Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis

FEBS Journal

Volumn 278, Issue 3, 2011, Pages 403-413

  Zhou, Feifan ^a   Yang, Ying ^a   Xing, Da ^a  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

Author keywords

apoptosis; autophagy; Bcl 2; Bcl xL; Beclin 1

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; AUTOPHAGY PROTEIN 5; BECLIN 1; BH3 PROTEIN; CALCIUM ION; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CALCIUM CELL LEVEL; CELLULAR DISTRIBUTION; HUMAN; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BCL-X PROTEIN; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; PROTO-ONCOGENE PROTEINS C-BCL-2;

MAMMALIA;

EID: 78751655392     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07965.x     Document Type: Article

References (87)

1. Hahn WC, &, Weinberg RA, (2002) Rules for making human tumor cells. N Engl J Med 347, 1593-1603.
2. Sasi N, Hwang M, Jaboin J, Csiki I, &, Lu B, (2009) Regulated cell death pathways: new twists in modulation of BCL2 family function. Mol Cancer Ther 8, 1421-1429.
3. Walensky LD, (2006) BCL-2 in the crosshairs: tipping the balance of life and death. Cell Death Differ 13, 1339-1350.
4. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, &, Levine B, (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939.
5. Uchiyama Y, Shibata M, Koike M, Yoshimura K, &, Sasaki M, (2008) Autophagy-physiology and pathophysiology. Histochem Cell Biol 129, 407-420.
6. Yip KW, &, Reed JC, (2008) Bcl-2 family proteins and cancer. Oncogene 27, 6398-6406.
7. Danial NN, &, Korsmeyer SJ, (2004) Cell death: critical control points. Cell 116, 205-219.
8. Levine B, &, Klionsky DJ, (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6, 463-477.
9. Mizushima N, &, Klionsky DJ, (2007) Protein turnover via autophagy: implications for metabolism. Annu Rev Nutr 27, 19-40. (Pubitemid 351373346)
10. Eisenberg-Lerner A, Bialik S, Simon HU, &, Kimchi A, (2009) Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 16, 966-975.
11. Yang Y, Xing D, Zhou F, &, Chen Q, (2010) Mitochondrial autophagy protects against heat shock-induced apoptosis through reducing cytosolic cytochrome c release and downstream caspase-3 activation. Biochem Biophys Res Commun 395, 190-195.
12. Zhuang W, Qin Z, &, Liang Z, (2009) The role of autophagy in sensitizing malignant glioma cells to radiation therapy. Acta Biochim Biophys Sin (Shanghai) 41, 341-351.
13. White E, &, DiPaola RS, (2009) The double-edged sword of autophagy modulation in cancer. Clin Cancer Res 15, 5308-5316.
14. Dikic I, Johansen T, &, Kirkin V, (2010) Selective autophagy in cancer development and therapy. Cancer Res 70, 3431-3434.
15. Luo S, &, Rubinsztein DC, (2007) Atg5 and Bcl-2 provide novel insights into the interplay between apoptosis and autophagy. Cell Death Differ 14, 1247-1250.
16. Swerdlow S, &, Distelhorst CW, (2007) Bcl-2-regulated calcium signals as common mediators of both apoptosis and autophagy. Dev Cell 12, 178-179.
17. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, &, Simon HU, (2006) Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 8, 1124-1132.
18. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, et al. (2007) Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 25, 193-205.
19. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, &, Croce CM, (1984) Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226, 1097-1099. (Pubitemid 15217831)
20. Oltvai ZN, Milliman CL, &, Korsmeyer SJ, (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609-619.
21. Szegezdi E, Macdonald DC, Ni Chonghaile T, Gupta S, &, Samali A, (2009) Bcl-2 family on guard at the ER. Am J Physiol Cell Physiol 296, C941-C953.
22. Reed JC, (2006) Proapoptotic multidomain Bcl-2/Bax-family proteins: mechanisms, physiological roles, and therapeutic opportunities. Cell Death Differ 13, 1378-1386.
23. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, &, Korsmeyer SJ, (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730.
24. Antonsson B, Montessuit S, Lauper S, Eskes R, &, Martinou JC, (2000) Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 345, 271-278.
25. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, &, Youle RJ, (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139, 1281-1292.
26. Finucane DM, Bossy-Wetzel E, Waterhouse NJ, Cotter TG, &, Green DR, (1999) Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J Biol Chem 274, 2225-2233.
27. Green DR, &, Reed JC, (1998) Mitochondria and apoptosis. Science 281, 1309-1312.
28. Gross A, McDonnell JM, &, Korsmeyer SJ, (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13, 1899-1911.
29. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams JM, &, Huang DC, (2005) Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19, 1294-1305.
30. Cohen-Saidon C, Carmi I, Keren A, &, Razin E, (2006) Antiapoptotic function of Bcl-2 in mast cells is dependent on its association with heat shock protein 90beta. Blood 107, 1413-1420.
31. Kuo CC, Liang CM, Lai CY, &, Liang SM, (2007) Involvement of heat shock protein (Hsp)90 beta but not Hsp90 alpha in antiapoptotic effect of CpG-B oligodeoxynucleotide. J Immunol 178, 6100-6108.
32. Chen J, Flannery JG, LaVail MM, Steinberg RH, Xu J, &, Simon MI, (1996) bcl-2 overexpression reduces apoptotic photoreceptor cell death in three different retinal degenerations. Proc Natl Acad Sci USA 93, 7042-7047. (Pubitemid 26243498)
33. Cheng EH, Kirsch DG, Clem RJ, Ravi R, Kastan MB, Bedi A, Ueno K, &, Hardwick JM, (1997) Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278, 1966-1968.
34. Lin B, Kolluri SK, Lin F, Liu W, Han YH, Cao X, Dawson MI, Reed JC, &, Zhang XK, (2004) Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 116, 527-540.
35. Bivona TG, Quatela SE, Bodemann BO, Ahearn IM, Soskis MJ, Mor A, Miura J, Wiener HH, Wright L, Saba SG, et al. (2006) PKC regulates a farnesyl-electrostatic switch on K-Ras that promotes its association with Bcl-XL on mitochondria and induces apoptosis. Mol Cell 21, 481-493.
36. Schwartz PS, Manion MK, Emerson CB, Fry JS, Schulz CM, Sweet IR, &, Hockenbery DM, (2007) 2-Methoxy antimycin reveals a unique mechanism for Bcl-x(L) inhibition. Mol Cancer Ther 6, 2073-2080.
37. Silvestrini R, Veneroni S, Daidone MG, Benini E, Boracchi P, Mezzetti M, Di Fronzo G, Rilke F, &, Veronesi U, (1994) The Bcl-2 protein: a prognostic indicator strongly related to p53 protein in lymph node-negative breast cancer patients. J Natl Cancer Inst 86, 499-504.
38. Levine B, &, Deretic V, (2007) Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 7, 767-777.
39. Gustafsson AB, &, Gottlieb RA, (2009) Autophagy in ischemic heart disease. Circ Res 104, 150-158.
40. Pattingre S, Espert L, Biard-Piechaczyk M, &, Codogno P, (2008) Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 90, 313-323.
41. Ravikumar B, Futter M, Jahreiss L, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Narayanan U, Renna M, et al. (2009) Mammalian macroautophagy at a glance. J Cell Sci 122, 1707-1711.
42. Paglin S, Lee NY, Nakar C, Fitzgerald M, Plotkin J, Deuel B, Hackett N, McMahill M, Sphicas E, Lampen N, et al. (2005) Rapamycin-sensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells. Cancer Res 65, 11061-11070.
43. Takeuchi H, Kondo Y, Fujiwara K, Kanzawa T, Aoki H, Mills GB, &, Kondo S, (2005) Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res 65, 3336-3346.
44. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, &, Levine B, (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676.
45. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, et al. (2007) Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 26, 2527-2539.
46. Maiuri MC, Zalckvar E, Kimchi A, &, Kroemer G, (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8, 741-752.
47. Topisirovic I, &, Sonenberg N, (2010) Cell biology Burn out or fade away? Science 327, 1210-1211.
48. Takahasi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, Liang C, Jung JU, Cheng JC, Mul JJ, et al. (2007) Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 9, 1142-1151.
49. 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.
50. Altman BJ, Wofford JA, Zhao Y, Coloff JL, Ferguson EC, Wieman HL, Day AE, Ilkayeva O, &, Rathmell JC, (2009) Autophagy provides nutrients but can lead to Chop-dependent induction of Bim to sensitize growth factor-deprived cells to apoptosis. Mol Biol Cell 20, 1180-1191.
51. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gelinas C, Fan Y, et al. (2006) Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10, 51-64.
52. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB, &, Tsujimoto Y, (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6, 1221-1228.
53. Zhang H, Kong X, Kang J, Su J, Li Y, Zhong J, &, Sun L, (2009) Oxidative stress induces parallel autophagy and mitochondria dysfunction in human glioma U251 cells. Toxicol Sci 110, 376-388.
54. Kihara A, Noda T, Ishihara N, &, Ohsumi Y, (2001) Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 152, 519-530.
55. Aziz MH, Nihal M, Fu VX, Jarrard DF, &, Ahmad N, (2006) Resveratrol-caused apoptosis of human prostate carcinoma LNCaP cells is mediated via modulation of phosphatidylinositol 3′-kinase/Akt pathway and Bcl-2 family proteins. Mol Cancer Ther 5, 1335-1341.
56. Fresno Vara JA, Casado E, de Castro J, Cejas P, Belda-Iniesta C, &, Gonzalez-Baron M, (2004) PI3K/Akt signalling pathway and cancer. Cancer Treat Rev 30, 193-204.
57. Tanaka S, Saito K, &, Reed JC, (1993) Structure-function analysis of the Bcl-2 oncoprotein. Addition of a heterologous transmembrane domain to portions of the Bcl-2 beta protein restores function as a regulator of cell survival. J Biol Chem 268, 10920-10926.
58. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, &, Korsmeyer SJ, (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301, 513-517.
59. Griffiths GJ, Dubrez L, Morgan CP, Jones NA, Whitehouse J, Corfe BM, Dive C, &, Hickman JA, (1999) Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J Cell Biol 144, 903-914.
60. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, &, Korsmeyer SJ, (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14, 2060-2071.
61. Suzuki M, Youle RJ, &, Tjandra N, (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103, 645-654.
62. Kang MH, &, Reynolds CP, (2009) Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res 15, 1126-1132.
63. Kim KW, Mutter RW, Cao C, Albert JM, Freeman M, Hallahan DE, &, Lu B, (2006) Autophagy for cancer therapy through inhibition of pro-apoptotic proteins and mammalian target of rapamycin signaling. J Biol Chem 281, 36883-36890. (Pubitemid 46042156)
64. Pattingre S, Bauvy C, Carpentier S, Levade T, Levine B, &, Codogno P, (2009) Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy. J Biol Chem 284, 2719-2728.
65. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, &, Yoshimori T, (2001) Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 152, 657-668.
66. Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, Natsume T, Ohsumi Y, &, Yoshimori T, (2003) Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 116, 1679-1688.
67. Mathiasen IS, Sergeev IN, Bastholm L, Elling F, Norman AW, &, Jaattela M, (2002) Calcium and calpain as key mediators of apoptosis-like death induced by vitamin D compounds in breast cancer cells. J Biol Chem 277, 30738-30745.
68. Vanden Abeele F, Skryma R, Shuba Y, Van Coppenolle F, Slomianny C, Roudbaraki M, Mauroy B, Wuytack F, &, Prevarskaya N, (2002) Bcl-2-dependent modulation of Ca(2+) homeostasis and store-operated channels in prostate cancer cells. Cancer Cell 1, 169-179.
69. Foyouzi-Youssefi R, Arnaudeau S, Borner C, Kelley WL, Tschopp J, Lew DP, Demaurex N, &, Krause KH, (2000) Bcl-2 decreases the free Ca2+ concentration within the endoplasmic reticulum. Proc Natl Acad Sci USA 97, 5723-5728.
70. Pinton P, Ferrari D, Magalhaes P, Schulze-Osthoff K, Di Virgilio F, Pozzan T, &, Rizzuto R, (2000) Reduced loading of intracellular Ca(2+) stores and downregulation of capacitative Ca(2+) influx in Bcl-2-overexpressing cells. J Cell Biol 148, 857-862.
71. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong SL, et al. (1996) X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381, 335-341.
72. Minn AJ, Velez P, Schendel SL, Liang H, Muchmore SW, Fesik SW, Fill M, &, Thompson CB, (1997) Bcl-x(L) forms an ion channel in synthetic lipid membranes. Nature 385, 353-357.
73. Schendel SL, Xie Z, Montal MO, Matsuyama S, Montal M, &, Reed JC, (1997) Channel formation by antiapoptotic protein Bcl-2. Proc Natl Acad Sci USA 94, 5113-5118. (Pubitemid 27214745)
74. Schlesinger PH, Gross A, Yin XM, Yamamoto K, Saito M, Waksman G, &, Korsmeyer SJ, (1997) Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc Natl Acad Sci USA 94, 11357-11362.
75. Orrenius S, Zhivotovsky B, &, Nicotera P, (2003) Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4, 552-565.
76. Wei Y, Pattingre S, Sinha S, Bassik M, &, Levine B, (2008) JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 30, 678-688.
77. Ham YM, Chun KH, Choi JS, Kim DH, &, Lee SK, (2003) SEK1-dependent JNK1 activation prolongs cell survival during G-Rh2-induced apoptosis. Biochem Biophys Res Commun 304, 358-364.
78. Wei Y, Sinha S, &, Levine B, (2008) Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4, 949-951.
79. Levine B, Sinha S, &, Kroemer G, (2008) Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 4, 600-606.
80. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, Willis SN, Scott CL, Day CL, Cory S, et al. (2006) The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10, 389-399.
81. Maiuri MC, Criollo A, Tasdemir E, Vicencio JM, Tajeddine N, Hickman JA, Geneste O, &, Kroemer G, (2007) 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.
82. Perkins G, Bossy-Wetzel E, &, Ellisman MH, (2009) New insights into mitochondrial structure during cell death. Exp Neurol 218, 183-192.
83. Boya P, &, Kroemer G, (2009) Beclin 1: a BH3-only protein that fails to induce apoptosis. Oncogene 28, 2125-2127.
84. Ciechomska IA, Goemans GC, Skepper JN, &, Tolkovsky AM, (2009) Bcl-2 complexed with Beclin-1 maintains full anti-apoptotic function. Oncogene 28, 2128-2141.
85. Yee KS, Wilkinson S, James J, Ryan KM, &, Vousden KH, (2009) PUMA- and Bax-induced autophagy contributes to apoptosis. Cell Death Differ 16, 1135-1145.
86. Abedin MJ, Wang D, McDonnell MA, Lehmann U, &, Kelekar A, (2007) Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ 14, 500-510.
87. Kim I, Rodriguez-Enriquez S, &, Lemasters JJ, (2007) Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462, 245-253.