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Current IssueEditorial BoardOnline First ArticlesArchive

Reviewer Article

volume 40 issue 4 (december 2020) : 440-444,   Doi: 10.18805/ag.D-5104

Ovarian Insulin-Like Growth Factor-I

M
M. Bijna
K
K. Karthiayini
1Department of Veterinary Physiology, College of Veterinary and Animal Sciences, Kerala Veterinary and Animal Sciences University, Mannuthy-680 651, Kerala, India.
Cite article:- Bijna M., Karthiayini K. (2020). Ovarian Insulin-Like Growth Factor-I. Agricultural Science Digest. 40(4): 440-444. doi: 10.18805/ag.D-5104.

ABSTRACT

The insulin-like growth factor-I is a pleotropic growth factor that modulates cell replication. Insulin-like growth factor-I is produced by granulosa, theca and luteal cells and have autocrine and paracrine actions. It plays a crucial role in animal fertility acting as a monitoring signal. Researches have shown that synergistically with gonadotropins it stimulates the growth, survivability and steroidogenesis of follicular cells.

REFERENCES

  1. Adashi, E.Y., Resnick, C.E., D’Ercole A.J., Svoboda, M.E., Wyk J.J. (1985). Insulin-like growth factors as intraovarian regulators of granulosa cell growth and function. Endocrine Reviews. 6(3): 400-420.
  2. Armstrong, D.G., Baxter, G., Hogg, C.O., Woad, K.J. (2002). Insulin- like growth factor (IGF) system in the oocyte and somatic cells of bovine pre-antral follicles. Reproduction. 123: 789-797.
  3. Berisha, B and Schams, D. (2005). Ovarian function in ruminants. Domestic Animal Endocrinology. 29: 305–317. 
  4. Behl, R and Pandey, R.S. (1999). Effect of recombinant insulin-    like growth factor 1 on caprine granulosa cell steroidogenesis, in vitro. Small Ruminant Research. 33: 165-169. 
  5. Brito, I.R., Saraiva, M.V.A., Araujo, V.R., Celestino, J.J.H., Magalhaes, D.M., Lima, I.M.T., Hurk, R., Figueiredo, J.R. and Silva, J.R.V. (2012). The effect of IGF1 and FSH on the in vitro development of caprine secondary follicles and on the IGF1, IGFR and FSHR mRNA levels. Researches in Veterinary Science. 93: 729-732.
  6. Clemmons, R.D. (2009). Role of IGF1 in skeletal muscle mass maintenance. Trends in Endocrinology and Metabolism. 20(7): 349-356.
  7. Denley, A., Cosarove, L.J., Booker, G.W., Wallace, J.W., Brinoy, E. (2005). Molecular interactions of the IGF system. Cytokine Growth Factor Reviews. 16: 421-429.
  8. Dev, R., Sharma, M.K., Dheer, S. (2010). Insulin-like growth factor- I and-II in buffalo ovary: mRNA expressions and partial sequences. Indian Journal of Animal Sciences. 80(4): 306-312.
  9. Dubey, P.K., Amar Nath., Vikash, C., Sarkar, M., Saikumar, G., Sharma, T. (2015). Expression of mRNA encoding IGF-I, IGF-II, Type-I, and II IGF-Receptors and IGFBPs 1-4 during ovarian follicular development in buffalo (Bubalus bubalis). Animal Biotechnology. 26(2): 81-91.
  10. Echternkamp SE, Howard HJ, Roberts AJ, Grizzle J, Wise T. (1994). Relationships among concentrations of steroids, insulin- like growth factor-I and insulin-like growth factor binding proteins in ovarian follicular fluid of beef cattle. Biology of Reproduction. 51(5): 971-981.
  11. El-Roeiy, A., Chen X.I., Roberts, V.J., LeRoith, D., Roberts, C.T., Yen, S.S. (1993). Expression of insulin-like growth factor-I (IGF-I) and IGF-II and the IGF-I, IGF-II, and insulin receptor genes and localization of the gene products in the human ovary. The Journal of Clinical Endocrinology and Metabolism. 77(5): 1411-1418.
  12. Fortune, J.E., Riveral, G.M. and Yang, M.Y. (2004). Follicular development: the role of microenvironment in selection of the dominant follicle. Animal Reproduction Science. 83: 109-126.
  13. Gouveia, B.B., Bezerral, M.E.S., Monte, A.P.O., Santos, J.M.S., Barberino, R.S., Macedo, T.J., Menezes, V.G., Barros, V.R.P., Lima, I.B. and Matos, M.H.T. (2015). Effect of IGF1 on the morphology and development of ovine pre-antral follicles cultured in situ. Proceedings of the 29th Annual Meeting of the Brazilian Embryo Technology Society (SBTE). pp. 581-600.
  14. Giudice, L.C. (1992). Insulin-like growth factors and ovarian follicular development. Endocrinology Society. 13: 641-670.
  15. Giudice, L.C. (2001). Insulin-like growth factor family in Graafian follicle development andfunction. Journal of the Society for Gynecologic Investigation. 8: 26-29.
  16. Hastie, P.M. and Haresign, W. 2006.Expression of mRNA encoding insulin-like growth factor (IGF) ligands, IGF receptors and IGF binding proteins during follicular growth and atresia in the ovine ovary throughout oestrous cycle. Animal Reproduction Science. 92: 284-299.
  17. Huanmin, Z. and Yong, Z. (2005). Effect of growth factors on in vitro development of caprine pre-antral follicle oocytes. Animal Reproduction Science. 90: 265-272.
  18. Jones, J.I. and Clemmons, D.R. (1995). Insulin like growth factors and their binding proteins: biological actions. Endocrinology Reviews. 16: 3-34.
  19. Kostecka, Z and Blahovec, J. (2002). Animal insulin-like growth factor binding proteins and their biological functions. Veterinarni Medicina-Praha. 2: 75-84.
  20. Kumar, A. and Laxmi, N. A. (2015). Role of IGF 1 in male and female reproduction in bovines: A review. Asia Pacific Journal of Research. 1(24): 17-25.
  21. Laron, Z. (2001). Insulin-like growth factor1 (IGF1): A growth hormone. Journal of Clinical Pathology. 54: 311-316.
  22. Lucy, M.C. (2000). Regulation of ovarian follicular growth by somatotropin and insulin-like growth factors in cattle. Journal of Dairy Science. 83: 1635-1647.
  23. Martins, F.S., Saraiva, M.V.A., Celestino, J.J.H., Bruno, J.B., Almeida, A.P., Cunha, R.M.S., Silva, J.R.V., Campello, C.C., Lucci, C.M., Matos, M.H.T., Figueiredo, J.R. (2010). Expression of protein and mRNA encoding insulin-like growth factor 1(IGF1) in goat ovarian follicles and the influence of IGF1 on in vitro development and survival of caprine pre-antral follicles. Animal Reproduction. 7: 349-361.
  24. Magalhaes, D.M., Lee, J.G., Wischral,A., Gastal, M.O., Fonseca, G.R., Eloy, Y.R.G., Geisler, M., Figueiredo, J.R., Gastal, E.L. (2013). Gene expression during early folliculogenesis in goats using microarray analysis. Bioogy of Reproduction. 89: 1-12.
  25. Matsui, M., Sonntag, B., Hwang, S.S., Byerly, T., Hourvitz, A., Adashi, E.Y., Shimasaki, S., Erickson, G.F. (2004). Pregnancy-associated plasma protein-A production in rat granulosa cells: stimulation by follicle-stimulating hormone and inhibition by the oocyte-derived bone morphogenetic protein-15. Endocrinology. 145(8): 3686–3695.
  26. Meiyu, Q., Roth, Z and Di, L. (2011). Insulin-like growth factor 1 (IGF1) in reproduction system of female bovine. Journal of Northeast Agriculture University, 18: 84-87.
  27. Mikawa, S., Yoshikawa, G., Aoki, H., Yamano, Y., Sakai, H., Komano, T. (1995). Dynamic aspects in the expression of the goat insulin-like growth factor-I (IGF-I) gene: diversity in transcription and post-transcription. Bioscience Biotech- -nology Biochemistry. 59: 87-92.
  28. Monget, P. and Bondy, C. (2000). Importance of IGF system in early folliculogenesis. Molecular and Cell Endocrinology. 163: 89-93.
  29. Monget, P., Monniaux, D., Pisselet, C., Durand, P. (1993). Changes in insulin- like growth factor I (IGF- I), IGF- II and their binding proteins during growth and atresia of ovine ovarian follicles. Endocrinology. 132: 1438-1446.
  30. Monniaux, D., Monget, P., Bernard, N., Huet, C., Pisselet, C. (1997). Growth factors and antral follicular development in domestic ruminants. Theriogenology. 47: 3-12.
  31. Monte, A.P.O., Barros, V.R.P., Santos, J.M., Menezes, V.G., Cavalcante, A.Y.P., Gouveia, B.B., Bezerra, M.E.S., Macedo, T.J.S. and Matos, M.H.T. (2019). Immunohistochemical localization of insulin-like growth factor-1 (IGF-1) in the sheep ovary and the synergistic effect of IGF-1 and FSH on follicular development in vitro and LH receptor immunostaining. Theriogenology. 129: 61-69.
  32. Nayan, V., Bhardwaj, A., Singh, D. (2013). PAPP-A in Indian Water Buffalo (Bubalus bubalis) Ovary: Phylogeny, Expression, Hormonal Regulation, and Sequence Characterization. Agricultural Research. 2: 153–165. https://doi.org/10.1007/s40003-013-0062-x
  33. Neirijnck Y., Papaioannou M.D., Nef S. (2019). The Insulin/IGF System in Mammalian Sexual Development and Reproduction. International Journal of Molecular Sciences. 18: 4440.
  34. Othman, O.E., Alam, S.S. and Aziem, A.S.H. (2014). Single nucleotide polymorphism in Egyptian cattle insulin-like growth factor binding protein-3 gene. Journal of Genetic Engineering and Biotechnology. 12: 143-147.
  35. Rebouças, E.L., Jose J.N., Costa, Passos, M.J., Silva, A.W.B., Rossi, R.O.D.S., Hurk, V.R., Silva, J.R.V. (2013). Expression levels of mRNA for insulin-like growth factors, IGF receptors and IGF binding proteins in in vivo and in vitro grown bovine follicles. Zygote. 22: 521–532.
  36. Satrapa, R.A., Castilho, S.A., Eduardo, M.R., Pegorer, F.M., Puelker, R., Barros. (2013). Differential expression of members of the IGF system in OPU-derived oocytes from Nelore (Bos indicus) and Holstein cows. Animal Reproduction Science. 138: 155-158.
  37. Sirotkin, A.V. (2010). Growth factors controlling ovarian functions. Journal of Cell Physiology. 226: 2222–2225. 
  38. Singh, J., Paul, A., Thakur, N., Yadav, V. P., Panda, R.P., Bhure, K., Sarkar M. (2015). Localization of IGF proteins in various stages of ovarian follicular development and modulatory role of IGF-I on granulosa cell steroid production in water buffalo (Bubalus bubalis). Animal Reproduction Science. 158: 31-52.
  39. Spicer, L.J and Aad, P.Y. (2007). Insulin like growth factor (IGF) 2 stimulates steroidogenesis and mitosis of bovine granulosa cells through the IGF1 receptor: role of follicle stimulating hormone and IGF2 receptor. Biology of Reproduction. 77: 18-27.
  40. Spicer, L.J and Echternkamp, S.E. (1995). The ovarian insulin and insulin like growth factor system with special emphasis to domestic animals. Domestic Animal Endocrinology. 12: 223-245.
  41. Thomas, F.H., Campbell, B.K., Armstrong, D.G., Telfer, E.E. (2007). Effects of IGF-I bioavailability on bovine preantral follicular development in vitro. Reproduction. 133(6): 1121-1128.
  42. Wandji, S,A., Wood, T.L., Crawford, J., Levison, S.W., Hammond J.M. (1998). Expression of mouse ovarian insulin growth factor system components during follicular development and atresia. Endocrinology. 139: 5205-5214
  43. Wood, J. R. and Strauss, I. J. F. (2002). Multiple signal transduction pathways regulate ovarian steroidogenesis. Reviews in Endocrine and Metabolic Disorders. 3: 3-46. 
  44. Yu, Y., Li, W., Han, Z., Luo, M., Chang, Z., Tan, J. (2003). The effect of follicle-stimulating hormone on follicular development, granulosa cell apoptosis and steroidogenesis and its mediation by insulin-like growth factor-I in the goat ovary. Theriogenology. 60: 1691–1704. 
  45. Zhao, J., Taverne, M.A.M., Weijden, V.G.C., Bevers, M.M., Hurk, V.R. (2001). Insulin-like growth factor-I (IGF-I) stimulates the development of cultured rat pre-antral follicles. Molecular Reproduction and Development: Incorporating Gamete Research. 58: 287-296.
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    Reviewer Article

    volume 40 issue 4 (december 2020) : 440-444,   Doi: 10.18805/ag.D-5104

    Ovarian Insulin-Like Growth Factor-I

    M
    M. Bijna
    K
    K. Karthiayini
    1Department of Veterinary Physiology, College of Veterinary and Animal Sciences, Kerala Veterinary and Animal Sciences University, Mannuthy-680 651, Kerala, India.
    Cite article:- Bijna M., Karthiayini K. (2020). Ovarian Insulin-Like Growth Factor-I. Agricultural Science Digest. 40(4): 440-444. doi: 10.18805/ag.D-5104.

    ABSTRACT

    The insulin-like growth factor-I is a pleotropic growth factor that modulates cell replication. Insulin-like growth factor-I is produced by granulosa, theca and luteal cells and have autocrine and paracrine actions. It plays a crucial role in animal fertility acting as a monitoring signal. Researches have shown that synergistically with gonadotropins it stimulates the growth, survivability and steroidogenesis of follicular cells.

    REFERENCES

    1. Adashi, E.Y., Resnick, C.E., D’Ercole A.J., Svoboda, M.E., Wyk J.J. (1985). Insulin-like growth factors as intraovarian regulators of granulosa cell growth and function. Endocrine Reviews. 6(3): 400-420.
    2. Armstrong, D.G., Baxter, G., Hogg, C.O., Woad, K.J. (2002). Insulin- like growth factor (IGF) system in the oocyte and somatic cells of bovine pre-antral follicles. Reproduction. 123: 789-797.
    3. Berisha, B and Schams, D. (2005). Ovarian function in ruminants. Domestic Animal Endocrinology. 29: 305–317. 
    4. Behl, R and Pandey, R.S. (1999). Effect of recombinant insulin-    like growth factor 1 on caprine granulosa cell steroidogenesis, in vitro. Small Ruminant Research. 33: 165-169. 
    5. Brito, I.R., Saraiva, M.V.A., Araujo, V.R., Celestino, J.J.H., Magalhaes, D.M., Lima, I.M.T., Hurk, R., Figueiredo, J.R. and Silva, J.R.V. (2012). The effect of IGF1 and FSH on the in vitro development of caprine secondary follicles and on the IGF1, IGFR and FSHR mRNA levels. Researches in Veterinary Science. 93: 729-732.
    6. Clemmons, R.D. (2009). Role of IGF1 in skeletal muscle mass maintenance. Trends in Endocrinology and Metabolism. 20(7): 349-356.
    7. Denley, A., Cosarove, L.J., Booker, G.W., Wallace, J.W., Brinoy, E. (2005). Molecular interactions of the IGF system. Cytokine Growth Factor Reviews. 16: 421-429.
    8. Dev, R., Sharma, M.K., Dheer, S. (2010). Insulin-like growth factor- I and-II in buffalo ovary: mRNA expressions and partial sequences. Indian Journal of Animal Sciences. 80(4): 306-312.
    9. Dubey, P.K., Amar Nath., Vikash, C., Sarkar, M., Saikumar, G., Sharma, T. (2015). Expression of mRNA encoding IGF-I, IGF-II, Type-I, and II IGF-Receptors and IGFBPs 1-4 during ovarian follicular development in buffalo (Bubalus bubalis). Animal Biotechnology. 26(2): 81-91.
    10. Echternkamp SE, Howard HJ, Roberts AJ, Grizzle J, Wise T. (1994). Relationships among concentrations of steroids, insulin- like growth factor-I and insulin-like growth factor binding proteins in ovarian follicular fluid of beef cattle. Biology of Reproduction. 51(5): 971-981.
    11. El-Roeiy, A., Chen X.I., Roberts, V.J., LeRoith, D., Roberts, C.T., Yen, S.S. (1993). Expression of insulin-like growth factor-I (IGF-I) and IGF-II and the IGF-I, IGF-II, and insulin receptor genes and localization of the gene products in the human ovary. The Journal of Clinical Endocrinology and Metabolism. 77(5): 1411-1418.
    12. Fortune, J.E., Riveral, G.M. and Yang, M.Y. (2004). Follicular development: the role of microenvironment in selection of the dominant follicle. Animal Reproduction Science. 83: 109-126.
    13. Gouveia, B.B., Bezerral, M.E.S., Monte, A.P.O., Santos, J.M.S., Barberino, R.S., Macedo, T.J., Menezes, V.G., Barros, V.R.P., Lima, I.B. and Matos, M.H.T. (2015). Effect of IGF1 on the morphology and development of ovine pre-antral follicles cultured in situ. Proceedings of the 29th Annual Meeting of the Brazilian Embryo Technology Society (SBTE). pp. 581-600.
    14. Giudice, L.C. (1992). Insulin-like growth factors and ovarian follicular development. Endocrinology Society. 13: 641-670.
    15. Giudice, L.C. (2001). Insulin-like growth factor family in Graafian follicle development andfunction. Journal of the Society for Gynecologic Investigation. 8: 26-29.
    16. Hastie, P.M. and Haresign, W. 2006.Expression of mRNA encoding insulin-like growth factor (IGF) ligands, IGF receptors and IGF binding proteins during follicular growth and atresia in the ovine ovary throughout oestrous cycle. Animal Reproduction Science. 92: 284-299.
    17. Huanmin, Z. and Yong, Z. (2005). Effect of growth factors on in vitro development of caprine pre-antral follicle oocytes. Animal Reproduction Science. 90: 265-272.
    18. Jones, J.I. and Clemmons, D.R. (1995). Insulin like growth factors and their binding proteins: biological actions. Endocrinology Reviews. 16: 3-34.
    19. Kostecka, Z and Blahovec, J. (2002). Animal insulin-like growth factor binding proteins and their biological functions. Veterinarni Medicina-Praha. 2: 75-84.
    20. Kumar, A. and Laxmi, N. A. (2015). Role of IGF 1 in male and female reproduction in bovines: A review. Asia Pacific Journal of Research. 1(24): 17-25.
    21. Laron, Z. (2001). Insulin-like growth factor1 (IGF1): A growth hormone. Journal of Clinical Pathology. 54: 311-316.
    22. Lucy, M.C. (2000). Regulation of ovarian follicular growth by somatotropin and insulin-like growth factors in cattle. Journal of Dairy Science. 83: 1635-1647.
    23. Martins, F.S., Saraiva, M.V.A., Celestino, J.J.H., Bruno, J.B., Almeida, A.P., Cunha, R.M.S., Silva, J.R.V., Campello, C.C., Lucci, C.M., Matos, M.H.T., Figueiredo, J.R. (2010). Expression of protein and mRNA encoding insulin-like growth factor 1(IGF1) in goat ovarian follicles and the influence of IGF1 on in vitro development and survival of caprine pre-antral follicles. Animal Reproduction. 7: 349-361.
    24. Magalhaes, D.M., Lee, J.G., Wischral,A., Gastal, M.O., Fonseca, G.R., Eloy, Y.R.G., Geisler, M., Figueiredo, J.R., Gastal, E.L. (2013). Gene expression during early folliculogenesis in goats using microarray analysis. Bioogy of Reproduction. 89: 1-12.
    25. Matsui, M., Sonntag, B., Hwang, S.S., Byerly, T., Hourvitz, A., Adashi, E.Y., Shimasaki, S., Erickson, G.F. (2004). Pregnancy-associated plasma protein-A production in rat granulosa cells: stimulation by follicle-stimulating hormone and inhibition by the oocyte-derived bone morphogenetic protein-15. Endocrinology. 145(8): 3686–3695.
    26. Meiyu, Q., Roth, Z and Di, L. (2011). Insulin-like growth factor 1 (IGF1) in reproduction system of female bovine. Journal of Northeast Agriculture University, 18: 84-87.
    27. Mikawa, S., Yoshikawa, G., Aoki, H., Yamano, Y., Sakai, H., Komano, T. (1995). Dynamic aspects in the expression of the goat insulin-like growth factor-I (IGF-I) gene: diversity in transcription and post-transcription. Bioscience Biotech- -nology Biochemistry. 59: 87-92.
    28. Monget, P. and Bondy, C. (2000). Importance of IGF system in early folliculogenesis. Molecular and Cell Endocrinology. 163: 89-93.
    29. Monget, P., Monniaux, D., Pisselet, C., Durand, P. (1993). Changes in insulin- like growth factor I (IGF- I), IGF- II and their binding proteins during growth and atresia of ovine ovarian follicles. Endocrinology. 132: 1438-1446.
    30. Monniaux, D., Monget, P., Bernard, N., Huet, C., Pisselet, C. (1997). Growth factors and antral follicular development in domestic ruminants. Theriogenology. 47: 3-12.
    31. Monte, A.P.O., Barros, V.R.P., Santos, J.M., Menezes, V.G., Cavalcante, A.Y.P., Gouveia, B.B., Bezerra, M.E.S., Macedo, T.J.S. and Matos, M.H.T. (2019). Immunohistochemical localization of insulin-like growth factor-1 (IGF-1) in the sheep ovary and the synergistic effect of IGF-1 and FSH on follicular development in vitro and LH receptor immunostaining. Theriogenology. 129: 61-69.
    32. Nayan, V., Bhardwaj, A., Singh, D. (2013). PAPP-A in Indian Water Buffalo (Bubalus bubalis) Ovary: Phylogeny, Expression, Hormonal Regulation, and Sequence Characterization. Agricultural Research. 2: 153–165. https://doi.org/10.1007/s40003-013-0062-x
    33. Neirijnck Y., Papaioannou M.D., Nef S. (2019). The Insulin/IGF System in Mammalian Sexual Development and Reproduction. International Journal of Molecular Sciences. 18: 4440.
    34. Othman, O.E., Alam, S.S. and Aziem, A.S.H. (2014). Single nucleotide polymorphism in Egyptian cattle insulin-like growth factor binding protein-3 gene. Journal of Genetic Engineering and Biotechnology. 12: 143-147.
    35. Rebouças, E.L., Jose J.N., Costa, Passos, M.J., Silva, A.W.B., Rossi, R.O.D.S., Hurk, V.R., Silva, J.R.V. (2013). Expression levels of mRNA for insulin-like growth factors, IGF receptors and IGF binding proteins in in vivo and in vitro grown bovine follicles. Zygote. 22: 521–532.
    36. Satrapa, R.A., Castilho, S.A., Eduardo, M.R., Pegorer, F.M., Puelker, R., Barros. (2013). Differential expression of members of the IGF system in OPU-derived oocytes from Nelore (Bos indicus) and Holstein cows. Animal Reproduction Science. 138: 155-158.
    37. Sirotkin, A.V. (2010). Growth factors controlling ovarian functions. Journal of Cell Physiology. 226: 2222–2225. 
    38. Singh, J., Paul, A., Thakur, N., Yadav, V. P., Panda, R.P., Bhure, K., Sarkar M. (2015). Localization of IGF proteins in various stages of ovarian follicular development and modulatory role of IGF-I on granulosa cell steroid production in water buffalo (Bubalus bubalis). Animal Reproduction Science. 158: 31-52.
    39. Spicer, L.J and Aad, P.Y. (2007). Insulin like growth factor (IGF) 2 stimulates steroidogenesis and mitosis of bovine granulosa cells through the IGF1 receptor: role of follicle stimulating hormone and IGF2 receptor. Biology of Reproduction. 77: 18-27.
    40. Spicer, L.J and Echternkamp, S.E. (1995). The ovarian insulin and insulin like growth factor system with special emphasis to domestic animals. Domestic Animal Endocrinology. 12: 223-245.
    41. Thomas, F.H., Campbell, B.K., Armstrong, D.G., Telfer, E.E. (2007). Effects of IGF-I bioavailability on bovine preantral follicular development in vitro. Reproduction. 133(6): 1121-1128.
    42. Wandji, S,A., Wood, T.L., Crawford, J., Levison, S.W., Hammond J.M. (1998). Expression of mouse ovarian insulin growth factor system components during follicular development and atresia. Endocrinology. 139: 5205-5214
    43. Wood, J. R. and Strauss, I. J. F. (2002). Multiple signal transduction pathways regulate ovarian steroidogenesis. Reviews in Endocrine and Metabolic Disorders. 3: 3-46. 
    44. Yu, Y., Li, W., Han, Z., Luo, M., Chang, Z., Tan, J. (2003). The effect of follicle-stimulating hormone on follicular development, granulosa cell apoptosis and steroidogenesis and its mediation by insulin-like growth factor-I in the goat ovary. Theriogenology. 60: 1691–1704. 
    45. Zhao, J., Taverne, M.A.M., Weijden, V.G.C., Bevers, M.M., Hurk, V.R. (2001). Insulin-like growth factor-I (IGF-I) stimulates the development of cultured rat pre-antral follicles. Molecular Reproduction and Development: Incorporating Gamete Research. 58: 287-296.
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