Bcl-2 complexed with Beclin-1 maintains full anti-apoptotic function

Oncogene

Volumn 28, Issue 21, 2009, Pages 2128-2141

  Ciechomska, I A ^a,b   Goemans, G C ^a,c   Skepper, J N ^a   Tolkovsky, A M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Apoptosis; Autophagy; Bcl 2; Beclin 1; Endoplasmic reticulum; Mitochondria

Indexed keywords

BECLIN 1; BH3 PROTEIN; CASPASE 3; CYCLOHEXIMIDE; PROTEIN BCL 2; STAUROSPORINE; THAPSIGARGIN; TUMOR NECROSIS FACTOR; TUNICAMYCIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CARCINOGENESIS; CELL DIFFERENTIATION; CELL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; ULTRAVIOLET RADIATION;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELLS, CULTURED; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SPACE; MEMBRANE PROTEINS; MICE; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 67349232611     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.60     Document Type: Article

References (53)

1. Adams JM, Cory S. (2007). The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26: 1324-1337.
2. Aita VM, Liang XH, Murty VV, Pincus DL, Yu W, Cayanis E et al. (1999). Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59: 59-65.
3. Akar U, Chaves-Reyez A, Barria M, Tari A, Sanguino A, Kondo Y et al. (2008). Silencing of Bcl-2 expression by small Interfering RNA induces autophagic cell death in MCF-7 breast cancer cells. Autophagy 4: 669-679.
4. Annis MG, Yethon JA, Leber B, Andrews DW. (2004). There is more to life and death than mitochondria: Bcl-2 proteins at the endoplasmic reticulum. Biochim Biophys Acta 1644: 115-123.
5. Arsov I, Li X, Matthews G, Coradin J, Hartmann B, Simon AK et al. (2008). BAC-mediated transgenic expression of fluorescent autophagic protein Beclin 1 reveals a role for Beclin 1 in lymphocyte development. Cell Death Differ 15: 1385-1395.
6. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N et al. (2005). Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25: 1025-1040.
7. Cao Y, Klionsky DJ. (2007). Physiological functions of Atg6/ Beclin 1: a unique autophagy-related protein. Cell Res 17: 839-849.
8. Certo M, Del Gaizo Moore V, Nishino M, Wei G, Korsmeyer S, Armstrong SA et al. (2006). Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9: 351-365.
9. Chu CT, Zhu J, Dagda R. (2007). Beclin 1-independent pathway of damage-induced mitophagy and autophagic stress: implications for neurodegeneration and cell death. Autophagy 3: 663-666.
10. Ciechomska IA, Goemans CG, Tolkovsky AM. (2008). Molecular links between autophagy and apoptosis. Methods Mol Biol 445: 175-193.
11. Erlich S, Mizrachy L, Segev O, Lindenboim L, Zmira O, Adi-Harel S et al. (2007). Differential interactions between Beclin 1 and Bcl-2 family members. Autophagy 3: 561-568.
12. Feng W, Huang S, Wu H, Zhang M. (2007). Molecular basis of Bcl-xL's target recognition versatility revealed by the structure of Bcl-xL in complex with the BH3 domain of Beclin-1. J Mol Biol 372: 223-235.
13. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R et al. (2007). Ambra1 regulates autophagy and development of the nervous system. Nature 447: 1121-1125.
14. Furuya N, Yu J, Byfield M, Pattingre S, Levine B. (2005). The evolutionarily conserved domain of Beclin 1 is required for Vps34 binding, autophagy and tumor suppressor function. Autophagy 1: 46-52.
15. Goemans CG, Boya P, Skirrow CJ, Tolkovsky AM. (2008). Intramitochondrial degradation of Tim23 curtails the survival of cells rescued from apoptosis by caspase inhibitors. Cell Death Differ 15: 545-554.
16. Hacki J, Egger L, Monney L, Conus S, Rosse T, Fellay I et al. (2000). Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene 19: 2286-2295.
17. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R et al. (2006). Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441: 885-889.
18. Jin S, White E. (2007). Role of autophagy in cancer: management of metabolic stress. Autophagy 3: 28-31.
19. Jin S, White E. (2008). Tumor suppression by autophagy through the management of metabolic stress. Autophagy 4: 563-566.
20. Karantza-Wadsworth V, Patel S, Kravchuk O, Chen G, Mathew R, Jin S et al. (2007). Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 21: 1621-1635.
21. Kaufmann T, Schlipf S, Sanz J, Neubert K, Stein R, Borner C. (2003). Characterization of the signal that directs Bcl-x(L), but not Bcl-2, to the mitochondrial outer membrane. J Cell Biol 160: 53-64.
22. Klionsky DJ. (2007). Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8: 931-937.
23. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S et al. (2008). Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172: 454-469.
24. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I et al. (2006). Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441: 880-884.
25. Ku B, Woo JS, Liang C, Lee KH, Hong HS, E X et al. (2008). Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog 4: e25.
26. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T et al. (2004). The role of autophagy during the early neonatal starvation period. Nature 432: 1032-1036.
27. Levine B, Sinha S, Kroemer G. (2008). Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 4: 1-7.
28. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH et al. (2006). Autophagic and tumour suppressor activity of a novel Beclin1binding protein UVRAG. Nat Cell Biol 8: 688-699.
29. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H et al. (1999). Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402: 672-676.
30. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G et al. (1998). Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 72: 8586-8596.
31. Maiuri MC, Criollo A, Tasdemir E, Vicencio JM, Tajeddine N, Hickman JA et al. (2007a). BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 3: 374-376.
32. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P et al. (2007b). Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 26: 2527-2539.
33. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. (2007c). Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8: 741-752.
34. Meijer AJ, Codogno P. (2004). Regulation and role of autophagy in mammalian cells. Int J Biochem Cell Biol 36: 2445-2462.
35. Michaelidis TM, Sendtner M, Cooper JD, Airaksinen MS, Holtmann B, Meyer M et al. (1996). Inactivation of Bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development. Neuron 17: 75-89.
36. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. (2008). Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075.
37. Mizushima N, Ohsumi Y, Yoshimori T. (2002). Autophagosome formation in mammalian cells. Cell Struct Funct 27: 421-429.
38. Noble CG, Dong JM, Manser E, Song H. (2008). BCL-XL and UVRAG cause a monomer-dimer switch in beclin1. J Biol Chem 283: 26274-26282.
39. Oberstein A, Jeffrey PD, Shi Y. (2007). Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem 282: 13123-13132.
40. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N et al. (2005). Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939.
41. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A et al. (2003). Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112: 1809-1820.
42. Ravikumar B, Berger Z, Vacher C, O'Kane CJ, Rubinsztein DC. (2006). Rapamycin pre-treatment protects against apoptosis. Hum Mol Genet 15: 1209-1216.
43. Samara C, Syntichaki P, Tavernarakis N. (2008). Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 15: 105-112.
44. Scarlatti F, Maffei R, Beau I, Codogno P, Ghidoni R. (2008). Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ 15: 1318-1329.
45. Scorrano L, Korsmeyer SJ. (2003). Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem Biophys Res Commun 304: 437-444.
46. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB et al. (2004). Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6: 1221-1228.
47. Sinha S, Colbert CL, Becker N, Wei Y, Levine B. (2008). Molecular basis of the regulation of Beclin 1-dependent autophagy by the gamma-herpesvirus 68 Bcl-2 homolog M11. Autophagy 4: 989-997.
48. Skepper JN. (2000). Immunocytochemical strategies for electron microscopy: choice or compromise. J Microsc 199: 1-36.
49. Swerdlow S, McColl K, Rong Y, Lam M, Gupta A, Distelhorst CW. (2008). Apoptosis inhibition by Bcl-2 gives way to autophagy in glucocorticoid-treated lymphocytes. Autophagy 4: 612-620.
50. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y et al. (2007). Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 9: 1142-1151.
51. Ullman E, Fan Y, Stawowczyk M, Chen HM, Yue Z, Zong WX. (2008). Autophagy promotes necrosis in apoptosis-deficient cells in response to ER stress. Cell Death Differ 15: 422-425.
52. Yoshimori T. (2004). Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Commun 313: 453-458.
53. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. (2003). Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA 100: 15077-15082.