Follicular growth and oocyte competence in the in vitro cultured mouse follicle: Effects of gonadotrophins and steroids

Molecular Human Reproduction

Volumn 14, Issue 2, 2008, Pages 75-83

  Murray, Alison A ^a   Swales, Anna K E ^a,c   Smith, Rowena E ^a   Molinek, Michael D ^a   Hillier, Stephen G ^b   Spears, Norah ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

DNA methylation; Gonadotrophins; Oocyte competence; Steroids

Indexed keywords

ANDROGEN; DNA; ESTROGEN; GONADOTROPIN; RECOMBINANT FOLLITROPIN; RECOMBINANT LUTEINIZING HORMONE; STEROID;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL CULTURE; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CULTURE MEDIUM; DNA METHYLATION; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MOUSE; NICK END LABELING; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; OVULATION; PRIORITY JOURNAL;

ANDROSTENEDIONE; ANIMALS; DNA METHYLATION; ESTRADIOL; FEMALE; FERTILIZATION IN VITRO; GONADOTROPINS; IMMUNOHISTOCHEMISTRY; MICE; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; OOCYTES; OVARIAN FOLLICLE; STEROIDS;

EID: 40049090673     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gam092     Document Type: Article

References (63)

1. Anderiesz C, Trounson AO. The effect of testosterone on the maturation and developmental capacity of murine oocytes in vitro. Hum Reprod 1995;10:2377-2381.
2. Baker SJ, Srsen V, Lapping R, Spears N. Combined effect of follicle-follicle interactions and declining follicle-stimulating hormone on murine follicle health in vitro. Biol Reprod 2001;65 1304-1310.
3. Balasch J, Miro F, Burzaco I. The role of LH in human follicle development and oocyte fertility; evidence from IVF in a woman with long-standing hypogonadotrophic hypogonadism and using rhFSH. Hum Reprod 1995;10:1678-1683.
4. Balasch J, Creus M, Fabregues F, Civico S, Carmona F, Puerto B, Casamitjana R, Vanrell JA. The effect of exogenous luteinizing hormone (LH) on oocyte viability: Evidence from a comparative study using recombinant human follicle-stimulating hormone (FSH) alone or in combination with recombinant. LH for ovarian stimulation in pituitary-suppressed women undergoing assisted reproduction. J Assist Reprod Genet 2001;18:250-256.
5. Balen AH, Tan SL, Jacobs HS. Hypersecretion of luteinizing hormone: A significant cause of infertility and miscarriage. Br J Obstet Gynaecol 1993;100:1082-1089.
6. Beker AR, Colanbrandel B, Bevers MM. Effect of 17beta-estradiol, on the in vitro maturation of bovine oocytes. Theriogenology 2002;58 1663-1673.
7. Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, Niveleau A, Guérin JF. Influence of global sperm DNA methylation on IVF results. Hum Reprod 2005;20:768-773.
8. Billig H, Furuta I, Hsueh AJ. Oestrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 1993;133 2204-2212.
9. Bley MA, Saragueta PE, Baranao JL. Concerted stimulation of rat granulosa cell deoxyribonucleic acid synthesis by sex steroids and follicle-stimulating hormone. J Steroid Biochem Mol Biol 1997; 62:11-19.
10. Chappel SC, Howles C. Reevaluation of the roles of LH and FSH in the ovulatory process (review). Hum Reprod 1991;6:1206-1212.
11. Combelles CM, Albertini DF. Assessment of oocytes quality following repeated gonadotrophin stimulation, in the mouse. Biol Reprod 2003;68:812-821.
12. Cortvrindt RG, Hu Y, Liu J, Smitz JE. Timed analysis of the nuclear maturation of oocytes in early preantral mouse follicle culture supplemented with recombinant gonadotrophin. Fertil Steril 1998; 70:1114-1125.
13. Couse JF, Bunch DO, Lindzey J, Schomberg DW, Korach KS. Prevention of the polycystic ovarian phenotype and characterization of ovulatory capacity in the oestrogen receptor-alpha knockout mouse. Endocrinology 1999;140:5855-5865.
14. Dahl C, Guldberg P. DNA methylation analysis techniques. Biogerontology 2003;4:233-250.
15. Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf E, Reik W. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA 2001;98:13734-13738.
16. Devreker F, Hardy K. Effects of glutamine and taurine on preimplantation development and cleavage of mouse embryos in vitro. Biol Reprod 1997;57:921-928.
17. Dierschte DJ, Chaffin CL, Hute RJ. Role and site of oestrogen action in follicular atresia. Trends Endocrinol Metab 1994;5:215-219.
18. Dorrington JH, Bendell JJ, Khan SA. Interactions between FSH, estradiol-17 beta and transforming growth factor-beta regulate growth and differentiation in the rat gonad. J Steroid Biochem Mol Biol 1993;44:441-447.
19. Ertzeid G, Storeng R. The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod 2001;16:221-225.
20. Gill A, Jamnongjit M, Hammes SR. Androgens promote maturation and signaling in mouse oocytes independent of transcription: A release of inhibition model for mammalian oocyte meiosis. Mol Endocrinol 2004;18:97-104.
21. Guo Y, Guo KJ, Huang L, Tong XG, Li X. Effect of oestrogen deprivation on follicle/oocyte maturation and embryo development in mice. Chin Med J (Engl) 2004;117:498-502.
22. Gutendorf B, Westendorf J. Comparison of an array of in vitro assays for the assessment of the oestrogenic potential of natural and synthetic oestrogens, phytoestrogens and xenoestrogens. Toxicology 2001; 166:79-89.
23. Hillier SG, Yong EL, Illingworth PJ, Baird DT, Schwall RH, Mason AJ. Effect of recombinant activin on androgen synthesis in cultured human thecal cells. J Clin Endocrinol Metab 1991;72;1206-1211.
24. Hillier SG. Current concepts of the roles of follicle stimulating hormone and luteinizing hormone in folliculogenesis. Hum Reprod 1994;9:188-191.
25. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T. Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 2006;11 353-361.
26. Homburg R. Adverse effects of luteinizing hormone on fertility: Fact or fantasy. Baillieres Clin Obstet Gynaecol 1998;12:555-563.
27. Huot RI, Shain SA. Differential metabolism of dehydroepiandrosterone sulfate and oestrogen conjugates by normal or malignant AXC/SSh rat prostate cells and effects of these steroid conjugates on cancer cell proliferation in vitro. J Steroid Biochem 1988;29:617-621.
28. Huynh K, Jones G, Thouas G, Britt KL, Simpson ER, Jones ME. Oestrogen is not directly required for oocyte developmental competence. Biol Reprod 2004;70:1263-1269.
29. Kageyama S, Liu H, Kaneko N, Ooga M, Nagata M, Aoki F. Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 2007;133:85-94.
30. Lang J. Assay for deletion in Gnrh (hpg) locus using PCR. Mouse Genome 1991;89:857.
31. Lees-Murdock DJ, DE Felici M, Walsh CP. Methylation dynamics of repetitive DNA elements in the mouse germ cell lineage. Genomics 2003;82:230-237.
32. Lonning PE, Geisler J, Dowsett M. Pharmacological and clinical profile of anastrozole. Breast Cancer Res Treat 1998;49(Suppl 1):S53-S57.
33. Loumaye E, Engrand P, Shoham Z, Hillier SG, Baird DT. Clinical evidence for an LH ceiling? Hum Reprod 2003;18:2719-2720.
34. Lucifero D, Mertineit C, Clarke HJ, Bestor TH, Trasler JM. Methylation dynamics of imprinted genes in mouse germ cells. Genomics 2002; 79:530-538.
35. Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 2004;13 839-849.
36. Mann RJ, Keri RA, Nilson JH. Transgenic mice with chronically elevated luteinizing hormone are infertile due to anovulation, defects in uterine receptivity, and midgestation pregnancy failure. Endocrinol 1999;140:2592-2601.
37. Marchal R, Chicheportiche A, Dutrillaux B, Bernardino-Sgherri J. DNA methylation in mouse gametogenesis. Cytogenet Genome Res 2004; 105:316-324.
38. Merk FB, Botticelli CR, Albright JT. An intercellular response to oestrogen by granulosa cells in the rat ovary; an electron microscope study. Endocrinol 1972;90:992-1007.
39. Mizuno S, Chijiwa T, Okamura T, Akashi K, Fukumaki Y, Niho Y, Sasaki H. Expression of DNA methyltransferases DNMT1, 3A, and 3B in normal hematopoiesis and in acute and chronic myelogenous leukemia. Blood 2001;97:1172-1179.
40. Moor RM, Dai Y, Lee C, Fulka J, Jr. Oocyte maturation and embryonic failure. Hum Reprod Update 1998;4:223-236.
41. Murdoch WJ, Van Kirk EA. Oestrogenic upregulation of DNA polymerase beta in oocytes of preovulatory ovine follicles. Mol Reprod Dev 2001; 58:417-423.
42. Murray AA, Gosden RG, Allison V, Spears N. Effect of androgens on the development of mouse follicles growing in vitro. J Reprod Fertil 1998;113:27-33.
43. Obata Y, Kaneko-Ishino T, Koide T, Takai Y, Ueda T, Domeki I, Shiroishi T, Ishino F, Kono T. Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development 1998;125:1553-1560.
44. Quinn P, Barros C, Whittingham DG. Preservation of hamster oocytes to assay the fertilizing capacity of human spermatozoa. J Reprod Fertil 1982;66:161-168.
45. Roberts AJ, Skinner MK. Oestrogen regulation of thecal cell steroidogenesis and differentiation: Thecal cell-granulusa cell interactions. Endocrinol 1990;127:2918-2929.
46. Rollins RA, Haghighi F, Edwards JR, Das R, Zhang MQ, Ju J, Bestor TH. Large-scale structure of genomic methylation patterns. Genome Res 2006;16:157-163.
47. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 2007;22:26-35.
48. Shoham Z, Jacobs HS, Insler V. Luteinizing hormone: Its role, mechanism of action, and detrimental effects when hypersecreted during the follicular phase. Fertil Steril 1993;59:1153-1161.
49. Shoham Z. The clinical therapeutic window for luteinizing hormone in controlled ovarian stimulation. Fertil Steril 2002;77 1170-1177.
50. Simon I, Tenzen T, Reubinoff BE, Hillman D, McCarrey JR, Cedar, H. Asynchronous replication of imprinted genes is established in the gametes. and maintained during development. Nature 1999;401 929-932.
51. Smyth CD, Gosden RG, McNeilly AS, Hillier SG. Effect of inhibin immunoneutralization on steroidogenesis in rat ovarian follicles in vitro. J Endocrinol 1994;140:437-443.
52. Spears N, Boland NI, Murray AA, Gosden RG. Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile. Hum Reprod 1994;9: 527-532.
53. Spears N, Murray, AA, Allison V, Boland NI, Gosden RG. Role of gonadotrophins and ovarian steroids in the development of mouse follicles in vitro. J Reprod Fertil 1998;113:19-26.
54. Szoltys M, Slomczynska M, Tabarowski Z. Immunohistochemical localization of androgen receptor in rat oocytes. Folia Histochem Cytobiol 2003;41: 59-64.
55. Tesarik J, Mendoza C. Nongenomic effects of 17 beta-estradiol on maturing human oocytes: Relationship to oocyte developmental potential. J Clin Endocrinol Metab 1995;80;1438-1443.
56. Tetsuka M, Hillier SG. Differential regulation of aromatase and androgen receptor in granulosa cells. J Steroid Biochem Mol Biol 1997;61 233-239.
57. Van der Auwera I, D'Hooghe T. Superovulation of female mice delays embryonic and fetal development. Hum Reprod 2001;16 1237-1243.
58. Vendola KA, Zhou J, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest 1998;101:2622-2629.
59. Weil S, Vendola K, Zhou J, Bondy CA. Androgen and follicle-stimulating hormone interactions in primate ovarian follicle development. J Clin Endocrinol Metab 1999;84:2951-2956.
60. Westergaard LG, Erb K, Laursen S, Rasmussen PE, Rex S. The effect of human menopausal gonadotrophin, and highly purified, urine-derived follicle stimulating hormone on the outcome of in-vitro fertilisation in down-regulated normogonadotrophic women. Hum Reprod 1996;11 1209-1213.
61. Xia P, Younglai EV. Relationship between steroid concentrations in ovarian follicular fluid, and oocyte morphology in patients undergoing intracytoplasmic sperm injection (ICSI) treatment. J Reprod Fertil 2000;118:229-233.
62. Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, Carolan C, Broadbent PJ, Robinson JJ, Wilmut I, Sinclair KD. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet 2001;27:153-154.
63. Zheng P, Si W, Bavister BD, Yang J, Ding C, Ji W. 17Beta-estradiol and progesterone improve in-vitro cytoplasmic maturation of oocytes from unstimulated prepupertal and adult rhesus monkeys. Hum Reprod 2003;18:2137-2144.