Bifidobacterium breve reduces apoptotic epithelial cell shedding in an exopolysaccharide and MyD88-dependent manner

Open Biology

Volumn 7, Issue 1, 2017, Pages

  Hughes, K R ^a,b   Harnisch, L C ^a,b   Alcon Giner, C ^a   Mitra, S ^a   Wright, C J ^a,b   Ketskemety, J ^a   Van Sinderen, D ^c,d   Watson, A J M ^a,b   Hall, L J ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c UNIVERSITY COLLEGE CORK   (Ireland)

^d UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Bifidobacterium; Epithelial cell shedding; Exopolysaccharide; Inflammatory bowel disease

Indexed keywords

BACTERIAL POLYSACCHARIDE; LIPOPOLYSACCHARIDE; MYD88 PROTEIN, MOUSE; MYELOID DIFFERENTIATION FACTOR 88;

ANIMAL; APOPTOSIS; BIFIDOBACTERIUM BREVE; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; MICROBIOLOGY; MOUSE; PHYSIOLOGY; SMALL INTESTINE;

ANIMALS; APOPTOSIS; BIFIDOBACTERIUM BREVE; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INTESTINE, SMALL; LIPOPOLYSACCHARIDES; MICE; MYELOID DIFFERENTIATION FACTOR 88; POLYSACCHARIDES, BACTERIAL;

EID: 85012932652     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.160155     Document Type: Article

References (62)

1. Ventura M, Turroni F, Lugli GA, van Sinderen D. 2014 Bifidobacteria and humans: our special friends, from ecological to genomics perspectives. J. Sci. Food Agric. 94, 163-168. (doi:10.1002/jsfa.6356)
2. Turnbaugh PJ, Gordon JI. 2009 The core gut microbiome, energy balance and obesity. J. Physiol. 587, 4153-4158. (doi:10.1113/jphysiol. 2009.174136)
3. Sivan A et al. 2015 Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350, 1084-1089. (doi:10.1126/science.aac4255)
4. Fukuda S et al. 2011 Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543-547. (doi:10.1038/nature09646)
5. Ishikawa H, Akedo I, Umesaki Y, Tanaka R, Imaoka A, Otani T. 2003 Randomized controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis. J. Am. Coll. Nutr. 22, 56-63. (doi:10.1080/07315724.2003.10719276)
6. Maukonen J, Kolho KL, Paasela M, Honkanen J, Klemetti P, Vaarala O, Saarela M. 2015 Altered fecal microbiota in paediatric inflammatory bowel disease. J. Crohns Colitis 9, 1088-1095. (doi:10.1093/ecco-jcc/jjv147)
7. Fanning S et al. 2012 Bifidobacterial surfaceexopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc. Natl Acad. Sci. USA 109, 2108-2113. (doi:10.1073/pnas.1115621109)
8. Backhed F, Manchester JK, Semenkovich CF, Gordon JI. 2007 Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl Acad. Sci. USA 104, 979-984. (doi:10.1073/pnas. 0605374104)
9. McDermott AJ, Huffnagle GB. 2014 The microbiome and regulation of mucosal immunity. Immunology 142, 24-31. (doi:10.1111/imm.12231)
10. Peterson LW, Artis D. 2014 Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 14, 141-153. (doi:10.1038/nri3608)
11. Sommer F, Nookaew I, Sommer N, Fogelstrand P, Backhed F. 2015 Site-specific programming of the host epithelial transcriptome by the gut microbiota. Genome Biol. 16, 62. (doi:10.1186/s13059-015-0614-4)
12. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. 2004 Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118, 229-241. (doi:10.1016/j.cell.2004.07.002)
13. Tamboli CP, Neut C, Desreumaux P, Colombel JF. 2004 Dysbiosis in inflammatory bowel disease. Gut 53, 1-4. (doi:10.1136/gut.53.1.1)
14. Sokol H et al. 2008 Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl Acad. Sci. USA 105, 16 731-16 736. (doi:10.1073/pnas.0804812105)
15. Duranti S et al. 2016 Elucidating the gut microbiome of ulcerative colitis: bifidobacteria as novel microbial biomarkers. FEMS Microbiol. Ecol. 92, fiw191. (doi:10.1093/femsec/fiw191)
16. Guan Y, Watson AJ, Marchiando AM, Bradford E, Shen L, Turner JR, Montrose MH. 2011 Redistribution of the tight junction protein ZO-1 during physiological shedding of mouse intestinal epithelial cells. Am. J. Physiol. Cell Physiol. 300, C1404-C1414. (doi:10.1152/ajpcell. 00270.2010)
17. Potten CS, Loeffler M. 1990 Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110, 1001-1020.
18. Bullen TF, Forrest S, Campbell F, Dodson AR, Hershman MJ, Pritchard DM, Turner JR, Montrose MH, Watson AJ. 2006 Characterization of epithelial cell shedding from human small intestine. Lab Invest. 86, 1052-1063. (doi:10.1038/labinvest. 3700464)
19. Watson AJ, Hughes KR. 2012 TNF-α-induced intestinal epithelial cell shedding: implications for intestinal barrier function. Ann. N.Y. Acad. Sci. 1258, 1-8. (doi:10.1111/j.1749-6632.2012.06523.x)
20. Kiesslich R et al. 2007 Identification of epithelial gaps in human small and large intestine by confocal endomicroscopy. Gastroenterology 133, 1769-1778. (doi:10.1053/j.gastro.2007.09.011)
21. Kiesslich R et al. 2012 Local barrier dysfunction identified by confocal laser endomicroscopy predicts relapse in inflammatory bowel disease. Gut 61, 1146-1153. (doi:10.1136/gutjnl-2011-300695)
22. Williams JM et al. 2013 A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide. Dis. Model. Mech. 6, 1388-1399. (doi:10.1242/dmm.013284)
23. Potten CS, Owen G, Booth D. 2002 Intestinal stem cells protect their genome by selective segregation of template DNA strands. J. Cell Sci. 115, 2381-2388.
24. McKaig BC, Hughes K, Tighe PJ, Mahida YR. 2002 Differential expression of TGF-beta isoforms by normal and inflammatory bowel disease intestinal myofibroblasts. Am. J. Physiol. Cell Physiol. 282, C172-C182. (doi:10.1152/ajpcell.00048.2001)
25. Pfaffl MW. 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45. (doi:10.1093/nar/29.9.e45)
26. McLarren KW, Cole AE, Weisser SB, Voglmaier NS, Conlin VS, Jacobson K, Popescu O, Boucher JL, Sly LM. 2011 SHIP-deficient mice develop spontaneous intestinal inflammation and arginase-dependent fibrosis. Am. J. Pathol. 179, 180-188. (doi:10.1016/j.ajpath.2011.03.018)
27. Schindelin J et al. 2012 Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682. (doi:10.1038/nmeth.2019)
28. Watson AJ, Chu S, Sieck L, Gerasimenko O, Bullen T, Campbell F, McKenna M, Rose T, Montrose MH. 2005 Epithelial barrier function in vivo is sustained despite gaps in epithelial layers. Gastroenterology 129, 902-912. (doi:10.1053/j.gastro.2005.06.015)
29. Manichanh C, Borruel N, Casellas F, Guarner F. 2012 The gut microbiota in IBD. Nat. Rev. Gastroenterol. Hepatol. 9, 599-608. (doi:10.1038/nrgastro.2012.152)
30. Wu MH, Pan TM, Wu YJ, Chang SJ, Chang MS, Hu CY. 2010 Exopolysaccharide activities from probiotic bifidobacterium: immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. Int. J. Food Microbiol. 144, 104-110. (doi:10.1016/j.ijfoodmicro.2010.09.003)
31. Fanning S, Hall LJ, van Sinderen D. 2012 Bifidobacterium breve UCC2003 surface exopolysaccharide production is a beneficial trait mediating commensal-host interaction through immune modulation and pathogen protection. Gut Microbes 3, 420-425. (doi:10.4161/gmic.20630)
32. Weiser MM. 1973 Intestinal epithelial cell surface membrane glycoprotein synthesis. I. An indicator of cellular differentiation. J. Biol. Chem. 248, 2536-2541.
33. Corr SC et al. 2014 MyD88 adaptor-like (Mal) functions in the epithelial barrier and contributes to intestinal integrity via protein kinase C. Mucosal Immunol. 7, 57-67. (doi:10.1038/mi.2013.24)
34. Bottacini F et al. 2014 Comparative genomics of the Bifidobacterium breve taxon. BMC Genomics 15, 170. (doi:10.1186/1471-2164-15-170)
35. Gevers D et al. 2014 The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe. 15, 382-392. (doi:10.1016/j.chom.2014. 02.005)
36. Saez-Lara MJ, Gomez-Llorente C, Plaza-Diaz J, Gil A. 2015 The role of probiotic lactic acid bacteria and bifidobacteria in the prevention and treatment of inflammatory bowel disease and other related diseas.es: a systematic review of randomized human clinical trials. Biomed. Res Int. 2015, 505878. (doi:10.1155/2015/505878)
37. Wang J et al. 2015 Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J. 9, 1-15. (doi:10.1038/ismej.2014.99)
38. Fite A, Macfarlane S, Furrie E, Bahrami B, Cummings JH, Steinke DT, Macfarlane GT. 2013 Longitudinal analyses of gut mucosal microbiotas in ulcerative colitis in relation to patient age and disease severity and duration. J. Clin. Microbiol. 51, 849-856. (doi:10.1128/JCM.02574-12)
39. Turroni F et al. 2012 Diversity of bifidobacteria within the infant gut microbiota. PLoS ONE 7, e0036957. (doi:10.1371/journal.pone.0036957)
40. Wall R, Hussey SG, Ryan CA, O'Neill M, Fitzgerald G, Stanton C, Ross RP. 2008 Presence of two Lactobacillus and Bifidobacterium probiotic strains in the neonatal ileum. ISME J. 2, 83-91. (doi:10.1038/ISMEJ.2007.69)
41. Fakhry S, Manzo N, D'Apuzzo E, Pietrini L, Sorrentini I, Ricca E, De Felice M, Baccigalupi L. 2009 Characterization of intestinal bacteria tightly bound to the human ileal epithelium. Res. Microbiol. 160, 817-823. (doi:10.1016/j.resmic.2009.09.009)
42. Roulis M, Armaka M, Manoloukos M, Apostolaki M, Kollias G. 2011 Intestinal epithelial cells as producers but not targets of chronic TNF suffice to cause murine Crohn-like pathology. Proc. Natl Acad. Sci. USA 108, 5396-5401. (doi:10.1073/pnas. 1007811108)
43. Wang F, Schwarz BT, Graham WV, Wang Y, Su L, Clayburgh DR, Abraham C, Turner JR. 2006 IFNgamma-induced TNFR2 expression is required for TNF-dependent intestinal epithelial barrier dysfunction. Gastroenterology 131, 1153-1163. (doi:10.1053/j.gastro.2006.08.022)
44. Cario E, Gerken G, Podolsky DK. 2004 Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology 127, 224-238. (doi:10.1053/j. gastro.2004.04.015)
45. Khailova L, Mount Patrick SK, Arganbright KM, Halpern MD, Kinouchi T, Dvorak B. 2010 Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 299, G1118-G1127. (doi:10.1152/ajpgi.00131.2010)
46. Surana NK, Kasper DL. 2012 The yin yang of bacterial polysaccharides: lessons learned from B. fragilis PSA. Immunol. Rev. 245, 13-26. (doi:10.1111/j.1600-065X.2011.01075.x)
47. Oliveira-Nascimento L, Massari P, Wetzler LM. 2012 The role of TLR2 in infection and immunity. Front. Immunol. 3, 79. (doi:10.3389/fimmu.2012.00079)
48. Jeon SG et al. 2012 Probiotic Bifidobacterium breve induces IL-10-producing Tr1 cells in the colon. PLoS Pathog. 8, e1002714. (doi:10.1371/journal.ppat. 1002714)
49. Jones SE, Paynich ML, Kearns DB, Knight KL. 2014 Protection from intestinal inflammation by bacterial exopolysaccharides. J. Immunol. 192, 4813-4820. (doi:10.4049/jimmunol.1303369)
50. Hidalgo-Cantabrana C, Lopez P, Gueimonde M, de Los Reyes-Gavilan CG, Suarez A, Margolles A, Ruas-Madiedo P. 2012 Immune Modulation capability of exopolysaccharides synthesised by lactic acid bacteria and bifidobacteria. Probiotics Antimicrob. Proteins 4, 227-237. (doi:10.1007/s12602-012-9110-2)
51. Patten DA, Leivers S, Chadha MJ, Maqsood M, Humphreys PN, Laws AP, Collett A. 2014 The structure and immunomodulatory activity on intestinal epithelial cells of the EPSs isolated from Lactobacillus helveticus sp. Rosyjski and Lactobacillus acidophilus sp. 5e2. Carbohydr. Res. 384, 119-127. (doi:10.1016/j.carres.2013.12.008)
52. Yasuda E, Serata M, Sako T. 2008 Suppressive effect on activation of macrophages by Lactobacillus casei strain Shirota genes determining the synthesis of cell wall-associated polysaccharides. Appl. Environ. Microbiol. 74, 4746-4755. (doi:10.1128/AEM. 00412-08)
53. Ciszek-Lenda M, Nowak B, Srottek M, Gamian A, Marcinkiewicz J. 2011 Immunoregulatory potential of exopolysaccharide from Lactobacillus rhamnosus KL37: effects on the production of inflammatory mediators by mouse macrophages. Int. J. Exp. Pathol. 92, 382-391. (doi:10.1111/j.1365-2613. 2011.00788.x)
54. Nwodo UU, Green E, Okoh AI. 2012 Bacterial exopolysaccharides: functionality and prospects. Int. J. Mol. Sci. 13, 14 002-14 015. (doi:10.3390/ijms131114002)
55. Ksonzekova P, Bystricky P, Vlckova S, Patoprsty V, Pulzova L, Mudronova D, Kubaskova T, Csank T, Tkacikova L. 2016 Exopolysaccharides of Lactobacillus reuteri: their influence on adherence of E. coli to epithelial cells and inflammatory response. Carbohyd. Polym. 141, 10-19. (doi:10.1016/j. carbpol.2015.12.037)
56. Lebeer S, Vanderleyden J, De Keersmaecker SC. 2010 Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8, 171-184. (doi:10.1038/nrmicro2297)
57. Bron PA, van Baarlen P, Kleerebezem M. 2012 Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat. Rev. Microbiol. 10, 66-78. (doi:10.1038/nrmicro2690)
58. Altemeier WA, Zhu X, Berrington WR, Harlan JM, Liles WC. 2007 Fas (CD95) induces macrophage proinflammatory chemokine production via a MyD88-dependent, caspase-independent pathway. J. Leukoc. Biol. 82, 721-728. (doi:10.1189/jlb. 1006652)
59. Green DR, Llambi F. 2015 Cell Death Signaling. Cold Spring Harb. Perspect. Biol. 7, a006080. (doi:10.1101/cshperspect.a006080)
60. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. 1997 Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489. (doi:10.1016/S0092-8674(00) 80434-1)
61. Oeckinghaus A, Hayden MS, Ghosh S. 2011 Crosstalk in NF-κB signaling pathways. Nat. Immunol. 12, 695-708. (doi:10.1038/ni.2065)
62. Sica G, Chen L. 1999 Biochemical and immunological characteristics of 4-1BB (CD137) receptor and ligand and potential applications in cancer therapy. Arch. Immunol. Ther. Exp. (Warsz). 47, 275-279.