Redirection of epithelial immune responses by short-chain fatty acids through inhibition of histone deacetylases

Frontiers in Immunology

Volumn 6, Issue NOV, 2015, Pages

  Lin, May Young ^a   De Zoete, Marcel R ^a   Van Putten, Jos P M ^a   Strijbis, Karin ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Butyrate; Flagellin; HDAC; Histone acetylation; NF B; SCFAs; TLR5; Toll like receptors

Indexed keywords

BUTYRIC ACID; FLAGELLIN; HISTONE DEACETYLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; LUCIFERASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROPIONIC ACID; SHORT CHAIN FATTY ACID; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 9; TRICHOSTATIN A; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; EPIGENETICS; EPITHELIUM CELL; GENE EXPRESSION; GENETIC TRANSFECTION; HISTONE ACETYLATION; HOST CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLAMMATION; INTRACELLULAR SIGNALING; LUCIFERASE ASSAY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RNA ISOLATION; WESTERN BLOTTING;

EID: 84949547309     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00554     Document Type: Article

References (47)

1. Mayer EA, Savidge T, Shulman RJ. Brain-gut microbiome interactions and functional bowel disorders. Gastroenterology (2014) 146:1500-12. doi: 10.1053/j.gastro.2014.02.037.
2. Macfarlane GT, Gibson GR, Cummings JH. Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol (1992) 72:57-64. doi:10.1111/j.1365-2672.1992.tb05187.x.
3. Cook SI, Sellin JH. Review article: short chain fatty acids in health and disease. Aliment Pharmacol Ther (1998) 12:499-507. doi:10.1046/j.1365-2036.1998.00337.x.
4. Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc (2003) 62:67-72. doi:10.1079/PNS2002207.
5. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut (1987) 28:1221-7. doi:10.1136/gut.28.10.1221.
6. 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.
7. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, et al. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell (2014) 156:84-96. doi:10.1016/j.cell.2013.12.016.
8. Scheppach W, Sommer H, Kirchner T, Paganelli GM, Bartram P, Christl S, et al. Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology (1992) 103:51-6.
9. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature (2009) 461:1282-6. doi:10.1038/nature08530.
10. Heerdt BG, Houston MA, Augenlicht LH. Potentiation by specific short-chain fatty acids of differentiation and apoptosis in human colonic carcinoma cell lines. Cancer Res (1994) 54:3288-93.
11. Bocker U, Nebe T, Herweck F, Holt L, Panja A, Jobin C, et al. Butyrate modulates intestinal epithelial cell-mediated neutrophil migration. Clin Exp Immunol (2003) 131:53-60. doi:10.1046/j.1365-2249.2003.02056.x.
12. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol (2010) 10:131-44. doi:10.1038/nri2707.
13. Cario E, Podolsky DK. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun (2000) 68:7010-7. doi:10.1128/IAI.68.12.7010-7017.2000.
14. Cullender TC, Chassaing B, Janzon A, Kumar K, Muller CE, Werner JJ, et al. Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host Microbe (2013) 14:571-81. doi:10.1016/j.chom.2013.10.009.
15. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol (2010) 11:373-84. doi:10.1038/ni.1863.
16. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell (2010) 140:805-20. doi:10.1016/j.cell.2010.01.022.
17. Rodriguez MS, Thompson J, Hay RT, Dargemont C. Nuclear retention of IkappaBalpha protects it from signal-induced degradation and inhibits nuclear factor kappaB transcriptional activation. J Biol Chem (1999) 274:9108-15. doi:10.1074/jbc.274.13.9108.
18. Keestra AM, De Zoete MR, Van Aubel RA, Van Putten JP. Functional characterization of chicken TLR5 reveals species-specific recognition of flagellin. Mol Immunol (2008) 45:1298-307. doi:10.1016/j.molimm.2007.09.013.
19. Keestra AM, De Zoete MR, Van Aubel RA, Van Putten JP. The central leucine-rich repeat region of chicken TLR16 dictates unique ligand specificity and species-specific interaction with TLR2. J Immunol (2007) 178:7110-9. doi:10.4049/jimmunol.178.11.7110.
20. van Aubel RA, Keestra AM, Krooshoop DJ, Van Eden W, Van Putten JP. Ligand-induced differential cross-regulation of toll-like receptors 2, 4 and 5 in intestinal epithelial cells. Mol Immunol (2007) 44:3702-14. doi:10.1016/j.molimm.2007.04.001.
21. Wosten MM, Van Dijk L, Parker CT, Guilhabert MR, Van Der Meer-Janssen YP, Wagenaar JA, et al. Growth phase-dependent activation of the DccRS regulon of Campylobacter jejuni. J Bacteriol (2010) 192:2729-36. doi:10.1128/JB.00024-10.
22. Barton GM, Kagan JC. A cell biological view of toll-like receptor function: regulation through compartmentalization. Nat Rev Immunol (2009) 9:535-42. doi:10.1038/nri2587.
23. Keestra AM, De Zoete MR, Bouwman LI, Van Putten JP. Chicken TLR21 is an innate CpG DNA receptor distinct from mammalian TLR9. J Immunol (2010) 185:460-7. doi:10.4049/jimmunol.0901921.
24. Boffa LC, Vidali G, Mann RS, Allfrey VG. Suppression of histone deacetylation in vivo and in vitro by sodium butyrate. J Biol Chem (1978) 253:3364-6.
25. Candido EP, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell (1978) 14:105-13. doi:10.1016/0092-8674(78)90305-7.
26. Sealy L, Chalkley R. The effect of sodium butyrate on histone modification. Cell (1978) 14:115-21. doi:10.1016/0092-8674(78)90306-9.
27. Shakespear MR, Halili MA, Irvine KM, Fairlie DP, Sweet MJ. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol (2011) 32:335-43. doi:10.1016/j.it.2011.04.001.
28. Cousens LS, Gallwitz D, Alberts BM. Different accessibilities in chromatin to histone acetylase. J Biol Chem (1979) 254:1716-23.
29. Finnin MS, Donigian JR, Cohen A, Richon VM, Rifkind RA, Marks PA, et al. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature (1999) 401:188-93. doi:10.1038/43710.
30. Davie JR. Inhibition of histone deacetylase activity by butyrate. J Nutr (2003) 133:2485S-93S.
31. Van Lint C, Emiliani S, Verdin E. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr (1996) 5:245-53.
32. Mariadason JM, Corner GA, Augenlicht LH. Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer. Cancer Res (2000) 60:4561-72.
33. Kruh J. Effects of sodium butyrate, a new pharmacological agent, on cells in culture. Mol Cell Biochem (1982) 42:65-82.
34. Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA. The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr (2002) 132:1012-7.
35. Falkenberg KJ, Johnstone RW. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat Rev Drug Discov (2014) 13:673-91. doi:10.1038/nrd4360.
36. Deng WG, Zhu Y, Wu KK. Role of p300 and PCAF in regulating cyclooxygenase-2 promoter activation by inflammatory mediators. Blood (2004) 103:2135-42. doi:10.1182/blood-2003-09-3131.
37. Lu J, Sun H, Wang X, Liu C, Xu X, Li F, et al. Interleukin-12 p40 promoter activity is regulated by the reversible acetylation mediated by HDAC1 and p300. Cytokine (2005) 31:46-51. doi:10.1016/j.cyto.2005.03.001.
38. Nusinzon I, Horvath CM. Positive and negative regulation of the innate antiviral response and beta interferon gene expression by deacetylation. Mol Cell Biol (2006) 26:3106-13. doi:10.1128/MCB.26.8.3106-3113.2006.
39. Gilchrist M, Thorsson V, Li B, Rust AG, Korb M, Roach JC, et al. Systems biology approaches identify ATF3 as a negative regulator of toll-like receptor 4. Nature (2006) 441:173-8. doi:10.1038/nature04768.
40. Pakala SB, Bui-Nguyen TM, Reddy SD, Li DQ, Peng S, Rayala SK, et al. Regulation of NF-kappaB circuitry by a component of the nucleosome remodeling and deacetylase complex controls inflammatory response homeostasis. J Biol Chem (2010) 285:23590-7. doi:10.1074/jbc. M110.139469.
41. Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science (2001) 293:1653-7. doi:10.1126/science.1062374.
42. Zhou Q, Dalgard CL, Wynder C, Doughty ML. Histone deacetylase inhibitors SAHA and sodium butyrate block G1-to-S cell cycle progression in neurosphere formation by adult subventricular cells. BMC Neurosci (2011) 12:50. doi:10.1186/1471-2202-12-50.
43. Ma P, Schultz RM. Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol (2008) 319:110-20. doi:10.1016/j.ydbio.2008.04.011.
44. Vaquero A, Sternglanz R, Reinberg D. NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs. Oncogene (2007) 26:5505-20. doi:10.1038/sj.onc.1210617.
45. Fusunyan RD, Quinn JJ, Ohno Y, Macdermott RP, Sanderson IR. Butyrate enhances interleukin (IL)-8 secretion by intestinal epithelial cells in response to IL-1beta and lipopolysaccharide. Pediatr Res (1998) 43:84-90. doi:10.1203/00006450-199804001-00501.
46. Vinolo MA, Rodrigues HG, Nachbar RT, Curi R. Regulation of inflammation by short chain fatty acids. Nutrients (2011) 3:858-76. doi:10.3390/nu3100858.
47. Segain JP, Raingeard De La Bletiere D, Bourreille A, Leray V, Gervois N, Rosales C, et al. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut (2000) 47:397-403. doi:10.1136/gut.47.3.397.