Amelioration of DSS-induced murine colitis by VSL#3 supplementation is primarily associated with changes in ileal microbiota composition.

References

• Langholz E. Current trends in inflammatory bowel disease: the natural history. Therap Adv Gastroenterol 2010; 3:77 - 86; http://dx.doi.org/10.1177/1756283X10361304; PMID: 21180592
   PubMedGoogle Scholar
• Packey CD, Sartor RB. 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; http://dx.doi.org/10.1111/j.1365-2796.2008.01962.x; PMID: 18479259
   PubMed Web of Science ®Google Scholar
• Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139:485 - 98; http://dx.doi.org/10.1016/j.cell.2009.09.033; PMID: 19836068
   PubMed Web of Science ®Google Scholar
• Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331:337 - 41; http://dx.doi.org/10.1126/science.1198469; PMID: 21205640
   PubMed Web of Science ®Google Scholar
• von Schillde MA, Hörmannsperger G, Weiher M, Alpert CA, Hahne H, Bäuerl C, van Huynegem K, Steidler L, Hrncir T, Pérez-Martínez G, et al. Lactocepin secreted by Lactobacillus exerts anti-inflammatory effects by selectively degrading proinflammatory chemokines. Cell Host Microbe 2012; 11:387 - 96; http://dx.doi.org/10.1016/j.chom.2012.02.006; PMID: 22520466
   PubMed Web of Science ®Google Scholar
• Yan F, Cao H, Cover TL, Washington MK, Shi Y, Liu L, Chaturvedi R, Peek RM Jr., Wilson KT, Polk DB. Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. J Clin Invest 2011; 121:2242 - 53; http://dx.doi.org/10.1172/JCI44031; PMID: 21606592
   PubMed Web of Science ®Google Scholar
• 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 - 9; http://dx.doi.org/10.1073/pnas.0909122107; PMID: 20566854
   PubMed Web of Science ®Google Scholar
• Bibiloni R, Mangold M, Madsen KL, Fedorak RN, Tannock GW. The bacteriology of biopsies differs between newly diagnosed, untreated, Crohn’s disease and ulcerative colitis patients. J Med Microbiol 2006; 55:1141 - 9; http://dx.doi.org/10.1099/jmm.0.46498-0; PMID: 16849736
   PubMed Web of Science ®Google Scholar
• Uronis JM, Arthur JC, Keku T, Fodor A, Carroll IM, Cruz ML, Appleyard CB, Jobin C. Gut microbial diversity is reduced by the probiotic VSL#3 and correlates with decreased TNBS-induced colitis. Inflamm Bowel Dis 2011; 17:289 - 97; http://dx.doi.org/10.1002/ibd.21366; PMID: 20564535
   PubMed Web of Science ®Google Scholar
• Nagalingam NA, Kao JY, Young VB. Microbial ecology of the murine gut associated with the development of dextran sodium sulfate-induced colitis. Inflamm Bowel Dis 2011; 17:917 - 26; http://dx.doi.org/10.1002/ibd.21462; PMID: 21391286
   PubMed Web of Science ®Google Scholar
• Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007; 104:13780 - 5; http://dx.doi.org/10.1073/pnas.0706625104; PMID: 17699621
   PubMed Web of Science ®Google Scholar
• Kabeerdoss J, Sankaran V, Pugazhendhi S, Ramakrishna BS. Clostridium leptum group bacteria abundance and diversity in the fecal microbiota of patients with inflammatory bowel disease: a case-control study in India. BMC Gastroenterol 2013; 13:20; http://dx.doi.org/10.1186/1471-230X-13-20; PMID: 23351032
   PubMed Web of Science ®Google Scholar
• Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Doré J. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 2009; 15:1183 - 9; http://dx.doi.org/10.1002/ibd.20903; PMID: 19235886
   PubMed Web of Science ®Google Scholar
• Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Fölsch UR, Timmis KN, Schreiber S. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 2004; 53:685 - 93; http://dx.doi.org/10.1136/gut.2003.025403; PMID: 15082587
   PubMed Web of Science ®Google Scholar
• Walker AW, Sanderson JD, Churcher C, Parkes GC, Hudspith BN, Rayment N, Brostoff J, Parkhill J, Dougan G, Petrovska L. 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; http://dx.doi.org/10.1186/1471-2180-11-7; PMID: 21219646
   PubMed Web of Science ®Google Scholar
• Kumari R, Ahuja V, Paul J. Fluctuations in butyrate-producing bacteria in ulcerative colitis patients of North India. World J Gastroenterol 2013; 19:3404 - 14; http://dx.doi.org/10.3748/wjg.v19.i22.3404; PMID: 23801832
   PubMed Web of Science ®Google Scholar
• Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 2009; 294:1 - 8; http://dx.doi.org/10.1111/j.1574-6968.2009.01514.x; PMID: 19222573
   PubMed Web of Science ®Google Scholar
• Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013; 341:569 - 73; http://dx.doi.org/10.1126/science.1241165; PMID: 23828891
   PubMed Web of Science ®Google Scholar
• Segain JP, Raingeard de la Blétière D, Bourreille A, Leray V, Gervois N, Rosales C, Ferrier L, Bonnet C, Blottière HM, Galmiche JP. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn’s disease. Gut 2000; 47:397 - 403; http://dx.doi.org/10.1136/gut.47.3.397; PMID: 10940278
   PubMed Web of Science ®Google Scholar
• Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, 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 - 6; http://dx.doi.org/10.1073/pnas.0804812105; PMID: 18936492
   PubMed Web of Science ®Google Scholar
• Okamoto T, Sasaki M, Tsujikawa T, Fujiyama Y, Bamba T, Kusunoki M. Preventive efficacy of butyrate enemas and oral administration of Clostridium butyricum M588 in dextran sodium sulfate-induced colitis in rats. J Gastroenterol 2000; 35:341 - 6; http://dx.doi.org/10.1007/s005350050358; PMID: 10832668
   PubMed Web of Science ®Google Scholar
• Hudcovic T, Kolinska J, Klepetar J, Stepankova R, Rezanka T, Srutkova D, Schwarzer M, Erban V, Du Z, Wells JM, et al. Protective effect of Clostridium tyrobutyricum in acute dextran sodium sulphate-induced colitis: differential regulation of tumour necrosis factor-α and interleukin-18 in BALB/c and severe combined immunodeficiency mice. Clin Exp Immunol 2012; 167:356 - 65; http://dx.doi.org/10.1111/j.1365-2249.2011.04498.x; PMID: 22236013
   PubMed Web of Science ®Google Scholar
• Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 2011; 474:298 - 306; http://dx.doi.org/10.1038/nature10208; PMID: 21677746
   PubMed Web of Science ®Google Scholar
• Harrison OJ, Maloy KJ. Innate immune activation in intestinal homeostasis. J Innate Immun 2011; 3:585 - 93; http://dx.doi.org/10.1159/000330913; PMID: 21912101
   PubMed Web of Science ®Google Scholar
• Brandtzaeg P, Carlsen HS, Halstensen TS. The B-cell system in inflammatory bowel disease. Adv Exp Med Biol 2006; 579:149 - 67; http://dx.doi.org/10.1007/0-387-33778-4_10; PMID: 16620017
   PubMed Web of Science ®Google Scholar
• Rembacken BJ, Snelling AM, Hawkey PM, Chalmers DM, Axon AT. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 1999; 354:635 - 9; http://dx.doi.org/10.1016/S0140-6736(98)06343-0; PMID: 10466665
   PubMed Web of Science ®Google Scholar
• Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, De Simone C, Sartor RB. VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 2005; 100:1539 - 46; http://dx.doi.org/10.1111/j.1572-0241.2005.41794.x; PMID: 15984978
   PubMed Web of Science ®Google Scholar
• Haller D, Antoine JM, Bengmark S, Enck P, Rijkers GT, Lenoir-Wijnkoop I. Guidance for substantiating the evidence for beneficial effects of probiotics: probiotics in chronic inflammatory bowel disease and the functional disorder irritable bowel syndrome. J Nutr 2010; 140:690S - 7S; http://dx.doi.org/10.3945/jn.109.113746; PMID: 20107148
   PubMed Web of Science ®Google Scholar
• Yui S, Nakamura T, Sato T, Nemoto Y, Mizutani T, Zheng X, Ichinose S, Nagaishi T, Okamoto R, Tsuchiya K, et al. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5⁺ stem cell. Nat Med 2012; 18:618 - 23; http://dx.doi.org/10.1038/nm.2695; PMID: 22406745
   PubMed Web of Science ®Google Scholar
• He XW, He XS, Lian L, Wu XJ, Lan P. Systemic infusion of bone marrow-derived mesenchymal stem cells for treatment of experimental colitis in mice. Dig Dis Sci 2012; 57:3136 - 44; http://dx.doi.org/10.1007/s10620-012-2290-5; PMID: 22752635
   PubMed Web of Science ®Google Scholar
• Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 2013; 31:814 - 21; http://dx.doi.org/10.1038/nbt.2676; PMID: 23975157
   PubMed Web of Science ®Google Scholar
• Berry D, Schwab C, Milinovich G, Reichert J, Ben Mahfoudh K, Decker T, Engel M, Hai B, Hainzl E, Heider S, et al. Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. ISME J 2012; 6:2091 - 106; http://dx.doi.org/10.1038/ismej.2012.39; PMID: 22572638
   PubMed Web of Science ®Google Scholar
• Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci U S A 2008; 105:20858 - 63; http://dx.doi.org/10.1073/pnas.0808723105; PMID: 19075245
   PubMed Web of Science ®Google Scholar
• Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A 2002; 99:15451 - 5; http://dx.doi.org/10.1073/pnas.202604299; PMID: 12432102
   PubMed Web of Science ®Google Scholar
• Bansal T, Alaniz RC, Wood TK, Jayaraman A. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc Natl Acad Sci U S A 2010; 107:228 - 33; http://dx.doi.org/10.1073/pnas.0906112107; PMID: 19966295
   PubMed Web of Science ®Google Scholar
• Medeiros MR, Prado LA, Fernandes VC, Figueiredo SS, Coppede J, Martins J, Fiori GM, Martinez-Rossi NM, Beleboni RO, Contini SH, et al. Antimicrobial activities of indole alkaloids from Tabernaemontana catharinensis. Nat Prod Commun 2011; 6:193 - 6; PMID: 21425672
   PubMed Web of Science ®Google Scholar
• Tamaoki J, Kadota J, Takizawa H. Clinical implications of the immunomodulatory effects of macrolides. Am J Med 2004; 117:Suppl 9A 5S - 11S; PMID: 15586558
   PubMed Web of Science ®Google Scholar
• Bartosh TJ, Ylöstalo JH, Mohammadipoor A, Bazhanov N, Coble K, Claypool K, Lee RH, Choi H, Prockop DJ. Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their antiinflammatory properties. Proc Natl Acad Sci U S A 2010; 107:13724 - 9; http://dx.doi.org/10.1073/pnas.1008117107; PMID: 20643923
   PubMed Web of Science ®Google Scholar
• Kruis W, Schütz E, Fric P, Fixa B, Judmaier G, Stolte M. Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 1997; 11:853 - 8; http://dx.doi.org/10.1046/j.1365-2036.1997.00225.x; PMID: 9354192
   PubMed Web of Science ®Google Scholar
• Kruis W, Fric P, Pokrotnieks J, Lukás M, Fixa B, Kascák M, Kamm MA, Weismueller J, Beglinger C, Stolte M, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 2004; 53:1617 - 23; http://dx.doi.org/10.1136/gut.2003.037747; PMID: 15479682
   PubMed Web of Science ®Google Scholar
• Möndel M, Schroeder BO, Zimmermann K, Huber H, Nuding S, Beisner J, Fellermann K, Stange EF, Wehkamp J. Probiotic E. coli treatment mediates antimicrobial human beta-defensin synthesis and fecal excretion in humans. Mucosal Immunol 2009; 2:166 - 72; http://dx.doi.org/10.1038/mi.2008.77; PMID: 19129752
   PubMed Web of Science ®Google Scholar
• Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, Cai J, Hippe H, Farrow JA. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 1994; 44:812 - 26; http://dx.doi.org/10.1099/00207713-44-4-812; PMID: 7981107
   PubMedGoogle Scholar
• Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE, Shen B, Schaeffeler E, Schwab M, Linzmeier R, et al. Reduced Paneth cell alpha-defensins in ileal Crohn’s disease. Proc Natl Acad Sci U S A 2005; 102:18129 - 34; http://dx.doi.org/10.1073/pnas.0505256102; PMID: 16330776
   PubMed Web of Science ®Google Scholar
• Garner CD, Antonopoulos DA, Wagner B, Duhamel GE, Keresztes I, Ross DA, Young VB, Altier C. Perturbation of the small intestine microbial ecology by streptomycin alters pathology in a Salmonella enterica serovar typhimurium murine model of infection. Infect Immun 2009; 77:2691 - 702; http://dx.doi.org/10.1128/IAI.01570-08; PMID: 19433544
   PubMed Web of Science ®Google Scholar
• Meisch JP, Nishimura M, Vogel RM, Sung HC, Bednarchik BA, Ghosh SK, Fu P, McCormick T, Weinberg A, Levine AD. Human β-defensin 3 peptide is increased and redistributed in Crohn’s ileitis. Inflamm Bowel Dis 2013; 19:942 - 53; http://dx.doi.org/10.1097/MIB.0b013e318280b11a; PMID: 23511030
   PubMed Web of Science ®Google Scholar
• Bassaganya-Riera J, Viladomiu M, Pedragosa M, De Simone C, Carbo A, Shaykhutdinov R, Jobin C, Arthur JC, Corl BA, Vogel H, et al. Probiotic bacteria produce conjugated linoleic acid locally in the gut that targets macrophage PPAR γ to suppress colitis. PLoS One 2012; 7:e31238; http://dx.doi.org/10.1371/journal.pone.0031238; PMID: 22363592
   PubMedGoogle Scholar
• Pagnini C, Saeed R, Bamias G, Arseneau KO, Pizarro TT, Cominelli F. Probiotics promote gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci U S A 2010; 107:454 - 9; http://dx.doi.org/10.1073/pnas.0910307107; PMID: 20018654
   PubMed Web of Science ®Google Scholar
• Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Shi S, Le AD. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 2009; 183:7787 - 98; http://dx.doi.org/10.4049/jimmunol.0902318; PMID: 19923445
   PubMed Web of Science ®Google Scholar
• Rojas M, Xu J, Woods CR, Mora AL, Spears W, Roman J, Brigham KL. Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol 2005; 33:145 - 52; http://dx.doi.org/10.1165/rcmb.2004-0330OC; PMID: 15891110
   PubMed Web of Science ®Google Scholar
• Matters GL, Harms JF, McGovern C, Fitzpatrick L, Parikh A, Nilo N, Smith JP. The opioid antagonist naltrexone improves murine inflammatory bowel disease. J Immunotoxicol 2008; 5:179 - 87; http://dx.doi.org/10.1080/15476910802131469; PMID: 18569389
   PubMed Web of Science ®Google Scholar
• Ishikura T, Kanai T, Uraushihara K, Iiyama R, Makita S, Totsuka T, Yamazaki M, Sawada T, Nakamura T, Miyata T, et al. Interleukin-18 overproduction exacerbates the development of colitis with markedly infiltrated macrophages in interleukin-18 transgenic mice. J Gastroenterol Hepatol 2003; 18:960 - 9; http://dx.doi.org/10.1046/j.1440-1746.2003.03097.x; PMID: 12859727
   PubMed Web of Science ®Google Scholar
• Roediger FC, Slusher NA, Allgaier S, Cox MJ, Pletcher SD, Goldberg AN, Lynch SV. Nucleic acid extraction efficiency and bacterial recovery from maxillary sinus mucosal samples obtained by brushing or biopsy. Am J Rhinol Allergy 2010; 24:263 - 5; http://dx.doi.org/10.2500/ajra.2010.24.3472; PMID: 20819463
   PubMed Web of Science ®Google Scholar
• Cox MJ, Allgaier M, Taylor B, Baek MS, Huang YJ, Daly RA, Karaoz U, Andersen GL, Brown R, Fujimura KE, et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One 2010; 5:e11044; http://dx.doi.org/10.1371/journal.pone.0011044; PMID: 20585638
   PubMed Web of Science ®Google Scholar
• Hazen TC, Dubinsky EA, DeSantis TZ, Andersen GL, Piceno YM, Singh N, Jansson JK, Probst A, Borglin SE, Fortney JL, et al. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 2010; 330:204 - 8; http://dx.doi.org/10.1126/science.1195979; PMID: 20736401
   PubMed Web of Science ®Google Scholar
• Cox MJ, Huang YJ, Fujimura KE, Liu JT, McKean M, Boushey HA, Segal MR, Brodie EL, Cabana MD, Lynch SV. Lactobacillus casei abundance is associated with profound shifts in the infant gut microbiome. PLoS One 2010; 5:e8745; http://dx.doi.org/10.1371/journal.pone.0008745; PMID: 20090909
   PubMed Web of Science ®Google Scholar
• Brodie EL, Desantis TZ, Joyner DC, Baek SM, Larsen JT, Andersen GL, Hazen TC, Richardson PM, Herman DJ, Tokunaga TK, et al. Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 2006; 72:6288 - 98; http://dx.doi.org/10.1128/AEM.00246-06; PMID: 16957256
   PubMed Web of Science ®Google Scholar
• Pielou EC. The measurement of diversity in different types of biological samples. J Theor Biol 1966; 13:131 - 44; http://dx.doi.org/10.1016/0022-5193(66)90013-0
   Web of Science ®Google Scholar
• Fujimura KE, Johnson CC, Ownby DR, Cox MJ, Brodie EL, Havstad SL, Zoratti EM, Woodcroft KJ, Bobbitt KR, Wegienka G, et al. Man’s best friend? The effect of pet ownership on house dust microbial communities. J Allergy Clin Immunol 2010; 126:410 - 2, e1-3; http://dx.doi.org/10.1016/j.jaci.2010.05.042; PMID: 20633927
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological) 1995; 57:6:289–300.
   Google Scholar