Effects of growth hormone on FSH, insulin and triiodothyronine-mediated estradiol production by granulosa cells from prepubertal gilts in vitro
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1 Effects of growth hormone on FSH, insulin and triiodothyronine-mediated estradiol production by granulosa cells from prepubertal gilts in vitro Rajkumar, K., Kirkwood, R. N. and Thacker, P. A Effects of growth hormone on FSH' insulin and triiodothyronine-mediated estradiol production by granulosa cells from prepubertal gilts in vitro. Can. J. Anim. Sci. 73: '7. Three experiments were performed using porcine granulosa cells from medium-sized follicles (2-4 mm) cultured in serum-free medium at a density of 2 x l0' viable cells per well. Cells were cultured in the presence of combinations of FSH, insulin, growth hormone (GH) and triiodothyronine (T3), and subsequent estradiol (E) production was monitored. In the presence of insulin, a dose-dependent E, production response to FSH was observed (exp. 1). However, in all experiments, E, production was reduced (P < 0.05) by the inclusion of GH in the media. The inclusion of T, augmented the E2 response to insulin, an effect attenuated by GH. We conclude that GH, at the dose employed, is inhibitory to E2 production in granulosa cells of medium-sized ovarian follicies. Key words: Granulosa cells, growth hormone, estradiol Rajkumar, K., Kirkwood, R. N. et Thacker, P. A Effets de I'hormone de croissance sur la production in vitro d'oestradiol en pr6sence de FSH, d'insuline et de triiodothyronine par les cellules de la granulosa de cochettes pr6pubdres. Can. J. Anim. Sci. 73: Trois exp6riences ont 6t6 r6alis6es sur les cellules de la granulosa (porcine) de follicules de taille moyenne (2-4 mm) mis en culture dans un milieu sans s6rum )r la densit6 de 2 x 10o cellules viables par puits. La mise en culture se faisait en pr6sence de FSH, d'insuline, d'hormone de croissance (GH) et de triiodothyronine (Tr) en diverses combinaisons et on suivait ensuite la production d'oestradiol (E ) r6sultante. En pr6sence d'insuline, on observait une production de E2 li6e d la dose de FSH (exp6rience 1). Toutefois, dans toutes les exp6riences, la production de E, 6tait r6duite (P < 0,05) par la pr6sence de GH dans le milieu de culture. L'inclusion de T3 amplifiait la r6ponse de E, )r I'insuline mais I'effet 6tait att6nu6 par la pr6sence de GH. Les auteurs concluent qu'd la dose utilis6e, GH avait un effet inhibiteur sur la production de E2 par les cellules de la granulosa de follicules ovariens de taille moyenne. Mots cl6s: Cellules de la granulosa, hormone de croissance, oestradiol Several studies have investigated the in vitro steroidogenic response of follicular granulosa cells to growth hormone (GH). Following in vivo GH treatment of prepubertal gilts, the subsequent in vitro steroidogenic responses of granulosa cells were found to be variable. In one study, gonadotrophin-stimulated progesterone secretion was reduced (Bryan et al. 1989), while in a further study from the same laboratory, steroidogenesis was shown to be enhanced (Bryan et al. 1991). Studies on the effect of in vitro GH on granulosa-cell steroidogenesis have also provided conflicting Can. J. Anim. Sci.73: (June 1993) 443 results. Hsu and Hammond (1987) demonstrated that GH enhanced progesterone production from porcine granulosa cells. However, in the absence of FSH, insulin or other growth factors, GH was without effect (Maruo et al. 1988). When a positive effect of GH has been observed, the effect was attributed to a GHmediated increase in insulin-like growth factor I 0GF-I). However, recent in vitro studies have shown that GH-stimulated estrogen production by human granulosa cells (Mason et al. 1990) and progesterone production by porcine granulosa cells (R.N. Kirkwood, unpubl. data) appeared to be independent of concentrations of IGF-I in the media. Thus,
2 444 CANADIAN JOURNAL OF ANIMAL SCIENCE a direct effect of GH on granulosa-cell function cannot be discounted. Studies investigating the relationship between GH and granulosa-cell steroidogenesis have observed stimulatory effects of GH on both gonadotropin-mediated (Hsu and Hammond 1987) and insulin-mediated progesterone production. Granulosa cells are also the major source of estradiol during preovulatory follicular development. The secretion of estradiol by granulosa cells is dependent on both aromatase activity and the availability of an aromatizable substrate. However, the observed occurrence ofanestrus in gilts following in vivo GH administration (for review see Kirkwood and Thacker 1991) suggests that the effects of GH on ovarian secretion of progesterone and estradiol may be different. Following in vivo administration of GH, there is an increase in serum concentrations of triiodothyronine (T3) and insulin (Kirkwood and Thacker 1991), both of which may impact on fertility. The relationship of these latter endocrine changes to GH-mediated anestrus is not known. Therefore, the present studies were undertaken to examine the effect of GH, T3 and insulin on FSH-induced aromatase activity (as measured by the ability of cells to metabolize androstenedione to estradiol) in porcine granulosa cells. Three experiments were performed using granulosa cells collected by fine-needle aspiration of medium-sized follicles (2-4 mm\ derived from prepubertal gilts at slaughter. The cells were recovered by centrifugation (250 x g) and cultured, in replicates of six wells per treatment, in serum-free medium at a density of 2 x lob viable cells per well. To facilitate cell adhesion. 200 ul of undiluted fetal bovine serum (FBS) lgibco. Burlington, Ontario) was added to the culture wells and incubated for 2 h at 3J ' C. Prior to seeding with granulosa cells, the FBS was removed by washing twice with sterile, serum-free culture medium. The culture medium consisted of Eagle's minimum essential medium (MEM) (Gibco) buffered with bicarbonate and HEPES (ph 7.a) containing penicillin (60 pg ml '). streptomyc.in (100 pg ml-') and fungizone (l pg ml-'). For exp. 1, cells were cultured in the presence of either bovine insulin (Sigma, St. Louis. Missouri) at 1.0 pg ml -r or bovine insulin plus porcine GH (USDA pgh-b-1) at 100 ng ml-r. To these cultures, FSH (USDA pfsh-b-1) was_added at either zero, 20,60 or 200 ng ml-'. Hormone concentrations were chosen on the basis of previously published protocols (e.g. Hsu and Hammond 1987). Hormone-enriched media were replaced at24,48 and-'72 h. Also at72h, androstenedione ( l0 - ' M) {Sigma) was added to provide a substrate for estradiol production. In this and subsequent experiments, the cultures were terminated at 96 h and the media from '72 to 96 h of culture were recovered and stored at -20"C until required for the determination of estradiol. The cells were collected at 96 h for the determination of protein content (Lowry et al. 1951). For exp. 2, granulosa cells were cultured as above, except that the culture medium contained either insulin (0.lpg ml-r) or insulin plus FSH (200 ng ml--t) from the time of plating. Additionally, GH was included at 0 or 100 ng ml-'. For exp. 3, granulosa cells were cultured with FSH at 200 ng ml I and insulin at I or I.0 pg ml -r. Additionally. GH (100 ng ml-') or Tj (5 ng ml-')or both GH and T3 were included. Media concentrations of estradiol were determined by an established radioimmunoassay (Joseph eial. 1992). Assay sensitivity and intra- and interassay_ coefficients of variation were 3.1 pg ml-', 5.8% and 9.0%, respectively. The cellular compartments were assayed for protein content using the method of Lowry et al. (1952). Treatment effects on estradiol production were examined by analysis of variance using the number cruncher statistical system (NCSS 1987; N.J. Hintze, Kaysville, Utah). Differences between individual treatment means within experiment were investigated using Tukey's w procedure. The results of exp. 1 clearly indicate that when cultured in the presence of insulin, estradiol production from porcine granulosa cells was increased (P < 0.05) in a dose-
3 RAJKUMAR ET AL. STEROIDOGENESIS IN PORCINE GRANULOSA CELLS o E 15 i- U ; 91s -9 : U o s - l) olo UJ 5 Insulin Insulin plus FSH -l FSH (n0 ml ) Fig. 1. Influence of GH on esrradiol producrion il::,:,r'unu,oru cetls in response to various levels of FSH (top; exp. l) or insulin with or without FSH (middle; exp. 2). The lower panel (exp. 3) shows the influence of pgh, T,, and pgh+t3 on estradiol production. Standard errors ranged from 0.2to2.3 ng mg-r protein. Within each experiment, means with different letters differ (P < 0.05). Means are compared both within treatment (a-c) and between treatments (w-y).
4 446 CANADIAN JOURNAL OF ANIMAL SCIENCE dependent manner in response to FSH (Fig. 1, top). It was further noted that the response to FSH was attenuated with the additional presence of GH. The results from exp. 2 demonstrate considerable estradiol production from insulinstimulated granulosa cells and further substantiate that FSH augments (P < 0.05) estradiol production in the presence of insulin (Fig. 1, middle). Furthermore, these data also indicated an inhibitory influence of GH on estradiol production, although differences were not statistically significant. In exp. 3, estradiol production in response to FSH was minimal in the absence of insulin (Fig. 1, bottom). With increasing levels of insulin in the media, FSH-induced estradiol production was increased (P < 0.05). This implies that insulin enhanced FSH-induced aromatase activity in granulosa cells. The addition of GH to cultures inhibited (P < 0.05) FSH and insulin-mediated estradiol production (Fig. 1, bottom). The greatest estradiol secretory response was observed from cells cultured with the highest insulin level and T: (P < 0.05). A stimulatory effect of T3 on granulosa-cell progesterone production from porcine granulosa cells has also been observed (Kirkwood et al. 1992). However, while previous data from this laboratory have demonstrated a stimulatory effect of co-culnrre with GH and T3 on progesterone production from porcine granulosa cells, the present data indicate that GH attenuated (P < 0.05) the stimulatory effect of T3. At the highest insulin level, the estradiol production in cultures with GH plus T3 was not different from that in control cultures. These data further support the suggestion that GH is inhibitory to estradiol production in granulosa cells. We have previously observed a high incidence of anestrus following GH administration to gilts in vivo and that GH injections were associated with increased serum concentrations of T3 and insulin (Kirkwood and Thacker 1991). However, the present results indicate that elevated Tr and insulin are not involved in the suppression of aromatase activity and, as such, are unlikely to be involved in the mediation of GH-associated anestrus. The present data demonstrate an inhibitory effect of GH on FSH-induced estradiol secretion. This is in contrast to the effect of GH on estradiol production by human granulosa cells observed by Mason et al. (1990). While an effect of species of origin cannot be discounted, the difference in response may be due to Mason et al.'s use of cells from different sized follicles (5-7 mm) and (or) their use of a lower dose of GH (10 ng ml - r). An effect of follicular size (and thus degree of maturation) on in vitro responses is consistent with the in vivo observation that a high dose of exogenous GH administered daily during the late-luteal-early-follicular phase of the estrous cycle induced anestrus in 5O% of gilts but was without effect when treafinent was initiated from the mid-follicular phase (Kirkwood and Thacker 1991). Although speculative, it is possible that the early administration of GH inhibited follicular aromatase activity and subsequent estradiol production. Since the combined effect of FSH and estradiol is the induction of receptors for LH, a reduced aromatase activity may be involved in the observed GH-mediated induction of anestrus in cyclic gilts and the occurrence of cystic ovaries in GH-treated gilts following PMSG injection (Kirkwood and Thacker 1991). From the present results, we conclude that GH at the dose employed has an inhibitory effect on estradiol production from granulosa cells of medium-sized ovarian follicles. However, further research is required to define the influence of hormone dose and stage of follicular development on the response obtained. We gratefully acknowledge the expert technical assistance of Ms. Dawn Caird. We wish to thank the National Institute of Diabetes and Digestive, and Kidney Diseases and National Hormone and Pituitary Program, University of Maryland School of Medicine, for the generous gift of porcine growth hormone and follicle-stimulating hormone. Financial support for these studies was provided by the Natural Sciences and Engineering Research Council of Canada and the Province of Saskatchewan Agriculture Development Fund.
5 RAJKUMAR ET AL. - STEROIDOGENESIS IN PORCINE GRANULOSA CELLS 447 Bryan, K. A., Hammond, J. M. Canning, S.' Mondschein, J., Carbaugh, D. E., Clark' A. M. and Hagen, D. R Reproductive and growth responses of gilts to exogenous porcine pituitary growth hormone. J. Anim. Sci. 67: Bryan, K. A., Clark, A. M., Hammond, J. M. and Hagen, D. R Effect of constant versus adjusted dose of exogenous porcine growth hormone (pgh) on growth and reproductive characterisrics of gilts. J. Anim. sci. 69: Hsu, J. C. and Hammond, J. M. 1987' Concomitant effects of growth hormone on secretion of insulin-like growth factor I and progesterone by cultured porcine granulosa cells. Endocrinology l2l: Joseph, I. B. J. K.,Currie,W. D.andRawlings' N. C Luteinizing hormone and follicle stimulating hormone secretion in ovariectomized ewes: effects oftime post ovariectomy, season and oestradiol. J. Reprod. Fertil. 94: Kirkwood, R. N. and Thacker, P. A Porcine somatotropin - effects on the breeding herd. C.A.B. Pig News and Information12: 4'7-51. Kirkwood, R. N., Thacker, P. A. and Rajkumar, K Effects of growth hormone and triiodothyronine on insulin-induced progesterone production by granulosa cells from prepubertal silts. Can. J. Anim. Sci. 72: Lowry, O. H., Rosebrough, N. J., Farr' A. L. and Randall, R. J Protein measurement with folin phenol reagent. J. Biol. Chem. 193: Maruo, T., Hayashi, M., Matsuo, H.' Ueda, Y.' Morikawa, H. and Mochizuki, M Comparison of the facilitatory roles of insulin and insulin-like growth factor I in the functional differentiation of granulosa cells: in vitro studies with the porcine model. Acta Endocrinol. (Copenhagen) 117: Mason, H. D., Martikainen, H., Beard, B. W., Anyaoku, V. and Franks, S Direct gonadotrophic effect of growth hormone on oestradiol production by human granulosa cells in vitro. J. Endocrinol. 126: Rl-R4. K. Rajkumarl, R. N. Kirkwood2 and P- A. Thacker2 Departments of I Obstetrics and Gynecology and 2Animal and Poultry Science, [Jniversiry of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N 0W0. Received 16 June 1992, accepted 18 Jan
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