Anti-apoptotic BCL-2 family members in development

Cell Death and Differentiation

Volumn 25, Issue 1, 2018, Pages 37-45

  Opferman, Joseph T ^a   Kothari, Anisha ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCL2 RELATED PROTEIN A1; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN MCL 1; APOPTOSIS REGULATORY PROTEIN;

APOPTOSIS; BONE MARROW CELL; CELL DEATH; CELL SURVIVAL; DEVELOPMENT; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; ERYTHROCYTE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; LYMPHOCYTE; MEGAKARYOCYTE; MELANOCYTE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; THROMBOCYTE; ANIMAL; EMBRYOLOGY; MOUSE; NERVOUS SYSTEM; PHYSIOLOGY;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; EMBRYONIC DEVELOPMENT; HEMATOPOIESIS; MICE; NERVOUS SYSTEM; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 85040948881     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2017.170     Document Type: Review

References (85)

1. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Mol Cell 2010; 37: 299-310.
2. Krajewski S, Tanaka S, Takayama S, Schibler MJ, Fenton W, Reed JC. Investigation of the subcellular distribution of the bcl-2 oncoprotein: Residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res 1993; 53: 4701-4714.
3. Fabian D, Koppel J, Maddox-Hyttel P. Apoptotic processes during mammalian preimplantation development. Theriogenology 2005; 64: 221-231.
4. Hardy K. Cell death in the mammalian blastocyst. Mol Hum Reprod 1997; 3: 919-925.
5. Hardy K. Apoptosis in the human embryo. Rev Reprod 1999; 4: 125-134.
6. Boumela I, Assou S, Haouzi D, Dechaud H, Ait-Ahmed O, Hamamah S. Developmental regulated expression of anti- and pro-apoptotic BCL-2 family genes during human early embryonic development. Curr Med Chem 2014; 21: 1361-1369.
7. Russell HR, Lee Y, Miller HL, Zhao J, McKinnon PJ. Murine ovarian development is not affected by inactivation of the bcl-2 family member diva. Mol Cell Biol 2002; 22: 6866-6870.
8. Rinkenberger JL, Horning S, Klocke B, Roth K, Korsmeyer SJ. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev 2000; 14: 23-27.
9. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Negishi I et al. Massive cell death of immature hematopoietic cells and neurons in Bcl-x- deficient mice. Science 1995; 267: 1506-1510.
10. Metcalfe AD, Hunter HR, Bloor DJ, Lieberman BA, Picton HM, Leese HJ et al. Expression of 11 members of the BCL-2 family of apoptosis regulatory molecules during human preimplantation embryo development and fragmentation. Mol Reprod Dev 2004; 68: 35-50.
11. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 1993; 75: 229-240.
12. Nakayama K, Nakayama K, Negishi I, Kuida K, Sawa H, Loh DY. Targeted disruption of Bcl-2 alpha beta in mice: Occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc Natl Acad Sci USA 1994; 91: 3700-3704.
13. Kamada S, Shimono A, Shinto Y, Tsujimura T, Takahashi T, Noda T et al. bcl-2 deficiency in mice leads to pleiotropic abnormalities: Accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Res 1995; 55: 354-359.
14. Bouillet P, Cory S, Zhang LC, Strasser A, Adams JM. Degenerative disorders caused by Bcl-2 deficiency prevented by loss of its BH3-only antagonist Bim. Dev Cell 2001; 1: 645-653.
15. Yamamura K, Kamada S, Ito S, Nakagawa K, Ichihashi M, Tsujimoto Y. Accelerated disappearance of melanocytes in bcl-2-deficient mice. Cancer Res 1996; 56: 3546-3550.
16. Lindsten T, Ross AJ, King A, Zong WX, Rathmell JC, Shiels HA et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 2000; 6: 1389-1399.
17. Kutscher LM, Shaham S. Non-apoptotic cell death in animal development. Cell Death Differ 2017; 24: 1326-1336.
18. Yaginuma H, Shiraiwa N, Shimada T, Nishiyama K, Hong J,Wang S et al. Caspase activity is involved in, but is dispensable for, early motoneuron death in the chick embryo cervical spinal cord. Mol Cell Neurosci 2001; 18: 168-182.
19. Dekkers MP, Nikoletopoulou V, Barde YA. Cell biology in neuroscience: Death of developing neurons: new insights and implications for connectivity. J Cell Biol 2013; 203: 385-393.
20. Depaepe V, Suarez-Gonzalez N, Dufour A, Passante L, Gorski JA, Jones KR et al. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 2005; 435: 1244-1250.
21. Haydar TF, Kuan CY, Flavell RA, Rakic P. The role of cell death in regulating the size and shape of the mammalian forebrain. Cereb Cortex 1999; 9: 621-626.
22. Kuan CY, Roth KA, Flavell RA, Rakic P. Mechanisms of programmed cell death in the developing brain. Trends Neurosci 2000; 23: 291-297.
23. Clarke PG, Posada A, Primi MP, Castagne V. Neuronal death in the central nervous system during development. Biomed Pharmacother 1998; 52: 356-362.
24. Finlay BL, Pallas SL. Control of cell number in the developing mammalian visual system. Prog Neurobiol 1989; 32: 207-234.
25. Oppenheim RW. Cell death during development of the nervous system. Annu Rev Neurosci 1991; 14: 453-501.
26. Krajewska M, Mai JK, Zapata JM, Ashwell KW, Schendel SL, Reed JC et al. Dynamics of expression of apoptosis-regulatory proteins Bid, Bcl-2, Bcl-X, Bax and Bak during development of murine nervous system. Cell Death Differ 2002; 9: 145-157.
27. Arbour N, Vanderluit JL, Le Grand JN, Jahani-Asl A, Ruzhynsky VA, Cheung EC et al. Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J Neurosci 2008; 28: 6068-6078.
28. Abe-Dohmae S, Harada N, Yamada K, Tanaka R. Bcl-2 gene is highly expressed during neurogenesis in the central nervous system. Biochem Biophys Res Commun 1993; 191: 915-921.
29. Merry DE, Veis DJ, Hickey WF, Korsmeyer SJ. Bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development 1994; 120: 301-311.
30. Allsopp TE, Wyatt S, Paterson HF, Davies AM. The proto-oncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis. Cell 1993; 73: 295-307.
31. Farlie PG, Dringen R, Rees SM, Kannourakis G, Bernard O. bcl-2 transgene expression can protect neurons against developmental and induced cell death. Proc Natl Acad Sci USA 1995; 92: 4397-4401.
32. Garcia I, Martinou I, Tsujimoto Y, Martinou JC. Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. Science 1992; 258: 302-304.
33. Michaelidis TM, Sendtner M, Cooper JD, Airaksinen MS, Holtmann B, Meyer M et al. Inactivation of bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development. Neuron 1996; 17: 75-89.
34. Savitt JM, Jang SS, Mu W, Dawson VL, Dawson TM. Bcl-x is required for proper development of the mouse substantia nigra. J Neurosci 2005; 25: 6721-6728.
35. Krajewski S, Bodrug S, Krajewska M, Shabaik A, Gascoyne R, Berean K et al. Immunohistochemical analysis of Mcl-1 protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am J Pathol 1995; 146: 1309-1319.
36. Magiera MM, Mora S, Mojsa B, Robbins I, Lassot I, Desagher S. Trim17-mediated ubiquitination and degradation of Mcl-1 initiate apoptosis in neurons. Cell Death Differ 2013; 20: 281-292.
37. Orkin SH, Zon LI. Hematopoiesis: An evolving paradigm for stem cell biology. Cell 2008; 132: 631-644.
38. Muller AM, Medvinsky A, Strouboulis J, Grosveld F, Dzierzak E. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1994; 1: 291-301.
39. Delassus S, Cumano A. Circulation of hematopoietic progenitors in the mouse embryo. Immunity 1996; 4: 97-106.
40. Fleming HE, Janzen V, Lo Celso C, Guo J, Leahy KM, Kronenberg HM et al. Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve selfrenewal in vivo. Cell Stem Cell 2008; 2: 274-283.
41. Domen J, Cheshier SH, Weissman IL. The role of apoptosis in the regulation of hematopoietic stem cells: Overexpression of Bcl-2 increases both their number and repopulation potential. J Exp Med 2000; 191: 253-264.
42. Domen J, Gandy KL, Weissman IL. Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood 1998; 91: 2272-2282.
43. Ma A, Pena JC, Chang B, Margosian E, Davidson L, Alt FW et al. Bclx regulates the survival of double-positive thymocytes. Proc Natl Acad Sci USA 1995; 92: 4763-4767.
44. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 2005; 307: 1101-1104.
45. Delbridge AR, Opferman JT, Grabow S, Strasser A. Antagonism between MCL-1 and PUMA governs stem/progenitor cell survival during hematopoietic recovery from stress. Blood 2015; 125: 3273-3280.
46. 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.
47. Miyazaki T, Liu ZJ, Kawahara A, Minami Y, Yamada K, Tsujimoto Y et al. Three distinct IL-2 signaling pathways mediated by bcl-2, c-myc, and lck cooperate in hematopoietic cell proliferation. Cell 1995; 81: 223-231.
48. Akbar AN, Borthwick NJ, Wickremasinghe RG, Panayoitidis P, Pilling D, Bofill M et al. Interleukin-2 receptor common gamma-chain signaling cytokines regulate activated T cell apoptosis in response to growth factor withdrawal: Selective induction of anti-apoptotic (bcl-2, bcl-xL) but not pro- apoptotic (bax, bcl-xS) gene expression. Eur J Immunol 1996; 26: 294-299.
49. von Freeden-Jeffry U, Solvason N, Howard M, Murray R. The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity 1997; 7: 147-154.
50. Opferman JT, Letai A, Beard C, Sorcinelli MD, Ong CC, Korsmeyer SJ. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 2003; 426: 671-676.
51. Dzhagalov I, Dunkle A, He YW. The anti-apoptotic Bcl-2 family member Mcl-1 promotes T lymphocyte survival at multiple stages. J Immunol 2008; 181: 521-528.
52. Vikstrom I, Carotta S, Luthje K, Peperzak V, Jost PJ, Glaser S et al. Mcl-1 is essential for germinal center formation and B cell memory. Science 2010; 330: 1095-1099.
53. Tripathi P, Koss B, Opferman JT, Hildeman DA. Mcl-1 antagonizes Bax/Bak to promote effector CD4(+) and CD8(+) T-cell responses. Cell Death Differ 2013; 20: 998-1007.
54. Pierson W, Cauwe B, Policheni A, Schlenner SM, Franckaert D, Berges J et al. Antiapoptotic Mcl-1 is critical for the survival and niche-filling capacity of Foxp3(+) regulatory T cells. Nat Immunol 2013; 14: 959-965.
55. Sathe P, Delconte RB, Souza-Fonseca-Guimaraes F, Seillet C, Chopin M, Vandenberg CJ et al. Innate immunodeficiency following genetic ablation of Mcl1 in natural killer cells. Nat Commun 2014; 5: 4539.
56. Hatakeyama S, Hamasaki A, Negishi I, Loh DY, Sendo F, Nakayama K et al. Multiple gene duplication and expression of mouse bcl-2-related genes, A1. Int Immunol 1998; 10: 631-637.
57. Sochalska M, Ottina E, Tuzlak S, Herzog S, Herold M, Villunger A. Conditional knockdown of BCL2A1 reveals rate-limiting roles in BCR-dependent B-cell survival. Cell Death Differ 2016; 23: 628-639.
58. Tuzlak S, Schenk RL, Vasanthakumar A, Preston SP, Haschka MD, Zotos D et al. The BCL-2 pro-survival protein A1 is dispensable for T cell homeostasis on viral infection. Cell Death Differ 2017; 24: 523-533.
59. Schenk RL, Tuzlak S, Carrington EM, Zhan Y, Heinzel S, Teh CE et al. Characterisation of mice lacking all functional isoforms of the pro-survival BCL-2 family member A1 reveals minor defects in the haematopoietic compartment. Cell Death Differ 2017; 24: 534-545.
60. Chao JR, Wang JM, Lee SF, Peng HW, Lin YH, Chou CH et al. mcl-1 is an immediate-early gene activated by the granulocyte- macrophage colony-stimulating factor (GM-CSF) signaling pathway and is one component of the GM-CSF viability response. Mol Cell Biol 1998; 18: 4883-4898.
61. Dzhagalov I St, John A, He YW. The antiapoptotic protein Mcl-1 is essential for the survival of neutrophils but not macrophages. Blood 2007; 109: 1620-1626.
62. Steimer DA, Boyd K, Takeuchi O, Fisher JK, Zambetti GP, Opferman JT. Selective roles for antiapoptotic MCL-1 during granulocyte development and macrophage effector function. Blood 2009; 113: 2805-2815.
63. Haverkamp JM, Smith AM, Weinlich R, Dillon CP, Qualls JE, Neale G et al. Myeloid-derived suppressor activity is mediated by monocytic lineages maintained by continuous inhibition of extrinsic and intrinsic death pathways. Immunity 2014; 41: 947-959.
64. Orlofsky A, Weiss LM, Kawachi N, Prystowsky MB. Deficiency in the anti-apoptotic protein A1 - A results in a diminished acute inflammatory response. J Immunol 2002; 168: 1840-1846.
65. Ottina E, Grespi F, Tischner D, Soratroi C, Geley S, Ploner A et al. Targeting antiapoptotic A1/Bfl-1 by in vivo RNAi reveals multiple roles in leukocyte development in mice. Blood 2012; 119: 6032-6042.
66. Sanz C, Benet I, Richard C, Badia B, Andreu EJ, Prosper F et al. Antiapoptotic protein Bcl-x (L) is up-regulated during megakaryocytic differentiation of CD34(+) progenitors but is absent from senescent megakaryocytes. Exp Hematol 2001; 29: 728-735.
67. Wagner KU, Claudio E, Rucker EB 3rd, Riedlinger G, Broussard C, Schwartzberg PL et al. Conditional deletion of the Bcl-x gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development 2000; 127: 4949-4958.
68. Delbridge AR, Aubrey BJ, Hyland C, Bernardini JP, Di Rago L, Garnier JM et al. The BH3-only proteins BIM and PUMA are not critical for the reticulocyte apoptosis caused by loss of the pro-survival protein BCL-XL. Cell Death Dis 2017; 8: E2914.
69. Jacobsen SE, Borge OJ, Ramsfjell V, Cui L, Cardier JE, Veiby OP et al. Thrombopoietin, a direct stimulator of viability and multilineage growth of primitive bone marrow progenitor cells. Stem Cells 1996; 14(Suppl 1): 173-180.
70. Borge OJ, Ramsfjell V, Veiby OP, Murphy MJ Jr., Lok S, Jacobsen SE. Thrombopoietin, but not erythropoietin promotes viability and inhibits apoptosis of multipotent murine hematopoietic progenitor cells in vitro. Blood 1996; 88: 2859-2870.
71. Kirito K, Watanabe T, Sawada K, Endo H, Ozawa K, Komatsu N. Thrombopoietin regulates Bcl-xL gene expression through Stat5 and phosphatidylinositol 3-kinase activation pathways. J Biol Chem 2002; 277: 8329-8337.
72. Josefsson EC, James C, Henley KJ, Debrincat MA, Rogers KL, Dowling MR et al. Megakaryocytes possess a functional intrinsic apoptosis pathway that must be restrained to survive and produce platelets. J Exp Med 2011; 208: 2017-2031.
73. Debrincat MA, Josefsson EC, James C, Henley KJ, Ellis S, Lebois M et al. Mcl-1 and Bcl-xL coordinately regulate megakaryocyte survival. Blood 2012; 119: 5850-5858.
74. Debrincat MA, Pleines I, Lebois M, Lane RM, Holmes ML, Corbin J et al. BCL-2 is dispensable for thrombopoiesis and platelet survival. Cell Death Dis 2015; 6: E1721.
75. Vanags DM, Orrenius S, Aguilar-Santelises M. Alterations in Bcl-2/Bax protein levels in platelets form part of an ionomycin-induced process that resembles apoptosis. Br J Haematol 1997; 99: 824-831.
76. Brown SB, Clarke MC, Magowan L, Sanderson H, Savill J. Constitutive death of platelets leading to scavenger receptor-mediated phagocytosis. A caspase-independent cell clearance program. J Biol Chem 2000; 275: 5987-5996.
77. Pereira J, Soto M, Palomo I, Ocqueteau M, Coetzee LM, Astudillo S et al. Platelet aging in vivo is associated with activation of apoptotic pathways: Studies in a model of suppressed thrombopoiesis in dogs. Thromb Haemost 2002; 87: 905-909.
78. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005; 435: 677-681.
79. Mason KD, Carpinelli MR, Fletcher JI, Collinge JE, Hilton AA, Ellis S et al. Programmed anuclear cell death delimits platelet life span. Cell 2007; 128: 1173-1186.
80. Zhang H, Nimmer PM, Tahir SK, Chen J, Fryer RM, Hahn KR et al. Bcl-2 family proteins are essential for platelet survival. Cell Death Differ 2007; 14: 943-951.
81. 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.
82. Ross AJ, Waymire KG, Moss JE, Parlow AF, Skinner MK, Russell LD et al. Testicular degeneration in Bclw-deficient mice. Nat Genet 1998; 18: 251-256.
83. Print CG, Loveland KL, Gibson L, Meehan T, Stylianou A, Wreford N et al. Apoptosis regulator bcl-w is essential for spermatogenesis but appears otherwise redundant. Proc Natl Acad Sci USA 1998; 95: 12424-12431.
84. Wang X, Bathina M, Lynch J, Koss B, Calabrese C, Frase S et al. Deletion of MCL-1 causes lethal cardiac failure and mitochondrial dysfunction. Genes Dev 2013; 27: 1351-1364.
85. Thomas RL, Roberts DJ, Kubli DA, Lee Y, Quinsay MN, Owens JB et al. Loss of MCL-1 leads to impaired autophagy and rapid development of heart failure. Genes Dev 2013; 27: 1365-1377