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Licensed Unlicensed Requires Authentication Published by De Gruyter November 2, 2013

Membranes in motion: mitochondrial dynamics and their role in apoptosis

  • Begoña Ugarte-Uribe

    Begoña Ugarte Uribe performed her PhD in the University of the Basque Country, as part of the Biophysics Unit. She is a postdoc in the group of Prof. Ana García Sáez since september 2012. Dr. Uribe has strong background in Molecular Biology, Biochemistry and Biophysics. She has wide experience in molecular cloning, purification and reconstitution of cytosolic and membrane proteins in model membranes and fluorescence confocal microscopy. Her investigation is focused on the role of Drp1 in mitochondrial dynamics and apoptosis.

    and Ana J. García-Sáez

    Ana J. Garcia-Saez characterized the membrane interacting domains of Bcl-2 proteins during her PhD at the University of Valencia, Spain. Between 2005 and 2009, she worked as a postdoc in the lab of Prof. Petra Schwille, where she focused on the use of advanced microscopy approaches to study membrane dynamics and organization. In 2010, she started her own independent group at the Max Planck Institute for Intelligent Systems and the German Cancer Research Centre in Heidelberg. Since 2013, she is full professor of Biochemistry at the Interfaculty Institute of Biochemstry in Tübingen. Her work focuses on the use on the use of single molecule microscopy and other advanced imaging methods to investigate the mitochondrial alterations during apoptosis.

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From the journal Biological Chemistry

Abstract

Mitochondrial dynamics is crucial for cell survival, development and homeostasis and impairment of these functions leads to neurologic disorders and metabolic diseases. The key components of mitochondrial dynamics have been identified. Mitofusins and OPA1 mediate mitochondrial fusion, whereas Drp1 is responsible for mitochondrial fission. In addition, an interplay between the proteins of the mitochondrial fission/fusion machinery and the Bcl-2 proteins, essential mediators in apoptosis, has been also described. Here, we review the molecular mechanisms regarding mitochondrial dynamics together with their role in apoptosis.


Corresponding author: Ana J. García-Sáez, German Cancer Research Center, BioQuant, Im Neuenheimer Feld 267, D-69120 Heidelberg, Germany; and Max-Planck Institute for Intelligent Systems, Stuttgart, Germany; and Interfaculty Institute for Biochemistry, University of Tübingen, Tübingen, Germany, e-mail:

About the authors

Begoña Ugarte-Uribe

Begoña Ugarte Uribe performed her PhD in the University of the Basque Country, as part of the Biophysics Unit. She is a postdoc in the group of Prof. Ana García Sáez since september 2012. Dr. Uribe has strong background in Molecular Biology, Biochemistry and Biophysics. She has wide experience in molecular cloning, purification and reconstitution of cytosolic and membrane proteins in model membranes and fluorescence confocal microscopy. Her investigation is focused on the role of Drp1 in mitochondrial dynamics and apoptosis.

Ana J. García-Sáez

Ana J. Garcia-Saez characterized the membrane interacting domains of Bcl-2 proteins during her PhD at the University of Valencia, Spain. Between 2005 and 2009, she worked as a postdoc in the lab of Prof. Petra Schwille, where she focused on the use of advanced microscopy approaches to study membrane dynamics and organization. In 2010, she started her own independent group at the Max Planck Institute for Intelligent Systems and the German Cancer Research Centre in Heidelberg. Since 2013, she is full professor of Biochemistry at the Interfaculty Institute of Biochemstry in Tübingen. Her work focuses on the use on the use of single molecule microscopy and other advanced imaging methods to investigate the mitochondrial alterations during apoptosis.

We thank Stephanie Bleicken for helpful discussions and Willian Aaron Grandy for critically reading the manuscript. This work was supported by the Max Planck Society, the German Cancer Research Center and the German Ministry for Education and Research (BMBF, grant N.0312040).

References

Akepati, V.R., Muller, E.C., Otto, A., Strauss, H.M., Portwich, M., and Alexander, C. (2008). Characterization of OPA1 isoforms isolated from mouse tissues. J. Neurochem. 106, 372–383.10.1111/j.1471-4159.2008.05401.xSearch in Google Scholar PubMed

Alirol, E., James, D., Huber, D., Marchetto, A., Vergani, L., Martinou, J.C., and Scorrano, L. (2006). The mitochondrial fission protein hFis1 requires the endoplasmic reticulum gateway to induce apoptosis. Mol. Biol. Cell 17, 4593–4605.10.1091/mbc.e06-05-0377Search in Google Scholar PubMed PubMed Central

Amati-Bonneau, P., Milea, D., Bonneau, D., Chevrollier, A., Ferre, M., Guillet, V., Gueguen, N., Loiseau, D., de Crescenzo, M.A., Verny, C., et al. (2009). OPA1-associated disorders: phenotypes and pathophysiology. Int. J. Biochem. Cell. Biol. 41, 1855–1865.10.1016/j.biocel.2009.04.012Search in Google Scholar PubMed

Anand, R., Langer, T., and Baker, M.J. (2013). Proteolytic control of mitochondrial function and morphogenesis. Biochimica et biophysica acta 1833, 195–204.10.1016/j.bbamcr.2012.06.025Search in Google Scholar PubMed

Anesti, V. and Scorrano, L. (2006). The relationship between mitochondrial shape and function and the cytoskeleton. Biochim. Biophys. Acta. 1757, 692–699.10.1016/j.bbabio.2006.04.013Search in Google Scholar PubMed

Anton, F., Fres, J.M., Schauss, A., Pinson, B., Praefcke, G.J., Langer, T., and Escobar-Henriques, M. (2011). Ugo1 and Mdm30 act sequentially during Fzo1-mediated mitochondrial outer membrane fusion. J. Cell. Sci. 124, 1126–1135.10.1242/jcs.073080Search in Google Scholar PubMed

Arnoult, D., Grodet, A., Lee, Y.J., Estaquier, J., and Blackstone, C. (2005). Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J. Biol. Chem. 280, 35742–35750.10.1074/jbc.M505970200Search in Google Scholar PubMed

Ashrafian, H., Docherty, L., Leo, V., Towlson, C., Neilan, M., Steeples, V., Lygate, C.A., Hough, T., Townsend, S., Williams, D., et al. (2010). A mutation in the mitochondrial fission gene Dnm1l leads to cardiomyopathy. PLoS Genet 6, e1001000.10.1371/journal.pgen.1001000Search in Google Scholar PubMed PubMed Central

Autret, A. and Martin, S.J. (2009). Emerging role for members of the Bcl-2 family in mitochondrial morphogenesis. Mol. Cell 36, 355–363.10.1016/j.molcel.2009.10.011Search in Google Scholar PubMed

Ban-Ishihara, R., Ishihara, T., Sasaki, N., Mihara, K., and Ishihara, N. (2013). Dynamics of nucleoid structure regulated by mitochondrial fission contributes to cristae reformation and release of cytochrome c. Proc. Natl. Acad. Sci. USA 110, 11863–11868.10.1073/pnas.1301951110Search in Google Scholar PubMed PubMed Central

Ban, T., Heymann, J.A., Song, Z., Hinshaw, J.E., and Chan, D.C. (2010). OPA1 disease alleles causing dominant optic atrophy have defects in cardiolipin-stimulated GTP hydrolysis and membrane tubulation. Hum. Mol. Genet. 19, 2113–2122.10.1093/hmg/ddq088Search in Google Scholar PubMed PubMed Central

Basanez, G., Sharpe, J.C., Galanis, J., Brandt, T.B., Hardwick, J.M., and Zimmerberg, J. (2002). Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J. Biol. Chem. 277, 49360–49365.10.1074/jbc.M206069200Search in Google Scholar PubMed

Bereiter-Hahn, J. and Voth, M. (1994). Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Techniq. 27, 198–219.10.1002/jemt.1070270303Search in Google Scholar PubMed

Berman, S.B., Chen, Y.B., Qi, B., McCaffery, J.M., Rucker, E.B., 3rd, Goebbels, S., Nave, K.A., Arnold, B.A., Jonas, E.A., Pineda, F.J., et al. (2009). Bcl-x L increases mitochondrial fission, fusion, and biomass in neurons. J. Cell. Biol. 184, 707–719.10.1083/jcb.200809060Search in Google Scholar PubMed PubMed Central

Bleazard, W., McCaffery, J.M., King, E.J., Bale, S., Mozdy, A., Tieu, Q., Nunnari, J., and Shaw, J.M. (1999). The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell. Biol. 1, 298–304.10.1038/13014Search in Google Scholar PubMed PubMed Central

Bleicken, S., Landeta, O., Landajuela, A., Basanez, G., and Garcia-Saez, A.J. (2013a). Proapoptotic Bax and Bak form stable protein-permeable pores of tunable size. J. Biol. Chem. Oct 7 [Epub ahead of print].10.1074/jbc.M113.512087Search in Google Scholar PubMed PubMed Central

Bleicken, S., Wagner, C., and Garcia-Saez, A.J. (2013b). Mechanistic differences in the membrane activity of Bax and Bcl-xL correlate with their opposing roles in apoptosis. Biophys. J. 104, 421–431.10.1016/j.bpj.2012.12.010Search in Google Scholar PubMed PubMed Central

Boldogh, I.R. and Pon, L.A. (2007). Mitochondria on the move. Trends Cell. Biol. 17, 502–510.10.1016/j.tcb.2007.07.008Search in Google Scholar PubMed

Breckenridge, D.G., Stojanovic, M., Marcellus, R.C., and Shore, G.C. (2003). Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J. Cell. Biol. 160, 1115–1127.10.1083/jcb.200212059Search in Google Scholar PubMed PubMed Central

Brooks, C., Wei, Q., Feng, L., Dong, G., Tao, Y., Mei, L., Xie, Z.J., and Dong, Z. (2007). Bak regulates mitochondrial morphology and pathology during apoptosis by interacting with mitofusins. Proc. Natl. Acad. Sci. USA 104, 11649–11654.10.1073/pnas.0703976104Search in Google Scholar PubMed PubMed Central

Bui, H.T., Karren, M.A., Bhar, D., and Shaw, J.M. (2012). A novel motif in the yeast mitochondrial dynamin Dnm1 is essential for adaptor binding and membrane recruitment. J. Cell. Biol. 199, 613–622.10.1083/jcb.201207079Search in Google Scholar PubMed PubMed Central

Cassidy-Stone, A., Chipuk, J.E., Ingerman, E., Song, C., Yoo, C., Kuwana, T., Kurth, M.J., Shaw, J.T., Hinshaw, J.E., Green, D.R., et al. (2008). Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 14, 193–204.10.1016/j.devcel.2007.11.019Search in Google Scholar PubMed PubMed Central

Chappie, J.S., Acharya, S., Leonard, M., Schmid, S.L., and Dyda, F. (2010). G domain dimerization controls dynamin’s assembly-stimulated GTPase activity. Nature 465, 435–440.10.1038/nature09032Search in Google Scholar PubMed PubMed Central

Chappie, J.S., Mears, J.A., Fang, S., Leonard, M., Schmid, S.L., Milligan, R.A., Hinshaw, J.E., and Dyda, F. (2011). A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell 147, 209–222.10.1016/j.cell.2011.09.003Search in Google Scholar PubMed PubMed Central

Chen, C.H., Howng, S.L., Hwang, S.L., Chou, C.K., Liao, C.H., and Hong, Y.R. (2000). Differential expression of four human dynamin-like protein variants in brain tumors. DNA Cell Biol. 19, 189–194.10.1089/104454900314573Search in Google Scholar PubMed

Chen, H. and Chan, D.C. (2010). Physiological functions of mitochondrial fusion. Ann. NY Acad. Sci. 1201, 21–25.10.1111/j.1749-6632.2010.05615.xSearch in Google Scholar PubMed

Chen, H., Chomyn, A., and Chan, D.C. (2005). Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280, 26185–26192.10.1074/jbc.M503062200Search in Google Scholar PubMed

Chen, H., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E., and Chan, D.C. (2003). Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell. Biol. 160, 189–200.10.1083/jcb.200211046Search in Google Scholar PubMed PubMed Central

Chen, H., McCaffery, J.M., and Chan, D.C. (2007). Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130, 548–562.10.1016/j.cell.2007.06.026Search in Google Scholar PubMed

Cho, D.H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z., and Lipton, S.A. (2009). S-nitrosylation of Drp1 mediates β-amyloid-related mitochondrial fission and neuronal injury. Science 324, 102–105.10.1126/science.1171091Search in Google Scholar PubMed PubMed Central

Chou, C.H., Lin, C.C., Yang, M.C., Wei, C.C., Liao, H.D., Lin, R.C., Tu, W.Y., Kao, T.C., Hsu, C.M., Cheng, J.T., et al. (2012). GSK3β-mediated Drp1 phosphorylation induced elongated mitochondrial morphology against oxidative stress. PloS One 7, e49112.Search in Google Scholar

Chung, K.W., Kim, S.B., Park, K.D., Choi, K.G., Lee, J.H., Eun, H.W., Suh, J.S., Hwang, J.H., Kim, W.K., Seo, B.C., et al. (2006). Early onset severe and late-onset mild Charcot-Marie-Tooth disease with mitofusin 2 (MFN2) mutations. Brain 129, 2103–2118.10.1093/brain/awl174Search in Google Scholar PubMed

Cipolat, S., Martins de Brito, O., Dal Zilio, B., and Scorrano, L. (2004). OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. USA 101, 15927–15932.10.1073/pnas.0407043101Search in Google Scholar PubMed PubMed Central

Cleland, M.M., Norris, K.L., Karbowski, M., Wang, C., Suen, D.F., Jiao, S., George, N.M., Luo, X., Li, Z., and Youle, R.J. (2011). Bcl-2 family interaction with the mitochondrial morphogenesis machinery. Cell Death Differ. 18, 235–247.10.1038/cdd.2010.89Search in Google Scholar PubMed PubMed Central

Cribbs, J.T. and Strack, S. (2007). Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8, 939–944.10.1038/sj.embor.7401062Search in Google Scholar PubMed PubMed Central

de Brito, O.M. and Scorrano, L. (2008). Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605–610.10.1038/nature07534Search in Google Scholar PubMed

De Palma, C., Falcone, S., Pisoni, S., Cipolat, S., Panzeri, C., Pambianco, S., Pisconti, A., Allevi, R., Bassi, M.T., Cossu, G., et al. (2010). Nitric oxide inhibition of Drp1-mediated mitochondrial fission is critical for myogenic differentiation. Cell Death Differ. 17, 1684–1696.10.1038/cdd.2010.48Search in Google Scholar PubMed PubMed Central

Delettre, C., Lenaers, G., Griffoin, J.M., Gigarel, N., Lorenzo, C., Belenguer, P., Pelloquin, L., Grosgeorge, J., Turc-Carel, C., Perret, E., et al. (2000). Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26, 207–210.10.1038/79936Search in Google Scholar PubMed

Detmer, S.A. and Chan, D.C. (2007). Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell. Biol. 8, 870–879.10.1038/nrm2275Search in Google Scholar PubMed

DeVay, R.M., Dominguez-Ramirez, L., Lackner, L.L., Hoppins, S., Stahlberg, H., and Nunnari, J. (2009). Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J. Cell. Biol. 186, 793–803.10.1083/jcb.200906098Search in Google Scholar PubMed PubMed Central

Ehses, S., Raschke, I., Mancuso, G., Bernacchia, A., Geimer, S., Tondera, D., Martinou, J.C., Westermann, B., Rugarli, E.I., and Langer, T. (2009). Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell. Biol. 187, 1023–1036.10.1083/jcb.200906084Search in Google Scholar PubMed PubMed Central

Elachouri, G., Vidoni, S., Zanna, C., Pattyn, A., Boukhaddaoui, H., Gaget, K., Yu-Wai-Man, P., Gasparre, G., Sarzi, E., Delettre, C., et al. (2011). OPA1 links human mitochondrial genome maintenance to mtDNA replication and distribution. Genome Res. 21, 12–20.10.1101/gr.108696.110Search in Google Scholar

Escobar-Henriques, M. and Anton, F. (2013). Mechanistic perspective of mitochondrial fusion: tubulation vs. fragmentation. Biochim. Biophys. Acta 1833, 162–175.10.1016/j.bbamcr.2012.07.016Search in Google Scholar

Estaquier, J. and Arnoult, D. (2007). Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ. 14, 1086–1094.10.1038/sj.cdd.4402107Search in Google Scholar

Faelber, K., Posor, Y., Gao, S., Held, M., Roske, Y., Schulze, D., Haucke, V., Noe, F., and Daumke, O. (2011). Crystal structure of nucleotide-free dynamin. Nature 477, 556–560.10.1038/nature10369Search in Google Scholar

Figueroa-Romero, C., Iniguez-Lluhi, J.A., Stadler, J., Chang, C.R., Arnoult, D., Keller, P.J., Hong, Y., Blackstone, C., and Feldman, E.L. (2009). SUMOylation of the mitochondrial fission protein Drp1 occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle. FASEB J 23, 3917–3927.10.1096/fj.09-136630Search in Google Scholar

Ford, M.G., Jenni, S., and Nunnari, J. (2011). The crystal structure of dynamin. Nature 477, 561–566.10.1038/nature10441Search in Google Scholar

Frank, S., Gaume, B., Bergmann-Leitner, E.S., Leitner, W.W., Robert, E.G., Catez, F., Smith, C.L., and Youle, R.J. (2001). The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515–525.10.1016/S1534-5807(01)00055-7Search in Google Scholar

Frezza, C., Cipolat, S., Martins de Brito, O., Micaroni, M., Beznoussenko, G.V., Rudka, T., Bartoli, D., Polishuck, R.S., Danial, N.N., De Strooper, B., et al. (2006). OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126, 177–189.10.1016/j.cell.2006.06.025Search in Google Scholar PubMed

Friedman, J.R., Lackner, L.L., West, M., DiBenedetto, J.R., Nunnari, J., and Voeltz, G.K. (2011). ER tubules mark sites of mitochondrial division. Science 334, 358–362.10.1126/science.1207385Search in Google Scholar PubMed PubMed Central

Frohlich, C., Grabiger, S., Schwefel, D., Faelber, K., Rosenbaum, E., Mears, J., Rocks, O., and Daumke, O. (2013). Structural insights into oligomerization and mitochondrial remodelling of dynamin 1-like protein. EMBO J. 32, 1280–1292.10.1038/emboj.2013.74Search in Google Scholar PubMed PubMed Central

Gandre-Babbe, S. and van der Bliek, A.M. (2008). The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell. 19, 2402–2412.10.1091/mbc.e07-12-1287Search in Google Scholar PubMed PubMed Central

Garcia-Saez, A.J. (2012). The secrets of the Bcl-2 family. Cell Death Differ. 19, 1733–1740.10.1038/cdd.2012.105Search in Google Scholar PubMed PubMed Central

Garcia-Saez, A.J., Ries, J., Orzaez, M., Perez-Paya, E., and Schwille, P. (2009). Membrane promotes tBID interaction with BCL(XL). Nat. Struct. Mol. Biol. 16, 1178–1185.10.1038/nsmb.1671Search in Google Scholar PubMed

Gegg, M.E., Cooper, J.M., Chau, K.Y., Rojo, M., Schapira, A.H., and Taanman, J.W. (2010). Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum. Mol. Genet. 19, 4861–4870.10.1093/hmg/ddq419Search in Google Scholar PubMed PubMed Central

Gerdes, F., Tatsuta, T., and Langer, T. (2012). Mitochondrial AAA proteases--towards a molecular understanding of membrane-bound proteolytic machines. Biochim. Biophys. Acta 1823, 49–55.10.1016/j.bbamcr.2011.09.015Search in Google Scholar PubMed

Germain, M., Mathai, J.P., McBride, H.M., and Shore, G.C. (2005). Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J. 24, 1546–1556.10.1038/sj.emboj.7600592Search in Google Scholar PubMed PubMed Central

Glancy, B. and Balaban, R.S. (2012). Role of mitochondrial Ca2+ in the regulation of cellular energetics. Biochemistry 51, 2959–2973.10.1021/bi2018909Search in Google Scholar PubMed PubMed Central

Glauser, L., Sonnay, S., Stafa, K., and Moore, D.J. (2011). Parkin promotes the ubiquitination and degradation of the mitochondrial fusion factor mitofusin 1. J. Neurochem. 118, 636–645.10.1111/j.1471-4159.2011.07318.xSearch in Google Scholar PubMed

Griffin, E.E. and Chan, D.C. (2006). Domain interactions within Fzo1 oligomers are essential for mitochondrial fusion. J. Biol. Chem. 281, 16599–16606.10.1074/jbc.M601847200Search in Google Scholar PubMed

Griffin, E.E., Graumann, J., and Chan, D.C. (2005). The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J. Cell. Biol. 170, 237–248.10.1083/jcb.200503148Search in Google Scholar PubMed PubMed Central

Guo, C., Hildick, K.L., Luo, J., Dearden, L., Wilkinson, K.A., and Henley, J.M. (2013). SENP3-mediated deSUMOylation of dynamin-related protein 1 promotes cell death following ischaemia. EMBO J. 32, 1514–1528.10.1038/emboj.2013.65Search in Google Scholar

Han, X.J., Lu, Y.F., Li, S.A., Kaitsuka, T., Sato, Y., Tomizawa, K., Nairn, A.C., Takei, K., Matsui, H., and Matsushita, M. (2008). CaM kinase I α-induced phosphorylation of Drp1 regulates mitochondrial morphology. J. Cell. Biol. 182, 573–585.10.1083/jcb.200802164Search in Google Scholar

Head, B., Griparic, L., Amiri, M., Gandre-Babbe, S., and van der Bliek, A.M. (2009). Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J. Cell. Biol. 187, 959–966.10.1083/jcb.200906083Search in Google Scholar

Honda, S., Aihara, T., Hontani, M., Okubo, K., and Hirose, S. (2005). Mutational analysis of action of mitochondrial fusion factor mitofusin-2. J. Cell Sci. 118, 3153–3161.10.1242/jcs.02449Search in Google Scholar

Hoppins, S., Edlich, F., Cleland, M.M., Banerjee, S., McCaffery, J.M., Youle, R.J., and Nunnari, J. (2011). The soluble form of Bax regulates mitochondrial fusion via MFN2 homotypic complexes. Mol Cell 41, 150–160.10.1016/j.molcel.2010.11.030Search in Google Scholar

Hudson, G., Amati-Bonneau, P., Blakely, E.L., Stewart, J.D., He, L., Schaefer, A.M., Griffiths, P.G., Ahlqvist, K., Suomalainen, A., Reynier, P., et al. (2008). Mutation of OPA1 causes dominant optic atrophy with external ophthalmoplegia, ataxia, deafness and multiple mitochondrial DNA deletions: a novel disorder of mtDNA maintenance. Brain 131, 329–337.10.1093/brain/awm272Search in Google Scholar

Ishihara, N., Eura, Y., and Mihara, K. (2004). Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J. Cell Sci. 117, 6535–6546.10.1242/jcs.01565Search in Google Scholar

Ishihara, N., Fujita, Y., Oka, T., and Mihara, K. (2006). Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 25, 2966–2977.10.1038/sj.emboj.7601184Search in Google Scholar

Ishihara, N., Jofuku, A., Eura, Y., and Mihara, K. (2003). Regulation of mitochondrial morphology by membrane potential, and DRP1-dependent division and FZO1-dependent fusion reaction in mammalian cells. Biochem. Biophys. Res. Commun. 301, 891–898.10.1016/S0006-291X(03)00050-0Search in Google Scholar

Ishihara, N., Nomura, M., Jofuku, A., Kato, H., Suzuki, S.O., Masuda, K., Otera, H., Nakanishi, Y., Nonaka, I., Goto, Y., et al. (2009). Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell Biol. 11, 958–966.10.1038/ncb1907Search in Google Scholar PubMed

Iwasawa, R., Mahul-Mellier, A.L., Datler, C., Pazarentzos, E., and Grimm, S. (2011). Fis1 and Bap31 bridge the mitochondria-ER interface to establish a platform for apoptosis induction. EMBO J. 30, 556–568.10.1038/emboj.2010.346Search in Google Scholar

James, D.I., Parone, P.A., Mattenberger, Y., and Martinou, J.C. (2003). hFis1, a novel component of the mammalian mitochondrial fission machinery. J. Biol. Chem. 278, 36373–36379.10.1074/jbc.M303758200Search in Google Scholar

Kanazawa, T., Zappaterra, M.D., Hasegawa, A., Wright, A.P., Newman-Smith, E.D., Buttle, K.F., McDonald, K., Mannella, C.A., and van der Bliek, A.M. (2008). The C. elegans Opa1 homologue EAT-3 is essential for resistance to free radicals. PLoS Genet 4, e1000022.Search in Google Scholar

Karbowski, M., Lee, Y.J., Gaume, B., Jeong, S.Y., Frank, S., Nechushtan, A., Santel, A., Fuller, M., Smith, C.L., and Youle, R.J. (2002). Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell. Biol. 159, 931–938.10.1083/jcb.200209124Search in Google Scholar

Karbowski, M., Neutzner, A., and Youle, R.J. (2007). The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell. Biol. 178, 71–84.10.1083/jcb.200611064Search in Google Scholar

Karbowski, M., Norris, K.L., Cleland, M.M., Jeong, S.Y., and Youle, R.J. (2006). Role of Bax and Bak in mitochondrial morphogenesis. Nature 443, 658–662.10.1038/nature05111Search in Google Scholar

Karren, M.A., Coonrod, E.M., Anderson, T.K., and Shaw, J.M. (2005). The role of Fis1p-Mdv1p interactions in mitochondrial fission complex assembly. J. Cell. Biol. 171, 291–301.10.1083/jcb.200506158Search in Google Scholar

Katsov, K., Muller, M., and Schick, M. (2004). Field theoretic study of bilayer membrane fusion. I. Hemifusion mechanism. Biophys J. 87, 3277–3290.Search in Google Scholar

Koirala, S., Guo, Q., Kalia, R., Bui, H.T., Eckert, D.M., Frost, A., and Shaw, J.M. (2013). Interchangeable adaptors regulate mitochondrial dynamin assembly for membrane scission. Proc. Natl. Acad. Sci. USA 110, E1342–1351.10.1073/pnas.1300855110Search in Google Scholar

Koshiba, T., Detmer, S.A., Kaiser, J.T., Chen, H., McCaffery, J.M., and Chan, D.C. (2004). Structural basis of mitochondrial tethering by mitofusin complexes. Science 305, 858–862.10.1126/science.1099793Search in Google Scholar

Kuwana, T., Mackey, M.R., Perkins, G., Ellisman, M.H., Latterich, M., Schneiter, R., Green, D.R., and Newmeyer, D.D. (2002). Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331–342.10.1016/S0092-8674(02)01036-XSearch in Google Scholar

Lackner, L.L., Horner, J.S., and Nunnari, J. (2009). Mechanistic analysis of a dynamin effector. Science 325, 874–877.10.1126/science.1176921Search in Google Scholar PubMed PubMed Central

Landeta, O., Landajuela, A., Gil, D., Taneva, S., Di Primo, C., Sot, B., Valle, M., Frolov, V.A., and Basanez, G. (2011). Reconstitution of proapoptotic BAK function in liposomes reveals a dual role for mitochondrial lipids in the BAK-driven membrane permeabilization process. J. Biol. Chem. 286, 8213–8230.10.1074/jbc.M110.165852Search in Google Scholar PubMed PubMed Central

Leber, B., Lin, J., and Andrews, D.W. (2010). Still embedded together binding to membranes regulates Bcl-2 protein interactions. Oncogene 29, 5221–5230.10.1038/onc.2010.283Search in Google Scholar PubMed PubMed Central

Lee, Y.J., Jeong, S.Y., Karbowski, M., Smith, C.L., and Youle, R.J. (2004). Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol. Biol. Cell 15, 5001–5011.10.1091/mbc.e04-04-0294Search in Google Scholar PubMed PubMed Central

Legros, F., Lombes, A., Frachon, P., and Rojo, M. (2002). Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol. Biol. Cell 13, 4343–4354.10.1091/mbc.e02-06-0330Search in Google Scholar PubMed PubMed Central

Li, H., Alavian, K.N., Lazrove, E., Mehta, N., Jones, A., Zhang, P., Licznerski, P., Graham, M., Uo, T., Guo, J., et al. (2013). A Bcl-xL-Drp1 complex regulates synaptic vesicle membrane dynamics during endocytosis. Nat. Cell Biol. 15, 773–785.10.1038/ncb2791Search in Google Scholar PubMed PubMed Central

Li, H., Chen, Y., Jones, A.F., Sanger, R.H., Collis, L.P., Flannery, R., McNay, E.C., Yu, T., Schwarzenbacher, R., Bossy, B., et al. (2008). Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 105, 2169–2174.10.1073/pnas.0711647105Search in Google Scholar PubMed PubMed Central

Livnat-Levanon, N. and Glickman, M.H. (2011). Ubiquitin-proteasome system and mitochondria-reciprocity. Biochim. Biophys. Acta 1809, 80–87.10.1016/j.bbagrm.2010.07.005Search in Google Scholar PubMed

Loson, O.C., Song, Z., Chen, H., and Chan, D.C. (2013). Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 24, 659–667.10.1091/mbc.e12-10-0721Search in Google Scholar

Lutter, M., Fang, M., Luo, X., Nishijima, M., Xie, X., and Wang, X. (2000). Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat. Cell Biol. 2, 754–761.10.1038/35036395Search in Google Scholar PubMed

Martinou, J.C. and Youle, R.J. (2006). Which came first, the cytochrome c release or the mitochondrial fission? Cell Death Differ. 13, 1291–1295.Search in Google Scholar

Martinou, J.C. and Youle, R.J. (2011). Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev. Cell 21, 92–101.10.1016/j.devcel.2011.06.017Search in Google Scholar PubMed PubMed Central

Mears, J.A., Lackner, L.L., Fang, S., Ingerman, E., Nunnari, J., and Hinshaw, J.E. (2011). Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat. Struct. Mol. Biol. 18, 20–26.10.1038/nsmb.1949Search in Google Scholar

Misko, A., Jiang, S., Wegorzewska, I., Milbrandt, J., and Baloh, R.H. (2010). Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J. Neurosci. 30, 4232–4240.10.1523/JNEUROSCI.6248-09.2010Search in Google Scholar

Montessuit, S., Somasekharan, S.P., Terrones, O., Lucken-Ardjomande, S., Herzig, S., Schwarzenbacher, R., Manstein, D.J., Bossy-Wetzel, E., Basanez, G., Meda, P., et al. (2010). Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142, 889–901.10.1016/j.cell.2010.08.017Search in Google Scholar

Munoz-Pinedo, C., Guio-Carrion, A., Goldstein, J.C., Fitzgerald, P., Newmeyer, D.D., and Green, D.R. (2006). Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is coordinately initiated but can vary in duration. Proc. Natl. Acad. Sci. USA 103, 11573–11578.10.1073/pnas.0603007103Search in Google Scholar

Nakamura, N., Kimura, Y., Tokuda, M., Honda, S., and Hirose, S. (2006). MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 7, 1019–1022.10.1038/sj.embor.7400790Search in Google Scholar

Neuspiel, M., Zunino, R., Gangaraju, S., Rippstein, P., and McBride, H. (2005). Activated mitofusin 2 signals mitochondrial fusion, interferes with Bax activation, and reduces susceptibility to radical induced depolarization. J. Biol. Chem. 280, 25060–25070.10.1074/jbc.M501599200Search in Google Scholar

Nunnari, J. and Suomalainen, A. (2012). Mitochondria: in sickness and in health. Cell 148, 1145–1159.10.1016/j.cell.2012.02.035Search in Google Scholar

Olichon, A., Baricault, L., Gas, N., Guillou, E., Valette, A., Belenguer, P., and Lenaers, G. (2003). Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278, 7743–7746.10.1074/jbc.C200677200Search in Google Scholar

Olichon, A., Emorine, L.J., Descoins, E., Pelloquin, L., Brichese, L., Gas, N., Guillou, E., Delettre, C., Valette, A., Hamel, C.P., et al. (2002). The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett. 523, 171–176.10.1016/S0014-5793(02)02985-XSearch in Google Scholar

Osman, C., Voelker, D.R., and Langer, T. (2011). Making heads or tails of phospholipids in mitochondria. J. Cell. Biol. 192, 7–16.10.1083/jcb.201006159Search in Google Scholar PubMed PubMed Central

Otera, H., Ishihara, N., and Mihara, K. (2013). New insights into the function and regulation of mitochondrial fission. Biochim. Biophys. Acta 1833, 1256–1268.10.1016/j.bbamcr.2013.02.002Search in Google Scholar PubMed

Otera, H., Wang, C., Cleland, M.M., Setoguchi, K., Yokota, S., Youle, R.J., and Mihara, K. (2010). Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell. Biol. 191, 1141–1158.10.1083/jcb.201007152Search in Google Scholar PubMed PubMed Central

Ott, M., Zhivotovsky, B., and Orrenius, S. (2007). Role of cardiolipin in cytochrome c release from mitochondria. Cell Death Differ. 14, 1243–1247.10.1038/sj.cdd.4402135Search in Google Scholar PubMed

Ow, Y.P., Green, D.R., Hao, Z., and Mak, T.W. (2008). Cytochrome c: functions beyond respiration. Nat. Rev. Mol. Cell. Biol.9, 532–542.10.1038/nrm2434Search in Google Scholar PubMed

Palmer, C.S., Osellame, L.D., Laine, D., Koutsopoulos, O.S., Frazier, A.E., and Ryan, M.T. (2011a). MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 12, 565–573.10.1038/embor.2011.54Search in Google Scholar PubMed PubMed Central

Palmer, C.S., Osellame, L.D., Stojanovski, D., and Ryan, M.T. (2011b). The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery. Cell Signal 23, 1534–1545.10.1016/j.cellsig.2011.05.021Search in Google Scholar PubMed

Park, Y.Y., Lee, S., Karbowski, M., Neutzner, A., Youle, R.J., and Cho, H. (2010). Loss of MARCH5 mitochondrial E3 ubiquitin ligase induces cellular senescence through dynamin-related protein 1 and mitofusin 1. J. Cell Sci. 123, 619–626.10.1242/jcs.061481Search in Google Scholar PubMed PubMed Central

Parone, P.A., James, D.I., Da Cruz, S., Mattenberger, Y., Donze, O., Barja, F., and Martinou, J.C. (2006). Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol. Cell. Biol. 26, 7397–7408.10.1128/MCB.02282-05Search in Google Scholar PubMed PubMed Central

Pelloquin, L., Belenguer, P., Menon, Y., Gas, N., and Ducommun, B. (1999). Fission yeast Msp1 is a mitochondrial dynamin-related protein. J. Cell Sci. 112, 4151–4161.10.1242/jcs.112.22.4151Search in Google Scholar PubMed

Praefcke, G.J. and McMahon, H.T. (2004). The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell. Biol. 5, 133–147.10.1038/nrm1313Search in Google Scholar PubMed

Puech, P.H., Borghi, N., Karatekin, E., and Brochard-Wyart, F. (2003). Line thermodynamics: adsorption at a membrane edge. Phys. Rev. Lett. 90, 128304.10.1103/PhysRevLett.90.128304Search in Google Scholar

Rakovic, A., Grunewald, A., Kottwitz, J., Bruggemann, N., Pramstaller, P.P., Lohmann, K., and Klein, C. (2011). Mutations in PINK1 and Parkin impair ubiquitination of Mitofusins in human fibroblasts. PloS One 6, e16746.10.1371/journal.pone.0016746Search in Google Scholar

Ramachandran, R., Pucadyil, T.J., Liu, Y.W., Acharya, S., Leonard, M., Lukiyanchuk, V., and Schmid, S.L. (2009). Membrane insertion of the pleckstrin homology domain variable loop 1 is critical for dynamin-catalyzed vesicle scission. Mol. Biol. Cell 20, 4630–4639.10.1091/mbc.e09-08-0683Search in Google Scholar

Rehm, M., Dussmann, H., and Prehn, J.H. (2003). Real-time single cell analysis of Smac/DIABLO release during apoptosis. J. Cell. Biol. 162, 1031–1043.10.1083/jcb.200303123Search in Google Scholar

Rojo, M., Legros, F., Chateau, D., and Lombes, A. (2002). Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J. Cell Sci. 115, 1663–1674.10.1242/jcs.115.8.1663Search in Google Scholar

Rujiviphat, J., Meglei, G., Rubinstein, J.L., and McQuibban, G.A. (2009). Phospholipid association is essential for dynamin-related protein Mgm1 to function in mitochondrial membrane fusion. J. Biol. Chem. 284, 28682–28686.10.1074/jbc.M109.044933Search in Google Scholar

Satoh, M., Hamamoto, T., Seo, N., Kagawa, Y., and Endo, H. (2003). Differential sublocalization of the dynamin-related protein OPA1 isoforms in mitochondria. Biochem. Biophys. Res. Commun. 300, 482–493.10.1016/S0006-291X(02)02874-7Search in Google Scholar

Scorrano, L., Ashiya, M., Buttle, K., Weiler, S., Oakes, S.A., Mannella, C.A., and Korsmeyer, S.J. (2002). A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2, 55–67.10.1016/S1534-5807(01)00116-2Search in Google Scholar

Sheridan, C., Delivani, P., Cullen, S.P., and Martin, S.J. (2008). Bax- or Bak-induced mitochondrial fission can be uncoupled from cytochrome C release. Mol. Cell 31, 570–585.10.1016/j.molcel.2008.08.002Search in Google Scholar PubMed

Smirnova, E., Griparic, L., Shurland, D.L., and van der Bliek, A.M. (2001). Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245–2256.10.1091/mbc.12.8.2245Search in Google Scholar PubMed PubMed Central

Song, Z., Chen, H., Fiket, M., Alexander, C., and Chan, D.C. (2007). OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J. Cell. Biol. 178, 749–755.10.1083/jcb.200704110Search in Google Scholar

Stojanovski, D., Koutsopoulos, O.S., Okamoto, K., and Ryan, M.T. (2004). Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology. J. Cell Sci. 117, 1201–1210.10.1242/jcs.01058Search in Google Scholar

Strack, S. and Cribbs, J.T. (2012). Allosteric modulation of Drp1 mechanoenzyme assembly and mitochondrial fission by the variable domain. J. Biol. Chem. 287, 10990–11001.10.1074/jbc.M112.342105Search in Google Scholar

Strack, S., Wilson, T.J., and Cribbs, J.T. (2013). Cyclin-dependent kinases regulate splice-specific targeting of dynamin-related protein 1 to microtubules. J. Cell. Biol. 201, 1037–1051.10.1083/jcb.201210045Search in Google Scholar

Suen, D.F., Norris, K.L., and Youle, R.J. (2008). Mitochondrial dynamics and apoptosis. Genes Dev. 22, 1577–1590.10.1101/gad.1658508Search in Google Scholar

Suzuki, M., Jeong, S.Y., Karbowski, M., Youle, R.J., and Tjandra, N. (2003). The solution structure of human mitochondria fission protein Fis1 reveals a novel TPR-like helix bundle. J. Mol. Biol. 334, 445–458.10.1016/j.jmb.2003.09.064Search in Google Scholar

Tanaka, A., Cleland, M.M., Xu, S., Narendra, D.P., Suen, D.F., Karbowski, M., and Youle, R.J. (2010). Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell. Biol. 191, 1367–1380.10.1083/jcb.201007013Search in Google Scholar

van der Bliek, A.M. (1999). Functional diversity in the dynamin family. Trends Cell Biol 9, 96–102.10.1016/S0962-8924(98)01490-1Search in Google Scholar

Vaux, D.L. (2011). Apoptogenic factors released from mitochondria. Biochim. Biophys. Acta 1813, 546–550.10.1016/j.bbamcr.2010.08.002Search in Google Scholar PubMed

Wakabayashi, J., Zhang, Z., Wakabayashi, N., Tamura, Y., Fukaya, M., Kensler, T.W., Iijima, M., and Sesaki, H. (2009). The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J. Cell. Biol. 186, 805–816.10.1083/jcb.200903065Search in Google Scholar PubMed PubMed Central

Wang, H., Song, P., Du, L., Tian, W., Yue, W., Liu, M., Li, D., Wang, B., Zhu, Y., Cao, C., et al. (2011). Parkin ubiquitinates Drp1 for proteasome-dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson disease. J. Biol. Chem. 286, 11649–11658.10.1074/jbc.M110.144238Search in Google Scholar PubMed PubMed Central

Wasiak, S., Zunino, R., and McBride, H.M. (2007). Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell. Biol. 177, 439–450.10.1083/jcb.200610042Search in Google Scholar PubMed PubMed Central

Waterham, H.R., Koster, J., van Roermund, C.W., Mooyer, P.A., Wanders, R.J., and Leonard, J.V. (2007). A lethal defect of mitochondrial and peroxisomal fission. N. Engl. J. Med. 356, 1736–1741.10.1056/NEJMoa064436Search in Google Scholar PubMed

Westermann, B. (2010a). Mitochondrial dynamics in model organisms: what yeasts, worms and flies have taught us about fusion and fission of mitochondria. Semin. Cell Dev. Biol. 21, 542–549.10.1016/j.semcdb.2009.12.003Search in Google Scholar PubMed

Westermann, B. (2010b). Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell. Biol. 11, 872–884.10.1038/nrm3013Search in Google Scholar PubMed

Wilson, T.J., Slupe, A.M., and Strack, S. (2013). Cell signaling and mitochondrial dynamics: Implications for neuronal function and neurodegenerative disease. Neurobiol. Dis. 51, 13–26.10.1016/j.nbd.2012.01.009Search in Google Scholar PubMed PubMed Central

Wong, E.D., Wagner, J.A., Gorsich, S.W., McCaffery, J.M., Shaw, J.M., and Nunnari, J. (2000). The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria. J. Cell. Biol. 151, 341–352.10.1083/jcb.151.2.341Search in Google Scholar PubMed PubMed Central

Yamaguchi, R., Lartigue, L., Perkins, G., Scott, R.T., Dixit, A., Kushnareva, Y., Kuwana, T., Ellisman, M.H., and Newmeyer, D.D. (2008). Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol. Cell 31, 557–569.10.1016/j.molcel.2008.07.010Search in Google Scholar PubMed PubMed Central

Yamaguchi, R. and Perkins, G. (2009). Dynamics of mitochondrial structure during apoptosis and the enigma of Opa1. Biochim. Biophys. Acta 1787, 963–972.10.1016/j.bbabio.2009.02.005Search in Google Scholar PubMed PubMed Central

Yonashiro, R., Ishido, S., Kyo, S., Fukuda, T., Goto, E., Matsuki, Y., Ohmura-Hoshino, M., Sada, K., Hotta, H., Yamamura, H., et al. (2006). A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J 25, 3618–3626.10.1038/sj.emboj.7601249Search in Google Scholar PubMed PubMed Central

Yoon, Y., Pitts, K.R., and McNiven, M.A. (2001). Mammalian dynamin-like protein DLP1 tubulates membranes. Mol. Biol. Cell 12, 2894–2905.10.1091/mbc.12.9.2894Search in Google Scholar PubMed PubMed Central

Zanna, C., Ghelli, A., Porcelli, A.M., Karbowski, M., Youle, R.J., Schimpf, S., Wissinger, B., Pinti, M., Cossarizza, A., Vidoni, S., et al. (2008). OPA1 mutations associated with dominant optic atrophy impair oxidative phosphorylation and mitochondrial fusion. Brain 131, 352–367.10.1093/brain/awm335Search in Google Scholar PubMed

Zhao, J., Liu, T., Jin, S., Wang, X., Qu, M., Uhlen, P., Tomilin, N., Shupliakov, O., Lendahl, U., and Nister, M. (2011). Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 30, 2762–2778.10.1038/emboj.2011.198Search in Google Scholar PubMed PubMed Central

Zheng, J., Cahill, S.M., Lemmon, M.A., Fushman, D., Schlessinger, J., and Cowburn, D. (1996). Identification of the binding site for acidic phospholipids on the pH domain of dynamin: implications for stimulation of GTPase activity. J. Mol. Biol. 255, 14–21.10.1006/jmbi.1996.0002Search in Google Scholar PubMed

Zick, M., Duvezin-Caubet, S., Schafer, A., Vogel, F., Neupert, W., and Reichert, A.S. (2009). Distinct roles of the two isoforms of the dynamin-like GTPase Mgm1 in mitochondrial fusion. FEBS Lett. 583, 2237–2243.10.1016/j.febslet.2009.05.053Search in Google Scholar PubMed

Zunino, R., Schauss, A., Rippstein, P., Andrade-Navarro, M., and McBride, H.M. (2007). The SUMO protease SENP5 is required to maintain mitochondrial morphology and function. J. Cell. Sci. 120, 1178–1188.10.1242/jcs.03418Search in Google Scholar PubMed

Received: 2013-7-30
Accepted: 2013-10-31
Published Online: 2013-11-2
Published in Print: 2014-03-01

©2014 by Walter de Gruyter Berlin Boston

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