Nitrated oleic acid up-regulates PPARγ and attenuates experimental inflammatory bowel disease

Free Radical Biology and Medicine

Volumn 48, Issue 4, 2010, Pages 499-505

  Borniquel, Sara ^a   Jansson, Emmelie Å ^a   Cole, Marsha P ^b   Freeman, Bruce A ^b   Lundberg, Jon O ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Experimental colitis; Free radicals; Nitrated fatty acids; Nitric oxide; PPAR

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; FATTY ACID; MESALAZINE; NITROOCTADECENOIC OLEIC ACID; OLEIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; ENTERITIS; FEMALE; HUMAN; HUMAN CELL; MOUSE; NITRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; CELL CULTURE TECHNIQUES; FATTY ACIDS; FEMALE; FREE RADICALS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INFLAMMATORY BOWEL DISEASES; MESALAMINE; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; NITRIC OXIDE; OLEIC ACID; PPAR GAMMA; UP-REGULATION;

EID: 74149084013     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.11.014     Document Type: Article

References (34)

1. Lichtenstein G.R., Abreu M.T., Cohen R., and Tremaine W. American Gastroenterological Association Institute technical review on corticosteroids, immunomodulators, and infliximab in inflammatory bowel disease. Gastroenterology 130 (2006) 940-987
2. Dubuquoy L., Rousseaux C., Thuru X., Peyrin-Biroulet L., Romano O., Chavatte P., Chamaillard M., and Desreumaux P. PPARgamma as a new therapeutic target in inflammatory bowel diseases. Gut 55 (2006) 1341-1349
3. Rogler G. Significance of anti-inflammatory effects of PPARgamma agonists?. Gut 55 (2006) 1067-1069
4. Saubermann L.J., Nakajima A., Wada K., Zhao S., Terauchi Y., Kadowaki T., Aburatani H., Matsuhashi N., Nagai R., and Blumberg R.S. Peroxisome proliferator-activated receptor gamma agonist ligands stimulate a Th2 cytokine response and prevent acute colitis. Inflamm. Bowel Dis. 8 (2002) 330-339
5. Katayama K., Wada K., Nakajima A., Mizuguchi H., Hayakawa T., Nakagawa S., Kadowaki T., Nagai R., Kamisaki Y., Blumberg R.S., and Mayumi T. A novel PPAR gamma gene therapy to control inflammation associated with inflammatory bowel disease in a murine model. Gastroenterology 124 (2003) 1315-1324
6. Rousseaux C., Lefebvre B., Dubuquoy L., Lefebvre P., Romano O., Auwerx J., Metzger D., Wahli W., Desvergne B., Naccari G.C., Chavatte P., Farce A., Bulois P., Cortot A., Colombel J.F., and Desreumaux P. Intestinal antiinflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferator-activated receptor-gamma. J. Exp. Med. 201 (2005) 1205-1215
7. Ramakers J.D., Verstege M.I., Thuijls G., Te Velde A.A., Mensink R.P., and Plat J. The PPARgamma agonist rosiglitazone impairs colonic inflammation in mice with experimental colitis. J. Clin. Immunol. 27 (2007) 275-283
8. Su C.G., Wen X., Bailey S.T., Jiang W., Rangwala S.M., Keilbaugh S.A., Flanigan A., Murthy S., Lazar M.A., and Wu G.D.A. novel therapy for colitis utilizing PPAR-gamma ligands to inhibit the epithelial inflammatory response. J. Clin. Invest. 104 (1999) 383-389
9. Lewis J.D., Lichtenstein G.R., Stein R.B., Deren J.J., Judge T.A., Fogt F., Furth E.E., Demissie E.J., Hurd L.B., Su C.G., Keilbaugh S.A., Lazar M.A., and Wu G.D. An open-label trial of the PPAR-gamma ligand rosiglitazone for active ulcerative colitis. Am. J. Gastroenterol. 96 (2001) 3323-3328
10. Lewis J.D., Lichtenstein G.R., Deren J.J., Sands B.E., Hanauer S.B., Katz J.A., Lashner B., Present D.H., Chuai S., Ellenberg J.H., Nessel L., and Wu G.D. Rosiglitazone for active ulcerative colitis: a randomized placebo-controlled trial. Gastroenterology 134 (2008) 688-695
11. Lundberg J.O., Lundberg J.M., Alving K., and Weitzberg E. Nitric oxide and inflammation: the answer is blowing in the wind. Nat. Med. 3 (1997) 30-31
12. Lundberg J.O., Hellstrom P.M., Lundberg J.M., and Alving K. Greatly increased luminal nitric oxide in ulcerative colitis. Lancet 344 (1994) 1673-1674
13. Rubbo H., Radi R., Trujillo M., Telleri R., Kalyanaraman B., Barnes S., Kirk M., and Freeman B.A. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation: formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 269 (1994) 26066-26075
14. Lima E.S., Di Mascio P., Rubbo H., and Abdalla D.S. Characterization of linoleic acid nitration in human blood plasma by mass spectrometry. Biochemistry 41 (2002) 10717-10722
15. Cui T., Schopfer F.J., Zhang J., Chen K., Ichikawa T., Baker P.R., Batthyany C., Chacko B.K., Feng X., Patel R.P., Agarwal A., Freeman B.A., and Chen Y.E. Nitrated fatty acids: endogenous anti-inflammatory signaling mediators. J. Biol. Chem. 281 (2006) 35686-35698
16. Baker P.R., Lin Y., Schopfer F.J., Woodcock S.R., Groeger A.L., Batthyany C., Sweeney S., Long M.H., Iles K.E., Baker L.M., Branchaud B.P., Chen Y.E., and Freeman B.A. Fatty acid transduction of nitric oxide signaling: multiple nitrated unsaturated fatty acid derivatives exist in human blood and urine and serve as endogenous peroxisome proliferator-activated receptor ligands. J. Biol. Chem. 280 (2005) 42464-42475
17. Schopfer F.J., Lin Y., Baker P.R., Cui T., Garcia-Barrio M., Zhang J., Chen K., Chen Y.E., and Freeman B.A. Nitrolinoleic acid: an endogenous peroxisome proliferator-activated receptor gamma ligand. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 2340-2345
18. Nettles K.W. Insights into PPARgamma from structures with endogenous and covalently bound ligands. Nat. Struct. Mol. Biol. 15 (2008) 893-895
19. Ito R., Shin-Ya M., Kishida T., Urano A., Takada R., Sakagami J., Imanishi J., Kita M., Ueda Y., Iwakura Y., Kataoka K., Okanoue T., and Mazda O. Interferon-gamma is causatively involved in experimental inflammatory bowel disease in mice. Clin. Exp. Immunol. 146 (2006) 330-338
20. Jansson E.A., Petersson J., Reinders C., Sobko T., Bjorne H., Phillipson M., Weitzberg E., Holm L., and Lundberg J.O. Protection from nonsteroidal anti-inflammatory drug (NSAID)-induced gastric ulcers by dietary nitrate. Free Radic. Biol. Med. 42 (2007) 510-518
21. Schopfer F.J., Batthyany C., Baker P.R., Bonacci G., Cole M.P., Rudolph V., Groeger A.L., Rudolph T.K., Nadtochiy S., Brookes P.S., and Freeman B.A. Detection and quantification of protein adduction by electrophilic fatty acids: mitochondrial generation of fatty acid nitroalkene derivatives. Free Radic. Biol. Med. 46 (2009) 1250-1259
22. Rudolph V., Schopfer F.J., Khoo N.K., Rudolph T.K., Cole M.P., Woodcock S.R., Bonacci G., Groeger A.L., Golin-Bisello F., Chen C.S., Baker P.R., and Freeman B.A. Nitro-fatty acid metabolome: saturation, desaturation, beta-oxidation, and protein adduction. J. Biol. Chem. 284 (2009) 1461-1473
23. Diaz-Granados N., Howe K., Lu J., and McKay D.M. Dextran sulfate sodium-induced colonic histopathology, but not altered epithelial ion transport, is reduced by inhibition of phosphodiesterase activity. Am. J. Pathol. 156 (2000) 2169-2177
24. Baker P.R., Schopfer F.J., Sweeney S., and Freeman B.A. Red cell membrane and plasma linoleic acid nitration products: synthesis, clinical identification, and quantitation. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 11577-11582
25. Adachi M., Kurotani R., Morimura K., Shah Y., Sanford M., Madison B.B., Gumucio D.L., Marin H.E., Peters J.M., Young H.A., and Gonzalez F.J. Peroxisome proliferator activated receptor gamma in colonic epithelial cells protects against experimental inflammatory bowel disease. Gut 55 (2006) 1104-1113
26. Desreumaux P., Dubuquoy L., Nutten S., Peuchmaur M., Englaro W., Schoonjans K., Derijard B., Desvergne B., Wahli W., Chambon P., Leibowitz M.D., Colombel J.F., and Auwerx J. Attenuation of colon inflammation through activators of the retinoid X receptor (RXR)/peroxisome proliferator-activated receptor gamma (PPARgamma) heterodimer: a basis for new therapeutic strategies. J. Exp. Med. 193 (2001) 827-838
27. Baker L.M., Baker P.R., Golin-Bisello F., Schopfer F.J., Fink M., Woodcock S.R., Branchaud B.P., Radi R., and Freeman B.A. Nitro-fatty acid reaction with glutathione and cysteine: kinetic analysis of thiol alkylation by a Michael addition reaction. J. Biol. Chem. 282 (2007) 31085-31093
28. Yong L., Zhang J., Schopfer F.J., Martynowski D., Garcia-Barrio M.T., Kovach A., Suino-Powell K., Baker P.R.S., Freeman B.A., Chen Y.E., and Xu H.E. Molecular recognition of nitrated fatty acids by PPAR γ. Nat. Struct. Mol. Biol. 15 (2008) 865-867
29. Chen C., Shah Y.M., Morimura K., Krausz K.W., Miyazaki M., Richardson T.A., Morgan E.T., Ntambi J.M., Idle J.R., and Gonzalez F.J. Metabolomics reveals that hepatic stearoyl-CoA desaturase 1 downregulation exacerbates inflammation and acute colitis. Cell Metab. 7 (2008) 135-147
30. Bassaganya-Riera J., Reynolds K., Martino-Catt S., Cui Y., Hennighausen L., Gonzalez F., Rohrer J., Benninghoff A.U., and Hontecillas R. Activation of PPAR gamma and delta by conjugated linoleic acid mediates protection from experimental inflammatory bowel disease. Gastroenterology 127 (2004) 777-791
31. Lundberg J.O., Weitzberg E., Lundberg J.M., and Alving K. Intragastric nitric oxide production in humans: measurements in expelled air. Gut 35 (1994) 1543-1546
32. Lundberg J.O., Weitzberg E., and Gladwin M.T. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat. Rev. Drug Discov. 7 (2008) 156-167
33. Lundberg J.O., Weitzberg E., Cole J.A., and Benjamin N. Nitrate, bacteria and human health. Nat. Rev. Microbiol. 2 (2004) 593-602
34. Alarcon de la Lastra C., Barranco M.D., Motilva V., and Herrerias J.M. Mediterranean diet and health: biological importance of olive oil. Curr. Pharm. Des. 7 (2001) 933-950