Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

A combination of insulin-like growth factor I (IGF-I) and FSH promotes proliferation of prepubertal bovine Sertoli cells isolated and cultured in vitro

A. Dance A , J. Kastelic A and J. Thundathil A B
+ Author Affiliations
- Author Affiliations

A Department of Production Animal Health, Faculty of Veterinary Medicine, University of Calgary, 3330 Hospital Dr. NW Calgary, AB T2N 4N1, Canada.

B Corresponding author. Email: jthundat@ucalgary.ca

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16122
Submitted: 17 March 2016  Accepted: 3 August 2016   Published online: 5 October 2016

Abstract

Beef and dairy bull calves fed a low-nutrition diet during early life had decreased concentrations of circulating insulin-like growth factor I (IGF-I), delayed increases in testosterone, smaller testes and delayed puberty compared with those fed high-nutrition diets. Although IGF-1 has important roles in Sertoli cell function in rats and mice, this has not been well documented in bulls. The objectives of this study were to: (1) isolate Sertoli cells from bull calves at 8 weeks of age, (2) culture them in vitro and (3) determine the effects of IGF-I, FSH and a combination of both hormones on cell proliferation. For Sertoli cell isolation, minced testicular tissues were treated with collagenase followed by trypsin and hyaluronidase to digest seminiferous tubules and release Sertoli cells. In this study, Sertoli cells were successfully isolated from 8-week-old Holstein bull calves (n = 4) and these cells were cultured for up to 8 days. A combination of IGF-I and FSH increased proliferation (~18%) and therefore cell number (1.5-fold) of prepubertal bovine Sertoli cells in culture, providing clear evidence that IGF-I has a similar role in bovine Sertoli cells as reported in rodents.

Additional keywords: bull, endocrine, godadotropins, nutrition, puberty, sperm, testicular somatic cells.


References

Almquist, J. O., and Barber, K. A. (1974). Pubertal characteristics and early growth of Charolais bulls on high nutrient allowance. J. Anim. Sci. 38, 831–834.
Pubertal characteristics and early growth of Charolais bulls on high nutrient allowance.CrossRef | 1:STN:280:DyaE2c7ksFKnug%3D%3D&md5=14e8cccd071f9f56a89352dfe0602aadCAS | 4856700PubMed | open url image1

Amann, R. P. (1983). Endocrine changes associated with onset of spermatogenesis in Holstein bulls. J. Dairy Sci. 66, 2606–2622.
Endocrine changes associated with onset of spermatogenesis in Holstein bulls.CrossRef | 1:CAS:528:DyaL2cXotVWntA%3D%3D&md5=21d9345d6132c9709ded68e0abba1a10CAS | 6365992PubMed | open url image1

Anway, M. D., Folmer, J., Wright, W. W., and Zirkin, B. R. (2003). Isolation of Sertoli cells from adult rat testes: an approach to ex vivo studies of Sertoli cell function. Biol. Reprod. 68, 996–1002.
Isolation of Sertoli cells from adult rat testes: an approach to ex vivo studies of Sertoli cell function.CrossRef | 1:CAS:528:DC%2BD3sXhsFGks7k%3D&md5=3e29831f8f00d8eaeb1229451333953bCAS | 12604653PubMed | open url image1

Baker, J., Hardy, M. P., Zhou, J., Bondy, C., Lupu, F., Bellve, A. R., and Efstratiadis, A. (1996). Effects of an Igf1 gene null mutation on mouse reproduction. Mol. Endocrinol. 10, 903–918.
| 1:CAS:528:DyaK28XktVagtrY%3D&md5=0a85d61a4a4007c004984ecb63cf8b2eCAS | 8813730PubMed | open url image1

Brito, L. F., Barth, A. D., Rawlings, N. C., Wilde, R. E., Crews, D. H., Boisclair, Y. R., Ehrhardt, R. A., and Kastelic, J. P. (2007). Effect of feed restriction during calfhood on serum concentrations of metabolic hormones, gonadotropins, testosterone, and on sexual development in bulls. Reproduction 134, 171–181.
Effect of feed restriction during calfhood on serum concentrations of metabolic hormones, gonadotropins, testosterone, and on sexual development in bulls.CrossRef | 1:CAS:528:DC%2BD2sXpvFGisL8%3D&md5=c27df325221c4100e7ea30990d53e118CAS | 17641099PubMed | open url image1

Butler, A. A., Yakar, S., Gewolb, I. H., Karas, M., Okubo, Y., and LeRoith, D. (1998). Insulin-like growth factor-I receptor signal transduction: at the interface between physiology and cell biology. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 121, 19–26.
Insulin-like growth factor-I receptor signal transduction: at the interface between physiology and cell biology.CrossRef | 1:STN:280:DyaK1M7jvVahug%3D%3D&md5=0a81d533b029be80f95d3fd8fabf5e20CAS | 9972281PubMed | open url image1

Cailleau, J., Vermeire, S., and Verhoeven, G. (1990). Independent control of the production of insulin-like growth factor I and its binding protein by cultured testicular cells. Mol. Cell. Endocrinol. 69, 79–89.
Independent control of the production of insulin-like growth factor I and its binding protein by cultured testicular cells.CrossRef | 1:CAS:528:DyaK3cXhsFams7o%3D&md5=82deba51fa8a383870529ed120fec441CAS | 2157618PubMed | open url image1

Chang, Y. F., Lee-Chang, J. S., Panneerdoss, S., MacLean, J. A., and Rao, M. K. (2011). Isolation of Sertoli, Leydig, and spermatogenic cells from the mouse testis. Biotechniques 51, 341–342, 344.
Isolation of Sertoli, Leydig, and spermatogenic cells from the mouse testis.CrossRef | 1:CAS:528:DC%2BC3MXhs1Siu73E&md5=589c4f83d6c018de7cbf10bca7ccd964CAS | 22054547PubMed | open url image1

Daftary, S. S., and Gore, A. C. (2004). The hypothalamic insulin-like growth factor-1 receptor and its relationship to gonadotropin-releasing hormones neurones during postnatal development. J. Neuroendocrinol. 16, 160–169.
The hypothalamic insulin-like growth factor-1 receptor and its relationship to gonadotropin-releasing hormones neurones during postnatal development.CrossRef | 1:CAS:528:DC%2BD2cXhs1Sls7g%3D&md5=c187be78a1d2d27d8582658b9137bafdCAS | 14764003PubMed | open url image1

Daftary, S. S., and Gore, A. C. (2005). IGF-1 in the brain as a regulator of reproductive neuroendocrine function. Exp. Biol. Med (Maywood). 230, 292–306.
| 1:CAS:528:DC%2BD2MXjvFaqtLY%3D&md5=3923138571356be2f1739104d48b9f76CAS | 15855296PubMed | open url image1

Dance, A., Thundathil, J., Wilde, R., Blondin, P., and Kastelic, J. (2015). Enhanced early-life nutrition promotes hormone production and reproductive development in Holstein bulls. J. Dairy Sci. 98, 987–998.
Enhanced early-life nutrition promotes hormone production and reproductive development in Holstein bulls.CrossRef | 1:CAS:528:DC%2BC2cXitFKnu73P&md5=27012cdeeb2996fb3c97a51ef22f78d5CAS | 25497791PubMed | open url image1

Froment, P., Vigier, M., Negre, D., Fontaine, I., Beghelli, J., Cosset, F. L., Holzenberger, M., and Durand, P. (2007). Inactivation of the IGF-I receptor gene in primary Sertoli cells highlights the autocrine effects of IGF-I. J. Endocrinol. 194, 557–568.
Inactivation of the IGF-I receptor gene in primary Sertoli cells highlights the autocrine effects of IGF-I.CrossRef | 1:CAS:528:DC%2BD2sXhtFKms7jI&md5=d3c4521cade05e4a9fae2761aaa10adbCAS | 17761895PubMed | open url image1

Griffeth, R. J., Bianda, V., and Nef, S. (2014). The emerging role of insulin-like growth factors in testis development and function. Basic Clin. Androl. 24, 12.
The emerging role of insulin-like growth factors in testis development and function.CrossRef | 25780585PubMed | open url image1

Hansson, H. A., Billig, H., and Isgaard, J. (1989). Insulin-like growth factor I in the developing and mature rat testis: immunohistochemical aspects. Biol. Reprod. 40, 1321–1328.
Insulin-like growth factor I in the developing and mature rat testis: immunohistochemical aspects.CrossRef | 1:CAS:528:DyaL1MXlsVOnsb4%3D&md5=ec1b91dc0d63b0019206dc7122dd669bCAS | 2775821PubMed | open url image1

Khan, S. A., Ndjountche, L., Pratchard, L., Spicer, L. J., and Davis, J. S. (2002). Follicle-stimulating hormone amplifies insulin-like growth factor I-mediated activation of AKT/protein kinase B signaling in immature rat Sertoli cells. Endocrinology 143, 2259–2267.
Follicle-stimulating hormone amplifies insulin-like growth factor I-mediated activation of AKT/protein kinase B signaling in immature rat Sertoli cells.CrossRef | 1:CAS:528:DC%2BD38XjvFKjtbw%3D&md5=ddafcef9080e4ce9c74cb7abd408e338CAS | 12021190PubMed | open url image1

Messager, S., Chatzidaki, E. E., Ma, D., Hendrick, A. G., Zahn, D., Dixon, J., Thresher, R. R., Malinge, I., Lomet, D., Carlton, M. B. L., Colledge, W. H., Caraty, A., and Aparicio, S. A. J. R. (2005). Kisspeptin directly stimulates gonadotropin-releasing hormone releases via G protein-coupled receptor 54. Proc. Natl. Acad. Sci. USA 102, 1761–1766.
Kisspeptin directly stimulates gonadotropin-releasing hormone releases via G protein-coupled receptor 54.CrossRef | 1:CAS:528:DC%2BD2MXhs1Klu7Y%3D&md5=5c90653551be5a8dcc7affc2c2e1cbf4CAS | 15665093PubMed | open url image1

Oliveira, P. F., Sousa, M., Barros, A., Moura, T., and Rebelo da Costa, A. (2009). Membrane transporters and cytoplasmatic pH regulation on bovine Sertoli cells. J. Membr. Biol. 227, 49–55.
Membrane transporters and cytoplasmatic pH regulation on bovine Sertoli cells.CrossRef | 1:CAS:528:DC%2BD1MXmtlSh&md5=1638dfab18949c04f0c2e81aa4236b98CAS | 19050954PubMed | open url image1

Orth, J. M., Gunsalus, G. L., and Lamperti, A. A. (1988). Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology 122, 787–794.
Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development.CrossRef | 1:STN:280:DyaL1c7jslWgug%3D%3D&md5=468d1f95fd07c28764e1a4502c85b3aaCAS | 3125042PubMed | open url image1

Pitetti, J. L., Calvel, P., Zimmermann, C., Conne, B., Papaioannou, M. D., Aubry, F., Cederroth, C. R., Urner, F., Fumel, B., Crausaz, M., Docquier, M., Herrera, P. L., Pralong, F., Germond, M., Guillou, F., Jegou, B., and Nef, S. (2013). An essential role for insulin and IGF1 receptors in regulating Sertoli cell proliferation, testis size, and FSH action in mice. Mol. Endocrinol. 27, 814–827.
An essential role for insulin and IGF1 receptors in regulating Sertoli cell proliferation, testis size, and FSH action in mice.CrossRef | 1:CAS:528:DC%2BC3sXnsFSisL4%3D&md5=15407045506f7862c47cf964ab97083aCAS | 23518924PubMed | open url image1

Rawlings, N., Evans, A. C., Chandolia, R. K., and Bagu, E. T. (2008). Sexual maturation in the bull. Reprod. Domest. Anim. 43, 295–301.
Sexual maturation in the bull.CrossRef | 18638138PubMed | open url image1

Salic, A., and Mitchison, T. J. (2008). A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA 105, 2415–2420.
A chemical method for fast and sensitive detection of DNA synthesis in vivo.CrossRef | 1:CAS:528:DC%2BD1cXis1Khtb0%3D&md5=081290e1c7c10304fee65213263eb495CAS | 18272492PubMed | open url image1

Sharpe, R. M. (1994). Regulation of spermatogenesis. In ‘The Physiology of Reproduction, Second Edn’. (Eds E. Knobil and J. D. Neill.) pp. 1363–1434. (Raven Press: New York.)

Sharpe, R. M., McKinnell, C., Kivlin, C., and Fisher, J. S. (2003). Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125, 769–784.
Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood.CrossRef | 1:CAS:528:DC%2BD3sXltFelt7c%3D&md5=10cf4b0261e962d361c84957f26be906CAS | 12773099PubMed | open url image1

Shojaei Saadi, H. A., van Riemsdijk, E., Dance, A. L., Rajamanickam, G. D., Kastelic, J. P., and Thundathil, J. C. (2013). Proteins associated with critical sperm functions and sperm head shape are differentially expressed in morphologically abnormal bovine sperm induced by scrotal insulation. J. Proteomics 82, 64–80.
Proteins associated with critical sperm functions and sperm head shape are differentially expressed in morphologically abnormal bovine sperm induced by scrotal insulation.CrossRef | 1:CAS:528:DC%2BC3sXmslehurs%3D&md5=176e5d66d6e9618a816ee6c5e5a0de9cCAS | 23500133PubMed | open url image1

Tarulli, G. A., Stanton, P. G., and Meachem, S. J. (2012). Is the adult Sertoli cell terminally differentiated? Biol. Reprod. 87, 13.
Is the adult Sertoli cell terminally differentiated?CrossRef | 22492971PubMed | open url image1

Villalpando, I., Lira, E., Medina, G., Garcia-Garcia, E., and Echeverria, O. (2008). Insulin-like growth factor 1 is expressed in mouse developing testis and regulates somatic cell proliferation. Exp. Biol. Med. (Maywood) 233, 419–426.
Insulin-like growth factor 1 is expressed in mouse developing testis and regulates somatic cell proliferation.CrossRef | 1:CAS:528:DC%2BD1cXlsF2hs7c%3D&md5=e8c59cf34047c8d9e5511079385cf70bCAS | 18367630PubMed | open url image1

Wang, G., and Hardy, M. P. (2004). Development of Leydig cells in the insulin-like growth factor-I (igf-I) knockout mouse: effects of igf-I replacement and gonadotropic stimulation. Biol. Reprod. 70, 632–639.
Development of Leydig cells in the insulin-like growth factor-I (igf-I) knockout mouse: effects of igf-I replacement and gonadotropic stimulation.CrossRef | 1:CAS:528:DC%2BD2cXhs1Chs7g%3D&md5=6a342a2c9ae6e5e544df80a83446af69CAS | 14585811PubMed | open url image1

Wolf, F. R., Almquist, J. O., and Hale, E. B. (1965). Prepubertal behavior and pubertal characteristics of beef bulls on high nutrient allowance. J. Anim. Sci. 24, 761–765.
Prepubertal behavior and pubertal characteristics of beef bulls on high nutrient allowance.CrossRef | 1:STN:280:DyaF2M7hvVequw%3D%3D&md5=31edcfa0d1ddf95ececbd3203f2d58a3CAS | 14313741PubMed | open url image1



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