Expression of mitochondrial transcription factor a (TFAM) during porcine gametogenesis and preimplantation embryo development

Journal of Cellular Physiology

Volumn 217, Issue 2, 2008, Pages 529-543

  Antelman, J ^a   Manandhar, G ^a   Yi, Y J ^a,b   Li, R ^a   Whitworth, K M ^a   Sutovsky, M ^a   Agca, C ^a   Prather, R S ^a   Sutovsky, P ^a,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b Chungnam National University   (South Korea)

^c University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN; UBIQUITIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYTE; CELL CULTURE; CELL FUNCTION; DEVELOPMENTAL STAGE; EMBRYO; FERTILIZATION; GAMETOGENESIS; GENE; IMMUNOREACTIVITY; MOLECULAR EVOLUTION; NONHUMAN; OOCYTE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PURIFICATION; SPERMATOZOON; SWINE; TFAM GENE; UBIQUITINATION; WESTERN BLOTTING; ZYGOTE; AFFINITY CHROMATOGRAPHY; ANIMAL; BLASTOCYST; CELL NUCLEUS TRANSPLANTATION; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; MEIOSIS; METABOLISM; MITOCHONDRION; OOCYTE DEVELOPMENT; PARTHENOGENESIS; SPERMATOGENESIS; SPERMATOZOON TAIL;

SUS; SUS SCROFA; SUS SCROFA DOMESTICA;

ANIMALS; BLASTOCYST; BLOTTING, WESTERN; CHROMATOGRAPHY, AFFINITY; DNA, MITOCHONDRIAL; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MEIOSIS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NUCLEAR TRANSFER TECHNIQUES; OOCYTES; OOGENESIS; PARTHENOGENESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; SPERM HEAD; SPERM TAIL; SPERMATOGENESIS; SPERMATOZOA; SUS SCROFA; TRANSCRIPTION FACTORS; UBIQUITIN; ZYGOTE;

EID: 51449114031     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21528     Document Type: Article

References (118)

1. Abeydeera LR, Wang WH, Prather RS, Day BN. 1998. Maturation in vitro of pig oocytes in protein-free culture media: Fertilization and subsequent embryo development in vitro. Biol Reprod 58:1316-1320.
2. Agca C, Fritz J, Walker L, Levey A, Chan A, Lah J, Agca Y. 2008. Development of transgenic rats producing human beta-amyloid precursor protein as a model for Alzheimer's disease: Transgene and endogenous APP genes are regulated tissue-specifically. BMC Neurosci 9:28.
3. Alcolea MP, Colom B, Llado I, Gianotti M, Garcia-Palmer FJ. 2006. Mitochondrial transcription factor A (TFAM) is increased in rat embryo during placentation and associated with mitochondrial differentiation. Cell Physiol Biochem 17:79-88.
4. Ankel-Simons F, Cummins JM. 1996. Misconceptions about mitochondria and mammalian fertilization: Implications for theories on human evolution. Proc Natl Acad Sci USA 93:13859-13863.
5. Aoyama H, Hagiwara Y, Misumi O, Kuroiwa T, Nakamura S. 2006. Complete elimination of maternal mitochondrial DNA during meiosis resulting in the paternal inheritance of the mitochondrial genome in Chlamydomonas species. Protoplasma 228:231-242.
6. Appleyard GD, Forsyth GW, Kiehlbauch LM, Sigfrid KN, Hanik HL, Quon A, Loewen ME, Grahn BH. 2006. Differential mitochondrial DNA and gene expression in inherited retinal dysplasia in miniature Schnauzer dogs. Invest Ophthalmol Vis Sci 47:1810-1816.
7. Baker HW. 1994. Clinical male infertility. II. Critical evaluation of the prospects for therapy. Reprod Fertil Dev 6:9-12.
8. Barnett DK, Kimura J, Bavister BD. 1996. Translocation of active mitochondria during hamster preimplantation embryo development studied by confocal laser scanning microscopy. Dev Dyn 205:64-72.
9. Barritt JA, Brenner CA, Malter HE, Cohen J. 2001a. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod 16:513-516.
10. Barritt JA, Brenner CA, Malter HE, Cohen J. 2001 b. Rebuttal: Interooplasmic transfers in humans. Reprod Biomed Online 3:47-48.
11. Barritt JA, Kokot M, Cohen J, Steuerwald N, Brenner CA. 2002. Quantification of human ooplasmic mitochondria. Reprod Biomed Online 4:243-247.
12. Bavister BD. 2006. The mitochondrial contribution to stem cell biology. Reprod Fertil Dev 18:829-838.
13. Bavister BD, Squirrell JM. 2000. Mitochondrial distribution and function in oocytes and early embryos. Hum Reprod 15:189-198.
14. Birky CW, Jr. 1995. Uniparental inheritance of mitochondrial and chloroplast genes: Mechanisms and evolution. Proc Natl Acad Sci USA 92:11331-11338.
15. Birky CW, Jr. 2001. The inheritance of genes in mitochondria and chloroplasts: Laws, mechanisms, and models. Annu Rev Genet 35:125-148.
16. Bowles EJ, Campbell KH, St John JC. 2007a. Nuclear transfer: Preservation of a nuclear genome at the expense of its associated mtDNA genome(s). Curr Top Dev Biol 77:251-290.
17. Bowles EJ, Lee JH, Alberio R, Lloyd RE, Stekel D, Campbell KH, St John JC. 2007b. Contrasting effects of in vitro fertilization and nuclear transfer on the expression of mtDNA replication factors. Genetics 176:1511-1526.
18. Calarco PG. 1995. Polarization of mitochondria in the unfertilized mouse oocyte. Dev Genet 16:36-43.
19. Ciechanover A, Elias S, Heller H, Ferber S, Hershko A. 1980. Characterization of the heat-stable polypeptide of the ATP-dependent proteolytic system from reticulocytes. J Biol Chem 2S5:7525-7528.
20. Clayton DA. 1998. Nuclear-mitochondrial intergenomic communication. Biofactors 7:203-205.
21. Cogswell AT, Kenchington EL, Zouros E. 2006. Segregation of sperm mitochondria in two-and four-cell embryos of the blue mussel Mytilus edulis: Implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. Genome 49:799-807.
22. Cran DG. 1985. Qualitative and quantitative structural changes during pig oocyte maturation. J Reprod Fertil 74:237-245.
23. Cummins JM, Jequier AM, Kan R. 1994. Molecular biology of human male infertility: Links with aging, mitochondrial genetics, and oxidative stress? Mol Reprod Dev 37:34S-362.
24. Cummins JM, Wakayama T, Yanagimachi R. 1998. Fate of microinjected spermatid mitochondria in the mouse oocyte and embryo. Zygote 6:213-222.
25. Debray FG, Lambert M, Chevalier I, Robitaille Y, Decarie JC, Shoubridge EA, Robinson BH, Mitchell GA. 2007. Long-term outcome and clinical spectrum of 73 pediatric patients with mitochondrial diseases. Pediatrics 119:722-733.
26. DeRenzo C, Seydoux G. 2004. A. clean start: Degradation of maternal proteins at the oocyte-to-embryo transition. Trends Cell Biol 14:420-426.
27. Diez-Sanchez C, Ruiz-Pesini E, Lapena AC, Montoya J, Perez-Martos A, Enriquez JA, Lopez-Perez MJ. 2003. Mitochondrial DNA content of human spermatozoa. Biol Reprod 68:180-185.
28. Dumollard R, Marangos P, Fitzharris G, Swann K, Duchen M, Carroll J. 2004. Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131:3057-3067.
29. Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M, Hultenby K, Rustin P, Gustafsson CM, Larsson NG. 2004. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet 13:935-944.
30. El Shourbagy SH, Spikings EC, Freitas M, St John JC. 2006. Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131:233-245.
31. Escalier D. 2003. New insights into the assembly of the periaxonemal structures in mammalian spermatozoa. Biol Reprod 69:373-378.
32. Escalier D, Bai XY, Silvius D, Xu PX, Xu X. 2003. Spermatid nuclear and sperm periaxonemal anomalies in the mouse Ube2b null mutant. Mol Reprod Dev 65:298-308.
33. Fisher RP, Clayton DA. 1988. Purification and characterization of human mitochondrial transcription factor I. Mol Cell Biol 8:3496-3509.
34. Folgero T, Bertheussen K, Lindal S, Torbergsen T, Oian P. 1993. Mitochondrial disease and reduced sperm motility. Hum Reprod 8:1863-1868.
35. Hecht NB, Liem H, Kleene KC, Distel RJ, Ho SM. 1984. Maternal inheritance of the mouse mitochondrial genome is not mediated by a loss or gross alteration of the paternal mitochondrial DNA or by methylation of the oocyte mitochondrial DNA. Dev Biol 102:452-461.
36. Hesselink MK, Mensink M, Schrauwen P. 2003. Human uncoupling protein-3 and obesity: An update. Obes Res 11:1429-1443.
37. Hiendleder S. 2007. Mitochondrial DNA inheritance after SCNT. Adv Exp Med Biol 591:103-116.
38. Hudson G, Chinnery PF. 2006. Mitochondrial DNA polymerase-gamma and human disease. Hum Mol Genet 15, R244-R252.
39. Igarashi H, Takahashi T, Takahashi E, Tezuka N, Nakahara K, Takahashi K, Kurachi H. 2005. Aged mouse oocytes fail to readjust intracellular adenosine triphosphates at fertilization. Biol Reprod 72:1256-1261.
40. Ikeuchi M, Matsusaka H, Kang D, Matsushima S, lde T, Kubota T, Fujiwara T, Hamasaki N, Takeshita A, Sunagawa K, et al. 2005. Overexpression of mitochondrial transcription factor a ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation 112:683-690.
41. Im GS, Lai L, Liu Z, Hao Y, Wax D, Bonk A, Prather RS. 2004. In vitro development of preimplantation porcine nuclear transfer embryos cultured in different media and gas atmospheres. Theriogenology 61:1125-1135.
42. Jansen RP, de Boer K. 1998. The bottleneck: Mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol 145:81-88.
43. Jose-Miller AB, Boyden JW, Frey KA. 2007. Infertility. Am Fam Physician 75:849-856.
44. Kameyama Y, Filion F, Yoo JG, Smith LC. 2007. Characterization of mitochondrial replication and transcription control during rat early development in vivo and in vitro. Reproduction 133:423-432.
45. Kaneda H, Hayashi J, Takahama S, Taya C, Lindahl KF, Yonekawa H. 1995. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92:4542-4546.
46. Kang D, Kim SH, Hamasaki N. 2007. Mitochondrial transcription factor A (TFAM): Roles in maintenance of mtDNA and cellular functions. Mitochondrion 7:39-44.
47. Kanki T, Ohgaki K, Gaspari M, Gustafsson CM, Fukuoh A, Sasaki N, Hamasaki N, Kang D. 2004. Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol Cell Biol 24:9823-9834.
48. Kierszenbaum AL. 2002. Intramanchette transport (IMT): Managing the making of the spermatid head, centrosome, and tail. Mol Reprod Dev 63:1-4.
49. Kim JH, Machaty Z, Cabot RA, Han YM, Do HJ, Prather RS. 1998. Development of pig oocytes activated by stimulation of an exogenous G protein-coupled receptor. Biol Reprod 59:655-660.
50. Kolber-Simonds D, Lai L, Watt SR, Denaro M, Arn S, Augenstein ML, Betthauser J, Carter DB, Greenstein JL, Hao Y, et al. 2004. Production of alpha-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations. Proc Natl Acad Sci USA 101:7335-7340.
51. Krause WJ, Charlson EJ, Sherman DM, Day BN. 1992. Three-dimensional reconstruction using a computer graphics System: Application to mitochondrial aggregates in porcine oocytes, zygotes, and early embryos usinga personal computer. Zoologischer Anz 229:21-36.
52. Kuroiwa T. 1991. The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128:1-62.
53. Kuusisto E, Suuronen T, Salminen A. 2001. Ubiquitin-binding protein p62 expression is induced during apoptosis and proteasomal inhibition in neuronal cells. Biochem Biophys Res Commun 280:223-228.
54. Lai L, Kolber-Simonds D, Park KW, Cheong HT, Greenstein JL, Im GS, Samuel M, Bonk A, Rieke A, Day BN, etal. 2002a. Production of alpha-1,3- galactosyltransferase knockout pigs by nuclear transfer cloning. Science 295:1089-1092.
55. Lai L, Park KW, Cheong HT, Kuhholzer B, Samuel M, Bonk A, Im GS, Rieke A, Day BN, Murphy CN, et al. 2002b. Transgenic pig expressing the enhanced green fluorescent protein produced by nuclear transfer using colchicine-treated fibroblasts as donor cells. Mol Reprod Dev 62:300-306.
56. Larsson NG, Oldfors A, Holme E, Clayton DA. 1994. Low levels of mitochondrial transcription factor A in mitochondrial DNA depletion. Biochem Biophys Res Commun 200:1374-1381.
57. Larsson NG, Garman JD, Oldfors A, Barsh GS, Clayton DA. 1996. A single mouse gene encodes the mitochondrial transcription factor A and a testis-specific nuclear HMG-box protein. Nat Genet 13:296-302.
58. Larsson NG, Barsh GS, Clayton DA. 1997a. Structure and chromosomal localization of the mouse mitochondrial transcription factor A gene (Tfam). Mamm Genome 8:139-140.
59. Larsson NG, Oldfors A, Garman JD, Barsh GS, Clayton DA. 1997b. Down-regulation of mitochondrial transcription factor A during spermatogenesis in humans. Hum Mol Genet 6:185-191.
60. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, Barsh GS, Clayton DA. 1998. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 18:231-236.
61. Latham KE, Gao S, Han Z. 2007. Somatic cell nuclei in cloning: Strangers traveling in a foreign land. Adv Exp Med Biol 591:14-29.
62. Li JF, Zhang JH. 2004. Progress in ooplasmic transfer. Yi Chuan 26:373-376.
63. Lovercamp KW, Safranski TJ, Fischer KA, Manandhar G, Sutovsky M, Herring W, Sutovsky P. 2007. Arachidonate 15-lipoxygenase and ubiquitin as fertility markers in boars. Theriogenology 67:704-718.
64. Machaty Z, Wang WH, Day BN, Prather RS. 1997. Complete activation of porcine oocytes induced by the sulfhydryl reagent, thimerosal. Biol Reprod 57:1123-1127.
65. Manandhar G, Feng D, Yi YJ, Lai L, Letko J, Laurincik J, Sutovsky M, Salisbury JL, Prather RS, Schatten H, et al. 2006. Centrosomal protein centrin is not detectable during early pre-implantation development but reappears during late blastocyst stage in porcine embryos. Reproduction 132:423-434.
66. May-Panloup P, Chretien MF, Savagner F, Vasseur C, Jean M, Malthiery Y, Reynier P. 2003. Increased sperm mitochondrial DNA content in male infertility. Hum Reprod 18:550-556.
67. May-Panloup P, Chretien MF, Malthiery Y, Reynier P. 2006. Spermatozoon mitochondrial DNA. Gynecol Obstet Fertil 34:847-854.
68. Miranda-Vizuete A, Tsang K, Yu Y, Jimenez A, Pelto-Huikko M, Flickinger CJ, Sutovsky P, Oko R. 2003. Cloning and developmental analysis of murid spermatid-specific thioredoxin-2 (SPTRX-2), a novel sperm fibrous sheath protein and autoantigen. J Biol Chem 278:44874-44885.
69. Moyes CD, Battersby BJ, Leary SC. 1998. Regulation of muscle mitochondrial design. J Exp Biol 201:299-307.
70. Muller-Hocker J, Schafer S, Copeland WC, Wiesner R, Seibel P. 1998. Immunohistochemical detection of human mtDNA polymerase gamma and of human mitochondrial transcription factor A in cytochrome-c-oxidase-deficient oxyphil cells of hyperfunctional parathyroids. Virchows Arch 433:529-536.
71. Nagai S, Mabuchi T, Hirata S, Shoda T, Kasai T, Yokota S, Shitara H, Yonekawa H, Hoshi K. 2004. Oocyte mitochondria: Strategies to improve embryogenesis. Hum Cell 17:195-201.
72. Nagy A, Wilhelm M, Kovacs G. 2003. Mutations of mtDNA in renal cell tumours arising in end-stage renal disease. J Pathol 199:237-242.
73. Nishimura Y, Yoshinari T, Naruse K, Yamada T, Sumi K, Mitani H, Higashiyama T, Kuroiwa T. 2006. Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers. Proc Natl Acad Sci USA 103:1382-1387.
74. Oko R. 1998. Occurrence and formation of cytoskeletal proteins in mammalian spermatozoa. Andrologia 30:193-206.
75. Petters RM, Wells KD. 1993. Culture of pig embryos. J Reprod Fertil Suppl 48:61-73.
76. Pitnick S, Karr TL. 1998. Paternal products and by-products in Drosophila development. Proc Biol Sci 265:821-826.
77. Poulton J, Morten K, Freeman-Emmerson C, Potter C, Sewry C, Dubowitz V, Kidd H, Stephenson J, Whitehouse W, Hansen FJ, et al. 1994. Deficiency of the human mitochondrial transcription factor h-mtTFA in infantile mitochondrial myopathy is associated with mtDNA depletion. Hum Mol Genet 3:1763-1769.
78. Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, Barriere P, Malthiery Y. 2001. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod 7:425-429.
79. Rolland P, Madjd Z, Durrant L, Ellis IO, Layfield R, Spendlove I. 2007. The ubiquitin-binding protein p62 is expressed in breast cancers showing features of aggressive disease. Endocr Relat Cancer 14:73-60.
80. Ruiz-Pesini E, Diez C, Lapena AC, Perez-Martos A, Montoya J, Alvarez E, Arenas J, Lopez-Perez MJ. 1998. Correlation of sperm motility with mitochondrial enzymatic activities. Clin Chem 44:1616-1620.
81. Ruiz-Pesini E, Lapena AC, Diez-Sanchez C, Perez-Martos A, Montoya J, Alvarez E, Diaz M, Urries A, Montoro L, Lopez-Perez MJ, et al. 2000. Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am J Hum Genet 67:682-696.
82. Sanaker PS, Husebye ES, Fondenes O, Bindoff LA. 2007. Clinical evolution of Kearns-Sayre syndrome with polyendocrinopathy and respiratory failure. Acta Neurol Scand Suppl 187:64-67.
83. Scarpulla RC. 2006. Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem 97:673-683.
84. Schatten H, Prather RS, Sun QY. 2005. The significance of mitochondria for embryo development in cloned farm animals. Mitochondrion 5:303-321.
85. Scheffler IE. 2001. A century of mitochondrial research: Achievements and perspectives. Mitochondrion 1:3-31.
86. Schwartz M, Vissing J. 2002. Paternal inheritance of mitochondrial DNA. N Engl J Med 347:576-580.
87. Schwartz M, Vissing J. 2003. New patterns of inheritance in mitochondrial disease. Biochem Biophys Res Commun 310:247-251.
88. Shitara H, Kaneda H, Sato A, Inoue K, Ogura A, Yonekawa H, Hayashi JI. 2000. Selective and continuous elimination of mitochondria microinjected into mouse eggs from spermatids, but not from liver cells, occurs throughout embryogenesis. Genetics 156:1277-1284.
89. Sills ES, Takeuchi T, Tucker MJ, Palermo GD. 2004. Genetic and epigenetic modifications associated with human ooplasm donation and mitochondrial heteroplasmy - Considerations for interpreting studies of heritability and reproductive outcome. Med Hypotheses 62:612-617.
90. Spikings EC, Alderson J, St John JC. 2006. Transmission of mitochondrial DNA following assisted reproduction and nuclear transfer. Hum Reprod Update 12:401-415.
91. Spikings EC, Alderson J, John JC. 2007. Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol Reprod 76:327-335.
92. Spiropoulos J, Turnbull DM, Chinnery PF. 2002. Can mitochondrial DNA mutations cause sperm dysfunction? Mol Hum Reprod 8:719-721.
93. St John JC, Jokhi RP, Barratt CL. 2005a. The impact of mitochondrial genetics on male infertility. Int J Androl 28:65-73.
94. St John JC, Ramalho-Santos J, Gray HL, Petrosko P, Rawe VY, Navara CS, Simerly CR, Schatten GP. 2005b. The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 7:141-153.
95. Stitzel ML, Seydoux G. 2007. Regulation of the oocyte-to-zygote transition. Science 316:407-408.
96. Sun QY, Wu GM, Lai L, Park KW, Cabot R, Cheong HT, Day BN, Prather RS, Schatten H. 2001. Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122:155-163.
97. Sutovsky P. 2004. Visualization of sperm accessory structures in the mammalian spermatids, spermatozoa, and zygotes by immunofluorescence, confocal, and immunoelectron microscopy. Methods Mol Biol 253:59-77.
98. Sutovsky P, Navara CS, Schatten G. 1996. Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization. Biol Reprod 55:1195-1205.
99. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G. 1999. Ubiquitin tag for sperm mitochondria. Nature 402:371-372.
100. Sutovsky P, McCauley TC, Sutovsky M, Day BN. 2003. Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biol Reprod 68:1793-1800.
101. Sutovsky P, Manandhar G, Laurincik J, Letko J, Caamano JN, Day BN, Lai L, Prather RS, Sharpe-Timms KL, Zimmer R, et al. 2005. Expression and proteasomal degradation of the major vault protein (MVP) in mammalian oocytes and zygotes. Reproduction 129:269-282.
102. Svoboda P, Stein P, Hayashi H, Schultz RM. 2000. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 127:4147-4156.
103. Thompson WE, Ramalho-Santos J, Sutovsky P. 2003. Ubiquitination of prohibitin in mammalian sperm mitochondria: Possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol Reprod 69:254-260.
104. Thouas GA, Trounson AO, Wolvetang EJ, Jones GM. 2004. Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol Reprod 71:1936-1942.
105. Thundathil J, Filion F, Smith LC. 2005. Molecular control of mitochondrial function in preimplantation mouse embryos. Mol Reprod Dev 71:405-413.
106. Tomlinson E, Palaniyappan N, Tooth D, Layfield R. 2007. Methods for the purification of ubiquitinated proteins. Proteomics 7:1016-1022.
107. Tovich PR, Oko RJ. 2003. Somatic histones are components of the perinuclear theca in bovine spermatozoa. J Biol Chem 278:32431-32438.
108. Tovich PR, Sutovsky P, Oko RJ. 2004. Novel aspect of perinuclear theca assembly revealed by immunolocalization of non-nuclear somatic histones during bovine spermiogenesis. Biol Reprod 71:1182-1194.
109. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from Polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354.
110. Vadlamudi RK, Joung I, Strominger JL, Shin J. 1996. p62, a phosphotyrosine-independent ligand of the SH2 domain of p56lck, belongs to a new class of ubiquitin-binding proteins. J Biol Chem 271:20235-20237.
111. Van Blerkom J. 2004. Mitochondria in human oogenesis and preimplantation embryogenesis: Engines of metabolism, ionic regulation and developmental competence. Reproduction 128:269-280.
112. Vassena R, Han Z, Gao S, Baldwin DA, Schultz RM, Latham KE. 2007. Tough beginnings: Alterations in the transcriptome of cloned embryos during the first two cell cycles. Dev Biol 304:75-69.
113. Wang WH, Day BN, Wu GM. 2003. How does polyspermy happen in mammalian oocytes? Microsc Res Tech 61:335-341.
114. Whitworth KM, Agca C, Kim JG, Patel RV, Springer GK, Bivens NJ, Forrester LJ, Mathialagan N, Green JA, Prather RS. 2005. Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos. Biol Reprod 72:1437-1451.
115. Wilding M, Dale B, Marino M, di Matteo L, Alviggi C, Pisaturo ML, Lombardi L, De Placido G. 2001. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod 16:909-917.
116. Yi YJ, Park CS. 2005. Parthenogenetic development of porcine oocytes treated by ethanol, cycloheximide, cytochalasin B and 6-dimethylaminopurine. Anim Reprod Sci 86:297-304.
117. Yu Y, Oko R, Miranda-Vizuete A. 2002. Developmental expression of spermatid-specific thioredoxin-1 protein: Transient association to the longitudinal columns of the fibrous sheath during sperm tail formation. Biol Reprod 67:1546-1554.
118. Zhao X, Li N, Guo W, Hu X, Liu Z, Gong G, Wang A, Feng J, Wu C. 2004. Further evidence for paternal inheritance of mitochondrial DNA in the sheep (Ovis aries). Heredity 93:399-403.