Altered gut microbiota promotes colitis-associated cancer in IL-1 receptor-associated kinase m-deficient mice

Inflammatory Bowel Diseases

Volumn 19, Issue 6, 2013, Pages 1266-1277

  Klimesova, Klara ^a   Kverka, Miloslav ^a   Zakostelska, Zuzana ^a   Hudcovic, Tomas ^a   Hrncir, Tomas ^a   Stepankova, Renata ^a   Rossmann, Pavel ^a   Ridl, Jakub ^b   Kostovcik, Martin ^a   Mrazek, Jakub ^c   Kopecny, Jan ^c   Kobayashi, Koichi S ^d,e   Tlaskalova Hogenova, Helena ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^c INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cancer in IBD; Colorectal cancer; Germ free; Microbiota; Mucosal immunity

Indexed keywords

AZOXYMETHANE; BETA GLUCURONIDASE; DEXTRAN SULFATE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; COLITIS; COLON CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; INTESTINE FLORA; MALE; MICROFLORA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYROSEQUENCING; WILD TYPE;

ANIMALS; AZOXYMETHANE; BLOTTING, WESTERN; CARCINOGENS; COLITIS; COLONIC NEOPLASMS; CYTOKINES; DEXTRAN SULFATE; FEMALE; FLOW CYTOMETRY; GASTROINTESTINAL TRACT; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; MALE; METAGENOME; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERLEUKIN-1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTORS;

EID: 84879232630     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0b013e318281330a     Document Type: Article

References (44)

1. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol. 2004;287:G7-17.
2. Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut. 2001;48:526-535.
3. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134:577-594.
4. Tlaskalova-Hogenova H, Stepankova R, Kozakova H, et al. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol. 2011;8:110-120.
5. Arthur JC, Jobin C. The struggle within: microbial influences on colorec-tal cancer. Inflamm Bowel Dis. 2011;17:396-409.
6. Tannock GW. The bowel microbiota and inflammatory bowel diseases. Int J Inflam. 2010;2010:954051.
7. Parsonnet J. Helicobacter pylori and gastric cancer. Gastroenterol Clin North Am. 1993;22:89-104.
8. Gionchetti P, Rizzello F, Lammers KM, et al. Antibiotics and probiotics in treatment of inflammatory bowel disease. World J Gastroenterol. 2006; 12:3306-3313.
9. Thangaraju M, Cresci GA, Liu K, et al. GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res. 2009;69:2826-2832.
10. Barc MC, Charrin-Sarnel C, Rochet V, et al. Molecular analysis of the digestive microbiota in a gnotobiotic mouse model during antibiotic treatment: influence of Saccharomyces boulardii. Anaerobe. 2008;14: 229-233.
11. Azcarate-Peril MA, Sikes M, Bruno-Barcena JM. The intestinal micro-biota, gastrointestinal environment and colorectal cancer: a putative role for probiotics in prevention of colorectal cancer? Am J Physiol Gastrointest Liver Physiol. 2011;301:G401-G424.
12. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34:637-650.
13. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol. 2010; 10:131-144.
14. Fukata M, Abreu MT. TLR4 signalling in the intestine in health and disease. Biochem Soc Trans. 2007;35:1473-1478.
15. Salcedo R, Worschech A, Cardone M, et al. MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J Exp Med. 2010;207:1625-1636.
16. Hubbard LL, Moore BB. IRAK-M regulation and function in host defense and immune homeostasis. Infect Dis Rep. 2010;2:e9.
17. Kobayashi K, Hernandez LD, Galan JE, et al. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell. 2002;110:191-202.
18. Biswas A, Wilmanski J, Forsman H, et al. Negative regulation of Toll-like receptor signaling plays an essential role in homeostasis of the intestine. Eur J Immunol. 2011;41:182-194.
19. Berglund M, Melgar S, Kobayashi KS, et al. IL-1 receptor-associated kinase M downregulates DSS-induced colitis. Inflamm Bowel Dis. 2010; 16:1778-1786.
20. Xiao H, Gulen MF, Qin J, et al. The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity. 2007;26:461-475.
21. Vannucci L, Stepankova R, Kozakova H, et al. Colorectal carcinogenesis in germ-free and conventionally reared rats: different intestinal environments affect the systemic immunity. Int J Oncol. 2008;32:609-617.
22. Stepankova R, Powrie F, Kofronova O, et al. Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RBhigh CD4+ T cells. Inflamm Bowel Dis. 2007;13:1202-1211.
23. Clapper ML, Cooper HS, Chang WC. Dextran sulfate sodium-induced colitis-associated neoplasia: a promising model for the development of chemopreventive interventions. Acta Pharmacol Sin. 2007;28:1450-1459.
24. Kverka M, Zakostelska Z, Klimesova K, et al. Oral administration of Parabacteroides distasonis antigens attenuates experimental murine colitis through modulation of immunity and microbiota composition. Clin Exp Immunol. 2011;163:250-259.
25. Zakostelska Z, Kverka M, Klimesova K, et al. Lysate of probiotic lacto-bacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS One. 2011; 6:e27961.
26. Shen XJ, Rawls JF, Randall T, et al. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes. 2010;1:138-147.
27. Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008; 105:16731-16736.
28. Fiala E. Investigations into the metabolism and mode of action of the colon carcinogen 1, 2-dimethylhydrazine. Cancer. 1975;36:2407-2412.
29. Chen W, Perruche S, Li J. CD4+CD25+ T regulatory cells and TGF-beta in mucosal immune system: the good and the bad. Curr Med Chem. 2007; 14:2245-2249.
30. Nishikawa H, Sakaguchi S. Regulatory T cells in tumor immunity. Int J Cancer. 2010;127:759-767.
31. Murai M, Krause P, Cheroutre H, et al. Regulatory T-cell stability and plasticity in mucosal and systemic immune systems. Mucosal Immunol. 2010;3:443-449.
32. Asquith M, Powrie F. An innately dangerous balancing act: intestinal homeostasis, inflammation, and colitis-associated cancer. J Exp Med. 2010;207:1573-1577.
33. Balaci L, Spada MC, Olla N, et al. IRAK-M is involved in the pathogenesis of early-onset persistent asthma. Am J Hum Genet. 2007;80:1103-1114.
34. Xie Q, Gan L, Wang J, et al. Loss of the innate immunity negative regulator IRAK-M leads to enhanced host immune defense against tumor growth. Mol Immunol. 2007;44:3453-3461.
35. Standiford TJ, Kuick R, Bhan U, et al. TGF-beta-induced IRAK-M expression in tumor-associated macrophages regulates lung tumor growth. Oncogene. 2011;30:2475-2484.
36. Dethlefsen L, Huse S, Sogin ML, et al. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008;6:e280.
37. Hamer HM, De Preter V, Windey K, et al. Review article: Functional analysis of colonic bacterial metabolism: relevant to health? Am J Physiol Gastrointest Liver Physiol. 2011.
38. Venturi M, Hambly RJ, Glinghammar B, et al. Genotoxic activity in human faecal water and the role of bile acids: a study using the alkaline comet assay. Carcinogenesis. 1997;18:2353-2359.
39. Bernstein C, Holubec H, Bhattacharyya AK, et al. Carcinogenicity of deoxycholate, a secondary bile acid. Arch Toxicol. 2011;85:863-871.
40. Rod TO, Midtvedt T. Origin of intestinal beta-glucuronidase in germfree, monocontaminated and conventional rats. Acta Pathol Microbiol Scand B. 1977;85:271-276.
41. Vannucci L, Stepankova R, Grobarova V, et al. Colorectal carcinoma: importance of colonic environment for anti-cancer response and systemic immunity. J Immunotoxicol. 2009;6:217-226.
42. Hrncir T, Stepankova R, Kozakova H, et al. Gut microbiota and lipopoly-saccharide content of the diet influence development of regulatory T cells: studies in germ-free mice. BMC Immunol. 2008;9:65.
43. Bartosch S, Fite A, Macfarlane GT, et al. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol. 2004;70:3575-3581.
44. Kreader CA. Design and evaluation of Bacteroides DNA probes for the specific detection of human fecal pollution. Appl Environ Microbiol. 1995;61:1171-1179.