Abstract
In order to clarify the cellular source and forms of bioactive inhibin in male Japanese macaques (Macaca fuscata), circulating concentrations of inhibin A and B, and immunohistochemical localization of inhibin subunits in testis were studied. Plasma concentrations of testosterone were also measured. The present study showed that inhibin B was clearly detected in the plasma of male Japanese macaques. Moreover, concentrations of both inhibin B and testosterone during the breeding (mating) season were significantly higher than those of the non-breeding season. On the other hand, plasma inhibin A was detected neither during the breeding seasons nor during the non-breeding seasons. Positive stainings with α and βB subunit antibodies were observed in the Sertoli cells, however staining with βA subunit antibody was not observed in the testicular samples. These results indicate that inhibin B is the major circulating inhibin and probably secreting from Sertoli cells in male Japanese macaques.
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References
Anawalt BD, Bebb RA, Matsumoto AM, Groome NP, Illingworth PJ, McNeilly AS, Bremner WJ (1996) Serum inhibin B levels reflect Sertoli cell function in normal men and men with testicular dysfunction. J Clin Endocrinol Metab 81:3341–3345
Andersson AM (2000) Inhibin B in the assessment of somniferous tubular function. Baillieres Best Pract Res Clin Endocrinol Metab 14:389–397
Andersson AM, Juul A, Petersen JH, Muller J, Groome NP, SkakkebaeK NE (1997) Serum inhibin B in healthy pubertal and adolescent boys: relation to age, stage of puberty, and follicle-stimulating hormone, luteinizing hormone, testosterone, and estradiol levels. J Clin Endocrinol Metab 82:3976–3981
Eckardstein S von, Simoni M, Bergmann M, Weinbauer GF, Gassner P, Schepers AG, Nieschlag E (1999) Serum inhibin B in combination with serum follicle-stimulating hormone (FSH) is a more sensitive marker than serum FSH alone for impaired spermatogenesis in men, but cannot predict the presence of sperm in testicular tissue samples. J Clin Endocrinol Metab 84:2496–2501
Foppiani L, Schlatt S, SimonI M, Weinbauer GF, Hacker-klom U, Nieschlag E (1999) Inhibin B is a more sensitive marker of spermatogenetic damage than FSH in the irradiated non-human primate model. J Endocrinol 162:393–400
Gay VL, Kerlan JT (1978) Serum LH and FSH following passive immunization against circulating testosterone in the intact male rat and in orchidectomized rats bearing subcutaneous silastic implants of testosterone. Arch Androl 1:257–266
Groome NP, Illingworth PJ, O'brien M, Pai R, Rodger FE, Mather JP, McNeilly AS (1996) Measurement of dimeric inhibin B throughout the human menstrual cycle. J Clin Endocrinol Metab 81:1401–1405
Groome NP, Tsigou A, Cranfield M, Knight PG, Robertson DM (2001) Enzyme immunoassays for inhibins, activins and follistatins. Mol Cell Endocrinol 180:73–77
Illingworth PJ, Groome NP, Byrd W, Rainey WE, McNeilly AS, Mather JP, Bremner WJ (1996) Inhibin-B: a likely candidate for the physiologically important form of inhibin in men. J Clin Endocrinol Metab 81:1321–1325
Jin W, Arai K Y, Herath CB, Kondo M, Kishi H, Tanioka Y, Watanabe G, Groome NP, Taya K (2001a) Inhibins in the male Gottingen miniature pig: Leydig cells are the predominant source of inhibin B. J Androl 22:953–960
Jin W, Wada S, Arai KY, Kishi H, Herath CB, Watanabe G, Suzuki A K, Groome NP, Taya K (2001b) Testicular secretion of inhibin in the male golden hamster (Mesocricetus auratus). J Androl 22:207–211
Kojima C, Kondo M, Jin W, Shimizu K, Itoh M, Watanabe G, Groome NP, Taya K (2002) Secretion of inhibin A and inhibin B during pregnancy and early postpartum period in Japanese monkeys. Endocrine 18:21–25
Kondo M, Udono T, Jin W-Z, Shimizu K, Funakoshi M, Itoh M, Watanabe G, Groome NP, Taya K (2000) Changes in plasma concentrations of inhibin A and inhibin B throughout sexual maturation in the male chimpanzee. Endocr J 47:707–714
Kretser DM de, Robertson DM (1989) The isolation and physiology of inhibin and related proteins. Biol Reprod 40:33–47
Majumdar SS, Winters SJ, Plant TM (1997) A study of the relative role of follicle stimulate hormone in the regulation of testicular inhibin secretion in the rhesus monkey (Macaca mulatta). Endocrinology 138:1363–1373
Matsubayashi K, Watanabe G, Taya K, Katakai Y, Sasamoto S, Suzuki J, Nozaki M (1991) Seasonal changes in plasma concentrations of immunoreactive inhibin and testicular activity in male Japanese monkeys. Biol Reprod 44:822–826
McNeilly AS, Souza CJ, Baird DT, Swanston IA, McVerry J, Crawford J, Cranfield M, Lincoln G A (2002) Production of inhibin A not B in rams: changes in plasma inhibin A during testis growth, and expression of inhibin/activin subunit mRNA and protein in adult testis. Reproduction 123:827-835
Nigi H (1975) Menstrual cycle and some other related aspects of Japanese monkeys (Macaca fuscata). Primates 16:207–216
Nozaki M, Oshima K (1987) Seasonal changes of the gonadotrophic function in the female Japanese monkey. In: Miura T (ed) Progress in biometeorology, vol 5. SPB Academic, The Hague, The Netherlands, pp 41–49
Pierik FH, Vreeburg JT, Stijnen T, de Jong FH, Weber RF (1998) Serum inhibin B as a marker of spermatogenesis. J Clin Endocrinol Metab 83:3110–3114
Plant TM, Padmanabhan V, Ramaswamy S, McConnell DS, Winters SJ, Groome NP, Midgley AR, Jr McNeilly AS (1997) Circulating concentrations of dimeric inhibin A and B in the male rhesus monkey (Macaca mulatta). J Clin Endocrinol Metab 82:2617–2621
Ramaswamy S, Plant TM (2001) Operation of follicle-stimulating hormone (FSH)-inhibin B feedback loop in the control of primate spermatogenesis. Mol Cell Endocrinol 180:93–101
Ramaswamy S, Marshall GR, McNeilly AS, Plant TM (1999) Evidence that in a physiological setting Sertoli cell number is the major determinant of circulating concentrations of inhibin B in the adult male rhesus monkey (Macaca mulatta). J Androl 20:430–434
Sharpe RM, Turner KJ, Mckinnell C, Groome NP, Atanassova N, Millar MR, Buchanan DL, Cooke P S (1999) Inhibin B levels in plasma of the male rat from birth to adulthood: effect of experimental manipulation of Sertoli cell number. J Androl 20:94–101
Shimizu K, Kondo M, Kojima C, Jin W, Itoh M, Watanabe G, Groome NP, Taya K (2002) Circulating inhibin A and inhibin B in normal menstrual cycle during breeding seasons of Japanese monkeys. J Reprod Dev 48:335–361
Weinbauwer GF, Schatt S, Walter V, Nieschlag E (2001) Testosterone-induced inhibition of spermatogenesis is more closely related to suppression of FSH than to testicular androgen levels in the cynomolgus monkey model (Macaca fascicularis). J Endocrinol 168:25–38
Ying S Y (1988) Inhibins, activins, and follistatins: gonadal proteins modulating the secretion of follicle-stimulating hormone. Endocrinol Rev 9:267–293
Acknowledgements
We are grateful to Dr. G.D. Niswender, Colorado State University, Fort Collins, Colo, USA for antisera against testosterone (GDN#250). This work was supported in part by a Cooperation Research Program of Primate Research Institute, Kyoto University, a Grant-in-Aid for scientific research (No. 12836005, No. 13027246) to K. S., a Grant-in-Aid for COE Research (No. 10 COE 2005), the MEXT Grant-in-Aid for the 21st Century COE Program (A2 to Kyoto University) from the Ministry of Education, Science, Sports, and Culture, Japan, and the Sasakawa Scientific Research Grant from The Japan Science Society. All animal care and the experimental protocol were approved by Guidelines for the Care and Use of Laboratory Primates prepared by the Primate Research Institute, Kyoto University, Japan.
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Itoh, M., Kondo, M., Kojima, C. et al. Inhibin B is the major form of inhibin secreted from testes in male Japanese macaques (Macaca fuscata). Primates 44, 253–257 (2003). https://doi.org/10.1007/s10329-003-0041-0
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DOI: https://doi.org/10.1007/s10329-003-0041-0