Voltage-dependent anion channels: The wizard of the mitochondrial outer membrane

Biological Chemistry

Volumn 395, Issue 12, 2014, Pages 1435-1442

  Mertins, Barbara ^a   Psakis, Georgios ^b   Essen, Lars Oliver ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF HUDDERSFIELD   (United Kingdom)

Author keywords

Eukaryotic porin structure; Intrinsic apoptotic pathway; Ion channel gating; Membrane protein phylogeny; Structural plasticity; barrel topology

Indexed keywords

VOLTAGE DEPENDENT ANION CHANNEL; CARRIER PROTEIN; ION;

APOPTOSIS; CONFERENCE PAPER; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENDOPLASMIC RETICULUM; GENE DUPLICATION; HUMAN; ION CONDUCTANCE; ION TRANSPORT; LIPID COMPOSITION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL OUTER MEMBRANE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OUTER MEMBRANE; PLANT IMMUNITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; VEGETATIVE GROWTH; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

EUKARYOTA;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; HUMANS; IONS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPS; SIGNAL TRANSDUCTION; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84925854108     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0203     Document Type: Conference Paper

References (43)

1. Arbel, N., Ben-Hail, D., and Shoshan-Barmatz, V. (2012). Mediation of the antiapoptotic activity of Bcl-xL protein upon interaction with VDAC1 protein. J. Biol. Chem. 287, 23152-23161.
2. Bayrhuber, M., Meins, T., Habeck, M., Becker, S., Giller, K., Villinger, S., Vonrhein, C., Griesinger, C., Zweckstetter, M., and Zeth, K. (2008). Structure of the human voltage-dependent anion channel. Proc. Natl. Acad. Sci. USA 105, 15370.
3. Betaneli, V., Petrov, E.P., and Schwille, P. (2012). The role of lipids in VDAC oligomerization. Biophys. J. 102, 523-531.
4. Chaanine, A.H., Gordon, R.E., Kohlbrenner, E., Benard, L., Jeong, D., and Hajjar, R.J. (2013). Potential role of BNIP3 in cardiac remodeling, myocardial stiffness, and endoplasmic reticulum mitochondrial calcium homeostasis in diastolic and systolic heart failure. Circ. Heart Fail 6, 572-583.
5. Choudhary, O.P., Ujwal, R., Kowallis, W., Coalson, R., Abramson, J., and Grabe, M. (2010). The electrostatics of VDAC: implications for selectivity and gating. J. Mol. Biol. 396, 580-592.
6. Colombini, M. (1989). Voltage gating in the mitochondrial channel, VDAC. J. Membrane Biol. 111, 103-111.
7. Colombini, M. (2012). VDAC structure, selectivity, and dynamics. Biochim. Biophys. Acta 1818, 1457-1465.
8. Godbole, A., Dubey, A.K., Reddy, P.S., Udayakumar, M., and Mathew, M.K. (2013). Mitochondrial VDAC and hexokinase together modulate plant programmed cell death. Protoplasma 250, 875-884.
9. Han, D., Antunes, F., Canali, R., Rettori, D., and Cadenas, E. (2003). Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem. 278, 5557-5563.
10. Hiller, S. and Wagner, G. (2009). The role of solution NMR in the structure determinations of VDAC-1 and other membrane proteins. Curr. Opin. Struct. Biol. 19, 396-401.
11. Hiller, S., Garces, R.G., Malia, T.J., Orekhov, V.Y., Colombini, M., and Wagner, G. (2008). Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Sci. STKE 321, 1206.
12. Homblé, F., Krammer, E.-M., and Prévost, M. (2012). Plant VDAC: facts and speculations. Biochim. Biophys. Acta 1818, 1486-1501.
13. Kasimova, M.A., Tarek, M., Shaytan, A.K., Shaitan, K.V., and Delemotte, L. (2014). Voltage-gated ion channel modulation by lipids: Insights from molecular dynamics simulations. Biochim. Biophys. Acta 1838, 1322-1331.
14. Kozuch, J., Weichbrodt, C., Millo, D., Giller, K., Becker, S., Hildebrandt, P., and Steinem, C. (2014). Voltage-dependent structural changes of the membrane-bound anion channel hVDAC1 probed by SEIRA and electrochemical impedance spectroscopy. Phys. Chem. Chem. Phys. 16, 9545-9555.
15. Krammer, E.-M., Saidani, H., Prévost, M., and Homblé, F. (2014). Origin of ion selectivity in Phaseolus coccineus mitochondrial VDAC. Mitochondrion DOI: 10.1016/j.mito.2014.04.03 [epub ahead of print].
16. Lee, K.I., Rui, H., Pastor, R.W., and Im, W. (2011). Brownian dynamics simulations of ion transport through the VDAC. Biophys. J. 100, 611-619.
17. Lemeshko, V.V. (2014). VDAC electronics: 2. A new, anaerobic mechanism of generation of the membrane potentials in mitochondria. Biochim. Biophys. Acta 1838, 1801-1808.
18. Malia, T.J. and Wagner, G. (2007). NMR structural investigation of the mitochondrial outer membrane protein VDAC and its interaction with antiapoptotic Bcl-xL. Biochemistry 46, 514-525.
19. Maurya, S.R. and Mahalakshmi, R. (2013). Modulation of human mitochondrial voltage-dependent anion channel 2 (hVDAC-2) structural stability by cysteine-assisted barrel-lipid interactions. J. Biol. Chem. 288, 25584-25592.
20. Maurya, S.R. and Mahalakshmi, R. (2014). Influence of protein-micelle ratios and cysteine residues on the kinetic stability and unfolding rates of human mitochondrial VDAC-2. PLoS One 9, e87701.
21. Mertins, B., Psakis, G., Grosse, W., Back, K.C., Salisowski, A., Reiss, P., Koert, U., and Essen, L.-O. (2012). Flexibility of the N-terminal mVDAC1 segment controls the channel's gating behavior. PLoS One 7, e47938.
22. Mlayeh, L., Chatkaew, S., Léonetti, M., and Homblé, F. (2010). Modulation of plant mitochondrial VDAC by phytosterols. Biophys. J. 99, 2097-2106.
23. Raemy, E. and Martinou, J.-C. (2013). Involvement of cardiolipin in tBID-induced activation of BAX during apoptosis. Chem. Phys. Lipids 179, 70-74.
24. Raschle, T., Hiller, S., Yu, T.-Y., Rice, A.J., Walz, T., and Wagner, G. (2009). Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs. J. Am. Chem. Soc. 131, 17777-17779.
25. Reina, S., Magrì, A., Lolicato, M., Guarino, F., Impellizzeri, A., Maier, E., Benz, R., Ceccarelli, M., De Pinto, V., and Messina, A. (2013). Deletion of β-strands 9 and 10 converts VDAC1 voltage-dependence in an asymmetrical process. Biochim. Biophys. Acta 1827, 793-805.
26. Rostovtseva, T.K., Antonsson, B., Suzuki, M., Youle, R.J., Colombini, M., and Bezrukov, S.M. (2004). Bid, but not Bax, regulates VDAC channels. J. Biol. Chem. 279, 13575-13583.
27. Rostovtseva, T.K., Kazemi, N., Weinrich, M., and Bezrukov, S.M. (2006). Voltage gating of VDAC is regulated by nonlamellar lipids of mitochondrial membranes. J. Biol. Chem. 281, 37496-37506.
28. Rui, H., Lee, K.I., Pastor, R.W., and Im, W. (2011). Molecular dynamics studies of ion permeation in VDAC. Biophys. J. 100, 602-610.
29. Sampson, M.J., Decker, W.K., Beaudet, A.L., Ruitenbeek, W., Armstrong, D., Hicks, M.J., and Craigen, W.J. (2001). Immotile sperm and infertility in mice lacking mitochondrial voltage-dependent anion channel type 3. J. Biol. Chem. 276, 39206-39212.
30. Schredelseker, J., Paz, A., López, C.J., Altenbach, C., Leung, C.S., Drexler, M.K., Chen, J.-N., Hubbell, W.L., and Abramson, J. (2014). High resolution structure and double electron-electron resonance of the zebrafish voltage-dependent anion channel 2 reveal an oligomeric population. J. Biol. Chem. 289, 12566-12577.
31. Shimizu, S., Matsuoka, Y., Shinohara, Y., Yoneda, Y., and Tsujimoto, Y. (2001). Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J. Cell Biol. 152, 237-250.
32. Shoshan-Barmatz, V. and Ben-Hail, D. (2012). VDAC, a multifunctional mitochondrial protein as a pharmacological target. Mitochondrion 12, 24-34.
33. Shoshan-Barmatz, V., De Pinto, V., Zweckstetter, M., Raviv, Z., Keinan, N., and Arbel, N. (2010). VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol. Aspects Med. 31, 227-285.
34. Takahashi, Y. and Tateda, C. (2013). The functions of voltage-dependent anion channels in plants. Apoptosis 18, 917-924.
35. Tateda, C., Kusano, T., and Takahashi, Y. (2012). The Arabidopsis voltage-dependent anion channel 2 is required for plant growth. Plant Signal Behav. 7, 31-33.
36. Ujwal, R., Cascio, D., Colletier, J.P., Faham, S., Zhang, J., Toro, L., Ping, P., and Abramson, J. (2008). The crystal structure of mouse VDAC1 at 2.3 Å resolution reveals mechanistic insights into metabolite gating. Proc. Natl. Acad. Sci. USA 105, 17742.
37. Veresov, G. V. and Davidovskii, A.I. (2014). Structural insights into proapoptotic signaling mediated by MTCH2, VDAC2, TOM40 and TOM22. Cell Signal 26, 370-382.
38. Vianello, A., Zancani, M., Peresson, C., Petrussa, E., Casolo, V., Krajòáková, J., Patui, S., Braidot, E., and Macrì, F. (2007). Plant mitochondrial pathway leading to programmed cell death. Physiologia Plantarum 129, 242-252.
39. Villinger, S., Briones, R., Giller, K., Zachariae, U., Lange, A., de Groot, B.L., Griesinger, C., Becker, S., and Zweckstetter, M. (2010). Functional dynamics in the voltage-dependent anion channel. Proc. Natl. Acad. Sci. USA 107, 22546-22551.
40. Weeber, E.J., Levy, M., Sampson, M.J., Anflous, K., Armstrong, D.L., Brown, S.E., Sweatt, J.D., and Craigen, W.J. (2002). The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity. J. Biol. Chem. 277, 18891-18897.
41. Wojtkowska, M., Jąkalski, M., Pieńkowska, J.R., Stobienia, O., Karachitos, A., Przytycka, T.M., Weiner, J., Kmita, H., and Makałowski, W. (2012). Phylogenetic analysis of mitochondrial outer membrane &beta-barrel channels. Genom. Biol. Evol. 4, 110-125.
42. Yu, T.-Y., Raschle, T., Hiller, S., and Wagner, G. (2012). Solution NMR spectroscopic characterization of human VDAC-2 in detergent micelles and lipid bilayer nanodiscs. Biochim. Biophys. Acta 1818, 1562-1569.
43. Zachariae, U., Schneider, R., Briones, R., Gattin, Z., Demers, J.-P., Giller, K., Maier, E., Zweckstetter, M., Griesinger, C., and Becker, S. (2012). β-Barrel mobility underlies closure of the voltage-dependent anion channel. Structure 20, 1540-1549.