Antiinflammatory effect of phytosterols in experimental murine colitis model: Prevention, induction, remission study

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Aldini, Rita ^a   Micucci, Matteo ^a   Cevenini, Monica ^a   Fato, Romana ^a   Bergamini, Christian ^a   Nanni, Cristina ^b   Cont, Massimiliano ^b   Camborata, Cecilia ^a   Spinozzi, Silvia ^a   Montagnani, Marco ^a   Roda, Giulia ^a   D'Errico Grigioni, Antonia ^a   Rosini, Francesca ^a   Roda, Aldo ^a   Mazzella, Giuseppe ^a   Chiarini, Alberto ^a   Budriesi, Roberta ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; BRASSICASTEROL; CAMPESTEROL; CHOLESTEROL; FLUORODEOXYGLUCOSE F 18; PHYTOSTEROL; SITOSTEROL; STIGMASTEROL; ANTIINFLAMMATORY AGENT; DEXTRAN SULFATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD ANALYSIS; CHOLESTEROL BLOOD LEVEL; COLITIS; COLON LENGTH; COLON MOTILITY; CONTROLLED STUDY; DISEASE ACTIVITY SCORE; DISEASE SEVERITY; HISTOPATHOLOGY; ILEUM; INTESTINE PARAMETERS; LONGITUDINAL STUDY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; POSITRON EMISSION TOMOGRAPHY; REMISSION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CHEMICALLY INDUCED; COLON; DISEASE MODEL; DRUG EFFECTS; GALLBLADDER; METABOLISM; PATHOLOGY; PERISTALSIS; SEVERITY OF ILLNESS INDEX;

MURINAE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BILE ACIDS AND SALTS; CHOLESTEROL; COLITIS; COLON; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; GALLBLADDER; ILEUM; MALE; MICE; MICE, INBRED BALB C; OXIDATIVE STRESS; PERISTALSIS; PHYTOSTEROLS; REMISSION INDUCTION; SEVERITY OF ILLNESS INDEX;

EID: 84907480659     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108112     Document Type: Article

References (75)

1. Ostlund RE Jr (2002) Phytosterols in human nutrition. Annu Rev Nutr 22: 533-549.
2. Brufau G, Canela MA, Rafecas M (2008) Phytosterols: physiologic and metabolic aspects related to cholesterol-lowering properties. Nutr Res 28: 217-225.
3. Moghadasian MH (2000) Pharmacological properties of plant sterols: in vivo and in vitro observations. Life Sci 67: 605-615.
4. Moreau RA, Whitaker BD, Hicks KB (2002) Phytosterols, phytostanols, and their conjugates in foods: structural diversity, quantitative analysis, and healthpromoting uses. Prog Lipid Res 41: 457-500.
5. Baskar AA, Al Numair KS, Gabriel Paulraj M, Alsaif MA, Muamar MA, et al. (2012) β-sitosterol prevents lipid peroxidation and improves antioxidant status and histoarchitecture in rats with 1, 2-dimethylhydrazine-induced colon cancer. J Med Food 15: 335-343.
6. Liz R, Pereira DF, Horst H, Dalmarco EM, Dalmarco JB, et al. (2011) Protected effect of Esenbeckia leiocarpa upon the inflammatory response induced by carrageenan in a murine air pouch model. Int Immunopharmacol 11: 1991-1999.
7. Baskar AA, Ignacimuthu S, Paulraj GM, Al Numair KS (2010) Chemopreventive potential of beta-Sitosterol in experimental colon cancer model -an in vitro and in vivo study. BMC Complement Altern Med 10: 24-30.
8. Gilani AH, Khan AU, Raoof M, Ghayur MN, Siddiqui BS, et al. (2008) Gastrointestinal, selective airways and urinary bladder relaxant effects of Hyoscyamus niger are mediated through dual blockade of muscarinic receptors and Ca2+ channels. Fundam Clin Pharmacol 22: 87-99.
9. Plat J, van Onselen EN, van Heugten MM, Mensink RP (2000) Effects on serum lipids, lipoproteins and fat soluble antioxidant concentrations of consumption frequency of margarines and shortenings enriched with plant stanol esters. Eur J Clin Nutr 54: 671-677.
10. Ostlund RE Jr, Lin X (2006) Regulation of cholesterol absorption by phytosterols. Curr Atheroscler Rep 8: 487-491.
11. De Smet E, Mensink RP, Plat J (2012) Effects of plant sterols and stanols on intestinal cholesterol metabolism: suggested mechanisms from past to present. Mol Nutr Food Res 56: 1058-1072.
12. Shishodia S, Aggarwal BB (2004) Guggulsterone inhibits NF-kappaB and IkappaBalpha kinase activation, suppresses expression of anti-apoptotic gene products, and enhances apoptosis. J Biol Chem. 279: 47148-47158.
13. Medeiros R, Otuki MF, Avellar MC, Calixto JB (2007) Mechanisms underlying the inhibitory actions of the pentacyclic triterpene alpha-amyrin in the mouse skin inflammation induced by phorbol ester 12-O-tetradecanoylphorbol-13- acetate. Eur J Pharmacol 559: 227-235.
14. Vitor CE, Figueiredo CP, Hara DB, Bento AF, Mazzuco TL, et al. (2009) Therapeutic action and underlying mechanisms of a combination of two pentacyclic triterpenes, alpha- and beta-amyrin, in a mouse model of colitis. Br J Pharmacol 157: 1034-1044.
15. Holanda Pinto SA, Pinto LM, Cunha GM, Chaves MH, Santos FA, et al. (2008) Anti-inflammatory effect of alpha, beta-amyrin, a pentacyclic triterpene from Protium heptaphyllum in rat model of acute periodontitis. Inflammopharmacology 16: 48-52.
16. De Jong A, Plat J, Bast A, Godschalk RW, Basu S, et al. (2008) Effects of plant sterol and stanol ester consumption on lipid metabolism, antioxidant status and markers of oxidative stress, endothelial function and low-grade inflammation in patients on current statin treatment. Eur J Clin Nutr 62: 263-273.
17. Hallikainen M, Lyyra-Laitinen T, Laitinen T, Moilanen L, Miettinen TA, et al. (2008) Effects of plant stanol esters on serum cholesterol concentrations, relative markers of cholesterol metabolism and endothelial function in type 1 diabetes. Atherosclerosis 199: 432-439.
18. Libby P (2002) Inflammation in atherosclerosis. Nature 420: 868-874.
19. Bak MJ, Hong SG, Lee JW, Jeong WS (2012) Red ginseng marc oil inhibits iNOS and COX-2 via NFkB and p38 pathways in LPS-stimulated RAW 264.7 macrophages. Molecules. 17: 13769-13786.
20. Liz R, Zanatta L, dos Reis GO, Horst H, Pizzolatti MG, et al. (2013) Acute effect of b-sitosterol on calcium uptake mediates anti-inflammatory effect in murine activated neutrophils. J Pharm Pharmacol 65: 115-122.
21. Othman RA, Moghadasian MH (2011) Beyond cholesterol-lowering effects of plant sterols: clinical and experimental evidence of anti-inflammatory properties. Nutr Rev 69: 371-382.
22. Aragão GF, Cunha Pinheiro MC, Nogueira Bandeira P, Gomes Lemos TL, de Barros Viana GS (2007) Analgesic and anti-inflammatory activities of the isomeric mixture of alpha- and beta amyrin from Protium heptaphyllum (Aubl.) march. J Herb Pharmacother 7: 31-47.
23. Shi XZ, Winston JH, Sarna SK (2011) Differential immune and genetic responses in rat models of Crohn's colitis and ulcerative colitis. Am J Physiol Gastrointest Liver Physiol 300: G41-51.
24. Melger S, Karlsson A, Michaelsson E (2005) Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms. Am J Physiol Gastrointest Liver Physiol 288: G1328-1338.
25. Lee IA, Kim EJ, Kim DH (2012) Inhibitory effect of b-sitosterol on TNBSinduced colitis in mice. Planta Med 78: 896-898.
26. Cheon JH, Kim JS, Kim JM, Kim N, Jung HC, et al. (2006) Plant sterol guggulsterone inhibits nuclear factor-kB signaling in intestinal epithelial cells by blocking IkB kinase and ameliorates acute murine colitis. Inflamm Bowel Dis 12: 1152-1161.
27. Kim JM, Kang HW, Cha MY, Yoo D, Kim N, et al. (2010) Novel guggulsterone derivative GG-52 inhibits NF-kappaB signaling in intestinal epithelial cells and attenuates acute murine colitis. Lab Invest 90: 1004-1015.
28. Islam MS, Murata T, Fujisawa M, Nagasaka R, Ushio H, et al. (2008) Antiinflammatory effects of phytosteryl ferulates in colitis induced by dextran sulphate sodium in mice. Br J Pharmacol 154: 812-824.
29. Villaseñor IM, Angelada J, Canlas AP, Echegoyen D (2002) Bioactivity studies on beta-sitosterol and its glucoside. Phytother Res 164: 17-21.
30. Calpe-Berdiel L, Escolà-Gil JC, Benítez S, Bancells C, González-Sastre F, et al. (2007) Dietary phytosterols modulate T-helper immune response but do not induce apparent anti-inflammatory effects in a mouse model of acute, aseptic inflammation. Life Sci 80: 1951-1956.
31. Ko JK, Auyeung KK (2014) Inflammatory Bowel Disease: Etiology, Pathogenesis and Current Therapy. Curr Pharm Res 20: 1082-1096.
32. Manz M, Vavricka SR, Wanner R, Lakatos PL, Rogler G, et al. (2012) Therapy of steroid-resistant inflammatory bowel disease. Digestion 86: 11-15.
33. Ardizzone S, Bianchi Porro G (2005) Biologic therapy for inflammatory bowel disease. Drugs 65: 2253-2286.
34. Hur SJ, Kang SH, Jung HS, Kim SC, Jeon HS, et al. (2012) Review of natural products actions on cytokines in inflammatory bowel disease. Nutr Res 32: 801-816.
35. Aldini R, Budriesi R, Roda G, Micucci M, Ioan P, et al. (2012) Curcuma longa extract exerts a myorelaxant effect on the ileum and colon in a mouse experimental colitis model, independent of the anti-inflammatory effect. PLOS One 7: e44650. Available: https://www journal.pone.0044650
36. Brewer S, McPherson M, Fujiwara D, Turovskaya O, Ziring D, et al. (2008) Molecular imaging of murine intestinal inflammation with 2-deoxy-2- [18F]fluoro-D-glucose and positron emission tomography. Gastroenterology 135: 744-755.
37. Hindryckx P, Staelens S, Devisscher L, Deleye S, De Vos F, et al. (2011) Longitudinal quantification of inflammation in the murine dextran sodium sulfate-induced colitis model using mPET/CT. Inflamm Bowel Dis 17: 2058-2064.
38. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. J Pharmacol Pharmacother 1: 94-99.
39. McGrath J, Drummond G, Kilkenny C, Wainwright C (2010) Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
40. Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22: 659-661.
41. Waldner MJ Neurath MF (2009) Chemically induced mouse models of colitis. Curr Protoc Pharmacol 46: 5.55.1-5.55.15.
42. Wirtz S, Neufert C, Weigmann B, Neurath MF (2007) Chemically induced mouse models of intestinal inflammation. Nat Protoc 2: 541-546.
43. Fitzpatrick LR, Wang J, Le M (2000) In vitro and in vivo effects of gliotoxin, a fungal metabolite: Efficacy against dextran sodium sulfate-induced colitis in rats. Dig Dis Sci 45: 2327-2336.
44. Durkee BY, Weichert JP, Halberg RB (2010) Small animal micro-CT colonography. Methods 50: 36-41.
45. GraphPad, version 5.0; GraphPad Software, Inc.: San Diego, CA.
46. Roda A, Gioacchini AM, Cerrè C, Baraldini M (1995) High-performance liquid chromatographic-electrospray mass spectrometric analysis of bile acids in biological fluids. J Chromatogr B Biomed Appl 665: 281-294.
47. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52: 302-310.
48. Takada M Ikenoya S, Yuzuriha T, Katayama K (1984) Simultaneous determination of reduced and oxidized ubiquinones. Methods Enzymol 105: 147-155.
49. Micucci M, Aldini R, Cevenini M, Colliva C, Spinozzi S, et al. (2013) Curcuma Longa L. as aTherapeutic Agent in Intestinal Motility Disorders.2: Safety Profile in Mouse. PLOS ONE 8: e80925. Available: http://www. plosone. journal.pone.0080925.
50. Arunlakshana D, Schild HO (1959) Some Quantitative Uses of Drug Antagonists. Br. J. Pharmacol 14: 48-58.
51. Tallarida RJ, Murray RB (1987) Manual of Pharmacologic Calculations with Computer Programs, 2nd ed. New York: Springer-Verlag.
52. Perlman SB, Perlman SB, Hall BS, Reichelderfer M (2013) PET/CT Imaging of Inflammatory Bowel Disease. Semin Nucl Med 43: 420-426.
53. Fenoglio-Preiser CM, Noffsinger AE, Stemmermann GN, Lantz PE, Isaacson PJ (2008) Gastrointestinal Pathology. 3rd edition. Lippincott WW 2008 Ed. p 64.
54. Strober W, Fuss IJ, Blumberg RS (2002) The immunology of mucosal models of inflammation. Annu Rev Immunol 20: 495-549.
55. Vaughn BP, Shah S, Cheifetz AS (2014) The role of mucosal healing in the treatment of patients with inflammatory bowel disease. Curr Treat Options Gastroenterol 12: 103-117.
56. Heylen M, Deleye S, De Man JG, Ruyssers NE, Vermeulen W, et al. (2013) Colonoscopy and mPET/CT arevalid techniques to monitor inflammation in the adoptive transfer colitis model in mice. Inflamm Bowel Dis 19: 967-976.
57. Moreno JJ (2003) Effect of olive oil minor components on oxidative stress and arachidonic acid mobilization and metabolism by macrophages RAW 264.7. Free Radic Biol Med 35: 1073-1081.
58. De Jong A, Plat J, Mensink RP (2003) Metabolic effects of plant sterols and stanols. J Nutr Biochem 14: 362-369.
59. Haç-Wydro K (2013) The effect of b-sitosterol on the properties of cholesterol/phosphatidylcholine/ganglioside monolayers-The impact of monolayer fluidity. Colloids Surf B Biointerfaces 110: 113-119.
60. Naito Y, Konishi C, Ohara N (2000) Blood coagulation and osmolar tolerance of erythrocytes in stroke-prone spontaneously hypertensive rats given rapeseed oil or soybean oil as the only dietary fat. Toxicol Lett 116: 209-215.
61. Demonty I, Ebine N, Jia X, Jones PJ (2005) Fish oil fatty acid esters of phytosterols alter plasma lipids but not red blood cell fragility in hamsters. Lipids 40: 695-702.
62. Choi M, Moschetta A, Bookout AL, Peng L, Umetani M, et al. (2006) Identification of a Hormonal Basis for Gallbladder Filling. Nature Med 12: 1253-1255.
63. Lavoie B, Balemba OB, Godfrey C, Watson CA, Vassileva G, et al (2010) Hydrophobic bile salts inhibit gallbladder smooth muscle function via stimulation of GPBAR1 receptors and activation of KATP channels. J Physiol 588: 3295-305.
64. Li T, Holmstrom SR, Kir S, Umetani M, Schmidt DR, et al. (2011) The G protein-coupled bile acid receptor, TGR5, stimulates gallbladder filling. Mol Endocrinol 25: 1066-1071.
65. Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, et al. (1999) Identification of a nuclear receptor for bile acids. Science 284: 1362-1365.
66. Maruyama T, Miyamoto Y, Nakamura T, Tamai Y, Okada H, et al. (2002) Identification of membrane-type receptor for bile acids (M-BAR). Biochem Biophys Res Commun 298: 714-719.
67. Grossi L, McHugh K, Collins SM (1993) On the specificity of altered muscle function in experimental colitis in rats. Gastroenterology 104: 1049-1056.
68. Wells RW, Blennerhassett MG (2004) Persistent and selective effects of inflammation on smooth muscle cell contractilityin rat colitis. Pflugers Arch 448: 515-524.
69. Villanacci V, Bassotti G, Nascimbeni R, Antonelli E, Cadei M, et al. (2008) Enteric nervous system abnormalities in inflammatory bowel diseases. Neurogastroenterol Motil 20: 1009-1016.
70. O'Hara JR, Lomax AE, Mawe GM, Sharkey KA (2007) Ileitis alters neuronal and enteroendocrine signalling in guinea pig distal colon. Gut 56: 186-194.
71. Hokama A, Ohira T, Kishimoto K, Kinjo F, Fujita J (2012) Impending megacolon: small bowel distension as a predictor of toxic megacolon in ulcerative colitis. Intern Emerg Med 7: 487-488.
72. Kerr PM, Hillier K, Wallis RM, Garland CJ (1995) Characterization of muscarinic receptors mediating contractions of circular and longitudinal muscle of human isolated colon. Br J Pharmacol 115: 1518-1524.
73. Hirota TCL, McKay DM (2006) Cholinergic regulation of epithelial ion transport in the mammalian intestine. Br J Pharmacol 149: 463-479.
74. Khan MR, Yazawa T, Anisuzzaman AS, Semba S, Ma Y, et al. (2014) Activation of focal adhesion kinase via M1 muscarinic acetylcholine receptor is required in restitution of intestinal barrier function after epithelial injury. Biochim Biophys Acta 1842: 635-645.
75. Khan MR, Anisuzzaman AS, Semba S, Ma Y, Uwada J, et al. (2013) M1 is a major subtype of muscarinic acetylcholine receptors on mouse colonic epithelial cells. J Gastroenterol 48: 885-896.