Abstract
The present study was designed to monitor the correlation of gonadal steroidogenic activity and nitric oxide (NO) of plasma and testis of male laboratory mouse, Mus musculus, under (1) control/basal and (2) experimental conditions. In the first study, male mice (n = 6) of three age groups (3-week-old sexually immature, 9-week-old sexually mature and 1.5-year-old) were assayed for plasma testosterone and level of NO in the plasma and testis. The immunoreactivity of 3-β-hydroxysteroid dehydrogenase (3-β-HSD) and androgen receptors (ARs) was also detected in testis and epididymis, respectively. In the second study, the reproductive state of mice was altered by injecting precursors of serotonin 5-hydroxytryptophan (5-HTP) and dopamine l-dihydroxyphenylalanine (l-DOPA) daily for 13 days. In one subgroup, mice received their daily injections 8 h apart and in another subgroup 12 h apart. A third subgroup of control mice received two daily injections of normal saline. After the completion of the experiment, the mentioned parameters were measured. The results showed a significant increase in levels of NO and a lowering of the immune reactivity of 3-β-HSD and AR, in both leydig cells and the epididymis in the sexually immature, old-age mice as well as in the mice that received 5-HTP and l-DOPA in the 8-h temporal relation, whereas opposite effects were observed in the sexually mature mice as well as in the mice that received 5-HTP and l-DOPA in the 12-h temporal relation. These findings led us to conclude that an inverse correlation exists between testicular steroidogenic activity and NO activity of laboratory mice under control and experimentally modulated gonadal conditions.
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C.M. Chaturvedi, P. Kumar, Nitric oxide modulates gonadal and adrenal function in Japanese quail Coturnix coturnix japonica. Gen. Comp. Endocrinol. 151, 285–299 (2007)
P. Kumar, C.M. Chaturvedi, Correlation of nitric oxide (NO) activity and gonadal function in Japanese quail, Coturnix coturnix japonica following temporal phase relation of serotonergic and dopaminergic oscillations. Anim. Repro. Sci. 106, 48–64 (2008)
P. Kumar, C.M. Chaturvedi, Reproductive response and nitric oxide activity in Japanese quail, Coturnix coturnix japonica, is altered by specific phase relation of neural (Serotonergic and Dopaminergic) oscillations and pineal function. Domest. Anim. Endocrinol. 36, 152–161 (2009)
N. Pathak, B. Lal, Seasonality in expression and distribution of nitric oxide synthase isoforms in the testis of the catfish, Clarias batrachus: role of nitric oxide in testosterone production. Comp. Biochem. Physio. Part C. 151, 286–293 (2010)
A. Banerjee, S. Anjum, R. Verma, A. Krishna, Alteration in expression of estrogen receptor isoforms alpha and beta and aromatase in the testis and its relation with changes in nitric oxide during aging in mice. Steroids. 77, 609–620 (2012)
V.P. Singh, C.M. Chaturvedi, Correlation of Nitric oxide and testicular activity in laboratory mouse, Mus musculus. Int. J. Innov. Res. Sci. Eng. Techn. 2, 721–729 (2013)
S.M. McCann, C. Mastronardi, A. Walczewska, S. Karanth, V. Rettoriand, W.H. Yu, The role of nitric oxide in reproduction. Braz. J. Med. Biol. Res. 32, 1367–1379 (1999)
R.G. Knowles, S. Moncada, Nitric oxide synthases in mammals. Biochem. J. 298, 249–258 (1994)
M. Rosselli, P.J. Keller, R.K. Dubey, Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Human Reproduction Update 4, 3–24 (1998)
A. Revelli, G. Soldati, C. Costamagna, O. Pellerey, E. Aldieri, M. Massobrio et al., Follicular fluid proteins stimulate nitric oxide (NO) synthesis in human sperm: a possible role for NO in acrosomal reaction. J. Cell. Physiol. 178, 85–92 (1999)
A.B. Grossman, W.G. Rossmanith, E.B. Kabigting, G. Cadd, D. Clifton, R.A. Steiner, The distribution of hypothalamic nitric oxide synthase mRNA in relation to gonadotrophin-releasing hormone neurons. J. Endocrinol. 140, R5–R8 (1994)
A.E. Herbison, S.X. Simonian, P.J. Norris, P.C. Emson, Relationship of neuronal nitric oxide synthase immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J. Neuroendocrinol. 8, 73–82 (1996)
C.M. Chaturvedi, R. Bhatt, The effects of different temporal relationships of 5-hydroxytryptophan (5-HTP) and L-dihydroxyphenylalanine (l-DOPA) on reproductive and metabolic responses of migratory Red Headed Bunting (Emberiza bruniceps). J. Interdisc. Cycles Res. 21, 129–139 (1990)
C.M. Chaturvedi, S.K. Prasad, Timed daily injections of neurotransmitter precursor alter the gonadal and body weights of spotted munia, Lonchura punctulata maintained under short daily photoperiods. J. Exp. Zool. 260, 194–201 (1991)
S.K. Prasad, J.P. Thapliyal, C.M. Chaturvedi, The effects of daily injections of L-dihydroxyphenylalanine and 5-Hydroxytryptophan in different temporal relationships on thyroid-gonadal interaction in an Indian Finch Spotted Munia Lonchura punctulata. Gen. Comp. Endocrinol. 86, 335–343 (1992)
D. Phillips, C.M. Chaturvedi, Functional maturation of neuroendocrine gonadal axis is altered by specific phase relations of circadian neurotransmitter activities in Japanese quail. Biomed. Environ. Sci. 8, 367–377 (1995)
C.M. Chaturvedi, A.C. Tiwari, P. Kumar, Effect of temporal synergism of neural oscillations on photorefractoriness in Japanese quail (Coturnix coturnix japonica). J. Exp. Zool. 305A, 3–12 (2006)
C.M. Chaturvedi, R. Jaiwal, Temporal synergism of neurotransmitter affecting drugs and seasonal reproductive responses of Indian palm squirrel Funambulus pennanti. J. Neural Transm. 81, 31–40 (1990)
R. Jaiwal, C.M. Chaturvedi, Elimination of testicular regression by 12-hr temporal relationship of serotonergic and dopaminergic activity in Indian Palm squirrel Funambulus pennanti. J. Neural Transm. 84, 45–52 (1991)
C.M. Chaturvedi, A.B. Singh, Suppression of annual testicular development in Indian Palm Squirrel, Funambulus pennanti by 8 h temporal relationship of serotonin and dopamine precursor drugs. J. Neural Transm. 88, 53–60 (1992)
S. Sethi, C.M. Chaturvedi, Temporal synergism of neurotransmitters (serotonin and dopamine) affects testicular development in mice. Zoology 112, 461–470 (2009)
S. Sethi, K. Tsutsui, C.M. Chaturvedi, Temporal phase relation of circadian neural oscillations alters RFamide-related peptide-3 and testicular function in the mouse. Neuroendocrinology 91, 189–199 (2010)
S. Sethi, C.M. Chaturvedi, Temporal phase relation of circadian neural oscillations as the basis of testicular maturation in mice: a test of coincidence model. J. Biosci. 35, 571–581 (2010)
J.P. Ternaux, A. Bioreu, S. Bourgoin, M. Hanon, F. Hery, J. Glowlnski, In vivo release of 5-HT in the lateral ventricle of the rat: effects of 5-hydroxytryptophan and tryptophan. Brain Res. 101, 533–548 (1975)
A.E. Jimenez, L.L. Voogt, L.A. Carr, L-3, 4-dihydroxyphenylalanine (l-DOPA) as an inhibitor of prolactin release. Endocrinology 102, 166–174 (1978)
K.V. Sastry, R.P. Moudgal, J. Mohan, J.S. Tyagi, G.S. Rao, Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal. Biochem. 306, 79–82 (2002)
Kotula-Balak, M., Hejmej, A., and Bilińska, B (2012) Hydroxysteroid Dehydrogenases: Localization, function and regulation in the testis. In ‘Biochemistry, genetics and molecular biology’ (R. A. Canuto). Intech. open Sci. pp. 265–288
D.S. Keeney, J.I. Mason, Expression of testicular 3 beta-hydroxysteroid dehydrogenase/delta 5-4-isomerase: regulation by luteinizing hormone and forskolin in Leydig cells of adult rats. Endocrinology 130, 2007–2015 (1992)
D.M. Keenan, J.D. Veldhuis, Age-dependent regression analysis of male gonadal axis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R1215–R1227 (2009)
S.M. Pincus, J.D. Veldhuis, T. Mulligan, A. Iranmanesh, W.S. Evans, Effects of age on the irregularity of LH and FSH serum concentrations in women and men. Am. J. Physiol. Endocrinol. Metab. 273, E989–E995 (1997)
J.S. Tenover, Effects of testosterone supplementation in the aging male. J. Clin. Endocrinol. Metabol. 75, 1092–1098 (1992)
A. Vermeulen, Androgens in the aging male. J. Clin. Endocrinol. Metabol. 73, 221–224 (1991)
Q. Zhou, R. Nie, Gail S. Prins, PhilippaTK Saunders, BenitaS Katzenellenbogen, RexA Hess, Localization of androgen and estrogen receptors in adult male mouse reproductive tract. J. Androl. 23, 870–881 (2002)
S. Dave, D.P. Farrance, S.A. Whitehead, Evidence that nitric oxide inhibits steroidogenesis in cultured rat granulosa cells. Clin. Sci. 92, 277–284 (1997)
M.L. Adams, E.R. Meyer, B.N. Sewing, T.J. Cicero, Effects of nitric oxide-related agents on rat testicular function. J. Pharmacol. Exp. Ther. 269, 230–237 (1994)
B.A. Weissman, E. Niu, R. Ge, C.M. Sottas, M. Holmes, J.C. Hutson, M.P. Hardy, Paracrine modulation of androgen synthesis in rat leydig cells by nitric oxide. J. Androl. 26, 369–378 (2005)
B.J. Van Voorhis, M.S. Dunn, G.A. Snyder, C.P. Weiner, Nitric oxide: an autocrine regulator of human granulosa–luteal cell steroidogenesis. Endocrinology 135, 1799–1806 (1994)
F. Grasselli, N. Ponderato, G. Basini, C. Tamanini, Nitric oxide synthase expression and nitric oxide/cyclic GMP pathway in swine granulosa cells. Domest. Anim. Endocrinol. 20, 241–252 (2001)
M. Masuda, T. Kubota, S. Kamada, T. Aso, Nitric oxide inhibits steroidogenesis in cultured porcine granulosa cells. Mol. Hum. Reprod. 3, 285–292 (1997)
H. Matsumi, T. Yano, Y. Osuga, K. Kugu, X. Tang, J.P. Xu et al., Regulation of nitric oxide synthase to promote cytostasis in ovarian follicular development. Biol. Reprod. 63, 141–146 (2000)
N. Ponderato, F. Grasselli, R. Saleri, C. Tamanini, Factors modulating apoptosis: an in vitro study in swine granulosa cells. Reprod. Domest. Anim. 35, 213–219 (2000)
G. Basini, M. Baratta, N. Ponderato, S. Bussolati, C. Tamanini, Is nitric oxide an autocrine modulator of bovine granulosa cell function? Reprod. Fertil. Dev. 10, 471–478 (1998)
G. Basini, C. Tamanini, Selenium stimulates estradiol production in bovine granulosa cells: possible involvement of nitric oxide. Domest. Anim. Endocrinol. 18, 1–17 (2000)
Acknowledgments
This work was funded by a research Grant (37/(1284)/07/EMR-II) to CMC from the Council of Scientific and Industrial Research, New Delhi, India. Authors are thankful to Dr. J. Mohan and Dr. K.V. Sastry of Central Avian Research Institute, Izatnagar, Bareilly, India, for providing copper cadmium alloy.
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Singh, V.P., Chaturvedi, C.M. Interrelationship between NO and androgenic activity in mice, Mus musculus, following temporal phase relation of serotonergic and dopaminergic neural oscillations. Endocrine 46, 624–633 (2014). https://doi.org/10.1007/s12020-013-0148-z
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DOI: https://doi.org/10.1007/s12020-013-0148-z