, Medline DOI 10.1038/sj.onc.1210908
43. Fukuyama M, Rokutan K, Sano T, Miyake H, Shimada M, Tashiro S (2005) Overexpression of a novel superoxide-producing enzyme, NADPH oxidase 1, in adenoma and well differentiated adenocarcinoma of the human colon. Cancer Lett 221:97-104, Medline DOI 10.1016/j.canlet.2004.08.031
44. Gallin JI, Buescher ES (1983) Abnormal regulation of inflammatory skin responses in male patients with chronic granulomatous disease. Inflammation 7:227-232, Medline DOI 10.1007/BF00917259
45. Geiszt M, Lekstrom K, Brenner S, Hewitt SM, Dana R, Malech HL, Leto TL (2003) NAD(P)H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. J Immunol 171:299-306, Medline
46. Geiszt M, Lekstrom K, Witta J, Leto TL (2003) Proteins homologous to p47phox and p67phox support superoxide production by NAD(P)H oxidase 1 in colon epithelial cells. J Biol Chem 278:20006-20012, Medline DOI 10.1074/jbc. M301289200
47. Geiszt M, Leto TL (2004) The Nox family of NAD(P)H oxidases: host defense and beyond. J Biol Chem 279:51715-51718, Medline DOI 10.1074/jbc.R400024200
48. Geiszt M, Witta J, Baffi J, Lekstrom K, Leto TL (2003) Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J 17:1502-1504, Medline
49. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL (2001) Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167:1882-1885, Medline
50. Goodwin CS, Armstrong JA, Marshall BJ (1986) Campylobacter pyloridis, gastritis, and peptic ulceration. J Clin Pathol 39:353-365, Medline DOI 10.1136/jcp.39.4.353
51. Grandvaux N, Soucy-Faulkner A, Fink K (2007) Innate host defense: Nox and Duox on phox's tail. Biochimie 89:1113-1122, Medline DOI 10.1016/j.biochi.2007. 04.008
52. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, Kagnoff MF, Karin M (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118:285-296, Medline DOI 10.1016/j.cell.2004.07. 013
53. Guilford P, Hopkins J, Harraway J, McLeod M, McLeod N, Harawira P, Taite H, Scoular R, Miller A, Reeve AE (1998) E-cadherin germline mutations in familial gastric cancer. Nature 392:402-405, Medline DOI 10.1038/32918
54. Hampton MB, Vissers MCM, Keenan JI, Winterbourn CC (2002) Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease. J Leukoc Biol 71:775-781, Medline
55. Hanna IR, Hilenski LL, Dikalova A, Taniyama Y, Dikalov S, Lyle A, Quinn MT, Lassegue B, Griendling KK (2004) Functional association of nox1 with p22phox in vascular smooth muscle cells. Free Radic Biol Med 37:1542-1549, Medline DOI 10.1016/j.freeradbiomed.2004.08.011
56. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-1103, Medline DOI 10.1038/35074106
57. Hershberg RM (2002) The epithelial cell cytoskeleton and intracellular trafficking: V. Polarized compartmentalization of antigen processing and Toll-like receptor signaling in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 283:G833-G839, Medline
58. Houghton J, Wang TC (2005) Helicobacter pylori and gastric cancer: a new paradigm for inflammation-associated epithelial cancers. Gastroenterology 128:1567-1578, Medline DOI 10.1053/j.gastro.2005.03.037
59. Huang JS, Noack D, Rae J, Ellis BA, Newbury R, Pong AL, Lavine JE, Curnutte JT, Bastian J (2004) Chronic granulomatous disease caused by a deficiency in p47(phox) mimicking Crohn's disease. Clin Gastroenterol Hepatol 2:690-695, Medline DOI 10.1016/S1542-3565(04)00292-7
60. Huber MA, Azoitei N, Baumann B, Grunert S, Sommer A, Pehamberger H, Kraut N, Beug H, Wirth T (2004) NF-κB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest 114:569-581, Medline
61. Itzkowitz SH, Yio X (2004) Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 287:G7-G17, Medline DOI 10.1152/ajpgi.00079.2004
62. Jackson SH, Devadas S, Kwon J, Pinto LA, Williams MS (2004) T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat Immunol 5:818-827, Medline DOI 10.1038/ni1096
63. Karin M, Lawrence T, Nizet V (2006) Innate immunity gone awry: linking microbial infections to chronic inflammation and cancer. Cell 124:823-835, Medline DOI 10.1016/j.cell.2006.02.016
64. Kawahara T, Kohjima M, Kuwano Y, Mino H, Teshima-Kondo S, Takeya R, Tsunawaki S, Wada A, Sumimoto H, Rokutan K (2005) Helicobacter pylori lipopolysaccharide activates Rac1 and transcription of NADPH oxidase Nox1 and its organizer NOXO1 in guinea pig gastric mucosal cells. Am J Physiol Cell Physiol 288:C450-C457, Medline DOI 10.1152/ajpcell.00319.2004
65. Kawahara T, Kuwano Y, Teshima-Kondo S, Takeya R, Sumimoto H, Kishi K, Tsunawaki S, Hirayama T, Rokutan K (2004) Role of nicotinamide adenine dinucleotide phosphate oxidase 1 in oxidative burst response to Toll-like receptor 5 signaling in large intestinal epithelial cells. J Immunol 172:3051-3058, Medline
66. Kawahara T, Ritsick D, Cheng G, Lambeth JD (2005) Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1- and Nox2-dependent reactive oxygen generation. J Biol Chem 280:31859-31869, Medline DOI 10.1074/jbc.M501882200
67. Kawahara T, Teshima S, Oka A, Sugiyama T, Kishi K, Rokutan K (2001) Type I Helicobacter pylori lipopolysaccharide stimulates Toll-like receptor 4 and activates mitogen oxidase 1 in gastric pit cells. Infect Immun 69:4382-4389, Medline DOI 10.1128/IAI.69.7.4382-4389.2001
68. Keenan JI, Peterson Ii RA, Hampton MB (2005) NADPH oxidase involvement i n the pathology of Helicobacter pylori infection. Free Radic Biol Med 38:1188-1196, Medline DOI 10.1016/j.freeradbiomed.2004.12.025
69. Kikuchi H, Hikage M, Miyashita H, Fukumoto M (2000) NADPH oxidase subunit, gp91phox homologue, preferentially expressed in human colon epithelial cells. Gene 254:237-243, Medline DOI 10.1016/S0378-1119(00)00258-4
70. Kruidenier L, Verspaget HW (2002) Oxidative stress as a pathogenic factor in inflammatory bowel disease - radicals or ridiculous? Aliment Pharmacol Ther 16:1997-2015, Medline DOI 10.1046/j.1365-2036.2002.01378.x
71. Kuwano Y, Kawahara T, Yamamoto H, Teshima-Kondo S, Tominaga K, Masuda K, Kishi K, Morita K, Rokutan K (2006) Interferon-γ activates transcription of NADPH oxidase 1 gene and upregulates production of superoxide anion by human large intestinal epithelial cells. Am J Physiol Cell Physiol 290:C433-C443, Medline DOI 10.1152/ajpcell.00135.2005
72. Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4:181-189, Medline DOI 10.1038/nri1312
73. Lambeth JD (2007) Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic Biol Med 43:332-347, Medline DOI 10.1016/j.freeradbiomed.2007.03.027
74. Marciano BE, Rosenzweig SD, Kleiner DE, Anderson VL, Darnell DN, Anaya-O'Brien S, Hilligoss DM, Malech HL, Gallin JI, Holland SM (2004) Gastrointestinal involvement in chronic granulomatous disease. Pediatrics 114:462-468, Medline DOI 10.1542/peds.114.2.462
75. Marshall B, Warren JR (1984) Undefined curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 323:1311-1315, DOI 10.1016/S0140-6736(84)91816-6
76. Matsukura N, Suzuki K, Kawachi T, Aoyagi M, Sugimura T, Kitaoka H, Numajiri H, Shirota A, Itabashi M, Hirota T (1980) Distribution of marker enzymes and mucin in intestinal metaplasia in human stomach and relation to complete and incomplete types of intestinal metaplasia to minute gastric carcinomas. J Natl Cancer Inst 65:231-240, Medline
77. Menon SG, Goswami PC (2006) A redox cycle within the cell cycle: ring in the old with the new. Oncogene 26:1101-1109, Medline DOI 10.1038/sj.onc.1209895
78. Miyano K, Ueno N, Takeya R, Sumimoto H (2006) Direct involvement of the small GTPase Rac in activation of the superoxide-producing NADPH oxidase Nox1. J Biol Chem 281:21857-21868, Medline DOI 10.1074/jbc.M513665200
79. Moreno JC, Visser TJ (2007) New phenotypes in thyroid dyshormonogenesis: hypothyroidism due to DUOX2 mutations. Endocr Dev 10:99-117, Medline
80. Morgenstern DE, Gifford MAC, Li LL, Doerschuk CM, Dinauer MC (1997) Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus. J Exp Med 185:207-218, Medline DOI 10.1084/jem.185.2.207
81. Moss SF, Blaser, Martin J (2005) Mechanisms of disease: inflammation and the origins of cancer. Nat Clin Pract Oncol 2:90-97, Medline DOI 10.1038/ncponc0081
82. Mutoh H, Sakurai S, Satoh K, Tamada K, Kita H, Osawa H, Tomiyama T, Sato Y, Yamamoto H, Isoda N, Yoshida T, Ido K, Sugano K (2004) Development of gastric carcinoma from intestinal metaplasia in Cdx2-transgenic mice. Cancer Res 64:7740-7747, Medline DOI 10.1158/0008-5472.CAN-04-1617
83. Naumann M, Crabtree JE (2004) Helicobacter pylori-induced epithelial cell signalling in gastric carcinogenesis. Trends in Microbiology 12:29-36, Medline DOI 10.1016/j.tim.2003.11.005
84. Nomura A, Stemmermann GN, Chyou PH, Kato I, Perez-Perez GI, Blaser MJ (1991) Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med 325:1132-1136, Medline
85. Obst B, Wagner S, Sewing KF, Beil W (2000) Helicobacter pylori causes DNA damage in gastric epithelial cells. Carcinogenesis 21:1111-1115, Medline DOI 10.1093/carcin/21.6.1111
86. Panchal PC, Forman J, Blumberg DR, Wilson KT (2003) Helicobacter pylori infection: pathogenesis. Curr Opin Gastroenterol 19:1-3, Medline DOI 10.1097/00001574-200301000-00002
87. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, Sibley RK (1991) Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325:1127-1131, Medline
88. Perner A, Andresen L, Pedersen G, Rask-Madsen J (2003) Superoxide production and expression of NAD(P)H oxidases by transformed and primary human colonic epithelial cells. Gut 52:231-236, Medline DOI 10.1136/gut.52.2.231
89. Jenks PJ, Jeremy AHT, Robinson PA, Walker MM, Crabtree JE (2003) Long-term infection with Helicobacter felis and inactivation of the tumour suppressor gene p53 cumulatively enhance the gastric mutation frequency in Big BlueÒ transgenic mice. The Journal of Pathology 201:596-602, Medline DOI 10.1002/path.1488
90. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S, Gutkovich-Pyest E, Urieli-Shoval S, Galun E, Ben-Neriah Y (2004) NF-κB functions as a tumour promoter in inflammation-associated cancer. Nature 431:461-466, Medline DOI 10.1038/nature02924
91. Ramarao N, Gray-Owen SD, Meyer TF (2000) Helicobacter pylori induces but survives the extracellular release of oxygen radicals from professional phagocytes using its catalase activity. Mol Microbiol 38:103-113, Medline DOI 10.1046/j.1365-2958.2000.02114.x
92. Rezaie A, Parker R, Abdollahi M (2007) Oxidative stress and pathogenesis of inflammatory bowel disease: an epiphenomenon or the cause? Dig Dis Sci 52:2015-2021, Medline DOI 10.1007/s10620-006-9622-2
93. Peek RMJEC Jr (2006) Helicobacter infection and gastric neoplasia. The J Pathol 208:233-248, Medline DOI 10.1002/path.1868
94. Rokutan K, Kawahara T, Kuwano Y, Tominaga K, Sekiyama A, Teshima-Kondo S (2006) NADPH oxidases in the gastrointestinal tract: a potential role of Nox1 in innate immune response and carcinogenesis. Antioxid Redox Signal 8:1573-1582, Medline DOI 10.1089/ars.2006.8.1573
95. Salles N, Szanto I, Herrmann F, Armenian B, Stumm M, Stauffer E, Michel JP, Krause KH (2005) Expression of mRNA for ROS-generating NADPH oxidases in the aging stomach. Exp Gerontol 40:353-357, Medline DOI 10.1016/j.exger.2005.01.007
96. PJ Sansonetti 2006 The innate signaling of dangers and the dangers of innate signaling Nat Immunol 7 1237 1242 Sansonetti PJ (2006) The innate signaling of dangers and the dangers of innate signaling. Nat Immunol 7:1237-1242, Medline DOI 10.1038/ni1420
97. Sansonetti PJ (2004) War and peace at mucosal surfaces. Nat Rev Immunol 4:953-964, Medline DOI 10.1038/nri1499
98. Satin B, Del Giudice G, Della Bianca V, Dusi S, Laudanna C, Tonello F, Kelleher D, Rappuoli R, Montecucco C, Rossi F (2000) The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a protective antigen and a major virulence factor. J Exp Med 191:1467-1476, Medline DOI 10.1084/jem.191.9.1467
99. SchmaussEr B, Andrulis M, Endrich S, Lee SK, Josenhans C, Muller-Hermelink HK, Eck M (2004) Expression and subcellular distribution of toll-like receptors TLR4, TLR5 and TLR9 on the gastric epithelium in Helicobacter pylori infection. Clin Exp Immunol 136:521-526, Medline DOI 10.1111/j.1365-2249.2004.02464.x
100. Silberg DG, Sullivan J, Kang E, Swain GP, Moffett J, Sund NJ, Sackett SD, Kaestner KH (2002) Cdx2 ectopic expression induces gastric intestinal metaplasia in transgenic mice. Gastroenterology 122:689-696, Medline DOI 10.1053/gast.2002.31902
101. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD (1999) Cell transformation by the superoxide- generating oxidase Mox1. Nature 401:79-82, Medline DOI 10.1038/43459
102. Suzuki H, Miura S, Imaeda H, Suzuki M, Han JY, Mori M, Fukumura D, Tsuchiya M, Ishii H (1996) Enhanced levels of chemiluminescence and platelet activating factor in urease-positive gastric ulcers. Free Radic Biol Med 20:449-454, Medline DOI 10.1016/0891-5849(96)02048-5
103. Szanto I, Rubbia-Brandt L, Kiss P, Steger K, Banfi B, Kovari E, Herrmann F, Hadengue A, Krause KH (2005) Expression of NOX1, a superoxide-generating NADPH oxidase, in colon cancer and inflammatory bowel disease. J Pathol 207:164-176, Medline DOI 10.1002/path.1824
104. Takeya R, Ueno N, Kami K, Taura M, Kohjima M, Izaki T, Nunoi H, Sumimoto H (2003) Novel human homologues of p47phox and p67phox participate in activation of superoxide-producing NADPH oxidases. J Biol Chem 278:25234-25246, Medline DOI 10.1074/jbc.M212856200
105. Teshima S, Kutsumi H, Kawahara T, Kishi K, Rokutan K (2000) Regulation of growth and apoptosis of cultured guinea pig gastric mucosal cells by mitogenic oxidase 1. Am J Physiol Gastrointest Liver Physiol 279:G1169-G1176, Medline
106. Teshima S, Rokutan K, Nikawa T, Kishi K (1998) Guinea pig gastric mucosal cells produce abundant superoxide anion through an NADPH oxidase-like system. Gastroenterology 115:1186-1196, Medline DOI 10.1016/S0016-5085(98)70090-3
107. Tominaga K, Kawahara T, Sano T, Toida K, Kuwano Y, Sasaki H, Kawai T, T eshima-Kondo S, Rokutan K (2007) Evidence for cancer-associated expression of NADPH oxidase 1 (Nox1)-based oxidase system in the human stomach. Free Radic Biol Med 43:1627-1638, Medline DOI 10.1016/j.freeradbiomed.2007.08.029
108. Tonello F, Dundon WG, Satin B, Molinari M, Tognon G, Grandi G, Del Giudice G, Rappuoli R, Montecucco C (1999) The Helicobacter pylori neutrophil-activating protein is an iron-binding protein with dodecameric structure. Mol Microbiol 34:238-246, Medline DOI 10.1046/j.1365-2958.1999.01584. x
109. Touati E, Michel V, Thiberge J-M, Wuscher N, Huerre M, Labigne A (2003) Chronic Helicobacter pylori infections induce gastric mutations in mice. Gastroenterology 124:1408-1419, Medline DOI 10.1016/S0016-5085(03)00266-X
110. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schlemper RJ (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345:784-789, Medline DOI 10.1056/NEJMoa001999
111. Ueyama T, Geiszt M, Leto TL (2006) Involvement of Rac1 in activation of multicomponent Nox1- and Nox3-based NADPH oxidases. Mol Cell Biol 26:2160-2174, Medline DOI 10.1128/MCB.26.6.2160-2174.2006
112. Ushio-Fukai M (2006) Redox signaling in angiogenesis: role of NADPH oxidase. Cardiovascular Res 71:226-235, Medline DOI 10.1016/j.cardiores.2006.04. 015
113. Valente AJ, Zhou Q, Lu Z, He W, Qiang M, Ma W, Li G, Wang L, Banfi B, Steger K, Krause KH, Clark RA, Li S (2007) Regulation of NOX1 expression by GATA, HNF-1α, and Cdx transcription factors. Free Radic Biol Med 22:22
114. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, Athman R, Memet S, Huerre MR, Coyle AJ, DiStefano PS, Sansonetti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5:1166-1174, Medline DOI 10.1038/ni1131
115. Wilson KT, Crabtree JE (2007) Immunology of Helicobacter pylori: insights into the failure of the immune response and perspectives on vaccine studies. Gastroenterology 133:288-308, Medline DOI 10.1053/j.gastro.2007.05.008
116. Xia C, Meng Q, Liu L-Z, Rojanasakul Y, Wang X-R, Jiang B-H (2007) Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res 67:10823-10830, Medline DOI 10.1158/0008-5472.CAN-07-0783
117. Xu H, Chaturvedi R, Cheng Y, Bussiere FI, Asim M, Yao MD, Potosky D, Meltzer SJ, Rhee JG, Kim SS, Moss SF, Hacker A, Wang Y, Casero RA Jr, Wilson KT (2004) Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res 64:8521-8525, Medline DOI 10.1158/0008-5472.CAN-04-3511
118. Yang S, Panoskaltsis-Mortari A, Shukla M, Blazar BR, Haddad IY (2002) Exuberant inflammation in nicotinamide adenine dinucleotide phosphate-oxidase- deficient mice after allogeneic marrow transplantation. J Immunol 168:5840-5847, Medline
119. Yuasa Y (2003) Control of gut differentiation and intestinal-type gastric carcinogenesis. Nat Rev Cancer 3:592-600, Medline DOI 10.1038/nrc1141