Suppressive effect of short-chain fatty acids on production of proinflammatory mediators by neutrophils

Journal of Nutritional Biochemistry

Volumn 22, Issue 9, 2011, Pages 849-855

  Vinolo, Marco A R ^a   Rodrigues, Hosana G ^a   Hatanaka, Elaine ^a,b   Sato, Fábio T ^a   Sampaio, Sandra C ^c   Curi, Rui ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b University Cruzeiro do Sul   (Brazil)

^c INSTITUTO BUTANTAN   (Brazil)

Author keywords

Butyrate; Inhibitors of HDAC; Neutrophils and cytokines; Short chain fatty acids

Indexed keywords

ACETIC ACID; ARACHIDONATE 5 LIPOXYGENASE; BUTYRIC ACID; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; GLYCOGEN; HISTONE DEACETYLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NITRIC OXIDE; PROPIONIC ACID; PROSTAGLANDIN SYNTHASE; SHORT CHAIN FATTY ACID; TRIBUTYRIN; TUMOR NECROSIS FACTOR ALPHA;

ANAEROBIC FERMENTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENERGY RESOURCE; ENZYME ACTIVITY; ENZYME INHIBITION; EX VIVO STUDY; IN VIVO STUDY; INFLAMMATION; INTESTINE EPITHELIUM CELL; LEUKOCYTE FUNCTION; MALE; NEUTROPHIL; NONHUMAN; RAT;

ACETIC ACID; ANIMALS; CHEMOKINES, CXC; CYTOKINES; FATTY ACIDS, VOLATILE; HISTONE DEACETYLASES; INFLAMMATION MEDIATORS; MALE; NEUTROPHILS; NF-KAPPA B; NITRIC OXIDE; PROPIONIC ACIDS; RATS; TRIGLYCERIDES; TUMOR NECROSIS FACTOR-ALPHA;

RATTUS;

EID: 80051471073     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2010.07.009     Document Type: Article

References (48)

1. Cook S.I., Sellin J.H. Review article: short chain fatty acids in health and disease. Aliment Pharmacol Ther 1998, 12:499-507.
2. Topping D.L., Clifton P.M. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 2001, 81:1031-1064.
3. Mortensen F.V., Hessov I., Birke H., Korsgaard N., Nielsen H. Microcirculatory and trophic effects of short chain fatty acids in the human rectum after Hartmann's procedure. Br J Surg 1991, 78:1208-1211.
4. Cherbut C., Aube A.C., Blottiere H.M., Galmiche J.P. Effects of short-chain fatty acids on gastrointestinal motility. Scand J Gastroenterol Suppl 1997, 222:58-61.
5. Binder H.J., Mehta P. Short-chain fatty acids stimulate active sodium and chloride absorption in vitro in the rat distal colon. Gastroenterology 1989, 96:989-996.
6. Louis P., Flint H.J. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 2009, 294:1-8.
7. Naito Y., Takagi T., Katada K., Uchiyama K., Kuroda M., Kokura S., et al. Partially hydrolyzed guar gum down-regulates colonic inflammatory response in dextran sulfate sodium-induced colitis in mice. J Nutr Biochem 2006, 17:402-409.
8. Kanauchi O., Suga T., Tochihara M., Hibi T., Naganuma M., Homma T., et al. Treatment of ulcerative colitis by feeding with germinated barley foodstuff: first report of a multicenter open control trial. J Gastroenterol 2002, 37(Suppl 14):67-72.
9. Hamer H.M., Jonkers D., Venema K., Vanhoutvin S., Troost F.J., Brummer R.J. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 2008, 27:104-119.
10. Zhang L.T., Yao Y.M., Lu J.Q., Yan X.J., Yu Y., Sheng Z.Y. Sodium butyrate prevents lethality of severe sepsis in rats. Shock 2007, 27:672-677.
11. Fukae J., Amasaki Y., Yamashita Y., Bohgaki T., Yasuda S., Jodo S., et al. 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.
12. 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.
13. Ogawa H., Rafiee P., Fisher P.J., Johnson N.A., Otterson M.F., Binion D.G. Butyrate modulates gene and protein expression in human intestinal endothelial cells. Biochem Biophys Res Commun 2003, 309:512-519.
14. Cassatella M.A. The production of cytokines by polymorphonuclear neutrophils. Immunol Today 1995, 16:21-26.
15. Sandoval A., Trivinos F., Sanhueza A., Carretta D., Hidalgo M.A., Hancke J.L., et al. Propionate induces pH(i) changes through calcium flux, ERK1/2, p38, and PKC in bovine neutrophils. Vet Immunol Immunopathol 2007, 115:286-298.
16. Le Poul E., Loison C., Struyf S., Springael J.Y., Lannoy V., Decobecq M.E., 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.
17. 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.
18. 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.
19. Carter G.W., Young P.R., Albert D.H., Bouska J., Dyer R., Bell R.L., et al. 5-lipoxygenase inhibitory activity of zileuton. J Pharmacol Exp Ther 1991, 256:929-937.
20. Niederberger E., Manderscheid C., Geisslinger G. Different COX-independent effects of the COX-2 inhibitors etoricoxib and lumiracoxib. Biochem Biophys Res Commun 2006, 342:940-948.
21. Ding A.H., Nathan C.F., Stuehr D.J. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 1988, 141:2407-2412.
22. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159.
23. Higuchi R., Dollinger G., Walsh P.S., Griffith R. Simultaneous amplification and detection of specific DNA sequences. Biotechnology (N Y) 1992, 10:413-417.
24. Liu W., Saint D.A. A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics. Anal Biochem 2002, 302:52-59.
25. Andrews N.C., Faller D.V. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 1991, 19:2499.
26. Hang C.H., Shi J.X., Tian J., Li J.S., Wu W., Yin H.X. Effect of systemic LPS injection on cortical NF-kappaB activity and inflammatory response following traumatic brain injury in rats. Brain Res 2004, 1026:23-32.
27. Egorin M.J., Yuan Z.M., Sentz D.L., Plaisance K., Eiseman J.L. Plasma pharmacokinetics of butyrate after intravenous administration of sodium butyrate or oral administration of tributyrin or sodium butyrate to mice and rats. Cancer Chemother Pharmacol 1999, 43:445-453.
28. 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.
29. Rotstein O.D., Pruett T.L., Simmons R.L. Lethal microbial synergism in intra-abdominal infections. Escherichia coli and Bacteroides fragilis. Arch Surg 1985, 120:146-151.
30. Khan N., Jeffers M., Kumar S., Hackett C., Boldog F., Khramtsov N., et al. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 2008, 409:581-589.
31. Planchon P., Pouillart P., Ronco G., Villa P., Pieri F. Differential elimination of synthetic butyric triglycerides in vivo: a pharmacokinetic study. J Pharm Sci 1993, 82:1046-1048.
32. 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 (Lond) 2009, 117:331-338.
33. Maslowski K.M., Vieira A.T., Ng A., Kranich J., Sierro F., Yu D., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461:1282-1286.
34. Davie J.R. Inhibition of histone deacetylase activity by butyrate. J Nutr 2003, 133:2485S-2493S.
35. de Ruijter A.J., van Gennip A.H., Caron H.N., Kemp S., van Kuilenburg A.B. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 2003, 370:737-749.
36. Ito K., Yamamura S., Essilfie-Quaye S., Cosio B., Ito M., Barnes P.J., et al. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-kappaB suppression. J Exp Med 2006, 203:7-13.
37. Chen L., Fischle W., Verdin E., Greene W.C. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001, 293:1653-1657.
38. Sun Y., Chin Y.E., Weisiger E., Malter C., Tawara I., Toubai T., et al. Cutting edge: Negative regulation of dendritic cells through acetylation of the nonhistone protein STAT-3. J Immunol 2009, 182:5899-5903.
39. Calao M., Burny A., Quivy V., Dekoninck A., Van Lint C. A pervasive role of histone acetyltransferases and deacetylases in an NF-kappaB-signaling code. Trends Biochem Sci 2008, 33:339-349.
40. Yin L., Laevsky G., Giardina C. Butyrate suppression of colonocyte NF-kappa B activation and cellular proteasome activity. J Biol Chem 2001, 276:44641-44646.
41. Usami M., Kishimoto K., Ohata A., Miyoshi M., Aoyama M., Fueda Y., et al. 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.
42. Shibata F., Konishi K., Kato H., Komorita N., al-Mokdad M., Fujioka M., et al. Recombinant production and biological properties of rat cytokine-induced neutrophil chemoattractants, GRO/CINC-2 alpha, CINC-2 beta and CINC-3. Eur J Biochem 1995, 231:306-311.
43. Mulligan M.S., Lentsch A.B., Miyasaka M., Ward P.A. Cytokine and adhesion molecule requirements for neutrophil recruitment during glycogen-induced peritonitis. Inflamm Res 1998, 47:251-255.
44. 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.
45. 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.
46. Daniel P., Brazier M., Cerutti I., Pieri F., Tardivel I., Desmet G., et al. Pharmacokinetic study of butyric acid administered in vivo as sodium and arginine butyrate salts. Clin Chim Acta 1989, 181:255-263.
47. Conley B.A., Egorin M.J., Tait N., Rosen D.M., Sausville E.A., Dover G., et al. Phase I study of the orally administered butyrate prodrug, tributyrin, in patients with solid tumors. Clin Cancer Res 1998, 4:629-634.
48. Edelman M.J., Bauer K., Khanwani S., Tait N., Trepel J., Karp J., et al. Clinical and pharmacologic study of tributyrin: an oral butyrate prodrug. Cancer Chemother Pharmacol 2003, 51:439-444.