Immunological alteration and changes of gut microbiota after dextran sulfate sodium (DSS) administration in mice

Clinical and Experimental Medicine

Volumn 15, Issue 1, 2015, Pages 107-120

  Hakansson A ^a   Tormo Badia, N ^b   Baridi, A ^b   Xu, J ^a   Molin, G ^a   Hagslatt M L ^a   Karlsson, C ^a   Jeppsson, B ^b   Cilio, C M ^b   Ahrne S ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

FACS; Immunological reactions; Inflammation; Microbial composition; T RFLP

Indexed keywords

BACTERIAL RNA; CHEMOKINE RECEPTOR CCR9; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DEXTRAN SULFATE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; MYELOPEROXIDASE; RNA 16S; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; PEROXIDASE;

AKKERMANSIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIA; CD3+ T LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLON FLORA; COLON MUCOSA; COMMUNITY STRUCTURE; CONTROLLED STUDY; DESULFOVIBRIO; ENTEROBACTERIACEAE; FEMALE; FLOW CYTOMETRY; FOOD INTAKE; HUMAN; IMMUNOPATHOGENESIS; MESENTERY LYMPH NODE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; ULCERATIVE COLITIS; WEIGHT CHANGE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CHEMICALLY INDUCED; COLON; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; LACTOBACILLUS; LYMPH NODE; MICROBIOLOGY; MICROFLORA; MONOCYTE; PATHOLOGY; PEYER PATCH; SPLEEN; T LYMPHOCYTE;

AKKERMANSIA; ANIMALIA; DESULFOVIBRIO; ENTEROBACTERIACEAE; MUS;

ANIMALS; COLITIS, ULCERATIVE; COLON; CYTOKINES; DESULFOVIBRIO; DEXTRAN SULFATE; ENTEROBACTERIACEAE; FEMALE; HUMANS; IMMUNITY, INNATE; LACTOBACILLUS; LYMPH NODES; MICE; MICE, INBRED C57BL; MICROBIOTA; MONOCYTES; PEROXIDASE; PEYER'S PATCHES; SPLEEN; T-LYMPHOCYTES;

EID: 84902262539     PISSN: 15918890     EISSN: 15919528     Source Type: Journal    
DOI: 10.1007/s10238-013-0270-5     Document Type: Article

References (53)

1. Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453:620–625
2. Podolsky DK (2002) The current future understanding of inflammatory bowel disease. Best Pract Res Clin Gastroenterol 16:933–943
3. Hendrickson BA, Gokhale R, Cho JH (2002) Clinical aspects and pathophysiology of inflammatory bowel disease. Clin Microbiol Rev 15:79–94
4. Fiocchi C (1997) The immune system in inflammatory bowel disease. Acta Gastroenterol Belg 60:156–162
5. Caradonna L, Amati L, Magrone T et al (2000) Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res 6:205–214
6. Cario E (2005) Bacterial interactions with cells of the intestinal mucosa: toll-like receptors and NOD2. Gut 54:1182–1193
7. Okayasu I, Hatakeyama S, Yamada M et al (1990) A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98:694–702
8. Cooper HS, Murthy SN, Shah RS et al (1993) Clinicopathologic study of dextran sulphates sodium experimental murine colitis. Lab Invest 69:238–249
9. Elson CO, Sartor RB, Tennyson GS et al (1995) Experimental models of inflammatory bowel disease. Gastroenterology 109:1344–1367
10. Melgar S, Karlsson A, Michaelsson E (2005) Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am J Physiol Gasterointest Liver Physiol 288:G1328–G1338
11. Geier MS, Smith CL, Butler RN et al (2009) Small intestinal manifestations of dextran sulphate sodium consumption in rats and assessment of the effects of Lactobacillus fermentum BR11. Dig Dis Sci 54:1222–1228
12. Rachmilewitz D, Simon PL, Schwartz LW et al (1989) Inflammatory mediators of experimental colitis in rats. Gastroenterology 97:326–337
13. Murthy S, Murthy NS, Coppola D et al (1997) The efficiency of BAY y 1015 in dextran sulfate model of mouse colitis. Inflamm Res 46:224–233
14. Håkansson A, Bränning C, Adawi D et al (2009) Blueberry husks, rye bran and multi-strain probiotics affect the severity of colitis induced by dextran sulphate sodium. Scand J Gastroenterol 44:1213–1225
15. Khan I, Al-Awadi FM (1997) Colonic muscle enhances the production of interleukin-1β messenger RNA in experimental colitis. Gut 40:307–312
16. Osman N, Adawi D, Ahrne′ S et al (2005) Probiotic strains of Lactobacillus and Bifidobacerium affect the translocation and intestinal load of Enterobacteriaceae differently after D-galactosamine-induced liver injury. Microbiol Ecol Health Dis 17:40–46
17. Karlsson C, Ahrné S, Molin G et al (2009) Probiotic therapy to men with incipient arteriosclerosis initiates increased bacterial diversity in colon: a randomized controlled trial. Atherosclerosis 208:228–233
18. Wang M, Ahrné S, Jeppsson B et al (2005) Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol 54:219–231
19. Walter J, Hertel C, Tannock GW et al (2001) Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67:2578–2585
20. Heilig HG, Zoetendal EG, Vaughan EE et al (2002) Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68:114–123
21. Bartosch S, Fite A, Macfarlane GT et al (2004) 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 70:3575–3581
22. Nadkarni MA, Martin FE, Jacques NA et al (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–266
23. Collado MC, Derrien M, Isolauri E et al (2007) Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol 73:7767–7770
24. Fite A, Macfarlane GT, Cummings JH et al (2004) Identification and quantitation of mucosal and faecal Desulfovibrio using real time polymerase chain reaction. Gut 53:523–529
25. Kristjánsson G, Venge P, Wanders A et al (2004) Clinical and subclinical intestinal inflammation assessed by the mucosal patch technique: studies of mucosal neutrophil and eosinophil activation in inflammatory bowel diseases and irritable bowel syndrome. Gut 53:1806–1812
26. Andoh A, Sakata S, Koizumi Y et al (2007) Terminal restriction fragment length polymorphism analysis of the diversity of fecal microbiota in patients with ulcerative colitis. Inflamm Bowel Dis 13:955–962
27. García-Lafuente A, Antolin M, Guarner F et al (1997) Incrimination of anaerobic bacteria in the induction of experimental colitis. Am J Physiol 272:G10–G15
28. Fabia R, Ar’Rajab A, Johansson ML et al (1993) Impairment of bacterial flora in human ulcerative colitis and experimental colitis in the rat. Digestion 54:248–255
29. Wang M, Molin G, Ahrné S et al (2007) High proportions of proinflammatory bacteria on the colonic mucosa in a young patient with ulcerative colitis as revealed by cloning and sequencing of 16S rRNA genes. Dig Dis Sci 52:620–627
30. Falk A, Olsson C, Ahrné S et al (2007) Ileal pelvic pouch microbiota from two former ulcerative colitis patients, analysed by DNA-based methods, were unstable over time and showed the presence of Clostridium perfringens. Scand J Gastroenterol 42:973–985
31. Bibiloni R, Mangold M, Madsen KL et al (2006) The bacteriology of biopsies differs between newly diagnosed, untreated, Crohn’s disease and ulcerative colitis patients. J Med Microbiol 55:1141–1149
32. Janeczko S, Atwater D, Bogel E et al (2008) The relationship of mucosal bacteria to duodenal histopathology, cytokine mRNA, and clinical disease activity in cats with inflammatory bowel disease. Vet Microbiol 128:178–193
33. Pullan RD, Thomas GAO, Rhodes M et al (1994) Thickness of adherent mucus gel on colonic mucosa in humans and its relevance to colitis. Gut 35:353–359
34. Corfield AP, Myerscough N, Bradfield N et al (1996) Colonic mucins in ulcerative colitis: evidence for loss of sulphation. Glycoconj J 13:809–822
35. Rowan FE, Docherty NG, Coffey JC et al (2009) Sulphate-reducing bacteria and hydrogen sulphide in the aetiology of ulcerative colitis. Br J Surg 96:151–158
36. Bambury N, Coffey JC, Burke J et al (2008) Sulphomucin expression in ileal pouches: emerging differences between ulcerative colitis and familial adenomatous polyposis pouches. Dis Colon Rectum 51:561–567
37. Rowan F, Docherty NG, Murphy M et al (2010) Desulfovibrio bacterial species are increased in ulcerative colitis. Dis Colon Rectum 53:1530–1536
38. Eckburg PB, Bik EM, Bernstein CN et al (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638
39. Osman N, Adawi D, Ahrne S et al (2004) Modulation of the effect of dextran sulfate sodium-induced acute colitis by the administration of different probiotic strains of Lactobacillus and Bifidobacterium. Dig Dis Sci 49:320–327
40. Mylonaki M, Rayment NB, Rampton DS et al (2005) Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm Bowel Dis 11:481–487
41. Rogler G, Andus T, Aschenbrenner E et al (1997) Alterations of the phenotype of colonic macrophages in inflammatory bowel disease. Eur J Gastroenterol Hepatol 9:893–899
42. Chow JC, Young DW, Golenbock DT et al (1999) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 274:10689–10692
43. Ortega-Cava CF, Ishihara S, Rumi MA et al (2003) Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J Immunol 170:3977–3985
44. Hart AL, Al-Hassi HO, Rigby RJ et al (2005) Characteristics of intestinal dendritic cells in inflammatory bowel diseases. Gastroenterology 129:50–65
45. Heimesaat MM, Fischer A, Siegmund B et al (2007) Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via Toll-like receptors 2 and 4. PLoS ONE 2:e662
46. Yu QT, Saruta M, Avanesyan A et al (2007) Expression and functional characterization of FOXP3+CD4+ regulatory T cells in ulcerative colitis. Inflamm Bowel Dis 13:191–199
47. Pasare C, Medzhitov R (2003) Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 299:1033–1036
48. Alex P, Zachos NC, Nguyen T et al (2009) Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm Bowel Dis 15:341–532
49. Yen D, Cheung J, Scheerens H et al (2006) IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 116:1310–1316
50. Nielsen OH, Kirman I, Rüdiger N et al (2003) Upregulation of interleukin-12 and -17 in active inflammatory bowel disease. Scand J Gastroenterol 38:180–185
51. Bozic CR, Kolakowski LF Jr, Gerard NP et al (1995) Expression and biologic characterization of the murine chemokine KC. J Immunol 154:6048–6057
52. Autschbach F, Funke B, Katzenmeier M, et al (2005) Expression of chemokine receptors in normal and inflamed human intestine, tonsil, and liver-an immunohistochemical analysis with new monoclonal antibodies from the 8th international workshop and conference on human leucocyte differentiation antigens. Cell Immunol vol 236, pp 110–114
53. Spahn TW, Herbst H, Rennert PD et al (2002) Induction of colitis in mice deficient of Peyer’s patches and mesenteric lymph nodes is associated with increased disease severity and formation of colonic lymphoid patches. Am J Pathol 161:2273–2282