Viewing BCL2 and cell death control from an evolutionary perspective

Cell Death and Differentiation

Volumn 25, Issue 1, 2018, Pages 13-20

  Strasser, Andreas ^a,b   Vaux, David L ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN MCL 1;

APOPTOSIS; CAENORHABDITIS ELEGANS; CARCINOGENESIS; CELL COUNT; CELL DEATH; CELL SURVIVAL; HOMEOSTASIS; HUMAN; INFLAMMATION; MITOSIS; MORPHOGENESIS; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; EVOLUTION; GENETICS; NEOPLASM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; APOPTOSIS; BIOLOGICAL EVOLUTION; CAENORHABDITIS ELEGANS; HUMANS; INFLAMMATION; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; STRESS, PHYSIOLOGICAL;

EID: 85047139231     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2017.145     Document Type: Review

References (79)

1. Fukuhara S, Rowley JD. Chromosome 14 translocations in non-Burkitt lymphomas. Int J Cancer 1978; 22: 14-21.
2. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 1984; 226: 1097-1099.
3. Tsujimoto Y, Jaffe E, Cossman J, Gorham J, Nowell PC, Croce CM. Clustering of breakpoints on chromosome 11 in human B-cell neoplasms with the t(11;14) chromosome translocation. Nature 1985; 315: 340-343.
4. Cleary ML, Smith SD, Sklar J. Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t(14;18) translocation. Cell 1986; 47: 19-28.
5. Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 1988; 335: 440-442.
6. Cook WD, Metcalf D, Nicola NA, Burgess AW, Walker F. Malignant transformation of a growth factor-dependent myeloid cell line by Abelson virus without evidence of an autocrine mechanism. Cell 1985; 41: 677-683.
7. Strasser A, Harris AW, Bath ML, Cory S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 1990; 348: 331-333.
8. Strasser A, Harris AW, Vaux DL, Webb E, Bath ML, Adams JM et al. Abnormalities of the immune system induced by dysregulated bcl-2 expression in transgenic mice. Curr Top Microbiol Immunol 1990; 166: 175-181.
9. Strasser A, Harris AW, Cory S. E mu-bcl-2 transgene facilitates spontaneous transformation of early pre-B and immunoglobulin-secreting cells but not T cells. Oncogene 1993; 8: 1-9.
10. Vandenberg CJ, Waring P, Strasser A, Cory S. Plasmacytomagenesis in Emu-v-abl transgenic mice is accelerated when apoptosis is restrained. Blood 2014; 124: 1099-1109.
11. Kerr JF, Wyllie AH, Currie AR. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239-257.
12. Ellis RE, Yuan JY, Horvitz HR. Mechanisms and functions of cell death. Annu Rev Cell Biol 1991; 7: 663-698.
13. Vaux DL, Weissman IL, Kim SK. Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 1992; 258: 1955-1957.
14. Yuan JY, Shaham S, Ledoux S, Ellis HM, Horvitz HR. The C. elegans cell death gene ced 3 encodes a protein similar to mammalian interleukin 1 beta converting enzyme. Cell 1993; 75: 641-652.
15. Hengartner MO, Horvitz HR. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 1994; 76: 665-676.
16. Hengartner MO, Ellis RE, Horvitz HR. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 1992; 356: 494-499.
17. Cerretti DP, Kozlosky CJ, Mosley B, Nelson N, Van NK, Greenstreet TA et al. Molecular cloning of the interleukin-1 beta converting enzyme. Science 1992; 256: 97-100.
18. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 1992; 356: 768-774.
19. Yuan J, Horvitz HR. The Caenorhabditis elegans cell death gene ced-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 1992; 116: 309-320.
20. Zou H, Henzel WJ, Liu XS, Lutschg A, Wang XD. Apaf-1, a human protein homologous to c-elegans ced-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997; 90: 405-413.
21. Strasser A, O'Connor L, Dixit VM. Apoptosis signaling. Annu Rev Biochem 2000; 69: 217-245.
22. Jabbour AM, Puryer MA, Yu JY, Lithgow T, Riffkin CD, Ashley DM et al. Human Bcl-2 cannot directly inhibit the Caenorhabditis elegans Apaf-1 homologue CED-4, but can interact with EGL-1. J Cell Sci 2006; 119(Pt 12): 2572-2582.
23. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74: 609-619.
24. Wei MC, Zong WX, Cheng EHY, Lindsten T, Panoutsakopoulou V, Ross AJ et al. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-730.
25. Kalkavan H, Green DR. MOMP, cell suicide as a BCL-2 family business. Cell death Diff 2018; 25: 46-55.
26. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES et al. Cytochrome c and datp-dependent formation of apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997; 91: 479-489.
27. Marsden VS, O'Connor L, O'Reilly LA, Silke J, Metcalf D, Ekert PG et al. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature 2002; 419: 634-637.
28. Ekert PG, Read SH, Silke J, Marsden VS, Kaufmann H, Hawkins CJ et al. Apaf-1 and caspase-9 accelerate apoptosis, but do not determine whether factor-deprived or drugtreated cells die. J Cell Biol 2004; 165: 835-842.
29. White MJ, McArthur K, Metcalf D, Lane RM, Cambier JC, Herold MJ et al. Apoptotic caspases suppress mtDNA-induced STING-mediated type I IFN production. Cell 2014; 159: 1549-1562.
30. Metzstein MM, Stanfield GM, Horvitz HR. Genetics of programmed cell death in C. elegans -past, present and future. Trends Genet 1998; 14: 410-416.
31. Huang DCS, Strasser A. BH3-Only proteins - essential initiators of apoptotic cell death. Cell 2000; 103: 839-842.
32. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Cory S et al. Bim: A novel member of the Bcl-2 family that promotes apoptosis. EMBO J 1998; 17: 384-395.
33. Bouillet P, Metcalf D, Huang DCS, Tarlinton DM, Kay TWH, Kontgen F et al. Proapoptotic Bcl-2 relative bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 1999; 286: 1735-1738.
34. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001; 7: 683-694.
35. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 2001; 7: 673-682.
36. Villunger A, Michalak EM, Coultas L, Mullauer F, Bock G, Ausserlechner MJ et al. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003; 302: 1036-1038.
37. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M et al. tBID, a membranetargeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 2000; 14: 2060-2071.
38. Conradt B, Horvitz HR. The c-elegans protein egl-1 is required for programmed cell death and interacts with the bcl-2-like protein ced-9. Cell 1998; 93: 519-529.
39. O'Neill KL, Huang K, Zhang J, Chen Y, Luo X. Inactivation of prosurvival Bcl-2 proteins activates Bax/Bak through the outer mitochondrial membrane. Genes Dev 2016; 30: 973-988.
40. Merino D, Giam M, Hughes PD, Siggs OM, Heger K, O'Reilly LA et al. The role of BH3-only protein Bim extends beyond inhibiting Bcl-2-like prosurvival proteins. J Cell Biol 2009; 186: 355-362.
41. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCormick LL et al. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 2011; 44: 517-531.
42. Chou JJ, Li HL, Salvesen GS, Yuan JY, Wagner G. Solution structure of BID, an intracellular amplifier of apoptotic signaling. Cell 1999; 96: 615-624.
43. Li HL, Zhu H, Xu CJ, Yuan JY. Cleavage of bid by caspase 8 mediates the mitochondrial damage in the fas pathway of apoptosis. Cell 1998; 94: 491-501.
44. Luo X, Budihardjo I, Zou H, Slaughter C, Wang XD. Bid, a bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998; 94: 481-490.
45. Ke F, Voss A, Kerr JB, O'Reilly LA, Tai L, Echeverry N et al. BCL-2 family member BOK is widely expressed but its loss has only minimal impact in mice. Cell Death Differ 2012; 19: 915-925.
46. Ke F, Grabow S, Kelly GL, Lin A, O'Reilly LA, Strasser A. Impact of the combined loss of BOK, BAX and BAK on the hematopoietic system is slightly more severe than compound loss of BAX and BAK. Cell Death Dis 2015; 6: E1938.
47. Llambi F, Wang YM, Victor B, Yang M, Schneider DM, Gingras S et al. BOK is a noncanonical BCL-2 family effector of apoptosis regulated by ER-associated degradation. Cell 2016; 165: 421-433.
48. Antonsson B, Conti F, Ciavatta A, Montessuit S, Lewis S, Martinou I et al. Inhibition of bax channel-forming activity by bcl-2. Science 1997; 277: 370-372.
49. Czabotar PE, Westphal D, Dewson G, Ma S, Hockings C, Fairlie WD et al. Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell 2013; 152: 519-531.
50. Wiens M, Krasko A, Muller CI, Muller WE. Molecular evolution of apoptotic pathways: Cloning of key domains from sponges (Bcl-2 homology domains and death domains) and their phylogenetic relationships. J Mol Evol 2000; 50: 520-531.
51. Degterev A, Yuan J. Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 2008; 9: 378-390.
52. Vaux DL, Haecker G, Strasser A. An evolutionary perspective on apoptosis. Cell 1994; 76: 777-779.
53. Vaux DL, Hacker G. Hypothesis: Apoptosis caused by cytotoxins represents a defensive response that evolved to combat intracellular pathogens. Clin Exp Pharmacol Physiol 1995; 22: 861-863.
54. Kayagaki N, Warming S, Lamkanfi M, Vande Walle L, Louie S, Dong J et al. Non-canonical inflammasome activation targets caspase-11. Nature 2011; 479: 117-121.
55. Ray CA, Black RA, Kronheim SR, Greenstreet TA, Sleath PR, Salvesen GS et al. Viral inhibition of inflammation: Cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell 1992; 69: 597-604.
56. Beidler DR, Tewari M, Friesen PD, Poirier G, Dixit VM. The baculovirus p35 protein inhibits Fas- and tumor necrosis factor-induced apoptosis. J Biol Chem 1995; 270: 16526-16528.
57. Tschopp J, Thome M, Hofmann K, Meinl E. The fight of viruses against apoptosis. Curr Opin Genet Dev 1998; 8: 82-87.
58. Upton JW, Kaiser WJ, Mocarski ES. Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 2010; 7: 302-313.
59. Vucic D, Kaiser WJ, Miller LK. Inhibitor of apoptosis proteins physically interact with and block apoptosis induced by drosophila proteins hid and grim. Mol Cell Biol 1998; 18: 3300-3309.
60. Trapani JA, Sutton VR, Granzyme B. pro-apoptotic, antiviral and antitumor functions. Curr Opin Immunol 2003; 15: 533-543.
61. Strasser A, Harris AW, Cory S. bcl-2 transgene inhibits T cell death and perturbs thymic selfcensorship. Cell 1991; 67: 889-999.
62. Vaux DL, Aguila HL, Weissman IL. Bcl-2 prevents death of factor-deprived cells but fails to prevent apoptosis in targets of cell mediated killing. Int Immunol 1992; 4: 821-824.
63. Strasser A, Harris AW, Huang DC, Krammer PH, Cory S. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J 1995; 14: 6136-6147.
64. Newton K, Harris AW, Bath ML, Smith KG, Strasser A. A dominant interfering mutant of FADD/MORT1 enhances deletion of autoreactive thymocytes and inhibits proliferation of mature T lymphocytes. EMBO J 1998; 17: 706-718.
65. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ et al. Two cd95 (apo-1/fas) signaling pathways. EMBO J 1998; 17: 1675-1687.
66. Jost PJ, Grabow S, Gray D, McKenzie MD, Nachbur U, Huang DC et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 2009; 460: 1035-1039.
67. Strasser A, Jost PJ, Nagata S. The many roles of FAS receptor signaling in the immune system. Immunity 2009; 30: 180-192.
68. Lowin B, Hahne M, Mattmann C, Tschopp J. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 1994; 370: 650-652.
69. Kagi D, Vignaux F, Ledermann B, Burki K, Depraetere V, Nagata S et al. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994; 265: 528-530.
70. Vaux DL, Strasser A. The molecular biology of apoptosis. Proc Natl Acad Sci USA 1996; 93: 2239-2244.
71. Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, Cory S et al. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci USA 1991; 88: 8661-8665.
72. Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K, Warming S et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 2015; 526: 666-671.
73. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 2015; 526: 660-665.
74. Rongvaux A, Jackson R, Harman CC, Li T, West AP, de Zoete MR et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell 2014; 159: 1563-1577.
75. Kultz D. Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 2005; 67: 225-257.
76. Tsujimoto Y. Stress-resistance conferred by high level of bcl-2 alpha protein in human B lymphoblastoid cell. Oncogene 1989; 4: 1331-1336.
77. Roberts AW, Davids MS, Pagel JM, Kahl BS, Puvvada SD, Gerecitano JF et al. Targeting BCL2 with venetoclax in relapsed chronic lymphocytic leukemia. N Engl J Med 2016; 374: 311-322.
78. Souers AJ, Leverson JD, Boghaert ER, Ackler SL, Catron ND, Chen J et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat Med 2013; 19: 202-208.
79. Kotschy A, Szlavik Z, Murray J, Davidson J, Maragno AL, Le Toumelin-Braizat G et al. The MCL1 inhibitor S63845 is tolerable and effective in diverse cancer models. Nature 2016; 538: 477-482.