Thiazolidinediones inhibit hepatocarcinogenesis in hepatitis B virus-transgenic mice by peroxisome proliferator-activated receptor γ-independent regulation of nucleophosmin

Hepatology

Volumn 52, Issue 2, 2010, Pages 493-505

  Galli, Andrea ^a   Ceni, Elisabetta ^a   Mello, Tommaso ^a   Polvani, Simone ^a,b   Tarocchi, Mirko ^a   Buccoliero, Francesca ^a   Lisi, Francesca ^a   Cioni, Laura ^a   Ottanelli, Barbara ^a   Foresta, Valeria ^a   Mastrobuoni, Guido ^a   Moneti, Gloriano ^a   Pieraccini, Giuseppe ^a   Surrenti, Calogero ^a   Milani, Stefano ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b FiorGen Foundation   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; N (2 BENZOYLPHENYL) O [2 (METHYL 2 PYRIDINYLAMINO)ETHYL]TYROSINE; NUCLEOPHOSMIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; PROTEIN P21; PROTEIN P53; ROSIGLITAZONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; GENE ACTIVITY; GENE CONTROL; GENE DELETION; HEPATITIS B VIRUS; LIVER CARCINOGENESIS; LIVER TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSGENIC ANIMAL;

ANIMALS; CARCINOMA, HEPATOCELLULAR; HEPATITIS B VIRUS; HEPATOCYTES; LIVER NEOPLASMS; MICE; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; NUCLEAR PROTEINS; PPAR GAMMA; THIAZOLIDINEDIONES; TUMOR CELLS, CULTURED;

EID: 77955685379     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.23669     Document Type: Article

References (45)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001;94:153-156.
2. Llovet JM, Di Bisceglie AM, Bruix J, Kramer BS, Lencioni R, Zhu AX, et al. Design and endpoints of clinical trials in hepatocellular carcinoma. J Natl Cancer Inst 2008;100:698-711.
3. Quinn CE, Hamilton PK, Lockhart CJ, McVeigh GE. Thiazolidinediones: effects on insulin resistance and the cardiovascular system. Br J Pharmacol 2008;153:636-645.
4. Rocchi S, Auverrx J. Peroxisome proliferator activated-receptor γ: a versatile metabolic regulator. Ann Med 1999;31:342-351.
5. Galli A, Mello T, Ceni E, Surrenti E, Surrenti C. The potential of anti-diabetic thiazolidinediones for anticancer therapy. Expert Opin Investig Drugs 2006;15:1039-1049.
6. Ondrey F. Peroxisome proliferator-activated receptor γ pathways targeting in carcinogenesis: implication for chemoprevention. Clin Cancer Res 2009;15:2-8.
7. Saez E, Tontonoz P, Nelson MC, Alvarez, Ming UT, Baird SM, et al. Activators of nuclear receptor PPARγ enhance colon polyp formation. Nat Med 1998;4:1058-1061.
8. Saez E, Rosenfeld J, Livolsi A, Olson P, Lombardo E, Nelson M, et al. PPAR gamma signaling exacerbates mammary gland tumor development. Genes Dev 2004;18:528-540.
9. Jiang JG, Johonson C, Zarnegar R. Peroxisome proliferator-activated receptor γ-mediated transcriptional up-regulation of hepatocyte growth factor gene promoter via a novel composite cis-acting element. J Biol Chem 2001;276:25049-25056.
10. Yu J, Qiao L, Zimmermann L, Ebert MP, Zhang H, Lin W, et al. Troglitazone inhibits tumor growth in hepatocellular carcinoma in vitro and in vivo. HEPATOLOGY 2006;43:134-143.
11. Schaefer KL, Wada K, Takahashi H, Matsuhashi H, Ohnisi S, Wolfe MM, et al. Peroxisome proliferator-activated receptor gamma inhibition prevents adhesion to the extracellular matrix and induces anoikis in hepatocellular carcinoma cells. Cancer Res 2005;65:2251-2259.
12. Dunsford HA, Sell S, Chisari FV. Hepatocarcinogenesis due to chronic liver cell injury in hepatitis B virus trangenic mice. Cancer Res 1990;50:3400-3407.
13. Rasband WS. ImageJ. Bethesda, MD: National Institutes of Health; 1997-2009. http://rsb.info.nih.gov/ij/.
14. Fujioka H, Hunt PJ, Rozga J, Wu GD, Cramer DV, Demetriu AA, et al. Carboxyfluorescein (CFSE) labelling of hepatocytes for short-term localization following intraportal transplantation. Cell Transplant 1994;3:397-408.
15. Ceni E, Crabb DW, Foschi M, Mello T, Tarocchi M, Patussi V, et al. Acetaldehyde inhibits PPARγ via H2O2-mediated c-Abl activation in human hepatic stellate cells. Gastroenterology 2006;131:1235-1252.
16. Im SS, Kim JW, Kim TH, Song XL, Kin SY, Ahn YH. Identification and characterization of peroxisome proliferator response element in the mouse GLUT2 promoter. Exp Mol Med 2005;37:101-110.
17. Crawford DR, Ostrowski S, Vakharia D, Ilic Z, Sell S. Separate origins of hepatitis B virus surface antigen-negative foci and hepatocellular carcinomas in trangenic HBsAg (alb/psx) mice. Am J Pathol 2006;169:223-232.
18. Grisendi S, Mecucci C, Falini B, Pandolfi P. Nucleophosmin and cancer. Nature Rev 2006;6:493-505.
19. Tarapore P, Shinmura K, Suzuki H, Tokuyama Y, Kim SH, Mayeda A, et al. Thr199 phosphorylation targets nucleophosmin to nuclear speckles and represses pre-mRNA processing. FEBS Lett 2006;23:399-409.
20. He G, Sung Y, DiGiovanni J, Fisher SM. Thiazolidinediones inhibit insulin-like growth factor-I-induced activation of p70S6 kinase and suppress indulin-like growth factor-I tumor promoting activity. Cancer Res 2006;66:1873-1879.
21. Li J, Zhang X, Sejas DP, Bagby GC, Pang Q. Hypoxia-induced nucleophosmiin protects cell death through inhibition of p53. J Biol Chem 2004;279:41275- 41279.
22. 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.
23. Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 2008;77:289-312.
24. Ceni E, Mello T, Tarocchi M, Crabb DW, Caldini A, Invernizzi P, et al. Antidiabetic thiazolidinediones induce ductal differentiation but not apoptosis in pancreatic cancer cells. World J Gastroenterol 2005;11:1122-1130.
25. Weng JR, Chen CY, Pinzone JJ, Ringel MD, Chen CS. Beyond peroxisome proliferator-activated receptor gamma signaling: the multi-facets of the antitumor effect of thiazolidinediones. Endocr Relat Cancer 2006;13:401-413.
26. Day C. Thiazolidinediones: a new class of antidiabetic drugs. Diabet Med 1999;16:179-192.
27. Saez E, Olson P, Evans RM. Genetic deficiency in Pparg does not alter development of experimental prostate cancer. Nature Med 2003;9:1265-1266.
28. Cui Y, Miyoshi K, Claudio E, Siebenlist UK, Gonzalez FJ, Flaws J, et al. Loss of peroxisome proliferator-activated receptor γ (PPARγ) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. J Biol Chem 2005;277:17830-17835.
29. Kristiansen G, Jacob J, Buckendahl AC, Grutzmann R, Alldinger I, Sipos B, et al. Peroxisome proliferator-activated receptor gamma is highly expressed in pancreatic cancer and is associated with shorter overall survival times. Clin Cancer Res 2006;12:6444-6451.
30. Zhang GY, Ahmed N, Riley C, Oliva K, Barker G, Quinn MA, et al. Enhanced expression of peroxisome proliferator-activated receptor gamma in epithelial ovarian carcinoma. Br J Cancer 2005;92:113-119.
31. Galli A, Stewart M, Dorris R, Crabb D. High-level expression of RXRalpha and the presence of endogenous ligands contribute to expression of a peroxisome proliferator-activated receptor-responsive gene in hepatoma cells. Arch Biochem Biophys 1998;354:288-294.
32. Mueller E, Smith M, Sarraf P, Kroll T, Aiyer A, Kaufman DS, et al. Effects of ligand activation of peroxisome proliferator activated receptor γ in human prostate cancer. Proc Natl Acad Sci USA 2000;97:10990-10995.
33. Giordano TJ, Au AY, Kuick R, Thomas DG, Rhodes DR, Wilhem KJ, et al. Delineation, functional validation, and bioinformatic evaluation of gene expression in thyroid follicular carcinomas with the PAX8-PPARG translocation. Clin Cancer Res 2006;12:1983-1993.
34. Wei S, Yang J, Lee SL, Kulp SK, Chen CS. PPARgamma-independent antitumor effects of thiazolidinediones. Cancer Lett 2009;276:119-124.
35. Wei S, Yang HC, Chuang HC, Yang J, Kulp SK, Lu PJ, et al. A novel mechanism by which thiazolidinediones facilitate the proteasomal degradation of cyclin D1 in cancer cells. J Biol Chem 2008;283:26759-26770.
36. Yun JP, Miao J, Chen GG, Tian QH, Zhang CQ, Xiang J, et al. Increased expression of nucleophosmin/B23 in hepatocellular carcinoma and correlation with clinicopathological parameters. Br J Cancer 2007;96:477-484.
37. Fryer LG, Parbu-Patel A, Carling D. The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J Biol Chem 2002;277:25226-25232.
38. Wang W, Guan KL. AMP-activated protein kinase and cancer. Acta Physiol 2009;196:55-63.
39. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, et al. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 2005;18:283-293.
40. Wu MH, Chang JH, Yung BY. Resistance to UV-induced cell-killing in nucleophosmin/B23 over-expressed NIH 3T3 fibroblasts: enhancement of DNA repair and up-regulation of PCNA in association with nucleophosmin/B23 over-expression. Carcinogenesis 2002;23:93-100.
41. Li J, Zhang X, Sejas DP, Pang Q. Negative regulation of p53 by nucleophosmin antagonizes stress-induced apoptosis in human normal and malignant hematopoietic cells. Leuk Res 2005;29:1415-1423.
42. Li J, Zhang X, Sejas DP, Bagby GC, Pang Q. Hypoxia-induced nucleophosmin protects cell death through inhibition of p53. J Biol Chem 2004;279:41275-41279.
43. Pang Q, Christianson TA, Koretsky T, Carlson H, David L, Keeble W, et al. Nucleophosmin interacts with and inhibits the catalytic function of eukaryotic initiation factor 2 kinase PKR. J Biol Chem 2003;278:41709-41717.
44. Galli A, Crabb DW, Ceni E, Salzano R, Mello T, Svegliati-Baroni G, et al. Antidiabetic thiazolidinediones inhibit collagen synthesis and hepatic stellate cell activation in vivo and in vitro. Gastroenterology 2002;122:1924-1940.
45. Belfort R, Harrison SA, Brown K, Darland C, Finch J, Hardies J, et al. A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis. N Engl J Med 2006;355:2297-2307.