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Research Article

volume 54 issue 10 (october 2020) : 1195-1200,   Doi: 10.18805/ijar.B-1141

Optimization of Novel Follicle Culture System to Generate Developmentally Competent Oocytes

J
Jongwon Kim
J
Jung Kyu Choi
1Department of fiber system engineering, Yeungnam University, Gyeongsan 38541, South Korea.
Cite article:- Kim Jongwon, Choi Kyu Jung (2020). Optimization of Novel Follicle Culture System to Generate Developmentally Competent Oocytes. Indian Journal of Animal Research. 54(10): 1195-1200. doi: 10.18805/ijar.B-1141.

ABSTRACT

This study aimed to develop a novel culture system for porcine ovarian follicles that yields developmentally competent oocytes. We mechanically isolated ovarian follicles of various sizes (325–500 mm) and treated them with ovine follicle stimulating hormone (OFSH) at different concentrations (0–400 mIU). Follicle diameter, antrum formation and cumulus oocyte complex (COC) recovery rate were significantly higher (p < 0.05) under the 0 and 50 mIU OFSH treatments compared with the remaining concentrations (100, 200 and 400 mIU). Additionally, follicles cultured for 3 and 4 d differed significantly (p < 0.05) in follicle diameter, antrum formation rate and COC recovery from those cultured for 5 and 6 d. Follicle characteristics did not differ across diameter: those at 250–300, 301–400 and 401–500 mm in vitro had antrum formation rates of 90%, 92% and 90%, along with COC recovery of 78%, 82% and 85%, respectively. Furthermore, nuclear maturation percentages for oocytes that experienced germinal vesicle breakdown (GVBD) were 10%, 13% and 14%, depending on the size of the originating follicle (250–300, 301–400 and 401–500 mm). Nuclear maturation for metaphase II (MII) oocytes derived from follicles of those three sizes were 1%, 2% and 1%, respectively. After 3 d of culture, the 250–300 mm group differed significantly from other size groups in follicle diameter and COC recovery. This study provides insight into establishing effective protocols of ovarian follicle culture, thus improving efforts to preserve large-mammal fertility. 

REFERENCES

  1. Abir, R., Franks, S., Mobberley, M.A., Moore, P.A., Margara, R.A., Winston, R.M. (1997). Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertility and Sterility. 68:682–688.
  2. Choi, J.K., Agarwal, P., He, X. (2013). In vitro culture of early secondary preantral follicles in hanging drop of ovarian cell-conditioned medium to obtain MII oocytes from outbred deer mice. Tissue Engineering Part A. 19:2626–2637.
  3. Choi, J.K., Agarwal, P., Huang, H., Zhao, S., He, X. (2014). The crucial role of mechanical heterogeneity in regulating follicle development and ovulation with engineered ovarian microtissue. Biomaterials. 35:5122-5128.
  4. Cortvrindt, R., Smitz, J., Steirteghe, A.C. (1997). Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Human Reproduction. 12: 759-768.
  5. Elizabeth, A.M., Emerald, P., Philip, S.L., Alex, T., Aaron J.W.H. (1997). Follicle-stimulating hormone enhances the development of preantral follicles in juvenile rats. Biology of Reproduction. 57: 990–998. 
  6. Eppig, J. and O’Brien, M. (1996). Development in vitro of mouse oocytes from primordial follicles. Biology of Reproduction. 54: 197-207.
  7. Gutierrez, C.G., Ralph, J.H., Telfer, E.E., Wilmut, I., Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biology of Reproduction. 62:1322-1328.
  8. Hirao, Y., Nagai, T., Kubo, M., Miyano, T., Miyake, M., Kato, S. (1994). In vitro growth and maturation of pig oocytes. Douglas T. Carrell2Division of Urology, University of Utah School of Medicine, Salt Lake City, Utah 84132 Search for other works by this author on: Oxford Academic Google Scholar Hsueh, A.J., Billig, H., Tsafriri, A. (1994). Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocrine Reviews. 15:707–724.
  9. Itoh, T., Kacchi, M., Abe, H., Sendai, Y., Hoshi, H. (2002). Growth, antrum formation and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biology of Reproduction. 67:1099-105.
  10. Jin, S.Y., Lei, L., Shikanov, A., Shea, L.D., Woodruff, T.K. (2010). A novel two-step strategy for in vitro culture of earlystage ovarian follicles in the mouse. Fertility and Sterility. 93: 2633-2639.
  11. Kim, I.W., Gong, S.P., Yoo, C.R., Choi, J.H., Kim, D.Y., Lim, J.M. (2009). Derivation of developmentally competent oocytes by the culture of preantral follicles retrieved from adult ovaries: maturation, blastocyst formation and embryonic stem cell transformation. Fertility and Sterility. 92: 1716-1724.
  12. Liu, J., Van der Elst, J., Van den Broecke, R., Dhont, M. (2001). Live offspring by in vitro fertilization of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation. Biology of Reproduction. 64: 171-178.
  13. Mao, J.G., Wu, M. F., Smith, T. C., McCauley, T. C., Cantley, R. S., Prather, B. A., Day, B. N. (2002). Effects of culture medium, serum type and various concentrations of follicle-stimulating hormone on porcine preantral follicular development and antrum formation in vitro. Biology of Reproduction. 67: 1197-1203. 
  14. Pracy, J. P., White, A., Mustafa, Y., Smith, D., Perry, M. E. (1998). The comparative anatomy of the pig middle ear cavity: a model for middle ear in¯ammation in the human? J Anatomy. 192: 359-368.
  15. Shikanov, A., Xu, M., Woodruff, T.K., Shea, L.D. (2009). Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials. 30:5476-5485.
  16. Swindle, M. M., Makin, A., Herron, A. J., Clubb Jr, F. J., Frazier, K. S. (2012). Swine as models in biomedical research and Toxicology Testing. Veterinary Pathology. 49: 344-356.
  17. Telfer, E.E. and McLaughlin, M. (2011). In vitro development of ovarian follicles. Seminars in Reproductive Medicine. 29:15-23. 
  18. West, E.R, Shea, L.D., Woodruff, T.K. (2007). Engineering the follicle microenvironment. Seminars in Reproductive Medicine. 25:287-299.
  19. Wu, J., Carrell, D.T., Wilcox, A.L. (2001). Development of in vitro-matured oocytes from porcine preantral follicles following intracytoplasmic sperm injection. Biology of Reproduction. 65:1579–1585.
  20. Xu, M., Woodruff, T.K., Shea, L.D. (2007). Bioengineering and the ovarian follicle. Cancer Treatment and Research. 138:75-82.
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Indian Journal of Animal Research
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    Research Article

    volume 54 issue 10 (october 2020) : 1195-1200,   Doi: 10.18805/ijar.B-1141

    Optimization of Novel Follicle Culture System to Generate Developmentally Competent Oocytes

    J
    Jongwon Kim
    J
    Jung Kyu Choi
    1Department of fiber system engineering, Yeungnam University, Gyeongsan 38541, South Korea.
    Cite article:- Kim Jongwon, Choi Kyu Jung (2020). Optimization of Novel Follicle Culture System to Generate Developmentally Competent Oocytes. Indian Journal of Animal Research. 54(10): 1195-1200. doi: 10.18805/ijar.B-1141.

    ABSTRACT

    This study aimed to develop a novel culture system for porcine ovarian follicles that yields developmentally competent oocytes. We mechanically isolated ovarian follicles of various sizes (325–500 mm) and treated them with ovine follicle stimulating hormone (OFSH) at different concentrations (0–400 mIU). Follicle diameter, antrum formation and cumulus oocyte complex (COC) recovery rate were significantly higher (p < 0.05) under the 0 and 50 mIU OFSH treatments compared with the remaining concentrations (100, 200 and 400 mIU). Additionally, follicles cultured for 3 and 4 d differed significantly (p < 0.05) in follicle diameter, antrum formation rate and COC recovery from those cultured for 5 and 6 d. Follicle characteristics did not differ across diameter: those at 250–300, 301–400 and 401–500 mm in vitro had antrum formation rates of 90%, 92% and 90%, along with COC recovery of 78%, 82% and 85%, respectively. Furthermore, nuclear maturation percentages for oocytes that experienced germinal vesicle breakdown (GVBD) were 10%, 13% and 14%, depending on the size of the originating follicle (250–300, 301–400 and 401–500 mm). Nuclear maturation for metaphase II (MII) oocytes derived from follicles of those three sizes were 1%, 2% and 1%, respectively. After 3 d of culture, the 250–300 mm group differed significantly from other size groups in follicle diameter and COC recovery. This study provides insight into establishing effective protocols of ovarian follicle culture, thus improving efforts to preserve large-mammal fertility. 

    REFERENCES

    1. Abir, R., Franks, S., Mobberley, M.A., Moore, P.A., Margara, R.A., Winston, R.M. (1997). Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertility and Sterility. 68:682–688.
    2. Choi, J.K., Agarwal, P., He, X. (2013). In vitro culture of early secondary preantral follicles in hanging drop of ovarian cell-conditioned medium to obtain MII oocytes from outbred deer mice. Tissue Engineering Part A. 19:2626–2637.
    3. Choi, J.K., Agarwal, P., Huang, H., Zhao, S., He, X. (2014). The crucial role of mechanical heterogeneity in regulating follicle development and ovulation with engineered ovarian microtissue. Biomaterials. 35:5122-5128.
    4. Cortvrindt, R., Smitz, J., Steirteghe, A.C. (1997). Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Human Reproduction. 12: 759-768.
    5. Elizabeth, A.M., Emerald, P., Philip, S.L., Alex, T., Aaron J.W.H. (1997). Follicle-stimulating hormone enhances the development of preantral follicles in juvenile rats. Biology of Reproduction. 57: 990–998. 
    6. Eppig, J. and O’Brien, M. (1996). Development in vitro of mouse oocytes from primordial follicles. Biology of Reproduction. 54: 197-207.
    7. Gutierrez, C.G., Ralph, J.H., Telfer, E.E., Wilmut, I., Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biology of Reproduction. 62:1322-1328.
    8. Hirao, Y., Nagai, T., Kubo, M., Miyano, T., Miyake, M., Kato, S. (1994). In vitro growth and maturation of pig oocytes. Douglas T. Carrell2Division of Urology, University of Utah School of Medicine, Salt Lake City, Utah 84132 Search for other works by this author on: Oxford Academic Google Scholar Hsueh, A.J., Billig, H., Tsafriri, A. (1994). Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocrine Reviews. 15:707–724.
    9. Itoh, T., Kacchi, M., Abe, H., Sendai, Y., Hoshi, H. (2002). Growth, antrum formation and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biology of Reproduction. 67:1099-105.
    10. Jin, S.Y., Lei, L., Shikanov, A., Shea, L.D., Woodruff, T.K. (2010). A novel two-step strategy for in vitro culture of earlystage ovarian follicles in the mouse. Fertility and Sterility. 93: 2633-2639.
    11. Kim, I.W., Gong, S.P., Yoo, C.R., Choi, J.H., Kim, D.Y., Lim, J.M. (2009). Derivation of developmentally competent oocytes by the culture of preantral follicles retrieved from adult ovaries: maturation, blastocyst formation and embryonic stem cell transformation. Fertility and Sterility. 92: 1716-1724.
    12. Liu, J., Van der Elst, J., Van den Broecke, R., Dhont, M. (2001). Live offspring by in vitro fertilization of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation. Biology of Reproduction. 64: 171-178.
    13. Mao, J.G., Wu, M. F., Smith, T. C., McCauley, T. C., Cantley, R. S., Prather, B. A., Day, B. N. (2002). Effects of culture medium, serum type and various concentrations of follicle-stimulating hormone on porcine preantral follicular development and antrum formation in vitro. Biology of Reproduction. 67: 1197-1203. 
    14. Pracy, J. P., White, A., Mustafa, Y., Smith, D., Perry, M. E. (1998). The comparative anatomy of the pig middle ear cavity: a model for middle ear in¯ammation in the human? J Anatomy. 192: 359-368.
    15. Shikanov, A., Xu, M., Woodruff, T.K., Shea, L.D. (2009). Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials. 30:5476-5485.
    16. Swindle, M. M., Makin, A., Herron, A. J., Clubb Jr, F. J., Frazier, K. S. (2012). Swine as models in biomedical research and Toxicology Testing. Veterinary Pathology. 49: 344-356.
    17. Telfer, E.E. and McLaughlin, M. (2011). In vitro development of ovarian follicles. Seminars in Reproductive Medicine. 29:15-23. 
    18. West, E.R, Shea, L.D., Woodruff, T.K. (2007). Engineering the follicle microenvironment. Seminars in Reproductive Medicine. 25:287-299.
    19. Wu, J., Carrell, D.T., Wilcox, A.L. (2001). Development of in vitro-matured oocytes from porcine preantral follicles following intracytoplasmic sperm injection. Biology of Reproduction. 65:1579–1585.
    20. Xu, M., Woodruff, T.K., Shea, L.D. (2007). Bioengineering and the ovarian follicle. Cancer Treatment and Research. 138:75-82.
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