The potential of antidiabetic thiazolidinediones for anticancer therapy

Expert Opinion on Investigational Drugs

Volumn 15, Issue 9, 2006, Pages 1039-1049

  Galli, Andrea ^a   Mello, Tommaso ^b   Ceni, Elisabetta ^b   Surrenti, Elisabetta ^b   Surrenti, Calogero ^b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b NONE

Author keywords

Cell proliferation; PPAR ; Thiazolidinediones

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; CELL NUCLEUS RECEPTOR; CIGLITAZONE; ISOXAZOLIDINE DERIVATIVE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; ROFECOXIB; ROSIGLITAZONE; TROFOSFAMIDE; TROGLITAZONE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CHEMOTHERAPY; CELL DIFFERENTIATION; CELL GROWTH; CELL MOTILITY; CHEMOPROPHYLAXIS; CLINICAL STUDY; CLINICAL TRIAL; DRUG ACTIVITY; DRUG MECHANISM; DRUG STRUCTURE; EXPERIMENTAL MODEL; HUMAN; IN VITRO STUDY; INSULIN RESISTANCE; LIVER TOXICITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PILOT STUDY; REVIEW; UNSPECIFIED SIDE EFFECT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; HYPOGLYCEMIC AGENTS; NEOPLASMS; THIAZOLIDINEDIONES;

EID: 33748167914     PISSN: 13543784     EISSN: None     Source Type: Journal    
DOI: 10.1517/13543784.15.9.1039     Document Type: Review

References (85)

1. KINTSCHER U, LAW RE: PPARγ-mediated insulin sensitization: the importance of fat versus muscle. Am. J. Physiol, Endocrinol. Metab (2005) 288:E287-E291.
2. MENON KVN, ANGULO P, LINDOR KD: Severe cholestatic hepatitis from troglicazone in a patient with nonalcoholic steatohepatitis and diabetes mellitus. Am. J. Gastroenterol, (2001) 96:1631-1634.
3. ISLEY WL: Hepatotoxicity of thiazolidinediones. Expert. Opin. Drug Saf. (2003) 2:581-586.
4. FURNSINN C, WALDHAUSL W: Thiazolidinediones: metabolic actions in vitro. Diabetologia (2002) 45:1211-1223.
5. HAMMARSTEDT A, ANDERSSON CX, ROTTER SV, SMITH U: The effect of PPARγ ligands on the adipose tissue in insulin resistance. Prostaglandins Leukot. Essent. Fatty Acids (2005) 73:65-75.
6. LEHMANN JM, MOORE LB, SMITH-OLIVER TA, WILKISON WO, WILLSON TM, KLIEWER SA: An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor γ (PPAR γ). J. Biol, Chem. (1995) 270:12953-12956.
7. TONTONOZ P, HU E, SPIEGELMAN BM: Stimulation of adipogenesis in fibroblasts by PPAR γ2, a lipid-activated transcription factor. Cell (1994) 79:1147-1156.
8. KOTA BP, HUANG TH, ROUFOGALIS BD: An overview on biological mechanisms of PPARs. Pharmacol. Res. (2005) 51:85-94.
9. SHAO D, RANGWALA SM, BAILEY ST, KRAKOW SL, REGINATO MJ, LAZAR MA: Interdomain communication regulating ligand binding by PPAR-γ. Nature (1998) 396:377-380.
10. XU HE, LAMBERT MH, MONTANA VG et al: Structural determinants of ligand binding selectivity between the peroxisome proliferator-activated receptors. Proc. Natl. Acad Sci. USA (2001) 98:13919-13924.
11. LAZAR MA: PPAR γ, 10 years later. Biochimie (2005) 87:9-13.
12. FEINSTEIN DL, SPAGNOLO A. AKAR C et al: Receptor-independent actions of PPAR thiazolidinedione agonists: is mitochondrial hinction the key? Biochem. Pharmacol. (2005) 70:177-188.
13. TONTONOZ P, SINGER S, FORMAN BM et al: 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 (1997) 94:237-241.
14. MUELLER E, SARRAF P, TONTONOZ P et al: Terminal differentiation of human breast cancer through PPAR 7. Mol. Cell (1998) 1:465-470.
15. TSUJIE M, NAKAMORI S, OKAMI J et al: Thiazolidinediones inhibit growth of gastrointestinal, biliary, and pancreatic adenocarcinoma cells through activation of the peroxisome proliferator-activated receptor γ/ retinoid X receptor α pathway. Exp. Cell Res. (2003) 289:143-151.
16. YOSHIZUMI T, OHTA T, NINOMIYA I et al: Thiazolidinedione, a peroxisome proliferator-activated receptor-γ ligand, inhibits growth and metastasis of HT-29 human colon cancer cells through differentiation-promoting effects. Int.J. OncoL (2004) 25:631-639.
17. ELSTNER E, MULLER C, KOSHIZUKA K et al: Ligands for peroxisome proliferator-activated receptorγ and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice. Proc. Natt Acad. Sci. USA (1998) 95:8806-8811.
18. QIN C, BURGHARDT R, SMITH R, WORMKE M, STEWART J, SAFE S: Peroxisome proliferator-activated receptor γ agonists induce proteasome-dependent degradation of cyclin D 1 and estrogen receptor α in MCF-7 breast cancer cells. Cancer Res. (2003) 63:958-964.
19. CENI E, MELLO T, TAROCCHI M et al.: Antidiabetic thiazolidinediones induce ductal differentiation but not apoptosis in pancreatic cancer cells. World J. Gastroenterol (2005) 11:1122-1130.
20. MOTOMURA W, TAKAHASHI N, NAGAMINE M et al.: Growth arrest by troglitazone is mediated by p27Kip 1 accumulation, which results from dual inhibition of proteasome activity and Skp2 expression in human hepatocellular carcinoma cells. Int. J. Cancer (2004) 108:41-46.
21. YANG FG, ZHANG ZW, XIN DQ et al: Peroxisome proliferator-activated receptor γ ligands induce cell cycle arrest and apoptosis in human renal carcinoma cell lines. Acta Pharmacol Sin. (2005) 26:753-761.
22. KESHAMOUNI VG, REDDY RC, ARENBERG DA et al: Peroxisome proliferator-activated receptor-γ activation inhibits tumor progression in non-small-cell lung cancer. Oncogene (2004) 23:100-108.
23. HAN S, SIDELL N, FISHER PB, ROMAN J: Up-regulation ofp2l gene expression by peroxisome proliferator-activated receptor γ in human lung carcinoma cells. Clin. Cancer Res. (2004) 10:1911-1919.
24. CENI E, CRABB D, MELLO T et al: Antidiabetic thiazolidinediones inhibit hepatic tumor formation in HBV transgenic mouse model. Hepatology (2003) 38(Suppl. 1):95A.
25. CHEN F, HARRISON LE: Ciglitazone-induced cellular anti-proliferation increases p27kip 1 protein levels through both increased transcriptional activity and inhibition of proteasome degradation. Cell Signal. (2005) 17:809-816.
26. HONG J, SAMUDIO I, LIU S, ABDELRAHIM M, SAFE S: Peroxisome proliferator-activated receptor γ-dependent activation of p2l in Panc-28 pancreatic cancer cells involves Sp1 and Sp4 proteins. Endocrinology (2004) 145:5774-5785.
27. HE G, THUILLIER P, FISCHER SM: Troglitazone inhibits cyclin D1 expression and cell cycling independently of PPARγ in normal mouse skin keratinocytes. J. Invest. Dermatol. (2004) 123:1110-1119.
28. LIM SC: Role of COX-2, VEGF and cyclin D1 in mammary infiltrating duct carcinoma. Oncol Rep. (2003) 10:1241-1249.
29. HUANG JW, SHIAU CW, YANG YT et al.: Peroxisome proliferator-activated receptor γ-independent ablation of cyclin D1 by thiazolidinediones and their derivatives in breast cancer cells. Mol. Pbarmacol. (2005) 67:1342-1348.
30. WANG C, PATTABIRAMAN N, ZHOU JN et al: Cyclin D1 repression of peroxisome proliferator-activated receptor γ expression and transactivation. Mol. Cell Biol. (2003) 23:6159-6173.
31. HAN C, DEMETRIS AJ, MICHALOPOULOS GK, ZHAN Q, SHELHAMER JH, WU T. PPARγ ligands; inhibit cholangiocarcinoma cell growth through p53-dependent GADD45 and p21 pathway. Hepatology (2003) 38:167-177.
32. GUPTA RA, BROCKMAN JA, SARRAF P, WILLSON TM, DUBOIS RN: Target genes of peroxisome proliferator-activated receptor γ in colorectal cancer cells. J. Biol Chem. (2001) 276:29681-29687.
33. JAMES SY, LIN F, KOLLURI SK, DAWSON MI, ZHANG XK: Regulation of retinoic acid receptor β expression by peroxisome proliferator-activated receptor γ ligands in cancer cells. Cancer Res. (2003) 63:3531-3538.
34. ZHANG XK, LIU Y, LEE MO: Retinoid receptors in human lung cancer and breast cancer. Mutat. Res. (1996) 350:267-277.
35. LIN B, CHEN GQ XIAO D et al.: Orphan receptor COUP-TF is required for induction of retinoic acid receptor β, growth inhibition, and apoptosis by retinoic acid in cancer cells. Mol. Cell Biol (2000) 20:957-970.
36. GALLI A, CENI E, CRABB DW et al.: Antidiabetic thiazolidinediones inhibit invasiveness of pancreatic cancer cells via PPARγ independent mechanisms. Gut (2004) 53:1688-1697.
37. BERGE K, TRONSTAD KJ, FLINDT EN et al: Tetradecylthioacetic acid inhibits growth of rat glioma cells ex vivo and in vivo via PPAR-dependent and PPAR-independent pathways. Carcinogenesis (2001) 22:1747-1755.
38. BROCKMAN JA, GUPTA RA, DUBOIS RN: Activation of PPARγ leads to inhibition of anchorage-independent growth of human colorectal cancer cells. Gastroenterology (1998) 115:1049-1055.
39. ABE A, KIRIYAMA Y HIRANO M et aL: Troglitazone suppresses cell growth of KU812 cells independently of PPARγ. Eur J. Pharmacol. (2002) 436:7-13.
40. PALAKURTHI SS, AKTAS 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) 61:6213-6218.
41. SHARMA C, PRADEEP A, WONG L, RANA A, RANA B: Peroxisome proliferator-activated receptor γ activation can regulate β-catenin levels via a proteasome-mediated and adenomatous polyposis coli-independent pathway. J. Biol. Chem. (2004) 279:35583-35594.
42. OHTA T, ELNEMR A, YAMAMOTO M et al: Thiazolidinedione, a peroxisome proliferator-activated receptor-γ ligand, modulates the E-cadherin/ β-catenin system in a human pancreatic cancer cell line, BxPC-3. Int. J. Oncol. (2002) 21:37-42.
43. ZANDER T, KRAUS, JA, GROMMES, C et al.: Induction of apoptosis in human and rat glioma by agonists of the nuclear receptor PPARγ. J. Neurochem. (2002) 81:1052-1060.
44. LU M, KWAN T, YU C et aL: Peroxisome proliferator-activated receptor γ agonists promote TRAIL-induced apoptosis by reducing survivin levels via cyclin D3 repression and cell cycle arrest. J. BioL Chem. (2005) 280:6742-6751.
45. KIM Y, SUH N, SPORN M, REED JC: An inducible pathway for degradation of FLIP protein sensitizes tumor cells to TRAIL-induced apoptosis. J. Biol. Chem. (2002) 277:22320-22329.
46. AKASAKI Y, LIU G, MATUNDAN HH et al.: A peroxisome proliferator-activated receptor-γ (PPARγ) agonist, troglitazone, facilitates caspase-8 and -9 activities by increasing the enzymatic activity of protein tyrosine phosphatase- 1B on human glioma cells. J. Biol. Chem. (2006) 281:6165-6174.
47. CHANG TH, SZABO E: Induction of differentiation and apoptosis by ligands of peroxisome proliferator-activated receptor γ in non-small cell lung cancer. Cancer Res. (2000) 60:1129-1138.
48. FERRUZZI P, CENI E, TAROCCHI M et al.: Thiazolidinediones inhibit growth and invasiveness of the human adrenocortical cancer cell line H295R. J. Clin. Endocrinol. Metab. (2005) 90:1332-1339.
49. LIU J, LU H, HUANG R et al.: Peroxisome proliferator activated receptor-γ ligands induced cell growth inhibition and its influence on matrix metalloproteinase activity in human myeloid leukemia cells. Cancer Chemother. Pharmacol. (2005) 56:400-408.
50. SUNAMI E, TSUNO NH, KITAYAMA J et al: Decreased synthesis of matrix metalloproteinase-7 and adhesion to the extracellular matrix proteins of human colon cancer cells treated with troglitazone. Surg. Today (2002) 32:343-350.
51. MASUDA T, WADA K, NAKAJIMA A et al.: Critical role of peroxisome proliferator-activated receptor γ on anoikis and invasion of squamous cell carcinoma. Clin. Cancer Res. (2005) 11:4012-4021.
52. HANAHAN D, FOLKMAN J: Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell (1996) 86:353-364.
53. FERRARA N: VEGF and the quest for tumour angiogenesis factors. Nat. Rev. Cancer (2002) 2:795-803.
54. RODRIGUEZ-MANZANEQUE JC, LANE TF, ORTEGA MA, HYNES RO, LAWLER J, IRUELA-ARISPE ML: Thrombospondin- 1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc. Natl. Acad Sci. USA (2001) 98:12485-12490.
55. BARAK Y, NELSON MC, ONG ES et al.: PPAR γ is required for placental, cardiac, and adipose tissue development. Mol Cell (1999) 4:585-595.
56. ASANO A, IRIE Y, SAITO M: Isoform-specific regulation of vascular endothelial growth factor (VEGF) family mRNA expression in cultured mouse brown adipocytes. Mol. Cell Endocrinol (2001) 174:71-76.
57. FAUCONNET S, LASCOMBE I, CHABANNES E et al.: Differential regulation of vascular enclothelial growth factor expression by peroxisome proliferator-activated receptors in bladder cancer cells. J. Biol. Chem. (2002) 277:23534-23543.
58. INOUE M, ITOH H, TANAKA T et al.: Oxidized LDL regulates vascular endothelial growth factor expression in human macrophages and enclothelial. cells through activation of peroxisome proliferator-activated receptor-γ. Arterioscler. Thromb. Vasc. Biol. (2001) 21:560-566.
59. YAMAKAWA K, HOSOI M, KOYAMA H et al.: Peroxisome proliferator-activated receptor-γ agonists increase vascular endothelial growth factor expression in human vascular smooth muscle cells. Biochem. Biophys. Res. Commun. (2000) 271:571-574.
60. TANAKA T, FUKUNAGA Y, ITOH H et al.: Therapeutic potential of thiazolidinediones in activation of peroxisome proliferator-activated receptor γ for monocyte recruitment and endothelial regeneration. Eur. J. Pharmacol. (2005) 508:255-265.
61. FUKUNAGA Y, ITOH H, DOI K et al.: Thiazolidinediones, peroxisome proliferator-activated receptor γ agonists, regulate endothelial cell growth and secretion of vasoactive peptides. Atherosclerosis (2001) 158:113-119.
62. XIN X, YANG S, KOWALSKI J, GERRITSEN ME: Peroxisome proliferator-activated receptor γ ligands are potent inhibitors of angiogenesis in vitro and in vivo. J. Biol. Chem. (1999) 274:9116-9121.
63. MURATA T, HE S, HANGAI M et al.: Peroxisome proliferator-activated receptor-γ ligands inhibit choroidal neovascularization. Invest. Ophthalmol. Vis. Sci. (2000) 41:2309-2317.
64. PANIGRAHY D, SINGERS, SHEN LQ et al.: PPARγ ligands inhibit primary tumor growth and metastasis by inhibiting angiogenesis. J Clin. Invest. (2002) 110:923-932.
65. 2. J. BioL. Chem. (1999) 274:17042-17048.
66. KIM KY, CHEON HG: Anti-angiogenic effect of rosiglitazone is mediated via PPARγ-activated Maxi-K channel opening in human umbilical vein endothelial cells. J. BioL Chem. (2006) 281:13503-13512.
67. ARTWOHL M, HOLZENBEIN T, FURNSINN C et al: Thiazolidinediones inhibit apoptosis and heat shock protein 60 expression in human vascular enclothelial cells. Thromh. Haemost. (2005) 93:810-815.
68. RIEUSSET J, AUWERX J, VIDAL H: Regulation of gene expression by activation of the peroxisome proliferator-activated receptor γ with rosiglirazone (BRL 49653) in human adipocytes. Biochem. Biophys. Res. Commun. (1999) 265:265-271.
69. MEHTA RG, WILLIAMSON E, PATEL MK, KOEFFLER HP: A ligand of peroxisome proliferator-activated receptor γ, retinoids, and prevention of preneoplastic mammary lesions. J. Natl.. Cancer Inst. (2000) 92:418-423.
70. SAEZ E, ROSENFELD J, LIVOLSI A et al.: PPAR γ signaling exacerbates mammary gland tumor development. Genes Dev. (2004) 18:528-540.
71. +/- double mutant mice. Int. J Cancer (2005) 116:495-499.
72. LEFEBVRE AM, CHEN I, DESREUMAUX P et al: Activation of the peroxisome proliferator-activated receptor γ promotes the development of colon tumors in C57BL/6J-APCMin/+ mice. Nat. Med. (1998) 4:1053-1057.
73. 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.
74. 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.
75. NIHO N, TAKAHASHI M, KITAMURA T et al.: Concomitant suppression of hyperlipidemia and intestinal polyp formation in Apc-deficient mice by peroxisome proliferator-activated receptor ligands. Cancer Res. (2003) 63:6090-6095.
76. DEMETRI GD, FLETCHER CD, MUELLER E et al.: Induction of solid tumor differentiation by the peroxisome proliferator-activated receptor-γ ligand troglitazone in patients with liposarcoma. Proc. Natl. Acad. Sci. USA (1999) 96:3951-3956.
77. DEBROCK G, VANHENTENRIJK V, SCIOT R, BIEC-RYCHTER M, OYEN R, VAN OA: A Phase II trial with rosiglitazone in liposarcoma. patients. Br. J. Cancer (2003) 89:1409-1412.
78. BURSTEIN HJ, DEMETRI GD, MUELLER E, SARRAF P, SPIEGELMAN BM, WINER EP: Use of the peroxisome proliferator-activated receptor (PPAR) γ ligand troglitazone as treatment for refractory breast cancer: a Phase II study. Breast Cancer Res, Treat. (2003) 79:391-397.
79. PHILIPS JC, PETITE C, WILLI JP, BUCHEGGER F, MEIER CA: Effect of peroxisome proliferator-activated receptor γ agonist, rosiglitazone, on dedifferentiated thyroid cancers. Nucl. Med. Commun. (2004) 25:1183-1186.
80. VOGT T, HAFNER C, BROSS K et al: Antiangiogenetic therapy with pioglitazone, rofecoxib, and metronomic trofosfamide in patients with advanced malignant vascular tumors. Cancer (2003) 98:2251-2256.
81. REICHLE A, BROSS K, VOGT T et al.: Pioglitazone and rofecoxib combined with angiostatically scheduled trofosfamide in the treatment of far-advanced melanoma and soft tissue sarcoma. Cancer (2004) 101:2247-2256.
82. DORMANDY JA, CHARBONNEL B, ECKLAND DJ et al.: Secondary prevention of macrovascular events in patients with Type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macro Vascular Events): a ramdomised controlled trial. Lancet (2005) 366: 1279-1289.
83. DA RR, ASSALONI R, CERIELLO A: The preventive anti-oxidant action of thiazolidinediones: a new therapeutic prospect in diabetes and insulin resistance. Diabet. Med. (2004) 21: 1249-1252.
84. SHIAU CW, YANG CC, KULP SK et al.: Thiazolidenediones mediate apoptosis in prostate cancer cells in part through inhibition of Bcl-xL/Bcl-2 functions independently of PPARγ. Cancer Res. (2005) 65: 1561-1569.
85. WENG JR, CHEN CY, PINZONE JJ, RINGEL MD, CHEN CS: Beyond peroxisome proliferator-activated receptor γ signaling: the multi-facets of the antitumor effect of thiazolidinediones. Endocr. Relat. Cancer (2006) 13:401-413.