Mitochondrial fission and apoptosis: An ongoing trial

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1763, Issue 5-6, 2006, Pages 522-530

  Parone, Philippe A ^a   Martinou, Jean Claude ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Apoptosis; Cytochrome c; Fission; Fusion; Mitochondria; Mitochondrial membrane permeabilisation

Indexed keywords

CELL PROTEIN; CYTOCHROME C;

APOPTOSIS; CELL DEATH; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CELL ORGANELLE; CELL STRUCTURE; CYTOTOXICITY; HOMEOSTASIS; HUMAN; METAZOON; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW;

ANIMALS; APOPTOSIS; HUMANS; MITOCHONDRIA;

ANIMALIA; METAZOA;

EID: 33745742159     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2006.04.005     Document Type: Review

References (104)

1. Leist M., and Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev., Mol. Cell Biol. 2 (2001) 589-598
2. Hacker G. The morphology of apoptosis. Cell Tissue Res. 301 (2000) 5-17
3. Hengartner M.O. The biochemistry of apoptosis. Nature 407 (2000) 770-776
4. Lavrik I., Golks A., and Krammer P.H. Death receptor signaling. J. Cell Sci. 118 (2005) 265-267
5. Martinou J.C., and Green D.R. Breaking the mitochondrial barrier. Nat. Rev., Mol. Cell Biol. 2 (2001) 63-67
6. Zamzami N., and Kroemer G. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev., Mol. Cell Biol. 2 (2001) 67-71
7. Parone P.A., James D., and Martinou J.C. Mitochondria: regulating the inevitable. Biochimie 84 (2002) 105-111
8. Cory S., and Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev., Cancer 2 (2002) 647-656
9. Bouchier-Hayes L., Lartigue L., and Newmeyer D.D. Mitochondria: pharmacological manipulation of cell death. J. Clin. Invest. 115 (2005) 2640-2647
10. Huang D.C., and Strasser A. BH3-only proteins-Essential initiators of apoptotic cell death. Cell 103 (2000) 839-842
11. Green D.R., and Kroemer G. The pathophysiology of mitochondrial cell death. Science 305 (2004) 626-629
12. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., and Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell. 1 (2001) 515-525
13. Okamoto K., and Shaw J.M. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 39 (2005) 503-536
14. Meeusen S.L., and Nunnari J. How mitochondria fuse. Curr. Opin. Cell Biol. 17 (2005) 389-394
15. Tondera D., Santel A., Schwarzer R., Dames S., Giese K., Klippel A., and Kaufmann J. Knockdown of MTP18, a novel phosphatidylinositol 3-kinase-dependent protein, affects mitochondrial morphology and induces apoptosis. J. Biol. Chem. 279 (2004) 31544-31555
16. Tondera D., Czauderna F., Paulick K., Schwarzer R., Kaufmann J., and Santel A. The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J. Cell Sci. 118 (2005) 3049-3059
17. Niemann A., Ruegg M., La Padula V., Schenone A., and Suter U. Ganglioside-induced differentiation associated protein 1 is a regulator of the mitochondrial network: new implications for Charcot-Marie-Tooth disease. J. Cell Biol. 170 (2005) 1067-1078
18. Pedrola L., Espert A., Wu X., Claramunt R., Shy M.E., and Palau F. GDAP1, the protein causing Charcot-Marie-Tooth disease type 4A, is expressed in neurons and is associated with mitochondria. Hum. Mol. Genet. 14 (2005) 1087-1094
19. Pitts K.R., Yoon Y., Krueger E.W., and McNiven M.A. The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol. Biol. Cell 10 (1999) 4403-4417
20. Smirnova E., Griparic L., Shurland D.L., and van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12 (2001) 2245-2256
21. Smirnova E., Shurland D.L., Ryazantsev S.N., and van der Bliek A.M. A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143 (1998) 351-358
22. Yu T., Fox R.J., Burwell L.S., and Yoon Y. Regulation of mitochondrial fission and apoptosis by the mitochondrial outer membrane protein hFis1. J. Cell Sci. 118 (2005) 4141-4151
23. Yoon Y., Krueger E.W., Oswald B.J., and McNiven M.A. The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell. Biol. 23 (2003) 5409-5420
24. Stojanovski D., Koutsopoulos O.S., Okamoto K., and Ryan M.T. Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology. J. Cell Sci. 117 (2004) 1201-1210
25. James D.I., Parone P.A., Mattenberger Y., and Martinou J.C. hFis1, a novel component of the mammalian mitochondrial fission machinery. J. Biol. Chem. 278 (2003) 36373-36379
26. Bossy-Wetzel E., Barsoum M.J., Godzik A., Schwarzenbacher R., and Lipton S.A. Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr. Opin. Cell Biol. 15 (2003) 706-716
27. Bardon S., Vignon F., Montcourrier P., and Rochefort H. Steroid receptor-mediated cytotoxicity of an antiestrogen and an antiprogestin in breast cancer cells. Cancer Res. 47 (1987) 1441-1448
28. Belloni A.S., Vassanelli P., Robba C., Rebuffat P., Mazzocchi G., and Nussdorfer G.G. Ultrastructural observations on the regeneration of adrenocortical autotransplants in the rat spleen. J. Anat. 135 (1982) 245-253
29. Kerr J.F., Wyllie A.H., and Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 (1972) 239-257
30. Russell S.W., Rosenau W., and Lee J.C. Cytolysis induced by human lymphotoxin. Am. J. Pathol. 69 (1972) 103-118
31. Sheridan J.W., Bishop C.J., and Simmons R.J. Biophysical and morphological correlates of kinetic change and death in a starved human melanoma cell line. J. Cell Sci. 49 (1981) 119-137
32. Hackenbrock C.R. Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states. Proc. Natl. Acad. Sci. U. S. A. 61 (1968) 598-605
33. Wachstein M., and Besen M. Electron microscopy of renal coagulative necrosis due to Dl-Serine, with special reference to mitochondrial pyknosis. Am. J. Pathol. 44 (1964) 383-400
34. Rouiller C. Electron microscopy for the study of the normal and pathological liver. Ann. Anat. Pathol. (Paris) 2 (1957) 548-562
35. Mannweiler K., and Bernhard W. Research on ultrastructures in an experimental renal tumor in the hamster. J. Ultrastruct. Res. 1 (1957) 158-169
36. James T.N., Terasaki F., Pavlovich E.R., and Vikhert A.M. Apoptosis and pleomorphic micromitochondriosis in the sinus nodes surgically excised from five patients with the long QT syndrome. J. Lab. Clin. Med. 122 (1993) 309-323
37. Mancini M., Anderson B.O., Caldwell E., Sedghinasab M., Paty P.B., and Hockenbery D.M. Mitochondrial proliferation and paradoxical membrane depolarization during terminal differentiation and apoptosis in a human colon carcinoma cell line. J. Cell Biol. 138 (1997) 449-469
38. Zhuang J., Dinsdale D., and Cohen G.M. Apoptosis, in human monocytic THP.1 cells, results in the release of cytochrome c from mitochondria prior to their ultracondensation, formation of outer membrane discontinuities and reduction in inner membrane potential. Cell Death Differ. 5 (1998) 953-962
39. Martinou I., Desagher S., Eskes R., Antonsson B., Andre E., Fakan S., and Martinou J.C. The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J. Cell Biol. 144 (1999) 883-889
40. De Vos K., Goossens V., Boone E., Vercammen D., Vancompernolle K., Vandenabeele P., Haegeman G., Fiers W., and Grooten J. The 55-kDa tumor necrosis factor receptor induces clustering of mitochondria through its membrane-proximal region. J. Biol. Chem. 273 (1998) 9673-9680
41. Breckenridge D.G., Stojanovic M., Marcellus R.C., and Shore G.C. Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J. Cell Biol. 160 (2003) 1115-1127
42. Karbowski M., Arnoult D., Chen H., Chan D.C., Smith C.L., and Youle R.J. Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis. J. Cell Biol. 164 (2004) 493-499
43. 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. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 159 (2002) 931-938
44. Neuspiel M., Zunino R., Gangaraju S., Rippstein P., and McBride H. Activated mitofusin 2 signals mitochondrial fusion, interferes with Bax activation, and reduces susceptibility to radical induced depolarization. J. Biol. Chem. 280 (2005) 25060-25070
45. Karbowski M., Jeong S.Y., and Youle R.J. Endophilin B1 is required for the maintenance of mitochondrial morphology. J. Cell Biol. 166 (2004) 1027-1039
46. Cuddeback S.M., Yamaguchi H., Komatsu K., Miyashita T., Yamada M., Wu C., Singh S., and Wang H.G. Molecular cloning and characterization of Bif-1. A novel Src homology 3 domain-containing protein that associates with Bax. J. Biol. Chem. 276 (2001) 20559-20565
47. Sugioka R., Shimizu S., and Tsujimoto Y. Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis. J. Biol. Chem. 279 (2004) 52726-52734
48. Desagher S., Osen-Sand A., Nichols A., Eskes R., Montessuit S., Lauper S., Maundrell K., Antonsson B., and Martinou J.C. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144 (1999) 891-901
49. Rojo M., Legros F., Chateau D., and Lombes A. Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J. Cell Sci. 115 (2002) 1663-1674
50. Chen H., Detmer S.A., Ewald A.J., Griffin E.E., Fraser S.E., and Chan D.C. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160 (2003) 189-200
51. Santel A., and Fuller M.T. Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114 (2001) 867-874
52. Eura Y., Ishihara N., Yokota S., and Mihara K. Two mitofusin proteins, mammalian homologues of FZO, with distinct functions are both required for mitochondrial fusion. J. Biochem. (Tokyo) 134 (2003) 333-344
53. Arnoult D., Grodet A., Lee Y.J., Estaquier J., and Blackstone C. Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J. Biol. Chem. 280 (2005) 35742-35750
54. Esseiva A.C., Chanez A.L., Bochud-Allemann N., Martinou J.C., Hemphill A., and Schneider A. Temporal dissection of Bax-induced events leading to fission of the single mitochondrion in Trypanosoma brucei. EMBO Rep. 5 (2004) 268-273
55. Gao W., Pu Y., Luo K.Q., and Chang D.C. Temporal relationship between cytochrome c release and mitochondrial swelling during UV-induced apoptosis in living HeLa cells. J. Cell Sci. 114 (2001) 2855-2862
56. Arnoult D., Rismanchi N., Grodet A., Roberts R.G., Seeburg D.P., Estaquier J., Sheng M., and Blackstone C. Bax/Bak-dependent release of DDP/TIMM8a promotes Drp1-mediated mitochondrial fission and mitoptosis during programmed cell death. Curr. Biol. 15 (2005) 2112-2118
57. Griparic L., van der Wel N.N., Orozco I.J., Peters P.J., and van der Bliek A.M. Loss of the intermembrane space protein Mgm1/OPA1 induces swelling and localized constrictions along the lengths of mitochondria. J. Biol. Chem. 279 (2004) 18792-18798
58. Olichon A., Baricault L., Gas N., Guillou E., Valette A., Belenguer P., and Lenaers G. Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278 (2003) 7743-7746
59. Lee Y.J., Jeong S.Y., Karbowski M., Smith C.L., and Youle R.J. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol. Biol. Cell 15 (2004) 5001-5011
60. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., and Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292 (2001) 727-730
61. Antonsson B., Conti F., Ciavatta A., Montessuit S., Lewis S., Martinou I., Bernasconi L., Bernard A., Mermod J.J., Mazzei G., Maundrell K., Gambale F., Sadoul R., and Martinou J.C. Inhibition of Bax channel-forming activity by Bcl-2. Science 277 (1997) 370-372
62. Schlesinger P.H., Gross A., Yin X.M., Yamamoto K., Saito M., Waksman G., and Korsmeyer S.J. Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 11357-11362
63. Shimizu S., Narita M., and Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399 (1999) 483-487
64. Marzo I., Brenner C., Zamzami N., Jurgensmeier J.M., Susin S.A., Vieira H.L., Prevost M.C., Xie Z., Matsuyama S., Reed J.C., and Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281 (1998) 2027-2031
65. Germain M., Mathai J.P., McBride H.M., and Shore G.C. Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J. 24 (2005) 1546-1556
66. Basanez G., Nechushtan A., Drozhinin O., Chanturiya A., Choe E., Tutt S., Wood K.A., Hsu Y., Zimmerberg J., and Youle R.J. Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5492-5497
67. Basanez G., Sharpe J.C., Galanis J., Brandt T.B., Hardwick J.M., and Zimmerberg J. Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J. Biol. Chem. 277 (2002) 49360-49365
68. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., and Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2 (2002) 55-67
69. Ott M., Robertson J.D., Gogvadze V., Zhivotovsky B., and Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 1259-1263
70. Bernardi P., and Azzone G.F. Cytochrome c as an electron shuttle between the outer and inner mitochondrial membranes. J. Biol. Chem. 256 (1981) 7187-7192
71. Frey T.G., and Mannella C.A. The internal structure of mitochondria. Trends Biochem. Sci. 25 (2000) 319-324
72. Goldstein J.C., Waterhouse N.J., Juin P., Evan G.I., and Green D.R. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell Biol. 2 (2000) 156-162
73. Akao M., O'Rourke B., Teshima Y., Seharaseyon J., and Marban E. Mechanistically distinct steps in the mitochondrial death pathway triggered by oxidative stress in cardiac myocytes. Circ. Res. 92 (2003) 186-194
74. Kim T.H., Zhao Y., Ding W.X., Shin J.N., He X., Seo Y.W., Chen J., Rabinowich H., Amoscato A.A., and Yin X.M. Bid-cardiolipin interaction at mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome C release. Mol. Biol. Cell 15 (2004) 3061-3072
75. Messerschmitt M., Jakobs S., Vogel F., Fritz S., Dimmer K.S., Neupert W., and Westermann B. The inner membrane protein Mdm33 controls mitochondrial morphology in yeast. J. Cell Biol. 160 (2003) 553-564
76. Hobbs A.E., Srinivasan M., McCaffery J.M., and Jensen R.E. Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J. Cell Biol. 152 (2001) 401-410
77. John G.B., Shang Y., Li L., Renken C., Mannella C.A., Selker J.M., Rangell L., Bennett M.J., and Zha J. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol. Biol. Cell 16 (2005) 1543-1554
78. Farsad K., Ringstad N., Takei K., Floyd S.R., Rose K., and De Camilli P. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155 (2001) 193-200
79. Schmidt A., Wolde M., Thiele C., Fest W., Kratzin H., Podtelejnikov A.V., Witke W., Huttner W.B., and Soling H.D. Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401 (1999) 133-141
80. Modregger J., Schmidt A.A., Ritter B., Huttner W.B., and Plomann M. Characterization of Endophilin B1b, a brain-specific membrane-associated lysophosphatidic acid acyl transferase with properties distinct from endophilin A1. J. Biol. Chem. 278 (2003) 4160-4167
81. Pierrat B., Simonen M., Cueto M., Mestan J., Ferrigno P., and Heim J. SH3GLB, a new endophilin-related protein family featuring an SH3 domain. Genomics 71 (2001) 222-234
82. Lee E., and De Camilli P. Dynamin at actin tails. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 161-166
83. Orth J.D., Krueger E.W., Cao H., and McNiven M.A. The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 167-172
84. Fish K.N., Schmid S.L., and Damke H. Evidence that dynamin-2 functions as a signal-transducing GTPase. J. Cell Biol. 150 (2000) 145-154
85. Schlunck G., Damke H., Kiosses W.B., Rusk N., Symons M.H., Waterman-Storer C.M., Schmid S.L., and Schwartz M.A. Modulation of Rac localization and function by dynamin. Mol. Biol. Cell 15 (2004) 256-267
86. Szabadkai G., Simoni A.M., Chami M., Wieckowski M.R., Youle R.J., and Rizzuto R. Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2+ waves and protects against Ca2+-mediated apoptosis. Mol. Cell. 16 (2004) 59-68
87. Skulachev V.P. Programmed death phenomena: from organelle to organism. Ann. N. Y. Acad. Sci. 959 (2002) 214-237
88. Xue L., Fletcher G.C., and Tolkovsky A.M. Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis. Curr. Biol. 11 (2001) 361-365
89. Tolkovsky A.M., Xue L., Fletcher G.C., and Borutaite V. Mitochondrial disappearance from cells: a clue to the role of autophagy in programmed cell death and disease?. Biochimie 84 (2002) 233-240
90. Xue L., Fletcher G.C., and Tolkovsky A.M. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol. Cell. Neurosci. 14 (1999) 180-198
91. Lockshin R.A., and Zakeri Z. Caspase-independent cell deaths. Curr. Opin. Cell Biol. 14 (2002) 727-733
92. Jagasia R., Grote P., Westermann B., and Conradt B. DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death in C. elegans. Nature 433 (2005) 754-760
93. Smaili S.S., Hsu Y.T., Sanders K.M., Russell J.T., and Youle R.J. Bax translocation to mitochondria subsequent to a rapid loss of mitochondrial membrane potential. Cell Death Differ. 8 (2001) 909-920
94. Lim M.L., Minamikawa T., and Nagley P. The protonophore CCCP induces mitochondrial permeability transition without cytochrome c release in human osteosarcoma cells. FEBS Lett. 503 (2001) 69-74
95. Legros F., Lombes A., Frachon P., and Rojo M. Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol. Biol. Cell 13 (2002) 4343-4354
96. Goldmacher V.S. vMIA, a viral inhibitor of apoptosis targeting mitochondria. Biochimie 84 (2002) 177-185
97. Borutaite V., Morkuniene R., and Brown G.C. Nitric oxide donors, nitrosothiols and mitochondrial respiration inhibitors induce caspase activation by different mechanisms. FEBS Lett. 467 (2000) 155-159
98. Fitch M.E., Chang C.M., and Parslow T.G. The BH3 domain is required for caspase-independent cell death induced by Bax and oligomycin. Cell Death Differ. 7 (2000) 338-349
99. Mills K.I., Woodgate L.J., Gilkes A.F., Walsh V., Sweeney M.C., Brown G., and Burnett A.K. Inhibition of mitochondrial function in HL60 cells is associated with an increased apoptosis and expression of CD14. Biochem. Biophys. Res. Commun. 263 (1999) 294-300
100. Wolvetang E.J., Johnson K.L., Krauer K., Ralph S.J., and Linnane A.W. Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett. 339 (1994) 40-44
101. Chen H., Chomyn A., and Chan D.C. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280 (2005) 26185-26192
102. Lodi R., Tonon C., Valentino M.L., Iotti S., Clementi V., Malucelli E., Barboni P., Longanesi L., Schimpf S., Wissinger B., Baruzzi A., Barbiroli B., and Carelli V. Deficit of in vivo mitochondrial ATP production in OPA1-related dominant optic atrophy. Ann. Neurol. 56 (2004) 719-723
103. Kim J.Y., Hwang J.M., Ko H.S., Seong M.W., Park B.J., and Park S.S. Mitochondrial DNA content is decreased in autosomal dominant optic atrophy. Neurology 64 (2005) 966-972
104. Fannjiang Y., Cheng W.C., Lee S.J., Qi B., Pevsner J., McCaffery J.M., Hill R.B., Basanez G., and Hardwick J.M. Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev. 18 (2004) 2785-2797