Microbial ecology of the murine gut associated with the development of dextran sodium sulfate-induced colitis

Inflammatory Bowel Diseases

Volumn 17, Issue 4, 2011, Pages 917-926

  Nagalingam, Nabeetha A ^a   Kao, John Y ^b   Young, Vincent B ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

16s rRNA encoding gene; Colitis; DSS; Ecology; Microbiota

Indexed keywords

DEXTRAN SULFATE; RNA 16S;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIUM; CCR2 GENE; CD209A GENE; CD40 GENE; CD80 GENE; CECUM; COLITIS; COMMUNITY STRUCTURE; CONTROLLED STUDY; CX3CR1 GENE; CXCL2 GENE; DIGESTIVE SYSTEM INFLAMMATION; DISEASE SEVERITY; GENE EXPRESSION; IL17 GENE; MICROBIAL DIVERSITY; MICROFLORA; MOLLICUTES; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPECIES RICHNESS; TLR 5 GENE; VERRUCOMICROBIA;

ANIMALS; COLITIS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; GASTROINTESTINAL TRACT; GENE EXPRESSION PROFILING; HUMANS; MICE; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, RIBOSOMAL, 16S;

EID: 79952478107     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.21462     Document Type: Article

References (84)

1. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007;449:811-818. (Pubitemid 47598621)
2. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;24:837-848. (Pubitemid 43261456)
3. Round J, Mazmanian S. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9:313-323.
4. Subramanian S, Campbell BJ, Rhodes JM. Bacteria in the pathogenesis of inflammatory bowel disease. Curr Opin Infect Dis. 2006:475-484. (Pubitemid 44338108)
5. Packey C, Sartor R. Interplay of commensal and pathogenic bacteria, genetic mutations, and immunoregulatory defects in the pathogenesis of inflammatory bowel diseases. J Intern Med. 2008;263:597-606. (Pubitemid 351678591)
6. Swidsinski A, Ladhoff A, Pernthaler A, et al. Mucosal flora in inflammatory bowel disease. Gastroenterology. 2002;122:44-54. (Pubitemid 34049193)
7. Ogura Y, Bonen DK, Inohara N, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature. 2001;411:603-606. (Pubitemid 32531409)
8. Kang SS, Bloom SM, Norian LA, et al. An antibiotic-responsive mouse model of fulminant ulcerative colitis. PLoS Med. 2008;5:e41.
9. Swidsinski A, Weber J, Loening-Baucke V, et al. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol. 2005;43:3380-3389. (Pubitemid 40981351)
10. 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. (Pubitemid 29044613)
11. Madsen KL, Doyle JS, Tavernini MM, et al. Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology. 2000;118:1094-1105. (Pubitemid 30346986)
12. Okayasu I, Hatakeyama S, Yamada M, et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98:694-702. (Pubitemid 20069706)
13. Rath H, Schultz M, Freitag R, et al. Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats and mice. Infect Immun. 2001;69:2277-2285. (Pubitemid 32241818)
14. Tai EKK, Wu WKK, Wong HPS, et al. A new role for cathelicidin in ulcerative colitis in mice. Exp Biol Med (Maywood). 2007;232:799-808. (Pubitemid 46827822)
15. Kitajima S, Takuma S, Morimoto M. Changes in colonic mucosal permeability in mouse colitis induced with dextran sulfate sodium. Exp Anim. 1999;48:137-143. (Pubitemid 129558679)
16. Frank DN, St. Amand AL, Feldman RA, et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104:13780-13785. (Pubitemid 350003397)
17. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell. 2004;118:229-241. (Pubitemid 38962578)
18. Vowinkel T, Kalogeris T, Mori M, et al. Impact of dextran sulfate sodium load on the severity of inflammation in experimental colitis. Dig Dis Sci. 2004;49:556-564. (Pubitemid 38992541)
19. Young VB, Knox KA, Pratt JS, et al. In vitro and in vivo characterization of Helicobacter hepaticus cytolethal distending toxin mutants. Infect Immun. 2004;72:2521-2527.
20. Berndt BE, Zhang M, Chen G-H, et al. The role of dendritic cells in the development of acute dextran sulfate sodium colitis. J Immunol. 2007;179:6255-6262.
21. Rachmilewitz D, Karmeli F, Takabayashi K, et al. Immunostimulatory DNA ameliorates experimental and spontaneous murine colitis. Gastroenterology. 2002;122:1428-1441. (Pubitemid 34465184)
22. Lees CW, Zacharias WJ, Tremelling M, et al. Analysis of germline GLI1 variation implicates hedgehog signalling in the regulation of intestinal inflammatory pathways. PLoS Med. 2008;5:1761-1775.
23. Sasmono RT, Ehrnsperger A, Cronau SL, et al. Mouse neutrophilic granulocytes express mRNA encoding the macrophage colony-stimulating factor receptor (CSF-1R) as well as many other macrophage-specific transcripts and can transdifferentiate into macrophages in vitro in response to CSF-1. J Leukoc Biol. 2007;82:111-123. (Pubitemid 47026422)
24. Cui W, Cuartas E, Ke J, et al. CD200 and its receptors, CD200R, modulate bone mass via the differentiation of osteoclasts. PNAS. 2007;104:14436-14441. (Pubitemid 350003279)
25. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45.
26. Guide to performing relative quantitation of gene expression using realtime quantitative PCR. Foster City, CA: Applied Biosystems; 2004.
27. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101-1108. (Pubitemid 351818697)
28. Young VB, Schimdt TM. Antibiotic-associated diarrhea accompanied by large-scale alterations in the composition of the fecal microbiota. J Clin Microbiol. 2004;42:1203-1206. (Pubitemid 38332848)
29. Cole JR, Chai B, Farris RJ, et al. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nuclic Acids Res. 2007;35:D169-172.
30. Schloss P, Westcott S, Ryabin T, et al. Introducing mothur: open source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537-7541.
31. Colwell RK. EstimateS: statistical estimation of species richness and shared species from samples. User's Guide and application. Available at: http://purloclcorg/estimates. 2006.
32. Kumar S, Tamura K, Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 2004;5:150-163.
33. Ludwig W, Strunk O, Westram R, et al. ARB: a software environment for sequence data. Nucleic Acid Res. 2004;32:1363-1371. (Pubitemid 38854737)
34. Liu WT, Marsh TL, Cheng H, et al. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol. 1997;63:4516-4522. (Pubitemid 27485783)
35. Keuhl CJ, Wood HD, Marsh TL, et al. Colonization of the cecal mucosa by Helicobacter hepaticus impacts the diversity of the indigenous microbiota. Infect Immun. 2005;73:6952-6961. (Pubitemid 41368864)
36. Abdo Z, Schuette UME, Bent SJ, et al. Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol. 2006;8:929-938.
37. Martin FE, Nadkarni MA, Jacques NA, et al. Quantitative microbiological study of human carious dentine by culture and real-time PCR: association of anaerobes with histopathological changes in chronic pulpitis. J Clin Microbiol. 2002;40:1698-1704. (Pubitemid 34493143)
38. Nitsche A, Becker M, Junghahn I, et al. Quantification of human cells in NOD/SCID mice by duplex real-time polymerase-chain reaction. Haematologica. 2001;86:693-699. (Pubitemid 32680994)
39. Wirtz S, Neurath MF. Mouse models of inflammatory bowel disease. Adv Drug Deliv Rev. 2007;59:1073-1083. (Pubitemid 47615208)
40. Erridge C, Duncan S, Bereswill S, et al. The induction of colitis and ileitis in mice is associated with marked increases in intestinal concentrations of stimulants of TLRs 2, 4, and 5. PLoS. 2010;5:e9125.
41. Tang Y, Clayburgh DR, Mittal N, et al. Epithelial NF-kappaB enhances transmucosal fluid movement by altering tight junction protein composition after T cell activation. Am J Pathol 2010;176:158-167.
42. Shea-Donohue T, Thomas K, Cody MJ, et al. Mice deficient in the CXCR2 ligand, CXCL1 (KC/GRO-alpha), exhibit increased susceptibility to dextran sodium sulfate (DSS)-induced colitis. Innate Immun. 2008;14:117-124.
43. Blumberg RS, Saubermann LJ, Strober W. Animal models of mucosal inflammation and their relation to human inflammatory bowel disease. Curr Opin Immunol. 1999;11:648-656.
44. Belardelli F, Ferrantini M. Cytokines as a link between innate and adaptive antitumor immunity. Trends Immunol. 2002;23:201-208. (Pubitemid 34260936)
45. Abt MC, Artis D. The intestinal microbiota in health and disease: the influence of microbial products on immune cell homeostasis. Curr Opin Gastroenterol. 2009;25:496-502.
46. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134:577-594. (Pubitemid 351173057)
47. Rath HC, Schultz M, Freitag R, et al. Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats and mice. Infect Immun. 2001;69:2277-2285. (Pubitemid 32241818)
48. Hudcovic T, Stepankova R, Cebra J, et al. The role of microflora in the development of intestinal inflammation: acute and chronic colitis induced by dextran sulfate in germ-free and conventionally reared immunocompetent and immunodeficient mice. Folia Microbiol (Praha). 2001;46:565-572. (Pubitemid 33638684)
49. Kitajima S, Morimoto M, Sagara E, et al. Dextran sodium sulfate-induced colitis in germ-free IQI/Jic mice. Exp Anim. 2001;50:387-395. (Pubitemid 33692774)
50. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell. 2004;118:229-241. (Pubitemid 38962578)
51. Heimesaat M, Fischer A, Siegmund B, et al. Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via Toll-like receptors 2 and 4. PLoS One. 2007;25:e662.
52. 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. (Pubitemid 37510391)
53. Hansen R, Thomson JM, El-Omar EM, et al. The role of infection in the aetiology of inflammatory bowel disease. J Gastroenterol. 2010;45:266-276.
54. Alexander S, Vera L-B, Mario V, et al. Active Crohn's disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora. Inflamm Bowel Dis. 2008;14:147-161.
55. Suchodolski JS, Xenoulis P, Paddock CG, et al. Molecular analysis of the bacterial microbiota in duodenal biopsies from dogs with idiopathic inflammatory bowel disease. Vet Microbiol. 2010;142:394-400.
56. Maukonen J, Satokari R, Matto J, et al. Prevalence and temporal stability of selected clostridial groups in irritable bowel syndrome in relation to predominant faecal bacteria. J Med Microbiol. 2006;55:625-633.
57. Cummings JH, Macfarlane GT. Role of intestinal bacteria in nutrient metabolism. JPEN J Parenter Enteral Nutr. 1997;21:357-365.
58. Deplancke B, Finster K, Graham WV, et al. Gastrointestinal and microbial responses to sulphate-supplemented drinking water in mice. Exp Biol Med. 2003;228:424-433. (Pubitemid 37203650)
59. Araki Y, Mukaisho K, Sugihara H, et al. Proteus mirabilis sp. intestinal microflora grow in a dextran sulfate sodium-rich environment. Int J Mol Med. 2010;25:203-208.
60. Wang M, Ahrne S, Jeppsson B, et al. Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol. 2005:219-231. (Pubitemid 41317922)
61. Derrien M, Vaughan EE, Plugge CM, et al. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 2004;54:1469-1476. (Pubitemid 39359958)
62. Antonopoulos D, Huse S, Morrison H, et al. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun. 2009;77:2367-2375.
63. Ivanov II, Frutos RL, Manel N, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell. 2008;4:337-349.
64. Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485-498.
65. Ahmad MS, Krishnan S, Ramakrishna BS, et al. Butyrate and glucose metabolism by colonocytes in experimental colitis in mice. Gut. 2000;46:493-499. (Pubitemid 30305813)
66. Barcenilla A, Pryde SE, Martin JC, et al. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol. 2000;66:1654-1661. (Pubitemid 30185646)
67. Arijs I, De Hertogh G, Lemaire K, et al. Mucosal gene expression of antimicrobial peptides in inflammatory bowel disease before and after first infliximab treatment. PLoS One. 2009;24:e7984.
68. Wostmann B. The germfree animal in nutritional studies. Annu Rev Nutr. 1981; 1.
69. Clarke TB, Davis KM, Lysenko ES, et al. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med. 2010;16:160-161.
70. Johansson MEV, Phillipson M, Petersson J, et al. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A. 2008;105:15064-15069.
71. Joerg DS, Svenja P, Maren A, et al. Epithelial tight junctions in intestinal inflammation. Ann N Y Acad Sci. 2009;1165:294-300.
72. Nenci A, Becker C, Wullaert A, et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature. 2007;446:557.
73. te Velde A, de Kort F, Sterrenburg E, et al. Comparative analysis of colonic gene expression of three experimental colitis models mimicking inflammatory bowel disease. Inflamm Bowel Dis. 2007;13:325-330.
74. Podolsky D, Gerken G, Eyking A, et al. Colitis-associated variant of TLR2 causes impaired mucosal repair because of TFF3 deficiency. Gastroenterology. 2009;137:209-220.
75. Yan Y, Kolachala V, Dalmasso G, et al. Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS One. 2009;4:e6073.
76. Ito R, Kita M, Shin-Ya M, et al. Involvement of IL-17A in the pathogenesis of DSS-induced colitis in mice. Biochem Biophys Res Commun. 2008;377:12-16.
77. Stefan L, Dick SD, Eva J, et al. The role of the Lps gene in experimental ulcerative colitis in mice. APMIS. 1996;104:823-833.
78. Salzman NH, Bevins CL. Negative interactions with the microbiota: IBD. Adv Exp Med Biol. 2008;635:67-78.
79. Rakoff-Nahoum S, Hao L, Medzhitov R. Role of Toll-like receptors in spontaneous commensal-dependent colitis. Immunity. 2006;25:319-329. (Pubitemid 44224143)
80. Stanislawowski M, Wierzbicki PM, Golab A, et al. Decreased Toll-like receptor-5 (TLR-5) expression in the mucosa of ulcerative colitis patients. J Physiol Pharmacol. 2009;60:71-75.
81. Sabine MI, Megan EH, Gijs H, et al. TLR5 is not required for flagellin-mediated exacerbation of DSS colitis. Inflamm Bowel Dis. 2010;16:401-409.
82. Gobert AP, Cheng Y, Akhtar M, et al. Protective role of arginase in a mouse model of colitis. J Immunol. 2004;173:2109-2117. (Pubitemid 38971649)
83. Horowitz S, Binion DG, Nelson VM, et al. Increased arginase activity and endothelial dysfunction in human inflammatory bowel disease. Am J Physiol Gastroint Liver Physiol. 2007;292:G1323-1336.
84. Philip A, Nicholas CZ, Thuan N, et al. Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm Bowel Dis. 2009;15:341-352.