Oral butyrate reduces oxidative stress in atherosclerotic lesion sites by a mechanism involving NADPH oxidase down-regulation in endothelial cells

Journal of Nutritional Biochemistry

Volumn 34, Issue , 2016, Pages 99-105

  Aguilar, Edenil C ^a   Santos, Lana Claudinez dos ^a   Leonel, Alda J ^a   de Oliveira, Jamil Silvano ^a   Santos, Elândia Aparecida ^a   Navia Pelaez, Juliana M ^a   da Silva, Josiane Fernandes ^a   Mendes, Bárbara Pinheiro ^a   Capettini, Luciano S A ^a   Teixeira, Lilian G ^b   Lemos, Virginia S ^a   Alvarez Leite, Jacqueline I ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF LAVRAS   (Brazil)

Author keywords

Atherosclerosis; Butyrate; Lipids; Oxidative stress; Reactive oxygen species; Short chain fatty acids

Indexed keywords

APOLIPOPROTEIN E; BUTYRIC ACID; FREE RADICAL; INOSINATE DEHYDROGENASE; LIPID; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; OXIDIZED LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN ANTIBODY; PROTEIN P22; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; ZYMOSAN; ANTIOXIDANT; BIOLOGICAL MARKER; INDUCIBLE NITRIC OXIDE SYNTHASE; LOW DENSITY LIPOPROTEIN; NOS2 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA VALVE; ARTICLE; ATHEROSCLEROSIS; CELL ACTIVATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME MECHANISM; EX VIVO STUDY; FLOW CYTOMETRY; FOOD INTAKE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID BLOOD LEVEL; LIPID STORAGE; MACROPHAGE; MACROPHAGE MIGRATION; MALE; MOUSE; NITROSYLATION; NONHUMAN; NORMAL HUMAN; OXIDATIVE STRESS; PERITONEUM MACROPHAGE; PROTEIN EXPRESSION; WEIGHT GAIN; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; CELL CULTURE; CYTOLOGY; DIETARY SUPPLEMENT; ENZYME REPRESSION; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE ACTIVATION; METABOLISM; PATHOLOGY; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIOXIDANTS; ATHEROSCLEROSIS; BIOMARKERS; BUTYRIC ACID; CELLS, CULTURED; DIETARY SUPPLEMENTS; ENDOTHELIUM, VASCULAR; ENZYME REPRESSION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIPOPROTEINS, LDL; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MALE; MICE, KNOCKOUT; NADPH OXIDASES; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84971422909     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2016.05.002     Document Type: Article

References (36)

1. Libby P., Ridker P.M., Hansson G.K. Progress and challenges in translating the biology of atherosclerosis. Nature 2011, 473:317-325.
2. Kinoshita H., Matsumura T., Ishii N., Fukuda K., Senokuchi T., Motoshima H., et al. Apocynin suppresses the progression of atherosclerosis in apoE-deficient mice by inactivation of macrophages. Biochem Biophys Res Commun 2013, 431:124-130.
3. Kaliora A.C., Dedoussis G.V., Schmidt H. Dietary antioxidants in preventing atherogenesis. Atherosclerosis 2006, 187:1-17.
4. Hamer H.M., Jonkers D.M., Bast A., Vanhoutvin S.A., Fischer M.A., Kodde A., et al. Butyrate modulates oxidative stress in the colonic mucosa of healthy humans. Clin Nutr 2009, 28:88-93.
5. Ferreira T.M., Leonel A.J., Melo M.A., Santos R.R., Cara D.C., Cardoso V.N., et al. Oral supplementation of butyrate reduces mucositis and intestinal permeability associated with 5-Fluorouracil administration. Lipids 2012, 47:669-678.
6. 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.
7. Segain J.P., 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.
8. Ranganna K., Mathew O.P., Yatsu F.M., Yousefipour Z., Hayes B.E., Milton S.G. Involvement of glutathione/glutathione S-transferase antioxidant system in butyrate-inhibited vascular smooth muscle cell proliferation. FEBS J 2007, 274:5962-5978.
9. Aguilar E.C., Leonel A.J., Teixeira L.G., Silva A.R., Silva J.F., Pelaez J.M.N., et al. Butyrate impairs atherogenesis by reducing plaque inflammation and vulnerability and decreasing NF kappa B activation. Nutr Metab Cardiovasc Dis 2014, 24:606-613.
10. Vogiatzi G., Tousoulis D., Stefanadis C. The role of oxidative stress in atherosclerosis. Hellenic J Cardiol 2009, 50:402-409.
11. Aguilar E.C., Jascolka T.L., Teixeira L.G., Lages P.C., Ribeiro A.C., Vieira E.L., et al. Paradoxical effect of a pequi oil-rich diet on the development of atherosclerosis: balance between antioxidant and hyperlipidemic properties. Braz J Med Biol Res 2012, 45:601-609.
12. Carter W.O., Narayanan P.K., Robinson J.P. Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J Leukoc Biol 1994, 55:253-258.
13. Palinski W., Ord V.A., Plump A.S., Breslow J.L., Steinberg D., Witztum J.L. ApoE-deficient mice are a model of lipoprotein oxidation in atherogenesis. Demonstration of oxidation-specific epitopes in lesions and high titers of autoantibodies to malondialdehyde-lysine in serum. Arterioscler Thromb 1994, 14:605-616.
14. Chung B.H., Segrest J.P., Ray M.J., Brunzell J.D., Hokanson J.E., Krauss R.M., et al. Single vertical spin density gradient ultracentrifugation. Methods Enzymol 1986, 128:181-209.
15. Vay D., Parodi M., Rolla R., Mottaran E., Vidali M., Bellomo G., et al. Circulating antibodies recognizing malondialdehyde-modified proteins in healthy subjects. Free Radic Biol Med 2001, 30:277-286.
16. Lee T.S., Yen H.C., Pan C.C., Chau L.Y. The role of interleukin 12 in the development of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 1999, 19:734-742.
17. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
18. Capettini L.S., Cortes S.F., Silva J.F., Alvarez-Leite J.I., Lemos V.S. Decreased production of neuronal NOS-derived hydrogen peroxide contributes to endothelial dysfunction in atherosclerosis. Br J Pharmacol 2011, 164:1738-1748.
19. 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.
20. Buege J.A., Aust S.D. Microsomal lipid peroxidation. Methods Enzymol 1978, 52:302-310.
21. O'Dowd Y., Driss F., Dang P.M., Elbim C., Gougerot-Pocidalo M.A., Pasquier C., et al. Antioxidant effect of hydroxytyrosol, a polyphenol from olive oil: scavenging of hydrogen peroxide but not superoxide anion produced by human neutrophils. Biochem Pharmacol 2004, 68:2003-2008.
22. Saunders D.R. Absorption of short-chain fatty acids in human stomach and rectum. Nutr Res 1991, 11:841-847.
23. Darwish R.S., Amiridze N., Aarabi B. Nitrotyrosine as an oxidative stress marker: evidence for involvement in neurologic outcome in human traumatic brain injury. J Trauma 2007, 63:439-442.
24. Shishehbor M.H., Aviles R.J., Brennan M.L., Fu X., Goormastic M., Pearce G.L., et al. Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapy. JAMA 2003, 289:1675-1680.
25. Upmacis R.K. Atherosclerosis: A Link Between Lipid Intake and Protein Tyrosine Nitration. Lipid Insights 2008, 2008:75.
26. Hulthe J., Bokemark L., Fagerberg B. Antibodies to oxidized LDL in relation to intima-media thickness in carotid and femoral arteries in 58-year-old subjectively clinically healthy men. Arterioscler Thromb Vasc Biol 2001, 21:101-107.
27. Huang Y., Jaffa A., Koskinen S., Takei A., Lopes-Virella M.F. Oxidized LDL-containing immune complexes induce Fc gamma receptor I-mediated mitogen-activated protein kinase activation in THP-1 macrophages. Arterioscler Thromb Vasc Biol 1999, 19:1600-1607.
28. Kiener P.A., Rankin B.M., Davis P.M., Yocum S.A., Warr G.A., Grove R.I. Immune complexes of LDL induce atherogenic responses in human monocytic cells. Arterioscler Thromb Vasc Biol 1995, 15:990-999.
29. Burut D.F., Karim Y., Ferns G.A. The role of immune complexes in atherogenesis. Angiology 2010, 61:679-689.
30. Manea A., Manea S.A., Gafencu A.V., Raicu M. Regulation of NADPH oxidase subunit p22(phox) by NF-kB in human aortic smooth muscle cells. Arch Physiol Biochem 2007, 113:163-172.
31. Perianayagam M.C., Liangos O., Kolyada A.Y., Wald R., MacKinnon R.W., Li L., et al. NADPH oxidase p22phox and catalase gene variants are associated with biomarkers of oxidative stress and adverse outcomes in acute renal failure. J Am Soc Nephrol 2007, 18:255-263.
32. Park Y.M., Febbraio M., Silverstein R.L. CD36 modulates migration of mouse and human macrophages in response to oxidized LDL and may contribute to macrophage trapping in the arterial intima. J Clin Invest 2009, 119:136-145.
33. Khan S., Jena G. Sodium butyrate, a HDAC inhibitor ameliorates eNOS, iNOS and TGF-β1-induced fibrogenesis, apoptosis and DNA damage in the kidney of juvenile diabetic rats. Food Chem Toxicol 2014, 73:127-139.
34. 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.
35. Stempelj M., Kedinger M., Augenlicht L., Klampfer L. Essential role of the JAK/STAT1 signaling pathway in the expression of inducible nitric-oxide synthase in intestinal epithelial cells and its regulation by butyrate. J Biol Chem 2007, 282:9797-9804.
36. Chakravortty D., Koide N., Kato Y., Sugiyama T., Mu M.M., Yoshida T., et al. 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.