Bcl-2 on the endoplasmic reticulum: Protecting the mitochondria from a distance

Journal of Cell Science

Volumn 116, Issue 22, 2003, Pages 4493-4499

  Thomenius, Michael J ^a   Distelhorst, Clark W ^a  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

Bcl 2; Bcl Cb5; BH3 only; Calcium; Cytochrome c; Endoplasmic reticulum; ER; Mitochondria

Indexed keywords

CALCIUM ION; PROTEIN BCL 2;

APOPTOSIS; CALCIUM SIGNALING; CELL DEATH; CELL PROTECTION; ENDOPLASMIC RETICULUM; HUMAN; HYPOTHESIS; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW;

ANIMALS; APOPTOSIS; BCL-X PROTEIN; CASPASES; CELLS, CULTURED; CYTOCHROMES C; ENDOPLASMIC RETICULUM; HUMANS; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 0344897663     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00829     Document Type: Review

References (84)

1. Akao, Y., Otsuki, Y., Kataoka, S., Ito, Y. and Tsujimoto, Y. (1994). Multiple subcellular localization of bcl-2: detection in nuclear outer membrane, endoplasmic reticulum membrane, and mitochondrial membranes. Cancer Res. 54, 2468-2471.
2. Annis, M. G., Zamzami, N., Zhu, W., Penn, L. Z., Kroemer, G., Leber, B. and Andrews, D. W. (2001). Endoplasmic reticulum localized Bcl-2 prevents apoptosis when redistribution of cytochrome c is a late event. Oncogene 20, 1939-1952.
3. Baffy, G., Miyashita, T., Williamson, J. R. and Reed, J. C. (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, 6511-6519.
4. Berridge, M. J., Bootman, M. D. and Roderick, H. L. (2003). Calcium signaling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell. Biol. 4, 517-529.
5. Bouillet, P. and Strasser, A. (2002). BH3-only proteins - evolutionarily conserved proapoptotic Bcl-2 family members essential for initiating programmed cell death. J. Cell. Sci. 115, 1567-1574.
6. Breckenridge, D. G., Nguyen, M., Kuppig, S., Reth, M. and Shore, G. C. (2002). The procaspase-8 isoform, procaspase-8L, recruited to the BAP31 complex at the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 99, 4331-4336.
7. Cheng, E. H., Levine, B., Boise, L. H., Thompson, C. B. and Hardwick, J. M. (1996). Bax-independent inhibition of apoptosis by Bcl-XL. Nature 379, 554-556.
8. Cory, S. and Adams, J. M. (2002). The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647-656.
9. Csordas, G., Madesh, M., Antonsson, B. and Hajnoczky, G. (2002). tcBid promotes Ca2+ signal propagation to the mitochondria: control of Ca2+ permeation through the outer mitochondrial membrane. EMBO J. 21, 2198-2206.
10. Desagher, S. and Martinou, J. C. (2000). Mitochondria as the central control point of apoptosis. Trends Cell Biol. 10, 369-377.
11. Desagher, S., Osen-Sand, A., Nichols, A., Eskes, R., Montessuit, S., Lauper, S., Maundrell, K., Antonsson, B. and Martinou, J. C. (1999). Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144, 891-901.
12. Distelhorst, C. W., Lam, M. and McCormick, T. S. (1996). Bcl-2 inhibits hydrogen peroxide-induced ER Ca2+ pool depletion. Oncogene 12, 2051-2055.
13. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A. and Nagata, S. (1998). A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391, 43-50.
14. Erin, N., Bronson, S. K. and Billingsley, M. L. (2003a). Calcium-dependent interaction of calcineurin with Bcl-2 in neuronal tissue. Neuroscience 117, 541-555.
15. Erin, N., Lehman, R. A. W., Boyer, P. J. and Billingsley, M. L. (2003b). In vitro hypoxia and excitotoxicity in human brain induce calcineurin-Bcl-2 interactions. Neuroscience 117, 557-565.
16. Ferri, K. E. and Kroemer, G. (2001). Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 3, E255-E263.
17. Foyouzi-Youssefi, R., Arnaudeau, S., Borner, C., Kelley, W. L., Tschopp, J., Lew, D. P., Demaurex, N. and Krause, K. H. (2000). Bcl-2 decreases the free Ca2+ concentration within the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 97, 5723-5728.
18. Germain, M., Mathai, J. P. and Shore, G. C. (2002). BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J. Biol. Chem. 277, 18053-18060.
19. Green, D. R. and Reed, J. C. (1998). Mitochondria and apoptosis. Science 281, 1309-1312.
20. Grinberg, M., Sarig, R., Zaltsman, Y., Frumkin, D., Grammatikakis, N., Reuveny, E. and Gross, A. (2002). tBID homooligomerizes in the mitochondrial membrane to induce apoptosis. J. Biol. Chem. 277, 12237-12245.
21. Hacki, J., Egger, L., Monney, L., Conus, S., Rosse, T., Fellay, I. and Borner, C. (2000). Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene 19, 2286-2295.
22. Hajnoczky, G., Csordas, G., Krishnamurthy, R. and Szalai, G. (2000). Mitochondrial calcium signaling driven by the IP3 receptor. J. Bioenerg. Biomembr. 32, 15-25.
23. Han, J., Flemington, C., Houghton, A. B., Gu, Z., Zambetti, G. P., Lutz, R. J., Zhu, L. and Chittenden, T. (2001). Expression of bbc3, a proapoptotic BH3-only gene, is regulated by diverse cell death and survival signals. Proc. Natl. Acad. Sci. USA 98, 11318-11323.
24. He, H., Lam, M., McCormick, T. S. and Distelhorst, C. W. (1997). Maintenance of calcium homeostasis in the endoplasmic reticulum by Bcl-2. J. Cell Biol. 138, 1219-1228.
25. Hockenbery, D. M., Oltvai, Z. N., Yin, X. M., Milliman, C. L. and Korsmeyer, S. J. (1993). Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75, 241-251.
26. Janiak, F., Leber, B. and Andrews, D. W. (1994). Assembly of Bcl-2 into microsomal and outer mitochondrial membranes. J Biol. Chem. 269, 9842-9849.
27. Jayaraman, T. and Marks, A. R. (1997). T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol. Cell. Biol. 17, 3005-3012.
28. Jiang, A. and Clark, E. A. (2001). Involvement of Bik, a proapoptotic member of the Bcl-2 family, in surface IgM-mediated B cell apoptosis. J. Immunol. 166, 6025-6033.
29. Kaufmann, T., Schlipf, S., Sanz, J., Neubert, K., Stein, R. and Borner, C. (2003). Characterization of the signal that directs Bcl-xL, but not Bcl-2, to the mitochondrial outer membrane. J. Cell Biol. 160, 53-64.
30. Kerr, J. F., Wyllie, A. H. and Currie, A. R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26, 239-257.
31. Khan, A. A., Soloski, M. J., Sharp, A. H., Schilling, G., Sabatini, D. M., Li, S.-H., Ross, C. A. and Snyder, S. H. (1996). Lymphocyte apoptosis: mediation by increased type 3 inositol 1,4,5,-trisphosphate receptor. Science 273, 503-507.
32. Krajewski, S., Tanaka, S., Takayama, S., Schibler, M. J., Fenton, W. and Reed, J. C. (1993). Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53, 4701-4714.
33. Lam, M., Dubyak, G., Chen, L., Nuñez, G., Miesfeld, R. L. and Distelhorst, C. W. (1994). Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc. Natl. Acad. Sci. USA 91, 6569-6573.
34. Lee, S. T., Hoeflich, K. P., Wasfy, G. W., Woodgett, J. R., Leber, B., Andrews, D. W., Hedley, D. W. and Penn, L. Z. (1999). Bcl-2 targeted to the endoplasmic reticulum can inhibit apoptosis induced by Myc but not etoposide in Rat-1 fibroblasts. Oncogene 18, 3520-3528.
35. Letai, A., Bassik, M., Walensky, L., Sorcinelli, M., Weiler, S. and Korsmeyer, S. (2002). Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2, 183-192.
36. Lewis, R. S. (2001). Calcium signaling mechanisms in T lymphocytes. Annu. Rev. Immunol. 19, 497-521.
37. Linette, G. P., Li, Y., Roth, K. and Korsmeyer, S. J. (1996). Cross talk between cell death and cell cycle progression: BCL-2 regulates NFAT-mediated activation. Proc. Natl. Acad. Sci. USA 93, 9545-9552.
38. Magnelli, L., Cinelli, M., Turchetti, A. and Chiarugi, V. P. (1994). Bcl-2 overexpression abolishes early calcium waving preceding apopto'sis in NIH-3T3 murine fibroblasts. Biochem. Biophys. Res. Commun. 204, 84-90.
39. Marani, M., Tenev, T., Hancock, D., Downward, J. and Lemoine, N. R. (2002). Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol. Cell. Biol. 22, 3577-3589.
40. Mathai, J. P., Germain, M., Marcellus, R. C. and Shore, G. C. (2002). Induction and endoplasmic reticulum location of BIK/NBK in response to apoptotic signaling by E1A and p53. Oncogene 21, 2534-2544.
41. Mitoma, J. and Ito, A. (1992). The carboxy-terminal 10 amino acid residues of cytochrome b5 are necessary for its targeting to the endoplasmic reticulum. EMBO J. 11, 4197-4203.
42. Monaghan, P., Robertson, D., Amos, T. A., Dyer, M. J., Mason, D. Y. and Greaves, M. F. (1992). Ultrastructural localization of bel-2 protein. J. Histochem. Cytochem. 40, 1819-1825.
43. Mund, T., Gewies, A., Schoenfeld, N., Bauer, M. K. and Grimm, S. (2003). Spike, a novel BH3-only protein, regulates apoptosis at the endoplasmic reticulum. FASEB J. 17, 696-698.
44. Ng, F. W. and Shore, G. C. (1998). Bcl-XL cooperatively associates with the Bap31 complex in the endoplasmic reticulum, dependent on procaspase-8 and Ced-4 adaptor. J. Biol. Chem. 273, 3140-3143.
45. Nguyen, M., Millar, D. G., Yong, V. W., Korsmeyer, S. J. and Shore, G. C. (1993). Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J. Biol. Chem. 268, 25265-25268.
46. Nguyen, M., Breckenridge, D. G., Ducret, A. and Shore, G. C. (2000). Caspase-resistant BAP31 inhibits fas-mediated apoptotic membrane fragmentation and release of cytochrome c from mitochondria. Mol. Cell. Biol. 20, 6731-6740.
47. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A. et al. (1995). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376, 37-43.
48. Nieminen, A.-L. (2003). Apoptosis and necrosis in health and disease: role of mitochondria. Int. Rev. Cytol. 224, 29-55.
49. Nutt, L. K., Pataer, A., Pahler, J., Fang, B., Roth, J., McConkey, D. J. and Swisher, S. G. (2002). Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial Ca2+ stores. J. Biol. Chem. 277, 9219-9225.
50. Oltvai, Z. N., Milliman, C. L. and Korsmeyer, S. J. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609-619.
51. Orrenius, S., Zhivotovsky, B. and Nicotera, P. (2003). Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell. Biol. 4, 552-565.
52. Pacher, P. and Hajnoczky, G. (2001). Propagation of the apoptotic signal by mitochondrial waves. EMBO J. 20, 4107-4121.
53. Parijs, L. V., Refaeli, Y., Lord, J. D., Nelson, B. H., Abbas, A. K. and Baltimore, D. (1999). Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation-induced cell death. Immunity 11, 281-288.
54. Patel, S., Joseph, S. K. and Thomas, A. P. (1999). Molecular properties of inositol 1,4,5-trisphosphate receptors. Cell Calcium 25, 247-264.
55. Petersen, O. H. (2002). Calcium signal compartmentalization. Biol. Res. 35, 177-182.
56. Pinton, P., Ferrari, D., Magalhaes, P., Schulze-Osthoff, K., di Virgilio, F., Pozzan, T. and 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.
57. Pinton, P., Ferrari, D., Rapizzi, E., de Virgilio, F., Pozzan, T. and Rizzuto, R. (2001). The Ca2+ 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, 2690-2701.
58. Putney, J. W., Jr, Broad, L. M., Braun, F. J., Lievremont, J. P. and Bird, G. S. (2001). Mechanisms of capacitative calcium entry. J. Cell Sci. 114, 2223-2229.
59. Rudner, J., Lepple-Wienhues, A., Budach, W., Berschauer, J., Friedrich, B., Wesselborg, S., Schulze-Osthoff, K. and Belka, C. (2001). Wild-type, mitochondrial and ER-restricted Bcl-2 inhibit DNA damage-induced apoptosis but do not affect death receptor-induced apoptosis. J. Cell Sci. 114, 4161-4172.
60. Rudner, J., Jendrossek, V. and Belka, C. (2002). New insights in the role of Bcl-2 Bcl-2 and the endoplasmic reticulum. Apoptosis 7, 441-447.
61. Saito, S., Hiroi, Y., Zou, Y., Aikawa, R., Toko, H., Shibasaki, F., Yazaki, Y., Nagai, R. and Komuro, I. (2000). β-adrenergic pathway induces apoptosis through calcineurin activation in cardiac myocytes. J. Biol. Chem. 275, 34528-34533.
62. Scorrano, L., Oakes, S. A., Opferman, J. T., Cheng, E. H., Sorcinelli, M. D., Pozzan, T. and Korsmeyer, S. J. (2003). BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300, 135-139.
63. Shibasaki, F. and McKeon, F. (1995). Calcineurin functions in Ca2+-activated cell death in mammalian cells. J Cell Biol. 131, 735-743.
64. Shibasaki, F., Kondo, E., Akagi, T. and McKeon, F. (1997). Suppression of signalling through transcription factor NF-AT by interactions between calcineurin and Bcl-2. Nature 386, 728-731.
65. Smaili, S. S., Hsu, Y. T., Youle, R. J. and Russell, J. T. (2000). Mitochondria in Ca2+ signaling and apoptosis. J. Bioenerg. Biomembr. 32, 35-46.
66. Srivastava, R. K., Sasaki, C. Y., Hardwick, J. M. and Longo, D. L. (1999). Bcl-2-mediated drug resistance: inhibition of apoptosis by blocking nuclear factor of activated T lymphocytes (NFAT)-induced Fax ligand transcription. J. Exp. Med. 190, 253-265.
67. Sugawara, H., Kurosaki, M., Takata, M. and 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, 3078-3088.
68. Sugiyama, T., Shimizu, S., Matsuoka, Y., Yoneda, Y. and Tsujimoto, Y. (2002). Activation of mitochondrial voltage-dependent anion channel by apro-apoptotic BH3-only protein Bim. Oncogene 21, 4944-4956.
69. Szalai, G., Krishnamurthy, R. and Hajnoczky, G. (1999). Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J. 18, 6349-6361.
70. Tanaka, S., Saito, K. and Reed, J. C. (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.
71. Tewari, M., Quan, L. T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, G. G., Salvesen, G. S. and Dixit, V. M. (1995). Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81, 801-809.
72. Thomenius, M. J., Wang, N. S., Reineks, E. Z., Wang, Z. and Distelhorst, C. W. (2003). Bcl-2 on the endoplasmic reticulurn regulates Bax activity by binding to BH3-only proteins. J. Biol. Chem. 278, 6243-6250.
73. Thrower, E. C., Hagar, R. E. and Ehrlich, B. E. (2001). Regulation of Ins(1,4,5)P3 receptor isoforms by endogenous modulators. Trends Pharmacol. Sci. 22, 580-586.
74. Uhlmann, E. J., Subramanian, T., Vater, C. A., Lutz, R. and Chinnadurai, G. (1998). A potent cell death activity associated with transient high level expression of BCL-2. J. Biol. Chem. 273, 17926-17932.
75. van Loo, G., Saelens, X., van Gurp, M., MacFarlane, M., Martin, S. J. and Vandenabeele, P. (2002). The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 9, 1031-1042.
76. Wang, H. G., Pathan, N., Ethell, I. M., Krajewski, S., Yamaguchi, Y., Shibasaki, F., McKeon, F., Bobo, T., Franke, T. F. and Reed, J. C. (1999). Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284, 339-343.
77. Wang, N. S., Unkila, M. T., Reineks, E. Z. and Distelhorst, C. W. (2001). Transient expression of wild-type or mitochondrially targeted Bcl-2 induces apoptosis, whereas transient expression of endoplasmic reticulum-targeted Bcl-2 is protective against Bax-induced cell death. J. Biol. Chem. 276, 44117-44128.
78. Wang, X. (2001). The expanding role of mitochondria in apoptosis. Genes Dev. 15, 2922-2933.
79. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B. and Korsmeyer, S. J. (2001). Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730.
80. Winslow, M. M., Neilson, J. R. and Crabtree, G. R. (2003). Calcium signaling in lymphocytes. Curr. Opin. Immunol. 15, 299-307.
81. Wolter, K. G., Hsu, Y. T., Smith, C. L., Nechushtan, A., Xi, X. G. and Youle, R. J. (1997). Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139, 1281-1292.
82. Wyllie, A. H., Kerr, J. F. and Currie, A. R. (1980). Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251-306.
83. Zhu, W., Cowie, A., Wasfy, G. W., Penn, L. Z., Leber, B. and Andrews, D. W. (1996). Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J. 15, 4130-4141.
84. Zong, W. X., Li, C., Hatzivassiliou, G., Lindsten, T., Yu, Q. C., Yuan, J. and Thompson, C. B. (2003). Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 162, 59-69.