Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
권호 표지
DOI QR코드

DOI QR Code

In vitro growth of mouse preantral follicles: effect of animal age and stem cell factor/insulin-like growth factor supplementation

  • Jee, Byung Chul (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Kim, Jee Hyun (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Park, Da Hyun (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Youm, Hyewon (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Suh, Chang Suk (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Kim, Seok Hyun (Department of Obstetrics and Gynecology, Seoul National University College of Medicine)
  • Received : 2012.06.18
  • Accepted : 2012.08.03
  • Published : 2012.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: To determine whether animal age impacts in vitro preantral follicle growth. Effects of hCG, stem cell factor (SCF), and/or insulin-like growth factor (IGF) supplementation in growth medium were also investigated. Methods: Intact preantral follicles were mechanically isolated from fresh ovaries of BDF1 mice and cultured in growth medium for 9 to 11 days. Surviving follicles with antrum formation were transferred to maturation medium for 14 to 18 hours. Follicle survival, antrum formation, and retrieval of metaphase II (MII) oocytes were compared among three age categories (4-5, 7-8, and 10-11 week-old). By using 7- to 8-week-old mice, preantral follicles were cultured in growth medium supplemented with hCG (0, 5, or 10 mIU/mL), SCF (50 ng/mL), IGF-1 (50 ng/mL), and SCF+IGF-1. Results: Seven- to eight-week-old mice showed a higher follicle survival and antrum formation and produced more MII oocytes compared to other groups. In the 7- to 8-week-old mice, supplementation of 5 mIU/mL hCG significantly enhanced the antrum formation but the percentage of MII oocytes was similar to that of the control. Supplementation of SCF+IGF-1 did not enhance follicle survival or antrum formation but the percentage of MII oocytes increased modestly (39.1%) than in the control (28.6%, p>0.05, statistically not significant). Conclusion: Seven- to eight-week-old mice showed better outcomes in growth of preantral follicles in vitro than 4- to 5- or 10- to 11-week-old mice. Supplementation of hCG enhanced antrum formation and supplementation of SCF+IGF-1 yielded more mature oocytes; hence, these should be considered in the growth of preantral follicles in vitro.

Keywords

References

  1. Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Orthotopic and heterotopic ovarian tissue transplantation. Hum Reprod Update 2009;15:649-65.
  2. Jeruss JS, Woodruff TK. Preservation of fertility in patients with cancer. N Engl J Med 2009;360:902-11.
  3. Rodriguez-Wallberg KA, Oktay K. Fertility preservation medicine: options for young adults and children with cancer. J Pediatr Hematol Oncol 2010;32:390-6.
  4. Telfer EE, McLaughlin M, Ding C, Thong KJ. A two-step serumfree culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum Reprod 2008;23:1151-8.
  5. Cortvrindt R, Smitz J, Van Steirteghem AC. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Hum Reprod 1996;11:2656-66.
  6. Lenie S, Cortvrindt R, Adriaenssens T, Smitz J. A reproducible twostep culture system for isolated primary mouse ovarian follicles as single functional units. Biol Reprod 2004;71:1730-8.
  7. Xu M, Kreeger PK, Shea LD, Woodruff TK. Tissue-engineered follicles produce live, fertile offspring. Tissue Eng 2006;12:2739-46.
  8. Liu J, Van der Elst J, Van den Broecke R, Dhont M. Live offspring by in vitro fertilization of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation. Biol Reprod 2001;64:171-8.
  9. 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;68:1682-6.
  10. Hasegawa A, Hamada Y, Mehandjiev T, Koyama K. In vitro growth and maturation as well as fertilization of mouse preantral oocytes from vitrified ovaries. Fertil Steril 2004;81 Suppl 1:824-30.
  11. Wang X, Catt S, Pangestu M, Temple-Smith P. Successful in vitro culture of pre-antral follicles derived from vitrified murine ovarian tissue: oocyte maturation, fertilization, and live births. Reproduction 2011;141:183-91.
  12. Hirshfeld-Cytron JE, Duncan FE, Xu M, Jozefik JK, Shea LD, Woodruff TK. Animal age, weight and estrus cycle stage impact the quality of in vitro grown follicles. Hum Reprod 2011;26:2473-85.
  13. Xu M, West E, Shea LD, Woodruff TK. Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol Reprod 2006;75:916-23.
  14. Xu M, Banc A, Woodruff TK, Shea LD. Secondary follicle growth and oocyte maturation by culture in alginate hydrogel following cryopreservation of the ovary or individual follicles. Biotechnol Bioeng 2009;103:378-86.
  15. Kim YJ, Ku SY, Rosenwaks Z, Liu HC, Chi SW, Kang JS, et al. MicroRNA expression profiles are altered by gonadotropins and vitamin C status during in vitro follicular growth. Reprod Sci 2010;17:1081-9.
  16. 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;93:2633-9.
  17. Segers I, Adriaenssens T, Ozturk E, Smitz J. Acquisition and loss of oocyte meiotic and developmental competence during in vitro antral follicle growth in mouse. Fertil Steril 2010;93:2695-700.
  18. Motohashi HH, Sankai T, Kada H. Live offspring from cryopreserved embryos following in vitro growth, maturation and fertilization of oocytes derived from preantral follicles in mice. J Reprod Dev 2011;57:715-22.
  19. Liu HC, He Z, Rosenwaks Z. In vitro culture and in vitro maturation of mouse preantral follicles with recombinant gonadotropins. Fertil Steril 2002;77:373-83.
  20. Choi JK, Ahn JI, Park JH, Lim JM. Derivation of developmentally competent oocytes by in vitro culture of preantral follicles retrieved from aged mice. Fertil Steril 2011;95:1487-9.
  21. Cortvrindt R, Smitz J, Van Steirteghem AC. Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Hum Reprod 1997;12:759-68.
  22. Adriaens I, Cortvrindt R, Smitz J. Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Hum Reprod 2004;19:398-408.
  23. Nottola SA, Cecconi S, Bianchi S, Motta C, Rossi G, Continenza MA, et al. Ultrastructure of isolated mouse ovarian follicles cultured in vitro. Reprod Biol Endocrinol 2011;9:3.
  24. Eppig JJ. Maintenance of meiotic arrest and the induction of oocyte maturation in mouse oocyte-granulosa cell complexes developed in vitro from preantral follicles. Biol Reprod 1991;45:824-30.
  25. Cortvrindt R, Hu Y, Smitz J. Recombinant luteinizing hormone as a survival and differentiation factor increases oocyte maturation in recombinant follicle stimulating hormone-supplemented mouse preantral follicle culture. Hum Reprod 1998;13:1292-302.
  26. Xu M, West-Farrell ER, Stouffer RL, Shea LD, Woodruff TK, Zelinski MB. Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol Reprod 2009;81:587-94.
  27. Guthrie HD, Garrett WM, Cooper BS. Follicle-stimulating hormone and insulin-like growth factor-I attenuate apoptosis in cultured porcine granulosa cells. Biol Reprod 1998;58:390-6.
  28. Liu X, Andoh K, Yokota H, Kobayashi J, Abe Y, Yamada K, et al. Effects of growth hormone, activin, and follistatin on the development of preantral follicle from immature female mice. Endocrinology 1998;139:2342-7.
  29. Klinger FG, De Felici M. In vitro development of growing oocytes from fetal mouse oocytes: stage-specific regulation by stem cell factor and granulosa cells. Dev Biol 2002;244:85-95.
  30. Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update 2005;11:461-71.
  31. Hutt KJ, McLaughlin EA, Holland MK. Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. Mol Hum Reprod 2006;12:61-9.
  32. Hunter MG, Paradis F. Intra-follicular regulatory mechanisms in the porcine ovary. Soc Reprod Fertil Suppl 2009;66:149-64.
  33. Celestino JJ, Bruno JB, Lima-Verde IB, Matos MH, Saraiva MV, Chaves RN, et al. Steady-state level of kit ligand mRNA in goat ovaries and the role of kit ligand in preantral follicle survival and growth in vitro. Mol Reprod Dev 2010;77:231-40.
  34. Pangas SA, Saudye H, Shea LD, Woodruff TK. Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes. Tissue Eng 2003;9:1013-21.
  35. Smitz J, Dolmans MM, Donnez J, Fortune JE, Hovatta O, Jewgenow K, et al. Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Hum Reprod Update 2010;16:395-414.
  36. Shikanov A, Xu M, Woodruff TK, Shea LD. Interpenetrating fibrinalginate matrices for in vitro ovarian follicle development. Biomaterials 2009;30:5476-85.

Cited by

  1. Physiologic Course of Female Reproductive Function: A Molecular Look into the Prologue of Life vol.2015, pp.None, 2015, https://doi.org/10.1155/2015/715735
  2. Effect of insulin supplementation on in vitro maturation of pre-antral follicles from adult and pre-pubertal mice vol.52, pp.5, 2012, https://doi.org/10.1007/s11626-016-0004-6
  3. Effects of Supplementation of Human Endometriotic Fluids on In Vitro Mouse Preantral Follicle Culture vol.25, pp.5, 2012, https://doi.org/10.1177/1933719116678687
  4. Figla promotes secondary follicle growth in mature mice vol.11, pp.1, 2012, https://doi.org/10.1038/s41598-021-89052-3