Disruption of nitric oxide signaling by Helicobacter pylori results in enhanced inflammation by inhibition of heme oxygenase-1

Journal of Immunology

Volumn 187, Issue 10, 2011, Pages 5370-5379

  Gobert, Alain P ^a,b,c   Asim, Mohammad ^a,b   Piazuelo, M Blanca ^a   Verriere, Thomas ^a   Scull, Brooks P ^a   De Sablet, Thibaut ^a,b   Glumac, Ashley ^a   Lewis, Nuruddeen D ^a,d   Correa, Pelayo ^a   Peek Jr , Richard M ^a,b,d   Chaturvedi, Rupesh ^a,b   Wilson, Keith T ^a,b,d,e  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b DEPARTMENT OF VETERANS AFFAIRS   (United States)

^c CEMAGREF   (France)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAGA PROTEIN; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; JANUS KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; GENE; GENE EXPRESSION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HMOX 1 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STOMACH EPITHELIUM;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE; CELL LINE, TRANSFORMED; GASTRIC MUCOSA; HELICOBACTER PYLORI; HEME OXYGENASE-1; HUMANS; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE; SIGNAL TRANSDUCTION; UP-REGULATION; VIRULENCE FACTORS;

EID: 81455141899     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102111     Document Type: Article

References (59)

1. Peek, R. M., Jr., C. Fiske, and K. T. Wilson. 2010. Role of innate immunity in Helicobacter pylori-induced gastric malignancy. Physiol. Rev. 90: 831-858.
2. Blaser, M. J., G. I. Perez-Perez, H. Kleanthous, T. L. Cover, R. M. Peek, P. H. Chyou, G. N. Stemmermann, and A. Nomura. 1995. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 55: 2111-2115.
3. Ogura, K., S. Maeda, M. Nakao, T. Watanabe, M. Tada, T. Kyutoku, H. Yoshida, Y. Shiratori, and M. Omata. 2000. Virulence factors of Helicobacter pylori responsible for gastric diseases in Mongolian gerbil. J. Exp. Med. 192: 1601-1610.
4. Odenbreit, S., J. Püls, B. Sedlmaier, E. Gerland, W. Fischer, and R. Haas. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287: 1497-1500. (Pubitemid 30127145)
5. Selbach, M., S. Moese, C. R. Hauck, T. F. Meyer, and S. Backert. 2002. Src is the kinase of the Helicobacter pylori CagA protein in vitro and in vivo. J. Biol. Chem. 277: 6775-6778. (Pubitemid 34953058)
6. Backert, S., S. Moese, M. Selbach, V. Brinkmann, and T. F. Meyer. 2001. Phosphorylation of tyrosine 972 of the Helicobacter pylori CagA protein is essential for induction of a scattering phenotype in gastric epithelial cells. Mol. Microbiol. 42: 631-644. (Pubitemid 33064475)
7. Brandt, S., T. Kwok, R. Hartig, W. König, and S. Backert. 2005. NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc. Natl. Acad. Sci. USA 102: 9300-9305. (Pubitemid 40923558)
8. Kim, S. Y., Y. C. Lee, H. K. Kim, and M. J. Blaser. 2006. Helicobacter pylori CagA transfection of gastric epithelial cells induces interleukin-8. Cell. Microbiol. 8: 97-106.
9. Suzuki, M., H. Mimuro, K. Kiga, M. Fukumatsu, N. Ishijima, H. Morikawa, S. Nagai, S. Koyasu, R. H. Gilman, D. Kersulyte, et al. 2009. Helicobacter pylori CagA phosphorylation-independent function in epithelial proliferation and inflammation. Cell Host Microbe 5: 23-34.
10. Oldani, A., M. Cormont, V. Hofman, V. Chiozzi, O. Oregioni, A. Canonici, A. Sciullo, P. Sommi, A. Fabbri, V. Ricci, and P. Boquet. 2009. Helicobacter pylori counteracts the apoptotic action of its VacA toxin by injecting the CagA protein into gastric epithelial cells. PLoS Pathog. 5: e1000603.
11. Schweitzer, K., O. Sokolova, P. M. Bozko, and M. Naumann. 2010. Helicobacter pylori induces NF-kappaB independent of CagA. EMBO Rep. 11: 10-11, author reply 11-12.
12. DeLyria, E. S., R. W. Redline, and T. G. Blanchard. 2009. Vaccination of mice against H pylori induces a strong Th-17 response and immunity that is neutrophil dependent. Gastroenterology 136: 247-256.
13. Shi, Y., X. F. Liu, Y. Zhuang, J. Y. Zhang, T. Liu, Z. Yin, C. Wu, X. H. Mao, K. R. Jia, F. J. Wang, et al. 2010. Helicobacter pylori-induced Th17 responses modulate Th1 cell responses, benefit bacterial growth, and contribute to pathology in mice. J. Immunol. 184: 5121-5129.
14. Bamford, K. B., X. Fan, S. E. Crowe, J. F. Leary, W. K. Gourley, G. K. Luthra, E. G. Brooks, D. Y. Graham, V. E. Reyes, and P. B. Ernst. 1998. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 114: 482-492. (Pubitemid 28141193)
15. Kao, J. Y., M. Zhang, M. J. Miller, J. C. Mills, B. Wang, M. Liu, K. A. Eaton, W. Zou, B. E. Berndt, T. S. Cole, et al. 2010. Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice. Gastroenterology 138: 1046-1054.
16. Chaturvedi, R., M. Asim, N. D. Lewis, H. M. Algood, T. L. Cover, P. Y. Kim, and K. T. Wilson. 2007. L-arginine availability regulates inducible nitric oxide synthase-dependent host defense against Helicobacter pylori. Infect. Immun. 75: 4305-4315. (Pubitemid 47378087)
17. Chaturvedi, R., M. Asim, S. Hoge, N. D. Lewis, K. Singh, D. P. Barry, T. de Sablet, M. B. Piazuelo, A. R. Sarvaria, Y. Cheng, et al. 2010. Polyamines impair immunity to Helicobacter pylori by inhibiting L-arginine uptake required for nitric oxide production. Gastroenterology 139: 1686-1698, 1698, e1-e6.
18. Gobert, A. P., D. J. McGee, M. Akhtar, G. L. Mendz, J. C. Newton, Y. Cheng, H. L. Mobley, and K. T. Wilson. 2001. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc. Natl. Acad. Sci. USA 98: 13844-13849. (Pubitemid 33115986)
19. Lewis, N. D., M. Asim, D. P. Barry, K. Singh, T. de Sablet, J. L. Boucher, A. P. Gobert, R. Chaturvedi, and K. T. Wilson. 2010. Arginase II restricts host defense to Helicobacter pylori by attenuating inducible nitric oxide synthase translation in macrophages. J. Immunol. 184: 2572-2582.
20. Ryter, S. W., J. Alam, and A. M. Choi. 2006. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86: 583-650.
21. Peek, R. M., Jr., M. J. Blaser, D. J. Mays, M. H. Forsyth, T. L. Cover, S. Y. Song, U. Krishna, and J. A. Pietenpol. 1999. Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res. 59: 6124-6131. (Pubitemid 30035632)
22. Franco, A. T., D. A. Israel, M. K. Washington, U. Krishna, J. G. Fox, A. B. Rogers, A. S. Neish, L. Collier-Hyams, G. I. Perez-Perez, M. Hatakeyama, et al. 2005. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc. Natl. Acad. Sci. USA 102: 10646-10651. (Pubitemid 41061608)
23. Arnold, I. C., J. Y. Lee, M. R. Amieva, A. Roers, R. A. Flavell, T. Sparwasser, and A. Müller. 2011. Tolerance rather than immunity protects from Helicobacter pylori-induced gastric preneoplasia. Gastroenterology 140: 199-209.
24. Donahue, J. P., D. A. Israel, R. M. Peek, M. J. Blaser, and G. G. Miller. 2000. Overcoming the restriction barrier to plasmid transformation of Helicobacter pylori. Mol. Microbiol. 37: 1066-1074.
25. Correa, P., E. T. Fontham, J. C. Bravo, L. E. Bravo, B. Ruiz, G. Zarama, J. L. Realpe, G. T. Malcom, D. Li, W. D. Johnson, and R. Mera. 2000. Chemoprevention of gastric dysplasia: randomized trial of antioxidant supplements and anti-helicobacter pylori therapy. J. Natl. Cancer Inst. 92: 1881-1888. (Pubitemid 32036918)
26. Sicinschi, L. A., P. Correa, R. M. Peek, Jr., M. C. Camargo, A. Delgado, M. B. Piazuelo, J. Romero-Gallo, L. E. Bravo, and B. G. Schneider. 2008. Helicobacter pylori genotyping and sequencing using paraffin-embedded biopsies from residents of colombian areas with contrasting gastric cancer risks. Helicobacter 13: 135-145. (Pubitemid 351347657)
27. Chaturvedi, R., M. Asim, J. Romero-Gallo, D. P. Barry, S. Hoge, T. de Sablet, A. G. Delgado, L. E. Wroblewski, M. B. Piazuelo, F. Yan, et al. 2011. Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA. Gastroenterology .
28. Choi, K. M., S. J. Gibbons, T. V. Nguyen, G. J. Stoltz, M. S. Lurken, T. Ordog, J. H. Szurszewski, and G. Farrugia. 2008. Heme oxygenase-1 protects interstitial cells of Cajal from oxidative stress and reverses diabetic gastroparesis. Gastroenterology 135: 2055-2064.
29. Xu, H., R. Chaturvedi, Y. Cheng, F. I. Bussiere, M. Asim, M. D. Yao, D. Potosky, S. J. Meltzer, J. G. Rhee, S. S. Kim, et al. 2004. Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res. 64: 8521-8525. (Pubitemid 39552063)
30. Yan, F., H. Cao, R. Chaturvedi, U. Krishna, S. S. Hobbs, P. J. Dempsey, R. M. Peek, Jr., T. L. Cover, M. K. Washington, K. T. Wilson, and D. B. Polk. 2009. Epidermal growth factor receptor activation protects gastric epithelial cells from Helicobacter pylori-induced apoptosis. Gastroenterology 136: 1297-1307, e1-e3.
31. Vareille, M., F. Rannou, N. Thélier, A. L. Glasser, T. de Sablet, C. Martin, and A. P. Gobert. 2008. Heme oxygenase-1 is a critical regulator of nitric oxide production in enterohemorrhagic Escherichia coli-infected human enterocytes. J. Immunol. 180: 5720-5726.
32. Hong, S. K., R. Chaturvedi, M. B. Piazuelo, L. A. Coburn, C. S. Williams, A. G. Delgado, R. A. Casero, Jr., D. A. Schwartz, and K. T. Wilson. 2010. Increased expression and cellular localization of spermine oxidase in ulcerative colitis and relationship to disease activity. Inflamm. Bowel Dis. 16: 1557-1566.
33. Guettouche, T., F. Boellmann, W. S. Lane, and R. Voellmy. 2005. Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem. 6: 4.
34. Chu, B., F. Soncin, B. D. Price, M. A. Stevenson, and S. K. Calderwood. 1996. Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem. 271: 30847-30857. (Pubitemid 26404108)
35. Algood, H. M., J. Gallo-Romero, K. T. Wilson, R. M. Peek, Jr., and T. L. Cover. 2007. Host response to Helicobacter pylori infection before initiation of the adaptive immune response. FEMS Immunol. Med. Microbiol. 51: 577-586. (Pubitemid 350076170)
36. Barton, S. G., D. S. Rampton, V. R. Winrow, P. Domizio, and R. M. Feakins. 2003. Expression of heat shock protein 32 (hemoxygenase-1) in the normal and inflamed human stomach and colon: an immunohistochemical study. Cell Stress Chaperones 8: 329-334. (Pubitemid 38222879)
37. Necchi, V., M. E. Candusso, F. Tava, O. Luinetti, U. Ventura, R. Fiocca, V. Ricci, and E. Solcia. 2007. Intracellular, intercellular, and stromal invasion of gastric mucosa, preneoplastic lesions, and cancer by Helicobacter pylori. Gastroenterology 132: 1009-1023. (Pubitemid 46440875)
38. Alam, J., and J. L. Cook. 2007. How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am. J. Respir. Cell Mol. Biol. 36: 166-174. (Pubitemid 46233469)
39. Lee, S. K., H. I. Choi, Y. S. Yang, G. S. Jeong, J. H. Hwang, S. I. Lee, K. H. Kang, J. H. Cho, J. M. Chae, S. K. Lee, et al. 2009. Nitric oxide modulates osteoblastic differentiation with heme oxygenase-1 via the mitogen activated protein kinase and nuclear factor-kappaB pathways in human periodontal ligament cells. Biol. Pharm. Bull. 32: 1328-1334.
40. Li, Q., Y. Guo, Q. Ou, C. Cui, W. J. Wu, W. Tan, X. Zhu, L. B. Lanceta, S. K. Sanganalmath, B. Dawn, et al. 2009. Gene transfer of inducible nitric oxide synthase affords cardioprotection by upregulating heme oxygenase-1 via a nuclear factor-kappaB-dependent pathway. Circulation 120: 1222-1230.
41. Liu, Z. M., G. G. Chen, E. K. Ng, W. K. Leung, J. J. Sung, and S. C. Chung. 2004. Upregulation of heme oxygenase-1 and p21 confers resistance to apoptosis in human gastric cancer cells. Oncogene 23: 503-513.
42. Lavrovsky, Y., M. L. Schwartzman, R. D. Levere, A. Kappas, and N. G. Abraham. 1994. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc. Natl. Acad. Sci. USA 91: 5987-5991. (Pubitemid 24188267)
43. Mimuro, H., T. Suzuki, J. Tanaka, M. Asahi, R. Haas, and C. Sasakawa. 2002. Grb2 is a key mediator of helicobacter pylori CagA protein activities. Mol. Cell 10: 745-755. (Pubitemid 35335631)
44. Churin, Y., L. Al-Ghoul, O. Kepp, T. F. Meyer, W. Birchmeier, and M. Naumann. 2003. Helicobacter pylori CagA protein targets the c-Met receptor and enhances the motogenic response. J. Cell Biol. 161: 249-255. (Pubitemid 36529844)
45. Bauer, B., S. Bartfeld, and T. F. Meyer. 2009. H. pylori selectively blocks EGFR endocytosis via the non-receptor kinase c-Abl and CagA. Cell. Microbiol. 11: 156-169.
46. Keates, S., A. C. Keates, K. Katchar, R. M. Peek, Jr., and C. P. Kelly. 2007. Helicobacter pylori induces up-regulation of the epidermal growth factor receptor in AGS gastric epithelial cells. J. Infect. Dis. 196: 95-103. (Pubitemid 46982743)
47. Keates, S., A. C. Keates, M. Warny, R. M. Peek, Jr., P. G. Murray, and C. P. Kelly. 1999. Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cag- Helicobacter pylori. J. Immunol. 163: 5552-5559.
48. Snider, J. L., C. Allison, B. H. Bellaire, R. L. Ferrero, and J. A. Cardelli. 2008. The beta1 integrin activates JNK independent of CagA, and JNK activation is required for Helicobacter pylori CagA+-induced motility of gastric cancer cells. J. Biol. Chem. 283: 13952-13963.
49. Allison, C. C., T. A. Kufer, E. Kremmer, M. Kaparakis, and R. L. Ferrero. 2009. Helicobacter pylori induces MAPK phosphorylation and AP-1 activation via a NOD1-dependent mechanism. J. Immunol. 183: 8099-8109.
50. Nakayama, M., J. Hisatsune, E. Yamasaki, H. Isomoto, H. Kurazono, M. Hatakeyama, T. Azuma, Y. Yamaoka, K. Yahiro, J. Moss, and T. Hirayama. 2009. Helicobacter pylori VacA-induced inhibition of GSK3 through the PI3K/Akt signaling pathway. J. Biol. Chem. 284: 1612-1619.
51. Chou, Y. H., F. M. Ho, D. Z. Liu, S. Y. Lin, L. H. Tsai, C. H. Chen, Y. S. Ho, L. F. Hung, and Y. C. Liang. 2005. The possible role of heat shock factor-1 in the negative regulation of heme oxygenase-1. Int. J. Biochem. Cell Biol. 37: 604-615.
52. Singh, I. S., R. M. Viscardi, I. Kalvakolanu, S. Calderwood, and J. D. Hasday. 2000. Inhibition of tumor necrosis factor-alpha transcription in macrophages exposed to febrile range temperature. A possible role for heat shock factor-1 as a negative transcriptional regulator. J. Biol. Chem. 275: 9841-9848. (Pubitemid 30185220)
53. Song, M., M. R. Pinsky, and J. A. Kellum. 2008. Heat shock factor 1 inhibits nuclear factor-kappaB nuclear binding activity during endotoxin tolerance and heat shock. J. Crit. Care 23: 406-415.
54. Wang, W. P., X. Guo, M. W. Koo, B. C. Wong, S. K. Lam, Y. N. Ye, and C. H. Cho. 2001. Protective role of heme oxygenase-1 on trinitrobenzene sulfonic acid-induced colitis in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 281: G586-G594.
55. Otterbein, L. E., F. H. Bach, J. Alam, M. Soares, H. Tao Lu, M. Wysk, R. J. Davis, R. A. Flavell, and A. M. Choi. 2000. Carbon monoxide has antiinflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6: 422-428. (Pubitemid 30208159)
56. Kapturczak, M. H., C. Wasserfall, T. Brusko, M. Campbell-Thompson, T. M. Ellis, M. A. Atkinson, and A. Agarwal. 2004. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am. J. Pathol. 165: 1045-1053. (Pubitemid 39129309)
57. Pae, H. O., G. S. Oh, B. M. Choi, S. C. Chae, Y. M. Kim, K. R. Chung, and H. T. Chung. 2004. Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of IL-2 production. J. Immunol. 172: 4744-4751.
58. Tzima, S., P. Victoratos, K. Kranidioti, M. Alexiou, and G. Kollias. 2009. Myeloid heme oxygenase-1 regulates innate immunity and autoimmunity by modulating IFN-beta production. J. Exp. Med. 206: 1167-1179.
59. Choi, B. M., H. O. Pae, Y. R. Jeong, Y. M. Kim, and H. T. Chung. 2005. Critical role of heme oxygenase-1 in Foxp3-mediated immune suppression. Biochem. Biophys. Res. Commun. 327: 1066-1071.