Thiazolidinediones inhibit growth of gastrointestinal, biliary, and pancreatic adenocarcinoma cells through activation of the peroxisome proliferator-activated receptor γ/retinoid X receptor α pathway

Experimental Cell Research

Volumn 289, Issue 1, 2003, Pages 143-151

  Tsujie, Masanori ^a   Nakamori, Shoji ^a   Okami, Jiro ^a   Hayashi, Nobuyasu ^a   Hiraoka, Nobuaki ^a   Nagano, Hiroaki ^a   Dono, Keizo ^a   Umeshita, Koji ^a   Sakon, Masato ^a   Monden, Morito ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

9 cis retinoic acid; Cell cycle; Differentiation; Growth inhibition; Peroxisome proliferator activated receptor; Thiazolidinedione

Indexed keywords

ALITRETINOIN; ANTINEOPLASTIC AGENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RETINOID X RECEPTOR; RS 1303; RS 1330; RS 1387; RS 1455; RS 1456; THIAZOLIDINE DERIVATIVE; TROGLITAZONE;

ADENOCARCINOMA; ANTINEOPLASTIC ACTIVITY; ARTICLE; BILE DUCT CARCINOMA; CANCER INHIBITION; CARCINOMA CELL; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFECT; GASTROINTESTINAL CARCINOMA; HUMAN; HUMAN CELL; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STATISTICAL SIGNIFICANCE; TRANSACTIVATION; TRANSCRIPTION INITIATION;

EID: 0043163884     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00263-5     Document Type: Article

References (45)

1. Mangelsdorf D.J., Thummel C., Beato M., Herrlich P., Schutz G., Umesono K., Blumberg B., Kastner P., Mark M., Chambon P., Evans R.M. The nuclear receptor superfamily the second decade. Cell. 83:1995;835-839.
2. Mukherjee R., Davies P.J.A., Crombie D.L., Bischoff E.D., Cesario R.M., Jow L., Hamann L.G., Boehm M.F., Monden C.E., Nadzan A.M., Paterniti J.R. Jr., Heyman R.A. Sensitization of diabetic and obese mice to insulin by retinoid X receptor agonists. Nature. 386:1997;407-410.
3. Schmidt A., Endo N., Rutledge S.J., Vogel R., Shinar D., Rodan G.A. Identification of a new member of the steroid hormone receptor superfamily that is activated by peroxisome proliferator and fatty acids. Mol. Endocrinol. 6:1992;1634-1641.
4. Kliewer S.A., Forman B.M., Blumberg B., Ong E.S., Borgmeyer U., Manglesdorf D.J., Umesono K., Evans R.M. Differential expression and activation of a family of murine peroxisome prolixferator-activated receptors. Proc. Natl. Acad. Sci. USA. 91:1994;7355-7359.
5. Tontonoz P., Hu E., Spiegelman B.M. Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor. Cell. 79:1994;1147-1156.
6. Hu E., Tontonoz P., Spiegelman B.M. Transdifferentiation of myoblasts by the adipogenic transcription factors PPARγ and C/EBPα Proc. Natl. Acad. Sci. USA. 92:1995;9856-9860.
7. Spiegelman B.M., Flier J.S. Adipogenesis and obesity rounding out the big picture. Cell. 87:1996;377-389.
8. 2 is a ligand for the adipocyte determination factor PPARγ Cell. 83:1995;803-812.
9. 2 metabolite binds peroxisome proliferator-activated receptor γ and promotes adipocyte differentiation. Cell. 83:1995;813-819.
10. Lehmann J.M., Moore L.B., Smith-Oliver T.A., Wilkison W.O., Wilson T.M., Kliewer S.A. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor γ (PPARγ). J. Biol. Chem. 270:1995;12953-12956.
11. Kliewer S.A., Sundseth S.S., Jones S.A., Brown P.J., Wisely G.B., Koble C.S., Devchand P., Wahli W., Wilson T.M., Lenhard J.M., Lehmann J.M. Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptor α and γ Proc. Natl. Acad. Sci. USA. 94:1997;4318-4323.
12. Lehmann J.M., Lenhard J.M., Oliver B.B., Ringold G.M., Kliewer S.A. Peroxisome proliferator-activated receptors alpha and gamma are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J. Biol. Chem. 272:1997;3406-3410.
13. Tontonoz P., Singer S., Forman B.M., Sarraf P., Fletcher J.A., Fletcher C.D.M., Brun R.P., Mueller E., Altiok S., Oppenheim H., Evans R.M., Spiegelman B.M. Terminal differentiation of human liposarcoma cells induced by ligands for peroxisome proliferator-activated receptor γ and the retinoid X receptor. Proc. Natl. Acad. Sci. USA. 94:1997;237-241.
14. Elstner E., Muller C., Koshizuka K., Williamson E.A., Park D., Asou H., Shintaku P., Said J.W., Heber D., Koeffler H.P. Ligands for peroxisome proliferator- activated receptor γ and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice. Proc. Natl. Acad. Sci. USA. 95:1998;8806-8811.
15. Kubota T., Koshizuka K., Williamson E.A., Asou H., Said J.W., Holden S., Miyoshi I., Koeffler H.P. Ligand for peroxisome proliferator-activated receptor γ (Troglitazone) has potent antitumor effect against human prostate cancer both in vitro and in vivo. Cancer Res. 58:1998;3344-3352.
16. Brockman J.A., Gupta R.A., Dubois R.N. Activation of PPARγ leads to inhibition of anchorage-independent growth of human colorectal cancer cells. Gastroenterology. 115:1998;1049-1055.
17. Kitamura S., Miyazaki Y., Shinomura Y., Kondo S., Kanayama S., Matsuzawa Y. Peroxisome proliferator-activated receptor γ induces growth arrest and differentiation markers of human colon cancer cells. Jpn. J. Cancer Res. 90:1999;75-80.
18. Sato H., Ishihara S., Kawashima K., Moriyama N., Suetsugu H., Kazumori H., Okuyama T., Rumi M.A.K., Fukuda R., Nagasue N., Kinoshita Y. Expression of peroxisome proliferator-activated receptor (PPAR) γ in gastric cancer and inhibitory effects of PPARγ agonists. Br. J. Cancer. 83:2000;1394-1400.
19. Takahashi N., Okumura T., Motomura W., Fujimoto Y., Kawabata I., Kohgo Y. Activation of PPARγ inhibits cell growth and induces apoptosis in human gastric cancer cells. FEBS Lett. 455:1999;135-139.
20. Kip1 in human pancreatic carcinoma cells. Cancer Res. 60:2000;5558-5564.
21. Meuller E., Sarraf S., Tontonoz P., Evans R.M., Martin K.J., Zhang M., Fletcher C., Singer S., Spiegelman M. Terminal differentiation of human breast cancer through PPARγ Mol. Cell. 1:1998;465-470.
22. Sarraf P., Mueller E., Jones D., King F.J., DeAngelo D.J., Partridge J.B., Holden S.A., Chen L.B., Singer S., Fletcher C., Spiegelman B.M. Differentiation and reversal of malignant changes in colon cancer through PPARγ Nature Med. 4:1998;1046-1052.
23. Kliewer S.A., Umesono K., Noonan D., Heyman R.A., Evans R.M. Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature. 358:1992;771-774.
24. Isseman I., Green S. Activation of a member of the steroid receptor superfamily by peroxisome proliferators. Nature. 347:1990;645-650.
25. DeLuca L.M. Retinoids and their receptors in differentiation, embryogenesis and neoplasia. FASEB J. 5:1991;2924-2933.
26. Kato M., Shimada Y., Tanaka H., Hosotani R., Ohshio G., Ishizaki K., Imamura M. Characterization of six cell lines established from human pancreatic adenocarcinomas. Cancer. 85:1999;832-840.
27. Chomezynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
28. Finke J., Fritzen R., Ternes P., Lange W., Dolken G. An improved strategy and a useful housekeeping gene for RNA analysis from formalin-fixed, paraffin- embedded tissues by PCR. Biotechniques. 14:1993;448-453.
29. Mori M., Mimori K., Inoue H., Barnard G.F., Tsuji K., Nanbara S., Ueo H., Akiyoshi T. Detection of cancer micrometastases in lymph nodes by reverse transcriptase-polymerase chain reaction. Cancer Res. 55:1995;3417-3420.
30. Gauthier B., Robb M., McPherson R. Cholesteryl ester transfer protein gene expression during differentiation of human preadipocytes to adipocytes in primary culture. Atherosclerosis. 142:1999;301-307.
31. Schoonjans K., Peinado O.J., Lefebvre A.M., Heyman R.A., Briggs M., Deeb S., Staels B., Auwerx J. PPARalpha and PPARgamma activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO J. 15:1996;5336-5348.
32. Tsubouchi Y., Sano H., Kawahito Y., Mukai S., Yamada R., Kohno M., Inoue K., Hla T., Kondo M. Inhibition of human lung cancer cell growth by the peroxisome proliferator-activated receptor-γ agonists through induction of apoptosis. Biochem. Biophys. Res. Commun. 270:2000;400-405.
33. Mosmann T. Rapid colorimetric assay for cellular growth and survival application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65:1983;55-63.
34. Yanagisawa H., Takamura M., Yamada E., Fujita S., Fujiwara T., Yachi M., Isobe A., Hasegawa Y. Novel oximes having 5-benzyl-2, 4-thiazolidinedione as antihyperglycemic agents synthesis and structure-activity relationship. Bioorg. Med. Chem. Lett. 10:2000;373-375.
35. Haskell C.M., Neoplasm of the gastrointestinal system, in: Cancer Treatment, 4th ed., Saunders, Philadelphia, 1995, pp. 438-547.
36. Vamecq J., Latruffe N. Medical significance of peroxisome proliferator-activated receptors. Lancet. 354:1999;141-148.
37. Kersten S., Desvergne B., Wahli W. Roles of PPARs in health and disease. Nature. 405:2000;421-424.
38. Willson T.M., Cobb J.E., Cowan D.J., Wiethe R.W., Correa I.D., Prakash S.R., Beck K.D., Moore L.B., Kliewer S.A., Lehmann J.M. The structure-activity relationship between peroxisome proliferator-activated receptor γ agonism and the antihyperglycemic activity of thiazolidinediones. J. Med. Chem. 39:1996;665-668.
39. Camp H.S., Li O., Wise S.C., Hong Y.M., Frankowski C.L., Shen X., Vanbogelen R., Leff T. Differential activation of peroxisome proliferator-activated receptor-γ by troglitazone and rosiglitazone. Diabetes. 49:2000;539-547.
40. Fukui Y., Masui S., Osada S., Umesono K., Motojima K. A new thiazolidinedione, NC-2100, which is a weak PPAR-γ activator, exhibits potent antidiabetic effects and induces uncoupling protein 1 in white adipose tissue of KKAy obese mice. Diabetes. 49:2000;759-767.
41. Sun S.-Y., Yue P., Mao L., Dawson M.I., Shroot B., Lamph W.W., Heyman R.A., Chandraratna R.A.S., Shudo K., Hong W.K., Lotan R. Identification of receptor-selective retinoids that are potent inhibitors of the growth of human head and neck squamous cell carcinoma cells. Clin. Cancer Res. 6:2000;1563-1573.
42. Benson S., Padmanabhan S., Kurtz T.W., Pershadsingh H.A. Ligands for the peroxisome proliferator-activated receptor-γ and the retinoid X receptorα exert synergistic antiproliferative effects on human coronary artery smooth muscle cells. Mol. Cell. Biol. Res. Commun. 3:2000;159-164.
43. Asou H., Verbeek W., Williamson E., Elstner E., Kubota T., Kamada N., Koeffler P. Growth inhibition of myeloid leukemia cells by troglitazone, a ligand for peroxisome proliferator activated receptor γ, and retinoids. Int. J. Oncol. 15:1999;1027-1031.
44. Demetri G.D., Fletcher C.D., Mueller E., Sarraf P., Naujoks R., Campbell N., Spiegelman B.M., Singer S. Induction of solid tumor differentiation by the peroxisome proliferator-activated receptor-gamma ligand troglitazone in patients with liposarcoma. Proc. Natl. Acad. Sci. USA. 96:1999;3951-3956.
45. Siegenthaler G., Saurat J.H. Plasma and skin carriers for natural and synthetic retinoids. Arch. Dermatol. 123:1987;1690a-1692a.