Butyrate produced by gut commensal bacteria activates TGF-beta1 expression through the transcription factor SP1 in human intestinal epithelial cells

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Martin Gallausiaux, Camille ^a,b   Béguet Crespel, Fabienne ^a   Marinelli, Ludovica ^a,b   Jamet, Alexandre ^a   Ledue, Florence ^a   Blottière, Hervé M ^a   Lapaque, Nicolas ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID DERIVATIVE; CELL SURFACE RECEPTOR; FFAR3 PROTEIN, HUMAN; G PROTEIN COUPLED RECEPTOR; G-PROTEIN COUPLED RECEPTOR 43, HUMAN; HCAR2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SP1; TRANSFORMING GROWTH FACTOR BETA1;

CYTOLOGY; EPITHELIUM CELL; GENETICS; HT-29 CELL LINE; HUMAN; INTESTINE; INTESTINE FLORA; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

BUTYRATES; EPITHELIAL CELLS; GASTROINTESTINAL MICROBIOME; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; INTESTINES; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; SP1 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA1;

EID: 85049121297     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-28048-y     Document Type: Article

References (66)

1. Gaboriau-Routhiau, V. et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31, 677-689, https://doi.org/10.1016/j.immuni.2009.08.020 (2009).
2. Ivanov, I. I. et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498 (2009).
3. Atarashi, K. et al. Th17 Cell Induction by Adhesion of Microbes to Intestinal Epithelial Cells. Cell 163, 367-380, https://doi. org/10.1016/j.cell.2015.08.058 (2015).
4. Atarashi, K. et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331, 337-341 (2011).
5. Schilderink, R., Verseijden, C. &de Jonge, W. J. Dietary inhibitors of histone deacetylases in intestinal immunity and homeostasis. Frontiers in immunology 4, 226, https://doi.org/10.3389/fimmu.2013.00226 (2013).
6. Furusawa, Y. et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446-450, https://doi.org/10.1038/nature12721 (2013).
7. Smith, P. M. et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569-573, https://doi.org/10.1126/science.1241165 (2013).
8. Arpaia, N. et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504, 451-455, https://doi.org/10.1038/nature12726 (2013).
9. Kashiwagi, I. et al. Smad2 and Smad3 Inversely Regulate TGF-beta Autoinduction in Clostridium butyricum-Activated Dendritic Cells. Immunity 43, 65-79, https://doi.org/10.1016/j.immuni.2015.06.010 (2015).
10. Frank, D. N. et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proceedings of the National Academy of Sciences of the United States of America 104, 13780-13785 (2007).
11. Sokol, H. et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proceedings of the National Academy of Sciences of the United States of America 105, 16731-16736 (2008).
12. Sokol, H. et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflammatory bowel diseases 15, 1183-1189 (2009).
13. Marafini, I., Zorzi, F., Codazza, S., Pallone, F. &Monteleone, G. TGF-Beta signaling manipulation as potential therapy for IBD. Curr Drug Targets 14, 1400-1404 (2013).
14. Ardizzone, S., Bevivino, G. &Monteleone, G. Mongersen, an oral Smad7 antisense oligonucleotide, in patients with active Crohn's disease. Therap Adv Gastroenterol 9, 527-532, https://doi.org/10.1177/1756283X16636781 (2016).
15. Monteleone, G. et al. Blocking Smad7 restores TGF-beta1 signaling in chronic inflammatory bowel disease. The Journal of clinical investigation 108, 601-609, https://doi.org/10.1172/JCI12821 (2001).
16. Andoh, A. et al. Faecal microbiota profile of Crohn's disease determined by terminal restriction fragment length polymorphism analysis. Aliment Pharmacol Ther 29, 75-82 (2009).
17. Iliev, I. D., Mileti, E., Matteoli, G., Chieppa, M. &Rescigno, M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal immunology 2, 340-350 (2009).
18. Iliev, I. D. et al. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 58, 1481-1489 (2009).
19. Di Sabatino, A. et al. Blockade of transforming growth factor beta upregulates T-box transcription factor T-bet, and increases T helper cell type 1 cytokine and matrix metalloproteinase-3 production in the human gut mucosa. Gut 57, 605-612, https://doi. org/10.1136/gut.2007.130922 (2008).
20. Geuking, M. B. et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34, 794-806 (2011).
21. Atarashi, K. et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500, 232-236, https://doi.org/10.1038/nature12331 (2013).
22. Li, M. O. &Flavell, R. A. TGF-beta: a master of all T cell trades. Cell 134, 392-404, https://doi.org/10.1016/j.cell.2008.07.025 (2008).
23. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65 (2010).
24. Mazmanian, S. K., Round, J. L. &Kasper, D. L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453, 620-625 (2008).
25. Lakhdari O. et al. Functional metagenomics: a high throughput screening method to decipher microbiota-driven NF-kappaB modulation in the human gut. PloS one 5 (2010)
26. Cohen, L. J. et al. Functional metagenomic discovery of bacterial effectors in the human microbiome and isolation of commendamide, a GPCR G2A/132 agonist. Proceedings of the National Academy of Sciences of the United States of America 112, E4825-4834, https://doi.org/10.1073/pnas.1508737112 (2015).
27. Vital, M., Howe, A. C. &Tiedje, J. M. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. mBio 5, e00889, https://doi.org/10.1128/mBio.00889-14 (2014).
28. Le Poul, E. et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. The Journal of biological chemistry 278, 25481-25489, https://doi.org/10.1074/jbc.M301403200 (2003).
29. Brown, A. J. et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. The Journal of biological chemistry 278, 11312-11319, https://doi.org/10.1074/jbc.M211609200 (2003).
30. Thangaraju, M. et al. GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res 69, 2826-2832, https://doi.org/10.1158/0008-5472.CAN-08-4466 (2009).
31. Cuff, M., Dyer, J., Jones, M. &Shirazi-Beechey, S. The human colonic monocarboxylate transporter Isoform 1: its potential importance to colonic tissue homeostasis. Gastroenterology 128, 676-686 (2005).
32. Thibault, R. et al. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflammatory bowel diseases 16, 684-695, https://doi.org/10.1002/ibd.21108 (2010).
33. Dokmanovic, M., Clarke, C. &Marks, P. A. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 5, 981-989, https://doi.org/10.1158/1541-7786.MCR-07-0324 (2007).
34. Candido, E. P., Reeves, R. &Davie, J. R. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 14, 105-113 (1978).
35. Sealy, L. &Chalkley, R. The effect of sodium butyrate on histone modification. Cell 14, 115-121 (1978).
36. Gallinari, P., Di Marco, S., Jones, P., Pallaoro, M. &Steinkuhler, C. HDACs, histone deacetylation and gene transcription: from molecular biology to cancer therapeutics. Cell Res 17, 195-211, https://doi.org/10.1038/sj.cr.7310149 (2007).
37. Kim, S. J. et al. Activation of the second promoter of the transforming growth factor-beta 1 gene by transforming growth factor-beta 1 and phorbol ester occurs through the same target sequences. The Journal of biological chemistry 264, 19373-19378 (1989).
38. Kim, S. J., Glick, A., Sporn, M. B. &Roberts, A. B. Characterization of the promoter region of the human transforming growth factor-beta 1 gene. The Journal of biological chemistry 264, 402-408 (1989).
39. Geiser, A. G. et al. Regulation of the transforming growth factor-beta 1 and-beta 3 promoters by transcription factor Sp1. Gene 129, 223-228 (1993).
40. Davie, J. R. Inhibition of histone deacetylase activity by butyrate. J Nutr 133, 2485S-2493S (2003).
41. Nakano, K. et al. Butyrate activates the WAF1/Cip1 gene promoter through Sp1 sites in a p53-negative human colon cancer cell line. The Journal of biological chemistry 272, 22199-22206 (1997).
42. Nepelska, M. et al. Butyrate produced by commensal bacteria potentiates phorbol esters induced AP-1 response in human intestinal epithelial cells. PloS one 7, e52869, https://doi.org/10.1371/journal.pone.0052869 (2012).
43. Yu, D. C., Waby, J. S., Chirakkal, H., Staton, C. A. &Corfe, B. M. Butyrate suppresses expression of neuropilin I in colorectal cell lines through inhibition of Sp1 transactivation. Mol Cancer 9, 276, https://doi.org/10.1186/1476-4598-9-276 (2010).
44. Thakur, B. K., Dasgupta, N., Ta, A. &Das, S. Physiological TLR5 expression in the intestine is regulated by differential DNA binding of Sp1/Sp3 through simultaneous Sp1 dephosphorylation and Sp3 phosphorylation by two different PKC isoforms. Nucleic Acids Res 44, 5658-5672, https://doi.org/10.1093/nar/gkw189 (2016).
45. Inan, M. S. et al. The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line. Gastroenterology 118, 724-734 (2000).
46. Weigert, C. et al. AP-1 proteins mediate hyperglycemia-induced activation of the human TGF-beta1 promoter in mesangial cells. J Am Soc Nephrol 11, 2007-2016 (2000).
47. Presser, L. D., McRae, S. &Waris, G. Activation of TGF-beta1 promoter by hepatitis C virus-induced AP-1 and Sp1: role of TGFbeta1 in hepatic stellate cell activation and invasion. PloS one 8, e56367, https://doi.org/10.1371/journal.pone.0056367 (2013).
48. Lee, K. Y. et al. NF-kappaB and activator protein 1 response elements and the role of histone modifications in IL-1beta-induced TGF-beta1 gene transcription. Journal of immunology 176, 603-615 (2006).
49. Weiss, A. &Attisano, L. The TGFbeta superfamily signaling pathway. Wiley Interdiscip Rev Dev Biol 2, 47-63, https://doi. org/10.1002/wdev.86 (2013).
50. Ihara, S., Hirata, Y. &Koike, K. TGF-beta in inflammatory bowel disease: a key regulator of immune cells, epithelium, and the intestinal microbiota. J Gastroenterol, https://doi.org/10.1007/s00535-017-1350-1 (2017).
51. Lees, C. W., Barrett, J. C., Parkes, M. &Satsangi, J. New IBD genetics: common pathways with other diseases. Gut 60, 1739-1753, https://doi.org/10.1136/gut.2009.199679 (2011).
52. Kagnoff, M. F. The intestinal epithelium is an integral component of a communications network. The Journal of clinical investigation 124, 2841-2843, https://doi.org/10.1172/JCI75225 (2014).
53. Staiano-Coico, L. et al. TGF-alpha and TGF-beta expression during sodium-N-butyrate-induced differentiation of human keratinocytes: evidence for subpopulation-specific up-regulation of TGF-beta mRNA in suprabasal cells. Exp Cell Res 191, 286-291 (1990).
54. Nathan, D. F., Burkhart, S. R. &Morin, M. J. Increased cell surface EGF receptor expression during the butyrate-induced differentiation of human HCT-116 colon tumor cell clones. Exp Cell Res 190, 76-84 (1990).
55. Schroder, O., Hess, S., Caspary, W. F. &Stein, J. Mediation of differentiating effects of butyrate on the intestinal cell line Caco-2 by transforming growth factor-beta 1. Eur J Nutr 38, 45-50 (1999).
56. Gill, R. K. et al. Expression and membrane localization of MCT isoforms along the length of the human intestine. Am J Physiol Cell Physiol 289, C846-852, https://doi.org/10.1152/ajpcell.00112.2005 (2005).
57. Hadjiagapiou, C., Schmidt, L., Dudeja, P. K., Layden, T. J. &Ramaswamy, K. Mechanism(s) of butyrate transport in Caco-2 cells: role of monocarboxylate transporter 1. American journal of physiology. Gastrointestinal and liver physiology 279, G775-780 (2000).
58. Hinnebusch, B. F., Meng, S., Wu, J. T., Archer, S. Y. &Hodin, R. A. The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 132, 1012-1017 (2002).
59. Birchenall-Roberts, M. C. et al. Transcriptional regulation of the transforming growth factor beta 1 promoter by v-src gene products is mediated through the AP-1 complex. Mol Cell Biol 10, 4978-4983 (1990).
60. Round, J. L. et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332, 974-977 (2011).
61. Round, J. L. &Mazmanian, S. K. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proceedings of the National Academy of Sciences of the United States of America 107, 12204-12209 (2010).
62. Hungate, R. E. The anaerobic mesophilic cellulolytic bacteria. Bacteriol Rev 14, 1-49 (1950).
63. Lakhdari, O. et al. Identification of NF-kappaB modulation capabilities within human intestinal commensal bacteria. Journal of biomedicine &biotechnology 2011, 282356, https://doi.org/10.1155/2011/282356 (2011).
64. Bourriaud, C. et al. Lactate is mainly fermented to butyrate by human intestinal microfloras but inter-individual variation is evident. J Appl Microbiol 99, 201-212, https://doi.org/10.1111/j.1365-2672.2005.02605.x (2005).
65. Derynck, R. et al. Human transforming growth factor-beta complementary DNA sequence and expression in normal and transformed cells. Nature 316, 701-705 (1985).
66. Shah, R., Rahaman, B., Hurley, C. K. &Posch, P. E. Allelic diversity in the TGFB1 regulatory region: characterization of novel functional single nucleotide polymorphisms. Hum Genet 119, 61-74, https://doi.org/10.1007/s00439-005-0112-y (2006).