The liver-specific tumor suppressor STAT5 controls expression of the reactive oxygen species-generating enzyme NOX4 and the proapoptotic proteins PUMA and BIM in mice

Hepatology

Volumn 56, Issue 6, 2012, Pages 2375-2386

  Yu, Ji Hoon ^a   Zhu, Bing Mei ^b   Riedlinger, Gregory ^c   Kang, Keunsoo ^a   Hennighausen, Lothar ^a,d  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

^c NATIONAL CANCER INSTITUTE   (United States)

^d Dankook University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; CASPASE 3; GROWTH HORMONE; PUMA PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; STAT5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; LIVER TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CARBON TETRACHLORIDE; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CELLS, CULTURED; FATTY LIVER; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GROWTH HORMONE; HEPATOCYTES; LIVER; LIVER NEOPLASMS; MEMBRANE PROTEINS; MICE; NADPH OXIDASE; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEINS;

EID: 84870574524     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.25900     Document Type: Article

References (34)

1. Hennighausen L, Robinson GW. Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes Dev 2008; 22: 711-721.
2. Zhang Q, Wang HY, Liu X, Wasik MA. STAT5A is epigenetically silenced by the tyrosine kinase NPM1-ALK and acts as a tumor suppressor by reciprocally inhibiting NPM1-ALK expression. Nat Med 2007; 13: 1341-1348.
3. Hosui A, Kimura A, Yamaji D, Zhu BM, Na R, Hennighausen L. Loss of STAT5 causes liver fibrosis and cancer development through increased TGF-beta and STAT3 activation. J Exp Med 2009; 206: 819-831.
4. Mallette FA, Gaumont-Leclerc MF, Ferbeyre G. The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev 2007; 21: 43-48.
5. Calabrese V, Mallette FA, Deschenes-Simard X, Ramanathan S, Gagnon J, Moores A, et al. SOCS1 links cytokine signaling to p53 and senescence. Mol Cell 2009; 36: 754-767.
6. Cui Y, Hosui A, Sun R, Shen K, Gavrilova O, Chen W, et al. Loss of signal transducer and activator of transcription 5 leads to hepatosteatosis and impaired liver regeneration. HEPATOLOGY 2007; 46: 504-513.
7. Holloway MG, Cui Y, Laz EV, Hosui A, Hennighausen L, Waxman DJ. Loss of sexually dimorphic liver gene expression upon hepatocyte-specific deletion of Stat5a-Stat5b locus. Endocrinology 2007; 148: 1977-1986.
8. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007; 26: 1324-1337.
9. Ren D, Tu HC, Kim H, Wang GX, Bean GR, Takeuchi O, et al. BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science 2010; 330: 1390-1393.
10. Karst AM, Dai DL, Martinka M, Li G. PUMA expression is significantly reduced in human cutaneous melanomas. Oncogene 2005; 24: 1111-1116.
11. Hemann MT, Zilfou JT, Zhao Z, Burgess DJ, Hannon GJ, Lowe SW. Suppression of tumorigenesis by the p53 target PUMA. Proc Natl Acad Sci U S A 2004; 101: 9333-9338.
12. Erlacher M, Labi V, Manzl C, Bock G, Tzankov A, Hacker G, et al. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J Exp Med 2006; 203: 2939-2951.
13. Nelson DA, Tan TT, Rabson AB, Anderson D, Degenhardt K, White E. Hypoxia and defective apoptosis drive genomic instability and tumorigenesis. Genes Dev 2004; 18: 2095-2107.
14. Cazanave SC, Mott JL, Elmi NA, Bronk SF, Werneburg NW, Akazawa Y, et al. JNK1-dependent PUMA expression contributes to hepatocyte lipoapoptosis. J Biol Chem 2009; 284: 26591-26602.
15. Akazawa Y, Cazanave S, Mott JL, Elmi N, Bronk SF, Kohno S, et al. Palmitoleate attenuates palmitate-induced Bim and PUMA up-regulation and hepatocyte lipoapoptosis. J Hepatol 2010; 52: 586-593.
16. Kaufmann T, Jost PJ, Pellegrini M, Puthalakath H, Gugasyan R, Gerondakis S, et al. Fatal hepatitis mediated by tumor necrosis factor TNFα requires caspase-8 and involves the BH3-only proteins Bid and Bim. Immunity 2009; 30: 56-66.
17. Schmich K, Schlatter R, Corazza N, Sá Ferreira K, Ederer M, Brunner T, et al. Tumor necrosis factor α sensitizes primary murine hepatocytes to Fas/CD95-induced apoptosis in a Bim- and Bid-dependent manner. HEPATOLOGY 2011; 53: 282-292.
18. Basuroy S, Tcheranova D, Bhattacharya S, Leffler CW, Parfenova H. Nox4 NADPH oxidase-derived reactive oxygen species, via endogenous carbon monoxide, promote survival of brain endothelial cells during TNF-α-induced apoptosis. Am J Physiol Cell Physiol 2011; 300: C256-C265.
19. Carmona-Cuenca I, Roncero C, Sancho P, Caja L, Fausto N, Fernández M, et al. Upregulation of the NADPH oxidase NOX4 by TGF-beta in hepatocytes is required for its pro-apoptotic activity. J Hepatol 2008; 49: 965-976.
20. Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, Sadoshima J. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci U S A 2010; 107: 15565-15570.
21. Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res 2010; 106: 1253-1264.
22. Senturk S, Mumcuoglu M, Gursoy-Yuzugullu O, Cingoz B, Akcali KC, Ozturk M. Transforming growth factor-beta induces senescence in hepatocellular carcinoma cells and inhibits tumor growth. HEPATOLOGY 2010; 52: 966-974.
23. Yakar S, Liu JL, Stannard B, Butler A, Accili D, Sauer B, et al. Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci U S A 1999; 96: 7324-7329.
24. Paik YH, Iwaisako K, Seki E, Inokuchi S, Schnabl B, Osterreicher CH, et al. The nicotinamide adenine dinucleotide phosphate oxidase (NOX) homologues NOX1 and NOX2/gp91(phox) mediate hepatic fibrosis in mice. HEPATOLOGY 2011; 53: 1730-1741.
25. Yu JH, Zhu BM, Wickre M, Riedlinger G, Chen W, Hosui A, et al. The transcription factors signal transducer and activator of transcription 5A (STAT5A) and STAT5B negatively regulate cell proliferation through the activation of cyclin-dependent kinase inhibitor 2b (Cdkn2b) and Cdkn1a expression. HEPATOLOGY 2010; 52: 1808-1818.
26. Carnesecchi S, Deffert C, Donati Y, Basset O, Hinz B, Preynat-Seauve O, et al. A key role for NOX4 in epithelial cell death during development of lung fibrosis. Antioxid Redox Signal 2011; 15: 607-619.
27. Jiang JX, Venugopal S, Serizawa N, Chen X, Scott F, Li Y, et al. Reduced nicotinamide adenine dinucleotide phosphate oxidase 2 plays a key role in stellate cell activation and liver fibrogenesis in vivo. Gastroenterology 2010; 139: 1375-1384.
28. Cui W, Matsuno K, Iwata K, Ibi M, Matsumoto M, Zhang J, et al. NOX1/nicotinamide adenine dinucleotide phosphate, reduced form (NADPH) oxidase promotes proliferation of stellate cells and aggravates liver fibrosis induced by bile duct ligation. HEPATOLOGY 2011; 54: 949-958.
29. Naik E, O'Reilly LA, Asselin-Labat ML, Merino D, Lin A, Cook M, et al. Destruction of tumor vasculature and abated tumor growth upon VEGF blockade is driven by proapoptotic protein Bim in endothelial cells. J Exp Med 2011; 208: 1351-1358.
30. Egle A, Harris AW, Bouillet P, Cory S. Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc Natl Acad Sci U S A 2004; 101: 6164-6169.
31. Qiu W, Wu B, Wang X, Buchanan ME, Regueiro MD, Hartman DJ, et al. PUMA-mediated intestinal epithelial apoptosis contributes to ulcerative colitis in humans and mice. J Clin Invest 2011; 121: 1722-1732.
32. Qiu W, Carson-Walter EB, Kuan SF, Zhang L, Yu J. PUMA suppresses intestinal tumorigenesis in mice. Cancer Res 2009; 69: 4999-5006.
33. Friedbichler K, Themanns M, Mueller KM, Schlederer M, Kornfeld JW, Terracciano LM, et al. Growth-hormone-induced signal transducer and activator of transcription 5 signaling causes gigantism, inflammation, and premature death but protects mice from aggressive liver cancer. HEPATOLOGY 2012; 55: 941-952.
34. Mueller KM, Kornfeld JW, Friedbichler K, Blaas L, Egger G, Esterbauer H, et al. Impairment of hepatic growth hormone and glucocorticoid receptor signaling causes steatosis and hepatocellular carcinoma in mice. HEPATOLOGY 2011; 54: 1398-1409.