Dynamic regulation of mitochondrial function in preimplantation embryos and embryonic stem cells

Mitochondrion

Volumn 11, Issue 5, 2011, Pages 829-838

  Harvey, Alexandra ^a,d   Gibson, Tiffini ^a,b   Lonergan, Thomas ^c   Brenner, Carol ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^c WESTERN CONNECTICUT STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Biogenesis; Development; Dynamics; Embryonic stem cell; Mitochondria; Preimplantation embryo

Indexed keywords

MITOCHONDRIAL TRANSCRIPTION FACTOR A; MITOCHONDRIAL TRANSCRIPTION FACTOR B;

BIOGENESIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL MOTION; CELL STRUCTURE; CELLULAR DISTRIBUTION; DEVELOPMENTAL STAGE; DNA TRANSCRIPTION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE DOSAGE; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MICROENVIRONMENT; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRION; MOLECULAR DYNAMICS; NONHUMAN; OOCYTE DEVELOPMENT; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BLASTOCYST; DNA REPLICATION; DNA, MITOCHONDRIAL; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; GENE DOSAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MITOCHONDRIA; TRANSCRIPTION, GENETIC;

EID: 79954549447     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2010.12.013     Document Type: Review

References (124)

1. Almeida-Santos T., El Shourbagy S., St John J.C. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 2006, 85:584-591.
2. Antelman J., Manandhar G., Yi Y.J., Li R., Whitworth K.M., Sutovsky M., Agca C., Prather R.S., Sutovsky P. Expression of mitochondrial transcription factor A (TFAM) during porcine gametogenesis and preimplantation embryo development. J. Cell. Physiol. 2008, 217:529-543.
3. Asin-Cayuela J., Gustafsson C.M. Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem. Sci. 2007, 32:111-117.
4. Baar K., Wende A.R., Jones T.E., Marison M., Nolte L.A., Chen M., Kelly D.P., Holloszy J.O. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J. 2002, 16:1879-1886.
5. Bach D., Pich S., Soriano F.X., Vega N., Baumgartner B., Oriola J., Daugaard J.R., Lloberas J., Camps M., Zierath J.R., Rabasa-Lhoret R., Wallberg-Henriksson H., Laville M., Palacin M., Vidal H., Rivera F., Brand M., Zorzano A., Bach D., Pich S., Soriano F.X., Vega N., Baumgartner B., Oriola J., Daugaard J.R., Lloberas J., Camps M., Zierath J.R., Rabasa-Lhoret R., Wallberg-Henriksson H., Laville M., Palacin M., Vidal H., Rivera F., Brand M., Zorzano A. Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 2003, 278:17190-17197.
6. Barnett D.K., Kimura J., Bavister B.D. Translocation of active mitochondria during hamster preimplantation embryo development studied by confocal laser scanning microscopy. Dev. Dyn. 1996, 205:64-72.
7. Barnett D.K., Clayton M.K., Kimura J., Bavister B.D. Glucose and phosphate toxicity in hamster preimplantation embryos involves disruption of cellular organisation, including distribution of active mitochondria. Mol. Reprod. Dev. 1997, 48:227-237.
8. Barritt J.A., Kokot M., Cohen J., Steuerwald N., Brenner C.A. Quantification of human ooplasmic mitochondria. Reprod. Biomed. Online 2002, 4:243-247.
9. Bavister B.D., Squirrell J.M. Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 2000, 15(Suppl. 2):189-198.
10. Benard G., Karbowski M. Mitochondrial fusion and division: regulation and role in cell viability. Semin. Cell Dev. Biol. 2009, 20:365-374.
11. Bowles E.J., Lee J.H., Alberio R., Lloyd R.E., Stekel D., Campbell K.H., St John J.C. Contrasting effects of in vitro fertilization and nuclear transfer on the expression of mtDNA replication factors. Genetics 2007, 176:1511-1526.
12. Bowmaker M., Yang M.Y., Yasukawa T., Reyes A., Jacobs H.T., Huberman J.A., Holt I.J. Mammalian mitochondrial DNA replicates bidirectionally from an initiation zone. J. Biol. Chem. 2003, 278:50961-50969.
13. Cai Q., Sheng Z.H. Mitochondrial transport and docking in axons. Exp. Neurol. 2009, 218:257-267.
14. Campbell K., Swann K. Ca2+ oscillations stimulate an ATP increase during fertilization of mouse eggs. Dev. Biol. 2006, 298:225-233.
15. Cannino G., Di Liegro C.M., Rinaldi A.M. Nuclear-mitochondrial interaction. Mitochondrion 2007, 7:359-366.
16. Chada S.R., Hollenbeck P.J. Nerve growth factor signaling regulates motility and docking of axonal mitochondria. Curr. Biol. 2004, 14:1272-1276.
17. Chen H., Chan D.C. Emerging functions of mammalian mitochondrial fusion and fission. Hum. Mol. Genet. 2005, 14(Spec No. 2):R283-R289.
18. Chen X., Prosser R., Simonetti S., Sadlock J., Jagiello G., Schon E.A. Rearranged mitochondrial genomes are present in human oocytes. Am. J. Hum. Genet. 1995, 57:239-247.
19. Chen H., Vermulst M., Wang Y.E., Chomyn A., Prolla T.A., McCaffery J.M., Chan D.C. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010, 141:280-289.
20. Cho Y.M., Kwon S., Pak Y.K., Seol H.W., Choi Y.M., Park do J., Park K.S., Lee H.K. Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem. Biophys. Res. Commun. 2006, 348:1472-1478.
21. Clayton D.A. Replication and transcription of vertebrate mitochondrial DNA. Annu. Rev. Cell Biol. 1991, 7:453-478.
22. Detmer S.A., Chan D.C. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 2007, 8:870-879.
23. Dumollard R., Hammar K., Porterfield M., Smith P.J., Cibert C., Rouviere C., Sardet C. Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion. Development 2003, 130:683-692.
24. Dumollard R., Marangos P., Fitzharris G., Swann K., Duchen M., Carroll J. Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 2004, 131:3057-3067.
25. El Shourbagy S.H., Spikings E.C., Freitas M., St John J.C. Mitochondria directly influence fertilisation outcome in the pig. Reproduction 2006, 131:233-245.
26. Facucho-Oliveira J.M., St John J.C. The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev. 2009, 5:140-158.
27. Facucho-Oliveira J.M., Alderson J., Spikings E.C., Egginton S., St John J.C. Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J. Cell Sci. 2007, 120:4025-4034.
28. Falkenberg M., Gaspari M., Rantanen A., Trifunovic A., Larsson N.G., Gustafsson C.M. Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 2002, 31:289-294.
29. Ferreira E.M., Vireque A.A., Adona P.R., Meirelles F.V., Ferriani R.A., Navarro P.A. Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 2009, 71:836-848.
30. Fisher R.P., Clayton D.A. A transcription factor required for promoter recognition by human mitochondrial RNA polymerase. Accurate initiation at the heavy- and light-strand promoters dissected and reconstituted in vitro. J. Biol. Chem. 1985, 260:11330-11338.
31. Fisher R.P., Clayton D.A. Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell. Biol. 1988, 8:3496-3509.
32. Fisher R.P., Lisowsky T., Parisi M.A., Clayton D.A. DNA wrapping and bending by a mitochondrial high mobility group-like transcriptional activator protein. J. Biol. Chem. 1992, 267:3358-3367.
33. FitzHarris G., Larman M., Richards C., Carroll J. An increase in [Ca2+]i is sufficient but not necessary for driving mitosis in early mouse embryos. J. Cell Sci. 2005, 118:4563-4575.
34. Frazier A.E., Kiu C., Stojanovski D., Hoogenraad N.J., Ryan M.T. Mitochondrial morphology and distribution in mammalian cells. Biol. Chem. 2006, 387:1551-1558.
35. Frederick R.L., Shaw J.M. Moving mitochondria: establishing distribution of an essential organelle. Traffic 2007, 8:1668-1675.
36. Fulka H. Distribution of mitochondria in reconstructed mouse oocytes. Reproduction 2004, 127:195-200.
37. Gardner D.K., Pool T.B., Lane M. Embryo nutrition and energy metabolism and its relationship to embryo growth, differentiation, and viability. Semin. Reprod. Med. 2000, 18:205-218.
38. Garesse R., Vallejo C.G. Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes. Gene 2001, 263:1-16.
39. Gibson T.C., Kubisch H.M., Brenner C.A. Mitochondrial DNA deletions in rhesus macaque oocytes and embryos. Mol. Hum. Reprod. 2005, 11:785-789.
40. Guo X., Macleod G.T., Wellington A., Hu F., Panchumarthi S., Schoenfield M., Marin L., Charlton M.P., Atwood H.L., Zinsmaier K.E. The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 2005, 47:379-393.
41. Handschin C. The biology of PGC-1alpha and its therapeutic potential. Trends Pharmacol. Sci. 2009, 30:322-329.
42. Handschin C., Spiegelman B.M. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 2006, 27:728-735.
43. Harvey A.J., Gibson T.C., Quebedeaux T.M., Brenner C.A. Impact of assisted reproductive technologies: a mitochondrial perspective of cytoplasmic transplantation. Curr. Top. Dev. Biol. 2007, 77:229-249.
44. Hock M.B., Kralli A. Transcriptional control of mitochondrial biogenesis and function. Annu. Rev. Physiol. 2009, 71:177-203.
45. Houghton F.D., Leese H.J. Metabolism and developmental competence of the preimplantation embryo. Eur. J. Obstet. Gynecol. Reprod. Biol. 2004, 115(Suppl. 1):S92-S96.
46. Huo L., Scarpulla R.C. Mitochondrial DNA instability and peri-implantation lethality associated with targeted disruption of nuclear respiratory factor 1 in mice. Mol. Cell. Biol. 2001, 21:644-654.
47. Hyde B.B., Twig G., Shirihai O.S. Organellar vs cellular control of mitochondrial dynamics. Semin. Cell Dev. Biol. 2010, 21:575-581.
48. Hyttel P., Niemann H. Ultrastructure of porcine embryos following development in vitro versus in vivo. Mol. Reprod. Dev. 1990, 27:136-144.
49. Hyttel P., Xu K.P., Smith S., Greve T. Ultrastructure of in-vitro oocyte maturation in cattle. J. Reprod. Fertil. 1986, 78:615-625.
50. Jansen R.P., de Boer K. The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol. Cell. Endocrinol. 1998, 145:81-88.
51. Jeyaraju D.V., Cisbani G., Pellegrini L. Calcium regulation of mitochondria motility and morphology. Biochim. Biophys. Acta 2009, 1787:1363-1373.
52. Kaguni L.S. DNA polymerase gamma, the mitochondrial replicase. Annu. Rev. Biochem. 2004, 73:293-320.
53. Kameyama Y., Filion F., Yoo J.G., Smith L.C. Characterization of mitochondrial replication and transcription control during rat early development in vivo and in vitro. Reproduction 2007, 133:423-432.
54. Korhonen J.A., Gaspari M., Falkenberg M. TWINKLE has 5'→3' DNA helicase activity and is specifically stimulated by mitochondrial single-stranded DNA-binding protein. J. Biol. Chem. 2003, 278:48627-48632.
55. Koshiba T., Detmer S.A., Kaiser J.T., Chen H., McCaffery J.M., Chan D.C. Structural basis of mitochondrial tethering by mitofusin complexes. Science 2004, 305:858-862.
56. Lackner L.L., Nunnari J.M. The molecular mechanism and cellular functions of mitochondrial division. Biochim. Biophys. Acta 2009, 1792:1138-1144.
57. Lane M., Bavister B.D. Calcium homeostasis in early hamster preimplantation embryos. Biol. Reprod. 1998, 59:1000-1007.
58. Larsson N.G., Wang J., Wilhelmsson H., Oldfors A., Rustin P., Lewandoski M., Barsh G.S., Clayton D.A. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 1998, 18:231-236.
59. Liu X., Hajnoczky G. Ca2+-dependent regulation of mitochondrial dynamics by the Miro-Milton complex. Int. J. Biochem. Cell Biol. 2009, 41:1972-1976.
60. Liu L., Hammar K., Smith P.J., Inoue S., Keefe D.L. Mitochondrial modulation of calcium signaling at the initiation of development. Cell Calcium 2001, 30:423-433.
61. Liu X., Weaver D., Shirihai O., Hajnoczky G. Mitochondrial 'kiss-and-run': interplay between mitochondrial motility and fusion-fission dynamics. EMBO J. 2009, 28:3074-3089.
62. Luoh Y., Wu M. Mitochondrial distribution of swine ova and embryos analyzed by rhodamine 123 fluorescent assay. J. Chin. Soc. Anim. Sci. 1996, 25:53-66.
63. Margineantu D.H., Gregory Cox W., Sundell L., Sherwood S.W., Beechem J.M., Capaldi R.A. Cell cycle dependent morphology changes and associated mitochondrial DNA redistribution in mitochondria of human cell lines. Mitochondrion 2002, 1:425-435.
64. Mattenberger Y., James D.I., Martinou J.C. Fusion of mitochondria in mammalian cells is dependent on the mitochondrial inner membrane potential and independent of microtubules or actin. FEBS Lett. 2003, 538:53-59.
65. Mattingly K.A., Ivanova M.M., Riggs K.A., Wickramasinghe N.S., Barch M.J., Klinge C.M. Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol. Endocrinol. 2008, 22:609-622.
66. May-Panloup P., Chretien M.F., Jacques C., Vasseur C., Malthiery Y., Reynier P. Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum. Reprod. 2005, 20:593-597.
67. May-Panloup P., Vignon X., Chretien M.F., Heyman Y., Tamassia M., Malthiery Y., Reynier P. Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors. Reprod. Biol. Endocrinol. 2005, 3:65.
68. McConnell J.M., Petrie L. Mitochondrial DNA turnover occurs during preimplantation development and can be modulated by environmental factors. Reprod. Biomed. Online 2004, 9:418-424.
69. Miller K.E., Sheetz M.P. Axonal mitochondrial transport and potential are correlated. J. Cell Sci. 2004, 117:2791-2804.
70. Mitchell M., Schulz S.L., Armstrong D.T., Lane M. Metabolic and mitochondrial dysfunction in early mouse embryos following maternal dietary protein intervention. Biol. Reprod. 2009, 80:622-630.
71. Morris R.L., Hollenbeck P.J. The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J. Cell Sci. 1993, 104(Pt 3):917-927.
72. Mtango N.R., Harvey A.J., Latham K.E., Brenner C.A. Molecular control of mitochondrial function in developing rhesus monkey oocytes and preimplantation-stage embryos. Reprod Fert Dev 2008, 20:846-859.
73. Muggleton-Harris A.L., Brown J.J. Cytoplasmic factors influence mitochondrial reorganization and resumption of cleavage during culture of early mouse embryos. Hum. Reprod. 1988, 3:1020-1028.
74. Nagai S., Mabuchi T., Hirata S., Shoda T., Kasai T., Yokota S., Shitara H., Yonekawa H., Hoshi K. Oocyte mitochondria: strategies to improve embryogenesis. Hum. Cell 2004, 17:195-201.
75. Nagano M., Katagiri S., Takahashi Y. ATP content and maturational/developmental ability of bovine oocytes with various cytoplasmic morphologies. Zygote 2006, 14:299-304.
76. Naimi M., Arous C., Van Obberghen E. Energetic cell sensors: a key to metabolic homeostasis. Trends Endocrinol. Metab. 2010, 21:75-82.
77. Noto V., Campo R., Roziers P., Swinnen K., Vercruyssen M., Gordts S. Mitochondrial distribution after fast embryo freezing. Hum. Reprod. 1993, 8:2115-2118.
78. Ojuka E.O., Jones T.E., Han D.H., Chen M., Holloszy J.O. Raising Ca2+ in L6 myotubes mimics effects of exercise on mitochondrial biogenesis in muscle. FASEB J. 2003, 17:675-681.
79. Pich S., Bach D., Briones P., Liesa M., Camps M., Testar X., Palacin M., Zorzano A. The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum. Mol. Genet. 2005, 14:1405-1415.
80. Piko L., Chase D.G. Role of the mitochondrial genome during early development in mice. Effects of ethidium bromide and chloramphenicol. J. Cell Biol. 1973, 58:357-378.
81. Piko L., Matsumoto L. Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev. Biol. 1976, 49:1-10.
82. Piko L., Taylor K.D. Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev. Biol. 1987, 123:364-374.
83. Reynier P., May-Panloup P., Chretien M.F., Morgan C.J., Jean M., Savagner F., Barriere P., Malthiery Y. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 2001, 7:425-429.
84. Sansinena M.J., Lynn J., Bondioli K.R., Denniston R.S., Godke R.A. Ooplasm transfer and interspecies somatic cell nuclear transfer: heteroplasmy, pattern of mitochondrial migration and effect on embryo development. Zygote 2010, 25:1-10.
85. Sardet C., Roegiers F., Dumollard R., Rouviere C., McDougall A. Calcium waves and oscillations in eggs. Biophys. Chem. 1998, 72:131-140.
86. Scarpulla R.C. Nuclear control of respiratory gene expression in mammalian cells. J. Cell. Biochem. 2006, 97:673-683.
87. Scarpulla R.C. Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann. NY Acad. Sci. 2008, 1147:321-334.
88. Scarpulla R.C. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 2008, 88:611-638.
89. Schatten G., Simerly C., Schatten H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc. Natl Acad. Sci. USA 1985, 82:4152-4156.
90. Schultz R.M. From egg to embryo: a peripatetic journey. Reproduction 2005, 130:825-828.
91. Scott L.A., Smith S. The successful use of pronuclear embryo transfers the day following oocyte retrieval. Hum. Reprod. 1998, 13:1003-1013.
92. Seshagiri P.B., Bavister B.D. Glucose and phosphate inhibit respiration and oxidative metabolism in cultured hamster eight-cell embryos: evidence for the "crabtree effect". Mol. Reprod. Dev. 1991, 30:105-111.
93. Shadel G.S., Clayton D.A. Mitochondrial DNA maintenance in vertebrates. Annu. Rev. Biochem. 1997, 66:409-435.
94. Soriano F.X., Liesa M., Bach D., Chan D.C., Palacin M., Zorzano A. Evidence for a mitochondrial regulatory pathway defined by peroxisome proliferator-activated receptor-gamma coactivator-1 alpha, estrogen-related receptor-alpha, and mitofusin 2. Diabetes 2006, 55:1783-1791.
95. Spelbrink J.N., Li F.Y., Tiranti V., Nikali K., Yuan Q.P., Tariq M., Wanrooij S., Garrido N., Comi G., Morandi L., Santoro L., Toscano A., Fabrizi G.M., Somer H., Croxen R., Beeson D., Poulton J., Suomalainen A., Jacobs H.T., Zeviani M., Larsson C. Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat. Genet. 2001, 28:223-231.
96. Spikings E.C., Alderson J., St John J.C. Transmission of mitochondrial DNA following assisted reproduction and nuclear transfer. Hum. Reprod. Update 2006, 12:401-415.
97. Spikings E.C., Alderson J., John J.C. Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol. Reprod. 2007, 76:327-335.
98. Squirrell J.M., Lane M., Bavister B.D. Altering intracellular pH disrupts development and cellular organization in preimplantation hamster embryos. Biol. Reprod. 2001, 64:1845-1854.
99. St John J.C., Ramalho-Santos J., Gray H.L., Petrosko P., Rawe V.Y., Navara C.S., Simerly C.R., Schatten G.P. The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 2005, 7:141-153.
100. St John J.C., Amaral A., Bowles E., Oliveira J.F., Lloyd R., Freitas M., Gray H.L., Navara C.S., Oliveira G., Schatten G.P., Spikings E., Ramalho-Santos J. The analysis of mitochondria and mitochondrial DNA in human embryonic stem cells. Meth. Mol. Biol. 2006, 331:347-374.
101. Steuerwald N., Barritt J.A., Adler R., Malter H., Schimmel T., Cohen J., Brenner C.A. Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid cycle fluorescence monitored PCR. Zygote 2000, 8:209-215.
102. Stojkovic M., Machado S.A., Stojkovic P., Zakhartchenko V., Hutzler P., Goncalves P.B., Wolf E. Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 2001, 64:904-909.
103. Stowers R.S., Megeath L.J., Gorska-Andrzejak J., Meinertzhagen I.A., Schwarz T.L. Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 2002, 36:1063-1077.
104. Suen D.F., Norris K.L., Youle R.J. Mitochondrial dynamics and apoptosis. Genes Dev. 2008, 22:1577-1590.
105. Sun Q.Y., Wu G.M., Lai L., Park K.W., Cabot R., Cheong H.T., Day B.N., Prather R.S., Schatten H. Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 2001, 122:155-163.
106. Thundathil J., Filion F., Smith L.C. Molecular control of mitochondrial function in preimplantation mouse embryos. Mol. Reprod. Dev. 2005, 71:405-413.
107. Tiranti V., Savoia A., Forti F., D'Apolito M.F., Centra M., Rocchi M., Zeviani M. Identification of the gene encoding the human mitochondrial RNA polymerase (h-mtRPOL) by cyberscreening of the Expressed Sequence Tags database. Hum. Mol. Genet. 1997, 6:615-625.
108. Todd L.R., Gomathinayagam R., Sankar U. A novel Gfer-Drp1 link in preserving mitochondrial dynamics and function in pluripotent stem cells. Autophagy 2010, 6:821-822.
109. Tyynismaa H., Sembongi H., Bokori-Brown M., Granycome C., Ashley N., Poulton J., Jalanko A., Spelbrink J.N., Holt I.J., Suomalainen A. Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum. Mol. Genet. 2004, 13:3219-3227.
110. Tyynismaa H., Mjosund K.P., Wanrooij S., Lappalainen I., Ylikallio E., Jalanko A., Spelbrink J.N., Paetau A., Suomalainen A. Mutant mitochondrial helicase Twinkle causes multiple mtDNA deletions and a late-onset mitochondrial disease in mice. Proc. Natl Acad. Sci. USA 2005, 102:17687-17692.
111. Van Blerkom J. Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc. Natl Acad. Sci. USA 1991, 88:5031-5035.
112. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 2004, 128:269-280.
113. Van Blerkom J. Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online 2008, 16:553-569.
114. Van Blerkom J., Bell H., Weipz D. Cellular and developmental biological aspects of bovine meiotic maturation, fertilization, and preimplantation embryogenesis in vitro. J. Electron Microsc. Tech. 1990, 16:298-323.
115. Van Blerkom J., Davis P., Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence. Hum. Reprod. 2000, 15:2621-2633.
116. Vercauteren K., Gleyzer N., Scarpulla R.C. Short hairpin RNA-mediated silencing of PRC (PGC-1-related coactivator) results in a severe respiratory chain deficiency associated with the proliferation of aberrant mitochondria. J. Biol. Chem. 2009, 284:2307-2319.
117. Wai T., Ao A., Zhang X., Cyr D., Dufort D., Shoubridge E.A. The role of mitochondrial DNA copy number in mammalian fertility. Biol. Reprod. 2010, 83:52-62.
118. Wakefield S.L., Lane M., Schulz S.J., Hebart M.L., Thompson J.G., Mitchell M. Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E425-E434.
119. Wang Q., Ratchford A.M., Chi M.M., Schoeller E., Frolova A., Schedl T., Moley K.H. Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol. Endocrinol. 2009, 23:1603-1612.
120. Wilding M., Dale B., Marino M., di Matteo L., Alviggi C., Pisaturo M.L., Lombardi L., De Placido G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 2001, 16:909-917.
121. Yoon Y.G., Koob M.D., Yoo Y.H. Re-engineering the mitochondrial genomes in mammalian cells. Anat. Cell Biol. 2010, 43:97-109.
122. Yu Y., Dumollard R., Rossbach A., Lai F.A., Swann K. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol. 2010, 224:672-680.
123. Zorzano A., Liesa M., Palacin M. Role of mitochondrial dynamics proteins in the pathophysiology of obesity and type 2 diabetes. Int. J. Biochem. Cell Biol. 2009, 41:1846-1854.
124. Zorzano A., Hernández-Alvarez M.I., Palacín M., Mingrone G. Alterations in the mitochondrial regulatory pathways constituted by the nuclear co-factors PGC-1alpha or PGC-1beta and mitofusin 2 in skeletal muscle in type 2 diabetes. Biochim. Biophys. Acta 2010, 1797:1028-1033.