Share This Article:

Involvement of mitochondrial swelling in cytochrome c release from mitochondria treated with calcium and Alloxan

Full-Text HTML Download Download as PDF (Size:278KB) PP. 10-18
DOI: 10.4236/jbpc.2011.21002    5,625 Downloads   10,992 Views   Citations

ABSTRACT

An early event in the induction of apoptosis is cytochrome c (Cyt c) release from mitochondria. We investigated the involvement of mitochonrial permeability transition (MPT) and mitochondrial swelling in Cyt c release from mitochondria treated with alloxan and/or calcium (Ca2+). When mitochondria were treated with a high concentration of Ca2+. alone or Ca2+. with alloxan (alloxan-Ca2+), the MPT was accompanied by mitochondrial swelling and the release of Cyt c. Cyclosporin A prevented the induction of MPT but only slightly decreased the release of Cyt c. High molecular weight polyethylene glycol almost completely inhibited MPT-dependent osmotic mitochondrial swelling and Cyt c release. However, MPT-independent mitochondrial swelling and Cyt c release induced by exogenous K+. were inhibited by the high molecular weight polyethylene glycol. Ruthenium red strongly decreased the amount of Cyt c released. These results suggest that mitochondrial swelling but not MPT is necessary for Cyt c release induced by Ca2+ alone or alloxan and Ca2+.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Ichimura, T. , Ito, M. , Takahashi, K. , Oyama, K. and Sakurai, K. (2011) Involvement of mitochondrial swelling in cytochrome c release from mitochondria treated with calcium and Alloxan. Journal of Biophysical Chemistry, 2, 10-18. doi: 10.4236/jbpc.2011.21002.

References

[1] Brookes, P.S., Yoon, Y., Robotham, J.L., Anders, M.W. and Sheu, S.S. (2004) Calcium, ATP, and ROS: A mitochondrial love-hate triangle. American Journal of Physiology. Cell Physiology, 287(4), c817-c833. doi:10.1152/ajpcell.00139.2004
[2] Passarella, S., Atlante, A., Valenti, D. and Bari, L.D. (2003) The role of mitochondrial transport in energy metabolism. Mitochondrion, 2(5), 319-343. doi:10.1016/S1567-7249(03)00008-4
[3] Gunter, T. E., Yule, D. I., Gunter, K. K., Eliseev, R. A. and Salter, J. D., (2004) Calcium and mitochondria. FEBS letters, 567(1), 96-102. doi:10.1016/j.febslet.2004.03.071
[4] Danial, N.N. and Korsmeyer, S.J., (2004) Cell death: Critical control points. Cell, 116(2), 205-219.
[5] Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. and Wang, X., (1997) Cytochrome c and dATP-dependent formation of Apaf-1/ caspase-9 complex initiates an apoptotic protease cascade. Cell, 91(4), 479-489.
[6] Sparagna, G.C., Hickson-Bick, D.L., Buja, LM. and McMillin, J.B. (2000) A metabolic role for mitochondria in palmitate-induced cardiac myocyte apoptosis. American Journal of Physiology. Heart and Circulatory Physiology, 279(5), H2124-H2132.
[7] Sakurai, K., Katoh, M., Someno, K. and Fujimoto, Y. (2001) Apoptosis and mitochondrial damage in INS-1 cells treated with alloxan. Biological & Pharmaceutical Bulletin, 24(8), 876-882. doi:10.1248/bpb.24.876
[8] Sakurai, K., Katoh, M. and Fujimoto, Y. (2001) Alloxan-induced mitochondrial permeability transition triggered by calcium, thiol oxidation, and matrix ATP. The Journal of Biological Chemistry, 276(29), 26942-26946. doi:10.1074/jbc.M102029200
[9] Kumarswamy, R. and Chandna, S. (2009) Putative partners in Bax mediated cytochrome-c release: ANT, CypD, VDAC or none of them? Mitochondrion, 9(1), 1-8. doi:10.1016/j.mito.2008.10.003
[10] Tsujimoto, Y., Nakagawa, T. and Shimizu, S. (2006) Mitochondrial membrane permeability transition and cell death. Biochimica et Biophysica Acta, 1757(9-10), 1297-1300. doi:10.1016/j.bbabio.2006.03.017
[11] Ott, M., Robertson, J.D., Gogvadze, V., Zhivotovsky, B. and Orrenius, S. (2002) Cytochrome c release from mitochondria proceeds by a two-step process. Proceedings of the National Academy of Sciences of the United States of America, 99(3), 1259-1263. doi:10.1073/pnas.241655498
[12] Petrosillo, G., Ruggiero, F.M. and Paradies, G. (2003) Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria. The FASEB Journal, 17(15), 2202-2208. doi:10.1096/fj.03-0012com
[13] Tsujimoto, Y. and Shimizu, S. (2000) VDAC regulation by the Bcl-2 family of proteins. Cell Death and Differentiation, 7(12), 1174-1181. doi:10.1038/sj.cdd.4400780
[14] Garrido, C., Galluzzi, L., Brunet, M., Puig, P. E., Didelot, C. and Kroemer, G. (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death and Differentiation, 13(9), 1423-1433. doi:10.1038/sj.cdd.4401950
[15] Brustovetsky, N., Brustovetsky, T., Jemmerson, R. and Dubinsky, J.M. (2002) Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. Journal of Neurochemistry, 80(2), 207-218. doi:10.1046/j.0022-3042.2001.00671.x
[16] Petit, P.X., Goubern, M., Diolez, P., Susin, S.A., Zamzami, N. and Kroemer, G. (1998) Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: the impact of irreversible permeability transition. The FASEB Journal, 426(1), 111-116.
[17] Doran, E. and Halestrap, A.P. (2000) Cytochrome c release from isolated rat liver mitochondria can occur independently of outer-membrane rupture: Possible role of contact sites. The Biochemical Journal, 348(2), 343-350. doi:10.1042/0264-6021:3480343
[18] Jürgensmeier, J.M., Xie, Z., Deveraux, Q., Ellerby, L., Bredesen, D. and Reed, J.C. (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proceedings of the National Academy of Sciences of the United States of America, 95(9), 4997-5002. doi:10.1073/pnas.95.9.4997
[19] Shimizu, S., Ide, T., Yanagida, T. and Tsujimoto, Y. (2000) Electrophysiological study of a novel large pore formed by Bax and the voltage-dependent anion channel that is permeable to cytochrome c. The Journal of Biological Chemistry, 275(16), 12321-12325. doi:10.1074/jbc.275.16.12321
[20] Kim, T.H., Zhao, Y., Barber, M.J., Kuharsky, D.K. and Yin, X.M. (2000) Bid-induced cytochrome c release is mediated by a pathway independent of mitochondrial permeability transition pore and Bax. The Journal of Biological Chemistry, 275(50), 39474-39481. doi:10.1074/jbc.M003370200
[21] Uren, R.T., Dewson, G., Bonzon, C., Lithgow, T., Newmeyer, D.D. and Kluck, R.M. (2005) Mitochondrial release of pro-apoptotic proteins: electrostatic interactions can hold cytochrome c but not Smac/DIABLO to mitochondrial membranes. The Journal of Biological Chemistry, 280(3), 2266-2274. doi:10.1074/jbc.M411106200
[22] Haworth, R.A. and Hunter, D.R. (1979) The Ca2+-induced membrane transition in mitochondria. II. Nature of the Ca2+ trigger site. Archives of Biochemistry and Biophysics, 195(2), 460-467. doi:10.1016/0003-9861(79)90372-2
[23] Johnston, J.D. and Brand, M.D. (1990) The mechanism of Ca2+ stimulation of citrulline and N-acetylglutamate synthesis by mitochondria. Biochimica et Biophysica Acta, 1033(1), 85-90.
[24] Paola, M.D. and Lorusso, M. (2006) Interaction of free fatty acids with mitochondria: Coupling, uncoupling and permeability transition. Biochimica et Biophysica Acta, 1757(9-10), 1330-1337. doi:10.1016/j.bbabio.2006.03.024
[25] Mironova, G.D., Gritsenko, E., Gateau-Roesch, O., Levrat, C., Agafonov, A., Belosludtsev, K., Prigent, A. F., Muntean, D., Dubois, M. and Ovize, M. (2004) Formation of palmitic acid/Ca2+ complexes in the mitochondrial membrane: a possible role in the cyclosporin-insensitive permeability transition. Journal of Bioenergetics and Biomembranes, 36(2), 171-178. doi:10.1023/B:JOBB.0000023620.42653.b7
[26] Halestrap, A.P., Woodfield, K.Y. and Connern, C.P. (1997) Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. The Journal of Biological Chemistry, 272(6), 3346-3354. doi:10.1074/jbc.272.6.3346
[27] Andreu, G.L.P., Delgado, R., Velho, J.A., Curti, C. and Vercesi, A.E. (2005) Mangiferin, a natural occurring glucosyl xanthone, increases susceptibility of rat liver mitochondria to calcium-induced permeability transition. Archives of Biochemistry and Biophysics, 439(2), 184-193. doi:10.1016/j.abb.2005.05.015
[28] Brustovetsky, N. and Dubinsky, J.M. (2000) Limitations of cyclosporin A inhibition of the permeability transition in CNS mitochondria. The Journal of Neuroscience, 20(22), 8229-8237.
[29] Gunter, T.E., Buntinas, L., Sparagna, G.C. and Gunter, K.K. (1998) The Ca2+ transport mechanisms of mitochondria and Ca2+ uptake from physiological-type Ca2+ transients. Biochimica et Biophysica Acta, 1366(1-2), 5-15. doi:10.1016/S0005-2728(98)00117-0
[30] Armstrong, J.S., Yang, H., Duan, W. and Whiteman, M. (2004) Cytochrome bc(1) regulates the mitochondrial permeability transition by two distinct pathways. The Journal of Biological Chemistry, 279(48), 50420-50428. doi:10.1074/jbc.M408882200
[31] Sakurai, K., Stoyanovsky, D.A., Fujimoto, Y. and Cederbaum, A.I. (2000) Mitochondrial permeability transition induced by 1-hydroxyethyl radical. Free Radical Biology & Medicine, 28(2), 273-280. doi:10.1016/S0891-5849(99)00236-1
[32] Halestrap, A.P., Quinlan, P.T., Whipps, D.E. and Armston, A.E. (1986) Regulation of the mitochondrial matrix volume in vivo and in vitro. The role of calcium. The Biochemical Journal, 236(3), 779-787.
[33] Korge, P., Honda, H.M. and Weiss, J.N. (2005) K+-dependent regulation of matrix volume improves mitochondrial function under conditions mimicking ischemia-reperfusion. American Journal of Physiology. Heart and Circulatory Physiology, 289(1), H66-H77. doi:10.1152/ajpheart.01296.2004
[34] Crouser, E.D., Gadd, M.E., Julian, M.W., Huff, J.E., Broekemeier, K.M., Robbins, K.A. and Pfeiffer, D.R. (2003) Quantitation of cytochrome c release from rat liver mitochondria. Analytical Biochemistry, 317(1), 67-75. doi:10.1016/S0003-2697(03)00044-7
[35] Colombini, M. (1980) Structure and mode of action of a voltage dependent anion-selective channel (VDAC) located in the outer mitochondrial membrane. Annals of the New York Academy of Sciences, 341, 552-63. doi:10.1111/j.1749-6632.1980.tb47198.x
[36] Zalman, L.S., Nikaido, H. and Kagawa, Y. (1980) Mitochondrial outer membrane contains a protein producing nonspecific diffusion channels. The Journal of Biological Chemistry. 255(5), 1771-1774.
[37] Shoshan-Barmatz, V., Israelson, A., Brdiczka, D. and Sheu, S.S. (2006) The voltage-dependent anion channel (VDAC): Function in intracellular signalling, cell life and cell death. Current Pharmaceutical Design, 12(18), 2249-2270. doi:10.2174/138161206777585111
[38] Gincel, D., Zaid, H. and Shoshan-Barmatz, V. (2001) Calcium binding and translocation by the voltage-dependent anion channel: A possible regulatory mechanism in mitochondrial function. The Biochemical Journal, 358(Pt1), 147-155. doi:10.1042/0264-6021:3580147
[39] Israelson, A., Abu-Hamad, S., Zaid, H., Nahon, E. and Shoshan-Barmatz, V. (2007) Localization of the voltage-dependent anion channel-1 Ca2+-binding sites. Cell Calcium, 41(3), 235-244. doi:10.1016/j.ceca.2006.06.005
[40] Tikunov, A., Johnson, C.B., Pediaditakis, P., Markevich, N., Macdonald, J.M., Lemasters, J.J. and Holmuhamedov, E. (2010) Closure of VDAC causes oxidative stress and accelerates the Ca(2+)-induced mitochondrial permeability transition in rat liver mitochondria. Archives of Biochemistry and Biophysics, 495(2), 174-181. doi:10.1016/j.abb.2010.01.008
[41] Gómez Dumm, C.L., Atwater, I., Epstein, P.N. and Gagliardino, J.J. (1994) Quantitative immunocytochemical study of islet cell populations in diabetic calmodulin-transgenic mice. Virchows Archiv, 425(1), 73-77.
[42] Epstein, P.N., Ribar, T.J., Decker, G.L., Yaney, G. and Means, A.R. (1992) Elevated beta-cell calmodulin produces a unique insulin secretory defect in transgenic mice. Endocrinology, 130(3), 1387-1393. doi:10.1210/en.130.3.1387
[43] Gwiazda, K.S., Yang, T.L., Lin, Y. and Johnson, J.D. (2009) Effects of palmitate on ER and cytosolic Ca2+ homeostasis in beta-cells. American Journal of Physiology. Endocrinology and Metabolism, 296(4), E690-E701. doi:10.1152/ajpendo.90525.2008

  
comments powered by Disqus

Copyright © 2018 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.