PPARγ inhibitors reduce tubulin protein levels by a PPARγ, PPARδ and proteasome-independent mechanism, resulting in cell cycle arrest, apoptosis and reduced metastasis of colorectal carcinoma cells

International Journal of Cancer

Volumn 120, Issue 3, 2007, Pages 702-713

  Schaefer, Katherine L ^a,d   Takahashi, Hirokazu ^b   Morales, Victor M ^a   Harris, Gianni ^a   Barton, Susan ^c   Osawa, Emi ^c   Nakajima, Atsushi ^b   Saubermann, Lawrence J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c BOSTON MEDICAL CENTER   (United States)

^d UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Apoptosis; Colorectal carcinoma; Cytoskeleton; Microtubule; Peroxisome proliferator activated receptor

Indexed keywords

2 CHLORO 5 NITRO N (4 PYRIDYL)BENZAMIDE; 2 CHLORO 5 NITROBENZANILIDE; BADGE; CASPASE; EPOXOMICIN; NOCODAZOLE; PACLITAXEL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA ANTAGONIST; PIOGLITAZONE; PROTEASOME; ROSIGLITAZONE; SMALL INTERFERING RNA; TROGLITAZONE; TUBULIN; 2,2 BIS(4 GLYCIDYLOXYPHENYL)PROPANE; 2,2-BIS(4-GLYCIDYLOXYPHENYL)PROPANE; 2-CHLORO-5-NITROBENZANILIDE; ANILIDE; BENZAMIDE DERIVATIVE; EPOXIDE; PEPTIDE CHLOROMETHYL KETONE; PYRIDINE DERIVATIVE; Z VAL ALA ASP(OME) FLUOROMETHYLKETONE; Z-VAL-ALA-ASP(OME)-FLUOROMETHYLKETONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE M PHASE; CELL MIGRATION; CELL STRAIN CACO 2; CELL STRAIN HT29; CELL STRUCTURE; CELL SURVIVAL; COLORECTAL CARCINOMA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSKELETON; DRUG EFFECT; ENZYME INHIBITION; HUMAN; HUMAN CELL; INHIBITION KINETICS; LIVER METASTASIS; LOW DRUG DOSE; MALE; METASTASIS; METASTASIS INHIBITION; MICROTUBULE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROCESSING; SCID MOUSE; ANIMAL; CELL CYCLE; CELL MOTION; CELL SHAPE; COLORECTAL TUMOR; DOSE RESPONSE; DRUG ANTAGONISM; DRUG SCREENING; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; TUMOR CELL LINE;

AMINO ACID CHLOROMETHYL KETONES; ANILIDES; ANIMALS; APOPTOSIS; BENZAMIDES; CACO-2 CELLS; CASPASES; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; COLORECTAL NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; EPOXY COMPOUNDS; HT29 CELLS; HUMANS; MALE; MICE; MICE, SCID; NEOPLASM METASTASIS; PPAR DELTA; PPAR GAMMA; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRIDINES; TUBULIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 33845711007     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22361     Document Type: Article

References (62)

1. Diaz-Rubio E. New chemotherapeutic advances in pancreatic, colorectal, and gastric cancers. Oncologist 2004;9:282-94.
2. Figueredo A, Charelle ML, Maroun J, Brouwers MC, Zuraw L. Adjuvant therapy for stage II colon cancer: a systematic review from the Cancer Care Ontario Program in evidence-based care's gastrointestinal cancer disease site group. J Clin Oncol 2004;22:3395-407.
3. Rougier P, Lepere C. Metastatic colorectal cancer: first- and second-line treatment in 2005. Semin Oncol 2005;32:15-20.
4. Montero A, Fossella F, Hortobagyi G, Valero V. Docetaxel for treatment of solid tumours: a systematic review of clinical data. Lancet Oncol 2005;6:229-39.
5. Elstner E, Muller C, Koshizuka K, Williamson EA, Park D, Asou H, Shintaku P, Said JW, Heber D, Koeffler HP. 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 1998;95:8806-11.
6. 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;60:1129-38.
7. Mueller E, Sarraf P, Tontonoz P, Evans RM, Martin KJ, Zhang M, Fletcher C, Singer S, Spiegelman BM. Terminal differentiation of human breast cancer through PPAR γ. Mol Cell 1998;1:465-70.
8. Mueller E, Smith M, Sarraf P, Kroll T, Aiyer A, Kaufman DS, Oh W, Demetri G, Figg WD, Zhou XP, Eng C, Spiegelman BM, et al. Effects of ligand activation of peroxisome proliferator-activated receptor γ in human prostate cancer. Proc Natl Acad Sci USA 2000;97:10990-5.
9. Rumi MA, Sato H, Ishihara S, Kawashima K, Hamamoto S, Kazumori H, Okuyama T, Fukuda R, Nagasue N, Kinoshita Y. Peroxisome proliferator-activated receptor γ ligand-induced growth inhibition of human hepatocellular carcinoma. Br J Cancer 2001;84:1640-7.
10. Sarraf P, Mueller E, Jones D, Kine 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.
11. 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 2000;270:400-5.
12. Kulke MH, Demetri GD, Sharpless NE, Ryan DP, Shivdasani R, Clark JS, Spiegelman BM, Kim H, Mayor RJ, Fuchs CS. A phase II study of troglitazone, an activator of the PPARγ receptor, in patients with chemotherapy-resistant metastatic colorectal cancer. Cancer J 2002;8:395-9.
13. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990;61:759-67.
14. 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.
15. Girnun GD, Spiegelman BM. PPARγ ligands: taking Ppart in chemoprevention. Gastroenterology 2003;124:564-7.
16. Osawa E, Nakajima A, Wada K, Ishimine S, Fujisawa N, Kawamori T, Matsuhashi N, Kadowaki T, Ochiai M, Sekihara H, Nakagama H. Peroxisome proliferator-activated receptor γ ligands suppress colon carcinogenesis induced by azoxymethane in mice. Gastroenterology 2003;124:361-7.
17. Lefebvre AM, Chen I, Desreumaux P, Najib J, Fruchart JC, Geboes K, Briggs M, Heyman R, Auwerx J. Activation of the peroxisome proliferator-activated receptor γ promotes the development of colon tumors in C57BL/6J-APCMin/+ mice. Nat Med 1998;4:1053-7.
18. 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 PPAR γ ligand. Cancer Sci 2003;94:960-4.
19. Pino MV, Kelley MF, Jayyosi Z. Promotion of colon tumors in C57B/6J-APC(min)/+ mice by thiazolidinedione PPARγ agonists and a structurally unrelated PPARγ agonist. Toxicol Pathol 2004;32:58-63.
20. Saez E, Tontonoz P, Nelson MC, Alvarez JG, Ming UT, Baird SM, Thomazy VA, Evans RM. Activators of the nuclear receptor PPARγ enhance colon polyp formation. Nat Med 1998;4:1058-61.
21. Yang K, Fan KH, Lamprecht SA, Edelmann W, Kopelovich L, Kucherlapati R, Lipkin M. Peroxisome proliferator-activated receptor γ agonist troglitazone induces colon tumors in normal C57BL/6J mice and enhances colonic carcinogenesis in Apc1638 N/+ Mlh1 +/- double mutant mice. Int J Cancer 2005;116:495-9.
22. Goss KH, Groden J. Biology of the adenomatous polyposis coli tumor suppressor. J Clin Oncol 2000;18:1967-79.
23. Masuda T, Wada K, Nakajima A, Okura M, Kudo C, Kadowaki T, Kogo M, Kamisaki Y. Critical role of peroxisome proliferator-activaled receptor γ on anoikis and invasion of squamous cell carcinoma. Clin Cancer Res 2005;11:4012-21.
24. Schaefer KL, Wada K, Takahashi H, Matsuhashi N, Ohnishi S, Wolfe MM, Turner JR, Nakajima A, Borkan SC, Saubermann LJ. Peroxisome proliferator- activated receptor γ inhibition prevents adhesion to the extracellular matrix and induces anoikis in hepatocellular carcinoma cells. Cancer Res 2005;65:2251-9.
25. Takahashi H, Fujita K, Fujisawa T, Yonemitsu K, Tomimoto A, Ikeda I, Yoneda M, Masuda T, Schaefer K, Saubermann LJ, Shimamura T, Saitoh S, et al. Inhibition of peroxisome proliferator-activated receptor γ activity in esophageal carcinoma cells results in a drastic decrease of invasive properties. Cancer Sci 2006;97:854-60.
26. Lea MA, Sura M, Desbordes C. Inhibition of cell proliferation by potential peroxisome proliferator-activated receptor (PPAR) γ agonists and antagonists. Anticancer Res 2004;24:2765-71.
27. Ramilo G, Valverde I, Lago J, Vieites JM, Cabado AG. Cytotoxic effects of BADGE (bisphenol A diglycidyl ether) and BFDGE (bisphenol F diglycidyl ether) on Caco-2 cells in vitro. Arch Toxicol 2006. 10.1007/s00204-006-0121-1.
28. O'Neil BH, Goldberg RM. Chemotherapy for advanced colorectal cancer: let's not forget how we got here (until we really can). Semin Oncol 2005;32:35-42.
29. Harper JV. Synchronization of cell populations in G1/S and G2/M phases of the cell cycle. Methods Mol Biol 2005;296:157-66.
30. Cooper S. Reappraisal of serum starvation, the restriction point, G0, and G1 phase arrest points. FASEB J 2003;17:333-40.
31. Meng L, Mohan R, Kwok BH, Elofsson M, Sin N, Crews CM. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc Natl Acad Sci USA 1999;96:10403-8.
32. Klominek J, Robert KH, Sundqvist KG. Chemotaxis and haptotaxis of human malignant mesothelioma cells: effects of fibronectin, laminin, type IV collagen, and an autocrine motility factor-like substance. Cancer Res 1993;53:4376-82.
33. Yasui N, Sakamoto M, Ochiai A, Ino Y, Akimoto S, Orikasa A, Kitajima M, Hirohashi S. Tumor growth and metastasis of human colorectal cancer cell lines in SCID mice resemble clinical metastatic behaviors. Invasion Metastasis 1997;17:259-69.
34. Castedo M, Perfettini JL, Roumier T, Kroemer G. Cyclin-dependent kinase-1: linking apoptosis to cell cycle and mitotic catastrophe. Cell Death Differ 2002;9:1287-93.
35. Bhalla KN. Microtubule-targeted anticancer agents and apoptosis. Oncogene 2003;22:9075-86.
36. Blajeski AL, Phan VA, Kottke TJ, Kaufmann SH. G(1) and G(2) cell-cycle arrest following microtubule depolymerization in human breast cancer cells. J Clin Invest 2002;110:91-9.
37. Tanabe H, Suzuki H, Mizukami H, Inoue M. Double blockade of cell cycle progression by coptisine in blaj. Biochem Pharmacol 2005;70:1176-84.
38. Jordan MA. Mechanism of action of antitumor drugs that interact with microtubules and tubulin. Curr Med Chem Anticancer Agents 2002;2:1-17.
39. Peterson JR, Mitchison TJ. Small molecules, big impact: a history of chemical inhibitors and the cytoskeleton. Chem Biol 2002;9:1275-85.
40. Ben-Ze'ev A, Farmer SR, Penman S. Mechanisms of regulating tubulin synthesis in cultured mammalian cells. Cell 1979;17:319-25.
41. Cleveland DW, Havercroft JC. Is apparent autoregulatory control of tubulin synthesis nontranscriptionally regulated? J Cell Biol 1983;97:919-24.
42. Vasquez RJ, Howell B, Yvon AM, Wadsworth P, Cassimeris L. Nanomolar concentrations of nocodazole after microtubule dynamic instability in vivo and in vitro. Mol Biol Cell 1997;8:973-85.
43. Fujiwara T, Horikoshi H. Troglitazone and related compounds: therapeutic potential beyond diabetes. Lite Sci 2000;67:2405-16.
44. Rumi MA, Ishihara S, Kazumori H, Kadowaki Y, Kinoshita Y. Can PPAR γ ligands be used in cancer therapy? Curr Med Chem Anticancer Agents 2004;4:465-77.
45. Burdick AD, Kim DJ, Peraza MA, Gonzalez FJ, Peters JM. The role of peroxisome proliferator-activated receptor-β/δ in epithelial cell growth and differentiation. Cell Signal 2006;18:9-20.
46. Kim DJ, Murray IA, Burns AM, Gonzalez FJ, Perdew GH, Peters JM. Peroxisome proliferator-activated receptor-β/δ inhibits epidermal cell proliferation by down-regulation of kinase activity. J Biol Chem 2005;280:9519-27.
47. Welch JS, Ricole M, Akiyama TE, Gonzalez FJ, Glass CK. PPARγ and PPARδ negatively regulate specific subsets of lipopolysaccharide and IFN-γ target genes in macrophages. Proc Natl Acad Sci USA 2003;100:6712-17.
48. Lee G, Elwood F, McNally J, Weiszmann J, Lindstrom M, Amaral K, Nakamura M, Miao S, Cao P, Learned RM, Chen JL, Li Y. T0070907, a selective ligand for peroxisome proliferator-activated receptor γ, functions as an antagonist of biochemical and cellular activities. J Biol Chem 2002;277:19649-57.
49. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 2005;6:56-68.
50. Leesnitzer LM, Parks DJ, Bledsoe RK, Cobb JE, Collins JL, Consler TG, Davis RG, Hull-Ryde EA, Lenhard JM, Patel L, Plunket KD, Shenk JL, et al. Functional consequences of cysteine modification in the ligand binding sites of peroxisome proliferator activated receptors by GW9662. Biochemistry 2002;41:6640-50.
51. Fenteany G, Zhu S. Small-molecule inhibitors of actin dynamics and cell motility. Curr Top Med Chem 2003;3:593-616.
52. Castedo M, Perfettini JL, Roumier T, Andreau K, Medema R, Kroemer G. Cell death by mitotic catastrophe: a molecular definition. Oncogene 2004;23:2825-37.
53. Palazzo AF, Gundersen GG. Microtubule-actin cross-talk at local adhesions. Sci STKE 2002;2002:PE31.
54. Wolf DH, Hill W. The proteasome: a proteolytic nanomachine of cell regulation and waste disposal. Biochim Biophys Acta 2004;1695:19-31.
55. Ciechanover A. Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ 2005;12:1178-90.
56. Ferruzzi P, Ceni E, Tarocchi M, Grappone C, Milani S, Galli A, Fiorelli G, Serio M, Mannelli M. Thiazolidinediones inhibit growth and invasiveness of the human adrenocortical cancer cell line H295R. J Clin Endocrinol Metab 2005;90:1332-9.
57. Liu J, Lu H, Huang R, Lin D, Wu X, Lin Q, Wu X, Zheng J, Pan X, Peng J, Song Y, Zhang M, 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;56:400-8.
58. Panigrahy D, Huang S, Kieran MW, Kaipainen A. PPARγ as a therapeutic target for tumor angiogenesis and metastasis. Cancer Biol Ther 2005;4:687-93.
59. Sunumi E, Tsuno NH, Kitayama J, Saito S, Osada T, Yamaguchi H, Tomozawa S, Tsuruo T, Shibata Y, Nagawa H. Decreased synthesis of matrix metalloproteinase-7 and adhesion to the extracellular matrix proteins of human colon cancer cells treated with troglitazone. Surg Today 2002;32:343-50.
60. Leslie EM, Deeley RG, Cole SP. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 2005;204:216-37.
61. Lin-Lee YC, Tatebe S, Savaraj N, Ishikawa T, Tien Kuo M. Differential sensitivities of the MRP gene family and γ-glutamylcysteine synthetase to prooxidants in human colorectal carcinoma cell lines with different p53 stains. Biochem Pharmacol 2001;61:555-63.
62. Orr GA, Verdier-Pinard P, McDaid H, Horwitz SB. Mechanisms of Taxol resistance related to microtubules. Oncogene 2003;22:7280-95.