Bcl-2 protein family members: Versatile regulators of calcium signaling in cell survival and apoptosis

Annual Review of Physiology

Volumn 70, Issue , 2008, Pages 73-91

  Rong, Yiping ^a   Distelhorst, Clark W ^a  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

Apoptosis; Calcium channel; Cell death; Endoplasmic reticulum; Inositol 1,4,5 trisphosphate receptor; Mitochondria

Indexed keywords

INOSITOL 1,4,5 TRISPHOSPHATE; PROTEIN BCL 2;

APOPTOSIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL FATE; CELL SURVIVAL; ENDOPLASMIC RETICULUM; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN INTERACTION; REVIEW; ANIMAL; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CALCIUM SIGNALING; CELL SURVIVAL; HUMANS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 42549144606     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.physiol.70.021507.105852     Document Type: Review

References (117)

1. Cory S, Adams JM. 2002. The Bcl-2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2:647-56
2. Danial NN, Korsmeyer SJ. 2004. Cell death: critical control points. Cell 116:205-19
3. Sharpe JC, Arnoult D, Youle RJ. 2004. Control of mitochondrial permeability by Bcl-2 family proteins. Biochim. Biophys. Acta 1644:107-13
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 1644:115-23
5. Baffy G, Miyashita T, Williamson JR, Reed JC. 1993. Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J. Biol. Chem. 268:6511-19
6. 2+ Huxes. Proc. Natl. Acad. Sci. USA 91:6569-73
7. Carafoli E. 2002. Calcium signaling: a tale for all seasons. Proc. Natl. Acad. Sci. USA 99:1115-22
8. Berridge MJ, Bootman MD, Lipp P. 1998. Calcium: a life and death signal. Nature 395:645-48
9. Berridge MJ, Bootman MD, Roderick HL. 2003. Calcium signaling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4:517-29
10. Petersen OH, Michalak M, Verkhratsky A. 2005. Calcium signalling: past, present and future. Cell Calcium 38:161-69
11. Taylor CW, Genazzani AA, Morris SA. 1999. Expression of inositol trisphosphate receptors. Cell Calcium 26:237-51
12. Bezprozvanny I. 2005. The inositol 1,4,5-trisphosphate receptors. Cell Calcium 38:261-72
13. 2+ release channel function. Biochem. J. 337:345-61
14. Thrower EC, Hagar RE, Ehrlich BE. 2001. Regulation of Ins(1,4,5)P3 receptor isoforms by endogenous modulators. Trends Pharmacol. Sci. 22:580-86
15. Roderick HL, Bootman MD. 2003. Bi-directional signalling from the InsP3 receptor: regulation by calcium and accessory factors. Biochem. Soc. Trans. 31:950-53
16. 2+ signals. J. Cell Sci. 114:2213-22
17. Lewis RS, Cahalan MD. 1990. Ion channels and signal transduction in lymphocytes. Annu. Rev. Physiol. 52:415-30
18. Berridge MJ. 1997. Lymphocyte activation in health and disease. Crit. Rev. Immunol. 17:155-78
19. Lewis RS. 2001. Calcium signaling mechanisms in T lymphocytes. Annu. Rev. Immunol. 19:497-521
20. Winslow MM, Neilson JR, Crabtree GR. 2003. Calcium signaling in lymphocytes. Curr. Opin. Immunol. 15:299-307
21. Neilson JR, Winslow MM, Hur EM, Crabtree GR. 2004. Calcineurin B1 is essential for positive but not negative selection during thymocyte development. Immunity 20:255-66
22. 2+ signaling. Biol. Cell 96:69-78
23. 2+ signals according to the strength of T cell receptor activation. J. Cell Biol. 172:127-37
24. 2+ release and beyond. Apoptosis 12:951-68
25. Orrenius S, Zhivotovsky B, Nicotera P. 2003. Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4:552-65
26. Rizzuto R, Pinton P, Ferrari D, Chami M, Szabadkai G, et al. 2003. Calcium and apoptosis: facts and hypotheses. Oncogene 22:8619-27
27. 3 receptors channel calcium into cell death. Curr. Biol. 14:R933-35
28. Kaiser N, Edelman IS. 1977. Calcium dependence of glucocorticoid-induced lymphocytolysis. Proc. Natl. Acad. Sci. USA 74:632-42
29. Orrenius S, McConkey DJ, Nicotera P. 1991. Role of calcium in toxic and programmed cell death. Adv. Exp. Med. Biol. 283:419-25
30. Dowd DR, MacDonald PN, Komm BS, Haussler MR, Miesfeld RL. 1992. Stable expression of the calbindin-D28K complementary DNA interferes with the apoptotic pathway in lymphocytes. Mol. Endo. 6:1843-48
31. Lam M, Dubyak G, Distelhorst CW. 1993. Effect of glucocorticosteroid treatment on intracellular calcium homeostasis in mouse lymphoma cells. Mol. Endo. 7:686-93
32. 2+ stores in induction and suppression of apoptosis in S49 cells. Am. J. Physiol. 272 (Cell Physiol. 41):C1241-49
33. Squier MK, Cohen JJ. 1997. Calpain, an upstream regulator of thymocyte apoptosis. J. Immunol. 158:3690-97
34. Magnelli L, Cinelli M, Turchetti A, Chiarugi VP. 1994. Bcl-2 overexpression abolishes early calcium waving preceding apoptosis in NIH-3T3 murine fibroblasts. Biochem. Biophys. Res. Commun. 204:84-90
35. 2+ fluxes. Oncogene 11:2165-74
36. 2+ pool depletion. Oncogene 12:2051-55
37. 2+. Oncogene 12:2259-66
38. Kruman II, Mattson MP. 1999. Pivotal role of mitochondrial calcium uptake in neural cell apoptosis and necrosis. J. Neurochem. 72:529-40
39. Rimpler MM, Rauen U, Schmidt T, Moroy T, De Groot H. 1999. Protection against hydrogen peroxide cytotoxicity in Rat-1 fibroblasts provided by the oncoprotein Bcl-2: Maintenance of calcium homeostasis is secondary to the effect of Bcl-2 on cellular glutathione. Biochem. J. 340:291-97
40. 2- concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J. 20:2690-701
41. 2+ release from the endoplasmic reticulum and suppressing Bcl-2 expression. J. Biol. Chem. 277:31381-89
42. Breckenridge DG, Stojanovic M, Marcellus RC, Shore GC. 2003. Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J. Cell Biol. 160:1115-27
43. 2+ from endoplasmic reticulum stores and mitochondrial apoptosis during stress-induced cell death. J. Biol. Chem. 280:23829-36
44. Hanson CJ, Distelhorst CW, Bootman MD, Berridge MJ, Roderick HL. 2004. Bcl-2 functionally interacts with the inositol 1,4,5-trisphosphate receptor (InsP3R) to inhibit calcium release. J. Physiol. 555P:PC69
45. Khan AA, Soloski MJ, Sharp AH, Schilling G, Sabatini DM, et al. 1996. Lymphocyte apoptosis: mediation by increased type 3 inositol 1,4,5-trisphosphate receptor. Science 273:503-7
46. Jayaraman T, Marks AR. 1997. T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol. Cell. Biol. 17:3005-12
47. Sugawara H, Kurosaki M, Takata M, Kurosaki T. 1997. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 16:3078-88
48. Blackshaw S, Sawa A, Sharp AH, Ross CA, Snyder SH, Khan AA. 2000. Type 3 inositol 1,4,5-trisphosphate receptor modulates cell death. FASEB J. 14:1375-79
49. Estrada M, Varshney A, Ehrlich BE. 2006. Elevated testosterone induces apoptosis in neuronal cells. J. Biol. Chem. 281:25492-501
50. 2+ elevation. J. Cell Biol. 175:709-14
51. Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH. 2003. Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat. Cell Biol. 5:1051-61
52. Assefa Z, Bultynck G, Szlufcik K, Kasri NN, Vermassen E, et al. 2 004. Caspase-3-induced truncation of type 1 inositol trisphosphate receptor accelerates apoptotic cell death and induces inositol trisphosphate-independent calcium release during apoptosis. J. Biol. Chem. 279:43227-36
53. Nakayama T, Hattori M, Uchida K, Nakamura T, Tateishi Y, et al. 2004. The regulatory domain of the inositol 1,4,5-trisphosphate receptor is necessary to keep the channel domain closed: possible physiological significance of specific cleavage by caspase 3. Biochem. J. 377:299-307
54. Szlufcik K, Bultynck G, Callewaert G, Missiaen L, Parys JB, De Smedt H. 2006. The suppressor domain of inositol 1,4,5-trisphosphate receptor plays an essential role in the protection against apoptosis. Cell Calcium 39:325-36
55. Higo T, Hattori M, Nakamura T, Natsume T, Michikawa T, Mikoshiba K. 2005. Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell 120:85-98
56. Kuwana T, Newmeyer DD. 2003. Bcl-2 family proteins and the role of mitochondria in apoptosis. Curr. Opin. Cell Biol. 15:691-99
57. 2+ release: an intimate connection. Trends Biochem. Sci. 25:215-21
58. Jacobson J, Duchen MR. 2004. Interplay between mitochondria and cellular calcium signaling. Mol. Cell. Biochem. 256-257:209-18
59. 2+ uptake in apoptosis. Cell Calcium 40:553-60
60. 2+-leak channel: cell biological and pathological consequences. Biol. Cell 98:1-14
61. Szalai G, Krishnamurthy R, Hajnoczky G. 1999. Apoptosis driven by IP3-linked mito-chondrial calcium signals. EMBO J. 18:6349-61
62. Pacher P, Hajnoczky G. 2001. Propagation of the apoptotic signal by mitochondrial waves. EMBO J. 20:4107-21
63. 2+ signals. J. Biol. Chem. 280:33637-44
64. 2+ signals into mitochondria. J. Biol. Chem. 280:40892-900
65. Gunter TE, Yule DI, Gunter KK, Eliseev RA, Salter JD. 2004. Calcium and mitochondria. FEBS Lett. 567:96-102
66. + thymocytes is altered by overexpression of the BCL-2 protooncogene in the thymus. J. Exp. Med. 179:145-53
67. Wilson BE, Mochon E, Boxer LM. 1996. Induction of bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Mol. Cell. Biol. 16:5546-56
68. Chao DT, Korsmeyer SJ. 1997. BCL-XL-regulated apoptosis in T cell development. Int. Immunol. 9:1375-84
69. Gomez J, Martinez-A C, Gonzalez A, Garcia A, Rebollo A. 1998. The Bcl-2 gene is differentially regulated by IL-2 and IL-4: role of the transcription factor NF-AT. Oncogene 17:1235-43
70. Oukka M, Ho I-C, de la Brousse FC, Hoey T, Grusby MJ, Glimcher LH. 1998. The transcription factor NFAT4 is involved in the generation and survival of T cells. Immunity 9:295-304
71. 3R. Nat. Cell Biol. 7:1021-28
72. 2+ stores. J. Biol. Chem. 277:9219-95
73. 2+ mobilization promotes cytochrome c release during apoptosis. J. Biol. Chem. 277:20301-8
74. Zhong WX, Li C, Hatzivassiliou G, Lindsten T, Yu Q-C, et al. 2003. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 162:59-69
75. 2+ wave propagation. Cell Death Differ. 11:1265-76
76. 2+ permeation through the outer mitochondrial membrane. EMBO J. 21:2198-206
77. 2+- dependent transcriptional induction of Bim of cell death. J. Immunol. 176:2299-306
78. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284:339-43
79. 2+ signaling to support the intrinsic regenerative capacity of CNS axons. EMBO J. 24:1068-78
80. 2+ analyzed with an improved genetically encoded fluorescent sensor. Proc. Natl. Acad. Sci. USA 101:17404-9
81. An J, Chen Y, Huang Z. 2004. Critical upstream signals of cytochrome c release induced by a novel Bcl-2 inhibitor. J. Biol. Chem. 279:19133-40
82. Prehn JHM, Bindokas VP, Maruccilli CJ, Krajewski S, Reed JC, Miller RJ. 1994. Regulation of neuronal Bcl-2 protein expression and calcium homeostasis by transforming growth factor type beta confers wide-ranging protection on rat hippocampal neurons. Proc. Natl. Acad. Sci. USA 91:12599-603
83. Murphy AN, Bredesen DE, Cortopassi G, Wang E, Fiskum G. 1996. Bcl-2 potentiates the maximal calcium uptake capacity of neural cell mitochondria. Proc. Natl. Acad. Sci. USA 93:9893-98
84. Nilsen J, Brinton RD. 2003. Mechanism of estrogen-mediated neuroprotection: regulation of mitochondrial calcium and Bcl-2 expression. Proc. Natl. Acad. Sci. USA 100:2842-47
85. Chen R, Valencia I, Zhong F, McColl KS, Roderick HL, et al. 2004. Bcl-2 functionally interacts with inositol 1,4,5-trisphosphate receptors to regulate calcium release from the ER. J. Cell Biol. 166:193-203
86. Basset O, Boittin F-X, Cognard C, Constantin B, Ruegg UT. 2006. Bcl-2 overexpression prevents calcium overload and subsequent apoptosis in dystrophic myotubes. Biochem. J. 395:267-76
87. 3-mediated calcium release and apoptosis by Bcl-2 involves the participation of protein phosphatase 1. Mol. Cell. Biochem. 295:153-65
88. 2+ flux. Cell 83:463-72
89. Tong G, Shepherd D, Jahr CE. 1995. Synaptic desensitization of NMDA receptors by calcineurin. Science 267:510-12
90. deSouza N, Reiken S, Ondrias K, Yang Y, Matkovich S, Marks AR. 2002. Protein kinase A and two phosphatases are components of the inositol 1,4,5-trisphosphate receptor macromolecular signaling complex. J. Biol. Chem. 277:39397-400
91. Soulsby MD, Wojcikiewicz RJ. 2005. The type III inositol 1,4,5-trisphosphate receptor is phosphorylated by cAMP-dependent protein kinase at three sites. Biochem. J. 392:493-97
92. Khan MT, Wagner L, Yule DI, Bhanumathy C, Joseph SK. 2006. Akt kinase phosphorylation of inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 281:3731-37
93. - inositol 1,4,5-trisphosphate receptor defines susceptibility to phosphorylation by protein kinase A. J. Biol. Chem. 281:17410-19
94. Shibasaki F, Kondo E, Akagi T, McKeon F. 1997. Suppression of signalling through transcription factor NF-AT by interactions between calcineurin and Bcl-2. Nature 386:728-31
95. Erin N, Bronson SK, Billingsley ML. 2003. Calcium-dependent interaction of calcineurin with Bcl-2 in neuronal tissue. Neuroscience 117:541-55
96. Erin N, Lehman RAW, Boyer PJ, Billingsley ML. 2003. In vitro hypoxia and excitotoxicity in human brain induce calcineurin-Bcl-2 interactions. Neuroscience 117:557-65
97. Erin N, Billingsley ML. 2004. Domoic acid enhances Bd-2-calcineurin- inositol-1,4,5-trisphosphate receptor interactions and delayed neuronal death in rat brain slices. Brain Res. 1014:45-52
98. Shitashige M, Tou M, Yano T, Shibata M, Matsuo Y, Shibasaki F. 2001. Dissociation of Bax from a Bcl-2/Bax heterodimer triggered by phosphorylation of serine 70 of Bcl-2. J Biochem. 130:741-48
99. 2+ homeostasis and apoptosis. EMBO J. 23:1207-16
100. 2+ homeostasis by altering expression of inositol 1,4,5-trisphosphate receptors. Proc. Natl. Acad. Sci. USA 99:9830-35
101. Oakes SA, Scorrano L, Opferman JT, Bassik MC, Nishino M, et al. 2005. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 102:105-10
102. 2+ influx in Bcl-2-overexpressing cells. J. Cell Biol. 148:857-62
103. 2+ concentration within the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 97:5723-28
104. 2+ homeostasis and store-operated channels in prostate cancer cells. Cancer Cell 1:169-79
105. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, et al. 2003. Regulation of endoplasmic reticulum calcium dynamics by Bax and Bak: a control point for apoptosis. Science 300:135139
106. 2+-ATPase (SERCA). Biochem. J. 383:361-70
107. Dremina ES, Sharov VS, Schoneich C. 2006. Displacement of SERCA from SR lipid caveolae-related domains by Bcl-2: a possible mechanism for SERCA inactivation. Biochemistry 45:175-84
108. Kuo TH, Kim H-RC, Zhu L, Yu Y, Lin H-M, Tsang W. 1998. Modulation of endoplasmic reticulum calcium pump by Bcl-2. Oncogene 17:1903-10
109. 2+ signaling, which do not depend on their putative pore-forming region. J. Biol. Chem. 279:54581-89
110. Distelhorst CW, Shore GC. 2004. Bcl-2 and calcium: controversy beneath the surface. Oncogene 23:2875-80
111. Zhong L-T, Sarafian T, Kane DJ, Charles AC, Mah SP, et al. 1993. bcl-2 inhibits death of central neural cells induced by multiple agents. Proc. Natl. Acad. Sci. USA 90:4533-37
112. He H, Lam M, McCormick TS, Distelhorst CW. 1997. Maintenance of calcium homeostasis in the endoplasmic reticulum by Bcl-2. J. Cell Biol. 138:1219-28
113. 2+ mobilization. Am. J. Physiol. 275:C832-39
114. Wei H, Wei W, Bredesen DE, Perry DC. 1998. Bcl-2 protects against apoptosis in neuronal cell line caused by thapsigargin-induced depletion of intracellular calcium stores. J. Neurochem. 70:2305-14
115. 2+ homeostasis by Bcl-2. J. Biol. Chem. 274:33276-73
116. Williams SS, French JN, Gilbert M, Rangaswami AA, Walleczek J, Knox SJ. 2000. Bcl-2 overexpression results in enhanced capacitative calcium entry and resistance to SKF-96395-induced apoptosis. Cancer Res. 60:4358-61
117. 2+ by caffeine and ryanodine induces apoptosis of chinese hamster ovary cells transfected with ryanodine receptor. J. Biol. Chem. 275:19978-84