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Reproductive Sciences

, Volume 18, Issue 4, pp 334–341 | Cite as

The Rate of In Vitro Maturation of Primary Follicles From Adult Mice and the Quality of Oocytes is Improved in the Absence of Anti-Müllerian Hormone

  • Joo Hyun Park
  • David T. MacLaughlin
  • Jose M. TeixeiraEmail author
Original Articles

Abstract

Anti-Müllerian hormone (AMH) inhibits the recruitment of primordial follicles into the growing pool, but its role in primary and secondary follicles is not clear. We isolated primary follicles from the ovaries of 9- to 10-week old mice and examined whether AMH affected follicular development. Follicles were matured in media that was prepared using unsexed fetal bovine serum (FBS) or female FBS (FFBS) with or without added AMH for approximately 2 weeks and maturation rates to secondary follicles and metaphase II (MII) oocytes were measured by standard morphological criteria. Rates of parthenogenetic activation and in vitro fertilization (IVF) were assessed by cleavage and blastocyst development, respectively. Whereas addition of AMH blocked primary to secondary follicle transition, the primary to secondary and secondary to MII follicle maturation rates was significantly improved with FFBS. Folliculogenesis resumed once AMH was removed from the media of the arrested primary follicles. The rates of IVF and parthenogenesis of oocytes after in vitro maturation (IVM) without AMH were also improved compared to controls. The results indicate that removal of AMH from culture conditions during IVM from primary follicular stages should be considered to improve outcome.

Keywords

oocytes folliculogenesis metaphase II Müllerian inhibiting substance 

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References

  1. 1.
    Eppig JJ, Schroeder AC. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod. 1989;41 (12): 268–276.CrossRefGoogle Scholar
  2. 2.
    O’Brien MJ, Pendola JK, Eppig JJ. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod. 2003;68 (5): 1682–1686.CrossRefGoogle Scholar
  3. 3.
    Jin SY, Lei L, Shikanov A, Shea LD, Woodruff TK. A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil Steril. 2010;93 (8): 2633–2639.CrossRefGoogle Scholar
  4. 4.
    Telfer EE, McLaughlin M, Ding C, Thong KJ. A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum Reprod. 2008;23 (5): 1151–1158.CrossRefGoogle Scholar
  5. 5.
    Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428 (6979): 145–150.CrossRefGoogle Scholar
  6. 6.
    Kim IW, Gong SP, Yoo CR, Choi JH, Kim DY, Lim JM. Derivation of developmentally competent oocytes by the culture of preantral follicles retrieved from adult ovaries: maturation, blastocyst formation, and embryonic stem cell transformation. Fertil Steril. 2009;92 (5): 1716–1724.CrossRefGoogle Scholar
  7. 7.
    Hsueh AJ, Eisenhauer K, Chun SY, Hsu SY, Billig H. Gonadal cell apoptosis. Recent Prog Horm Res. 1996;51:433–455.PubMedGoogle Scholar
  8. 8.
    Slot KA, Kastelijn J, Bachelot A, Kelly PA, Binart N, Teerds KJ. Reduced recruitment and survival of primordial and growing follicles in GH receptor-deficient mice. Reproduction. 2006;131 (131): 525–532.CrossRefGoogle Scholar
  9. 9.
    Bolamba D, Dubuc A, Dufour JJ, Sirard MA. Effects of gonadotropin treatment on ovarian follicle growth, oocyte quality and in vitro fertilization of oocytes in prepubertal gilts. Theriogenology. 1996;46 (4): 717–726.CrossRefGoogle Scholar
  10. 10.
    Schoevers EJ, Kidson A, Verheijden JH, Bevers MM. Effect of follicle-stimulating hormone on nuclear and cytoplasmic maturation of sow oocytes in vitro. Theriogenology. 2003;59 (9): 2017–2028.CrossRefGoogle Scholar
  11. 11.
    Wu J, Nayudu PL, Kiesel PS, Michelmann HW. Luteinizing hormone has a stage-limited effect on preantral follicle development in vitro. Biol Reprod. 2000;63 (1): 320–327.CrossRefGoogle Scholar
  12. 12.
    Berisha B, Schams D, Kosmann M, Amselgruber W, Einspanier R. Expression and localisation of vascular endothelial growth factor and basic fibroblast growth factor during the final growth of bovine ovarian follicles. J Endocrinol. 2000;167 (3): 371–382.CrossRefGoogle Scholar
  13. 13.
    Nilsson EE, Skinner MK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod. 2003;69 (4): 1265–1272.CrossRefGoogle Scholar
  14. 14.
    Souza CJ, Campbell BK, McNeilly AS, Baird DT. Bone morphogenetic proteins and folliculogenesis: lessons from the Booroola mutation. Reprod Suppl. 2003;61:361–370.PubMedGoogle Scholar
  15. 15.
    de Castro EPLA, Hansen PJ. Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation. Theriogenology. 2007;68 (5): 763–770.CrossRefGoogle Scholar
  16. 16.
    Guignot F, Bezard J, Palmer E. Effect of time during transport of excised mare ovaries on oocyte recovery rate and quality after in vitro maturation. Theriogenology. 1999;52 (5): 757–766.CrossRefGoogle Scholar
  17. 17.
    Kim HJ, Choi SH, Son DS, et al. Effect of exposure duration of ovaries and oocytes at ambient temperature on parthenogenetic development of porcine follicular oocytes. J Reprod Dev. 2006;52 (5): 633–638.CrossRefGoogle Scholar
  18. 18.
    Ravindranatha BM, Nandi S, Raghu HM, Reddy SM. In vitro maturation and fertilization of buffalo oocytes: effects of storage of ovaries, IVM temperatures, storage of processed sperm and fertilization media. Reprod Domest Anim. 2003;38 (1): 21–26.CrossRefGoogle Scholar
  19. 19.
    Sutton ML, Gilchrist RB, Thompson JG. Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Hum Reprod Update. 2003;9 (1): 35–48.CrossRefGoogle Scholar
  20. 20.
    Tas M, Evecen M, Ozdas OB, et al. Effect of transport and storage temperature of ovaries on in vitro maturation of bitch oocytes. Anim Reprod Sci. 2006;96 (1–2): 30–34.CrossRefGoogle Scholar
  21. 21.
    Wongsrikeao P, Otoi T, Karja NW, Agung B, Nii M, Nagai T. Effects of ovary storage time and temperature on DNA fragmentation and development of porcine oocytes. J Reprod Dev. 2005;51 (1): 87–97.CrossRefGoogle Scholar
  22. 22.
    MacLaughlin DT, Donahoe PK. Mullerian inhibiting substance: an update. Adv Exp Med Biol. 2002;511:25–38.CrossRefGoogle Scholar
  23. 23.
    Salmon NA, Handyside AH, Joyce IM. Oocyte regulation of anti-Mullerian hormone expression in granulosa cells during ovarian follicle development in mice. Dev Biol. 2004;266 (1): 201–208.CrossRefGoogle Scholar
  24. 24.
    Weenen C, Laven JS, Von Bergh AR, et al. Anti-Mullerian hormone expression pattern in the human ovary: Potential Implications For Initial And Cyclic Follicle Recruitment. Mol Hum Reprod. 2004;10:77–83.CrossRefGoogle Scholar
  25. 25.
    Ficicioglu C, Kutlu T, Baglam E, Bakacak Z. Early follicular antimullerian hormone as an indicator of ovarian reserve. Fertil Steril. 2006;85 (3): 592–596.CrossRefGoogle Scholar
  26. 26.
    Kevenaar ME, Meerasahib MF, Kramer P, et al. Serum anti-mullerian hormone levels reflect the size of the primordial follicle pool in mice. Endocrinology. 2006;147 (7): 3228–3234.CrossRefGoogle Scholar
  27. 27.
    Silberstein T, MacLaughlin DT, Shai I, et al. Mullerian inhibiting substance levels at the time of HCG administration in IVF cycles predict both ovarian reserve and embryo morphology. Hum Reprod. 2006;21 (1): 159–163.CrossRefGoogle Scholar
  28. 28.
    Visser JA, de Jong FH, Laven JS, Themmen AP. Anti-Mullerian hormone: a new marker for ovarian function. Reproduction. 2006;131 (1): 1–9.CrossRefGoogle Scholar
  29. 29.
    Durlinger AL, Kramer P, Karels B, et al. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology. 1999;140 (12): 5789–5796.CrossRefGoogle Scholar
  30. 30.
    Durlinger AL, Gruijters MJ, Kramer P, et al. Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology. 2002;143 (3): 1076–1084.CrossRefGoogle Scholar
  31. 31.
    Nilsson E, Rogers N, Skinner MK. Actions of anti-Mullerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction. 2007;134 (2): 209–221.CrossRefGoogle Scholar
  32. 32.
    Durlinger AL, Gruijters MJ, Kramer P, et al. Anti-Mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology. 2001;142 (11): 4891–4899.CrossRefGoogle Scholar
  33. 33.
    Sanchez F, Adriaenssens T, Romero S, Smitz J. Different follicle-stimulating hormone exposure regimens during antral follicle growth alter gene expression in the cumulus-oocyte complex in mice. Biol Reprod. 2010;83 (4): 514–524.CrossRefGoogle Scholar
  34. 34.
    Lee HJ, Teixeira J. Parthenogenesis in human oocytes that were collected from resected ovarian tissue and matured in vitro. Stem Cells Dev. 2009;18 (6): 941–946.CrossRefGoogle Scholar
  35. 35.
    Lorenzo HK, Teixeira J, Pahlavan N, Laurich VM, Donahoe PK, MacLaughlin DT. New approaches for high-yield purification of Mullerian inhibiting substance improve its bioactivity. J Chromatogr B Analyt Technol Biomed Life Sci. 2002;766 (1): 89–98.CrossRefGoogle Scholar
  36. 36.
    Lee ST, Choi MH, Gong SP, Han JY, Lim JM. Establishment of a basic method for manipulating preantral follicles: effects of retrieval method on in vitro growth of preantral follicles and intrafollicular oocytes. Zygote. 2007;15 (2): 109–116.CrossRefGoogle Scholar
  37. 37.
    McGee EA, Smith R, Spears N, Nachtigal MW, Ingraham H, Hsueh AJ. Mullerian inhibitory substance induces growth of rat preantral ovarian follicles. Biol Reprod. 2001;64 (1): 293–298.CrossRefGoogle Scholar
  38. 38.
    Bromfield JJ, Coticchio G, Hutt K, Sciajno R, Borini A, Albertini DF. Meiotic spindle dynamics in human oocytes following slow-cooling cryopreservation. Hum Reprod. 2009;24 (9): 2114–2123.CrossRefGoogle Scholar
  39. 39.
    Hamatani T, Falco G, Carter MG, et al. Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet. 2004;13 (19): 2263–2278.CrossRefGoogle Scholar

Copyright information

© Society for Reproductive Investigation 2011

Authors and Affiliations

  • Joo Hyun Park
    • 1
  • David T. MacLaughlin
    • 2
  • Jose M. Teixeira
    • 1
    Email author
  1. 1.Vincent Center for Reproductive Biology, Department of Obstetrics and GynecologyThier 931, Massachusetts General Hospital and Harvard Medical SchoolBostonUSA
  2. 2.Pediatric Surgical Research Laboratories, Department of SurgeryMassachusetts General Hospital and Harvard Medical SchoolBostonUSA

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