Effects of estradiol on bovine thecal cell function in vitro: Dependence on insulin and gonadotropins

Journal of Dairy Science

Volumn 88, Issue 7, 2005, Pages 2412-2421

  Spicer, L J ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Estradiol; Insulin like growth factor; Steroidogenesis; Thecal cell

Indexed keywords

BOS TAURUS; BOVINAE;

EID: 22944481160     PISSN: 00220302     EISSN: None     Source Type: Journal    
DOI: 10.3168/jds.S0022-0302(05)72919-2     Document Type: Article

References (70)

1. Badinga, L., M. A. Driancourt, J. D. Savio, D. Wolfenson, M. Drost, R. L. de la Sota, and W. W. Thatcher. 1992. Endocrine and ovarian responses associated with the first-wave dominant follicle in cattle. Biol. Reprod. 47:871-883.
2. Bao, B., N. Kumar, R. M. Karp, H. A. Garverick, and K. Sundaram. 2000. Estrogen receptor-β expression in relation to the expression of luteinizing hormone receptor and cytochrome P450 enzymes in rat ovarian follicles. Biol. Reprod. 63:1747-1755.
3. Beam, S. W., and W. R. Butler. 1998. Energy balance, metabolic hormones, and early postpartum follicular development in dairy cows fed prilled lipid. J. Dairy Sci. 81:121-131.
4. Berisha, B., M. W. Pfaffl, and D. Schams. 2002. Expression of estrogen and progesterone receptors in the bovine ovary during estrous cycle and pregnancy. Endocrine 17:207-214.
5. Brandenberger, A. W., M. K. Tee, and R. B. Jaffe. 1998. Estrogen receptor alpha (ER-α) and beta (ER-β) mRNAs in normal ovary, ovarian serous cystadenocarcinoma and ovarian cancer cell lines: Down-regulation of ER-β in neoplastic tissues. J. Clin. Endocrinol. Metab. 83:1025-1028.
6. Buhi, W. C. 2002. Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123:355-362.
7. Byers, M., G. G. Kuiper, J. A. Gustafsson, and O. K. Park-Sarge. 1997. Estrogen receptor-β mRNA expression in rat ovary: Down-regulation by gonadotropins. Mol. Endocrinol. 11:172-182.
8. Couse, J. F., D. O. Bunch, J. Lindzey, D. W. Schomberg, and K. S. Korach. 1999. Prevention of the polycystic ovarian phenotype and characterization of ovulatory capacity in the estrogen receptor-α knockout mouse. Endocrinology 140:5855-5865.
9. Cushman, R. A., J. C. DeSouza, V. S. Hedgpeth, and J. H. Britt. 2001a. Effect of long-term treatment with recombinant bovine somatotropin and estradiol on hormone concentrations and ovulatory response of superovulated cattle. Theriogenology 55:1533-1547.
10. Cushman, R. A., J. C. DeSouza, V. S. Hedgpeth, and J. H. Britt. 2001b. Alteration of activation, growth, and atresia of bovine preantral follicles by long-term treatment of cows with estradiol and recombinant bovine somatotropin. Biol. Reprod. 65:581-586.
11. Fitzpatrick, S. L., J. M. Funkhouser, D. M. Sindoni, P. E. Stevis, D. C. Deecher, A. R. Bapat, I. Merchenthaler, and D. E. Frail. 1999. Expression of estrogen receptor-β protein in rodent ovary. Endocrinology 140:2581-2591.
12. Fortune, J. E. 1986. Bovine theca and granulosa cells interact to promote androgen production. Biol. Reprod. 35:292-299.
13. Fortune, J. E., and W. Hansel. 1979a. The effects of 17β-estradiol on progesterone secretion by bovine theca and granulosa cells. Endocrinology 104:1834-1838.
14. Fortune, J. E., and W. Hansel. 1979b. Modulation of thecal progesterone secretion by estradiol-17β. Adv. Exp. Med. Biol. 112:203-208.
15. Gilling-Smith, C., D. S. Willis, and S. Franks. 1997. Oestradiol feedback stimulation of androgen biosynthesis by human thecal cells. Hum. Reprod. 12:1621-1628.
16. Hulshof, S. C. J., J. R. Figueiredo, J. F. Beckers, M. M. Bevers, J. A. van der Donk, and R. van den Hurk. 1995. Effects of fetal bovine serum, FSH and 17β-estradiol on the culture of bovine preantral follicles. Theriogenology 44:217-226.
17. Hunter, M. G., and D. T. Armstrong. 1987. Oestrogens inhibit steroid production by dispersed porcine thecal cells. Mol. Cell. Endocrinol. 50:165-170.
18. Jakimiuk, A. J., S. R. Weitsman, H.-W. Yen, M. Bogusiewicz, and D. A. Magoffin. 2002. Estrogen receptor α and β expression in theca and granulosa cells from women with polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 87:5532-5538.
19. Johnson, D. C., and L. H. Crane. 1995. Inhibitory and stimulatory effect of oestrogens upon ovarian 17α-hydroxylase/C17, 20-lyase in immature hypophysectomized rats treated with gonadotropin. J. Endocrinol. 145:59-67.
20. Lacroix, E., W. Eechaute, and I. Leusen. 1974. The biosynthesis of estrogens by cow follicles. Steroids 23:337-356.
21. Langhout, D. J., L. J. Spicer, and R. D. Geisert. 1991. Development of a culture system for bovine granulosa cells: Effects of growth hormone, estradiol and gonadotropins on cell proliferation, steroidogenesis and protein synthesis. J. Anim. Sci. 69:3321-3334.
22. Liu, Y. X., and A. J. Hsueh. 1986. Synergism between granulosa and theca-interstitial cells in estrogen biosynthesis by gonadotropin-treated rat ovaries: Studies on the two-cell, two-gonadotropin hypothesis using steroid antisera. Biol. Reprod. 35:27-36.
23. Magoffin, D. A., and G. F. Erickson. 1981. Mechanism by which 17β-estradiol inhibits ovarian androgen production in the rat. Endocrinology 108:962-969.
24. Magoffin, D. A., and G. F. Erickson. 1982. Direct inhibitory effect of estrogen on LH-stimulated androgen synthesis by ovarian cells cultured in defined medium. Mol. Cell. Endocrinol. 28:81-89.
25. Manikkam, M., B. Bao, C. S. Rosenfeld, X. Yuan, B. E. Salfen, M. D. Calder, R. S. Youngquist, D. H. Keisler, D. B. Lubahn, and H. A. Garverick. 2001. Expression of the bovine oestrogen receptor-β (bERβ) messenger ribonucleic acid (mRNA) during the first ovarian follicular wave and lack of change in the expression of bERβ mRNA of second wave follicles after LH infusion into cows. Anim. Reprod. Sci. 67:159-169.
26. Morley, P., M. W. Khalil, F. R. Calaresu, and D. T. Armstrong. 1989. Catecholestrogens inhibit basal and luteinizing hormone-stimulated androgen production by porcine thecal cells. Biol. Reprod. 41:446-453.
27. Orikasa, C., and Y. Sakuma. 2003. Possible involvement of preoptic estrogen receptor β positive cells in luteinzing hormone surge in the rat. Domest. Anim. Endocrinol. 25:83-92.
28. Ott, L. 1977. Pages 384-388 in An Introduction to Statistical Methods and Data Analysis. Duxbury Press, North Scituate, MA.
29. Pelletier, G., C. Labrie, and F. Labrie. 2000. Localization of oestrogen receptor α, oestrogen receptor β and androgen receptors in the rat reproductive organs. J. Endocrinol. 165:359-370.
30. 3H]-thymidine incorporation by porcine granulosa and theca cells. Anim. Reprod. Sci. 47:229-236.
31. Richards, J. S. 1975. Estradiol receptor content in rat granulosa cells during follicular development: Modification by estradiol and gonadotropins. Endocrinology 97:1174-1184.
32. Richards, J. S., J. J. Ireland, M. C. Rao, G. A. Bernath, A. R. Midgley, Jr., and L. E. Reichert, Jr. 1976. Ovarian follicular development in the rat: Hormone receptor regulation by estradiol, follicle stimulating hormone and luteinizing hormone. Endocrinology 99:1562-1570.
33. Roberts, A. J., and M. K. Skinner. 1990a. Estrogen regulation of thecal cell steroidogenesis and differentiation: Thecal cell-granulosa cell interactions. Endocrinology 127:2918-2929.
34. Roberts, A. J., and M. K. Skinner. 1990b. Mesenchymal-epithelial cell interactions in the ovary: Estrogen-induced theca cell steroidogenesis. Mol. Cell. Endocrinol. 72:R1-R5.
35. Rosenfeld, C. S., X. Yuan, M. Manikkam, M. D. Calder, H. A. Garverick, and D. B. Lubahn. 1999. Cloning, sequencing, and localization of bovine estrogen receptor-β within the ovarian follicle. Biol. Reprod. 60:691-697.
36. Sar, M., and F. Welsch. 1999. Differential expression of estrogen receptor-β and estrogen receptor-α in the rat ovary. Endocrinology 140:963-971.
37. SAS Institute. 1999. The SAS system for Windows: Version 8. SAS Institute, Inc., Cary, NC.
38. Saunders, P. T. K., M. R. Millar, K. Williams, S. Macpherson, D. Harkiss, R. A. Anderson, B. Orr, N. P. Groome, G. Scobie, and H. M. Fraser. 2000. Differential expression of estrogen receptor-α and β and androgen receptor in the ovaries of marmosets and humans. Biol. Reprod. 63:1098-1105.
39. Sharma, S. C., J. W. Clemens, M. D. Pisarska, and J. S. Richards. 1999. Expression and function of estrogen receptor subtypes in granulosa cells: Regulation by estradiol and forskolin. Endocrinology 140:4320-4334.
40. Slomczynska, M., and J. Wozniak. 2001. Differential distribution of estrogen receptor-β and estrogen receptor-α in the porcine ovary. Exp. Clin. Endocrinol. Diabetes 109:238-244.
41. Spicer, L. J. 2001. Receptors for insulin-like growth factor-I and tumor necrosis factor-α are hormonally regulated in bovine granulosa and thecal cells. Anim. Reprod. Sci. 67:45-58.
42. Spicer, L. J., J. Alonso, and C. S. Chamberlain. 2001a. Effects of thyroid hormones on bovine granulosa and thecal cell function in vitro: Dependence on insulin and gonadotropins. J. Dairy Sci. 84:1069-1076.
43. Spicer, L. J., E. Alpizar, and R. K. Vernon. 1994. Insulin-like growth factor-I receptors in ovarian granulosa cells: Effect of follicle size and hormones. Mol. Cell. Endocrinol. 102:69-76.
44. Spicer, L. J., and C. S. Chamberlain. 1998. Influence of cortisol on insulin and insulin-like growth factor I (IGF-I)-induced steroid production and on IGF-I receptors in cultured bovine granulosa cells and thecal cells. Endocrine 9:153-161.
45. Spicer, L. J., C. S. Chamberlain, and G. L. Morgan. 2001b. Proteolysis of insulin-like growth factor binding proteins during preovulatory follicular development in cattle. Domest. Anim. Endocrinol. 21:1-15.
46. 125I-labeled gonadotropins to granulosa and thecal cells, and concentrations of steroids in serum and various sized ovarian follicles. J. Anim. Sci. 62:742-750.
47. 125I-labeled gonadotropins to granulosa and theca, and concentrations of steroids in serum and ovarian follicles during postpartum anovulation in suckled beef cows. J. Anim. Sci. 62:1324-1331.
48. Spicer, L. J., and S. E. Echternkamp. 1986. Ovarian follicular growth, function and turnover in cattle: A review. J. Anim. Sci. 62:428-451.
49. Spicer, L. J., T. D. Hamilton, and B. E. Reefer. 1996. Insulin-like growth factor I enhancement of steroidogenesis by bovine granulosa cells and thecal cells: Dependence on de novo cholesterol synthesis. J. Endocrinol. 151:365-373.
50. Spicer, L. J., and J. M. Hammond. 1987. Catecholestrogens stimulate progestin secretion by cultured porcine granulosa cells. Mol. Cell. Endocrinol. 50:139-147.
51. Spicer, L. J., and J. M. Hammond. 1989. Catecholestrogens inhibit proliferation and DNA synthesis of porcine granulosa cells in vitro: Comparison with estradiol, 5α-dihydrotestosterone, gonadotropins and catecholamines. Mol. Cell. Endocrinol. 64:119-126.
52. Spicer, L. J., P. Matton, S. E. Echternkamp, E. M. Convey, and H. A. Tucker. 1987. Relationships between histological signs of atresia, steroids in follicular fluid, and gonadotropin binding in individual bovine antral follicles during postpartum anovulation. Biol. Reprod. 36:890-898.
53. Spicer, L. J., and R. E. Stewart. 1996a. Interaction among bovine somatotropin, insulin and gonadotropins on steroid production by bovine granulosa and thecal cells. J. Dairy Sci. 79:813-821.
54. Spicer, L. J., and R. E. Stewart. 1996b. Interactions among basic fibroblast growth factor, epidermal growth factor, insulin, and insulin-like growth factor-I (IGF-I) on cell numbers and steroidogenesis of bovine thecal cells: Role of IGF-I receptors. Biol. Reprod. 54:255-263.
55. Stewart, R. E., L. J. Spicer, T. D. Hamilton, and B. Keefer. 1995. Effect of insulin-like growth factor-I and insulin on proliferation and on luteinizing hormone-induced-steroidogenesis of bovine theca cells: Involvement of glucose and receptors for insulin-like growth factor I and luteinizing hormone. J. Anim. Sci. 73:3719-3731.
56. Stewart, R. E., L. J. Spicer, T. D. Hamilton, B. E. Reefer, L. J. Dawson, G. L. Morgan, and S. E. Echternkamp. 1996. Levels of insulin-like growth factor (IGF) binding proteins, luteinizing hormone and IGF-I receptors, and steroids in dominant follicles during the first follicular wave in cattle exhibiting regular estrous cycles. Endocrinology 137:2842-2850.
57. Tonetta, S. A., R. S. DeVinna, and G. S. diZerega. 1986. Modulation of porcine thecal cell aromatase activity by human chorionic gonadotropin, progesterone, estradiol-17 β, and dihydrotestosterone. Biol. Reprod. 35:785-791.
58. Tonetta, S. A., L. J. Spicer, and J. J. Ireland. 1985. CI628 inhibits follicle-stimulating hormone (FSH)-induced increases in FSH receptors of the rat ovary: Requirement of estradiol for FSH action. Endocrinology 116:715-722.
59. Tsang, B. K., P. C. Leung, and D. T. Armstrong. 1979. Inhibition by estradiol-17 β of porcine thecal androgen production in vitro. Mol. Cell. Endocrinol. 14:131-139.
60. Van Den Broeck, W., M. Coryn, P. Simoens, and H. Lauwers. 2002. Cell-specific distribution of oestrogen receptor-α in the bovine ovary. Reprod. Domst. Anim. 37:291-293.
61. Veldhuis, J. D. 1985. Bipotential actions of estrogen on progesterone biosynthesis by ovarian cells. II. Relation of estradiol's stimulatory actions to cholesterol and progestin metabolism in cultured swine granulosa cells. Endocrinology 117:1076-1083.
62. Veldhuis, J. D., J. T. Gwynne, J. F. Strauss, III, and L. M. Demers. 1984. Role of estradiol as a biological amplifier of gonadotropin action in the ovary: In vitro studies using swine granulosa cells and homologous lipoproteins. Endocrinology 114:2312-2322.
63. Veldhuis, J. D., P. A. Klase, and J. M. Hammond. 1981. Direct actions of 17 β-estradiol on progesterone production by highly differentiated porcine granulosa cells in vitro. II. Regulatory interactions of estradiol with luteinizing hormone and cyclic nucleotides. Endocrinology 109:433-442.
64. Veldhuis, J. D., P. A. Klase, J. F. Strauss, III, and J. M. Hammond. 1982. The role of estradiol as a biological amplifier of the actions of follicle-stimulating hormone: In vitro studies in swine granulosa cells. Endocrinology 111:144-151.
65. Veldhuis, J. D., R. J. Rodgers, and R. W. Furlanetto. 1986. Synergistic actions of estradiol and the insulin-like growth factor somatomedin-C on swine ovarian (granulosa) cells. Endocrinology 119:530-538.
66. Voge, J. L., C. A. Santiago, P. Y. Aad, D. W. Goad, J. R. Malayer, and L. J. Spicer. 2004. Quantification of insulin-like growth factor binding protein mRNA using real-time PCR in bovine granulosa and theca cells: Effect of estradiol, insulin, and gonadotropins. Domest. Anim. Endocrinol. 26:241-258.
67. Wang, H., H. Eriksson, and L. Sahlin. 2000. Estrogen receptors α and β in the female reproductive tract of the rat during the estrous cycle. Biol. Reprod. 63:1331-1340.
68. Wilson, S. J., R. S. Marion, J. N. Spain, D. E. Spiers, D. H. Keisler, and M. C. Lucy. 1998. Effects of controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows. J. Dairy Sci. 81:2124-2131.
69. Wolfenson, D., B. J. Lew, W. W. Thatcher, Y. Graber, and R. Meidan. 1997. Seasonal and acute heat stress effects on steroid production by dominant follicles in cows. Anim. Reprod. Sci. 47:9-19.
70. Wrathall, J. H. M., and P. G. Knight. 1995. Effects of inhibin-related peptides and oestradiol on androstenedione and progesterone secretion by bovine theca cells in vitro. J. Endocrinol. 145:491-500.