Regulation of inflammation by short chain fatty acids

Nutrients

Volumn 3, Issue 10, 2011, Pages 858-876

  Vinolo, Marco A R ^a   Rodrigues, Hosana G ^a   Nachbar, Renato T ^a   Curi, Rui ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Acetate; Butyrate; Inflammation; Leukocytes; Neutrophils; Propionate; Short chain fatty acids

Indexed keywords

ACETIC ACID; BUTYRIC ACID; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT 2; ELECTROLYTE; ENEMA; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 41; G PROTEIN COUPLED RECEPTOR 43; HISTONE DEACETYLASE; ICOSANOID; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 6; MESALAZINE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROPIONIC ACID; PROSTAGLANDIN E2; SHORT CHAIN FATTY ACID; TRICHOSTATIN A; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; WATER;

ACUTE LUNG INJURY; ANAEROBIC BACTERIUM; ANAEROBIC FERMENTATION; ANTIINFLAMMATORY ACTIVITY; BACTERIAL METABOLISM; CELL ISOLATION; CYTOKINE PRODUCTION; DIET SUPPLEMENTATION; DRUG DOSE COMPARISON; ELECTROLYTE TRANSPORT; ENDOTHELIUM CELL; ENTERITIS; ENZYME INHIBITION; GASTROINTESTINAL ABSORPTION; HUMAN; IMMUNE RESPONSE; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; ISCHEMIA; LEUKOCYTE; LEUKOCYTE ACTIVATION; LEUKOCYTE FUNCTION; LEUKOCYTE MIGRATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROSTAGLANDIN SYNTHESIS INHIBITION; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REVIEW; SEPSIS; WATER ABSORPTION;

EID: 80054980812     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu3100858     Document Type: Review

References (101)

1. O'Hara, A.M.; Shanahan, F. The gut flora as a forgotten organ. EMBO Rep. 2006, 7, 688-693.
2. Heijtz, R.D.; Wang, S.; Anuar, F.; Qian, Y.; Bjorkholm, B.; Samuelsson, A.; Hibberd, M.L.; Forssberg, H.; Pettersson, S. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. USA 2011, 108, 3047-3052.
3. Vijay-Kumar, M.; Aitken, J.D.; Carvalho, F.A.; Cullender, T.C.; Mwangi, S.; Srinivasan, S.; Sitaraman, S.V.; Knight, R.; Ley, R.E.; Gewirtz, A.T. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 2010, 328, 228-231.
4. Maslowski, K.M.; Vieira, A.T.; Ng, A.; Kranich, J.; Sierro, F.; Yu, D.; Schilter, H.C.; Rolph, M.S.; Mackay, F.; Artis, D. et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461, 1282-1286.
5. Uronis, J.M.; Muhlbauer, M.; Herfarth, H.H.; Rubinas, T.C.; Jones, G.S.; Jobin, C. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS One 2009, 4, e6026.
6. De Filippo, C.; Cavalieri, D.; Di Paola, M.; Ramazzotti, M.; Poullet, J.B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 2010, 107, 14691-14696.
7. Cani, P.D.; Amar, J.; Iglesias, M.A.; Poggi, M.; Knauf, C.; Bastelica, D.; Neyrinck, A.M.; Fava, F.; Tuohy, K.M.; Chabo, C. et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007, 56, 1761-1772.
8. Atarashi, K.; Nishimura, J.; Shima, T.; Umesaki, Y.; Yamamoto, M.; Onoue, M.; Yagita, H.; Ishii, N.; Evans, R.; Honda, K. et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008, 455, 808-812.
9. Huda-Faujan, N.; Abdulamir, A.S.; Fatimah, A.B.; Anas, O.M.; Shuhaimi, M.; Yazid, A.M.; Loong, Y.Y. The impact of the level of the intestinal short chain Fatty acids in inflammatory bowel disease patients versus healthy subjects. Open Biochem. J. 2010, 4, 53-58.
10. Vernia, P.; Caprilli, R.; Latella, G.; Barbetti, F.; Magliocca, F.M.; Cittadini, M. Fecal lactate and ulcerative colitis. Gastroenterology 1988, 95, 1564-1568.
11. Murphy, E.F.; Cotter, P.D.; Healy, S.; Marques, T.M.; O'Sullivan, O.; Fouhy, F.; Clarke, S.F.; O'Toole, P.W.; Quigley, E.M.; Stanton, C. et al. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 2010, 59, 1635-1642.
12. McIntyre, A.; Gibson, P.R.; Young, G.P. Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut 1993, 34, 386-391.
13. Schwiertz, A.; Taras, D.; Schafer, K.; Beijer, S.; Bos, N.A.; Donus, C.; Hardt, P.D. Microbiota and SCFA in lean and overweight healthy subjects. Obesity 2010, 18, 190-195.
14. Cummings, J.H.; Pomare, E.W.; Branch, W.J.; Naylor, C.P.; Macfarlane, G.T. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 1987, 28, 1221-1227.
15. McNeil, N.I. The contribution of the large intestine to energy supplies in man. Am. J. Clin. Nutr. 1984, 39, 338-342.
16. Zaibi, M.S.; Stocker, C.J.; O'Dowd, J.; Davies, A.; Bellahcene, M.; Cawthorne, M.A.; Brown, A.J.; Smith, D.M.; Arch, J.R. Roles of GPR41 and GPR43 in leptin secretory responses of murine adipocytes to short chain fatty acids. FEBS Lett. 2010, 584, 2381-2386.
17. Plaisancie, P.; Dumoulin, V.; Chayvialle, J.A.; Cuber, J.C. Luminal peptide YY-releasing factors in the isolated vascularly perfused rat colon. J. Endocrinol. 1996, 151, 421-429.
18. Vinolo, M.A.; Rodrigues, H.G.; Hatanaka, E.; Sato, F.T.; Sampaio, S.C.; Curi, R. Suppressive effect of short-chain fatty acids on production of proinflammatory mediators by neutrophils. J. Nutr. Biochem. 2011, 22, 849-855.
19. Luster, A.D.; Alon, R.; von Andrian, U.H. Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 2005, 6, 1182-1190.
20. Vinolo, M.A.; Rodrigues, H.G.; Hatanaka, E.; Hebeda, C.B.; Farsky, S.H.; Curi, R. Short-chain fatty acids stimulate the migration of neutrophils to inflammatory sites. Clin. Sci. 2009, 117, 331-338.
21. Vinolo, M.A.; Rodrigues, H.G.; Hatanaka, E.; Sato, F.T.; Sampaio, S.C.; Curi, R. Suppressive effect of short chain fatty acids on production of proinflammatory mediators by neutrophils. J. Nutr. Biochem. 2011, 22, 849-855.
22. Le Poul, E.; Loison, C.; Struyf, S.; Springael, J.Y.; Lannoy, V.; Decobecq, M.E.; Brezillon, S.; Dupriez, V.; Vassart, G.; Van Damme, J. et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J. Biol. Chem. 2003, 278, 25481-25489.
23. Park, J.S.; Lee, E.J.; Lee, J.C.; Kim, W.K.; Kim, H.S. Anti-inflammatory effects of short chain fatty acids in IFN-gamma-stimulated RAW 264.7 murine macrophage cells: Involvement of NF-kappaB and ERK signaling pathways. Int. Immunopharmacol. 2007, 7, 70-77.
24. Sina, C.; Gavrilova, O.; Forster, M.; Till, A.; Derer, S.; Hildebrand, F.; Raabe, B.; Chalaris, A.; Scheller, J.; Rehmann, A. et al. G protein-coupled receptor 43 is essential for neutrophil recruitment during intestinal inflammation. J. Immunol. 2009, 183, 7514-7522.
25. Vinolo, M.A.; Ferguson, G.J.; Kulkarni, S.; Damoulakis, G.; Anderson, K.; Bohlooly, Y.M.; Stephens, L.; Hawkins, P.T.; Curi, R. SCFAs Induce Mouse Neutrophil Chemotaxis through the GPR43 Receptor. PLoS One 2011, 6, e21205.
26. Brown, A.J.; Goldsworthy, S.M.; Barnes, A.A.; Eilert, M.M.; Tcheang, L.; Daniels, D.; Muir, A.I.; Wigglesworth, M.J.; Kinghorn, I.; Fraser, N.J. et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J. Biol. Chem. 2003, 278, 11312-11319.
27. Nilsson, N.E.; Kotarsky, K.; Owman, C.; Olde, B. Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids. Biochem. Biophys. Res. Commun. 2003, 303, 1047-1052.
28. Itoh, Y.; Kawamata, Y.; Harada, M.; Kobayashi, M.; Fujii, R.; Fukusumi, S.; Ogi, K.; Hosoya, M.; Tanaka, Y.; Uejima, H. et al. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 2003, 422, 173-176.
29. Maa, M.C.; Chang, M.Y.; Hsieh, M.Y.; Chen, Y.J.; Yang, C.J.; Chen, Z.C.; Li, Y.K.; Yen, C.K.; Wu, R.R.; Leu, T.H. Butyrate reduced lipopolysaccharide-mediated macrophage migration by suppression of Src enhancement and focal adhesion kinase activity. J. Nutr. Biochem. 2010, 21, 1186-1192.
30. Owen, K.A.; Pixley, F.J.; Thomas, K.S.; Vicente-Manzanares, M.; Ray, B.J.; Horwitz, A.F.; Parsons, J.T.; Beggs, H.E.; Stanley, E.R.; Bouton, A.H. Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J. Cell Biol. 2007, 179, 1275-1287.
31. Zapolska-Downar, D.; Naruszewicz, M. Propionate reduces the cytokine-induced VCAM-1 and ICAM-1 expression by inhibiting nuclear factor-kappa B (NF-kappaB) activation. J. Physiol. Pharmacol. 2009, 60, 123-131.
32. Zapolska-Downar, D.; Siennicka, A.; Kaczmarczyk, M.; Kolodziej, B.; Naruszewicz, M. Butyrate inhibits cytokine-induced VCAM-1 and ICAM-1 expression in cultured endothelial cells: The role of NF-kappaB and PPARalpha. J. Nutr. Biochem. 2004, 15, 220-228.
33. Miller, S.J.; Zaloga, G.P.; Hoggatt, A.M.; Labarrere, C.; Faulk, W.P. Short-chain fatty acids modulate gene expression for vascular endothelial cell adhesion molecules. Nutrition 2005, 21, 740-748.
34. Cox, M.A.; Jackson, J.; Stanton, M.; Rojas-Triana, A.; Bober, L.; Laverty, M.; Yang, X.; Zhu, F.; Liu, J.; Wang, S. et al. Short-chain fatty acids act as antiinflammatory mediators by regulating prostaglandin E(2) and cytokines. World J. Gastroenterol. 2009, 15, 5549-5557.
35. Blais, M.; Seidman, E.G.; Asselin, C. Dual effect of butyrate on IL-1beta-mediated intestinal epithelial cell inflammatory response. DNA Cell Biol. 2007, 26, 133-147.
36. Leung, C.H.; Lam, W.; Ma, D.L.; Gullen, E.A.; Cheng, Y.C. Butyrate mediates nucleotide-binding and oligomerisation domain (NOD) 2-dependent mucosal immune responses against peptidoglycan. Eur. J. Immunol. 2009, 39, 3529-3537.
37. Bocker, U.; Nebe, T.; Herweck, F.; Holt, L.; Panja, A.; Jobin, C.; Rossol, S.; Sartor, R.B.; Singer, M.V. Butyrate modulates intestinal epithelial cell-mediated neutrophil migration. Clin. Exp. Immunol. 2003, 131, 53-60.
38. Fusunyan, R.D.; Quinn, J.J.; Fujimoto, M.; MacDermott, R.P.; Sanderson, I.R. Butyrate switches the pattern of chemokine secretion by intestinal epithelial cells through histone acetylation. Mol. Med. 1999, 5, 631-640.
39. Inatomi, O.; Andoh, A.; Kitamura, K.; Yasui, H.; Zhang, Z.; Fujiyama, Y. Butyrate blocks interferon-gamma-inducible protein-10 release in human intestinal subepithelial myofibroblasts. J. Gastroenterol. 2005, 40, 483-489.
40. Menzel, T.; Luhrs, H.; Zirlik, S.; Schauber, J.; Kudlich, T.; Gerke, T.; Gostner, A.; Neumann, M.; Melcher, R.; Scheppach, W. Butyrate inhibits leukocyte adhesion to endothelial cells via modulation of VCAM-1. Inflamm. Bowel Dis. 2004, 10, 122-128.
41. Bohmig, G.A.; Krieger, P.M.; Saemann, M.D.; Wenhardt, C.; Pohanka, E.; Zlabinger, G.J. n-Butyrate downregulates the stimulatory function of peripheral blood-derived antigen-presenting cells: A potential mechanism for modulating T-cell responses by short-chain fatty acids. Immunology 1997, 92, 234-243.
42. Dianzani, C.; Cavalli, R.; Zara, G.P.; Gallicchio, M.; Lombardi, G.; Gasco, M.R.; Panzanelli, P.; Fantozzi, R. Cholesteryl butyrate solid lipid nanoparticles inhibit adhesion of human neutrophils to endothelial cells. Br. J. Pharmacol. 2006, 148, 648-656.
43. Allport, J.R.; Ding, H.T.; Ager, A.; Steeber, D.A.; Tedder, T.F.; Luscinskas, F.W. L-selectin shedding does not regulate human neutrophil attachment, rolling, or transmigration across human vascular endothelium in vitro. J. Immunol. 1997, 158, 4365-4372.
44. Olefsky, J.M.; Glass, C.K. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 2010, 72, 219-246.
45. Kinne, R.W.; Brauer, R.; Stuhlmuller, B.; Palombo-Kinne, E.; Burmester, G.R. Macrophages in rheumatoid arthritis. Arthritis Res. 2000, 2, 189-202.
46. Griffin, W.S. Inflammation and neurodegenerative diseases. Am. J. Clin. Nutr. 2006, 83, 470S-474S.
47. Boyle, JJ. Macrophage activation in atherosclerosis: Pathogenesis and pharmacology of plaque rupture. Curr. Vasc. Pharmacol. 2005, 3, 63-68.
48. Chakravortty, D.; Koide, N.; Kato, Y.; Sugiyama, T.; Mu, M.M.; Yoshida, T.; Yokochi, T. The inhibitory action of butyrate on lipopolysaccharide-induced nitric oxide production in RAW 264.7 murine macrophage cells. J. Endotoxin Res. 2000, 6, 243-247.
49. Usami, M.; Kishimoto, K.; Ohata, A.; Miyoshi, M.; Aoyama, M.; Fueda, Y.; Kotani, J. Butyrate and trichostatin A attenuate nuclear factor kappaB activation and tumor necrosis factor alpha secretion and increase prostaglandin E2 secretion in human peripheral blood mononuclear cells. Nutr. Res. 2008, 28, 321-328.
50. Fukae, J.; Amasaki, Y.; Yamashita, Y.; Bohgaki, T.; Yasuda, S.; Jodo, S.; Atsumi, T.; Koike, T. Butyrate suppresses tumor necrosis factor alpha production by regulating specific messenger RNA degradation mediated through a cis-acting AU-rich element. Arthritis Rheum. 2005, 52, 2697-2707.
51. Saemann, M.D.; Bohmig, G.A.; Osterreicher, C.H.; Burtscher, H.; Parolini, O.; Diakos, C.; Stockl, J.; Horl, W.H.; Zlabinger, G.J. Anti-inflammatory effects of sodium butyrate on human monocytes: Potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J. 2000, 14, 2380-2382.
52. Huuskonen, J.; Suuronen, T.; Nuutinen, T.; Kyrylenko, S.; Salminen, A. Regulation of microglial inflammatory response by sodium butyrate and short-chain fatty acids. Br. J. Pharmacol. 2004, 141, 874-880.
53. Park, J.S.; Woo, M.S.; Kim, S.Y.; Kim, W.K.; Kim, H.S. Repression of interferon-gamma-induced inducible nitric oxide synthase (iNOS) gene expression in microglia by sodium butyrate is mediated through specific inhibition of ERK signaling pathways. J. Neuroimmunol. 2005, 168, 56-64.
54. Chen, P.S.; Wang, C.C.; Bortner, C.D.; Peng, G.S.; Wu, X.; Pang, H.; Lu, R.B.; Gean, P.W.; Chuang, D.M.; Hong, J.S. Valproic acid and other histone deacetylase inhibitors induce microglial apoptosis and attenuate lipopolysaccharide-induced dopaminergic neurotoxicity. Neuroscience 2007, 149, 203-212.
55. Perez, R.; Stevenson, F.; Johnson, J.; Morgan, M.; Erickson, K.; Hubbard, N.E.; Morand, L.; Rudich, S.; Katznelson, S.; German, J.B. Sodium butyrate upregulates Kupffer cell PGE2 production and modulates immune function. J. Surg. Res. 1998, 78, 1-6.
56. Waldecker, M.; Kautenburger, T.; Daumann, H.; Busch, C.; Schrenk, D. Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J. Nutr. Biochem. 2008, 19, 587-593.
57. Glozak, M.A.; Sengupta, N.; Zhang, X.; Seto, E. Acetylation and deacetylation of non-histone proteins. Gene 2005, 363, 15-23.
58. Cox, H.M.; Tough, I.R.; Woolston, A.M.; Zhang, L.; Nguyen, A.D.; Sainsbury, A.; Herzog, H. Peptide YY is critical for acylethanolamine receptor Gpr119-induced activation of gastrointestinal mucosal responses. Cell Metab. 2010, 11, 532-542.
59. Yao, C.; Sakata, D.; Esaki, Y.; Li, Y.; Matsuoka, T.; Kuroiwa, K.; Sugimoto, Y.; Narumiya, S. Prostaglandin E2-EP4 signaling promotes immune inflammation through Th1 cell differentiation and Th17 cell expansion. Nat. Med. 2009, 15, 633-640.
60. Sakata, D.; Yao, C.; Narumiya, S. Prostaglandin E2, an immunoactivator. J. Pharmacol. Sci. 2010, 112, 1-5.
61. Serhan, C.N.; Krishnamoorthy, S.; Recchiuti, A.; Chiang, N. Novel anti-inflammatory- pro-resolving mediators and their receptors. Curr. Top. Med. Chem. 2011, 11, 629-647.
62. Tedelind, S.; Westberg, F.; Kjerrulf, M.; Vidal, A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: A study with relevance to inflammatory bowel disease. World J. Gastroenterol. 2007, 13, 2826-2832.
63. Nakamura, Y. Regulating factors for microglial activation. Biol. Pharm. Bull. 2002, 25, 945-953.
64. Kim, H.J.; Rowe, M.; Ren, M.; Hong, J.S.; Chen, P.S.; Chuang, D.M. Histone deacetylase inhibitors exhibit anti-inflammatory and neuroprotective effects in a rat permanent ischemic model of stroke: Multiple mechanisms of action. J. Pharmacol. Exp. Ther. 2007, 321, 892-901.
65. Vinolo, M.A.; Hatanaka, E.; Lambertucci, R.H.; Newsholme, P.; Curi, R. Effects of short chain fatty acids on effector mechanisms of neutrophils. Cell Biochem. Funct. 2009, 27, 48-55.
66. Mills, S.W.; Montgomery, S.H.; Morck, D.W. Evaluation of the effects of short-chain fatty acids and extracellular pH on bovine neutrophil function in vitro. Am. J. Vet. Res. 2006, 67, 1901-1907.
67. Eftimiadi, C.; Buzzi, E.; Tonetti, M.; Buffa, P.; Buffa, D.; van Steenbergen, M.T.; de Graaff, J.; Botta, G.A. Short-chain fatty acids produced by anaerobic bacteria alter the physiological responses of human neutrophils to chemotactic peptide. J. Infect. 1987, 14, 43-53.
68. Eftimiadi, C.; Tonetti, M.; Cavallero, A.; Sacco, O.; Rossi, G.A. Short-chain fatty acids produced by anaerobic bacteria inhibit phagocytosis by human lung phagocytes. J. Infect. Dis. 1990, 161, 138-142.
69. Millard, A.L.; Mertes, P.M.; Ittelet, D.; Villard, F.; Jeannesson, P.; Bernard, J. Butyrate affects differentiation, maturation and function of human monocyte-derived dendritic cells and macrophages. Clin. Exp. Immunol. 2002, 130, 245-255.
70. Stringer, R.E.; Hart, C.A.; Edwards, S.W. Sodium butyrate delays neutrophil apoptosis: Role of protein biosynthesis in neutrophil survival. Br. J. Haematol. 1996, 92, 169-175.
71. Nakao, S.; Moriya, Y.; Furuyama, S.; Niederman, R.; Sugiya, H. Propionic acid stimulates superoxide generation in human neutrophils. Cell Biol. Int. 1998, 22, 331-337.
72. Tonetti, M.; Cavallero, A.; Botta, G.A.; Niederman, R.; Eftimiadi, C. Intracellular pH regulates the production of different oxygen metabolites in neutrophils: Effects of organic acids produced by anaerobic bacteria. J. Leukoc. Biol. 1991, 49, 180-188.
73. Liu, Q.; Shimoyama, T.; Suzuki, K.; Umeda, T.; Nakaji, S.; Sugawara, K. Effect of sodium butyrate on reactive oxygen species generation by human neutrophils. Scand. J. Gastroenterol. 2001, 36, 744-750.
74. Sandoval, A.; Trivinos, F.; Sanhueza, A.; Carretta, D.; Hidalgo, M.A.; Hancke, J.L.; Burgos, R.A. Propionate induces pH(i) changes through calcium flux, ERK1/2, p38, and PKC in bovine neutrophils. Vet. Immunol. Immunopathol. 2007, 115, 286-298.
75. Cavaglieri, C.R.; Nishiyama, A.; Fernandes, L.C.; Curi, R.; Miles, E.A.; Calder, P.C. Differential effects of short-chain fatty acids on proliferation and production of pro- and anti-inflammatory cytokines by cultured lymphocytes. Life Sci. 2003, 73, 1683-1690.
76. 4+ T cells. Int. Immunopharmacol. 2009, 9, 1289-1297.
77. Tao, R.; de Zoeten, E.F.; Ozkaynak, E.; Chen, C.; Wang, L.; Porrett, P.M.; Li, B.; Turka, L.A.; Olson, E.N.; Greene, M.I.; Wells, A.D.; Hancock, W.W. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat. Med. 2007, 13, 1299-1307.
78. Jacobasch, G.; Schmiedl, D.; Kruschewski, M.; Schmehl, K. Dietary resistant starch and chronic inflammatory bowel diseases. Int. J. Colorectal Dis. 1999, 14, 201-211.
79. Nishimura, T.; Andoh, A.; Hashimoto, T.; Kobori, A.; Tsujikawa, T.; Fujiyama, Y. Cellobiose prevents the development of dextran sulfate sodium (DSS)-induced experimental colitis. J. Clin. Biochem. Nutr. 2010, 46, 105-110.
80. Rodriguez-Cabezas, M.E.; Galvez, J.; Lorente, M.D.; Concha, A.; Camuesco, D.; Azzouz, S.; Osuna, A.; Redondo, L.; Zarzuelo, A. Dietary fiber down-regulates colonic tumor necrosis factor alpha and nitric oxide production in trinitrobenzenesulfonic acid-induced colitic rats. J. Nutr. 2002, 132, 3263-3271.
81. Tarrerias, A.L.; Millecamps, M.; Alloui, A.; Beaughard, C.; Kemeny, J.L.; Bourdu, S.; Bommelaer, G.; Eschalier, A.; Dapoigny, M.; Ardid, D. Short-chain fatty acid enemas fail to decrease colonic hypersensitivity and inflammation in TNBS-induced colonic inflammation in rats. Pain 2002, 100, 91-97.
82. Scheppach, W.; Sommer, H.; Kirchner, T.; Paganelli, G.M.; Bartram, P.; Christl, S.; Richter, F.; Dusel, G.; Kasper, H. Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 1992, 103, 51-56.
83. Hamer, H.M.; Jonkers, D.M.; Vanhoutvin, S.A.; Troost, F.J.; Rijkers, G.; de Bruine, A.; Bast, A.; Venema, K.; Brummer, R.J. Effect of butyrate enemas on inflammation and antioxidant status in the colonic mucosa of patients with ulcerative colitis in remission. Clin. Nutr. 2010, 29, 738-744.
84. Vernia, P.; Annese, V.; Bresci, G.; d'Albasio, G.; D'Inca, R.; Giaccari, S.; Ingrosso, M.; Mansi, C.; Riegler, G.; Valpiani, D. et al. Topical butyrate improves efficacy of 5-ASA in refractory distal ulcerative colitis: results of a multicentre trial. Eur. J. Clin. Invest. 2003, 33, 244-248.
85. Vieira, E.L.; Leonel, A.J.; Sad, A.P.; Beltrao, N.R.; Costa, T.F.; Ferreira, T.M.; Gomes-Santos, A.C.; Faria, A.M.; Peluzio, M.C.; Cara, D.C. et al. Oral administration of sodium butyrate attenuates inflammation and mucosal lesion in experimental acute ulcerative colitis. J. Nutr. Biochem. 2011, doi:10.1016/j.jnutbio.2011.01.007.
86. Zhang, L.T.; Yao, Y.M.; Lu, J.Q.; Yan, X.J.; Yu, Y.; Sheng, Z.Y. Sodium butyrate p events lethality of severe sepsis in rats. Shock 2007, 27, 672-677.
87. Ni, Y.F.; Wang, J.; Yan, X.L.; Tian, F.; Zhao, J.B.; Wang, Y.J.; Jiang, T. Histone deacetylase inhibitor, butyrate, attenuates lipopolysaccharide-induced acute lung injury in mice. Respir. Res. 2010, 11, 33.
88. Zhang, L.; Jin, S.; Wang, C.; Jiang, R.; Wan, J. Histone deacetylase inhibitors attenuate acute lung injury during cecal ligation and puncture-induced polymicrobial sepsis. World J. Surg. 2010, 34, 1676-1683.
89. Hu, X.; Xu, C.; Zhou, X.; He, B.; Wu, L.; Cui, B.; Lu, Z.; Jiang, H. Sodium butyrate protects against myocardial ischemia and reperfusion injury by inhibiting high mobility group box 1 protein in rats. Biomed. Pharmacother. 2010, doi:10.1016/j.biopha.2010.09.005.
90. Weber, T.E.; Kerr, B.J. Effect of sodium butyrate on growth performance and response to lipopolysaccharide in weanling pigs. J. Anim. Sci. 2008, 86, 442-450.
91. Wang, H.; Bloom, O.; Zhang, M.; Vishnubhakat, J.M.; Ombrellino, M.; Che, J.; Frazier, A.; Yang, H.; Ivanova, S.; Borovikova, L. et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999, 285, 248-251.
92. Ulloa, L.; Tracey, K.J. The "cytokine profile": A code for sepsis. Trends Mol. Med. 2005, 11, 56-63.
93. Zhang, L.; Jin, S.; Wang, C.; Jiang, R.; Wan, J. Histone deacetylase inhibitors attenuate acute lung injury during cecal ligation and puncture-induced polymicrobial sepsis. World J. Surg. 2010, 34, 1676-1683.
94. Ware, L.B.; Matthay, M.A. The acute respiratory distress syndrome. N. Engl. J. Med. 2000, 342, 1334-1349.
95. Balibrea, J.L.; Arias-Diaz, J. Acute respiratory distress syndrome in the septic surgical patient. World J. Surg. 2003, 27, 1275-1284.
96. Kurita-Ochiai, T.; Ochiai, K.; Fukushima, K. Butyric acid-induced T-cell apoptosis is mediated by caspase-8 and -9 activation in a Fas-independent manner. Clin. Diagn. Lab. Immunol. 2001, 8, 325-332.
97. Bailon, E.; Cueto-Sola, M.; Utrilla, P.; Rodriguez-Cabezas, M.E.; Garrido-Mesa, N.; Zarzuelo, A.; Xaus, J.; Galvez, J.; Comalada, M. Butyrate in vitro immune-modulatory effects might be mediated through a proliferation-related induction of apoptosis. Immunobiology 2010, 215, 863-873.
98. Ramos, M.G.; Rabelo, F.L.; Duarte, T.; Gazzinelli, R.T.; Alvarez-Leite, J.I. Butyrate induces apoptosis in murine macrophages via caspase-3, but independent of autocrine synthesis of tumor necrosis factor and nitric oxide. Braz. J. Med. Biol. Res. 2002, 35, 161-173.
99. Aoyama, M.; Kotani, J.; Usami, M. Butyrate and propionate induced activated or non-activated neutrophil apoptosis via HDAC inhibitor activity but without activating GPR-41/GPR-43 pathways. Nutrition 2010, 26, 653-661.
100. Niederman, R.; Buyle-Bodin, Y.; Lu, B.Y.; Robinson, P.; Naleway, C. Short-chain carboxylic acid concentration in human gingival crevicular fluid. J. Dent. Res. 1997, 76, 575-579.
101. Halili, M.A.; Andrews, M.R.; Labzin, L.I.; Schroder, K.; Matthias, G.; Cao, C.; Lovelace, E.; Reid, R.C.; Le, G.T.; Hume, D.A. et al. Differential effects of selective HDAC inhibitors on macrophage inflammatory responses to the Toll-like receptor 4 agonist LPS. J. Leukoc. Biol. 2010, 87, 1103-1114.s