Influences of the colonic microbiome on the mucous gel layer in ulcerative colitis

Gut Microbes

Volumn 5, Issue 3, 2014, Pages

  Lennon, Gráinne ^a,b   Balfe, Áine ^a,b   Early, Helen ^a,b   Devane, Liam A ^a,b   Lavelle, Aonghus ^a,b   Winter, Desmond C ^a,b   Coffey, J Calvin ^c   Ronan O'Connell, P ^a,b  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^c UNIVERSITY HOSPITAL LIMERICK   (Ireland)

Author keywords

Bacteria; Colon; Mucins; Mucus gel layer; Ulcerative colitis

Indexed keywords

N ACETYLGALACTOSAMINE;

EPITHELIUM CELL; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; IMMUNE SYSTEM; INFLAMMATION; MICROBIOME; NONHUMAN; PROTEIN DEGRADATION; REVIEW; SEQUENCE ANALYSIS; ULCERATIVE COLITIS; BACTERIUM; COLON; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; MUCUS; PATHOLOGY; SECRETION (PROCESS);

BACTERIA; COLITIS, ULCERATIVE; COLON; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROBIOTA; MUCUS;

EID: 84903973629     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.28793     Document Type: Review

References (100)

1. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008; 6:e280; PMID:19018661; http://dx.doi.org/10.1371/journal.pbio.0060280
2. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002; 22:283-307; PMID:12055347; http://dx.doi.org/10.1146/annurev.nutr.22.011602.092259
3. Guarner F, Malagelada JR. Gut flora in health and disease. Lancet 2003; 361:512-9; PMID:12583961; http://dx.doi.org/10.1016/S0140-6736(03)12489-0
4. Hooper LV, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 2010; 10:159-69; PMID:20182457; http://dx.doi.org/10.1038/nri2710
5. Johansson MEV, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 2008; 105:15064-9; PMID:18806221; http://dx.doi.org/10.1073/pnas.0803124105
6. Suzuki K, Meek B, Doi Y, Muramatsu M, Chiba T, Honjo T, Fagarasan S. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci U S A 2004; 101:1981-6; PMID:14766966; http://dx.doi.org/10.1073/pnas.0307317101
7. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl JP, Ricciardi-Castagnoli P. Dendritic cells express tight junction proteins and penetrate gut epithelial mono-layers to sample bacteria. Nat Immunol 2001; 2:361-7; PMID:11276208; http://dx.doi.org/10.1038/86373
8. Beeken W, Northwood I, Beliveau C, Gump D. Phagocytes in cell suspensions of human colon mucosa. Gut 1987; 28:976-80; PMID:3666566; http://dx.doi.org/10.1136/gut.28.8.976
9. Barnes MJ, Powrie F. Regulatory T cells reinforce intestinal homeostasis. Immunity 2009; 31:401-11; PMID: 19766083; http://dx.doi.org/10.1016/j.immuni.2009.08.011
10. Campieri M, Gionchetti P. Bacteria as the cause of ulcerative colitis. Gut 2001; 48:132-5; PMID:11115835; http://dx.doi.org/10.1136/gut.48.1.132
11. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9:313-23; PMID:19343057; http://dx.doi.org/10.1038/nri2515
12. Dupaul-Chicoine J, Dagenais M, Saleh M. Crosstalk between the intestinal microbiota and the innate immune system in intestinal homeostasis and inflammatory bowel disease. Inflamm Bowel Dis 2013; 19:2227-37; PMID:23669404; http://dx.doi.org/10.1097/MIB.0b013e31828dcac7
13. Deplancke B, Gaskins HR. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 2001; 73:1131S-41S; PMID:11393191
14. Bansil R, Turner BS. Mucin structure, aggregation, physiological functions and biomedical applications. Curr Opin Colloid Interface Sci 2006; 11:164-70; http://dx.doi.org/10.1016/j.cocis.2005.11.001
15. Brockhausen I, Schutzbach J, Kuhns W. Glycoproteins and their relationship to human disease. Acta Anat (Basel) 1998; 161:36-78; PM ID:9780351; http://dx.doi.org/10.1159/000046450
16. Thomsson KA, Holmén-Larsson JM, Angström J, Johansson ME, Xia L, Hansson GC. Detailed O-glycomics of the Muc2 mucin from colon of wild-type, core 1- and core 3-transferase-deficient mice highlights differences compared with human MUC2. Glycobiology 2012; 22:1128-39; PMID:22581805; http://dx.doi.org/10.1093/glycob/cws083
17. Croix JA, Carbonero F, Nava GM, Russell M, Greenberg E, Gaskins HR. On the relationship between sialomucin and sulfomucin expression and hydrogenotrophic microbes in the human colonic mucosa. PLoS One 2011; 6:e24447; PMI D: 21931721; http://dx.doi.org/10.1371/journal.pone.0024447
18. Lennon G, Balfe A, Bambury N, Lavelle A, Maguire A, Docherty NG, Coffey JC, Winter D, Sheahan K, O'Connell PR. Correlations between colonic crypt mucin chemotype, inflammatory grade and Desulfovibrio species in ulcerative colitis. Colorectal Dis 2013; PMID:24345279; http://dx.doi.org/10.1111/codi.12503
19. Kaftan SM, Wright NA. Studies on the mechanisms of mucous cell depletion in experimental colitis. J Pathol 1989; 159:75-85; PMID:2809887; http://dx.doi.org/10.1002/path.1711590115
20. McCormick DA, Horton LW, Mee AS. Mucin depletion in inflammatory bowel disease. J Clin Pathol 1990; 43:143-6; PMID:2318990; http://dx.doi.org/10.1136/jcp.43.2.143
21. Pullan RD, Thomas GA, Rhodes M, Newcombe RG, Williams GT, Allen A, Rhodes J. Thickness of adherent mucus gel on colonic mucosa in humans and its relevance to colitis. Gut 1994; 35:353-9; PMID:8150346; http://dx.doi.org/10.1136/gut.35.3.353
22. Theodossi A, Spiegelhalter DJ, Jass J, Firth J, Dixon M, Leader M, Levison DA, Lindley R, Filipe I, Price A, et al. Observer variation and discriminatory value of biopsy features in inflammatory bowel disease. Gut 1994; 35:961-8; PMID:8063225; http://dx.doi.org/10.1136/gut.35.7.961
23. Teague RH, Fraser D, Clamp JR. Changes in monosaccharide content of mucous glycopro-teins in ulcerative colitis. Br Med J 1973; 2:645-6; PMID: 4714849; http://dx.doi.org/10.1136/bmj.2.5867.645
24. Clamp JR, Fraser G, Read AE. Study of the carbohydrate content of mucus glycoproteins from normal and diseased colons. Clin Sci (Lond) 1981; 61:229-34; PMID:7261546
25. Morita H, Kettlewell MG, Jewell DP, Kent PW. Glycosylation and sulfation of colonic mucus glycoproteins in patients with ulcerative colitis and in healthy subjects. Gut 1993; 34:926-32; PMID:8344580; http://dx.doi.org/10.1136/gut.34.7.926
26. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Järnerot G, Tysk C, Jansson JK, Engstrand L. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phe-notypes. Gastroenterology 2010; 139:1844-U105, e1; PMID:20816835; http://dx.doi.org/10.1053/j.gastro.2010.08.049
27. An G, Wei B, Xia B, McDaniel JM, Ju T, Cummings RD, Braun J, Xia L. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med 2007; 204:1417-29; PMID:17517967; http://dx.doi.org/10.1084/jem.20061929
28. Stone EL, Ismail MN, Lee SH, Luu Y, Ramirez K, Haslam SM, Ho SB, Dell A, Fukuda M, Marth JD. Glycosyltransferase function in core 2-type protein O glycosylation. Mol Cell Biol 2009; 29:3770-82; PMID:19349303; http://dx.doi.org/10.1128/MCB.00204-09
29. Fu J, Wei B, Wen T, Johansson ME, Liu X, Bradford E, Thomsson KA, McGee S, Mansour L, Tong M, et al. Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice. J Clin Invest 2011; 121:1657-66; PMID:21383503; http://dx.doi.org/10.1172/JCI45538
30. Nieuw Amerongen AV, Bolscher JGM, Bloemena E, Veerman ECI. Sulfomucins in the human body. Biol Chem 1998; 379:1-18; PMID:9504711
31. Gibson GR, Cummings JH, Macfarlane GT. Growth and Activities of Sulfate-Reducing Bacteria in Gut Contents of Healthy-Subjects and Patients with Ulcerative-Colitis. FEMS Microbiol Ecol 1991; 86:103-11; http://dx.doi.org/10.1111/j.1574-6968.1991.tb04799.x
32. Rowan F, Docherty NG, Murphy M, Murphy B, Calvin Coffey J, O'Connell PR. Desulfovibrio bacterial species are increased in ulcerative colitis. Dis Colon Rectum 2010; 53:1530-6; PMID:20940602; http://dx.doi.org/10.1007/DCR.0b013e3181f1e620
33. Swidsinski A, Loening-Baucke V, Lochs H, Hale L P. Spatial organization of bacterial flora in normal and inflamed intestine: a fluorescence in situ hybridization study in mice. World J Gastroenterol 2005; 11:1131-40; PMID:15754393
34. Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Büller HA, Dekker J, Van Seuningen I, Renes IB, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 2006; 131:117-29; PMID: 1683159 6; http://dx.doi.org/10.1053/j.gastro.2006.04.020
35. Velcich A, Yang W, Heyer J, Fragale A, Nicholas C, Viani S, Kucherlapati R, Lipkin M, Yang K, Augenlicht L. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 2002; 295:1726-9; PMID:11872843; http://dx.doi.org/10.1126/science.1069094
36. Nowacki MR. Cell proliferation in colonic crypts of germ-free and conventional mice--preliminary report. Folia Histochem Cytobiol 1993; 31:77-81; PMID:8405572
37. Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, Taupin D, Thornton DJ, Png CW, Crockford TL, Cornall RJ, et al. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med 2008; 5:e54; PMID:18318598; http://dx.doi.org/10.1371/journal.pmed.0050054
38. Johansson ME, Gustafsson JK, Holmén-Larsson J, Jabbar KS, Xia L, Xu H, Ghishan FK, Carvalho FA, Gewirtz AT, Sjövall H, et al. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcer-ative colitis. Gut 2014; 63:281-91; PMID:23426893
39. Palestrant D, Holzknecht ZE, Collins BH, Parker W, Miller SE, Bollinger RR. Microbial biofilms in the gut: visualization by electron microscopy and by acridine orange staining. Ultrastruct Pathol 2004; 28:23-7; PMID:14967595; http://dx.doi.org/10.1080/01913120490275196
40. Swidsinski A, Sydora BC, Doerffel Y, Loening-Baucke V, Vaneechoutte M, Lupicki M, Scholze J, Lochs H, Dieleman LA. Viscosity gradient within the mucus layer determines the mucosal barrier function and the spatial organization of the intestinal microbiota. Inflamm Bowel Dis 2007; 13:963-70; PMID: 17455202; http://dx.doi.org/10.1002/ibd.20163
41. Chen W, Liu F, Ling Z, Tong X, Xiang C. Human intestinal lumen and mucosa-associated micro-biota in patients with colorectal cancer. PLoS One 2012; 7:e39743; PMID:22761885; http://dx.doi.org/10.1371/journal.pone.0039743
42. Carroll IM, Ringel-Kulka T, Keku TO, Chang Y-H, Packey CD, Sartor RB, Ringel Y. Molecular analysis of the luminal- and mucosal-associated intestinal microbiota in diarrhea-predominant irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2011; 301:G799-807; PMID:21737778; http://dx.doi.org/10.1152/ajpgi.00154.2011
43. Gillevet P, Sikaroodi M, Keshavarzian A, Mutlu EA. Quantitative assessment of the human gut microbi-ome using multitag pyrosequencing. Chem Biodivers 2010; 7:1065-75; PMID:20491064; http://dx.doi.org/10.1002/cbdv.200900322
44. Lepage P, Seksik P, Sutren M, de la Cochetière M-F, Jian R, Marteau P, Doré J. Biodiversity of the mucosa-associated microbiota is stable along the distal digestive tract in healthy individuals and patients with IBD. Inflamm Bowel Dis 2005; 11:473-80; http://dx.doi.org/10.1097/01.MIB.0000159662.62651.06; PMID:15867587
45. Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben-Amor K, Akkermans AD, de Vos WM. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 2002; 68:3401-7; PMID:12089021; http://dx.doi.org/10.1128/AEM.68.7.3401-3407.2002
46. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science 2005; 308:1635-8; PMID:15831718; http://dx.doi.org/10.1126/science.1110591
47. Nava GM, Friedrichsen HJ, Stappenbeck TS. Spatial organization of intestinal microbiota in the mouse ascending colon. ISME J 2011; 5:627-38; PMID:20981114; http://dx.doi.org/10.1038/ismej.2010.161
48. Van den Abbeele P, Gérard P, Rabot S, Bruneau A, El Aidy S, Derrien M, Kleerebezem M, Zoetendal EG, Smidt H, Verstraete W, et al. Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degrada-tion in humanized rats. Environ Microbiol 2011; 13:2667-80; PMID:21883787; http://dx.doi.org/10.1111/j.1462-2920.2011.02533.x
49. Rowan FE, Docherty NG, Coffey JC, O'Connell PR. Sulfate-reducing bacteria and hydrogen sulfide in the aetiology of ulcerative colitis. Br J Surg 2009; 96:151-8; PMID:19160346; http://dx.doi.org/10.1002/bjs.6454
50. Strugala V, Dettmar PW, Pearson JP. Thickness and continuity of the adherent colonic mucus barrier in active and quiescent ulcerative colitis and Crohn's disease. Int J Clin Pract 2008; 62:762-9; PMID:18194279; http://dx.doi.org/10.1111/j.1742-1241.2007.01665.x
51. 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 USA 2007; 104:13780-5; PMID: 1769 9 621; http://dx.doi.org/10.1073/pnas.0706625104
52. Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Ballet V, Claes K, Van Immerseel F, Verbeke K, et al. A decrease of the butyrate-produc-ing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcer-ative colitis. Gut 2013; PMID:24021287; http://dx.doi.org/10.1136/gutjnl-2013-304833
53. 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 micro-biota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol 2011; 11: 7; PMID:21219646; http://dx.doi.org/10.1186/1471-2180-11-7
54. Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 2010; 105:2420-8; PMID:20648002; http://dx.doi.org/10.1038/ajg.2010.281
55. Norin KE, Gustafsson BE, Lindblad BS, Midtvedt T. The establishment of some microflora associated biochemical characteristics in feces from children during the first years of life. Acta Paediatr Scand 1985; 74: 207-12; PMID: 3922199; http://dx.doi.org/10.1111/j.1651-2227.1985.tb10951.x
56. Savage DC. Associations and physiological interactions of indigenous microorganisms and gastrointestinal epithelia. Am J Clin Nutr 1972; 25:1372-9; PMID:4565354
57. Probert HM, Gibson GR. Bacterial biofilms in the human gastrointestinal tract. Curr Issues Intest Microbiol 2002; 3:23-7; PMID:12400635
58. Gibson GR, Macfarlane GT, Cummings JH. Sulfate reducing bacteria and hydrogen metabolism in the human large intestine. Gut 1993; 34:437-9; PMID:8491386; http://dx.doi.org/10.1136/gut.34.4.437
59. Roos S, Jonsson H. A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 2002; 148:433-42; PMID:11832507
60. Boekhorst J, Helmer Q, Kleerebezem M, Siezen RJ. Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology 2006; 152:273-80; PMID:16385136; http://dx.doi.org/10.1099/mic.0.28415-0
61. Pretzer G, Snel J, Molenaar D, Wiersma A, Bron PA, Lambert J, de Vos WM, van der Meer R, Smits MA, Kleerebezem M. Biodiversity-based identification and functional characterization of the mannose-spe-cific adhesin of Lactobacillus plantarum. J Bacteriol 2005; 187:6128-36; PMID:16109954; http://dx.doi.org/10.1128/JB.187.17.6128-6136.2005
62. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx APA, Lebeer S, et al. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein. Proc Natl Acad Sci U S A 2009; 106:17193-8; PMID:19805152; http://dx.doi.org/10.1073/pnas.0908876106
63. Bergonzelli GE, Granato D, Pridmore RD, Marvin-Guy LF, Donnicola D, Corthésy-Theulaz IE. GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect Immun 2006; 74:425-34; PMID:16368998; http://dx.doi.org/10.1128/IAI.74.1.425-434.2006
64. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, O'Brien F, Flynn K, Casey PG, Munoz JAM, et al. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci U S A 2011; 108:11217-22; PMID:21690406; http://dx.doi.org/10.1073/pnas.1105380108
65. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen M-C, Desiere F, Bork P, Delley M, et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A 2002; 99:14422-7; PMID:12381787; http://dx.doi.org/10.1073/pnas.212527599
66. Huang JY, Lee SM, Mazmanian SK. The human commensal Bacteroides fragilis binds intestinal mucin. Anaerobe 2011; 17:137-41; PMID:21664470; http://dx.doi.org/10.1016/j.anaerobe.2011.05.017
67. Hoskins LC, Zamcheck N. Bacterial degradation of gastrointestinal mucins. I. Comparison of mucus constituents in the stools of germ-free and conventional rats. Gastroenterology 1968; 54:210-7; PMID:5711903
68. Hoskins LC, Agustines M, McKee WB, Boulding ET, Kriaris M, Niedermeyer G. Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J Clin Invest 1985; 75:944-53; PMID:3920248; http://dx.doi.org/10.1172/JCI111795
69. Hoskins LC, Boulding ET. Mucin degradation in human colon ecosystems. Evidence for the existence and role of bacterial subpopulations producing gly-cosidases as extracellular enzymes. J Clin Invest 1981; 67:163-72; PMID: 6161136; http://dx.doi.org/10.1172/JCI110009
70. Hoskins LC, Boulding ET, Gerken TA, Harouny VR, Kriaris MS. Mucin Glycoprotein Degradation by Mucin Oligosaccharide-degrading Strains of Human Faecal Bacteria. Characterisation of Saccharide Cleavage Products and their Potential Role in Nutritional Support of Larger Faecal Bacterial Populations. Microb Ecol Health Dis 1992; 5:193-207; http://dx.doi.org/10.3109/08910609209141586
71. Corfield AP, Wagner SA, Clamp JR, Kriaris MS, Hoskins LC. Mucin degradation in the human colon: production of sialidase, sialate O-acetylesterase, N-acetylneuraminate lyase, arylesterase, and glycos-ulfatase activities by strains of fecal bacteria. Infect Immun 1992; 60:3971-8; PMID:1398908
72. Wesley A, Mantle M, Man D, Qureshi R, Forstner G, Forstner J. Neutral and acidic species of human intestinal mucin. Evidence for different core peptides. J Biol Chem 1985; 260:7955-9; PMID:4008485
73. Miller RS, Hoskins LC. Mucin degradation in human colon ecosystems. Fecal population densities of mucin-degrading bacteria estimated by a "most probable number" method. Gastroenterology 1981; 81:759-65; PMID:7262520
74. Willis CL, Cummings JH, Neale G, Gibson GR. In VitroEffects of Mucin Fermentation on the Growth of Human Colonic Sulfate-Reducing Bacteria. Anaerobe 1996; 2:117-22; http://dx.doi.org/10.1006/anae.1996.0015
75. Midtvedt AC, Carlstedt-Duke B, Midtvedt T. Establishment of a mucin-degrading intestinal microflora during the first two years of human life. J Pediatr Gastroenterol Nutr 1994; 18:321-6; PMID:8057215; http://dx.doi.org/10.1097/00005176-199404000-00012
76. Cooke CL, An HJ, Kim J, Canfield DR, Torres J, Lebrilla CB, Solnick JV. Modif ication of gastric mucin oligosaccharide expression in rhesus macaques after infection with Helicobacter pylori. Gastroenterology 2009; 137:1061-71, e1-8; PMID:19375420; http://dx.doi.org/10.1053/j.gastro.2009.04.014
77. Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 2009; 5:200-11; PMID: 19218090; http://dx.doi.org/10.1016/j.chom.2009.01.003
78. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, Buhler JD, Gordon JI. Glycan foraging in vivo by an intestine-adapted bacterial sym-biont. Science 2005; 307:1955-9; PMID:15790854; http://dx.doi.org/10.1126/science.1109051
79. Turroni F, Milani C, van Sinderen D, Ventura M. Genetic strategies for mucin metabolism in Bifidobacterium bifidum PRL2010: an example of possible human-microbe co-evolution. Gut Microbes 2011; 2:183-9; PMID:21804355; http://dx.doi.org/10.4161/gmic.2.3.16105
80. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 2013; 502:96-9; PMID:23995682; http://dx.doi.org/10.1038/nature12503
81. Stahl M, Friis LM, Nothaft H, Liu X, Li J, Szymanski CM, Stintzi A. L-fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci U S A 2011; 108:7194-9; PMID:21482772; http://dx.doi.org/10.1073/pnas.1014125108
82. Fabich AJ, Jones SA, Chowdhury FZ, Cernosek A, Anderson A, Smalley D, McHargue JW, Hightower GA, Smith JT, Autieri SM, et al. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun 2008; 76:1143-52; PMID:18180286; http://dx.doi.org/10.1128/IAI.01386-07
83. Marcobal A, Southwick AM, Earle KA, Sonnenburg JL. A refined palate: bacterial consumption of host glycans in the gut. Glycobiology 2013; 23:1038-46; PMID:23720460; http://dx.doi.org/10.1093/glycob/cwt040
84. Bocci V. The neglected organ: bacterial flora has a crucial immunostimulatory role. Perspect Biol Med 1992; 35:251-60; PM ID:1557302
85. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P, et al. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 2007; 5:e156; PMID:17579514; http://dx.doi.org/10.1371/journal.pbio.0050156
86. Tsai HH, Hart CA, Rhodes JM. Production of mucin degrading sulfatase and glycosidases by Bacteroides thetaiotaomicron. Lett Appl Microbiol 1991; 13:97-101; http://dx.doi.org/10.1111/j.1472-765X.1991.tb00580.x
87. Wrzosek L, Miquel S, Noordine ML, Bouet S, Joncquel Chevalier-Curt M, Robert V, Philippe C, Bridonneau C, Cherbuy C, Robbe-Masselot C, et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus gly-cans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol 2013; 11:61; PMID:23692866; http://dx.doi.org/10.1186/1741-7007-11-61
88. 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; PMID:19235886; http://dx.doi.org/10.1002/ibd.20903
89. Gibson GR, Cummings JH, Macfarlane GT. Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria. Appl Environ Microbiol 1988; 54:2750-5; PM I D: 3214155
90. Florin T, Neale G, Gibson GR, Christl SU, Cummings JH. Metabolism of dietary sulfate: absorption and excretion in humans. Gut 1991; 32:766-73; PMID:1855683; http://dx.doi.org/10.1136/gut.32.7.766
91. Duffy M, O'Mahony L, Coffey JC, Collins JK, Shanahan F, Redmond HP, Kirwan WO. Sulfate-reducing bacteria colonize pouches formed for ulcerative colitis but not for familial adenoma-tous polyposis. Dis Colon Rectum 2002; 45:384-8; PMID:12068199; http://dx.doi.org/10.1007/s10350-004-6187-z
92. Bambury N, Coffey JC, Burke J, Redmond HP, Kirwan WO. Sulfomucin expression in ileal pouches: emerging differences between ulcerative colitis and familial adenomatous polyposis pouches. Dis Colon Rectum 2008; 51:561-7; PMID:18299930; http://dx.doi.org/10.1007/s10350-008-9200-0
93. Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 2004; 54:1469-76; PMID: 15388697; http://dx.doi.org/10.1099/ijs.0.02873-0
94. Cervera-Tison M, Tailford LE, Fuell C, Bruel L, Sulzenbacher G, Henrissat B, Berrin JG, Fons M, Giardina T, Juge N. Functional analysis of family GH36 α-galactosidases from Ruminococcus gnavus E1: insights into the metabolism of a plant oligo-saccharide by a human gut symbiont. Appl Environ Microbiol 2012; 78:7720-32; PMI D:22923411; http://dx.doi.org/10.1128/AEM.01350-12
95. Hoskins LC, Boulding ET, Larson G. Purification and characterization of blood group A-degrading isoforms of alpha-N-acetylgalactosaminidase from Ruminococcus torques strain IX-70. J Biol Chem 1997; 272:7932-9; PMID:9065462; http://dx.doi.org/10.1074/jbc.272.12.7932
96. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 2003; 299:2074-6; PMID:12663928; http://dx.doi.org/10.1126/science.1080029
97. Macfarlane GT, Gibson GR. Formation of glycopro-tein degrading enzymes by Bacteroides fragilis. FEMS Microbiol Lett 1991; 61:289-93; PMID:1903753; http://dx.doi.org/10.1111/j.1574-6968.1991.tb04363.x
98. Macfarlane GT, Macfarlane S, Gibson GR. Synthesis and release of proteases byBacteroides fragilis. Curr Microbiol 1992; 24:55-9; http://dx.doi.org/10.1007/BF01570100
99. Prindiville T P, Sheikh RA, Cohen SH, Tang YJ, Cantrell MC, Silva J Jr. Bacteroides fragi-lis enterotoxin gene sequences in patients with inflammatory bowel disease. Emerg Infect Dis 2000; 6:171-4; PMID:10756151; http://dx.doi.org/10.3201/eid0602.000210
100. Onderdonk AB, Cisneros RL, Bronson RT. Enhancement of experimental ulcerative colitis by immunization with Bacteroides vulgatus. Infect Immun 1983; 42:783-8; PMID: 6642651