Intestinal-specific PPARγ deficiency enhances tumorigenesis in ApcMin/+ mice

International Journal of Cancer

Volumn 119, Issue 10, 2006, Pages 2339-2346

  McAlpine, Christen A ^a   Barak, Yaacov ^b   Matise, Ilze ^c   Cormier, Robert T ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b JACKSON LABORATORY   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Apc; Colon cancer; Min; PPAR

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; LIGAND; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; 2 THIAZOLINETHIONE; THIAZOLE DERIVATIVE; THIAZOLIDINE DERIVATIVE; THIAZOLINE-2-THIONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INCIDENCE; COLON CANCER; COLON CARCINOGENESIS; COLON POLYP; CONTROLLED STUDY; FEMALE; GENDER; GENOTYPE; HETEROZYGOTE; HOMOZYGOTE; KNOCKOUT MOUSE; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; SMALL INTESTINE; ANIMAL; COLON TUMOR; DISEASE COURSE; GENETICS; IMMUNOHISTOCHEMISTRY; INTESTINE TUMOR; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHENOTYPE; SEX DIFFERENCE; TUMOR SUPPRESSOR GENE;

ANIMALS; COLONIC NEOPLASMS; DISEASE PROGRESSION; FEMALE; GENES, APC; GENOTYPE; IMMUNOHISTOCHEMISTRY; INTESTINAL NEOPLASMS; MALE; MICE; MICE, KNOCKOUT; PHENOTYPE; PPAR GAMMA; SEX FACTORS; THIAZOLES; THIAZOLIDINES;

EID: 33749633136     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22115     Document Type: Article

References (67)

1. Zhu Y, Qi C, Korenberg JR, Chen X-N, Noya D, Rao MS, Reddy JK. Structural organization of mouse peroxisome proliferator-activated receptor γ (mPPARγ) gene: alternative promoter use and different splicing yield two mPPARγ isoforms. Proc Natl Acad Sci USA 1995; 92:7921-5.
2. Berger J, Moller DE. The mechanisms of action of PPARs. Annu Rev Med 2002;53:409-35.
3. Kliewer SA, Forman BM, Blumberg B, Ong ES, Borgmeyer U, Mangelsdorf DJ, Umesono K, Evans RM. Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc Natl Acad Sci USA 1994;91:7355-9.
4. Tontonoz P, Hu E, Spiegelman BM. Regulation of adipocyte gene expression and differentiation by peroxisome proliferator activated receptor γ. Curr Opin Genet Dev 1995;5:571-6.
5. Kersten S, Desvergne B, Wahli W. Roles of PPARs in health and disease. Nature 2000;405:421-4.
6. Evans RM, Barish GD, Wang Y-X. PPARs and the complex journey to obesity. Nat Med 2004;10:1-7.
7. Lazar MA. PPARγ, 10 years later. Biochimie 2005;87:9-13.
8. Kota BP, Huang TH-W, Roufogalis BD. An overview on biological mechanisms of PPARs. Pharmacol Res 2005;51:85-94.
9. Michalik L, Desvergne B, Wahli W. Peroxisome-proliferator-activated receptors and cancers: complex stories. Nat Rev Cancer 2004; 4:61-70.
10. Gupta RA, Sarraf P, Mueller E, Brockman JA, Prusakiewicz JJ, Eng C, Willson TM, DuBois RN. Peroxisome proliferators-activated receptor γ-mediated differentiation. A mutation in colon cancer cells reveals divergent and cell type-specific mechanisms. J Biol Chem 2003;278:22669-77.
11. Sarraf P, Mueller E, Jones D, King FJ, DeAngelo DJ, Partridge JB, Holden SA, Chen LB, Singer S, Fletcher C, Spiegelman BM. Differentiation and reversal of malignant changes in colon cancer through PPARγ. Nat Med 1998;4:1046-52.
12. Matthiessen MW, Pedersen G, Albrektsen T, Adamsen S, Fleckner J, Brynskov J. Peroxisome proliferators-activated receptor expression and activation in normal human colonic epithelial cells and tubular adenomas. Scand J Gastroenterol 2005;40:198-205.
13. Chen GG, Xu H, Lee JFY, Subramaniam M, Leung KL, Wang SH, Chan UPF, Spelsberg TC. 15-hydroxy-eicosatetraenoic acid arrests growth of colorectal cancer cells via a peroxisome proliferators-activated receptorγ-dependent pathway. Int J Cancer 2003;107:837-43.
14. Huin C, Schohn H, Hatier R, Bentejac M, Antunes L, Plenat F, Bugaut M, Dauca M. Expression of peroxisome proliferator-activated receptors α and γ in differentiating human colon carcinoma Caco-2 cells. Biol Cell 2002;94:15-27.
15. Lauer C, Volkl A, Riedl S, Fahimi HD, Beier K. Impairment of peroxisomal biogenesis in human colon carcinoma. Carcinogenesis 1999;20:985-9.
16. Bogazzi F, Ultimieri F, Raggi F, Costa A, Gasperi M, Cecconi E, Mosca F, Bartalena L, Martino E. Peroxisome proliferator activated receptorγ expression is reduced in the colonic mucosa of acromegalic patients. J Clin Endocrinol Metab 2002;87:2403-6.
17. Sarraf P, Mueller E, Smith WM, Wright HM, Kum JB, Aaltonen LA, de la Chapelle A, Spiegelman BM, Eng C. Loss-of-function mutations in PPARγ associated with human colon cancer. Mol Cell 1999;3:799-804.
18. Feilchenfeldt J, Brundler M-A, Soravia C, Totsch M, Meier CA. Peroxisome proliferators-activated receptors (PPARs) and associated transcription factors in colon cancer: reduced expression of PPARγ-coactivator 1 (PGC-1). Cancer Lett 2004;203:25-33.
19. Su CG, Wen X, Bailey ST, Jiang W, Rangwala SM, Keilbaugh SA, Flanigan A, Murthy S, Lazar MA, Wu GD. A novel therapy for colitis utilizing PPAR-γ ligands to inhibit the epithelial inflammatory response. J Clin Invest 1999;104:383-9.
20. Wada K, Nakajima A, Blumberg RS. PPARγ and inflammatory bowel disease: a new therapeutic target for ulcerative colitis and Crohn's disease. Trends Mol Med 2001;7:329-31.
21. Desreumaux P, Dubuquoy L, Nutten S, Peuchmaur M, Englaro W, Schoonjans K, Derijard B, Desvergne B, Wahli W, Chambon P, Leibowitz MD, Colombel J-F, 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;193:827-38.
22. Tanaka T, Kohno H, Yoshitani S, Takashima S, Okumura A, Murakami A, Hosokawa M. Ligands for peroxisome proliferator-activated receptors α and γ inhibit chemically induced colitis and formation of aberrant crypt foci in rats. Cancer Res 2001;61:2424-8.
23. Saubermann LJ, Nakajima A, Wada K, Zhao S, Terauchi Y, Kadowaki T, Aburatani H, Matsuhashi N, Nagai R, Blumberg RS. Peroxisome proliferators- activated receptorγ agonist ligands stimulate a Th2 cytokine response and prevent acute colitis. Inflamm Bowel Dis 2002;8:330-9.
24. Dubuquoy L, Jansson EA, Deeb S, Rakotobe S, Karoui M, Colombel J-F, Auwerx J, Pettersson S, Desreumaux P. Impaired expression of peroxisome proliferators-activated receptor γ in ulcerative colitis. Gastroenterology 2003;124:1265-76.
25. Sanchez-Hidalgo M, Martin AR, Villegas I, Alarcon De La Lastra C. Rosiglitazone, an agonist of peroxisome proliferators-activated receptorγ, reduces chronic colonic inflammation in rats. Biochem Pharmacol 2005;69:1733-44.
26. Kohno H. Suzuki R, Sugie S, Tanaka T. Suppression of colitis-related mouse colon carcinogenesis by a COX-2 inhibitor and PPAR ligands. BMC Cancer 2005;5:46.
27. Saez E, Tontonoz P, Nelson MC, Alvarez JGA, U TM, Baird SM, Thomazy VA, Evans RM. Activators of the nuclear receptor PPARγ enhance colon polyp formation. Nat Med 1998;4:1058-61.
28. Min/+ mice. Nat Med 1998;4:1053-7.
29. min/+ mice by thiazolidinedione PPARγ agonists and a structurally unrelated PPARγ agonist. Toxicol Pathol 2004;32:58-63.
30. +/- double mutant mice. Int J Cancer 2005;116:495-9.
31. Jansson EA, Are A, Greicius G, Kuo I-C, Kelly D, Arulampalam V, Pettersson S. The Wnt/β-catenin signaling pathway targets PPARγ activity in colon cancer cells. Proc Natl Acad Sci USA 2005;102:1460-5.
32. Liu J, Farmer SR. Regulating the balance between peroxisome proliferators-activated receptorγ and β-catenin signaling during adipogenesis. A glycogen synthase kinase 3 β-phosphorylation-defective mutant of β-catenin inhibits expression of a subset of adipogenic genes. J Biol Chem 2004;279:45020-7.
33. Sharma C, Pradeep A, Wong L, Rana A, Rana B. Peroxisome proliferators-activated receptorγ activation can regulate β-catenin levels via a proteasome-mediated and adenomatous polyposis coli-independent pathway. J Biol Chem 2004;279:35583-94.
34. Niho N, Takahashi M, Kitamura T, Shoji Y, Itoh M, Noda T, Sugimura T, Wakabayashi K. Concomitant suppression of hyperlipidemia and intestinal polyp formation in Apc-deficient mice by peroxisome proliferators-activated receptor ligands. Cancer Res 2003;63:6090-5.
35. Niho N, Takahashi M, Shoji Y, Takeuchi Y, Matsubara S, Sugimura T, Wakabayashi K. Dose-dependent suppression of hyperlipidemia and intestinal polyp formation in Min mice by pioglitazone, a PPARγ ligand. Cancer Sci 2003;94:960-4.
36. Girnun GD, Smith WM, Drori S, Sarraf P, Mueller E, Eng C, Nambiar P, Rosenberg DW, Bronson RT, Edelmann W, Kucherlapati R, Gonzalez FJ, et al. APC-dependent suppression of colon carcinogenesis by PPARγ. Proc Natl Acad Sci USA 2002;99:13771-6.
37. He W, Barak Y, Hevener A, Olson P, Liao D, Le J, Nelson M, Ong E, Olefsky J, Evans RM. Adipose-specific peroxisome proliferators-activated receptor γ knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci USA 2003;100:15712-17.
38. Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM. PPARγ is required for placental, cardiac, and adipose tissue development. Mol Cell 1999;4:585-95.
39. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 2002;277:33275-83.
40. Pinto D, Robine S, Jaisser F, El Marjou F, Louvard D. Regulatory sequences of the mouse villin gene that efficiently drive transgenic expression in immature and differentiated epithelial cells of small and large intestines. J Biol Chem 1999;274:6476-82.
41. El Marjou F, Janssen K-P, Chang BH-J, Li M, Hindie V, Chan L, Louvard D, Chambon P, Metzger D, Robine S. Tissue-specific and inducible cre-mediated recombination in the gut epithelium. Genesis 2004;39:186-93.
42. Su L-K, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, Gould KA, Dove WF. Multiple intestinal neoplasia is caused by a mutation in the murine homolog of the APC gene. Science 1992;256:668-70.
43. Moser AR, Pilot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990;247:322-4.
44. AKR intestinal tumor resistance region consists of Pla2g2a and a locus distal to D4Mit64. Oncogene 2000;19:3182-92.
45. Xu B, Gottschalk W, Chow A, Wilson RI, Schnell E, Zang K, Wang D, Nocill RA, Lu B, Reichardt LF. Role of TrkB in the mature hippocampus. J Neurosci 2000;20:6888-97.
46. Cormier RT, Dove WF. Dnmt1 N/+ reduces the net growth rate and multiplicity of intestinal adenomas in C57BL/6-multiple intestinal neoplasia (Min)/+ mice independently of p53 but demonstrates strong synergy with the modifier of Min 1 (AKR) resistance allele. Cancer Res 2000;60:3965-70.
47. Boivin GP, Washington K, Yang K, Ward JM, Pretlow TP, Russell R, Besselsen DG, Godfrey VL, Doetschman T, Dove WF, Pilot HC, Halberg RB et al. Pathology of mouse models of intestinal cancer: consensus report and recommendations. Gastroenterology 2003;124:762-77.
48. Takano H, Hasegawa H, Zou Y, Komuro I. Pleiotropic actions of PPARγ activators thiazolidinediones in cardiovascular diseases. Curr Pharm Des 2004;10:2779-86.
49. Watkins SM, Reifsnyder PR, Pan HJ, German JB, Leiter EH. Lipid metabolome-wide effects of the PPARγ agonist rosiglitazone. J Lipid Res 2002;43:1809-17.
50. Palakurthi SS, Aklas H, Grubissich LM, Mortensen RM, Halperin JA. Anticancer effects of thiazolidinediones are independent of peroxisome proliferator-activated receptor γ and mediated by inhibition of translation initiation. Cancer Res 2001;61:6213-18.
51. Baek SJ, Wilson LC, Hsi LC, Eling TE. Troglilazone, a peroxisome proliferators-activated receptor γ (PPARγ) ligand, selectively induces the early growth response-1 gene independently of PPARγ. J Biol Chem 2003;278:5845-53.
52. Rumi MA, Ishihara S, Kadowaski Y, Ortega-Cava CF, Kazumori H, Kawashima K, Yoshino N, Yuki T, Ishimura N, Kinoshita Y. Peroxisome proliferators- activated receptorγ-dependent and -independent growth inhibition of gastrointestinal tumour cells. Genes Cells 2004;9:1113-23.
53. Wang YL, Frauwirth KA, Rangwala SM, Lazar MA, Thompson CB. Thiazolidinedione activation of peroxisome proliferators-activated receptor γ can enhance mitochondrial potential and promote cell survival. J Biol Chem 2002;277:31781-8.
54. Naigamwalla D, Chia MC, Tran TT, Medline A, Hay K, Gallinger S, Bruce WR. Polyethylene glycol 8000 and colon carcinogenesis: inhibition in the F344 rat, promotion in the Min mouse. Cancer Res 2000; 60:6856-8.
55. Andreassen A, Vikse R, Steffensen IL, Paulson JA, Alexander J. Intestinal tumours induced by the food carcinogen 2-amino-1-melhyl-6-phenylimidazol[4,5- β]pyridine in multiple intestinal neoplasia mice have truncation mutations as well as loss of the wild-type Apc(+) allele. Mutagenesis 2001;16:309-15.
56. Cooper HS, Chang W-C, Coudry R, Gary MA, Everly L, Spittle CS, Wang H, Litwin S, Clapper ML. Generation of a unique strain of multiple intestinal neoplasia (Apc (+/Min-FCCC)) mice with significantly increased numbers of colorectal adenomas. Mol Carcinogen 2005;44:31-41.
57. Sorensen IK, Kristiansen E, Mortensen A, Nicolaisen GM, Wijnands JAH, van Kranen HJ, van Kreijl CF. The effect of soy isoflavones on the development of intestinal neoplasia in the ApcMin mouse. Cancer Lett 1998;130:217-25.
58. Paulsen JA, Elvsaas I-KO, Steffensen IL, Alexander J. A fish oil derived concentrate enriched in eicosapentaenoic and docosahexaenoic acid as ethyl ester suppresses the formation and growth of intestinal polyps in the Min mouse. Carcinogenesis 1997;18:1905-10.
59. Min/+ mouse model of colorectal cancer. Carcinogenesis 2005;26:587-95.
60. Kamei Y, Suzuki M, Miyazaki H, Tsuboyama-Kasaoka N, Wu J, Ishimi Y, Ezaki O. Ovariectomy in mice decreases lipid metabolism-related gene expression in adipose tissue and skeletal muscle with increased body fat. J Nutr Sci Vitaminol 2005;51:110-17.
61. Papadaki I, Mylona E, Giannopoulou I, Markaki S, Keramopoulos A, Nakapoulou L. PPARγ expression in breast cancer: clinical value and correlation with ERβ. Histopathology 2005;46:37-42.
62. Nunez SB, Medin JA, Braissant O, Kemp L, Wahli W, Ozato K, Segars JH. Retinoid X receptor and peroxisome proliferators-activated receptor activate an estrogen responsive gene independent of the estrogen receptor. Mol Cell Endocrinol 1997;127:27-40.
63. Rieusset J, Seydoux J, Anghel SI, Escher P, Michalik L, Soon TN, Metzger D, Chambon P, Wahli W, Desvergne B. Altered growth in male peroxisome proliferators-activated receptorγ (PPARγ) heterozygous mice: involvement of PPARγ in a negative feedback regulation of growth hormone action. Mol Endocrinol 2004;18:2363-77.
64. Miles PDG, Barak Y, He W, Evans RM, Olefsky JM. Improved insulin-sensitivity in mice heterozygous for PPAR-γ deficiency. J Clin Invest 2000;105:287-92.
65. Mehl KA, Davis JM, Clements JM, Berger FG, Pena MM, Carson JA. Decreased intestinal polyp multiplicity is related to exercise mode and gender in Apc Min/+ mice. J Appl Physiol 2005;98:2219-25.
66. Yamauchi T, Kamon J, Waki H, Murakami K, Motojima K, Komeda K, Ide T, Kubota N, Terauchi Y, Tobe K, Miki H, Tsuchida A et al. The mechanisms by which both heterozygous peroxisome proliferators-activated receptor γ (PPARγ) deficiency and PPARγ agonist improve insulin resistance. J Biol Chem 2001;276:41245-54.
67. Norris AW, Chen L, Fisher SJ, Szanto I, Ristow M, Jozsi AC, Hirshman MF, Rosen ED, Goodyear LJ, Gonzalez FJ, Spiegelman BM, Kahn CR. Muscle-specific PPARγ-deficient mice develop increased adiposity and insulin resistance but respond to thiazolidinediones. J Clin Invest 2003;112:608-18.