Maternal age and ovarian stimulation independently affect oocyte mtDNA copy number and cumulus cell gene expression in bovine clones

Human Reproduction

Volumn 30, Issue 6, 2015, Pages 1410-1420

  Cree, Lynsey M ^a,b   Hammond, Elizabeth R ^a   Shelling, Andrew N ^a   Berg, Martin C ^c   Peek, John C ^b   Green, Mark P ^c,d,e  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b Fertility Assciats   (New Zealand)

^c RUAKURA RESEARCH CENTRE   (New Zealand)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

cumulus cells; gene expression; mtDNA copy number; oocyte ageing; ovarian stimulation

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BOVINE MODEL; CELL NUCLEUS TRANSPLANTATION; CLONE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; CUMULUS CELL; DOWN REGULATION; ECHOGRAPHY; ENDOPLASMIC RETICULUM STRESS; FEMALE; FERTILIZATION IN VITRO; GENE DOSAGE; GENE EXPRESSION; MATERNAL AGE; MITOCHONDRIAL GENOME; NONHUMAN; OOCYTE; OVARY FOLLICLE DEVELOPMENT; OVULATION INDUCTION; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOMATIC CELL; SOMATIC CELL NUCLEAR TRANSFER; ANIMAL; BOVINE; CLONING; COPY NUMBER VARIATION; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OVARY FOLLICLE;

BOVINAE;

ANIMALS; CATTLE; CLONING, ORGANISM; CROSS-SECTIONAL STUDIES; CUMULUS CELLS; DNA COPY NUMBER VARIATIONS; DNA, MITOCHONDRIAL; ENDOPLASMIC RETICULUM; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MATERNAL AGE; OVARIAN FOLLICLE; OVULATION INDUCTION;

EID: 84937868759     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dev066     Document Type: Article

References (67)

1. Adams GP, Jaiswal R, Singh J, Malhi P. Progress in understanding ovarian follicular dynamics in cattle. Theriogenology 2008;69:72-80.
2. Aflatoonian A, Mansoori Moghaddam F, Mashayekhy M, Mohamadian F. Comparison of early pregnancy and neonatal outcomes after frozen and fresh embryo transfer in ART cycles. J Assist Reprod Genet 2010; 27:695-700.
3. Baart EB, Martini E, Eijkemans MJ, Van Opstal D, Beckers NGM, Verhoeff A, Macklon NS, Fauser BCJM. Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial. Human Reprod 2007;22:980-988.
4. Barritt J, Willadsen S, Brenner C, Cohen J. Cytoplasmic transfer in assisted reproduction. Hum Reprod Update 2001;7:428-435.
5. Barritt J, Kokot M, Cohen J, Steuerwald N, Brenner C. Quantification of human ooplasmic mitochondria. Reprod Biomed Online 2002;4:243-247.
6. Bentov Y, Casper RF. The aging oocyte-can mitochondrial function be improved? Fertil Steril 2013;99:18-22.
7. Borghol N, Lornage J, Blachere T, Sophie Garret A, Lefevre A. Epigenetic status of the H19 lous in human oocytes following in vitro maturation. Genomics 2006;87:417-426.
8. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009;55:611-622.
9. Chan C, Liu V, Lau E, YeungW, Ng E, Ho P. MitochondrialDNAcontent and 4977 bp deletion in unfertilized oocytes. Mol Hum Reprod 2005; 11:843-846.
10. Chiaratti MR, Bressan FF, Ferreira CR, Caetano AR, Smith LC, Vercesi AE, Meirelles FV. Embryo mitochondrial DNA depletion is reversed during early embryogenesis in cattle. Biol Reprod 2010;82:76-85.
11. Chu T, Dufort I, Sirard MA. Effect of ovarian stimulation on oocyte gene expression in cattle. Theriogenology 2012;77:1928-1938.
12. Cillo F, Brevini T, Antonini S, Paffoni A, Ragni G, Gandolfi F. Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction 2007;134:645-650.
13. Cotterill M, Harris S, Collado F, Lu J, Huntriss J, Campbell B, Picton H. The activity and copy number of mitochondrial DNA in ovine oocytes throughout oogenesis in vivo and during oocyte maturation in vitro. Mol Hum Reprod 2013;19:444-450.
14. Cree LM, Samuels DC, de Sousa Lopes SC, Rajasimha HK, Wonnapinij P, Mann JR, Dahl HM, Chinnery PF. A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat Genet 2008;40:249-254.
15. Cummins JM. The role of maternal mitochondria during oogenesis, fertilization and embryogenesis. Reprod Biomed Online 2002;4:176-182.
16. Dale B,Wilding M, Botta G, Rasile M, Marino M, Di Matteo L, De Placido G, Izzo A. Pregnancy after cytoplasmic transfer in a couple suffering from idiopathic infertility: Case report. Hum Reprod 2001;16:1469-1472.
17. Denomme MM, Zhang L, Mann MRW. Embryonic imprinting perturbations do not originate from superovulation-induced defects inDNAmethylation acquisition. Fertil Steril 2011;96:734-738.
18. Dias FCF, Khan MIR, AdamsGP, SiradMA, Singh J.Granulosa cell function and oocyte competence: super-follicles, super-moms and super-stimualtion in cattle. Anim Reprod Sci 2014;149:80-89.
19. de los Santos MJ, Garcia-Laez V, Beltran-Torregrosa D, Horcajadas JA, Martinez-Conejero JA, Esteban FJ, Pellicer A, Labarta E. Hormonal and molecular characterization of follicular fluid, cumulus cells and oocytes from pre-ovulatory follicles in stimulated and unstimulated cycles. Hum Reprod 2012;27:1596-1605.
20. Dell'Aquila ME, Ambruosi B, De Santis T, Cho YS. Mitochondrial distribution and activity in human mature oocytes: gonadotropin-releasing hormone agonist versus antagonist for pituitary down-regulation. Fertil Steril 2009; 91:249-255.
21. Dias F, Khan M, Sirard M, Adams G, Singh J. Differential gene expression of granulosa cells after ovarian superstimulation in beef cattle. Reproduction 2013;146:181-191.
22. Ekart J, McNatty K, Hutton J, Pitman J. Ranking and selection of MII oocytes in human ICSI cycles using gene expression levels from associated cumulus cells. Hum Reprod 2013;28:2930-2942.
23. El Shourbagy SH, Spikings EC, Freitas M, St John JC. Mitochondria directly influence fertilisation outcome in the pig. Reproduction 2006; 131:233-245.
24. Evans J, Hannan NJ, Edgell TA, Vollenhoven BJ, Lutjen PJ, Osianlis T, Salamonsen LA, Rombauts LJF. Fresh versus frozen embryo transfer: backing clinical decisions with scientific and clinical evidence. Hum Reprod Update 2014;20:808-821.
25. Fragouli E,Wells D, Delhanty JDA.Chromosomeabnormalities in the human oocyte. Cytogenet Genome Res 2011;133:107-118.
26. Fragouli E, Lalioti M,Wells D. The transcriptome of follicular cells: biological insights and clinical implications for the treatment of infertility. Hum Reprod Update 2013;20:1-11.
27. Gebhardt KM, Feil DK, Dunning KR, Lane M, Russell DL. Human cumulus cell gene expression as a biomarker of pregnancy outcome after single embryo transfer. Fertil Steril 2011;96:47-52.
28. Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 2008; 14:159-177.
29. Green MP, Berg MC, Back PJ, Lee RSF, Peek JC. Ovarian stimulation regimens and maternal age alter follicular concentrations of key metabolites and the proportion of abnormal follicles recruited. In: 14th World Congress for Human Reproduction, Melbourne, Australia, 2011,226.
30. Grondahl ML, Yding Andersen C, Bogstad J, Nielsen FC, Meinertz H, Borup R. Gene expression profiles of single human mature oocytes in relation to age. Hum Reprod 2010;25:957-968.
31. 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.
32. Ji J, LiuY,Tong X, Luo L,MaJ, Chen Z. The optimum number of oocytes in IVF treatment: an analysis of 2455 cycles in China. Hum Reprod 2013; 28:2728-2734.
33. Kushnir V, Ludaway T, Russ R, Fields E, Koczor C, LewisW. Reproductive aging is associated with decreased mitochondrial abundance and altered structure in murine oocytes. J Assist Reprod Genet 2012;29:637-642.
34. Lanzendorf SE, Mayer JF, Toner J, Oehninger S, Saffan DS, Muasher S. Pregnancy following transfer of ooplasm from cryopreserved-thawed donor oocytes into recipient oocytes. Fertil Steril 1999;71:575-577.
35. Lee M, Liu C, Lee L,WuH, Huang C, Huang L, Chen C, Cheng E. Association of creatin kinase B and peroxiredoxin 2 expression with age and embryo quality in cumulus cells. J Assist Reprod Genet 2010;27:629-639.
36. Malhi PS, Adams GP, Singh J. Bovine model of reproductive aging in women: follicular, luteal, and endocrine characteristics. Biol Reprod 2005; 73:45-53.
37. Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Man MRW. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum Mol Genet 2010; 19:36-51.
38. May-Panloup P, Chretien M, Malthiery Y, Reynier P. Mitochondrial DNA in the oocyte and the developing embryo. Curr Top Dev Biol 2007;77:51-83.
39. McKenzie L, Pangas S, Carson S, Kovanci E, Cisneros P, Buster J, Amato P, Matzuk M. Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum Reprod 2004;19:2869-2874.
40. McNatty KP, Heath DA, Hudson NL, Reader KL, Quirke L, Lun S, Juengel JL. The conflict between hierarchical ovarian follicular development and superovulation treatment. Reproduction 2010;140:287-294.
41. McReynolds S, Dzieciatkowska M, McCallie BR, Mitchell SD, Stevens J, Hansen K, SchoolcraftWB, Katz-Jaffe MG. Impact of maternal aging on the molecular signature of human cumulus cells. Fertil Steril 2012;98:1574-1580.
42. Murakoshi Y, Sueoka K, Takahashi K, Sato S, Sakurai T, Tajima H, Yoshimura Y. Embryo developmental capability and pregnancy outcome are related to the mitochondrial DNA copy number and ooplasmic volume. J Assist Reprod Genet 2013;30:1367-1375.
43. Pacella L, Zander-Fox DL, Armstrong DT, Lane M. Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment. Fertil Steril 2012;98:986-994.e2.
44. Pacella-Ince L, Zander-Fox DL, Lane M. Mitochondrial SIRT3 and its target glutamate dehydrogenase are altered in follicular cells of women with reduced ovarian reserve or advanced maternal age. Hum Reprod 2014; 29:1490-1499.
45. Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stemcells. HumReprodUpdate 2009;15:553-572.
46. Reynier P, May-Panloup P, Chretien M, Morgan CJ, Jean M, Savagner F, Barriere P, Malthiery Y. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod 2001;7:425-429.
47. Santos TA, El Shourbagy S, St. John JC. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil Steril 2006;85:584-591.
48. Santos MA, KuijkEW, Macklon NS. The impact of ovarian stimulation for IVF on the developing embryo. Reproduction 2010;139:23-34.
49. Sato A,Otsu E,NegishiH,UtsunomiyaT,ArimaT.AberrantDNAmethylation of imprinted loci in superovulated oocytes. Hum Reprod 2007;22:26-35.
50. Schon E, Kim S, Ferreora J, Magalhaes P, Grace M, Warburton D, Gross S. Chromosomal non-disjunction in human oocytes: is there a mitochondrial connection? Hum Reprod 2000;15:160-172.
51. Shapiro BS, Daneshmand ST, Garner FC, Aguirre M, Hudson C, Thomas S. Evidence of impaired endometrial receptivity after ovarian stimulation for in vitro fertilization: a prospective randomized trial comparing fresh and frozen-thawed embryo transfer in normal responders. Fertil Steril 2011a;96:344-348.
52. Shapiro BS, Daneshmand ST, Garner FC, Aguirre M, Hudson C, Thomas S. Evidence of impaired endometrial receptivity after ovarian stimulation for in vitro fertilization: a prospective randomized trial comparing fresh and frozen-thawed embryo transfers in high responders. Fertil Steril 2011b;96:516-518.
53. Shoubridge EA,WaiT. MitochondrialDNAand the Mammalian Oocyte. Curr Top Dev Biol 2007;77:87-111.
54. Steuerwald NM, Bermudez MG, Wells D, Munne S, Cohen J. Maternal age-related differential global expression profiles observed in human oocytes. Reprod Biomed Online 2007;14:700-708.
55. Steward RG, Lan L, Shah AA, Yeh JS, Price TM, Goldfarb JM, Muasher SJ. Oocyte number as a predictor for ovarian hyperstimulation syndrome and live birth: an analysis of 256,381 in vitro fertilization cycles. Fertil Steril 2014;101:967-973.
56. Sutton-McDowall ML, Gilchrist RB, ThompsonJG. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 2010;139:685-695.
57. Takeo S, Kawahara-Miki R, Goto H, Cao F, Kimura K, Monji Y, Kuwayama T, Iwata H. Age-associated changes in gene expression and developmental competence of bovine oocytes, and a possible countermeasure against age-associated events. Mol Reprod Dev 2013;80:508-521.
58. Tsai H, Hsieh Y, Hsieh J, Chang C, Yang C, Yang J, ChengW, Tsai F, Liu C. Mitochondria DNA deletion and copy numbers of cumulus cells associated with in vitro fertilization outcomes. J Reprod Med 2010; 55:491-497.
59. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3-new capabilities and interfaces. Nucleic Acids Res 2012;40:e115.
60. Uyar A, Torrealday S, Seli E. Cumulus and granulosa cell markers of oocyte and embryo quality. Fertil Steril 2013;99:979-997.
61. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 2004;128:269-280.
62. van der Gaast M, Eijkemans M, van der Net J, de Boer E, Burger C, van Leeuwen F, Fauser B, Macklon N. Optimum number of oocytes for a successful first IVF treatment cycle. Reprod Biomed Online 2006; 13:476-480.
63. Verberg MFG, Macklon NS, Nargund G, Frydman R, Devroey P, Broekmans FJ, Fauser BCJM. Mild ovarian stimulation for IVF. Hum Reprod Update 2009;15:13-29.
64. Wai T, Ao A, Zhang X, Cyr D, Dufort D, Shoubridge E. The role of mitochondrial DNA copy number in mammalian fertility. Biol Reprod 2010;83:52-62.
65. Wathlet S, Adriaenssens T, Segers I, Verheyen G, Janssens R, Coucke W, Devroey P, Smitz J. New candidate genes to predict pregnancy outcome in single embryo transfer cycles when using cumulus cell gene expression. Fertil Steril 2012;98:432-439.
66. Wells DN, Misica PM, Tervit HR. Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol Reprod 1999;60:996-1005.
67. Ziebe S, Bangsboll S, Schmidt KLT, Loft A, Lindhard A, Nyboe Andersen A. Embryo quality in natural versus stimulated IVF cycles. Human Reprod 2004;19:1457-1460.