Abstract
Mitochondria exist as dynamic networks that often change shape and subcellular distribution. The number and morphology of mitochondria within a cell are controlled by precisely regulated rates of organelle fusion and fission. Recent reports have described dramatic alterations in mitochondrial morphology during the early stages of apoptotic cell death, a fragmentation of the network and the remodeling of the cristae. Surprisingly, proteins discovered to control mitochondrial morphology appear to also participate in apoptosis and proteins associated with the regulation of apoptosis have been shown to affect mitochondrial ultrastructure. In this review the recent progress in understanding the mechanisms governing mitochondrial morphology and the latest advances connecting the regulation of mitochondrial morphology with programmed cell death are discussed.
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Abbreviations
- AKAP:
-
A kinase anchoring protein
- Bif1:
-
Bax-interacting factor 1
- COX:
-
cytochrome c oxidase
- OPA1:
-
dominant optic atrophy-associated protein
- Drp1:
-
dynamin-related protein 1
- FRAP:
-
fluorescence recovery after photobleaching
- mito-GFP:
-
green fluorescent protein targeted to the mitochondrial matrix
- IMM:
-
inner mitochondrial membrane
- Mdm:
-
mitochondrial distribution and maintenance
- mtDNA:
-
mitochondrial DNA
- ΔΨm:
-
mitochondrial membrane potential
- Mmm:
-
mitochondrial morphology maintenance
- Mfn1&2:
-
mitofusins 1&2
- MEFs:
-
mouse embryonic fibroblasts
- OMM:
-
outer mitochondrial membrane
- PTP:
-
permeability transition pore
- STS:
-
staurosporine
- vMIA:
-
viral mitochondrion-localized inhibitor of apoptosis
- VDAC:
-
voltage-dependent anion-selective channel
References
Bereiter-Hahn J and Voth M (1994) Dynamics of mitochondria in living cells, shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27: 198–219
Chen LB (1988) Mitochondrial membrane potential in living cells. Annu. Rev. Cell. Biol. 4: 155–181
Rizzuto R, Simpson AW, Brini M and Pozzan T (1992) Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature 358: 325–327
Frey TG and Mannella CA (2000) The internal structure of mitochondria. Trends Biochem. Sci. 25: 319–324
Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA and Pozzan T (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280: 1763–1766
De Giorgi F, Lartigue L and Ichas F (2000) Electrical coupling and plasticity of the mitochondrial network. Cell Calcium 28: 365–370
Skulachev VP (2001) Mitochondrial filaments and clusters as intracellular power-transmitting cables. Trends Biochem. Sci. 26: 23–29
Nakada K, Inoue K, Ono T, Isobe K, Ogura A, Goto YI, Nonaka I and Hayashi JI (2001) Inter-mitochondrial complementation: mitochondria-specific system preventing mice from expression of disease phenotypes by mutant mtDNA. Nat. Med. 7: 934–940
Egner A, Jakobs S and Hell SW (2002) Fast 100-nm resolution three-dimensional microscope reveals structural plasticity of mitochondria in live yeast. Proc. Natl. Acad. Sci. USA 99: 3370–3375
Hoffmann HP and Avers CJ (1973) Mitochondrion of yeast: ultrastructural evidence for one giant, branched organelle per cell. Science 181: 749–751
Nunnari J, Marshall W, Straight A, Murray A, Sedat J and Walter P (1997) Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell. 8: 1233–1242
Collins TJ, Berridge MJ, Lipp P and Bootman MD (2002) Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 21: 1616–1627
Park MK, Ashby MC, Erdemli G, Petersen OH and Tepikin AV (2001) Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport. EMBO J. 20: 1863–1874
Gilkerson RW, Margineantu DH, Capaldi RA and Selker JML (2000) Mitochondrial DNA depletion causes morphological changes in the mitochondrial reticulum of cultured human cells. FEBS Lett. 474: 1–4
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
Bleazard W, McCaffery JM, King EJ, Bale S, Mozdy A, Tieu Q, Nunnari J and Shaw JM (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell. Biol. 1: 298–304
Sesaki H and Jensen RE (1999) Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell. Biol. 147: 699–706
Yaffe MP (1999) The machinery of mitochondrial inheritance and behavior. Science 283: 1493–1497
Dimmer KS, Fritz S, Fuchs F, Messerschmitt M, Weinbach N, Neupert W and Westermann B . (2002) Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell., 13: 847–853
Sogo LF and Yaffe MP (1994) Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. J. Cell. Biol. 126: 1361–1373
Burgess SM, Delannoy M and Jensen RE (1994) MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J. Cell. Biol., 126: 1375–1391
Berger KH, Sogo LF and Yaffe MP (1997) Mdm12p, a component required for mitochondrial inheritance that is conserved between budding and fission yeast. J. Cell. Biol., 136: 545–553
Boldogh I, Vojtov N, Karmon S and Pon LA (1998) Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p. J. Cell Biol., 141: 1371–1381
Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, Harada A and Hirokawa N (1998) Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93: 1147–1158
Nangaku M, Sato-Yoshitake R, Okada Y, Noda Y, Takemura R, Yamazaki H and Hirokawa N (1994) KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79: 1209–1220
Hinshaw JE (2000) Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16: 483–519
van der Bliek AM (1999) Functional diversity in the dynamin family. Trends Cell. Biol. 9: 96–102
Otsuga D, Keegan BR, Brisch E, Thatcher JW, Hermann GJ, Bleazard W and Shaw JM . (1998) The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell. Biol., 143: 333–349
Shepard KA, Yaffe MP (1999) The yeast dynamin-like protein, Mgm1p, functions on the mitochondrial outer membrane to mediate mitochondrial inheritance. J. Cell Biol., 144: 711–720
Wong ED, Wagner JA, Gorsich SW, McCaffery JM, Shaw JM 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
Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, Astarie-Dequeker C, Lasquellec L, Arnaud B, Ducommun B, Kaplan J and Hamel CP (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26: 207–210
Imoto M, Tachibana I and Urrutia R (1998) Identification and functional characterization of a novel human protein highly related to the yeast dynamin-like GTPase Vps1p. J. Cell. Sci. 111 (Part 10): 1341–1349
Labrousse AM, Zappaterra MD, Rube DA and van der Bliek AM (1999) C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol. Cell 4: 815–826
Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, Moore A, Rodriguez M, Kellner U, Leo-Kottler B, Auburger G, Bhattacharya SS and Wissinger B (2000) OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26: 211–215
Misaka T, Miyashita T and Kubo Y (2002) Primary structure of a dynamin-related mouse mitochondrial GTPase and its distribution in brain, subcellular localization, and effect on mitochondrial morphology. J. Biol. Chem., 277: 15834–15842
Shin HW, Shinotsuka C, Torii S, Murakami K and Nakayama K (1997) Identification and subcellular localization of a novel mammalian dynamin-related protein homologous to yeast Vps1p and Dnm1p. J. Biochem. (Tokyo) 122: 525–530
Yoon Y, Pitts KR, Dahan S and McNiven MA . (1998) A novel dynamin-like protein associates with cytoplasmic vesicles and tubules of the endoplasmic reticulum in mammalian cells. J. Cell. Biol., 140: 779–793
Kamimoto T, Nagai Y, Onogi H, Muro Y, Wakabayashi T and Hagiwara M (1998) Dymple, a novel dynamin-like high molecular weight GTPase lacking a proline-rich carboxyl-terminal domain in mammalian cells. J. Biol. Chem. 273: 1044–1051
Smirnova E, Griparic L, Shurland D-L and van der Bliek AM . (2001) Dynamin-related Protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell., 12: 2245–2256
Cerveny KL, McCaffery JM and Jensen RE (2001) Division of mitochondria requires a novel DNM1-interacting protein, Net2p. Mol. Biol. Cell., 12: 309–321
Fekkes P, Shepard KA and Yaffe MP (2000) Gag3p, an outer membrane protein required for fission of mitochondrial tubules. J. Cell. Biol., 151: 333–340
Mozdy AD, McCaffery JM and Shaw JM . (2000) Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J. Cell. Biol. 151: 367–380
Tieu Q and Nunnari J . (2000) Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division. J. Cell. Biol. 151: 353–366
Tieu Q, Okreglak V, Naylor K and Nunnari J (2002) The WD repeat protein, Mdv1p, functions as a molecular adaptor by interacting with Dnm1p and Fis1p during mitochondrial fission. J. Cell. Biol. 158: 445–452
Fukushima NH, Brisch E, Keegan BR, Bleazard W and Shaw JM . (2001) The GTPase effector domain sequence of the Dnm1p GTPase regulates self-assembly and controls a rate-limiting step in mitochondrial fission. Mol. Biol. Cell. 12: 2756–2766
Shin H-W, Takatsu H, Mukai H, Munekata E, Murakami K, Nakayama K (1999) Intermolecular and interdomain interactions of a dynamin-related GTP-binding protein, Dnm1p/Vps1p-like protein. J. Biol. Chem. 274: 2780–2785
Hinshaw JE and Schmid SL (1995) Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374: 190–192
Koch A, Thiemann M, Grabenbauer M, Yoon Y, McNiven MA and Schrader M (2002) The dynamin-like protein DLP1 is involved in peroxisomal fission. J. Biol. Chem. 278: 8597–8605
Takai Y, Sasaki T and Matozaki T (2001) Small GTP-binding proteins. Physiol. Rev. 81: 153–208
Alto NM, Soderling J and Scott JD (2002) Rab32 is an A-kinase anchoring protein and participates in mitochondrial dynamics. J. Cell Biol. 158: 659–668
Hales KG and Fuller MT (1997) Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell. 90: 121–129
Rapaport D, Brunner M, Neupert W and Westermann B (1998) Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J. Biol. Chem. 273: 20150–20155
Hermann GJ, Thatcher JW, Mills JP, Hales KG, Fuller MT, Nunnari J and Shaw JM (1998) Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell. Biol. 143: 359–373
Santel A and Fuller M (2001) Control of mitochondrial morphology by a human mitofusin. J. Cell. Sci. 114: 867–874
Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE and Chan DC (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell. Biol. 160: 189–200
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
Fritz S, Rapaport D, Klanner E, Neupert W and Westermann B (2001) Connection of the mitochondrial outer and inner membranes by Fzo1 is critical for organellar fusion. J. Cell. Biol. 152: 683–692
Karbowski M, Lee Y-J, Gaume B, Jeong S-Y, Frank S, Nechushtan A, Santel A, Fuller M, Smith CL and Youle RJ . (2002) Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell. Biol. 159: 931–938
Sesaki H and Jensen RE (2001) UGO1 Encodes an Outer Membrane Protein Required for Mitochondrial Fusion. J. Cell. Biol. 152: 1123–1134
Olichon A, Emorine LJ, Descoins E, Pelloquin L, Brichese L, Gas N, Guillou E, Delettre C, Valette A, Hamel CP, Ducommun B, Lenaers G and Belenguer P (2002) The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett. 523: 171–176
Zamzami N, Marchetti P, Castedo M, Zanin C, Vayssiere JL, Petit PX and Kroemer G . (1995) Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181: 1661–1672
Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S and Korsmeyer SJ (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell. 2: 183–192
Wei MC, Zong W-X, Cheng EH-Y, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB and Korsmeyer SJ . (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727–730
Shimizu S, Narita M and Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 483–487
Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC and Kroemer G (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027–2031
Antonsson B, Conti F, Ciavatta A, Montessuit S, Lewis S, Martinou I, Bernasconi L, Bernard A, Mermod JJ, Mazzei G, Maundrell K, Gambale F, Sadoul R and Martinou JC (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277: 370–372
Schlesinger PH, Gross A, Yin XM, Yamamoto K, Saito M, Waksman G and Korsmeyer SJ (1997) Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc. Natl. Acad. Sci. USA 94: 11357–11362
Kluck RM, Esposti MD, Perkins G, Renken C, Kuwana T, Bossy-Wetzel E, Goldberg M, Allen T, Barber MJ, Green DR and Newmeyer DD (1999) The pro-apoptotic Proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J. Cell. Biol. 147: 809–822
von Ahsen O, Renken C, Perkins G, Kluck RM, Bossy-Wetzel E and Newmeyer DD (2000) Preservation of mitochondrial structure and function after Bid- or Bax-mediated cytochrome c release. J. Cell. Biol. 150: 1027–1036
Scorrano L, Ashiya M, Buttle K, Weiller S, Oakes SA, Mannella CA and Korsmeyer SJ (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell. 2: 55–67
Esposti MD, Erler JT, Hickman JA and Dive C (2001) Bid, a widely expressed proapoptotic protein of the Bcl-2 family, displays lipid transfer activity. Mol. Cell. Biol. 21: 7268–7276
Epand RF, Martinou J-C, Fornallaz-Mulhauser M, Hughes DW and Epand RM (2002) The apoptotic protein tBid promotes leakage by altering membrane curvature. J. Biol. Chem. 277: 32632–32639
Paumard P, Vaillier J, Coulary B, Schaeffer J, Soubannier V, Mueller DM, Brethes D, di Rago J-P and Velours J (2002) The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21: 221–230
Olichon A, Baricault L, Gas N, Guillou E, Valette A, Belenguer P and Lenaers G (2002) Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278: 7743–7746
Desagher S and Martinou JC (2000) Mitochondria as the central control point of apoptosis. Trends Cell. Biol. 10: 369–377
Capano M and Crompton M (2002) Biphasic translocation of Bax to mitochondria. Biochem. J. 367: 169–178
Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F, Smith CL and Youle RJ (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell. 1: 515–525
Pinton P, Ferrari D, Rapizzi E, Virgilio FD, Pozzan T and Rizzuto R (2001) The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J. 20: 2690–2701
Rapizzi E, Pinton P, Szabadkai G, Wieckowski MR, Vandecasteele G, Baird G, Tuft RA, Fogarty KE and Rizzuto R . (2002) Recombinant expression of the voltage-dependent anion channel enhances the transfer of Ca2+ microdomains to mitochondria. J. Cell Biol. 159: 613–624
Mancini M, Anderson BO, Caldwell E, Sedghinasab M, Paty PB and Hockenbery DM . (1997) Mitochondrial proliferation and paradoxical membrane depolarization during terminal differentiation and apoptosis in a human colon carcinoma cell line. J. Cell. Biol. 138: 449–469
Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O'Neill R, Schickli J, Palese P, Henklein P, Bennink JR and Yewdell JW (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med. 7: 1306–1312
Breckenridge DG, Stojanovic M, Marcellus RC and Shore GC (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
Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG and Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell. Biol. 139: 1281–1292
Nechushtan A, Smith CL, Lamensdorf I, Yoon S-H and Youle RJ (2001) Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J. Cell. Biol. 153: 1265–1276
Cuddeback SM, Yamaguchi H, Komatsu K, Miyashita T, Yamada M, Wu C, Singh S and Wang H-G (2001) Molecular cloning and characterization of Bif-1. A NOVEL Src HOMOLOGY 3 DOMAIN-CONTAINING PROTEIN THAT ASSOCIATES WITH Bax. J. Biol. Chem. 276: 20559–20565
Pierrat B, Simonen M, Cueto M, Mestan J, Ferrigno P and Heim J (2001) SH3GLB, a new endophilin-related protein family featuring an SH3 domain. Genomics 71: 222–234
Farsad K, Ringstad N, Takei K, Floyd SR, Rose K and De Camilli P . (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell. Biol. 155: 193–200
Yamaguchi H, Paranawithana SR, Lee MW, Huang Z, Bhalla KN and Wang H-G (2002) Epothilone B analogue (BMS-247550)-mediated cytotoxicity through induction of bax conformational change in human breast cancer cells. Cancer Res. 62: 466–471
Ringstad N, Gad H, Low P, Di Paolo G, Brodin L, Shupliakov O and De Camilli P (1999) Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24: 143–154
Schmidt A, Wolde M, Thiele C, Fest W, Kratzin H, Podtelejnikov AV, Witke W, Huttner WB and Soling HD (1999) Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401: 133–141
Hsu YT and Youle RJ (1998) Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J. Biol. Chem. 273: 10777–10783
Basanez G, Sharpe JC, Galanis J, Brandt TB, Hardwick JM 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
Nemoto Y and De Camilli P (1999) Recruitment of an alternatively spliced form of synaptojanin 2 to mitochondria by the interaction with the PDZ domain of a mitochondrial outer membrane protein. EMBO J. 18: 2991–3006
Duncan CJ, Greenaway HC, Publicover SJ, Rudge MF and Smith JL (1980) Experimental production of ‘septa’ and apparent subdivision of muscle mitochondria. J. Bioenerg. Biomembr. 12: 13–33
Csordas G, Madesh M, Antonsson B and Hajnoczky G (2002) tcBid promotes Ca2+ signal propagation to the mitochondria: control of Ca2+ permeation through the outer mitochondrial membrane. EMBO J. 21: 2198–2206
McCormick AL, Smith VL, Chow D and Mocarski ES . (2003) Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis. J. Virol. 77: 631–641
Goldmacher VS, Bartle LM, Skaletskaya A, Dionne CA, Kedersha NL, Vater CA, Han J-w, Lutz RJ, Watanabe S, Cahir McFarland ED, Kieff ED, Mocarski ES and Chittenden T . (1999) A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci USA 96: 12536–12541
Colberg-Poley AM, Patel MB, Erezo DP and Slater JE (2000) Human cytomegalovirus UL37 immediate-early regulatory proteins traffic through the secretory apparatus and to mitochondria. J. Gen. Virol. 81: 1779–1789
Kowaltowski AJ, Cosso RG, Campos CB and Fiskum G (2002) Effect of Bcl-2 overexpression on mitochondrial structure and function. J. Biol. Chem. 277: 42802–42807
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Karbowski, M., Youle, R. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ 10, 870–880 (2003). https://doi.org/10.1038/sj.cdd.4401260
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