The activity and copy number of mitochondrial DNA in ovine oocytes throughout oogenesis in vivo and during oocyte maturation in vitro

Molecular Human Reproduction

Volumn 19, Issue 7, 2013, Pages 444-450

  Cotterill, Matthew ^a   Harris, Sarah E ^a   Fernandez, Esther Collado ^a   Lu, Jianping ^a   Huntriss, John D ^a   Campbell, Bruce K ^b   Picton, Helen M ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

JC1; Meiotic maturation; Mitochondria activity; Mitochondrial DNA; Sheep oocyte

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA EXTRACTION; FEMALE; FOLLICULAR ASPIRATION; GENE DOSAGE; GERMINAL VESICLE; IN VITRO STUDY; IN VIVO STUDY; MEIOSIS; METAPHASE; MITOCHONDRION; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY; OVARY FOLLICLE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SOMATIC CELL; STAINING;

JC1; MEIOTIC MATURATION; MITOCHONDRIA ACTIVITY; MITOCHONDRIAL DNA; SHEEP OOCYTE;

ANIMALS; DNA, MITOCHONDRIAL; FEMALE; FLUOROMETRY; MEIOSIS; OOCYTES; OOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; SHEEP;

EID: 84880144874     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat013     Document Type: Article

References (54)

1. Barritt JA, Brenner CA, Cohen J, Matt DW. Mitochondrial DNA rearrangements in human oocytes and embryos. Mol Human Reprod 1999;5:927-933.
2. Barritt JA, Brenner CA, Malter HE, Cohen J. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod 2001; 16:513-516.
3. Barritt JA, Kokot M, Cohen J, Steuerwald N, Brenner CA. Quantification of human ooplasmic mitochondria. Reprod Biomed Online 2002; 4:243-247.
4. Brevini TAL, Vassena R, Francisci C, Gandolfi F. Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol Reprod 2005;72:1218-1223.
5. Campbell BK, Souza C, Gong J, Webb R, Kendall N, Marsters P, Robinson G, Mitchell A, Telfer EE, Baird DT. Domestic ruminants as models for the elucidation of the mechanisms controlling ovarian follicle development in humans. Reproduction (Cambridge, England) Supplement 2003;61:429-443.
6. Chen X, Prosser R, Simonetti S, Sadlock J, Jagiello G, Schon EA. Rearranged mitochondrial genomes are present in human oocytes. Am J Hum Genet 1995;57:239-247.
7. Cohen J, Scott R, Schimmel T, Levron J, Willadsen S. Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet 1997;350:186-187.
8. Cotterill M, Catt SL, Picton HM. Characterisation of the cellular and molecular responses of ovine oocytes and their supporting somatic cells to pre-ovulatory levels of LH and FSH during in vitro maturation. Reproduction 2012;144:195-207.
9. Cummins JM, Wakayama T, Yanagimachi R. Fate of microinjected sperm components in the mouse oocyte and embryo. Zygote 1997;5:301-308.
10. Ferguson EM, Leese HJ. A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol Reprod Dev 2006;73:1195-1201.
11. Giles RE, Blanc H, Cann HM, Wallace DC. Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 1980;77:6715-6719.
12. Harris SE, Picton HM. Metabolism of follicles and oocytes during growth and maturation. In: Tan SL, Chian RC, Bucket W (ed.). In Vitro Maturation of Human Oocytes: Basic Science to Clinical Application. Abingdon: Informa UK Ltd, 2007, 15-36.
13. Harris SE, Adriaens I, Leese HJ, Gosden RG, Picton HM. Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro. Reproduction 2007;134:415-424.
14. Harris SE, Leese HJ, Gosden RG, Picton HM. Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Mol Reprod Dev 2009;76:231-238.
15. Harris SE, Maruthini D, Tang T, Balen AH, Picton HM. Metabolism and karyotype analysis of oocytes from patients with polycystic ovary syndrome. Hum Reprod 2010;25:2305-2315.
16. Hiendleder S, Lewalski H, Wassmuth R, Janke A. The complete mitochondrial DNA sequence of the domestic sheep (Ovis aries) and comparison with the other major ovine haplotype. J Mol Evol 1998; 47:441-448.
17. Huntriss J, Gosden R, Hinkins M, Oliver B, Miller D, Rutherford AJ, Picton HM. Isolation, characterization and expression of the human factor in the germline alpha (FIGLA) gene in ovarian follicles and oocytes. Mol Human Reprod 2002;8:1087-1095.
18. Iwata H, Goto H, Tanaka H, Sakaguchi Y, Kimura K, Kuwayama T, Monji Y. Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod Fertil Dev 2011;23:424-432.
19. Jansen RP. Germline passage of mitochondria: quantitative considerations and possible embryological sequelae. HumReprod 2000;15(Suppl. 2):112-128.
20. Jansen RPS, de Boer K. The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol 1998;145:81-88.
21. Jones A, Van Blerkom J, Davis P, Toledo AA. Cryopreservation of metaphase II human oocytes effects mitochondrial membrane potential: implications for developmental competence. Hum Reprod 2004;19:1861-1866.
22. Lopez-Lluch G, Irusta PM, Navas P, de Cabo R. Mitochondrial biogenesis and healthy aging. Exp Gerontol 2008;43:813-819.
23. Lundy T, Smith P, o'Connell A, Hudson NL, McNatty KP. Populations of granulosa cells in small follicles of the sheep ovary. J Reprod Fertil 1999; 115:251-262.
24. Mao J, Whitworth KM, Spate LD, Walters EM, Zhao J, Prather RS. Regulation of oocyte mitochondrial DNA copy number by follicular fluid, EGF, and neuregulin 1 during in vitro maturation affects embryo development in pigs. Theriogenology 2012;78:887-897.
25. Martino NA, Lacalandra GM, Filioli Uranio M, Ambruosi B, Caira M, Silvestre F, Pizzi F, Desantis S, Accogli G, DelĺAquila ME. Oocyte mitochondrial bioenergy potential and oxidative stress: within-/ between-subject, in vivo versus in vitro maturation, and age-related variations in a sheep model. Fertil Steril 2012;97:720-728 e1.
26. Michaels GS, Hauswirth WW, Laipis PJ. Mitochondrial DNA copy number in bovine oocytes and somatic cells. Dev Biol 1982;94:246-251. Naviaux RK, McGowan KA. Organismal effects of mitochondrial dysfunction. Hum Reprod 2000;15(Suppl. 2):44-56.
27. Naviaux RK, McGowan KA. Organismal effects of mitochondrial dysfunction. Hum Reprod 2000;15(Suppl. 2):44-56.
28. Newton H, Picton H, Gosden RG. In vitro growth of oocyte-granulosa cell complexes isolated from cryopreserved ovine tissue. J Reprod Fertil 1999;115:141-150.
29. Oktay K, Briggs D, Gosden RG. Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocrinol Metab 1997;82:3748-3751.
30. Activity and copy number of mitochondria in oocytes 449 Picton H, Briggs D, Gosden R. The molecular basis of oocyte growth and development. Mol Cell Endocrinol 1998;145:27-37.
31. Picton HM, Elder K, Houghton FD, Hawkhead JA, Rutherford AJ, Hogg JE, Leese HJ, Harris SE. Association between amino acid turnover and chromosome aneuploidy during human preimplantation embryo development in vitro. Mol Human Reprod 2010;16:557-569.
32. Piko L, Matsumoto L. Number of mitochondria and some properites of mitochondrial-DNA in mouse egg. Dev Biol 1976;49:1-10.
33. Piko L, Taylor KD. Amounts of mitochondrial-DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev Biol 1987;123:364-374.
34. Reers M, Smiley ST, MottolaHartshorn C, Chen A, Lin M, Chen LB. Mitochondrial membrane potential monitored by JC-1 dye. Mitochond Biogen Genet A 1995;260:406-417.
35. Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, Barriere P, Malthiery Y. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Human Reprod 2001;7:425-429.
36. Santos TA, El Shourbagy S, St John JC. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil Steril 2006;85:584-591.
37. Schon EA, Kim SH, Ferreira JC, Magalhaes P, Grace M, Warburton D, Gross SJ. Chromosomal non-disjunction in human oocytes: is there a mitochondrial connection? Hum Reprod (Oxford, England). 2000; 15(Suppl. 2):160-172.
38. Schultz RM, Lamarca MJ, Wassarman PM. Absolute rates of protein synthesis during meiotic maturation of mammalian oocytes in vitro. Proc Natl Acad Sci USA 1978;75:4160-4164.
39. Spikings EC, Alderson J, John JCS. Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol Reprod 2007;76:327-335.
40. Steuerwald N, Barritt JA, Adler R, Malter H, Schimmel T, Cohen J, Brenner CA. Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid cycle fluorescence monitored PCR. Zygote 2000;8:209-215.
41. Stojkovic M, Machado SA, Stojkovic P, Zakhartchenko V, Hutzler P, Goncalves PB, 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.
42. Sugiura K, Pendola FL, Eppig JJ. Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev Biol 2005;279:20-30.
43. Sugiura K, Su YQ, Diaz FJ, Pangas SA, Sharma S, Wigglesworth K, O'Brien MJ, Matzuk MM, Shimasaki S, Eppig JJ. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 2007;134:2593-2603.
44. Torner H, Brussow KP, Alm H, Ratky J, Pohland R, Tuchscherer A, Kanitz W. Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation. Theriogenology 2004;61:1675-1689.
45. Trounson A, Anderiesz C, Jones G. Maturation of human oocytes in vitro and their developmental competence. Reproduction 2001;121:51-75. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 2004;128:269-280.
46. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 2004;128:269-280
47. Van Blerkom J, Davis P. High-polarized (Delta Psi m(HIGH)) mitochondria are spatially polarized in human oocytes and early embryos in stable subplasmalemmal domains: developmental significance and the concept of vanguard mitochondria. Reprod Biomed Online 2006;13:246-254.
48. Van Blerkom J, Davis P, Mathwig V, Alexander S. Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum Reprod 2002;17:393-406.
49. Van Blerkom J, Davis P, Alexander S. Inner mitochondrial membrane potential (Delta Psi m), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes. Hum Reprod 2003;18:2429-2440.
50. Wai T, Ao A, Zhang X, Cyr D, Dufort D, Shoubridge EA. The role of mitochondrial DNA copy number in mammalian fertility. Biol Reprod 2010;83:52-62.
51. Wilding M, Dale B, Marino M, di Matteo L, Alviggi C, Pisaturo ML, Lombardi L, De Placido G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod 2001;16:909-917.
52. Wilding M, Fiorentino A, De Simone ML, Infante V, De Matteo L, Marino M, Dale B. Energy substrates, mitochondrial membrane potential and human preimplantation embryo division. Reprod Biomed Online 2002;5:39-42.
53. Yu Y, Dumollard R, Rossbach A, Lai FA, Swann K. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol 2010;224:672-680.
54. Zeng HT, Ren Z, Yeung WSB, Shu YM, Xu YW, Zhuang GL, Liang XY. Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum Reprod 2007;22:1681-1686