Wnt/β-catenin signaling protects mouse liver against oxidative stress-induced apoptosis through the inhibition of forkhead transcription factor FoxO3

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17214-17224

  Tao, Guo Zhong ^a   Lehwald, Nadja ^a,b   Jang, Kyu Yun ^a,c   Baek, Joy ^a   Xu, Baohui ^a   Omary, M Bishr ^d   Sylvester, Karl G ^a,e  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c Chonbuk National University Medical School   (South Korea)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e LUCILE PACKARD CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC FUNCTION; CATENIN SIGNALING; FORKHEAD TRANSCRIPTIONS; HEPATOCELLULAR; IMMUNOFLUORESCENCE STAINING; LIVER INJURIES; STRESS-INDUCED; WILD-TYPE CONTROLS;

GENES; LIVING SYSTEMS STUDIES; MAMMALS; NUTRITION; OXIDATIVE STRESS; TISSUE; TRANSCRIPTION FACTORS;

SIGNALING;

BETA CATENIN; BIM PROTEIN; PARAQUAT; PROTEIN P27; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR FKHRL1; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIM GENE; CELL SURVIVAL; CONTROLLED STUDY; GENE TARGETING; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LIVER INJURY; LIVER PROTECTION; MOUSE; NONHUMAN; OXIDATIVE STRESS; P27 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SGK1 GENE; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE;

CYTOPROTECTION; FOXO; LIVER INJURY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES (ROS); WNT SIGNALING;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE; CELL NUCLEUS; DRUG-INDUCED LIVER INJURY; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEPATOCYTES; IMMEDIATE-EARLY PROTEINS; LIVER; MICE; MICE, TRANSGENIC; OXIDATIVE STRESS; PARAQUAT; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; PYRIDINES; RNA, SMALL INTERFERING; WNT SIGNALING PATHWAY;

MUS;

EID: 84879054654     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.445965     Document Type: Article

References (53)

1. Loguercio, C., and Federico, A. (2003) Oxidative stress in viral and alcoholic hepatitis. Free Radic. Biol. Med. 34, 1-10 (Pubitemid 36043881)
2. Diesen, D. L., and Kuo, P. C. (2010) Nitric oxide and redox regulation in the liver. Part I. General considerations and redox biology in hepatitis. J. Surg. Res. 162, 95-109
3. Dey, A., and Cederbaum, A. I. (2006) Alcohol and oxidative liver injury. Hepatology 43, S63-S74
4. Fausto, N. (2004) Liver regeneration and repair. Hepatocytes, progenitor cells, and stem cells. Hepatology 39, 1477-1487
5. Kaplowitz, N. (2000) Mechanisms of liver cell injury. J. Hepatol. 32, 39-47
6. Zatloukal, K., French, S. W., Stumptner, C., Strnad, P., Harada, M., Toivola, D. M., Cadrin, M., and Omary, M. B. (2007) From Mallory to Mallory-Denk bodies. What, how and why? Exp. Cell Res. 313, 2033-2049 (Pubitemid 46842981)
7. Strnad, P., Zatloukal, K., Stumptner, C., Kulaksiz, H., and Denk, H. (2008) Mallory-Denk-bodies. Lessons from keratin-containing hepatic inclusion bodies. Biochim. Biophys. Acta 1782, 764-774
8. Thompson, M. D., and Monga, S. P. (2007) WNT/β-catenin signaling in liver health and disease. Hepatology 45, 1298-1305 (Pubitemid 46775794)
9. Monga, S. P. (2011) Role of Wnt/β-catenin signaling in liver metabolism and cancer. Int. J. Biochem. Cell Biol. 43, 1021-1029
10. Behari, J., Yeh, T. H., Krauland, L., Otruba, W., Cieply, B., Hauth, B., Apte, U., Wu, T., Evans, R., and Monga, S. P. (2010) Liver-specific β-catenin knockout mice exhibit defective bile acid and cholesterol homeostasis and increased susceptibility to diet-induced steatohepatitis. Am. J. Pathol. 176, 744-753
11. Lehwald, N., Tao, G. Z., Jang, K. Y., Papandreou, I., Liu, B., Liu, B., Pysz, M. A., Willmann, J. K., Knoefel, W. T., Denko, N. C., and Sylvester, K. G. (2012) β-Catenin regulates hepatic mitochondrial function and energy balance in mice. Gastroenterology 143, 754-764
12. Lehwald, N., Tao, G. Z., Jang, K. Y., Sorkin, M., Knoefel, W. T., and Sylvester, K. G. (2011) Wnt-β-catenin signaling protects against hepatic ischemia and reperfusion injury in mice. Gastroenterology 141, 707-718
13. Essers, M. A., de Vries-Smits, L. M., Barker, N., Polderman, P. E., Burgering, B. M., and Korswagen, H. C. (2005) Functional interaction between β-catenin and FOXO in oxidative stress signaling. Science 308, 1181-1184 (Pubitemid 40696437)
14. Hoogeboom, D., Essers, M. A., Polderman, P. E., Voets, E., Smits, L. M., and Burgering, B. M. (2008) Interaction of FOXO with β-catenin inhibits β-catenin/T cell factor activity. J. Biol. Chem. 283, 9224-9230
15. van der Horst, A., and Burgering, B. M. (2007) Stressing the role of FoxO proteins in lifespan and disease. Nat. Rev. Mol. Cell Biol. 8, 440-450
16. van der Vos, K. E., and Coffer, P. J. (2008) FOXO-binding partners. It takes two to tango. Oncogene 27, 2289-2299
17. Calnan, D. R., and Brunet, A. (2008) The FoxO code. Oncogene 27, 2276-2288 (Pubitemid 351501779)
18. Salih, D. A., and Brunet, A. (2008) FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr. Opin. Cell Biol. 20, 126-136
19. Burgering, B. M., and Kops, G. J. (2002) Cell cycle and death control. Long live Forkheads. Trends Biochem. Sci. 27, 352-360 (Pubitemid 34756518)
20. Wilk, A., Urbanska, K., Grabacka, M., Mullinax, J., Marcinkiewicz, C., Impastato, D., Estrada, J. J., and Reiss, K. (2012) Fenofibrate-induced nuclear translocation of FoxO3A triggers Bim-mediated apoptosis in glioblastoma cells in vitro. Cell Cycle 11, 2660-2671
21. Stahl, M., Dijkers, P. F., Kops, G. J., Lens, S. M., Coffer, P. J., Burgering, B. M., and Medema, R. H. (2002) The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J. Immunol. 168, 5024-5031 (Pubitemid 34495965)
22. Huang, H., and Tindall, D. J. (2007) Dynamic FoxO transcription factors. J. Cell Sci. 120, 2479-2487 (Pubitemid 47323857)
23. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, M. J., Arden, K. C., Blenis, J., and Greenberg, M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868 (Pubitemid 29165088)
24. Khatri, S., Yepiskoposyan, H., Gallo, C. A., Tandon, P., and Plas, D. R. (2010) FOXO3a regulates glycolysis via transcriptional control of tumor suppressor TSC1. J. Biol. Chem. 285, 15960-15965
25. Kolligs, F. T., Hu, G., Dang, C. V., and Fearon, E. R. (1999) Neoplastic transformation of RK3E by mutant β-catenin requires deregulation of Tcf/Lef transcription but not activation of c-myc expression. Mol. Cell. Biol. 19, 5696-5706 (Pubitemid 29339926)
26. Schwartz, D. R., Wu, R., Kardia, S. L., Levin, A. M., Huang, C. C., Shedden, K. A., Kuick, R., Misek, D. E., Hanash, S. M., Taylor, J. M., Reed, H., Hendrix, N., Zhai, Y., Fearon, E. R., and Cho, K. R. (2003) Novel candidate targets of β-catenin/T-cell factor signaling identified by gene expression profiling of ovarian endometrioid adenocarcinomas. Cancer Res. 63, 2913-2922 (Pubitemid 36667164)
27. Listenberger, L. L., Ory, D. S., and Schaffer, J. E. (2001) Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J. Biol. Chem. 276, 14890-14895
28. Deleted in proof
29. Hanada, S., Snider, N. T., Brunt, E. M., Hollenberg, P. F., and Omary, M. B. (2010) Gender dimorphic formation of mouse Mallory-Denk bodies and the role of xenobiotic metabolism and oxidative stress. Gastroenterology 138, 1607-1617
30. Tao, G. Z., Looi, K. S., Toivola, D. M., Strnad, P., Zhou, Q., Liao, J., Wei, Y., Habtezion, A., and Omary, M. B. (2009) Keratins modulate the shape and function of hepatocyte mitochondria. A mechanism for protection from apoptosis. J. Cell Sci. 122, 3851-3855
31. Weerasinghe, S. V., Moons, D. S., Altshuler, P. J., Shah, Y. M., and Omary, M. B. (2011) Fibrinogen-γ proteolysis and solubility dynamics during apoptotic mouse liver injury. Heparin prevents and treats liver damage. Hepatology 53, 1323-1332
32. Tao, G. Z., Li, D. H., Zhou, Q., Toivola, D. M., Strnad, P., Sandesara, N., Cheung, R. C., Hong, A., and Omary, M. B. (2008) Monitoring of epithelial cell caspase activation via detection of durable keratin fragment formation. J. Pathol. 215, 164-174 (Pubitemid 351786035)
33. Habtezion, A., Toivola, D. M., Asghar, M. N., Kronmal, G. S., Brooks, J. D., Butcher, E. C., and Omary, M. B. (2011) Absence of keratin 8 confers a paradoxical microflora-dependent resistance to apoptosis in the colon. Proc. Natl. Acad. Sci. U.S.A. 108, 1445-1450
34. Tan, X., Behari, J., Cieply, B., Michalopoulos, G. K., and Monga, S. P. (2006) Conditional deletion of β-catenin reveals its role in liver growth and regeneration. Gastroenterology 131, 1561-1572 (Pubitemid 44708943)
35. Tan, X., Apte, U., Micsenyi, A., Kotsagrelos, E., Luo, J. H., Ranganathan, S., Monga, D. K., Bell, A., Michalopoulos, G. K., and Monga, S. P. (2005) Epidermal growth factor receptor. A novel target of the Wnt/β-catenin pathway in liver. Gastroenterology 129, 285-302 (Pubitemid 41002061)
36. Funato, Y., Michiue, T., Asashima, M., and Miki, H. (2006) The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-β-catenin signalling through dishevelled. Nat. Cell Biol. 8, 501-508
37. Hoogeboom, D., and Burgering, B. M. (2009) Should I stay or should I go. β-Catenin decides under stress. Biochim. Biophys. Acta 1796, 63-74
38. Kaidi, A., Williams, A. C., and Paraskeva, C. (2007) Interaction between β-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat. Cell Biol. 9, 210-217 (Pubitemid 46420864)
39. Snider, N. T., Weerasinghe, S. V., Singla, A., Leonard, J. M., Hanada, S., Andrews, P. C., Lok, A. S., and Omary, M. B. (2011) Energy determinants GAPDH and NDPK act as genetic modifiers for hepatocyte inclusion formation. J. Cell Biol. 195, 217-229
40. Zhang, K., Li, L., Qi, Y., Zhu, X., Gan, B., DePinho, R. A., Averitt, T., and Guo, S. (2012) Hepatic suppression of Foxo1 and Foxo3 causes hypoglycemia and hyperlipidemia in mice. Endocrinology 153, 631-646
41. Tao, R., Wei, D., Gao, H., Liu, Y., DePinho, R. A., and Dong, X. C. (2011) Hepatic FoxOs regulate lipid metabolism via modulation of expression of the nicotinamide phosphoribosyltransferase gene. J. Biol. Chem. 286, 14681-14690
42. Tenbaum, S. P., Ordonez-Moran, P., Puig, I., Chicote, I., Arques, O., Landolfi, S., Fernandez, Y., Herance, J. R., Gispert, J. D., Mendizabal, L., Aguilar, S., Cajal, S. R., Schwartz, S., Jr., Vivancos, A., Espin, E., Rojas, S., Baselga, J., Tabernero, J., Munoz, A., and Palmer, H. G. (2012) β-Catenin confers resistance to PI3K and AKT inhibitors and subverts FOXO3a to promote metastasis in colon cancer. Nat. Med. 18, 892-901
43. Yan, Y., and Lackner, M. R. (2012) FOXO3a and β-catenin co-localization. Double trouble in colon cancer? Nat. Med. 18, 854-856
44. Shin, I., Bakin, A. V., Rodeck, U., Brunet, A., and Arteaga, C. L. (2001) Transforming growth factor β enhances epithelial cell survival via Akt-dependent regulation of FKHRL1. Mol. Biol. Cell 12, 3328-3339 (Pubitemid 33108468)
45. Dehner, M., Hadjihannas, M., Weiske, J., Huber, O., and Behrens, J. (2008) Wnt signaling inhibits Forkhead box O3a-induced transcription and apoptosis through up-regulation of serum- and glucocorticoid-inducible kinase 1. J. Biol. Chem. 283, 19201-19210
46. Czaja, M. J. (2007) Cell signaling in oxidative stress-induced liver injury. Semin. Liver Dis. 27, 378-389
47. Nejak-Bowen, K., Kikuchi, A., and Monga, S. P. (2013) β-Catenin-NF-κB interactions in murine hepatocytes. A complex to die for. Hepatology 57, 763-774
48. Kim, P. J., Plescia, J., Clevers, H., Fearon, E. R., and Altieri, D. C. (2003) Survivin and molecular pathogenesis of colorectal cancer. Lancet 362, 205-209 (Pubitemid 36859937)
49. Tapia, J. C., Torres, V. A., Rodriguez, D. A., Leyton, L., and Quest, A. F. (2006) Casein kinase 2 (CK2) increases survivin expression via enhanced β-catenin-T cell factor/lymphoid enhancer binding factor-dependent transcription. Proc. Natl. Acad. Sci. U.S.A. 103, 15079-15084 (Pubitemid 44583167)
50. Leong, M. L., Maiyar, A. C., Kim, B., O'Keeffe, B. A., and Firestone, G. L. (2003) Expression of the serum- and glucocorticoid-inducible protein kinase, Sgk, is a cell survival response to multiple types of environmental stress stimuli in mammary epithelial cells. J. Biol. Chem. 278, 5871-5882 (Pubitemid 36800834)
51. Xie, X. W., Liu, J. X., Hu, B., and Xiao, W. (2011) Zebrafish foxo3b negatively regulates canonical Wnt signaling to affect early embryogenesis. PloS One 6, e24469
52. Kamo, N., Ke, B., Busuttil, R. W., and Kupiec-Weglinski, J. W. (2013) PTEN-mediated Akt/β-catenin/Foxo1 signaling regulates innate immune responses in mouse liver ischemia/reperfusion injury. Hepatology 57, 289-298
53. Brookheart, R. T., Michel, C. I., and Schaffer, J. E. (2009) As a matter of fat. Cell Metab. 10, 9-12