The role of calcium in VDAC1 oligomerization and mitochondria-mediated apoptosis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 7, 2013, Pages 1745-1754

  Keinan, Nurit ^a   Pahima, Hadas ^a   Ben Hail, Danya ^a   Shoshan Barmatz, Varda ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Apoptosis; Ca2+; Mitochondria; Oligomerization; VDAC1

Indexed keywords

ARSENIC TRIOXIDE; CALCIUM; CISPLATIN; CYTOCHROME C; IONOMYCIN; SELENITE; THAPSIGARGIN; VOLTAGE DEPENDENT ANION CHANNEL 1;

APOPTOSIS; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENZYME RELEASE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR MECHANICS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

APOPTOSIS; CALCIMYCIN; CALCIUM; CALCIUM IONOPHORES; ENZYME INHIBITORS; HELA CELLS; HUMANS; IMMUNOBLOTTING; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PROTEIN MULTIMERIZATION; THAPSIGARGIN; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 84878225780     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.03.017     Document Type: Article

References (87)

1. Gunter T.E., Buntinas L., Sparagna G., Eliseev R., Gunter K. Mitochondrial calcium transport: mechanisms and functions. Cell Calcium 2000, 28:285-296.
2. + exchanger in the regulation of oxidative phosphorylation in isolated heart mitochondria. J. Biol. Chem. 1993, 268:938-947.
3. + uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ. Res. 2006, 99:172-182.
4. + as a key regulator of cell life and death. Cell Death Differ. 2007, 14:1267-1274.
5. Mattson M.P., Chan S.L. Calcium orchestrates apoptosis. Nat. Cell Biol. 2003, 5:1041-1043.
6. Rimessi A., Giorgi C., Pinton P., Rizzuto R. The versatility of mitochondrial calcium signals: from stimulation of cell metabolism to induction of cell death. Biochim. Biophys. Acta 2008, 1777:808-816.
7. + exchanger increases mitochondrial metabolism and potentiates glucose-stimulated insulin secretion in rat pancreatic islets. Diabetes 2003, 52:965-973.
8. Baughman J.M., Perocchi F., Girgis H.S., Plovanich M., Belcher-Timme C.A., Sancak Y., Bao X.R., Strittmatter L., Goldberger O., Bogorad R.L., Koteliansky V., Mootha V.K. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011, 476:341-345.
9. De Stefani D., Raffaello A., Teardo E., Szabo I., Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011, 476:336-340.
10. Santo-Domingo J., Demaurex N. Calcium uptake mechanisms of mitochondria. Biochim. Biophys. Acta 2010, 1797:907-912.
11. + antiporter. Science 2009, 326:144-147.
12. Nowikovsky K., Pozzan T., Rizzuto R., Scorrano L., Bernardi P. Perspectives on: SGP symposium on mitochondrial physiology and medicine: the pathophysiology of LETM1. J. Gen. Physiol. 2012, 139:445-454.
13. 2+ exchange. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:436-441.
14. Gincel D., Zaid H., Shoshan-Barmatz V. Calcium binding and translocation by the voltage-dependent anion channel: a possible regulatory mechanism in mitochondrial function. Biochem. J. 2001, 358:147-155.
15. 2+ microdomains to mitochondria. J. Cell Biol. 2002, 159:613-624.
16. Tan W., Colombini M. VDAC closure increases calcium ion flux. Biochim. Biophys. Acta 2007, 1768:2510-2515.
17. Israelson A., Zaid H., Abu-Hamad S., Nahon E., Shoshan-Barmatz V. Mapping the ruthenium red-binding site of the voltage-dependent anion channel-1. Cell Calcium 2008, 43:196-204.
18. Shoshan-Barmatz V., Gincel D. The voltage-dependent anion channel: characterization, modulation, and role in mitochondrial function in cell life and death. Cell Biochem. Biophys. 2003, 39:279-292.
19. Shoshan-Barmatz V., De Pinto V., Zweckstetter M., Raviv Z., Keinan N., Arbel N. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol. Aspects Med. 2010, 31:227-285.
20. Israelson A., Arzoine L., Abu-hamad S., Khodorkovsky V., Shoshan-Barmatz V. A photoactivable probe for calcium binding proteins. Chem. Biol. 2005, 12:1169-1178.
21. 2+-dependent control of the permeability properties of the mitochondrial outer membrane and voltage-dependent anion-selective channel (VDAC). J. Biol. Chem. 2006, 281:17347-17358.
22. Gincel D., Vardi N., Shoshan-Barmatz V. Retinal voltage-dependent anion channel: characterization and cellular localization. Invest. Ophthalmol. Vis. Sci. 2002, 43:2097-2104.
23. 2+-binding sites. Cell Calcium 2007, 41:235-244.
24. Zaid H., Abu-Hamad S., Israelson A., Nathan I., Shoshan-Barmatz V. The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death Differ. 2005, 12:751-760.
25. Abu-Hamad S., Sivan S., Shoshan-Barmatz V. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5787-5792.
26. 2+ depletion and cytochrome c release. Biochem. Biophys. Res. Commun. 2003, 303:1073-1079.
27. 2+ release mediates ursolic acid-induced apoptosis in human leukemic HL-60 cells. Int. J. Cancer 1997, 73:725-728.
28. 2+) in microcystin-induced mitochondrial permeability transition in rat hepatocytes. Biochem. Biophys. Res. Commun. 2001, 285:1155-1161.
29. Shoshan-Barmatz V., Keinan N., Abu-Hamad S., Tyomkin D., Aram L. Apoptosis is regulated by the VDAC1 N-terminal region and by VDAC oligomerization: release of cytochrome c, AIF and Smac/Diablo. Biochim. Biophys. Acta 2010, 1797:1281-1291.
30. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 2004, 287:C817-C833.
31. 2+ requirement for mitochondrial permeability transition pore (mPTP) opening. J. Biol. Chem. 2009, 284:20796-20803.
32. Kinnally K.W., Peixoto P.M., Ryu S.Y., Dejean L.M. Is mPTP the gatekeeper for necrosis, apoptosis, or both?. Biochim. Biophys. Acta 2011, 1813:616-622.
33. Tsujimoto Y., Shimizu S. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 2007, 12:835-840.
34. Csordas G., Varnai P., Golenar T., Roy S., Purkins G., Schneider T.G., Balla T., Hajnoczky G. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol. Cell 2010, 39:121-132.
35. Grimm S. The ER-mitochondria interface: the social network of cell death. Biochim. Biophys. Acta 2012, 1823:327-334.
36. 2+) transfer from the ER to mitochondria: when, how and why. Biochim. Biophys. Acta 2009, 1787:1342-1351.
37. Hajnoczky G., Davies E., Madesh M. Calcium signaling and apoptosis. Biochem. Biophys. Res. Commun. 2003, 304:445-454.
38. Shoshan-Barmatz V., Israelson A. The voltage-dependent anion channel in endoplasmic/sarcoplasmic reticulum: characterization, modulation and possible function. J. Membr. Biol. 2005, 204:57-66.
39. Shoshan-Barmatz V., Zalk R., Gincel D., Vardi N. Cellular and sub-cellular localization of VDAC in cerebellum and its function in ER-mitochondria cross-talk. Biochim. Biophys. Acta 2004, 1657:105-114.
40. 2+ signals to mitochondria. Cell Death Differ. 2012, 19:267-273.
41. Abu-Hamad S., Arbel N., Calo D., Arzoine L., Israelson A., Keinan N., Ben-Romano R., Friedman O., Shoshan-Barmatz V. The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins. J. Cell Sci. 2009, 122:1906-1916.
42. Keinan N., Tyomkin D., Shoshan-Barmatz V. Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis. Mol. Cell. Biol. 2010, 30:5698-5709.
43. Shoshan-Barmatz V., Israelson A., Brdiczka D., Sheu S.S. The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death. Curr. Pharm. Des. 2006, 12:2249-2270.
44. Shoshan-Barmatz V., Keinan N., Zaid H. Uncovering the role of VDAC in the regulation of cell life and death. J. Bioenerg. Biomembr. 2008, 40:183-191.
45. Zalk R., Israelson A., Garty E.S., Azoulay-Zohar H., Shoshan-Barmatz V. Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria. Biochem. J. 2005, 386:73-83.
46. Deniaud A., Sharaf el dein O., Maillier E., Poncet D., Kroemer G., Lemaire C., Brenner C. Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene 2008, 27:285-299.
47. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
48. 2+ dynamics in individual mitochondria in situ. Am. J. Physiol. 1999, 276:C1193-C1204.
49. Muriel M.P., Lambeng N., Darios F., Michel P.P., Hirsch E.C., Agid Y., Ruberg M. Mitochondrial free calcium levels (Rhod-2 fluorescence) and ultrastructural alterations in neuronally differentiated PC12 cells during ceramide-dependent cell death. J. Comp. Neurol. 2000, 426:297-315.
50. 2+) loads. J. Neurosci. Res. 2001, 66:1019-1027.
51. Qian T., Herman B., Lemasters J.J. The mitochondrial permeability transition mediates both necrotic and apoptotic death of hepatocytes exposed to Br-A23187. Toxicol. Appl. Pharmacol. 1999, 154:117-125.
52. +)-ATPase. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:2466-2470.
53. Florea A.M., Busselberg D. Anti-cancer drugs interfere with intracellular calcium signaling. Neurotoxicology 2009, 30:803-810.
54. Li J.J., Tang Q., Li Y., Hu B.R., Ming Z.Y., Fu Q., Qian J.Q., Xiang J.Z. Role of oxidative stress in the apoptosis of hepatocellular carcinoma induced by combination of arsenic trioxide and ascorbic acid. Acta Pharmacol. Sin. Aug 2006, 27(8):1078-1084.
55. Bustamante J., Nutt L., Orrenius S., Gogvadze V. Arsenic stimulates release of cytochrome c from isolated mitochondria via induction of mitochondrial permeability transition. Toxicol. Appl. Pharmacol. Sep 1 2005, 207(2 Suppl.):110-116. (Review).
56. Rana S.V. Metals and apoptosis: recent developments. J. Trace Elem. Med. Biol. 2008, 22:262-284.
57. Florea A.M., Yamoah E.N., Dopp E. Intracellular calcium disturbances induced by arsenic and its methylated derivatives in relation to genomic damage and apoptosis induction. Environ. Health Perspect. Jun 2005, 113(6):659-664. (Review).
58. Lam M., Dubyak G., Distelhorst C.W. Effect of glucocorticosteroid treatment on intracellular calcium homeostasis in mouse lymphoma cells. Mol. Endocrinol. 1993, 7:686-693.
59. Feng X.Q., You Y., Xiao J., Zou P. Thapsigargin-induced apoptosis of K562 cells and its mechanism. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2006, 14:25-30.
60. Zhang H.N., Zhou J.G., Qiu Q.Y., Ren J.L., Guan Y.Y. ClC-3 chloride channel prevents apoptosis induced by thapsigargin in PC12 cells. Apoptosis 2006, 11:327-336.
61. Chaudhari A.A., Seol J.W., Lee Y.J., Seol D.W., Park S.Y. Hypoxia protects articular chondrocytes from thapsigargin-induced apoptosis. Biochem. Biophys. Res. Commun. 2009, 381:513-517.
62. Matsumoto H., Sasaki Y. Staurosporine, a protein kinase C inhibitor interferes with proliferation of arterial smooth muscle cells. Biochem. Biophys. Res. Commun. 1989, 158:105-109.
63. Hirota J., Furuichi T., Mikoshiba K. Inositol 1,4,5-trisphosphate receptor type 1 is a substrate for caspase-3 and is cleaved during apoptosis in a caspase-3-dependent manner. J. Biol. Chem. 1999, 274:34433-34437.
64. Gil J., Almeida S., Oliveira C.R., Rego A.C. Cytosolic and mitochondrial ROS in staurosporine-induced retinal cell apoptosis. Free Radic. Biol. Med. 2003, 35:1500-1514.
65. 2+ is required for the activation of mitochondrial calpain to release AIF during cell death. Cell Death Differ. 2008, 15:1857-1864.
66. Xiang N., Zhao R., Zhong W. Sodium selenite induces apoptosis by generation of superoxide via the mitochondrial-dependent pathway in human prostate cancer cells. Cancer Chemother. Pharmacol. 2009, 63:351-362.
67. Wang H., Yang X., Zhang Z., Xu H. Both calcium and ROS as common signals mediate Na(2)SeO(3)-induced apoptosis in SW480 human colonic carcinoma cells. J. Inorg. Biochem. 2003, 97:221-230.
68. Shidoji Y., Hayashi K., Komura S., Ohishi N., Yagi K. Loss of molecular interaction between cytochrome c and cardiolipin due to lipid peroxidation. Biochem. Biophys. Res. Commun. 1999, 264:343-347.
69. 2+ on cardiolipin-cytochrome c interaction. Biochim. Biophys. Acta 2006, 1760:1827-1830.
70. Liu J., Weiss A., Durrant D., Chi N.W., Lee R.M. The cardiolipin-binding domain of Bid affects mitochondrial respiration and enhances cytochrome c release. Apoptosis 2004, 9:533-541.
71. 2+ increases transcriptional activity and mRNA stability. J. Biol. Chem. 1992, 267:20465-20470.
72. 2+-operated transcriptional networks: molecular mechanisms and in vivo models. Physiol. Rev. 2008, 88:421-449.
73. Deisseroth K., Mermelstein P.G., Xia H., Tsien R.W. Signaling from synapse to nucleus: the logic behind the mechanisms. Curr. Opin. Neurobiol. 2003, 13:354-365.
74. 2+)-dependent transcription. Curr. Opin. Neurobiol. 2001, 11:312-319.
75. West A.E., Chen W.G., Dalva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., Takasu M.A., Tao X., Greenberg M.E. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:11024-11031.
76. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 2000, 1:11-21.
77. Carafoli E. Calcium signaling: a tale for all seasons. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1115-1122.
78. Godbole A., Varghese J., Sarin A., Mathew M.K. VDAC is a conserved element of death pathways in plant and animal systems. Biochim. Biophys. Acta 2003, 1642:87-96.
79. Lu A.J., Dong C.W., Du C.S., Zhang Q.Y. Characterization and expression analysis of Paralichthys olivaceus voltage-dependent anion channel (VDAC) gene in response to virus infection. Fish Shellfish Immunol. 2007, 23:601-613.
80. Ghosh T., Pandey N., Maitra A., Brahmachari S.K., Pillai B. A role for voltage-dependent anion channel Vdac1 in polyglutamine-mediated neuronal cell death. PLoS One 2007, 2:e1170.
81. Castagna A., Antonioli P., Astner H., Hamdan M., Righetti S.C., Perego P., Zunino F., Righetti P.G. A proteomic approach to cisplatin resistance in the cervix squamous cell carcinoma cell line A431. Proteomics 2004, 4:3246-3267.
82. Cheng S.L., Liu R.H., Sheu J.N., Chen S.T., Sinchaikul S., Tsay G.J. Toxicogenomics of A375 human malignant melanoma cells treated with arbutin. J. Biomed. Sci. 2007, 14:87-105.
83. Jiang N., Kham S.K., Koh G.S., Suang Lim J.Y., Ariffin H., Chew F.T., Yeoh A.E. Identification of prognostic protein biomarkers in childhood acute lymphoblastic leukemia (ALL). J. Proteomics 2011, 74:843-857.
84. Jung J.Y., Han C.R., Jeong Y.J., Kim H.J., Lim H.S., Lee K.H., Park H.O., Oh W.M., Kim S.H., Kim W.J. Epigallocatechin gallate inhibits nitric oxide-induced apoptosis in rat PC12 cells. Neurosci. Lett. 2007, 411:222-227.
85. Moin S.M., Panteva M., Jameel S. The hepatitis E virus Orf3 protein protects cells from mitochondrial depolarization and death. J. Biol. Chem. 2007, 282:21124-21133.
86. Nawarak J., Huang-Liu R., Kao S.H., Liao H.H., Sinchaikul S., Chen S.T., Cheng S.L. Proteomics analysis of A375 human malignant melanoma cells in response to arbutin treatment. Biochim. Biophys. Acta 2009, 1794:159-167.
87. Voehringer D.W., Hirschberg D.L., Xiao J., Lu Q., Roederer M., Lock C.B., Herzenberg L.A., Steinman L., Herzenberg L.A. Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:2680-2685.