CLC number: R574.62
On-line Access: 2015-03-05
Received: 2014-07-07
Revision Accepted: 2014-12-03
Crosschecked: 2015-02-17
Cited: 6
Clicked: 4364
Joshua J. Malago, Catherine L. Sangu. Intraperitoneal administration of butyrate prevents the severity of acetic acid colitis in rats[J]. Journal of Zhejiang University Science B, 2015, 16(3): 224-234.
@article{title="Intraperitoneal administration of butyrate prevents the severity of acetic acid colitis in rats",
author="Joshua J. Malago, Catherine L. Sangu",
journal="Journal of Zhejiang University Science B",
volume="16",
number="3",
pages="224-234",
year="2015",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1400191"
}
%0 Journal Article
%T Intraperitoneal administration of butyrate prevents the severity of acetic acid colitis in rats
%A Joshua J. Malago
%A Catherine L. Sangu
%J Journal of Zhejiang University SCIENCE B
%V 16
%N 3
%P 224-234
%@ 1673-1581
%D 2015
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1400191
TY - JOUR
T1 - Intraperitoneal administration of butyrate prevents the severity of acetic acid colitis in rats
A1 - Joshua J. Malago
A1 - Catherine L. Sangu
J0 - Journal of Zhejiang University Science B
VL - 16
IS - 3
SP - 224
EP - 234
%@ 1673-1581
Y1 - 2015
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1400191
Abstract: Intrarectal infusion of butyrate improves colorectal disorders including ulcerative colitis (UC). However, it is not established whether systemically administered butyrate benefits such patients. The current study aimed at exploring and comparing the potential of intraperitoneally, intrarectally, and orally administered butyrate against acetic acid (AA)-induced UC in rats. intrarectal administration of 2 ml of 50% AA was done after or without prior treatment of rats for 7 consecutive days with 100 mg/kg sodium butyrate (SB) intraperitoneally, intrarectally, or orally. Rats were sacrificed after 48 h of AA-treatment. Subsequently, colon sections were processed routinely for histopathological examination. We clinically observed diarrhea, loose stools, and hemoccult-positive stools, and histologically, epithelial loss and ulceration, crypt damage, goblet cell depletion, hemorrhage, and mucosal infiltration of inflammatory cells. The changes were significantly reduced by intraperitoneal, intrarectal, or oral butyrate, with intraperitoneal butyrate exhibiting the highest potency. It is concluded that intraperitoneal administration of butyrate abrogates the lesions of AA-induced UC and its potency surpasses that of intrarectal or oral butyrate.
[1]Bloemen, J.G., Schreinemacher, M.H., de Bruine, A.P., et al., 2010. Butyrate enemas improve intestinal anastomotic strength in rat model. Dis. Colon Rectum., 53(7):1069-1075.
[2]Cetinkaya, A., Bulbuloglu, E., Kurutas, E.B., et al., 2005. Beneficial effects of N-acetylcysteine on acetic acid-induced colitis in rats. Tohoku J. Exp. Med., 206(2):131-139.
[3]Chang, P.V., Hao, L., Offermanns, S., et al., 2014. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. PNAS, 111(6):2247-2252.
[4]Clark, A.J., 1921. Absorption from the peritoneal cavity. J. Pharmacol. Exp. Ther., 16(6):415-433.
[5]Cummings, J.H., Pomare, E.W., Branch, W.J., et al., 1987. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut, 28(10):1221-1227.
[6]Dabard, J., Hudault, S., Saby, M.A., 1987. Production of butyric acid in human premature baby suffering from necrotizing enterocolitis. Proceedings of the 9th International Symposium on Gnotobiology. Versailles, p.90-95.
[7]de Preter, V., Geboes, K.P., Bulteel, V., et al., 2011. Kinetics of butyrate metabolism in the normal colon and in ulcerative colitis: the effects of substrate concentration and carnitine on the β-oxidation pathway. Aliment. Pharmacol. Ther., 34(5):526-532.
[8]de Preter, V., Arijs, I., Windey, K., et al., 2012. Impaired butyrate oxidation in ulcerative colitis is due to decreased butyrate uptake and a defect in the oxidation pathway. Inflamm. Bowel Dis., 18(6):1127-1136.
[9]Eeckhaut, V., Machiels, K., Perrier, C., et al., 2013. Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut, 62(12):1745-1752.
[10]Fabia, R., Willén, R., Ar'Rajab, A., et al., 1992. Acetic acid-induced colitis in the rat: a reproducible experimental model for acute ulcerative colitis. Eur. Surg. Res., 24(4):211-225.
[11]Fernández-Bañares, F., Hinojosa, J., Sánchez-Lombraña, J.L., et al., 1999. Randomized clinical trial of Plantago ovata seeds (dietary fiber) as compared with mesalamine in maintaining remission in ulcerative colitis. Spanish Group for the Study of Crohn’s Disease and Ulcerative Colitis (GETECCU). Am. J. Gastroenterol., 94(2):427-433.
[12]Ferrante, R.J., Kubilus, J.K., Lee, J., et al., 2003. Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington’s disease mice. J. Neurosci., 23(28):9418-9427.
[13]Fusunyan, R.D., Quinn, J.J., Ohno, Y., et al., 1998. Butyrate enhances interleukin (IL)-8 secretion by intestinal epithelial cells in response to IL-1( and lipopolysaccharide. Pediatr. Res., 43(1):84-90.
[14]Fusunyan, R.D., Quinn, J.J., Fujimoto, M., et al., 1999. Butyrate switches the pattern of chemokine secretion by intestinal epithelial cells through histone acetylation. Mol. Med., 5(9):631-640.
[15]Hamer, H.M., Jonkers, D.M., Renes, I.B., et al., 2010a. Butyrate enemas do not affect human colonic MUC2 and TFF3 expression. Eur. J. Gastroenterol. Hepatol., 22(9):1134-1140.
[16]Hamer, H.M., Jonkers, D.M., Vanhoutvin, S.A., et al., 2010b. Effect of butyrate enemas on inflammation and antioxidant status in the colonic mucosa of patients with ulcerative colitis in remission. Clin. Nutr., 29(6):738-744.
[17]Harig, J.M., Soergel, K.H., Komorowski, R.A., et al., 1989. Treatment of diversion colitis with short chain fatty acid irrigation. N. Engl. J. Med., 320(1):23-28.
[18]Holtug, K., Hove, H., Mortensen, P.B., 1995. Stimulation of butyrate absorption in the human rectum in vivo. Scand. J. Gastroenterol., 30(10):982-988.
[19]Hou, Y., Wang, L., Yi, D., et al., 2014. Dietary supplementation with tributyrin alleviates intestinal injury in piglets challenged with intrarectal administration of acetic acid. Br. J. Nutr., 111(10):1748-1758.
[20]Hove, H., Holtug, K., Jeppesen, P.B., et al., 1995. Butyrate absorption and lactate secretion in ulcerative colitis. Dis. Colon Rectum, 38(5):519-525.
[21]Huang, N., Katz, J.P., Martin, D.R., et al., 1997. Inhibition of IL-8 gene expression in Caco-2 cells by compounds which induce histone hyperacetylation. Cytokine, 9(1):27-36.
[22]Hudcovic, T., Kolinska, J., Klepetar, J., et al., 2012. Protective effect of Clostridium tyrobutyricum in acute dextran sodium sulphate-induced colitis: differential regulation of tumour necrosis factor-α and interleukin-18 in BALB/c and severe combined immunodeficiency mice. Clin. Exp. Immunol., 167(2):356-365.
[23]Ke, X., Chen, J., Zhang, X., et al., 2013. Qing Hua Chang Yin attenuates lipopolysaccharide-induced inflammatory response in human intestinal cells by inhibiting NF-κB activation. Exp. Ther. Med., 6(1):189-193.
[24]Kovarik, J.J., Tillinger, W., Hofer, J., et al., 2011. Impaired anti-inflammatory efficacy of n-butyrate in patients with IBD. Eur. J. Clin. Invest., 41(3):291-298.
[25]La, J.H., Kim, T.W., Sung, T.S., et al., 2003. Visceral hypersensitivity and altered colonic motility after subsidence of inflammation in a rat model of colitis. World J. Gastroenterol., 9(12):2791-2795.
[26]Liu, H., Patel, N.R., Walter, L., et al., 2013. Constitutive expression of MMP9 in intestinal epithelium worsens murine acute colitis and is associated with increased levels of proinflammatory cytokine Kc. Am. J. Physiol. Gastrointest. Liver Physiol., 304(9):G793-G803.
[27]Malago, J.J., Nondoli, H., 2008. Sodium arsenite reduces severity of dextran sulfate sodium-induced ulcerative colitis in rats. J. Zhejiang Univ.-Sci. B, 9(4):341-350.
[28]Malago, J.J., Koninkx, J.F.J.G., van Dijk, J.E., 2002. The heat shock response and cytoprotection of the intestinal epithelium. Cell Stress. Chaperones, 7(2):191-199.
[29]Malago, J.J., Koninkx, J.F.J.G., Tooten, P.C.J., et al., 2005. Anti-inflammatory properties of heat shock protein 70 and butyrate on Salmonella-induced interleukin-8 secretion in enterocyte-like Caco-2 cells. Clin. Exp. Immun., 141(1):62-71.
[30]Mathew, A.J., Wann, V.C., Abraham, D.T., et al., 2010. The effect of butyrate on the healing of colonic anastomoses in rats. J. Invest. Surg., 23(2):101-104.
[31]Mikhailova, T.L., Sishkova, E., Poniewierka, E., et al., 2011. Randomised clinical trial: the efficacy and safety of propionyl-
[32]Miller, A.A., Kurschel, E., Osieka, R., et al., 1987. Clinical pharmacology of sodium butyrate in patients with acute leukemia. Eur. J. Cancer Clin. Oncol., 23(9):1283-1287.
[33]Minaiyan, M., Ghassemi-Dehkordi, N., Mahzouni, P., et al., 2014. Anti-inflammatory effect of Helichrysum oligocephalum DC extract on acetic acid-induced acute colitis in rats. Adv. Biomed. Res., 3(1):87.
[34]O'Morain, C., Segal, A.W., Levi, A.J., 1984. Elemental diet as primary treatment of acute Crohn’s disease: a controlled trial. Br. Med. J. (Clin. Res. Ed.), 288(6434):1859-1862.
[35]Randhawa, P.K., Singh, K., Singh, N., et al., 2014. A review on chemical-induced inflammatory bowel disease models in rodents. Korean J. Physiol. Pharmacol., 18(4):279-288.
[36]Reolon, G.K., Maurmann, N., Werenicz, A., et al., 2011. Posttraining systemic administration of the histone deacetylase inhibitor sodium butyrate ameliorates aging-related memory decline in rats. Behav. Brain Res., 221(1):329-332.
[37]Roediger, W.E.W., 1980. The colonic epithelium in ulcerative colitis: an energy deficiency disease. Lancet, 2(8197):712-715.
[38]Sakthivel, K.M., Chandrasekaran, G., 2014. Protective effect of Acacia ferruginea against ulcerative colitis via modulating inflammatory mediators, cytokine profile and NF-κb signal transduction pathways. J. Environ. Pathol. Toxicol. Oncol., 33(2):83-98.
[39]Sanderson, I.R., 1997. Diet and gut inflammation. Curr. Opin. Gastroenterol., 13(6):518-524.
[40]Sauer, J., Richter, K.K., Pool-Zobel, B.L., 2007. Physiological concentrations of butyrate favorably modulate genes of oxidative and metabolic stress in primary human colon cells. J. Nutr. Biochem., 18(11):736-745.
[41]Scheppach, W., Sommer, H., Kirchner, T., et al., 1992. Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology, 103(1):51-56.
[42]Silingardi, D., Scali, M., Belluomini, G., et al., 2010. Epigenetic treatments of adult rats promote recovery from visual acuity deficits induced by long-term monocular deprivation. Eur. J. Neurosci., 31(12):2185-2192.
[43]Sotnikova, R., Nosalova, V., Navarova, J., 2013. Efficacy of quercetin derivatives in prevention of ulcerative colitis in rats. Interdiscip. Toxicol., 6(1):9-12.
[44]Sun, X., Zhang, B., Hong, X., et al., 2013. Histone deacetylase inhibitor, sodium butyrate, attenuates gentamicin-induced nephrotoxicity by increasing prohibitin protein expression in rats. Eur. J. Pharmacol., 707(1-3):147-154.
[45]Thibault, R., de Coppet, P., Daly, K., et al., 2007. Down-regulation of the monocarboxylate transporter 1 is involved in butyrate deficiency during intestinal inflammation. Gastroenterology, 133(6):1916-1927.
[46]Thibault, R., Blachier, F., Darcy-Vrillon, B., et al., 2010. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflamm. Bowel Dis., 16(4):684-965.
[47]Torpy, J.M., Lynm, C., Golub, R.M., 2012. Ulcerative colitis. JAMA, 307(1):104.
[48]Treem, W.R., Ahsan, N., Shoup, M., et al., 1994. Fecal short-chain fatty acids in children with inflammatory bowel disease. J. Pediatr. Gastroenterol. Nutr., 18(2):159-164.
[49]Venkatraman, A., Ramakrishna, B.S., Shaji, R.V., et al., 2003. Amelioration of dextran sulfate colitis by butyrate: role of heat shock protein 70 and NF-κB. Am. J. Physiol. Gastrointest. Liver Physiol., 285(1):G177-G184.
[50]Vernia, P., Monteleone, G., Grandinetti, G., et al., 2000. Combined oral sodium butyrate and mesalazine treatment compared to oral mesalazine alone in ulcerative colitis: randomized, double-blind, placebo-controlled pilot study. Dig. Dis. Sci., 45(5):976-981.
[51]Vieira, E.L., Leonel, A.J., Sad, A.P., et al., 2012. Oral administration of sodium butyrate attenuates inflammation and mucosal lesion in experimental acute ulcerative colitis. J. Nutr. Biochem., 23(5):430-436.
[52]Vinod, P.V., Guruvayoorappan, C., 2014. Protective effect of marine mangrove Rhizophora apiculata on acetic acid induced experimental colitis by regulating anti-oxidant enzymes, inflammatory mediators and nuclear factor-kappa B subunits. Int. Immunopharmacol., 18(1):124-134.
[53]Wu, G.D., Huang, N., Wen, X., et al., 1999. High-level expression of I(B-( in the surface epithelium of the colon: in vitro evidence for an immunomodulatory role. J. Leukoc. Biol., 66(6):1049-1056.
[54]Wu, W.T., Chen, H.L., 2011. Konjac glucomannan and inulin systematically modulate antioxidant defense in rats fed a high-fat fiber-free diet. J. Agric. Food Chem., 59(17):9194-9200.
[55]Zhao, L., Wu, H., Zhao, A., et al., 2014. The in vivo and in vitro study of polysaccharides from a two-herb formula on ulcerative colitis and potential mechanism of action. J. Ethnopharmacol., 153(1):151-159.
[56]Zhong, T., Qing, Q.J., Yang, Y., et al., 2014. Repression of contexual fear memory induced by isoflurane is accompanied by reduction in histone acetylation and rescued by sodium butyrate. Br. J. Anaesth., 113(4):634-643.
[57]Zimmerman, M.A., Singh, N., Martin, P.M., et al., 2012. Butyrate suppresses colonic inflammation through HDAC1-dependent Fas upregulation and Fas-mediated apoptosis of T cells. Am. J. Physiol. Gastrointest. Liver Physiol., 302(12):G1405-G1415.
Open peer comments: Debate/Discuss/Question/Opinion
<1>