Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Butyrate modulates bacterial adherence on LS174T human colorectal cells by stimulating mucin secretion and MAPK signaling pathway

  • Jung, Tae-Hwan (Department of Animal Biotechnology and Resource, Sahmyook University) ;
  • Park, Jeong Hyeon (Institute of Fundamental Sciences, Massey University) ;
  • Jeon, Woo-Min (Department of Animal Biotechnology and Resource, Sahmyook University) ;
  • Han, Kyoung-Sik (Department of Animal Biotechnology and Resource, Sahmyook University)
  • Received : 2015.03.31
  • Accepted : 2015.05.18
  • Published : 2015.08.01
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Abstract

BACKGROUND/OBJECTIVES: Fermentation of dietary fiber results in production of various short chain fatty acids in the colon. In particular, butyrate is reported to regulate the physical and functional integrity of the normal colonic mucosa by altering mucin gene expression or the number of goblet cells. The objective of this study was to investigate whether butyrate modulates mucin secretion in LS174T human colorectal cells, thereby influencing the adhesion of probiotics such as Lactobacillus and Bifidobacterium strains and subsequently inhibiting pathogenic bacteria such as E. coli. In addition, possible signaling pathways involved in mucin gene regulation induced by butyrate treatment were also investigated. MATERIALS/METHODS: Mucin protein content assay and periodic acid-Schiff (PAS) staining were performed in LS174T cells treated with butyrate at various concentrations. Effects of butyrate on the ability of probiotics to adhere to LS174T cells and their competition with E. coli strains were examined. Real time polymerase chain reaction for mucin gene expression and Taqman array 96-well fast plate-based pathway analysis were performed on butyrate-treated LS174T cells. RESULTS: Treatment with butyrate resulted in a dose-dependent increase in mucin protein contents in LS174T cells with peak effects at 6 or 9 mM, which was further confirmed by PAS staining. Increase in mucin protein contents resulted in elevated adherence of probiotics, which subsequently reduced the adherent ability of E. coli. Treatment with butyrate also increased transcriptional levels of MUC3, MUC4, and MUC12, which was accompanied by higher gene expressions of signaling kinases and transcription factors involved in mitogen-activated protein kinase (MAPK) signaling pathways. CONCLUSIONS: Based on our results, butyrate is an effective regulator of modulation of mucin protein production at the transcriptional and translational levels, resulting in changes in the adherence of gut microflora. Butyrate potentially stimulates the MAPK signaling pathway in intestinal cells, which is positively correlated with gut defense.

Keywords

References

  1. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 2001;81:1031-64. https://doi.org/10.1152/physrev.2001.81.3.1031
  2. Shimotoyodome A, Meguro S, Hase T, Tokimitsu I, Sakata T. Short chain fatty acids but not lactate or succinate stimulate mucus release in the rat colon. Comp Biochem Physiol A Mol Integr Physiol 2000;125:525-31. https://doi.org/10.1016/S1095-6433(00)00183-5
  3. Blottiere HM, Buecher B, Galmiche JP, Cherbut C. Molecular analysis of the effect of short-chain fatty acids on intestinal cell proliferation. Proc Nutr Soc 2003;62:101-6. https://doi.org/10.1079/PNS2002215
  4. Young GP, Hu Y, Le Leu RK, Nyskohus L. Dietary fibre and colorectal cancer: a model for environment--gene interactions. Mol Nutr Food Res 2005;49:571-84. https://doi.org/10.1002/mnfr.200500026
  5. Olmo N, Turnay J, Perez-Ramos P, Lecona E, Barrasa JI, Lopez de Silanes I, Lizarbe MA. In vitro models for the study of the effect of butyrate on human colon adenocarcinoma cells. Toxicol In Vitro 2007;21:262-70. https://doi.org/10.1016/j.tiv.2006.09.011
  6. Yang J, Kawai Y, Hanson RW, Arinze IJ. Sodium butyrate induces transcription from the G alpha(i2) gene promoter through multiple Sp1 sites in the promoter and by activating the MEK-ERK signal transduction pathway. J Biol Chem 2001;276:25742-52. https://doi.org/10.1074/jbc.M102821200
  7. Shah P, Nankova BB, Parab S, La Gamma EF. Short chain fatty acids induce TH gene expression via ERK-dependent phosphorylation of CREB protein. Brain Res 2006;1107:13-23. https://doi.org/10.1016/j.brainres.2006.05.097
  8. Zhang Y, Zhou L, Bao YL, Wu Y, Yu CL, Huang YX, Sun Y, Zheng LH, Li YX. Butyrate induces cell apoptosis through activation of JNK MAP kinase pathway in human colon cancer RKO cells. Chem Biol Interact 2010;185:174-81. https://doi.org/10.1016/j.cbi.2010.03.035
  9. Zuo L, Lu M, Zhou Q, Wei W, Wang Y. Butyrate suppresses proliferation and migration of RKO colon cancer cells though regulating endocan expression by MAPK signaling pathway. Food Chem Toxicol 2013;62:892-900. https://doi.org/10.1016/j.fct.2013.10.028
  10. Corfield AP, Myerscough N, Longman R, Sylvester P, Arul S, Pignatelli M. Mucins and mucosal protection in the gastrointestinal tract: new prospects for mucins in the pathology of gastrointestinal disease. Gut 2000;47:589-94. https://doi.org/10.1136/gut.47.4.589
  11. Han KS, Deglaire A, Sengupta R, Moughan PJ. Hydrolyzed casein influences intestinal mucin gene expression in the rat. J Agric Food Chem 2008;56:5572-6. https://doi.org/10.1021/jf800080e
  12. Allen A, Hutton DA, Pearson JP. The MUC2 gene product: a human intestinal mucin. Int J Biochem Cell Biol 1998;30:797-801. https://doi.org/10.1016/S1357-2725(98)00028-4
  13. Gaudier E, Jarry A, Blottiere HM, de Coppet P, Buisine MP, Aubert JP, Laboisse C, Cherbut C, Hoebler C. Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose. Am J Physiol Gastrointest Liver Physiol 2004;287: G1168-74. https://doi.org/10.1152/ajpgi.00219.2004
  14. Trompette A, Blanchard C, Zoghbi S, Bara J, Claustre J, Jourdan G, Chayvialle JA, Plaisance P. The DHE cell line as a model for studying rat gastro-intestinal mucin expression: effects of dexamethasone. Eur J Cell Biol 2004;83:347-58. https://doi.org/10.1078/0171-9335-00391
  15. Delcenserie V, Martel D, Lamoureux M, Amiot J, Boutin Y, Roy D. Immunomodulatory effects of probiotics in the intestinal tract. Curr Issues Mol Biol 2008;10:37-54.
  16. Ouwehand AC, Salminen S. In vitro adhesion assays for probiotics and their in vivo relevance: a review. Microb Ecol Health Dis 2003;15:175-84. https://doi.org/10.1080/08910600310019886
  17. Valeriano VD, Parungao-Balolong MM, Kang DK. In vitro evaluation of the mucin-adhesion ability and probiotic potential of Lactobacillus mucosae LM1. J Appl Microbiol 2014;117:485-97. https://doi.org/10.1111/jam.12539
  18. Bucki R, Namiot DB, Namiot Z, Savage PB, Janmey PA. Salivary mucins inhibit antibacterial activity of the cathelicidin-derived LL-37 peptide but not the cationic steroid CSA-13. J Antimicrob Chemother 2008;62:329-35. https://doi.org/10.1093/jac/dkn176
  19. Kim YS, Ho SB. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 2010; 12:319-30. https://doi.org/10.1007/s11894-010-0131-2
  20. Kober OI, Ahl D, Pin C, Holm L, Carding SR, Juge N. gammadelta T-cell-deficient mice show alterations in mucin expression, glycosylation, and goblet cells but maintain an intact mucus layer. Am J Physiol Gastrointest Liver Physiol 2014;306:G582-93. https://doi.org/10.1152/ajpgi.00218.2013
  21. Louis P, Scott KP, Duncan SH, Flint HJ. Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 2007;102:1197-208. https://doi.org/10.1111/j.1365-2672.2007.03322.x
  22. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 2002;217:133-9. https://doi.org/10.1111/j.1574-6968.2002.tb11467.x
  23. Gaudier E, Rival M, Buisine MP, Robineau I, Hoebler C. Butyrate enemas upregulate Muc genes expression but decrease adherent mucus thickness in mice colon. Physiol Res 2009;58:111-9.
  24. Hatayama H, Iwashita J, Kuwajima A, Abe T. The short chain fatty acid, butyrate, stimulates MUC2 mucin production in the human colon cancer cell line, LS174T. Biochem Biophys Res Commun 2007;356:599-603. https://doi.org/10.1016/j.bbrc.2007.03.025
  25. Barcelo A, Claustre J, Moro F, Chayvialle JA, Cuber JC, Plaisancie P. Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon. Gut 2000;46:218-24. https://doi.org/10.1136/gut.46.2.218
  26. Carraway KL, Ramsauer VP, Haq B, Carothers Carraway CA. Cell signaling through membrane mucins. Bioessays 2003;25:66-71. https://doi.org/10.1002/bies.10201
  27. Rangel JM, Sparling PH, Crowe C, Griffin PM, Swerdlow DL. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg Infect Dis 2005;11:603-9. https://doi.org/10.3201/eid1104.040739
  28. Deplancke B, Gaskins HR. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 2001;73: 1131S-1141S. https://doi.org/10.1093/ajcn/73.6.1131S
  29. Mack DR, Ahrne S, Hyde L, Wei S, Hollingsworth MA. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 2003;52:827-33. https://doi.org/10.1136/gut.52.6.827
  30. Fujiwara S, Hashiba H, Hirota T, Forstner JF. Proteinaceous factor(s) in culture supernatant fluids of bifidobacteria which prevents the binding of enterotoxigenic Escherichia coli to gangliotetraosylceramide. Appl Environ Microbiol 1997;63:506-12.
  31. Mattar AF, Teitelbaum DH, Drongowski RA, Yongyi F, Harmon CM, Coran AG. Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr Surg Int 2002;18:586-90. https://doi.org/10.1007/s00383-002-0855-7
  32. Adjei AA. Blocking oncogenic Ras signaling for cancer therapy. J Natl Cancer Inst 2001;93:1062-74. https://doi.org/10.1093/jnci/93.14.1062
  33. Wu KL, Huang EY, Jhu EW, Huang YH, Su WH, Chuang PC, Yang KD. Overexpression of galectin-3 enhances migration of colon cancer cells related to activation of the K-Ras-Raf-Erk1/2 pathway. J Gastroenterol 2013;48:350-9. https://doi.org/10.1007/s00535-012-0663-3
  34. Roux PP, Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 2004;68:320-44. https://doi.org/10.1128/MMBR.68.2.320-344.2004
  35. Holz MK, Ballif BA, Gygi SP, Blenis J. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 2005;123:569-80. https://doi.org/10.1016/j.cell.2005.10.024
  36. Reber L, Vermeulen L, Haegeman G, Frossard N. Ser276 phosphorylation of NF-${\kappa}B$ p65 by MSK1 controls SCF expression in inflammation. PLoS One 2009;4:e4393. https://doi.org/10.1371/journal.pone.0004393
  37. Gancz D, Lusthaus M, Fishelson Z. A role for the NF-kappaB pathway in cell protection from complement-dependent cytotoxicity. J Immunol 2012;189:860-6. https://doi.org/10.4049/jimmunol.1103451
  38. Daniel P, Filiz G, Brown DV, Hollande F, Gonzales M, D'Abaco G, Papalexis N, Phillips WA, Malaterre J, Ramsay RG, Mantamadiotis T. Selective CREB-dependent cyclin expression mediated by the PI3K and MAPK pathways supports glioma cell proliferation. Oncogenesis 2014;3:e108. https://doi.org/10.1038/oncsis.2014.21
  39. Lane DP. Cancer. p53, guardian of the genome. Nature 1992;358: 15-6. https://doi.org/10.1038/358015a0
  40. Horn HF, Vousden KH. Coping with stress: multiple ways to activate p53. Oncogene 2007;26:1306-16. https://doi.org/10.1038/sj.onc.1210263
  41. Williams EA, Coxhead JM, Mathers JC. Anti-cancer effects of butyrate: use of micro-array technology to investigate mechanisms. Proc Nutr Soc 2003;62:107-15. https://doi.org/10.1079/PNS2002230
  42. Wang HG, Huang XD, Shen P, Li LR, Xue HT, Ji GZ. Anticancer effects of sodium butyrate on hepatocellular carcinoma cells in vitro. Int J Mol Med 2013;31:967-74. https://doi.org/10.3892/ijmm.2013.1285
  43. Perrais M, Pigny P, Copin MC, Aubert JP, Van Seuningen I. Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signal-regulated kinase cascade and Sp1. J Biol Chem 2002;277: 32258-67. https://doi.org/10.1074/jbc.M204862200

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