Gastric colonisation with a restricted commensal microbiota replicates the promotion of neoplastic lesions by diverse intestinal microbiota in the Helicobacter pylori INS-GAS mouse model of gastric carcinogenesis

Gut

Volumn 63, Issue 1, 2014, Pages 54-63

  Lertpiriyapong, Kvin ^a   Whary, Mark T ^a   Muthupalani, Sureshkumar ^a   Lofgren, Jennifer L ^a   Gamazon, Eric R ^b   Feng, Yan ^a   Ge, Zhongming ^a   Wang, Timothy C ^c   Fox, James G ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 11; MESSENGER RNA; PROSTAGLANDIN E RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIUM IDENTIFICATION; CANCER GROWTH; CARCINOGENESIS; COMMENSAL; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; FEMALE; GASTROINTESTINAL INTRAEPITHELIAL NEOPLASIA; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GROWTH RATE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; IMMUNE RESPONSE; INTESTINE FLORA; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRECANCER AND CANCER-IN-SITU; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PTGER4 GENE; SEX DIFFERENCE; STOMACH CANCER; TGF BETA GENE; TUMOR INVASION;

GASTRIC ADENOCARCINOMA; GASTRIC INFLAMMATION; HELICOBACTER PYLORI - GASTRITIS; INTESTINAL BACTERIA;

ADENOCARCINOMA; ANIMALS; BACTEROIDES; BIOLOGICAL MARKERS; CARCINOGENESIS; CLOSTRIDIUM; CYTOKINES; FEMALE; GASTRIC MUCOSA; GASTRITIS, ATROPHIC; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; INTESTINE, LARGE; LACTOBACILLUS; MALE; MICE; SPECIFIC PATHOGEN-FREE ORGANISMS; STOMACH NEOPLASMS; SYMBIOSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84889663851     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2013-305178     Document Type: Article

References (48)

1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process - First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992;52:6735-40. (Pubitemid 23006271)
3. Fox JG, Wang TC. Inflammation, atrophy, and gastric cancer. J Clin Invest 2007;117:60-9. (Pubitemid 46048450)
4. Peek RM Jr, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2002;2:28-37. (Pubitemid 37328805)
5. Krejs GJ. Gastric cancer: epidemiology and risk factors. Digest Dis 2010;28:600-3.
6. Nagini S. Carcinoma of the stomach: a review of epidemiology, pathogenesis, molecular genetics and chemoprevention. World J Gastrointest Oncol 2012;4:156-69.
7. Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010;23:713-39.
8. Smith MG, Hold GL, Tahara E, et al. Cellular and molecular aspects of gastric cancer. World J Gastroenterol 2006;12:2979-90. (Pubitemid 43811073)
9. Wu MS, Chen CJ, Lin JT. Host-environment interactions: their impact on progression from gastric inflammation to carcinogenesis and on development of new approaches to prevent and treat gastric cancer. Cancer Epidemiol Biomarkers Prev 2005;14:1878-82.
10. Fox JG, Wang TC, Rogers AB, et al. Host and microbial constituents influence Helicobacter pylori-induced cancer in a murine model of hypergastrinemia. Gastroenterology 2003;124:1879-90. (Pubitemid 36666783)
11. Toller IM, Neelsen KJ, Steger M, et al. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci USA 2011;108:14944-9.
12. Wang M, Zhang R, He J, et al. Potentially Functional Variants of PLCE1 Identified by GWASs Contribute to Gastric Adenocarcinoma Susceptibility in an Eastern Chinese Population. PLoS ONE 2012;7:e31932.
13. Shi Y, Hu Z, Wu C, et al. A genome-wide association study identifies new susceptibility loci for non-cardia gastric cancer at 3q13.31 and 5p13.1. Nat Genet 2011;43:1215-8.
14. Whary MT, Sundina N, Bravo LE, et al. Intestinal helminthiasis in Colombian children promotes a Th2 response to Helicobacter pylori: possible implications for gastric carcinogenesis. Cancer Epidemiol Biomarkers Prev 2005;14:1464-9. (Pubitemid 40807347)
15. Stearns JC, Lynch MD, Senadheera DB, et al. Bacterial biogeography of the human digestive tract. Sci Rep 2011;1:170.
16. Maldonado-Contreras A, Goldfarb KC, Godoy-Vitorino F, et al. Structure of the human gastric bacterial community in relation to Helicobacter pylori status. ISME J 2011;5:574-9.
17. Roos S, Engstrand L, Jonsson H. Lactobacillus gastricus sp. nov., Lactobacillus antri sp. nov., Lactobacillus kalixensis sp. nov. and Lactobacillus ultunensis sp. nov., isolated from human stomach mucosa. Int J Syst Evol Microbiol 2005;55:77-82. (Pubitemid 40185477)
18. Ryan KA, Jayaraman T, Daly P, et al. Isolation of lactobacilli with probiotic properties from the human stomach. Lett Appl Microbiol 2008;47:269-74.
19. Sanduleanu S, Jonkers D, De Bruine A, et al. Non-Helicobacter pylori bacterial flora during acid-suppressive therapy: differential findings in gastric juice and gastric mucosa. Aliment Pharmacol Ther 2001;15:379-88. (Pubitemid 32187560)
20. Mowat C, Williams C, Gillen D, et al. Omeprazole, Helicobacter pylori status, and alterations in the intragastric milieu facilitating bacterial N-nitrosation. Gastroenterology 2000;119:339-47. (Pubitemid 30621984)
21. Fox JG, Kuipers EJ. Long-term proton pump inhibitor administration, H. pylori and gastric cancer: lessons from the gerbil. Gut 2011;60:567-8.
22. Dicksved J, Lindberg M, Rosenquist M, et al. Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J Med Microbiol 2009;58:509-16.
23. Zavros Y, Rieder G, Ferguson A, et al. Gastritis and hypergastrinemia due to Acinetobacter lwoffii in mice. Infect Immun 2002;70:2630-9. (Pubitemid 34408409)
24. Lofgren JL, Whary MT, Ge Z, et al. Lack of commensal flora in Helicobacter pylori-infected INS-GAS mice reduces gastritis and delays intraepithelial neoplasia. Gastroenterology 2011;140:210-20.
25. Lee CW, Rickman B, Rogers AB, et al. Combination of sulindac and antimicrobial eradication of Helicobacter pylori prevents progression of gastric cancer in hypergastrinemic INS-GAS mice. Cancer Res 2009;69:8166-74.
26. Oshima H, Hioki K, Popivanova BK, et al. Prostaglandin E signaling and bacterial infection recruit tumor-promoting macrophages to mouse gastric tumors. Gastroenterology 2011;140:596-607 e7.
27. Dewhirst FE, Chien CC, Paster BJ, et al. Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl Environ Microbiol 1999;65:3287-92. (Pubitemid 29398945)
28. Sarma-Rupavtarm RB, Ge Z, Schauer DB, et al. Spatial distribution and stability of the eight microbial species of the altered Schaedler flora in the mouse gastrointestinal tract. Appl Environ Microbiol 2004;70:2791-800. (Pubitemid 38657794)
29. Fox JG, Rogers AB, Ihrig M, et al. Helicobacter pylori-associated gastric cancer in INS-GAS mice is gender specific. Cancer Res 2003;63:942-50. (Pubitemid 36278423)
30. Howlett M, Chalinor HV, Buzzelli JN, et al. IL-11 is a parietal cell cytokine that induces atrophic gastritis. Gut 2012;61:1398-409.
31. Ge Z, Feng Y, Taylor NS, et al. Colonization dynamics of altered Schaedler flora is influenced by gender, aging, and Helicobacter hepaticus infection in the intestines of Swiss Webster mice. Appl Environ Microbiol 2006;72:5100-3. (Pubitemid 44078848)
32. Zang ZJ, Cutcutache I, Poon SL, et al. Exome sequencing of gastric adenocarcinoma identifies recurrent somatic mutations in cell adhesion and chromatin remodeling genes. Nat Genet 2012.
33. Achyut BR, Yang L. Transforming growth factor-beta in the gastrointestinal and hepatic tumor microenvironment. Gastroenterology 2011;141:1167-78.
34. Chandanos E, Lagergren J. Oestrogen and the enigmatic male predominance of gastric cancer. Eur J Cancer 2008;44:2397-403.
35. Wang TC, Dangler CA, Chen D, et al. Synergistic interaction between hypergastrinemia and Helicobacter infection in a mouse model of gastric cancer. Gastroenterology 2000;118:36-47. (Pubitemid 30020371)
36. Kokkola A, Kosunen TU, Puolakkainen P, et al. Spontaneous disappearance of Helicobacter pylori antibodies in patients with advanced atrophic corpus gastritis. APMIS 2003;111:619-24. (Pubitemid 37130032)
37. Bik EM, Eckburg PB, Gill SR, et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA 2006;103:732-7. (Pubitemid 43153094)
38. Markle JG, Frank DN, Mortin-Toth S, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013;339:1084-8.
39. Sheh A, Ge Z, Parry NM, et al. 17 beta-estradiol and tamoxifen prevent gastric cancer by modulating leukocyte recruitment and oncogenic pathways in Helicobacter pylori-infected INS-GAS male mice. Cancer Prev Res (Phila) 2011;4:1426-35.
40. Ohtani M, Garcia A, Rogers AB, et al. Protective role of 17 beta-estradiol against the development of Helicobacter pylori-induced gastric cancer in INS-GAS mice. Carcinogenesis 2007;28:2597-604. (Pubitemid 350238963)
41. Schmitz JM, Durham CG, Schoeb TR, et al. Helicobacter felis-Associated Gastric Disease in Microbiota-Restricted Mice. J Histochem Cytochem 2011;59:826-41.
42. Rolig AS, Cech C, Ahler E, et al. The degree of Helicobacter pylori-triggered inflammation is manipulated by preinfection host microbiota. Infect Immun 2013;81:1382-9.
43. Valle J, Kekki M, Sipponen P, et al. Long-term course and consequences of Helicobacter pylori gastritis. Results of a 32-year follow-up study. Scand J Gastroenterol 1996;31:546-50. (Pubitemid 26196134)
44. Niemela S, Karttunen T, Kerola T. Helicobacter pylori-associated gastritis. Evolution of histologic changes over 10 years. Scand J Gastroenterol 1995;30:542-9.
45. Ziebarth D, Spiegelhalder B, Bartsch H. N-nitrosation of medicinal drugs catalysed by bacteria from human saliva and gastro-intestinal tract, including Helicobacter pylori. Carcinogenesis 1997;18:383-9. (Pubitemid 28132433)
46. Sharma BK, Santana IA, Wood EC, et al. Intragastric bacterial activity and nitrosation before, during, and after treatment with omeprazole. Br Med J (Clin Res Ed) 1984;289:717-9. (Pubitemid 14009890)
47. Reading NC, Kasper DL. The starting lineup: key microbial players in intestinal immunity and homeostasis. Front Microbiol 2011;2:148.
48. Boivin GP, Washington K, Yang K, et al. Pathology of mouse models of intestinal cancer: consensus report and recommendations. Gastroenterology 2003;124:762-77. (Pubitemid 36268493)