Pro-oxidant and proapoptotic effects of cholesterol oxidation products on human colonic epithelial cells: A potential mechanism of inflammatory bowel disease progression

Free Radical Biology and Medicine

Volumn 47, Issue 12, 2009, Pages 1731-1741

  Biasi, Fiorella ^a   Mascia, Cinzia ^a   Astegiano, Marco ^b   Chiarpotto, Elena ^a   Nano, Mario ^a   Vizio, Barbara ^a   Leonarduzzi, Gabriella ^a   Poli, Giuseppe ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b MOLINETTE HOSPITAL   (Italy)

Author keywords

Apoptosis; Colonic mucosa; Free radicals; Inflammatory bowel disease; NADPH oxidase; Oxysterols; Reactive oxygen species

Indexed keywords

ALKALINE PHOSPHATASE; CASPASE 3; CHOLESTEROL; CYTOCHROME C; OXYSTEROL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN CACO 2; COLON MUCOSA; DISEASE COURSE; ENTERITIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; MITOCHONDRION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

APOPTOSIS; CACO-2 CELLS; CELL DIFFERENTIATION; CHOLESTEROL; COLON; CYTOPROTECTION; DISEASE PROGRESSION; ENZYME ACTIVATION; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; NADPH OXIDASE; OXIDANTS; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES;

EID: 70449528623     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.09.020     Document Type: Article

References (41)

1. Leonarduzzi G., Sottero B., and Poli G. Oxidized products of cholesterol: dietary and metabolic origin, and proatherosclerotic effects. J. Nutr. Biochem. 13 (2002) 700-710
2. Poli G., Sottero B., Gargiulo S., and Leonarduzzi G. Cholesterol oxidation products in the vascular remodeling due to atherosclerosis. Mol. Aspects Med. 30 (2009) 180-189
3. Pie J.E., Spahis K., and Seillan C. Evaluation of oxidative degradation of cholesterol in food and food ingredients: identification and quantification of cholesterol oxides. J. Agric. Food Chem. 38 (1990) 973-979
4. Rey A.I., Kerry J.P., Lynch P.B., Lopez-Bote C.J., Buckley D.J., and Morrissey P.A. Effect of dietary oils and alpha-tocopheryl acetate supplementation on lipid (TBARS) and cholesterol oxidation in cooked pork. J. Anim. Sci. 79 (2001) 1201-1208
5. Constant J. The role of eggs, margarines and fish oils in the nutritional management of coronary artery disease and strokes. Keio J. Med. 53 (2004) 131-136
6. Wójcicka G., Jamroz-Wiśniewska A., Horoszewicz K., Bełtowski J., and Liver X. receptors (LXRs). Part I. Structure, function, regulation of activity, and role in lipid metabolism. Postepy. Hig. Med. Dosw. 61 (2007) 736-759
7. Plat J., Nichols J.A., and Mensink R.P. Plant sterols and stanols: effects on mixed micellar composition and LXR (target gene) activation. J. Lipid Res. 46 (2005) 2468-2476
8. Eder K., Muller G., Kluge H., Hirche F., and Brandsch C. Concentrations of oxysterols in meat and meat products from pigs fed diets differing in type of fat (palm oil or soybean oil) and vitamin E concentrations. Meat Sci. 70 (2005) 15-23
9. Vejux A., Malvitte L., and Lizard G. Side effects of oxysterols: cytotoxicity, oxidation, inflammation, and phospholipidosis. Braz. J. Med. Biol. Res. 41 (2008) 545-556
10. Kanner J. Dietary advanced lipid oxidation endproducts are risk factors to human health. Mol. Nutr. Food Res. 51 (2007) 1094-1101
11. Brown A.J., and Jessup W. Oxysterols and atherosclerosis. Atherosclerosis 142 (1999) 1-28
12. Schroepfer Jr. G.J. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol. Rev. 80 (2000) 361-554
13. Van Amerongen A., Demel R.A., Westerman J., and Wirtz K.W. Transfer of cholesterol and oxysterol derivatives by the nonspecific lipid transfer protein (sterol carrier protein 2): a study on its mode of action. Biochim. Biophys. Acta 1004 (1989) 36-43
14. Kan C.C., Yan J., and Bittman R. Rates of spontaneous exchange of synthetic radiolabeled sterols between lipid vesicles. Biochemistry 31 (1992) 1866-1874
15. Vejux A., and Lizard G. Cytotoxic effects of oxysterols associated with human diseases: induction of cell death (apoptosis and/or oncosis), oxidative and inflammatory activities, and phospholipidosis. Mol. Aspects Med. 30 (2009) 153-170
16. Lordan S., Mackrill J.J., and O'Brien N.M. Oxysterols and mechanisms of apoptotic signaling: implications in the pathology of degenerative diseases. J. Nutr. Biochem. 20 (2009) 321-336
17. Biasi F., Leonarduzzi G., Vizio B., Zanetti D., Sevanian A., Sottero B., Verde V., Zingaro B., Chiarpotto E., and Poli G. Oxysterol mixtures prevent pro-apoptotic effects of 7-ketocholesterol in macrophages: implications for proatherogenic gene modulation. FASEB J. 18 (2004) 693-695
18. Berthier A., Lemaire-Ewing S., Prunet C., Montange T., Vejux A., Pais de Barros J.P., Monier S., Gambert P., Lizard G., and Néel D. 7-Ketocholesterol-induced apoptosis: involvement of several apoptotic but also anti-apoptotic calcium-dependent transduction pathways. FEBS Lett. 272 (2005) 3093-3104
19. Leonarduzzi G., Poli G., Sottero B., and Biasi F. Activation of the mitochondrial pathway of apoptosis by oxysterols. Front. Biosci. 12 (2007) 791-799
20. Lemaire-Ewing S., Prunet C., Montange T., Vejux A., Berthier A., Bessède G., Corcos L., Gambert P., Néel D., and Lizard G. Comparison of the cytotoxic, pro-oxidant and pro-inflammatory characteristics of different oxysterols. Cell. Biol. Toxicol. 21 (2005) 97-114
21. Rosenblat M., and Aviram M. Oxysterol-induced activation of macrophage NADPH-oxidase enhances cell-mediated oxidation of LDL in the atherosclerotic apolipoprotein E deficient mouse: inhibitory role for vitamin E. Atherosclerosis 160 (2002) 69-80
22. Pedruzzi E., Guichard C., Ollivier V., Driss F., Fay M., Prunet C., Marie J.C., Pouzet C., Samadi M., Elbim C., O'Dowd Y., Bens M., Vandewalle A., Gougerot-Pocidalo M.A., Lizard G., and Ogier-Denis E. NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol. Cell. Biol. 24 (2004) 10703-10717
23. Leonarduzzi G., Vizio B., Sottero B., Verde V., Gamba P., Mascia C., Chiarpotto E., Poli G., and Biasi F. Early involvement of ROS overproduction in apoptosis induced by 7-ketocholesterol. Antioxid. Redox Signaling 8 (2006) 375-380
24. O'Sullivan A.J., O'Callaghan Y.C., and O'Brien N.M. Differential effects of mixtures of cholesterol oxidation products on bovine aortic endothelial cells and human monocytic U937 cells. Int. J. Toxicol. 24 (2005) 173-179
25. Steffen Y., Wiswedel I., Peter D., Schewe T., and Sies H. Cytotoxicity of myeloperoxidase/nitrite-oxidized low-density lipoprotein toward endothelial cells is due to a high 7β-hydroxycholesterol to 7-ketocholesterol ratio. Free Radic. Biol. Med. 41 (2006) 1139-1150
26. Björkhem I., Cedazo-Minguez A., Leoni V., and Meaney S. Oxysterols and neurodegenerative diseases. Mol. Aspects Med. 30 (2009) 171-179
27. Biasi F., Mascia C., and Poli G. The contribution of animal fat oxidation products to colon carcinogenesis, through modulation of TGF-beta1 signaling. Carcinogenesis 29 (2008) 890-894
28. Podolsky D.K. Inflammatory bowel disease. N. Engl. J. Med. 347 (2002) 417-429
29. Ostanin D.V., Bao J., Koboziev I., Gray L., Robinson-Jackson S.A., Kosloski-Davidson M., Price V.H., and Grisham M.B. T cell transfer model of chronic colitis: concepts, considerations and tricks of the trade. Am. J. Physiol. Gastrointest. Liver Physiol. 296 (2009) 135-146
30. Rokutan K., Kawahara T., Kuwano Y., Tominaga K., Nishida K., and Teshima-Kondo S. Nox enzymes and oxidative stress in the immunopathology of the gastrointestinal tract. Semin. Immunopathol. 30 (2008) 315-327
31. Forsyth C.B., Banan A., Farhadi A., Fields J.Z., Tang Y., Shaikh M., Zhang L.J., Engen P.A., and Keshavarzian A. Regulation of oxidant-induced intestinal permeability by metalloprotease-dependent epidermal growth factor receptor signalling. J. Pharmacol. Exp. Ther. 321 (2007) 84-97
32. Hidalgo I.J., Raub T.J., and Borchardt R.T. Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96 (1989) 736-749
33. Lee I.J., Hom K., Bai G., and Shapiro M. NMR metabolomic analysis of Caco-2 cell differentiation. J. Proteome Res. 8 (2009) 4104-4108
34. Hossain Z., Konishi M., Hosokawa M., and Takahashi K. Effect of polyunsaturated fatty acid-enriched phosphatidylcholine and phosphatidylserine on butyrate-induced growth inhibition, differentiation and apoptosis in Caco-2 cells. Cell Biochem. Funct. 24 (2006) 159-165
35. Peterson G.L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83 (1977) 346-356
36. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
37. O'Sullivan A.J., O'Callaghan Y.C., Woods J.A., and O'Brien N.M. Toxicity of cholesterol oxidation products to Caco-2 and HepG2 cells: modulatory effects of alpha- and gamma-tocopherol. J. Appl. Toxicol. 23 (2003) 191-197
38. Ryan E., Chopra J., McCarthy F., Maguire A.R., and O'Brien N.M. Qualitative and quantitative comparison of the cytotoxic and apoptotic potential of phytosterol oxidation products with their corresponding cholesterol oxidation products. Br. J. Nutr. 94 (2005) 443-451
39. Roussi S., Winter A., Gosse F., Werner D., Zhang X., Marchioni E., Geoffroy P., Miesch M., and Raul F. Different apoptotic mechanisms are involved in the antiproliferative effects of 7beta-hydroxysitosterol and 7beta-hydroxycholesterol in human colon cancer cells. Cell Death Differ. 12 (2005) 128-135
40. Aupeix K., Weltin D., Mejia J.E., Christ M., Marchal J., Freyssinet J.M., and Bischoff P. Oxysterol-induced apoptosis in human monocytic cell lines. Immunobiology 194 (1995) 415-428
41. Larsson D.A., Baird S., Nyhalah J.D., Yuan X.M., and Li W. Oxysterol mixtures, in atheroma-relevant proportions, display synergistic and proapoptotic effects. Free Radic. Biol. Med. 41 (2006) 902-910