A multihit model: Colitis lessons from the interleukin-10-deficient mouse

Inflammatory Bowel Diseases

Volumn 21, Issue 8, 2015, Pages 1967-1975

  Keubler, Lydia M ^a   Buettner, Manuela ^a   Häger, Christine ^a   Bleich, André ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Colitis; Disease susceptibility; IBD; Interleukin 10 deficient mouse; Microbiota; Microflora

Indexed keywords

BACTERIAL ANTIGEN; INTERLEUKIN 10; IL10 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; COLITIS; CONTROLLED STUDY; DENDRITIC CELL; DISEASE PREDISPOSITION; ENTEROCOCCUS FAECALIS; ENVIRONMENTAL FACTOR; EPITHELIUM HYPERPLASIA; GENETIC SUSCEPTIBILITY; IMMUNOLOGICAL TOLERANCE; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; INTESTINE FLORA; MICROFLORA; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; DISEASE MODEL; GENETIC PREDISPOSITION; KNOCKOUT MOUSE; PATHOLOGY; PHYSIOLOGY;

ANIMALS; COLITIS; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; INTERLEUKIN-10; MICE; MICE, KNOCKOUT;

EID: 84941770102     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000468     Document Type: Review

References (102)

1. Izcue A, Coombes JL, Powrie F. Regulatory lymphocytes and intestinal inflammation. Annu Rev Immunol. 2009;27:313-338.
2. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology. 2004;126:1504-1517.
3. Ng SC, Bernstein CN, Vatn MH, et al. Geographical variability and environmental risk factors in inflammatory bowel disease. Gut. 2013;62:630-649.
4. Molodecky NA, Soon IS, Rabi DM, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142:46-54.e42; quiz e30.
5. Larsen S, Bendtzen K, Nielsen OH. Extraintestinal manifestations of inflammatory bowel disease: epidemiology, diagnosis, and management. Ann Med. 2010;42:97-114.
6. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427-434.
7. Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119-124.
8. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134:577-594.
9. Kühn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263-274.
10. Steidler L, Hans W, Schotte L, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science. 2000;289:1352-1355.
11. Bleich A, Mahler M, Most C, et al. Refined histopathologic scoring system improves power to detect colitis QTL in mice. Mamm Genome. 2004;15:865-871.
12. Berg DJ, Davidson N, Kuhn R, et al. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest. 1996;98:1010-1020.
13. Paul G, Khare V, Gasche C. Inflamed gut mucosa: downstream of interleukin-10. Eur J Clin Invest. 2012;42:95-109.
14. Moore KW, O'Garra A, de Waal Malefyt R, et al. Interleukin-10. Annu Rev Immunol. 1993;11:165-190.
15. Murray PJ. Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr Opin Pharmacol. 2006;6:379-386.
16. Davidson NJ, Leach MW, Fort MM, et al. T helper cell 1-type CD4+ T cells, but not B cells, mediate colitis in interleukin 10-deficient mice. J Exp Med. 1996;184:241-251.
17. Yen D, Cheung J, Scheerens H, et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest. 2006;116:1310-1316.
18. Kullberg MC, Rothfuchs AG, Jankovic D, et al. Helicobacter hepaticus-induced colitis in interleukin-10-deficient mice: cytokine requirements for the induction and maintenance of intestinal inflammation. Infect Immun. 2001;69:4232-4241.
19. Oppmann B, Lesley R, Blom B, et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity. 2000;13:715-725.
20. Kullberg MC, Jankovic D, Feng CG, et al. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med. 2006;203:2485-2494.
21. Hue S, Ahern P, Buonocore S, et al. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med. 2006;203:2473-2483.
22. Wilson MS, Ramalingam TR, Rivollier A, et al. Colitis and intestinal inflammation in IL10-/- mice results from IL-13Ralpha2-mediated attenuation of IL-13 activity. Gastroenterology. 2011;140:254-264.
23. Uno JK, Rao KN, Matsuoka K, et al. Altered macrophage function contributes to colitis in mice defective in the phosphoinositide-3 kinase subunit p110delta. Gastroenterology. 2010;139:1642-1653, 1653. e1641-1646.
24. Steinbach EC, Kobayashi T, Russo SM, et al. Innate PI3K p110delta regulates Th1/Th17 development and microbiota-dependent colitis. J Immunol. 2014;192:3958-3968.
25. Ruiz PA, Shkoda A, Kim SC, et al. IL-10 gene-deficient mice lack TGF-beta/Smad-mediated TLR2 degradation and fail to inhibit proinflammatory gene expression in intestinal epithelial cells under conditions of chronic inflammation. Ann N Y Acad Sci. 2006;1072:389-394.
26. Kole A, Maloy KJ. Control of intestinal inflammation by interleukin-10. Curr Top Microbiol Immunol. 2014;380:19-38.
27. Werner T, Shkoda A, Haller D. Intestinal epithelial cell proteome in IL-10 deficient mice and IL-10 receptor reconstituted epithelial cells: impact on chronic inflammation. J Proteome Res. 2007;6:3691-3704.
28. Shkoda A, Ruiz PA, Daniel H, et al. Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology. 2007;132:190-207.
29. Veenbergen S, Samsom JN. Maintenance of small intestinal and colonic tolerance by IL-10-producing regulatory T cell subsets. Curr Opin Immunol. 2012;24:269-276.
30. Rubtsov YP, Rasmussen JP, Chi EY, et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity. 2008;28:546-558.
31. Mantovani A, Marchesi F. IL-10 and macrophages orchestrate gut homeostasis. Immunity. 2014;40:637-639.
32. Shouval DS, Biswas A, Goettel JA, et al. Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity. 2014;40:706-719.
33. Zigmond E, Bernshtein B, Friedlander G, et al. Macrophage-restricted interleukin-10 receptor deficiency, but not IL-10 deficiency, causes severe spontaneous colitis. Immunity. 2014;40:720-733.
34. Pils MC, Bleich A, Prinz I, et al. Commensal gut flora reduces susceptibility to experimentally induced colitis via T-cell-derived interleukin-10. Inflamm Bowel Dis. 2011;17:2038-2046.
35. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010;107:12204-12209.
36. Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331:337-341.
37. Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 2011;474:298-306.
38. Mähler M, Leiter EH. Genetic and environmental context determines the course of colitis developing in IL-10-deficient mice. Inflamm Bowel Dis. 2002;8:347-355.
39. Takeda K, Clausen BE, Kaisho T, et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity. 1999;10:39-49.
40. Bristol IJ, Farmer MA, Cong Y, et al. Heritable susceptibility for colitis in mice induced by IL-10 deficiency. Inflamm Bowel Dis. 2000;6:290-302.
41. Farmer MA, Sundberg JP, Bristol IJ, et al. A major quantitative trait locus on chromosome 3 controls colitis severity in IL-10-deficient mice. Proc Natl Acad Sci U S A. 2001;98:13820-13825.
42. Mahler M, Most C, Schmidtke S, et al. Genetics of colitis susceptibility in IL-10-deficient mice: backcross versus F2 results contrasted by principal component analysis. Genomics. 2002;80:274-282.
43. Jurisic G, Sundberg JP, Bleich A, et al. Quantitative lymphatic vessel trait analysis suggests Vcam1 as candidate modifier gene of inflammatory bowel disease. Genes Immun. 2010;11:219-231.
44. Beckwith J, Cong Y, Sundberg JP, et al. Cdcs1, a major colitogenic locus in mice, regulates innate and adaptive immune response to enteric bacterial antigens. Gastroenterology. 2005;129:1473-1484.
45. Bleich A, Buchler G, Beckwith J, et al. Cdcs1 a major colitis susceptibility locus in mice; subcongenic analysis reveals genetic complexity. Inflamm Bowel Dis. 2010;16:765-775.
46. Ermann J, Garrett WS, Kuchroo J, et al. Severity of innate immune-mediated colitis is controlled by the cytokine deficiency-induced colitis susceptibility-1 (Cdcs1) locus. Proc Natl Acad Sci U S A. 2011;108:7137-7141.
47. Buettner M, Bleich A. Mapping colitis susceptibility in mouse models: distal chromosome 3 contains major loci related to Cdcs1. Physiol Genomics. 2013;45:925-930.
48. Bruesch I, Keubler LM, Messner B, et al. Relation of Cdcs1 and the development of a colitogenic T cell population. Paper presented at: 7th Seeon Conference: Microbiota, Probiota and Host. Monastery Seeon, Germany; 2014:29.
49. de Buhr MF, Hedrich HJ, Westendorf AM, et al. Analysis of Cd14 as a genetic modifier of experimental inflammatory bowel disease (IBD) in mice. Inflamm Bowel Dis. 2009;15:1824-1836.
50. de Buhr MF, Mahler M, Geffers R, et al. Cd14, Gbp1, and Pla2g2a: three major candidate genes for experimental IBD identified by combining QTL and microarray analyses. Physiol Genomics. 2006;25:426-434.
51. Bleich A, Mahler M. Environment as a critical factor for the pathogenesis and outcome of gastrointestinal disease: experimental and human inflammatory bowel disease and helicobacter-induced gastritis. Pathobiology. 2005;72:293-307.
52. Sellon RK, Tonkonogy S, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66:5224-5231.
53. Sydora BC, Tavernini MM, Wessler A, et al. Lack of interleukin-10 leads to intestinal inflammation, independent of the time at which luminal microbial colonization occurs. Inflamm Bowel Dis. 2003;9:87-97.
54. Hoentjen F, Harmsen HJ, Braat H, et al. Antibiotics with a selective aerobic or anaerobic spectrum have different therapeutic activities in various regions of the colon in interleukin 10 gene deficient mice. Gut. 2003;52:1721-1727.
55. Panwala CM, Jones JC, Viney JL. A novel model of inflammatory bowel disease: mice deficient for the multiple drug resistance gene, mdr1a, spontaneously develop colitis. J Immunol. 1998;161:5733-5744.
56. Tamagawa H, Hiroi T, Mizushima T, et al. Therapeutic effects of roxithromycin in interleukin-10-deficient colitis. Inflamm Bowel Dis. 2007;13:547-556.
57. Hans W, Scholmerich J, Gross V, et al. The role of the resident intestinal flora in acute and chronic dextran sulfate sodium-induced colitis in mice. Eur J Gastroenterol Hepatol. 2000;12:267-273.
58. Madsen KL, Doyle JS, Tavernini MM, et al. Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology. 2000;118:1094-1105.
59. Madsen KL. Inflammatory bowel disease: lessons from the IL-10 gene-deficient mouse. Clin Invest Med. 2001;24:250-257.
60. Karrasch T, Kim JS, Muhlbauer M, et al. Gnotobiotic IL-10-/-;NF-kappa B(EGFP) mice reveal the critical role of TLR/NF-kappa B signaling in commensal bacteria-induced colitis. J Immunol. 2007;178:6522-6532.
61. Uronis JM, Muhlbauer M, Herfarth HH, et al. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS One. 2009;4:e6026.
62. Rakoff-Nahoum S, Hao L, Medzhitov R. Role of toll-like receptors in spontaneous commensal-dependent colitis. Immunity. 2006;25:319-329.
63. Rachmilewitz D, Karmeli F, Takabayashi K, et al. Immunostimulatory DNA ameliorates experimental and spontaneous murine colitis. Gastroenterology. 2002;122:1428-1441.
64. Bleich A, Janus LM, Smoczek A, et al. CpG motifs of bacterial DNA exert protective effects in mouse models of IBD by antigen-independent tolerance induction. Gastroenterology. 2009;136:278-287.
65. Schultz M, Veltkamp C, Dieleman LA, et al. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm Bowel Dis. 2002;8:71-80.
66. Burich A, Hershberg R, Waggie K, et al. Helicobacter-induced inflammatory bowel disease in IL-10- and T cell-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2001;281:G764-G778.
67. Kullberg MC, Ward JM, Gorelick PL, et al. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect Immun. 1998;66:5157-5166.
68. Balish E, Warner T. Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol. 2002;160:2253-2257.
69. McCarthy J, O'Mahony L, O'Callaghan L, et al. Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut. 2003;52:975-980.
70. Kim SC, Tonkonogy SL, Albright CA, et al. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology. 2005;128:891-906.
71. Kim SC, Tonkonogy SL, Karrasch T, et al. Dual-association of gnotobiotic IL-10-/- mice with 2 nonpathogenic commensal bacteria induces aggressive pancolitis. Inflamm Bowel Dis. 2007;13:1457-1466.
72. Barnett MP, McNabb WC, Cookson AL, et al. Changes in colon gene expression associated with increased colon inflammation in interleukin-10 gene-deficient mice inoculated with Enterococcus species. BMC Immunol. 2010;11:39.
73. Hoffmann M, Messlik A, Kim SC, et al. Impact of a probiotic Enterococcus faecalis in a gnotobiotic mouse model of experimental colitis. Mol Nutr Food Res. 2011;55:703-713.
74. Dieleman LA, Arends A, Tonkonogy SL, et al. Helicobacter hepaticus does not induce or potentiate colitis in interleukin-10-deficient mice. Infect Immun. 2000;68:5107-5113.
75. Whary MT, Taylor NS, Feng Y, et al. Lactobacillus reuteri promotes Helicobacter hepaticus-associated typhlocolitis in gnotobiotic B6.129P2-IL-10(tm1Cgn) (IL-10(-/-)) mice. Immunology. 2011;133:165-178.
76. Buchler G, Wos-Oxley ML, Smoczek A, et al. Strain-specific colitis susceptibility in IL10-deficient mice depends on complex gut microbiota-host interactions. Inflamm Bowel Dis. 2012;18:943-954.
77. Basic M, Keubler LM, Buettner M, et al. Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice. Inflamm Bowel Dis. 2014;20:431-443.
78. Devkota S, Wang Y, Musch MW, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature. 2012;487:104-108.
79. Bloom SM, Bijanki VN, Nava GM, et al. Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease. Cell Host Microbe. 2011;9:390-403.
80. Eun CS, Mishima Y, Wohlgemuth S, et al. Induction of bacterial antigen-specific colitis by a simplified human microbiota consortium in gnotobiotic interleukin-10-/- mice. Infect Immun. 2014;82:2239-2246.
81. Madsen K, Cornish A, Soper P, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology. 2001;121:580-591.
82. Yang I, Eibach D, Kops F, et al. Intestinal microbiota composition of interleukin-10 deficient C57BL/6J mice and susceptibility to Helicobacter hepaticus-induced colitis. PloS One. 2013;8:e70783.
83. Nagalingam NA, Robinson CJ, Bergin IL, et al. The effects of intestinal microbial community structure on disease manifestation in IL-10-/- mice infected with Helicobacter hepaticus. Microbiome. 2013;1:15.
84. Cadwell K, Patel KK, Maloney NS, et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell. 2010;141:1135-1145.
85. Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. 2014;146:1489-1499.
86. Hunter P. The secret garden's gardeners. Research increasingly appreciates the crucial role of gut viruses for human health and disease. EMBO Rep. 2013;14:683-685.
87. Khan RR, Lawson AD, Minnich LL, et al. Gastrointestinal norovirus infection associated with exacerbation of inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2009;48:328-333.
88. Bleich A, Hansen AK. Time to include the gut microbiota in the hygienic standardisation of laboratory rodents. Comp Immunol Microbiol Infect Dis. 2012;35:81-92.
89. Tamboli CP, Neut C, Desreumaux P, et al. Dysbiosis as a prerequisite for IBD. Gut. 2004;53:1057.
90. Sartor RB. Induction of mucosal immune responses by bacteria and bacterial components. Curr Opin Gastroenterol. 2001;17:555-561.
91. Ott SJ, Musfeldt M, Wenderoth DF, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53:685-693.
92. Walker AW, Sanderson JD, Churcher C, et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol. 2011;11:7.
93. Carriere J, Darfeuille-Michaud A, Nguyen HT. Infectious etiopathogenesis of Crohn's disease. World J Gastroenterol. 2014;20:12102-12117.
94. Martinez-Medina M, Aldeguer X, Gonzalez-Huix F, et al. Abnormal microbiota composition in the ileocolonic mucosa of Crohn's disease patients as revealed by polymerase chain reaction-denaturing gradient gel electrophoresis. Inflamm Bowel Dis. 2006;12:1136-1145.
95. Mondot S, Kang S, Furet JP, et al. Highlighting new phylogenetic specificities of Crohn's disease microbiota. Inflamm Bowel Dis. 2011;17:185-192.
96. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453:620-625.
97. Madsen KL, Doyle JS, Jewell LD, et al. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology. 1999;116:1107-1114.
98. Knoch B, Nones K, Barnett MP, et al. Diversity of caecal bacteria is altered in interleukin-10 gene-deficient mice before and after colitis onset and when fed polyunsaturated fatty acids. Microbiology. 2010;156:3306-3316.
99. Maharshak N, Packey CD, Ellermann M, et al. Altered enteric microbiota ecology in interleukin 10-deficient mice during development and progression of intestinal inflammation. Gut Microbes. 2013;4:316-324.
100. Wohlgemuth S, Keller S, Kertscher R, et al. Intestinal steroid profiles and microbiota composition in colitic mice. Gut Microbes. 2011;2:159-166.
101. Basso PJ, Fonseca MT, Bonfa G, et al. Association among genetic predisposition, gut microbiota, and host immune response in the etiopathogenesis of inflammatory bowel disease. Braz J Med Biol Res. 2014;47:727-737.
102. Gevers D, Kugathasan S, Denson LA, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe. 2014;15:382-392.