GSK-3β promotes cell survival by modulating Bif-1-dependent autophagy and cell death

Journal of Cell Science

Volumn 123, Issue 6, 2010, Pages 861-870

  Yang, Jun ^a,b   Takahashi, Yoshinori ^c   Cheng, Erdong ^a   Liu, Jihong ^b   Terranova, Paul F ^d   Zhao, Bin ^e   Thrasher, J Brantley ^a   Wang, Hong Gang ^c   Li, Benyi ^a,d,e  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^e GUANGDONG MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Autophagy; Bif 1; GSK 3 ; Necrosis

Indexed keywords

BIOLOGICAL MARKER; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN; PROTEIN BIF 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PROTEIN KINASE INHIBITOR; SH3GLB1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL; CELL DEATH; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; ENZYME SPECIFICITY; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MALE; NECROSIS; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN FUNCTION; BIOLOGICAL MODEL; CULTURE MEDIUM; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; CELL SURVIVAL; CULTURE MEDIA, SERUM-FREE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MALE; MODELS, BIOLOGICAL; NECROSIS; PROTEIN KINASE INHIBITORS;

EID: 77951200644     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.060475     Document Type: Article

References (52)

1. Artal-Sanz, M., Samara, C., Syntichaki, P. and Tavernarakis, N. (2006). Lysosomal biogenesis and function is critical for necrotic cell death in Caenorhabditis elegans. J. Cell Biol. 173, 231-239.
2. Bhat, R., Xue, Y., Berg, S., Hellberg, S., Ormö, M., Nilsson, Y., Radesäter, A. C., Jerning, E., Markgren, P. O., Borgegård, T. et al. (2003). Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J. Biol. Chem. 278, 45937-45945.
3. Boya, P. and Kroemer, G. (2008). Lysosomal membrane permeabilization in cell death. Oncogene 27, 6434-6451.
4. Boya, P., González-Polo, R. A., Casares, N., Perfettini, J. L., Dessen, P., Larochette, N., Métivier, D., Meley, D., Souquere, S., Yoshimori, T. et al. (2005). Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol. 25, 1025-1040.
5. Cao, C., Subhawong, T., Albert, J. M., Kim, K. W., Geng, L., Sekhar, K. R., Gi, Y. J. and Lu, B. (2006). Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer Res. 66, 10040-10047.
6. Carmichael, J., Sugars, K. L., Bao, Y. P. and Rubinsztein, D. C. (2002). Glycogen synthase kinase-3beta inhibitors prevent cellular polyglutamine toxicity caused by the Huntington's disease mutation. J. Biol. Chem. 277, 33791-33798.
7. Chan, F. K., Shisler, J., Bixby, J. G., Felices, M., Zheng, L., Appel, M., Orenstein, J., Moss, B. and Lenardo, M. J. (2003). A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J. Biol. Chem. 278, 51613-51621.
8. Cho, Y. S., Challa, S., Moquin, D., Genga, R., Ray, T. D., Guildford, M. and Chan, F. K. (2009). Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137, 1112-1123.
9. Cuddeback, S. M., Yamaguchi, H., Komatsu, K., Miyashita, T., Yamada, M., Wu, C., Singh, S., Wang, H. G. (2001). Molecular cloning and characterization of Bif-1. A novel Src homology 3 domain-containing protein that associates with Bax. J. Biol. Chem. 276, 20559-20565.
10. Degenhardt, K., Mathew, R., Beaudoin, B., Bray, K., Anderson, D., Chen, G., Mukherjee, C., Shi, Y., Gélinas, C., Fan, Y. et al. (2006). Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10, 51-64.
11. Degterev, A., Huang, Z., Boyce, M., Li, Y., Jagtap, P., Mizushima, N., Cuny, G. D., Mitchison, T. J., Moskowitz, M. A. and Yuan, J. (2005). Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1, 112-119.
12. Etxebarria, A., Terrones, O., Yamaguchi, H., Landajuela, A., Landeta, O., Antonsson, B., Wang, H. G. and Basañez, G. (2009). Endophilin B1/Bif-1 stimulates BAX activation independently from its capacity to produce large scale membrane morphological rearrangements. J. Biol. Chem. 284, 4200-4212.
13. Forde, J. E. and Dale, T. C. (2007). Glycogen synthase kinase 3, a key regulator of cellular fate. Cell Mol. Life Sci. 64, 1930-1944.
14. Giusti, C., Luciani, M. F., Klein, G., Aubry, L., Tresse, E., Kosta, A. and Golstein, P. (2009). Necrotic cell death: From reversible mitochondrial uncoupling to irreversible lysosomal permeabilization. Exp. Cell Res. 315, 26-38.
15. Golstein, P. and Kroemer, G. (2007). Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 32, 37-43.
16. He, S., Wang, L., Miao, L., Wang, T., Du, F., Zhao, L. and Wang, X. (2009). Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137, 1100-1111.
17. Hitomi, J,., Christofferson, D. E., Ng, A., Yao, J., Degterev, A., Xavier, R. J. and Yuan, J. (2008). Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135, 1311-1323.
18. Hoeflich, K. P., Luo, J., Rubie, E. A., Tsao, M. S., Jin, O. and Woodgett, J. R. (2000). Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 406, 86-90.
19. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S., Bodmer, J. L., Schneider, P., Seed, B. and Tschopp, J. (2000). Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1, 489-495.
20. Hsu, Y. T. and Youle, R. J. (1997). Nonionic detergents induce dimerization among members of the Bcl-2 family. J. Biol. Chem. 272, 13829-13834.
21. Idziorek, T., Estaquier, J., De Bels, F. and Ameisen, J. C. (1995). YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. J. Immunol. Methods 185, 249-258.
22. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y. and Yoshimori. T. (2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO. J. 19, 5720-5728.
23. Klionsky, D. J. and Emr, S. D. (2000). Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721.
24. Klionsky, D. J., Abeliovich, H., Agostinis, P., Agrawal, D. K., Alievm. G., Askew, D. S., Baba, M., Baehrecke, E. H., Bahr, B. A., Ballabio, A. et al. (2008). Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175.
25. Kourtis, N. and Tavernarakis, N. (2009). Autophagy and cell death in model organisms. Cell Death Differ. 16, 21-30.
26. Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., El-Deiry, W. S., Golstein, P., Green, D. R. et al. (2009). Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16, 3-11.
27. Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T., Mizushima, N. (2004). The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036.
28. Liao, X., Tang, S., Thrasher, J. B., Griebling, T. L. and Li, B. (2005). Small-interfering RNA-induced androgen receptor silencing leads to apoptotic cell death in prostate cancer. Mol. Cancer Ther. 4, 505-515.
29. Maiuri, M. C., Zalckvar, E., Kimchi, A. and Kroemer, G. (2007). Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell. Biol. 8, 741-752.
30. Martinez, A., Alonso, M., Castro, A., Pérez, C. and Moreno, F. J. (2002). First non-ATP competitive glycogen synthase kinase 3 beta (GSK-3beta) inhibitors: thiadiazolidinones (TDZD) as potential drugs for the treatment of Alzheimer's disease. J. Med. Chem. 45, 1292-1299.
31. Mora, R. and Régnier-Vigouroux, A. (2009). Autophagy-driven cell fate decision maker: activated microglia induce specific death of glioma cells by a blockade of basal autophagic flux and secondary apoptosis/necrosis. Autophagy 5, 419-421.
32. Okada, M., Adachi, S., Imai, T., Watanabe, K., Toyokuni, S. Y., Ueno, M., Zervos, A. S., Kroemer, G. and Nakahata, T. (2004). A novel mechanism for imatinib mesylate-induced cell death of BCR-ABL-positive human leukemic cells: caspase-independent, necrosis-like programmed cell death mediated by serine protease activity. Blood 103, 2299-2307.
33. Pierrat, B., Simonen, M., Cueto, M., Mestan, J., Ferrigno, P. and Heim, J. (2001). SH3GLB, a new endophilin-related protein family featuring an SH3 domain. Genomics 71, 222-234.
34. Plotkin, B., Kaidanovich, O., Talior, I. and Eldar-Finkelman, H. (2003). Insulin mimetic action of synthetic phosphorylated peptide inhibitors of glycogen synthase kinase-3. J. Pharmacol. Exp. Ther. 305, 974-980.
35. Raymond, M. A., Mollica, L., Vigneault, N., Désormeaux, A., Chan, J. S., Filep, J. G. and Hébert, M. J. (2003). Blockade of the apoptotic machinery by cyclosporin A redirects cell death toward necrosis in arterial endothelial cells: regulation by reactive oxygen species and cathepsin D. FASEB J. 17, 515-517.
36. Samara, C., Syntichaki, P. and Tavernarakis, N. (2008). Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ. 15, 105-112.
37. Seglen, P. O. and Gordon, P. B. (1982). 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA 79, 1889-1892.
38. Smiley, S. T., Reers, M., Mottola-Hartshorn, C., Lin, M., Chen, A., Smith, T. W., Steele, G. D., Jr and Chen, L. B. (1991). Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA 88, 3671-3675.
39. Sun, A., Shanmugam, I., Song, J., Terranova, P. F., Thrasher, J. B. and Li, B. (2007). Lithium suppresses cell proliferation by interrupting E2F-DNA interaction and subsequently reducing S-phase gene expression in prostate cancer. Prostate 67, 976-988.
40. Takacs-Vellai, K., Vellai, T., Puoti, A., Passannante, M., Wicky, C., Streit, A., Kovacs, A. L. and Müller, F. (2005). Inactivation of the autophagy gene bec-1 triggers apoptotic cell death in C. elegans. Curr. Biol. 15, 1513-1517.
41. Takahashi, Y., Karbowski, M., Yamaguchi, H., Kazi, A., Wu, J., Sebti, S. M., Youle, R. J. and Wang, H. G. (2005). Loss of Bif-1 suppresses Bax/Bak conformational change and mitochondrial apoptosis. Mol. Cell. Biol. 25, 9369-9382.
42. Takahashi, Y., Coppola, D., Matsushita, N., Cualing, H. D., Sun, M., Sato, Y., Liang, C., Jung, J. U., Cheng, J. Q., Mul, J. J. et al. (2007). Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat. Cell Biol. 9, 1142-1151.
43. Takahashi, Y., Meyerkord, C. L. and Wang, H. G. (2009). Bif-1/Endophilin B1: a candidate for crescent driving force in autophagy. Cell Death Differ. 16, 947-955.
44. Thorburn, J., Horita, H., Redzic, J., Hansen, K., Frankel, A. E. and Thorburn, A. (2009). Autophagy regulates selective HMGB-1 release in tumor cells that are destined to die. Cell Death Differ. 16, 175-183.
45. Ullman, E., Fan, Y., Stawowczyk, M., Chen, H. M., Yue, Z. and Zong, W. X. (2008). Autophagy promotes necrosis in apoptosis-deficient cells in response to ER stress. Cell Death Differ. 15, 422-425.
46. Walker, N. I., Harmon, B. V., Gobé, G. C. and Kerr, J. F. (1988). Patterns of cell death. Methods Achiev. Exp. Pathol. 13, 18-54.
47. Wang, Y., Singh, R., Massey, A. C., Kane, S. S., Kaushik, S., Grant, T., Xiang, Y., Cuervo, A. M. and Czaja, M. J. (2008). Loss of macroautophagy promotes or prevents fibroblast apoptosis depending on the death stimulus. J. Biol. Chem. 283, 4766-4777.
48. Yamaguchi, H., Woods, N. T., Dorsey, J. F., Takahashi, Y., Gjertsen, N. R., Yeatman, T., Wu, J. and Wang, H. G. (2008). SRC directly phosphorylates Bif-1 and prevents its interaction with Bax and the initiation of anoikis. J. Biol. Chem. 283, 19112-19118.
49. Zhang, D. W., Shao, J., Lin, J., Zhang, N., Lu, B. J., Lin, S. C., Dong, M. Q. and Han, J. (2009). RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325, 332-336.
50. Zhong, Y., Wang, Q. J., Li, X., Yan, Y., Backer, J. M., Chait, B. T., Heintz, N. and Yue, Z. (2009). Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat. Cell Biol. 11, 468-476.
51. Zong, W. X. and Thompson, C. B. (2006). Necrotic death as a cell fate. Genes Dev. 20, 1-15.
52. Zong, W. X., Ditsworth, D., Bauer, D. E., Wang, Z. Q. and Thompson, C. B. (2004). Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 18, 1272-1282.