Voltage-dependent anion channels (VDAC) in the plasma membrane play a critical role in apoptosis in differentiated hippocampal neurons but not in neural stem cells

Cell Cycle

Volumn 7, Issue 20, 2008, Pages 3225-3234

  Akanda, Nesar ^a,b   Tofighi, Roshan ^b   Brask, Johan ^a   Tamm, Christoffer ^b   Elinder, Fredrik ^a   Ceccatelli, Sandra ^b  

^a LINKÖPING UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Apoptosis; Hippocampal neurons; Neural stem cells; Patch clamp; Single channel recordings; Sodium channels; VDAC

Indexed keywords

AMILORIDE; ANTIBODY; CHLORIDE ION; CYTOCHROME B5 REDUCTASE; POTASSIUM ION; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL LINE; CELL MEMBRANE; CHLORIDE TRANSPORT; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; HIPPOCAMPUS; NERVE CELL; NERVE CELL CULTURE; NEURAL STEM CELL; NONHUMAN; POTASSIUM TRANSPORT; PROTEIN FUNCTION; RAT;

EID: 54049158483     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.7.20.6831     Document Type: Article

References (40)

1. Yuan J, 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; 75:641-52.
2. Barbiero G, Duranti F, Bonelli G, Amenta JS, Baccino FM. Intracellular ionic variations in the apoptotic death of L cells by inhibitors of cell cycle progression. Exp Cell Res 1995; 217:410-8.
3. Benson RS, Heer S, Dive C, Watson AJ. Characterization of cell volume loss in CEM-C7A cells during dexamethasone-induced apoptosis. Am J Physiol 1996; 270:1190-203.
4. + efflux in the activation of apoptosis. The Journal of biological chemistry 1997; 272:32436-42.
5. Yu SP, Yeh CH, Sensi SL, Gwag BJ, Canzoniero LM, Farhangrazi ZS, Ying HS, Tian M, Dugan LL, Choi DW. Mediation of neuronal apoptosis by enhancement of outward potassium current. Science 1997; 278:114-7.
6. Colom LV, Diaz ME, Beers DR, Neely A, Xie WJ, Appel SH. Role of potassium channels in amyloid-induced cell death. J Neurochem 1998; 70:1925-34.
7. + channel mediates apoptosis of myeloblastic leukemia cells. The Journal of biological chemistry 1999; 274:3678-85.
8. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y. Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci USA 2000; 97:9487-92.
9. + inhibit cytochrome c-dependent formation of the apoptosome. The Journal of biological chemistry 2001; 276:41985-90.
10. + suppresses the activation of apoptosis in lymphocytes. The Journal of biological chemistry 1997; 272:30567-76.
11. Elinder F, Akanda N, Tofighi R, Shimizu S, Tsujimoto Y, Orrenius S, Ceccatelli S. Opening of plasma membrane voltage-dependent anion channels (VDAC) precedes caspase activation in neuronal apoptosis induced by toxic stimuli. Cell Death Differ 2005; 12:1134-40.
12. Baker MA, Lane DJ, Ly JD, De Pinto V, Lawen A. VDAC1 is a transplasma membrane NADH-ferricyanide reductase. The Journal of biological chemistry 2004; 279:4811-9.
13. Akanda N, Elinder F. Biophysical properties of the apoptosis-inducing plasma membrane voltage-dependent anion channel. Biophysical journal 2006; 90:4405-17.
14. Colombini M, Blachly-Dyson E, Forte M. VDAC, a channel in the outer mitochondrial membrane. Ion Channels 1996; 4:169-202.
15. Thinnes FP, Gotz H, Kayser H, Benz R, Schmidt WE, Kratzin HD, Hilschmann N. [Identification of human porins I. Purification of a porin from human B-lymphocytes (Porin 31HL) and the topochemical proof of its expression on the plasmalemma of the progenitor cell]. Biol Chem Hoppe Seyler 1989; 370:1253-64.
16. Jalonen T. Single-channel characteristics of the large-conductance anion channel in rat cortical astrocytes in primary culture. Glia 1993; 9:227-37.
17. Bathori G, Szabo I, Schmehl I, Tombola F, Messina A, De Pinto V, Zoratti M. Novel aspects of the electrophysiology of mitochondrial porin. Biochem Biophys Res Commun 1998; 243:258-63.
18. Guibert B, Dermietzel R, Siemen D. Large conductance channel in plasma membranes of astrocytic cells is functionally related to mitochondrial VDAC-channels. Int J Biochem Cell Biol 1998; 30:379-91.
19. Bathori G, Parolini I, Szabo I, Tombola F, Messina A, Oliva M, Sargiacomo M, De Pinto V, Zoratti M. Extramitochondrial porin: facts and hypotheses. Journal of bioenergetics and biomembranes 2000; 32:79-89.
20. Garty H, Palmer LG. Epithelial sodium channels: function, structure and regulation. Physiological reviews 1997; 77:359-96.
21. Kellenberger S, Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiological reviews 2002; 82:735-67.
22. Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacological reviews 2005; 57:397-409.
23. Colombini M. A candidate for the permeability pathway of the outer mitochondrial membrane. Nature 1979; 279:643-5.
24. Shimizu S, Matsuoka Y, Shinohara Y, Yoneda Y, Tsujimoto Y. Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J Cell Biol 2001; 152:237-50.
25. - currents in C1300 neuroblastoma cells. The Journal of biological chemistry 2003; 278:33284-9.
26. Mannella CA. Minireview: on the structure and gating mechanism of the mitochondrial channel, VDAC. Journal of bioenergetics and biomembranes 1997; 29:525-31.
27. Sabirov RZ, Okada Y. Wide nanoscopic pore of maxi-anion channel suits its function as an ATP-conductive pathway. Biophysical journal 2004; 87:1672-85.
28. Rostovtseva T, Colombini M. VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function. Biophysical journal 1997; 72:1954-62.
29. Sabirov RZ, Okada Y. ATP-conducting maxi-anion channel: a new player in stress-sensory transduction. The Japanese journal of physiology 2004; 54:7-14.
30. Sabirov RZ, Sheiko T, Liu H, Deng D, Okada Y, Craigen WJ. Genetic demonstration that the plasma membrane maxianion channel and voltage-dependent anion channels are unrelated proteins. The Journal of biological chemistry 2006; 281:1897-904.
31. Marin R, Ramirez CM, Gonzalez M, Gonzalez-Munoz E, Zorzano A, Camps M, Alonso R, Diaz M. Voltage-dependent anion channel (VDAC) participates in amyloid beta-induced toxicity and interacts with plasma membrane estrogen receptor alpha in septal and hippocampal neurons. Molecular membrane biology 2007; 24:148-60.
32. Canessa CM, Horisberger JD, Rossier BC. Epithelial sodium channel related to proteins involved in neurodegeneration. Nature 1993; 361:467-70.
33. Waldmann R, Lazdunski M. H(+)-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Current opinion in neurobiology 1998; 8:418-24.
34. Chalfie M, Wolinsky E. The identification and suppression of inherited neurodegeneration in Caenorhabditis elegans. Nature 1990; 345:410-6.
35. Driscoll M, Chalfie M. The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature 1991; 349:588-93.
36. Waldmann R, Champigny G, Voilley N, Lauritzen I, Lazdunski M. The mammalian degenerin MDEG, an amiloride-sensitive cation channel activated by mutations causing neurodegeneration in Caenorhabditis elegans. The Journal of biological chemistry 1996; 271:10433-6.
37. Bottenstein JE, Sato GH. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci USA 1979; 76:514-7.
38. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995; 376:37-43.
39. Gorman AM, Hirt UA, Orrenius S, Ceccatelli S. Dexamethasone pre-treatment interferes with apoptotic death in glioma cells. Neuroscience 2000; 96:417-25.
40. Norfleet AM, Thomas ML, Gametchu B, Watson CS. Estrogen receptor-alpha detected on the plasma membrane of aldehyde-fixed GH3/B6/F10 rat pituitary tumor cells by enzyme-linked immunocytochemistry. Endocrinology 1999; 140:3805-14.