The peroxisome proliferator-activated receptor γ ligand rosiglitazone delays the onset of inflammatory bowel disease in mice with interleukin 10 deficiency

Inflammatory Bowel Diseases

Volumn 11, Issue 3, 2005, Pages 231-243

  Lytle, Christian ^a   Tod, Tara J ^a   Vo, Kathy T ^a   Lee, Jimmy W ^a   Atkinson, Roscoe D ^a   Straus, Daniel S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aquaporin 8; Crypt hyperplasia; Interferon ; Interleukin 17; PPAR

Indexed keywords

AQUAPORIN 8; CYTOKINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 17; LIGAND; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA LIGAND; ROSIGLITAZONE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; COLITIS; CONTROLLED STUDY; CRYPT CELL; DISEASE ACTIVITY; DISEASE COURSE; DISEASE MODEL; DRUG ACTIVITY; DRUG EFFECT; DRUG TARGETING; ENTERITIS; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; IN VIVO STUDY; INTESTINE CRYPT; MALE; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION; HYPERPLASIA; HYPOGLYCEMIC AGENTS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-10; MALE; MICE; PPAR GAMMA; THIAZOLIDINEDIONES;

EID: 15944422109     PISSN: 10780998     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.MIB.0000160805.46235.eb     Document Type: Article

References (72)

1. Friedman S, Blumberg RS. Inflammatory bowel disease. In: Braunwald E, Fauci AS, et al., eds. Harrison's Principles of Internal Medicine. 15th ed. New York: McGraw-Hill; 2001:1679-1695.
2. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347:417-429.
3. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol. 2003;3:521-531.
4. Wong NA, Harrison DJ. Colorectal neoplasia in ulcerative colitis: recent advances. Histopathology. 2001;39:221-234.
5. Berger J, Moller DE. The mechanisms of action of PPARs. Annu Rev Med. 2002;53:409-435.
6. Daynes RA, Jones DC. Emerging roles of PPARs in inflammation and immunity. Nat Rev Immunol. 2002;2:748-759.
7. Ricote M, Li AC, Willson TJ, et al. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature. 1998; 391:79-82.
8. Faveeuw C, Fougeray S, Angeli V, et al. Peroxisome proliferator-activated receptor γ activators inhibit interleukin-12 production in murine dendritic cells. FEBS Lett. 2000;486:261-266.
9. Harris SG, Phipps RP. The nuclear receptor PPARγ is expressed by mouse T lymphocytes and PPAR gamma agonists induce apoptosis. Eur J Immunol. 2001;31:1098-1105.
10. Yang XY, Wang LH, Chen T, et al. Activation of human T lymphocytes is inhibited by peroxisome proliferator-activated receptor γ (PPARγ) agonists. J Biol Chem. 2000;275:4541-4544.
11. 2 inhibits multiple steps in the NF-κB signaling pathway. Proc Natl Acad Sci USA. 2000;97:4844-4849.
12. Saez E, Tontonoz P, Nelson MC, et al. Activators of the nuclear receptor PPARγ enhance colon polyp formation. Nat Med. 1998;4:1058-1061.
13. Lefebvre M, Paulweber B, Fajas L, et al. Peroxisome proliferator-activated receptor γ is induced during differentiation of colon epithelium cells. J Endocrinol. 1999; 162:331-340.
14. Girnun GD, Smith WM, Drori S, et al. APC-dependent suppression of colon carcinogenesis by PPARγ. Proc Natl Acad Sci USA 2002;99: 13771-13776.
15. Sarraf P, Mueller E, Jones D, et al. Differentiation and reversal of malignant changes in colon cancer through PPARγ. Nat Med. 1998;4: 1046-1052.
16. Gupta RA, Brockman JA, Sarraf P, et al. Target genes of peroxisome proliferator-activated receptor γ in colorectal cancer cells. J Biol Chem. 2001;276:29681-29687.
17. Gupta RA, Sarraf P, Brockman JA, et al. Peroxisome proliferator-activated receptor γ and transforming growth factor-β pathways inhibit intestinal epithelial cell growth by regulating levels of TSC-22. J Biol Chem. 2003; 278:7431-7438.
18. Su CG, Wen X, Bailey ST, et al. A novel therapy for colitis utilizing PPARγ ligands to inhibit the epithelial inflammatory response. J Clin Invest. 1999;104:383-389.
19. Tanaka T, Kohno H, Yoshitani S, et al. Ligands for peroxisome proliferator-activated receptors α and γ inhibit chemically induced colitis and formation of aberrant crypt foci in rats. Cancer Res. 2001;61:2424-2428.
20. Desreumaux P, Dubuquoy L, Nutten S, et al. Attenuation of colon inflammation through activators of the retinoid X receptor (RXR)/peroxisome proliferator-activated receptor γ (PPARγ) heterodimer: A basis for new therapeutic strategies. J Exp Med. 2001;193:827-838.
21. Saubermann LJ, Nakajima A, Wada K, et al. Peroxisome proliferatoractivated receptor γ agonist ligands stimulate a Th2 cytokine response and prevent acute colitis. Inflamm Bowel Dis. 2002;8:330-339.
22. Lewis JD, Lichtenstein GR, Stein RB, et al. An open-label trial for PPARγ ligand rosiglitazone for active ulcerative colitis. Am J Gastroenterol. 2001;96:3323-3328.
23. Osawa E, Nakajima A, Wada K, et al. Peroxisome proliferator-activated receptor γ ligands suppress colon carcinogenesis induced by azoxymethane in mice. Gastroenterology. 2003;124:361-367.
24. Girnun GD, Spiegelman BM. PPARγ ligands: taking Ppart in chemoprevention. Gastroenterology. 2003;124:564-567.
25. Wu GD. Is there a role for PPARγ in IBD? Yes, No, Maybe. Gastroenterology. 2003;124:1538-1542.
26. Kühn R, Löhler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263-274.
27. + TH1-like responses. J Clin Invest. 1996;98:1010-1020.
28. Davidson NJ, Hudak SA, Lesley RE, et al. IL-12, but not IFN-γ, plays a major role in sustaining the chronic phase of colitis in IL-10-deficient mice. J Immunol. 1998;161:3143-3149.
29. Spencer DM, Veldman GM, Banerjee S, et al. Distinct inflammatory mechanisms mediate early versus late colitis in mice. Gastroenterology. 2002;122:94-105.
30. Bristol IJ, Farmer MA, Cong Y, et al. Heritable susceptibility for colitis in mice induced by IL-10 deficiency. Inflamm Bowel Dis. 2000;6:290-302.
31. Farmer MA, Sundberg JP, Bristol IJ, et al. A major quantitative trait locus on chromosome 3 controls colitis severity in IL-10-deficient mice. Proc Natl Acad Sci USA. 2001;98:13820-13825.
32. Gennaro AR, eds. Remington's Pharmaceutical Sciences. 18th ed. Easton, PA: Mack Publishing Co.; 1990:1632.
33. McDaniel N, Lytle C. Parietal cells express high levels of Na-K-2C1 cotransporter on migrating into the gastric gland neck. Am J Physiol. 1999;276:G1273-G1278.
34. 2. Cell Growth Differ. 2002;13:409-420.
35. van de Wetering M, Sancho E, Verweij C, et al. The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell. 2002;111:241-250.
36. Aggarwal S, Gurney AL. IL-17: prototype member of an emerging cytokine family. J Leukoc Biol. 2002;7:1-8.
37. Aggarwal S, Ghilardi N, Xie MH, et al. Interleukin- 23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin17. J Biol Chem. 2003;278:1910-1914.
38. Nakae S, Komiyama Y, Nambu A, et al. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity. 2002; 17:375-377.
39. Ghilardi N, Kljavin N, Chen Q, et al. Compromised humoral and delayedtype hypersensitivity responses in IL-23-deficient mice. J Immunol. 2004;172:2827-2833.
40. Nakae S, Nambu A, Sudo K, et al. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol. 2003;171: 6173-6177.
41. Nakae S, Saijo S, Horai R, et al. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci USA. 2003;100: 5986-5990.
42. Ferretti S, Bonneau O, Dubois GR, et al. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J Immunol. 2003;170:2106-2112.
43. Fujino S, Andoh A, Bamba S, et al. Increased expression of interleukin 17 in inflammatory bowel disease. Gut. 2003;52:65-70.
44. Nielsen OH, Kirman I, Rudiger N, et al. Upregulation of interleukin-12 and -17 in active inflammatory bowel disease. Scand J Gastroenterol. 2003;38:180-185.
45. Dubuquoy L, Jansson EA, Deeb S, et al. Impaired expression of peroxisome proliferator-activated receptor γ in ulcerative colitis. Gastroenterology. 2003;124:1265-1276.
46. Hertzel AV, Bernlohr DA. The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends Endocrinol Metab. 2000;11:175-180.
47. Sweetser DA, Birkenmeier EH, Hoppe PC, et al. Mechanisms underlying generation of gradients in gene expression within the intestine: an analysis using transgenic mice containing fatty acid binding protein-human growth hormone fusion genes. Genes Dev. 1988;2:1318-1332.
48. Simon TC, Roth KA, Gordon JI. Use of transgenic mice to map cis-acting elements in the liver fatty acid-binding protein gene (Fabpl) that regulate its cell lineage-specific, differentiation-dependent, and spacial patterns of expression in the gut epithelium and in the liver acinus. J Biol Chem. 1993;268:18345-18358.
49. Poirier H, Braissant O, Niot I, et al. 9-cis-Retinoic acid enhances fatty acid-induced expression of the liver fatty acid-binding protein gene. FEBS Lett. 1997;412:480-484.
50. Chen M, Yang Y, Braunstein E, et al. Gut expression and regulation of FAT/CD36: possible role in fatty acid transport in rat enterocytes. Am J Physiol Endocrinol Metab. 2001;281:E916 E923.
51. Lobo MV, Huerta L, Ruiz-Velasco N, et al. Localization of the lipid receptors CD36 and CLA-1/SR-BI in the human gastrointestinal tract: towards the identification of receptors mediating the intestinal absorption of dietary lipids. J Histochem Cytochem. 2001;49:1253-1260.
52. Zhang X, Fitzsimmons RL, Cleland LG, et al. CD36/fatty acid translocase in rats: distribution, isolation from hepatocytes, and comparison with the scavenger receptor SR-B1. Lab Invest. 2003;83:317-332.
53. Tontonoz P, Nagy L, Alvarez JG, et al. PPARγ promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 1998;93: 241-252.
54. Sato O, Kuriki C, Fukui Y, et al. Dual promoter structure of mouse and human fatty acid translocase/CD36 genes and unique transcriptional activation by peroxisome proliferator-activated receptor α and γ ligands. J Biol Chem. 2002;277:15703-15711.
55. Welch JS, Ricote M, Akiyama TE, et al. PPARγ and PPARδ negatively regulate specific subsets of lipopolysaccharide and IFN-γ target genes in macrophages. Proc Natl Acad Sci USA. 2003;100:6712-6717.
56. Koyama Y, Yamamoto T, Tani T, et al. Expression and localization of aquaporins in rat gastrointestinal tract. Am J Physiol. 1999;276:C621-C627.
57. Elkjaer ML, Nejsum LN, Gresz V, et al. Immunolocalization of aquaporin8 in rat kidney, gastrointestinal tract, testis, and airways. Am J Physiol Renal Physiol. 2001;281:F1047-F1057.
58. Lodish H, Berk A, Zipursky SL, et al. Molecular Cell Biology. 4th ed. 2000:393-394.
59. Bishop-Bailey D, Hla T, Warner TD. Bisphenol A diglycidyl ether (BADGE) is a PPARγ agonist in an ECV304 cell line. Br J Pharmacol. 2000;131:651-654.
60. Shibuya A, Wada K, Nakajima A, et al. Nitration of PPARγ inhibits ligand-dependent translocation into the nucleus in a macrophage-like cell line, RAW 264. FEBS Lett. 2002;525:43-47.
61. Han J, Hajjar DP, Zhou X, et al. Regulation of peroxisome proliferatoractivated receptor-γ-mediated gene expression: a new mechanism of action for high density lipoprotein. J Biol Chem. 2002;277:23582-23586.
62. Hornung D, Waite LL, Ricke EA, et al. Nuclear peroxisome proliferatoractivated receptors α and γ have opposing effects on monocyte chemotaxis in endometriosis. J Clin Endocrinol Metab. 2002;86:3108-3114.
63. Akiyama TE, Baumann CT, Sakai S, et al. Selective intranuclear redistribution of PPAR isoforms by RXRα. Mol Endocrinol. 2002;16:707-721.
64. Berger J, Patel HV, Woods J, et al. A PPARγ mutant serves as a dominant negative inhibitor of PPAR signaling and is localized in the nucleus. Mol Cell Endocrinol. 2000;162:57-67.
65. Tontonoz P, Hu E, Spiegelman BM. Stimulation of adipogenesis in fibroblasts by PPARγ 2, a lipid-activated transcription factor. Cell. 1994; 79:1147-1156.
66. Li Y, Lazar MA. Differential gene regulation by PPARγ agonist and constitutively active PPARγ2. Mol Endocrinol. 2002;16:1040-1048.
67. Katayama K, Wada K, Nakajima A, et al. A Novel PPARγ gene therapy to control inflammation associated with inflammatory bowel disease in a murine model. Gastroenterology. 2003;124:1315-1324.
68. Greger R, Bleich M, Leipziger J, et al. Regulation of ion transport in colonic crypts. News Physiol Sci. 1997;12:62-66.
69. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 1996;87:159-170.
70. Li AC, Brown KK, Silvestre MJ, et al. Peroxisome proliferator-activated receptor γ ligands inhibit development of atherosclerosis in LDL receptordeficient mice. J Clin Invest. 2000;106:523-531.
71. Bolton GC, Keogh JP, East PD, et al. The fate of thiazolidinedione antidiabetic agent in rat and dog. Xenobiotica. 1996;26:627-636.
72. Cox PJ, Ryan DA, Hollis FJ, et al. Absorption, disposition, and metabolism of rosiglitazone, a potent thiazolidinedione insulin sensitizer, in humans. Drug Metab Dispos. 2000;28:772-780.