Hormonal Interrelationships Between Hypothalamus, Pituitary and Testis of Rams and Bulls
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1 University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Publications from USDA-ARS / UNL Faculty USDA Agricultural Research Service --Lincoln, Nebraska Hormonal Interrelationships Between Hypothalamus, Pituitary and Testis of Rams and Bulls Bruce D. Schanbacher USDA-ARS Follow this and additional works at: Part of the Agricultural Science Commons Schanbacher, Bruce D., "Hormonal Interrelationships Between Hypothalamus, Pituitary and Testis of Rams and Bulls" (1982). Publications from USDA-ARS / UNL Faculty. Paper This Article is brought to you for free and open access by the USDA Agricultural Research Service --Lincoln, Nebraska at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Publications from USDA-ARS / UNL Faculty by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln.
2 Journal of Animal Science 55 (1982), pp Hormonal Interrelationships Between Hypothalamus, Pituitary and Testis of Rams and Bulls Bruce D. Schanbacher 1 US Department of Agriculture 2, Clay Center, NE Summary This mini-review aims to summarize some of our recent findings relating to testicular function and feedback control of the hypothalamicpituitary axis by testicular steroids in rams and bulls. Testosterone secretion in intact males is not tonic, but is characterized by episodic pulses. This pattern of secretion is dictated by inputs of the central nervous system via secretions of the hypothalamus (luteinizing hormone-releasing hormone; LHRH) and anterior pituitary (luteinizing hormone; LH). A temporal relationship exists between concentrations of LH and testosterone in serum and evidence is presented that strongly suggests that their episodic secretion is dependent on discrete episodes of LHRH discharge from the hypothalamus. Based on data from experiments with rams and bulls, I suggest that acutely castrated males (but not chronic castrates) remain susceptible to the negative feedback effects of testosterone, i.e., LH concentrations remain suppressed in serum of animals given testosterone replacement therapy immediately following castration. Estradiol-17j3, on the other hand, abolishes pulsatile LH release and suppresses mean LH concentrations in both acute and chronic castrates. Therefore, testosterone feedback on LH secretion may, in part, involve extragonadal conversion to estradiol-17j3 to block pulsatile LHRH release. The potent inhibitory effects of estradiol on LH secretion provide an experimental probe for future investigations relating to mechanisms controlling male reproduction. (Key Words; Hypothalamus, Pituitary, Testicular Steroids, Negative Feedback.) 'The author acknowledges the cooperation of the Nebraska Agr. Exp. Sta., Univ. of Nebraska, Lincoln, and the assistance of Michael J. D'Occhio, James E. Kinder and Cindy Rainbolt in obtaining some of the original data cited. Appreciation is extended to Kathy Leising for typing the manuscript. 2 Roman L. Hruska U.S. Meat Animal Research Center, Agr. Res. Ser. Introduction Despite the need for efficient reproduction by males and the important contribution males make to propagation of the species, limited information has been accumulated on the basic physiological mechanisms that regulate reproductive processes in males. This is true for domestic species, particularly rams and bulls. Livestock production contributes substantially to the economic stability of agriculture in this country; therefore, a better understanding of those factors contributing to the reproductive success or failure in these species is warranted. A number of reproductive characteristics are quantifiable in males, however, it seems that the testes should be of paramount importance. Two major functions of the testis include androgen biosynthesis by the interstitial cells and sperm production within the seminiferous tubules. Although these two functions are segregated anatomically, intercellular communication exists between them. Recent reviews have been prepared on quantitiative aspects of spermatogenesis (Amann, 1981) and regulation of the hypothalamic-pituitary seminiferous tubule axis by inhibin (Setchell et al, 1977). Therefore, this paper will review our current understanding of testosterone secretion and the hypothalamic-pituitary-leydig cell axis in rams and bulls. Hypothalamic-Pituitary-Gonadal Axis The anterior pituitary through its secretion of the gonadotropins, luteinizing hormone (LH) and follicle stimulating hormone (FSH) participate in regulation of testicular function. The anterior pituitary, itself, is regulated by inputs from the central nervous system, which are coordinated via the hypothalamic secretion of luteinizing hormone releasing hormone (LHRH; also referred to as GnRH). The interrelationships of hypothalamus, pituitary and testis are schematically presented in figure 1. Testicular steroidogenesis depends on con- 56
3 ENDOCRINOLOGY AND REGULATION OF TESTICULAR FUNCTION 57 tinuous support from the pituitary in the form of LH. This gonadotropin binds to specific receptors on the plasma membrane of Leydig cells to activate adenyl cyclase. This enzyme catalyzes the conversion of ATP to camp, which serves as a second messenger to activate a cytoplasmic protein kinease that is responsible for the conversion of cholesterol to sex steroids, primarily testosterone (Neaves, 1975). The remainder of this report will deal with the interrelationships between inputs of the hypothalamus (i.e., LHRH), LH secretion and feedback control of the hypothalamic-pituitary axis by testicular steroids. Hypothalamic Control of Testosterone Secretion Testosterone secretion in intact males is not tonic, but is characterized by episodic pulses. This pattern of secretion varies from one animal to the next and is probably a function of age, reproductive status, health, external environment and other unidentified factors (Schanbacher and Ford, 1977; Lincoln, 1978; Lacroix and Pelletier, 1979a,b; Schanbacher, 1980a). Diurnal rhythms in serum testosterone are not evident in rams or bulls (Falvo et al., 1975). Several investigators have reported a temporal relationship between secretory episodes of LH and testosterone with a lag period of approximately 60 min between peak concentrations (Katongole et al., 1971, 1974;Sanford et al., 1974; Schanbacher and Ford, 1976; Lincoln et al., 1977; Schams et al., 1978; D'Occhio et al., 1982b). The ability of iv injections of either LH or LHRH to induce normal surges of testosterone in serum (Thibier, 1976; Schanbacher and Echternkamp, 1978; Schanbacher, 1979a, 1980b) has provided supplementary evidence that pulsatile testosterone secretion is the result of a pulsatile pattern of LHRH secretion from the hypothalamus. Further evidence for this conclusion is illustrated in figure 2, wherein striking similarity exists for the naturally occurring LH-testosterone episode observed in an intact bull (figure 2A) and the LHtestosterone episodes that have been induced by an injection of synthetic LHRH (figure 2B). Based on these data I suggest that an intermittent pattern of LH secretion is dictated by a similar pattern of LHRH secretion by the hypothalamus. Indeed, LHRH concentrations in blood taken from pituitary portal vessels of rhesus monkeys (Carmel et al., 1976) and rats Figure 1. Hypothalamic-pituitary control of testicular function. Gonadotropin releasing hormone (GnRH) from the hypothalamus mediates pituitary release of LH and FSH, which in turn binds to specific membrane receptors on Leydig cells and Sertoli cells, respectively. Testicular secretions (testosterone and estradiol from Leydig cells and inhibin from Sertoli cells) act on the brain and anterior pituitary, where they exert control of gonadotropin release via negative feedback mechanisms. Testosterone also facilitates spermatogenesis by binding to cytoplasmic receptors in the Sertoli cells of the seminiferous tubules. (Fink and Jamieson, 1976) varies in a pulsatile manner. Lincoln and Frazer (1979) studied the importance of neural inputs from the hypothalamus indirectly by neutralizing LHRH secretion with LHRH antibodies. Passive immunization of intact Soay rams with LHRH antiserum resulted in an immediate blockage of the episodic fluctuations of both LH and testosterone. Similar observations have been made for ram lambs (Schanbacher, 1982) and for bull calves (B. D. Schanbacher, unpublished data) following active immunization against LHRH. Failure of these lambs and calves to respond to exogenous LHRH showed that LHRH immunoneutralization provides a physiological block to the hypothalamic-pituitary-leydig cell axis. Data
4 58 SCHANBACHER m c E 2 s c * 10 ' W 6 B A <* m CO I o 10 ^ m 33 _ m ' * * ' i TIME OF DAY (h) Figure 2. Luteinizing hormone (o) and testosterone ( ) concentrations in serum of a mature bull during a 14-h intensive bleeding period (A) and another mature bull injected iv every 4 h with 1,000 ng of LHRH (B). (From Schanbacher and D'Occhio, 1982) that illustrate the biological consequences of LHRH immunization in lambs are presented in table 1. Note the marked reduction in testicular weight, the low to nondetectable concentrations of LH, FSH and testosterone in serum and the lack of LH release in response to exogenous LHRH. The above results clearly demonstrate the temporal relationship that exists between serum concentrations of LH and testosterone and provide evidence that their episodic secretion is dependent on secretory episodes of LHRH from the hypothalamus. Regulation of LH Secretion by Testosterone Luteinizing hormone is the principal regulator of testicular steroidogenesis; however, the TABLE 1. PAIRED TESTES WEIGHTS AND CONCENTRATIONS OF LH, FSH AND TESTOSTERONE IN SERUM OF RAM LAMBS IMMUNIZED AGAINST LUTEINIZING HORMONE RELEASING HORMONE (LHRH) OR BOVINE SERUM ALBUMIN (BSA) a Paired testes weight, g LH, ng/ml Serum FSH, ng/ml Testosterone, ng/ml Serum LH response to 250 ng LHRH, ng/ml 342 ± t ** 2.0 ± t.02.6 ±.04** ** 101 ± 9 81 ± ** 376 ± 28** 2.4 ± ±.3.3 ±.1**.3 ±.1** 8.5 ± ± ±.1** 13.4 ± 2.3** a Values are means ± SE. "Different from intact group (P<.01).
5 ENDOCRINOLOGY AND REGULATION OF TESTICULAR FUNCTION 59 W W 2 tit I4O TIME OF DAY (h) Figure 3. Luteinizing hormone ( ) and testosterone (o) profiles in serum of two wethers bled at 10-min intervals for 24 h, 6 wk after castration. (From D'Oechio et al., 1982b.) amount of LH required to maintain adequate serum testosterone is less than the animal is capable of secreting (Neaves, 1975). Feedback inhibition by gonadal steroids forms an integral part of the hypothalamic-pituitary-testicular axis in males (Lipsett, 1979; Schanbacher, 1980c; Santen, 1981) and provides a plausible explanation for the major differences in LH secretory patterns between castrate and intact males. Because testosterone is quantitatively the most important hormone secreted by the testis (Ewing and Brown, 1977), it seems reasonable to assume that this steroid is largely responsible for the pattern of LH secretion in intact males. This hypothesis was recently tested by monitoring the LH secretory pattern of intact rams and comparing them with those of castrate rams given testosterone replacement therapy (D'Oechio et al., 1982b). Castrate animals showed frequent, rhythmic pulses of LH (figure 3), whereas intact animals showed infrequent pulses of LH that occurred episodically (figure 4). These profiles are similar to those reported previously for castrate (Riggs and Malven, 1974) and intact rams (Katongole et al., 1974; Sanford et al., 1974; Galloway and Pelletier, 1975; Schanbacher and Ford, 1976; Lincoln, 1976). Secretory profiles for castrate rams implanted with Silastic capsules containing testosterone are shown in figure 5. The implants not only provided normal physiological concentrations of testosterone in blood (2.01 ±.09 vs 2.25 ±.49 ng/ml of serum for implanted castrate and intact control rams, respectively), but suppressed mean serum LH concentrations (2.2 ±.8 ng/ml) to those values observed in intact rams (2.1 ±.2 ng/ml). In spite of these similarities, testosterone implanted castrates, like intact rams, were variable with regard to number of LH secretory episodes exhibited per 24 h. These data indicate that testosterone is the testicular steroid responsible for feedback regulation of LH secretion in rams. Regulation of LH Secretion by Androgenic and Estrogenic Metabolites of Testosterone Testosterone may be the secretory product of the testis responsible for feedback regulation of LH secretion, but systemically and (or) centrally produced androgenic and estrogenic metabolites may mediate the suppressive effects of testosterone on LH (Baird et al., 1968; Santen, 1981). Enzymes that metabolize testos-
6 60 SCHANBACHER R I TIME OF DAY (h) Figure 4. Luteinizing hormone ( ) and testosterone (o) profiles in serum of three rams bled at 10-min intervals for 24 h. (From D'Occhio et al., 1982b.) terone to Sa-reduced and aromatized steroids (figure 6) are present in the brain of males in areas that are associated with gonadotropin secretion (Naftolin et al., 1975; Callard et al., 1978). Furthermore, these same areas contain specific receptors that bind androgens and estrogens with high affinity (MacLusky and Clark, 1980;McEwen, 1980). Several studies have been conducted using rats (Swerdloff et al., 1972; Eldridge and Mahesh, 1974) or humans (Santen, 1975; Winters et al., 1979a,b) to test the susceptibility of LH secretion to 5a-reduced androgens and estrogens. Conclusions from studies with these species indicate that both 5a-dihydrotestosterone and estradiol-17/3 are potent inhibitors of LH secretion. Studies in sheep (Schanbacher and Ford, 1977; Parrott and Davies, 1979) and cattle (D'Occhio et al., 1982a) have shown a potent, inhibitory effect of estradiol- 17/3, but have left some uncertainty regarding the proposed role of 5a-dihydrotestosterone. A recent study with steers (D'Occhio et al., 1982a) demonstrated the importance of estra-
7 ENDOCRINOLOGY AND REGULATION OF TESTICULAR FUNCTION 61 diol-17/3 as a regulator of LH secretion. Angus calves that had been castrated at birth were infused with one-of-four different steriods at approximately 10 mo of age. Each steroid was infused at a rate that would cause a blood concentration equal or exceeding levels normally associated with intact bulls. Neither testosterone, 5a-dihydrotestosterone nor estrone affected the LH secretory profiles of these steers (figure 7). Secretion of LH continued in the pulsatile manner characteristic of long-term castrates. On the other hand, estra- OH diol-17/3 abolished pulsatile LH release and suppressed mean LH concentrations in these animals (figure 8). Steers infused with estradiol- 17/3 released LH normally in response to an iv injection of LHRH. Thus, LH release was probably blocked at the level of the hypothalamus and not the pituitary per se. Although the question arises from this study as to whether longterm castrates are suitable models for the study of acute androgen feedback (McCarthy and Swanson, 1976; Resko et al., 1977; Schanbacher, 1981a), negative feedback by estradiol- 17/3 has been demonstrated in castrate males of other farm animal species (Parrott and Davies, 1979). Data presented above are consistent with the view that in the male bovine, estradiol-17/3 exerts negative feedback at the level of the hypothalamus to block pulsatile LHRH release. 5a-reducta3e Aromofase 5*-Dhydrotestosterone Estradiol -17/3 Figure 6. Metabolic conversion of testosterone to 5a-dihydrotestosterone and estradiol-17(3. Estradiol-17/3: Puberty in the Male Bovine Initiation of spermatogenesis and sexual maturation (i.e., puberty) in bulls is a slow developmental process associated with increasing concentrations of LH, FSH and testosterone in blood (Karg et al., 1976; Schams et al., 1978; Schanbacher, 1979b). Important interactions exist between pituitary sensitivity to LHRH and gonadal steroid feedback (Odell et al., 1970; Mongkonpunya et al., 1975;
8 62 SCHANBACHER EXPERIMENT I 30 1 VEHICLE" 200 ul 30% ETHANOL/mml 20 ioi 0 30, ESTRONE 2 ug/min 20^ ioi 0 _L_I I I I I,1 _1 L_l ' 30r 1 5 C- DIHYDROTESTOSTERONE 20 ug/min (ng, 20 X i 10 o- I l-l I II- JU., I MM-J I I I I I I ZD CC UJ CO 30r TESTOSTERONE 20 pg/min 20) ioi II 12-1 U_i t_ EXPERIMENT 2 30 TESTOSTERONE 80 ug/min II TIME OF DAY (h) Figure 7. Representative LH profiles for chronic castrate steers infused iv for 12 h with vehicle, estrone, 5a-dihydrotestosteronc and testosterone. Pituitary lesponsc to LHRH (1.000 ng iv) was determined at the end of the infusion period ( ). (From D'Oechio et al., 1982a.)
9 ENDOCRINOLOGY AND REGULATION OF TESTICULAR FUNCTION ANIMAL I ESTRADIOL-I7 2 ug/min ANIMAL 2 J ESTRADIOL-17,8 2 ug/min L 1 1 E \ 30- ANIMAL 3 o> c 20- I _J 10-1 ESTRADJOtTiTfi 2 ug/min CC LU CO 0-30r ESTRADIOL- \7j3 _i i i i 2 pg/roi" \ L i i ' i- i -j i i i k _ 3 Or ANIMAL 5 ESTRADIOL-17^9 2 ug/min Q L I 1_1 I I I I L l 1 I I II TIME OF DAY (h) Figure 8. Profiles of LH secretion in five chronic castrate steers infused iv for 12 h with estradiol-17/3. Pituitary response to LHRH (1,000 ng iv) was determined at the end of the infusion period ( ). (From D'Occhio et al., 1982a.)
10 l 64 SCHANBACHER _i 1, f AGE (wks) Figure 9. Changes in testicular diameter in young bull calves implanted with estradiol-17(3 at 26 wk of age. Note the rapid testicular growth immediately following implant removal. Lacroix and Pelletier, 1979a; Schanbacher, 1981b) to determine age at puberty. Although controversy persists regarding the ability of young bulls to respond to exogenous LHRH during the prepubertal-pubertal period (Mongkonpunya et al, 1975; Tannen and Convey, 1977; Kesler and Garverick, 1977; Chantaraprateep and Thibier, 1979), an increase in episodic LH activity may be responsible for the testicular development that then initiates puberty (Lacroix and Pelletier, 1979a,b). From these results and the assumption that episodic LH release is the result of an episodic pattern of LHRH release from the hypothalamus, it can be hypothesized that endocrine events associated with puberty in bulls are initiated at the level of the central nervous system. Recently, a limited number of experiments were conducted to test the above hypothesis and determine the importance of episodic LH activity during pubertal development in beef bulls. Young bulls were implanted with estradiol- 17(3 at dosages known to knhibit hypothalamic LHRH activity and episodic LH release (Schanbacher, 1981b). Figure 9 shows the effectiveness by which this treatment delays testicular growth and also suggests that the inhibitory effects of estradiol are acute because implant removal results in the immediate restoration of testicular growth. This growth is temporally associated with increased episodic LH activity (Schanbacher, 1981b). To ensure that the inhibitory effects of oj.,,, ^,,,,,,, i i. i r i i i i i i i i i i i i. i, i i. i i i TIME OF DAY(h) Figure 10. Serum LH ( ) and testosterone ( ) profiles in three bull calves implanted with estradiol-17 3 immediately before (left panel), 4 wk (middle panel) and 8 wk (right panel) after continuous pulsatile infusion of LHRH (500 ng/h iv). The calves were 34, 38 and 42 wk of age during the three sampling periods. (From Schanbacher et al., 1982.)
11 ENDOCRINOLOGY AND REGULATION OF TESTICULAR FUNCTION 65 TABLE 2. PAIRED TESTES WEIGHT AND TOTAL DAILY SPERM PRODUCTION (TDSP) IN CONTROL BULLS, ESTRADIOL-IMPLANTED BULLS AND ESTRADIOL-IMPLANTED BULLS INFUSED HOURLY WITH 500 NG OF LUTEINIZING HORMONE 3 RELEASING HORMONE (LHRH) Paired Total daily testes weigh t, sperm production. Treatment o X 10' Control bulls 352 ± ±.9 b b Estradiol-implanted bulls 105 ± 14c 0 Estradiol-implanted bulls, LHRH-infused bulls 254 i 12<1 1.2 ±,3 C Values are means ± SE for three calves 10 mo of age.,,c '^Means within column without a common superscript differ (P<.05). estradiol were at the hypothalamic level and not at the level of the pituitary and (or) testes, a second experiment (Schanbacher et al., 1982) was conducted whereby calves implanted with estradiol were administered exogenous LHRH intermittently for a period of 8 wk. Figure 10 shows the endocrine profiles for three implanted calves immediately before (left panel), 4 wk after (middle panel) and 8 wk after (right panel) hourly pulsatile injection of 500 ng of LHRH. As in the first experiment, episodic LH activity was not apparent in calves implanted with estradiol. However, pulse infusion of LHRH in these calves resulted in a rhythmic, pulsatile secretory pattern for LH. The secretory profiles of LH and testosterone were similar after 4 and 8 wk of LHRH treatment with mean serum concentrations increased over those of estradiol-implanted, saline-infused control calves (LH:3.4 vs 1.8 ng/ml; testosterone: 13.0 vs.3 ng/ml). The effects of estradiol and saline or LHRH treatment on testes weight and total daily sperm production are shown in table 2. Not only did estradiol treatment restrict testicular growth, but sperm production was not evident. Pulsatile administration of LHRH resulted in episodic LH release, enhanced testosterone secretion and initiation of spermatogenesis in bull calves treated with estradiol. Therefore, hypothalamic inputs appear necessary for the occurrence of endocrine events associated with puberty in bull calves. Secondly, estradiol implants provide an experimental probe for future investigations aimed at understanding the mechanisms controlling reproduction in males. This review describes the close temporal relationship that exists between secretions of the hypothalamus, pituitary and testis of rams and bulls. The testicular responses to exogenous LHRH and biological consequences of LHRH immunoneutralization suggest that the hypothalamus is primarily responsible for normal testicular function. The endocrine and exocrine functions of the testis appear to be regulated by steroid feedback inhibition of gonadotropin secretion at both hypothalamic and pituitary levels. Literature Cited Amann, R. P A critical review of methods for evaluation of spermatogenesis from seminal characteristics. J. Androl. 2:37. Baird, D., R. Horton, L. Longcope and J. F. Tait Steroid prehormones. Perspect. Biol. Med. 11:384. Callard, G. V., Z. Petro and K. J. Ryan Conversion of androgen to estrogen and other steroids in the vertebrate brain. Amer. Zool. 18:511. Carmel, P. W., S. Araki and M. Ferin Pituitary stalk portal blood collection in rhesus monkeys: Evidence for pulsatile release of gonadotropin releasing hormone (GnRH). Endocrinology 99: 243. Chantaraprateep, P. and M. Thibier, LH and testosterone responses to gonadoliberin (LRH) treatment in young bulls prior to and during puberty. Ann. Biol. Anim. Biochem. Biophys. 19:637. D'Occhio, M. J., J. E. Kinder and B. D. Schanbacher. 1982a. Patterns of LH secretion in castrated bulls (steers) during intravenous infusion of androgenic and estrogenic steroids: Pituitary response to exogenous luteinizing hormone releasing hormone. Biol. Reprod. 26:249. D'Occhio, M. J,, B. D. Schanbacher and J, E. Kinder. 1982b. Relationship between serum testosterone concentration and patterns of LH secretion in male sheep. Endocrinology 110:1547. Eldridge, J. C. and V. B. Mahesh Pituitarygonadal axis before puberty: Evaluation of testicular steroids in the male rat. Biol. Reprod. 11:385.
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J Is aromatization of testosterone to estradiol required for inhibition of luteinizing hormone secretion in men? J. Clin. Invest. 56:1555. Santen, R. J Independent control of luteinizing hormone secretion by testosterone and estradiol in males. In: K. Fortherby and S. B. Pal (Eds.) Hormones in Normal and Abnormal Human Tissues, p 459. Walter de Gruyter, New York. Schams, D., S. Gombe, E. Schallenberger, V, Reinhard and R, Claus Relationships between shortterm variations of LH, FSH, prolactin and testosterone in peripheral plasma of prepubertal bulls. J. Reprod. Fertil. 54:145. Schanbacher, B. D. 1979a. Testosterone secretion in cryptorchid and intact bulls injected with gonadotropin-releasing hormone and luteinizing hormone. Endocrinology 104:360. Schanbacher, B. D. 1979b. Relationship of in vitro gonadotropin binding to bovine testes and the onset of spermatogenesis. J. Anim, Sci. 48:591. Schanbacher, B. D. 1980a. Testosterone regulation of luteinizing hormone and follicle stimulating hormone secretion in young male lambs. J. Anim. Sci. 51:679.
13 ENDOCRINOLOGY AND REGULATION OF TESTICULAR FUNCTION 67 Schanbacher, B. D. 1980b. Androgen response of cryptorchid and intact rams to ovine LH. J. Reprod. Fertil. 59:151. Schanbacher, B. D. 1980c. The feedback control of gonadotroph"! secretion by testicular steroids. Proc. 9th Int. Congr. Anim. Prod. Artif. Insem., RT-D-4, pp Madrid. Schanbacher, B. D. 1981a. Testosterone regulation of LH secretion: Effect of time after castration. J. Androl. 2:26. Schanbacher, B. D. 1981b. Importance of the episodic nature of luteinizing hormone secretion for normal development of the bovine testis during puberty: Interference with oestradiol-17/3. J. Endocrinol. 88:393. Schanbacher, B. D Responses of ram lambs to active immunization against testosterone and luteinizing hormone releasing hormone. Amer. J. Physiol. 242:E201. Schanbacher, B. D. and M. J. D'Occhio Validation of a direct radioimmunoassay for testosterone in unextracted serum from five species: Application to study of the hypothalamic-pituitarygonadai axis in males. J. Androl. 3:45. Schanbacher, B. D., M. J. D'Occhio and J. E. Kinder Initiation of spermatogenesis and testicular growth in oestradiol-17(3-implanted bull calves with pulsatile infusion of luteinizing hormone-releasing hormone. J. Endocrinol 93:183. Schanbacher, B. D. and S. E. Echternkamp Testicular steroid secretion in response to GnRHmediated LH and FSH release in bulls. J. Anim. Sci. 47:514. Schanbacher, B. D. and J. J. Ford Seasonal profiles of plasma luteinizing hormone, testosterone and estradiol in the ram. Endocrinology 99:752. Schanbacher, B. D. and J. J. Ford Gonadotropin secretion in cryptorchid and castrate rams and the acute effects of exogenous steroid treatment. Endocrinology 100:387. Setchell, B. P., R. V. Davies and S. J. Main Inhibin. In: A. D. Johnson and W. R. Gomes (Eds.) The Testis, Vol. 4. pp Academic Press, New York. Swerdloff, R. S., P. C. Walsh and W. D. Odell Control of LH and FSH secretion in the male: Evidence that aromatization of androgens to estradiol is not required for inhibition of gonadotropin secretion. Steroids 20:13. Tannen, K. J. and E. M. Convey Gonadotropin releasing hormone-induced change in serum luteinizing hormone, testosterone and androstenedione in bulls, steers and steers given testosterone. J. Anim. Sci. 44:1080. Thibier, M Effect of synthetic gonadotropin-releasing hormone (Gn-RH) on circulating luteinizing hormone (LH) and testosterone in young post-pubertal bulls. Acta Endocrinol. 81: 635. Winters, S. J., J. J. Janick, D. L. Loriaux and R. J. Sherins. 1979a. Studies on the role of sex steroids in the feedback control of gonadotropin concentrations in men. II. Use of the estrogen antagonist, clomiphene citrate. J. Clin. Endocrinol. Metab. 48:222. Winters, S. J., R. J. Sherins and D. L, Loriaux. 1979b. Studies on the role of sex steroids in the feedback control of gonadotropin concentrations in men. III. Androgen resistance in primary gonadal failure. J. Clin. Endocrinol. Metab. 48:553.
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