Underexpression of PPARγ is associated with aneuploidy and lower differentiation of thyroid tumours of follicular origin

Oncology Reports

Volumn 22, Issue 4, 2009, Pages 907-913

  Espadinha, Carla ^a   Pinto, António E ^a   Leite, Valeriano ^a,b  

^a INSTITUTO PORTUGUÊS DE ONCOLOGIA DE LISBOA FRANCISCO GENTIL   (Portugal)

^b UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

Aneuploidy; Na+ I symporter; PPAR ; Thyroglobulin; Thyroid; TSH receptor

Indexed keywords

MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SODIUM IODIDE SYMPORTER; THYROGLOBULIN; THYROTROPIN RECEPTOR; TUMOR MARKER;

ANEUPLOIDY; ARTICLE; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THYROID FOLLICULAR CARCINOMA; THYROID TUMOR; ADENOCARCINOMA; BIOSYNTHESIS; CELL DIFFERENTIATION; GENETICS; METABOLISM; PATHOLOGY; PROGNOSIS;

ADENOCARCINOMA, FOLLICULAR; ANEUPLOIDY; CELL DIFFERENTIATION; HUMANS; PPAR GAMMA; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; THYROID NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 70350364844     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or_00000516     Document Type: Article

References (48)

1. Kroll TG, Sarraf P, Pecciarini L, Chen CJ, Mueller E, Spiegelman BM and Fletcher JA: PAX8-PPARgammal fusion oncogene in human thyroid carcinoma (corrected). Science 289: 1357-1360, 2000. Erratum in: Science 289: 1474, 2000.
2. Marques AR, Espadinha C, Catarino AL, Moniz S, Pereira T, Sobrinho LG and Leite V: Expression of PAX8-PPAR gamma 1 rearrangements in both follicular thyroid carcinomas and adenomas. J Clin Endocrinol Metab 87: 3947-3952, 2002.
3. Nikiforova MN, Biddinger PW, Caudill CM, Kroll TG and Nikiforov YE: PAX8-PPARgamma rearrangement in thyroid tumors: RT-PCR and immunohistochemicalanalyses. Am J Surg Pathol 26: 1016-1023, 2002.
4. Vidal-Puig A, Jimenez-Linan M, Lowell BB, Hamann A, Hu E, Spiegelman B, Flier JS and Moller DE: Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. J Clin Invest 97: 2553-2561, 1996.
5. Lefebvre AM, Laville M, Vega N, Riou JP, van Gaal L, Auwerx J and Vidal H: Depot-specific differences in adipose tissue gene expression in lean and obese subjects. Diabetes 47: 98-103, 1998.
6. Rieusset J, Andreelli F, Auboeuf D, Roques M, Vallier P, Riou JP, Auwerx J, Laville M and Vidal H: Insulin acutely regulates the expression of the peroxisome proliferator-activated receptor-gamma in human adipocytes. Diabetes 48: 699-705, 1999.
7. Auwerx J: PPARgamma, the ultimate thrifty gene (Review). Diabetologia 42: 1033-1049, 1999.
8. Elstner E, Müller C, Koshizuka K, Williamson EA, Park D, Asou H, Shintaku P, Said JW, Heber D and Koeffler HP: Ligands for peroxisome proliferator-activated receptorgamma 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: 8806-8811, 1998.
9. Kubota T, Koshizuka K, Williamson EA, Asou H, Said JW, Holden S, Miyoshi I and Koeffler HP: Ligand for peroxisome proliferator-activated receptor gamma (troglitazone) has potent antitumor effect against human prostate cancer both in vitro and in vivo. Cancer Res 58: 3344-3352, 1998.
10. Tontonoz P, Singer S, Forman BM, Sarraf P, Fletcher JA, Fletcher CD, Brun RP, Mueller E, Altiok S, Oppenheim H, Evans RM and Spiegelman BM: Terminal differentiation of human liposarcoma cells induced by ligands for peroxisome proliferator-activated receptor gamma and the retinoid X receptor. Proc Natl Acad Sci USA 94: 237-241, 1997.
11. Ohta K, Endo T, Haraguchi K, Hershman JM and Onaya T: Ligands for peroxisome proliferator-activated receptor gamma inhibit growth and induce apoptosis of human papillary thyroid carcinoma cells. J Clin Endocrinol Metab 86: 2170-2177, 2001.
12. Inoue K, Kawahito Y, Tsubouchi Y, Kohno M, Yoshimura R, Yoshikawa T and Sano H: Expression of peroxisome proliferator-activated receptor gamma in renal cell carcinoma and growth inhibition by its agonists. Biochem Biophys Res Commun 287: 727-732, 2001.
13. Hase T, Yoshimura R, Mitsuhashi M, Segawa Y, Kawahito Y, Wada S, Nakatani T and Sano H: Expression of peroxisome proliferator-activated receptors in human testicular cancer and growth inhibition by its agonists. Urology 60: 542-547, 2002.
14. Terashita Y, Sasaki H, Haruki N, Nishiwaki T, Ishiguro H, Shibata Y, Kudo J, Konishi S, Kato J, Koyama H, Kimura M, Sato A, Shinoda N, Kuwabara Y and Fujii Y: Decreased peroxisome proliferator-activated receptor gamma gene expression is correlated with poor prognosis in patients with esophageal cancer. Jpn J Clin Oncol 32: 238-243, 2002.
15. Sarraf P, Mueller E, Jones D, King FJ, DeAngelo DJ, Partridge JB, Holden SA, Chen LB, Singer S, Fletcher C and Spiegelman BM: Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat Med 4: 1046-1052, 1998.
16. Sarraf P, Mueller E, Smith WM, Wright HM, Kum JB, Aaltonen LA, De la Chapelle A, Spiegelman BM and Eng C: Loss-of-function mutations in PPAR gamma associated with human colon cancer. Mol Cell 3: 799-804, 1999.
17. Fabarius A, Wilier A, Yerganian G, Hehlmann R and Duesberg P: Specific aneusomies in Chinese hamster cells at different stages of neoplastic transformation, initiated by nitrosomethylurea. Proc Natl Acad Sci USA 99: 6778-6783, 2002.
18. Oyama T, Vickery AL Jr, Preffer FT and Colvin RB: A comparative study of flow cytometry and histopathologic findings in thyroid follicular carcinomas and adenomas. Hum Pathol 25: 271-275, 1994.
19. Hostetter AL, Hrafnkelsson J, Wingren SO, Enestrom S and Nordenskjöld B: A comparative study of DNA cytometry methods for benign and malignant thyroid tissue. Am J Clin Pathol 89: 760-763, 1988.
20. Soares P and Sobrinho-Simões M: Recent advances in cytometry, cytogenetics and molecular genetics of thyroid tumours and tumour-like lesions (Review). Pathol Res Pract 191: 304-317, 1995.
21. Francia G, Azzolina L, Mantovani T, Daví MV, Brazzarola P, Valerio A, Petronio R and Sussi P: Heterogeneity of nuclear DNA pattern and its relationship with cell cycle activity parameters in multinodular goitre. Clin Endocrinol (Oxf) 46: 649-654, 1997.
22. Marques AR, Espadinha C, Frias MJ, Roque L, Catarino AL, Sobrinho LG and Leite V: Underexpression of peroxisome proliferator-activated receptor (PPAR)gamma in PAX8/PPARgamma-negative thyroid tumours. Br J Cancer 91: 732-738, 2004.
23. Sugg SL, Ezzat S, Rosen IB, Freeman JL and Asa SL: Distinct multiple RET/ PTC gene rearrangements in multifocal papillary thyroid neoplasia. J Clin Endocrinol Metab 83: 4116-4122, 1998.
24. Deitch AD, Law H and DeVere White R: A stable propidium iodide staining procedure for flow cytometry. J Histochem Cytochem 30: 967-972, 1982.
25. Dean PN and Jett JH: Mathematical analysis of DNA distributions derived from flow microfluorometry. J Cell Biol 60: 523-527, 1974.
26. Joensuu H, Klemi P, Eerola E and Tuominen J: Influence of cellular DNA content on survival in differentiated thyroid cancer. Cancer 58: 2462-2467, 1986.
27. Joensuu H and Klemi PJ: Comparison of nuclear DNA content in primary and metastatic differentiated thyroid carcinoma. Am J Clin Pathol 89: 35-40, 1988.
28. Sturgis CD, Caraway NP, Johnston DA, Sherman SI, Kidd L and Katz RL: Image analysis of papillary thyroid carcinoma fine-needle aspirates: significant association between aneuploidy and death from disease. Cancer 87: 155-160, 1999.
29. Demetri GD, Fletcher CD, Mueller E, Sarraf P, Naujoks R, Campbell N, Spiegelman BM and 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: 3951-3956, 1999.
30. Mueller E, Sarraf P, Tontonoz P, Evans RM, Martin KJ, Zhang M, Fletcher C, Singer S and Spiegelman BM: Terminal differentiation of human breast cancer through PPAR gamma. Mol Cell 1: 465-470, 1998.
31. Brockman JA, Gupta RA and Dubois RN: Activation of PPARgamma leads to inhibition of anchorage-independent growth of human colorectal cancer cells. Gastroenterology 115: 1049-1055, 1998.
32. Kitamura S, Miyazaki Y, Shinomura Y, Kondo S, Kanayama S and Matsuzawa Y: Peroxisome proliferator-activated receptor gamma induces growth arrest and differentiation markers of human colon cancer cells. Jpn J Cancer Res 90: 75-80, 1999.
33. Guan YF, Zhang YH, Breyer RM, Davis L and Breyer MD: Expression of peroxisome proliferator-activated receptor gamma (PPARgamma) in human transitional bladder cancer and its role in inducing cell death. Neoplasia 1: 330-339, 1999.
34. Chang TH and Szabo E: Induction of differentiation and apoptosis by ligands of peroxisome proliferator-activated receptor gamma in non-small cell lung cancer. Cancer Res 60: 1129-1138, 2000.
35. Motomura W, Okumura T, Takahashi N, Obara T and Kohgo Y: Activation of peroxisome proliferator-activated receptor gamma by troglitazone inhibits cell growth through the increase of p27KiP1 in human pancreatic carcinoma cells. Cancer Res 60: 5558-5564, 2000.
36. Fajas L, Debril MB and Auwerx J: Peroxisome proliferator-activated receptor-gamma: from adipogenesis to carcinogenesis (Review). J Mol Endocrinol 27: 1-9, 2001.
37. Zheng L and Lee WH: The retinoblastoma gene: a prototypic and multifunctional tumor suppressor (Review). Exp Cell Res 264: 2-18, 2001.
38. DiCiommo D, Gallie BL and Bremner R: Retinoblastoma: the disease, gene and protein provide critical leads to understand cancer (Review). Semin Cancer Biol 10: 255-269, 2000.
39. Altiok S, Xu M and Spiegelman BM: PPARgamma induces cell cycle withdrawal: inhibition of E2F/DP DNA-binding activity via down-regulation of PP2A. Genes Dev 11: 1987-1998, 1997.
40. La Thangue NB and Rigby PW: An adenovirus E1A-like transcription factor is regulated during the differentiation of murine embryonal carcinoma stem cells. Cell 49: 507-513, 1987.
41. Hara E, Okamoto S, Nakada S, Taya Y, Sekiya S and Oda K: Protein phosphorylation required for the formation of E2F complexes regulates N-myc transcription during differentiation of human embryonal carcinoma cells. Oncogene 8: 1023-1032, 1993.
42. Melamed D, Tiefenbrun N, Yarden A and Kimchi A: Interferons and interleukin-6 suppress the DNA-binding activity of E2F in growth-sensitive hematopoietic cells. Mol Cell Biol 13: 5255-5265, 1993.
43. Kranenburg O, De Groot RP, van der Eb AJ and Zantema A: Differentiation of P19 EC cells leads to differential modulation of cyclin-dependent kinase activities and to changes in the cell cycle profile. Oncogene 10: 87-95, 1995.
44. Harlow SP, Duda RB and Bauer KD: Diagnostic utility of DNA content flow cytometry in follicular neoplasms of the thyroid. J Surg Oncol 50: 1-6, 1992.
45. Konarska L, Skierski J, Ellert A, Steinbrich J, Wozniak A and Kalczak M: Comparative studies of nuclear DNA content in benign and malignant thyroid lesions. Acta Biochim Pol 48: 783-793, 2001.
46. Wakino S, Kintscher U, Kim S, Yin F, Hsueh WA and Law RE: Peroxisome proliferator-activated receptor gamma ligands inhibit retinoblastoma phosphorylation and G1→S transition in vascular smooth muscle cells. J Biol Chem 275: 22435-22441, 2000.
47. Chung SH, Onoda N, Ishikawa T, Ogisawa K, Takenaka C, Yano Y, Hato F and Hirakawa K: Peroxisome proliferator-activated receptor gamma activation induces cell cycle arrest via the p53-independent pathway in human anaplastic thyroid cancer cells. Jpn J Cancer Res 93: 1358-1365, 2002.
48. Martelli ML, Iuliano R, Le Pera I, Sama' I, Monaco C, Cammarota S, Kroll T, Chiariotti L, Santoro M and Fusco A: Inhibitory effects of peroxisome poliferator-activated receptor gamma on thyroid carcinoma cell growth. J Clin Endocrinol Metab 87: 4728-4735, 2002.