The Gastric Mucosa from Patients Infected with CagA+ or VacA+ Helicobacter pylori Has a Lower Level of Dual Oxidase-2 Expression than Uninfected or Infected with CagA−/VacA− H. pylori

Digestive Diseases and Sciences

Volumn 61, Issue 8, 2016, Pages 2328-2337

  Li, Hongqian ^a,e   Zhou, Yunfeng ^b   Zheng, Yufeng ^a   Guo, Hong ^a   Gao, Lei ^a   Chen, Pan ^a   Feng, Dandan ^a   Wu, Lijuan ^a   Yang, Moli ^a   Qi, Yanli ^a   Guo, Hao ^a   Chang, Yongchao ^a   Chu, Fong Fong ^c   Gao, Qiang ^a,d  

^a HENAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b Shenzhen University School of Medicine   (China)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^d CAPITAL MEDICAL UNIVERSITY   (China)

^e Puyang Oilfield General Hospital   (China)

Author keywords

Dual oxidase 2 (DUOX2); Gastric mucosa; Helicobacter pylori (H. pylori); Lactoperoxidase (LPO); NOX2

Indexed keywords

CAGA PROTEIN; DUAL OXIDASE 2; IMMUNOGLOBULIN G; LACTOPEROXIDASE; MYELOPEROXIDASE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG; VACUOLATING TOXIN; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; BACTERIUM ANTIBODY; CAGA PROTEIN, HELICOBACTER PYLORI; CYBB PROTEIN, HUMAN; DUOX2 PROTEIN, HUMAN; MEMBRANE PROTEIN; MESSENGER RNA; NOX1 PROTEIN, HUMAN; PEROXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; VACA PROTEIN, HELICOBACTER PYLORI;

ADULT; AGED; ARTICLE; ATROPHIC GASTRITIS; DUODENUM ULCER; EPITHELIUM CELL; FEMALE; GASTRIC MUCOSA; GASTRITIS; GENE EXPRESSION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFECTION RATE; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STOMACH BIOPSY; STOMACH ULCER; SURVIVAL; WESTERN BLOTTING; ADOLESCENT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PEPTIC ULCER; STOMACH MUCOSA; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GASTRIC MUCOSA; GASTRITIS; GASTRITIS, ATROPHIC; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; IMMUNOGLOBULIN G; IMMUNOHISTOCHEMISTRY; LACTOPEROXIDASE; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; NADPH OXIDASE; PEPTIC ULCER; PEROXIDASE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; YOUNG ADULT;

EID: 84962660794     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-016-4144-z     Document Type: Article

References (64)

1. Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet. 1984;1:1311–1315.
2. Everhart JE. Recent developments in the epidemiology of Helicobacter pylori. Gastroenterol Clin North Am. 2000;29:559–578.
3. Malnick SD, Melzer E, Attali M, Duek G, Yahav J. Friend or foe? World J Gastroenterol. 2014;20:8979–8985.
4. McColl KE. Clinical practice. Helicobacter pylori infection. N Engl J Med. 2010;362:1597–1604.
5. Sonnenberg A, Lash RH, Genta RM. A national study of Helicobactor pylori infection in gastric biopsy specimens. Gastroenterology. 2010;139:1894–1901.
6. Corley DA, Kubo A, Levin TR, et al. Helicobacter pylori and gastroesophageal reflux disease: a case-control study. Helicobacter. 2008;13:352–360.
7. Chen Y, Blaser MJ. Inverse associations of Helicobacter pylori with asthma and allergy. Arch Intern Med. 2007;167:821–827.
8. Luther J, Dave M, Higgins PD, Kao JY. Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Inflamm Bowel Dis. 2010;16:1077–1084.
9. Gebert B, Fischer W, Haas R. The Helicobacter pylori vacuolating cytotoxin: from cellular vacuolation to immunosuppressive activities. Rev Physiol Biochem Pharmacol. 2004;152:205–220.
10. Yuan J, Li P, Tao J, et al. H. pylori escape host immunoreaction through inhibiting ILK expression by VacA. Cell Mol Immunol. 2009;6:191–197.
11. Salama NR, Hartung ML, Muller A. Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat Rev Microbiol. 2013;11:385–399.
12. Posselt G, Backert S, Wessler S. The functional interplay of Helicobacter pylori factors with gastric epithelial cells induces a multi-step process in pathogenesis. Cell Commun Signal. 2013;11:77.
13. Bridge DR, Merrell DS. Polymorphism in the Helicobacter pylori CagA and VacA toxins and disease. Gut Microbes. 2013;4:101–117.
14. Jones KR, Whitmire JM, Merrell DS. A Tale of Two Toxins: Helicobacter Pylori CagA and VacA modulate host pathways that impact disease. Front Microbiol. 2010;1:115.
15. Censini S, Lange C, Xiang Z, et al. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA. 1996;93:14648–14653.
16. Odenbreit S, Puls J, Sedlmaier B, Gerland E, Fischer W, Haas R. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science. 2000;287:1497–1500.
17. Backert S, Tegtmeyer N, Selbach M. The versatility of Helicobacter pylori CagA effector protein functions: the master key hypothesis. Helicobacter. 2010;15:163–176.
18. McCracken KW, Cata EM, Crawford CM, et al. Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature. 2014;516:5.
19. Rassow J. Helicobacter pylori vacuolating toxin A and apoptosis. Cell Commun Signal. 2011;9:26.
20. Blaser MJ, Atherton JC. Helicobacter pylori persistence: biology and disease. J Clin Invest. 2004;113:321–333.
21. Katsuyama M, Matsuno K, Yabe-Nishimura C. Physiological roles of NOX/NADPH oxidase, the superoxide-generating enzyme. J Clin Biochem Nutr. 2012;50:9–22.
22. Rada B, Leto TL. Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib Microbiol. 2008;15:164–187.
23. Szanto I, Rubbia-Brandt L, Kiss P, et al. Expression of NOX1, a superoxide-generating NADPH oxidase, in colon cancer and inflammatory bowel disease. J Pathol. 2005;207:164–176.
24. Esworthy RS, Kim BW, Chow J, Shen B, Doroshow JH, Chu FF. Nox1 causes ileocolitis in mice deficient in glutathione peroxidase-1 and -2. Free Radic Biol Med. 2014;68:315–325.
25. Teshima S, Rokutan K, Nikawa T, Kishi K. Guinea pig gastric mucosal cells produce abundant superoxide anion through an NADPH oxidase-like system. Gastroenterology. 1998;115:1186–1196.
26. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245–313.
27. Salles N, Szanto I, Herrmann F, et al. Expression of mRNA for ROS-generating NADPH oxidases in the aging stomach. Exp Gerontol. 2005;40:353–357.
28. Ameziane-El-Hassani R, Morand S, Boucher JL, et al. Dual oxidase-2 has an intrinsic Ca2 + -dependent H2O2-generating activity. J Biol Chem. 2005;280:30046–30054.
29. El Hassani RA, Benfares N, Caillou B, et al. Dual oxidase2 is expressed all along the digestive tract. Am J Physiol Gastrointest Liver Physiol. 2005;288:G933–G942.
30. Bae YS, Choi MK, Lee WJ. Dual oxidase in mucosal immunity and host-microbe homeostasis. Trends Immunol. 2010;31:278–287.
31. Allaoui A, Botteaux A, Dumont JE, Hoste C, De Deken X. Dual oxidases and hydrogen peroxide in a complex dialogue between host mucosae and bacteria. Trends Mol Med. 2009;15:571–579.
32. Moskwa P, Lorentzen D, Excoffon KJ, et al. A novel host defense system of airways is defective in cystic fibrosis. Am J Respir Crit Care Med. 2007;175:174–183.
33. Geiszt M, Witta J, Baffi J, Lekstrom K, Leto TL. Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J. 2003;17:1502–1504.
34. Kim BW, Esworthy RS, Hahn MA, Pfeifer GP, Chu FF. Expression of lactoperoxidase in differentiated mouse colon epithelial cells. Free Radic Biol Med. 2012;52:1569–1576.
35. MacFie TS, Poulsom R, Parker A, et al. DUOX2 and DUOXA2 form the predominant enzyme system capable of producing the reactive oxygen species H2O2 in active ulcerative colitis and are modulated by 5-aminosalicylic acid. Inflamm Bowel Dis. 2014;20:514–524.
36. Lipinski S, Till A, Sina C, et al. DUOX2-derived reactive oxygen species are effectors of NOD2-mediated antibacterial responses. J Cell Sci. 2009;122:3522–3530.
37. Csillag C, Nielsen OH, Vainer B, et al. Expression of the genes dual oxidase 2, lipocalin 2 and regenerating islet-derived 1 alpha in Crohn’s disease. Scand J Gastroenterol. 2007;42:454–463.
38. Hornsby MJ, Huff JL, Kays RJ, Canfield DR, Bevins CL, Solnick JV. Helicobacter pylori induces an antimicrobial response in rhesus macaques in a cag pathogenicity island-dependent manner. Gastroenterology. 2008;134:1049–1057.
39. Esworthy RS, Kim BW, Wang Y, et al. The Gdac1 locus modifies spontaneous and Salmonella-induced colitis in mice deficient in either Gpx2 or Gpx1 gene. Free Radic Biol Med. 2013;65:1273–1283.
40. Grasberger H, El-Zaatari M, Dang DT, Merchant JL. Dual oxidases control release of hydrogen peroxide by the gastric epithelium to prevent Helicobacter felis infection and inflammation in mice. Gastroenterology. 2013;145:1045–1054.
41. Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney system. International workshop on the histopathology of gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161–1181.
42. Fang JYLW, Li ZS, Du YQ, et al. Consensus on chronic gastritis in China-third national consensus meeting on chronic gastritis, (2012 Shanghai, China). Chin J Dig Dis. 2013;2013:11.
43. Koh H, Noh TW, Baek SY, Chung KS. Nodular gastritis and pathologic findings in children and young adults with Helicobacter pylori infection. Yonsei Med J. 2007;48:240–246.
44. Gao Q, Meijer MJ, Kubben FJ, et al. Expression of matrix metalloproteinases-2 and -9 in intestinal tissue of patients with inflammatory bowel diseases. Dig Liver Dis. 2005;37:584–592.
45. Untergasser A, Cutcutache I, Koressaar T, et al. Primer3–new capabilities and interfaces. Nucleic Acids Res. 2012;40:e115.
46. Singh K, Ghoshal UC. Causal role of Helicobacter pylori infection in gastric cancer: an Asian enigma. World J Gastroenterol. 2006;12:1346–1351.
47. Limburg P, Qiao Y, Mark S, et al. Helicobacter pylori seropositivity and subsite-specific gastric cancer risks in Linxian, China. J Natl Cancer Inst. 2001;93:226–233.
48. Cadamuro AC, Rossi AF, Maniezzo NM, Silva AE. Helicobacter pylori infection: host immune response, implications on gene expression and microRNAs. World J Gastroenterol. 2014;20:1424–1437.
49. Leoni G, Alam A, Neumann PA, et al. Annexin A1, formyl peptide receptor, and NOX1 orchestrate epithelial repair. J Clin Invest. 2013;123:443–454.
50. Wilson KT, Crabtree JE. Immunology of Helicobacter pylori: insights into the failure of the immune response and perspectives on vaccine studies. Gastroenterology. 2007;133:288–308.
51. Ding SZ, Minohara Y, Fan XJ, et al. Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun. 2007;75:4030–4039.
52. Fritz EL, Slavik T, Delport W, Olivier B, van der Merwe SW. Incidence of Helicobacter felis and the effect of coinfection with Helicobacter pylori on the gastric mucosa in the African population. J Clin Microbiol. 2006;44:1692–1696.
53. Zhang Q, Dawodu JB, Etolhi G, Husain A, Gemmell CG, Russell RI. Relationship between the mucosal production of reactive oxygen radicals and density of Helicobacter pylori in patients with duodenal ulcer. Eur J Gastroenterol Hepatol. 1997;9:261–265.
54. Davies GR, Simmonds NJ, Stevens TR, et al. Helicobacter pylori stimulates antral mucosal reactive oxygen metabolite production in vivo. Gut. 1994;35:179–185.
55. Rokutan K, Kawahara T, Kuwano Y, Tominaga K, Nishida K, Teshima-Kondo S. Nox enzymes and oxidative stress in the immunopathology of the gastrointestinal tract. Semin Immunopathol. 2008;30:315–327.
56. Keenan JI, Peterson RA 2nd, Hampton MB. NADPH oxidase involvement in the pathology of Helicobacter pylori infection. Free Radic Biol Med. 2005;38:1188–1196.
57. Wang G, Alamuri P, Maier RJ. The diverse antioxidant systems of Helicobacter pylori. Mol Microbiol. 2006;61:847–860.
58. Bryk R, Griffin P, Nathan C. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature. 2000;407:211–215.
59. Allen LA, Beecher BR, Lynch JT, Rohner OV, Wittine LM. Helicobacter pylori disrupts NADPH oxidase targeting in human neutrophils to induce extracellular superoxide release. J Immunol. 2005;174:3658–3667.
60. Satin B, Del Giudice G, Della Bianca V, et al. The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a protective antigen and a major virulence factor. J Exp Med. 2000;191:1467–1476.
61. Sheshachalam A, Srivastava N, Mitchell T, Lacy P, Eitzen G. Granule protein processing and regulated secretion in neutrophils. Front Immunol. 2014;5:448.
62. Kruger P, Saffarzadeh M, Weber AN, et al. Neutrophils: between host defence, immune modulation, and tissue injury. PLoS Pathog. 2015;11:e1004651.
63. Tominaga K, Kawahara T, Sano T, et al. Evidence for cancer-associated expression of NADPH oxidase 1 (Nox1)-based oxidase system in the human stomach. Free Radic Biol Med. 2007;43:1627–1638.
64. Augusto AC, Miguel F, Mendonca S, Pedrazzoli J Jr, Gurgueira SA. Oxidative stress expression status associated to Helicobacter pylori virulence in gastric diseases. Clin Biochem. 2007;40:615–622.