Coinfection with enterohepatic helicobacter species can aeliorate or promote helicobacter pylori-induced gastric pathology in C57BL/6 Mice

Infection and Immunity

Volumn 79, Issue 10, 2011, Pages 3861-3871

  Ge, Zhongming ^a   Feng, Yan ^a   Muthupalani, Sureshkumar ^a   Eurell, Laura Lemke ^a,c   Taylor, Nancy S ^a   Whary, Mark T ^a   Fox, James G ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 1BETA; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; FEMALE; GASTROINTESTINAL INFECTION; HELICOBACTER HEPATICUS INFECTION; HELICOBACTER INFECTION; HELICOBACTER MURIDARUM INFECTION; HISTOPATHOLOGIC ACTIVITY INDEX; HISTOPATHOLOGY; MIXED INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH17 CELL;

ANIMALS; CYTOKINES; DOWN-REGULATION; FEMALE; GASTRIC MUCOSA; GASTRITIS; HELICOBACTER; HELICOBACTER HEPATICUS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; MICE; MICE, INBRED C57BL; SEVERITY OF ILLNESS INDEX; STOMACH; TH1 CELLS; TH17 CELLS;

EID: 80855141281     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05357-11     Document Type: Article

References (52)

1. Alm, R. A., et al. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
2. Amieva, M. R., and E. M. El-Omar. 2008. Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134:306-323.
3. Anonymous. 1994. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. IARC Monogr. Eval. Carcinog. Risks Hum. 61:1-241.
4. Bravo, L. E., L. J. van Doom, J. L. Realpe, and P. Correa. 2002. Virulenceassociated genotypes of Helicobacter pylori: do they explain the African enigma? Am. J. Gastroenterol. 97:2839-2842.
5. Chaouche-Drider, N., et al. 2009. A commensal Helicobacter sp. of the rodent intestinal flora activates TLR2 and NOD1 responses in epithelial cells. PLoS One 4:e5396.
6. Cheung, T. K., and B. C. Wong. 2008. Treatment of Helicobacter pylori and prevention of gastric cancer. J. Dig. Dis. 9:8-13.
7. Crabtree, J. E., et al. 2004. Gastric mucosal cytokine and epithelial cell responses to Helicobacter pylori infection in Mongolian gerbils. J. Pathol. 202:197-207.
8. Curotto de Lafaille, M. A., and J. J. Lafaille. 2009. Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 30:626-635.
9. 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.
10. Fontenot, J. D., M. A. Gavin, and A. Y. Rudensky. 2003. Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells. Nat. Immunol. 4:330-336.
11. Fox, J. G., et al. 2000. Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nat. Med. 6:536-542.
12. Fox, J. G., Z. Ge, M. T. Whary, S. E. Erdman, and B. H. Horwitz. 2011. Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer. Mucosal Immunol. 4:22-30.
13. -/- C57BL6 × Sv129 Helicobacter pylori-infected mice. Am. J. Pathol. 171:1520-1528.
14. Fox, J. G., and T. C. Wang. 2007. Inflammation, atrophy, and gastric cancer. J. Clin. Invest. 117:60-69.
15. Fox, J. G., et al. 2003. Host and microbial constituents influence Helicobacter pylori-induced cancer in a murine model of hypergastrinemia. Gastroenterology 124:1879-1890.
16. Ge, Z., D. A. White, M. T. Whary, and J. G. Fox. 2001. Fluorogenic PCRbased quantitative detection of a murine pathogen, Helicobacter hepaticus. J. Clin. Microbiol. 39:2598-2602.
17. Haggerty, T. D., S. Perry, L. Sanchez, G. Perez-Perez, and J. Parsonnet. 2005. Significance of transiently positive enzyme-linked immunosobent assay results in detection Helicobacter pylori in stool samples from children. J. Clin. Microbiol. 43:2220-2223.
18. Harrington, L. E., et al. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6:1123-1132.
19. Harris, P. R., et al. 2008. Helicobacter pylori gastritis in children is associated with a regulatory T-cell response. Gastroenterology 134:491-499.
20. Higgins, P. D., L. A. Johnson, J. Luther, M. Zhang, and J. Y. Kao. 2011. Prior Helicobacter pylori infection ameliorates Salmonella typhimurium-induced colitis: mucosal crosstalk between stomach and distal intestine. Inflamm. Bowel Dis. 17:1398-1408.
21. Hooper, L. V., and J. I. Gordon. 2001. Commensal host-bacterial relationships in the gut. Science 292:1115-1118.
22. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057-1061.
23. Jiang, H., and L. Chess. 2004. An integrated view of suppressor T cell subsets in immunoregulation. J. Clin. Invest. 114:1198-1208.
24. Jiang, H. Q., N. Kushnir, M. C. Thurnheer, N. A. Bos, and J. J. Cebra. 2002. Monoassociation of SCID mice with Helicobacter muridarum, but not four other enterics, provokes IBD upon receipt of T cells. Gastroenterology 122:1346-1354.
25. Kao, J. et al. 2010. Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice. Gastroenterology 138:1046-1054.
26. Lee, A., et al. 1993. Long term infection of the gastric mucosa with Helicobacter species does induce atrophic gastritis in an animal model of Helicobacter pylori infection. Zentralbl. Bakteriol. 280:38-50.
27. -/- mice, but only wild-type regulatory T cells suppress Helicobacter pylori gastritis. Infect. Immun. 75:2699-2707.
28. Lemke, L. B., et al. 2009. Concurrent Helicobacter bilis infection in C57BL/6 mice attenuates proinflammatory H. pylori-induced gastric pathology. Infect. Immun. 77:2147-2158.
29. Lundgren, A., E. Suri-Payer, K. Enarsson, A. M. Svennerholm, and B. S. Lundin. 2003. Helicobacter pylori-specific CD4+ CD25high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals. Infect. Immun. 71:1755-1762.
30. Luzza, F., et al. 2000. Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa. J. Immunol. 165:5332-5337.
31. Maizels, R. M., and M. Yazdanbakhsh. 2003. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3:733-744.
32. Maurer, K. J., et al. 2006. Helicobacter pylori and cholesterol gallstone formation in C57L/J. mice: a prospective study. Am. J. Physiol. Gastrointest. Liver Physiol. 290:G175-G182.
33. Mazmanian, S. K., J. L. Round, and D. L. Kasper. 2008. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453:620-625.
34. McBee, M. E., P. Z. Zheng, A. B. Rogers, J. G. Fox, and D. B. Schauer. 2008. Modulation of acute diarrheal illness by persistent bacterial infection. Infect. Immun. 76:4851-4858.
35. Peterson, R. A., T. Hoepf, and K. A. Eaton. 2003. Adoptive transfer of splenocytes in SCID mice implicates CD4+ T cells in apoptosis and epithelial proliferation associated with Helicobacter pylori-induced gastritis. Comp. Med. 53:498-509.
36. Rad, R., et al. 2006. CD25+/Foxp3+ T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo. Gastroenterology 131:525-537.
37. Raghavan, S., E. Suri-Payer, and J. Holmgren. 2004. Antigen-specific in vitro suppression of murine Helicobacter pylori-reactive immunopathological T cells by CD4CD25 regulatory T cells. Scand. J. Immunol. 60:82-88.
38. Min/+ mice. Cancer Res. 66:57-61.
39. Rogers, A. B., et al. 2005. Helicobacter pylori but not high salt induces gastric intraepithelial neoplasia in B6129 mice. Cancer Res. 65:10709-10715.
40. Sayi, A., et al. 2009. The CD4+ T cell-mediated IFN-gamma response to Helicobacter infection is essential for clearance and determines gastric cancer risk. J. Immunol. 182:7085-7101.
41. Shi, Y., 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.
42. Shiomi, S., et al. 2008. IL-17 is involved in Helicobacter pylori-induced gastric inflammatory responses in a mouse model. Helicobacter 13:518-524.
43. Solnick, J. V., and D. B. Schauer. 2001. Emergence of diverse Helicobacter species in the pathogenesis of gastric and enterohepatic diseases. Clin. Microbiol. Rev. 14:59-97.
44. Stoicov, C., et al. 2004. Coinfection modulates inflammatory responses and clinical outcome of Helicobacter felis and Toxoplasma gondii infections. J. Immunol. 173:3329-3336.
45. Suerbaum, S., et al. 2003. The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc. Natl. Acad. Sci. U. S. A. 100:7901-7906.
46. Sugimoto, M., T. Ohno, D. Y. Graham, and Y. Yamaoka. 2009. Gastric mucosal interleukin-17 and -18 mRNA expression in Helicobacter pyloriinduced Mongolian gerbils. Cancer Sci. 100:2152-2159.
47. Tomb, J. F., et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
48. Welsh, R. M., and R. S. Fujinami. 2007. Pathogenic epitopes, heterologous immunity and vaccine design. Nat. Rev. Microbiol. 5:555-563.
49. Whary, M. T., et al. 2001. Long-term colonization levels of Helicobacter hepaticus in the cecum of hepatitis-prone A/JCr mice are significantly lower than those in hepatitis-resistant C57BL/6 mice. Comp. Med. 51:413-417.
50. Whary, M. T., et al. 2005. Intestinal helminthiasis in Colombian children promotes a Th2 response to Helicobacter pylori: possible implications for gastric carcinogenesis. Cancer Epidemiol. Biomarkers Prev. 14:1464-1469.
51. -/-) mice. Immunology 133:165-178.
52. Wiedemann, T., et al. 2009. Helicobacter pylori cag-pathogenicity islanddependent early immunological response triggers later precancerous gastric changes in Mongolian gerbils. PLoS One 4:e4754.