Testis of prepubertal rhesus monkeys receives a dual catecholaminergic input provided by the extrinsic innervation and an intragonadal source of catecholamines

Biology of Reproduction

Volumn 55, Issue 3, 1996, Pages 509-518

  Mayerhofer, Artur ^a,b   Danilchik, Michael ^c   Pau, K Y Francis ^b   Lara, Hernan E ^d   Russell, Lonnie D ^e   Ojeda, Sergio R ^b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF CHILE   (Chile)

^e SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATECHOLAMINE;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CATECHOLAMINE NERVE CELL; ENZYME ACTIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SYMPATHETIC INNERVATION; TESTIS;

ANIMALIA; MACACA MULATTA; MAMMALIA; PRIMATES;

EID: 0029820367     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod55.3.509     Document Type: Article

References (67)

1. Faiman C, Winter JSD. Gonadotropins and sex hormone patterns in puberty: Clinical data. In: Grumbach MM, Grave GD, Mayer FE (eds.), Control of the Onset of Puberty. New York: John Wiley & Sons; 1974: 32-55.
2. Odell WD, Swerdloff RS. Etiologies of sexual maturation: a model system based on the sexually maturing rat. Recent Prog Horm Res 1976; 32:245-288.
3. Boujrad N, Ogwuegbu SO, Gamier M, Lee C-H, Martin BM, Papadopoulos V. Identification of a stimulator of steroid hormone synthesis isolated from testis. Science 1995; 268:1609-1612.
4. Setchell BP. Nerves of the testis and scrotum. In: Finn CA (ed.), The Mammalian Testis. Reproductive Biology Handbooks. Ithaca, NY: Cornell University Press; 1978: 77-89.
5. Setchell BP, Maddocks S, Brooks DE. Anatomy, vasculature, innervation, and fluids of the male reproductive tract. In: Knobil E, Neill JD (eds.), The Physiology of Reproduction, 2nd Edition. New York: Raven Press; 1994: 1063-1175.
6. Rauchenwald M, Steers WD, Desjardins C. Efferent innervation of the rat testis. Biol Reprod 1995; 52:1136-1143.
7. Zhu BC, Chiocchio SR, Suburo AM, Tramezzani JH. Monoaminergic and peptidergic contributions of the superior and the inferior spermatic nerves to the innervation of the testis in the rat. J Androl 1995; 16: 248-258.
8. Baumgarten HG, Holstein AF. Catecholaminhaltige Nervenfasern im Hoden des Menschen. Z Zellforsch Mikroskop Anat 1967; 79:389-395.
9. Okkels H, Sand K. Morphological relationship between testicular nerves and Leydig cells in man. J Endocrinol 1940; 2:38-46.
10. Heindel JJ, Steinberger A, Strada SJ. Identification and characterization of a beta-1-adrenergic receptor in the rat Sertoli cell. Mol Cell Endocrinol 1981; 22:349-358.
11. Anakwe OO, Moger WH. Ontogeny of rodent testicular androgen production in response to isoproterenol and luteinizing hormone in vitro. Biol Reprod 1984; 30:1142-1152.
12. Anakwe OO, Moger WH. Catecholamine stimulation of androgen production by rat Leydig cells: interaction with luteinizing hormone and luteinizing hormone-releasing hormone. Biol Reprod 1986; 35:806-814.
13. Anakwe OO, Murphy PR, Moger WH. Characterization of beta-adrenergic binding sites on rodent Leydig cells. Biol Reprod 1985; 33: 815-826.
14. Poyet P, Labrie F. Characterization of beta-adrenergic receptors in dispersed rat testicular interstitial cells. J Androl 1987; 8:7-13.
15. Cooke BA, Golding M, Dix CJ, Hunter MG. Catecholamine stimulation of testosterone production via cyclic AMP in mouse Leydig cells in monolayer culture. Mol Cell Endocrinol 1982; 27:221-231.
16. Levin J, Lloyd CW, Lobotsky J, Friedrich EH. The effect of epinephrine on testosterone production. Acta Endocrinol (Copenh) 1967; 55: 184-192.
17. Eik-Nes KB. An effect of isoproterenol on rates of synthesis and secretion of testosterone. Am J Physiol 1969; 217:1764-1770.
18. Damber J-E, Janson PO. The effects of LH, adrenaline and noradrenaline on testicular blood flow and plasma testosterone concentrations in anesthetized rats. Acta Endocrinol (Copenh) 1978; 88:390-396.
19. Mayerhofer A, Bartke A, Steger RS. Catecholamine effects on testicular testosterone production in the gonadally active and the gonadally regressed adult golden hamster. Biol Reprod 1989; 40:752-761.
20. Mayerhofer A, Amador AG, Steger RS, Bartke A. Testicular function after local injection of 6-hydroxydopamine or norepinephrine in the golden hamster (Mesocricetus auratus). J Androl 1990; 11:301-311.
21. Mayerhofer A, Bartke A, Steger RS, Gow G. Catecholamines stimulate testicular testosterone release in the immature golden hamster via interaction with testicular alpha- and beta-adrenergic receptors. Acta Endocrinol (Copenh) 1992; 127:526-530.
22. Mayerhofer A, Began T, Bartke A. Catecholamines stimulate testicular steroidogenesis in vitro in the Siberian hamster, Phodopus sungorus. Biol Reprod 1993; 48:883-888.
23. Mayerhofer A, Amador AG, Steger RS, Shire JGM, Bartke A. Catecholamines and testicular function: a study in BALB/cJ mice, a substrain with high levels of adrenomedullary catecholamine synthesizing enzymes. Neuroendocrinol Lett 1993; 15:417-424.
24. Favaretto ALV, Valenca MM, Hattori M, Wakabayashi K, Antunes-Rodriges J. Characterization of adrenergic control of the Leydig cell steroidogenesis: identification of both stimulatory and inhibitory components. Braz J Mcd Biol Res 1988; 21:539-543.
25. Frankel AI, Ryan EL. Testicular innervation is necessary for the response of plasma testosterone levels to acute stress. Biol Reprod 1981; 24:491-495.
26. Bergh A, Blom H, Damber JE, Henriksson R. The effect of long-term variation in sympathetic activity on testicular morphology in immature rats. Andrologia 1987; 19:448-451.
27. Gerandai I, Nemeskeri A, Csernus V. Depending on the dose 6-OHDA stimulates or inhibits the testis of immature rats. Exp Clin Endocrinol 1984; 84:27-36.
28. Nagai K, Murano S, Minokoshi Y, Okuda H, Kinutani M. Effects of denervation and local 6-hydroxydopamine injection on testicular growth in rats. Experientia 1982; 38:592-594.
29. Dees WL, Hiney JK, Schultea TD, Mayerhofer A, Danilchik M, Dissen GA, Ojeda SR. The primate ovary contains a population of catecholaminergic neuron-like cells expressing nerve growth factor receptors. Endocrinology 1995; 136:5760-5768.
30. Mayerhofer A, Russell LD, Ojeda SR. The primate testis contains an intratesticular source of catecholamines complementary to its extrinsic innervation. Proc XIIIth Testis Workshop: Cell Mol Regulation of Testicular Cells 1995; 54.
31. Saller CF, Zigmond MJ. A radioenzymatic assay for catecholamines and dihydroxphenylacetic acid. Life Sci 1978; 23:1117-1130.
32. Lara HE, Ferruz JL, Luza S, Bustamante DA, Borges Y, Ojeda SR. Activation of ovarian sympathetic nerves in polycystic ovary syndrome. Endocrinology 1993; 133:2690-2695.
33. Hirst JJ, Haluska GJ, Cook MJ, Hess DL, Novy MJ. Comparison of plasma oxytocin and catecholamine concentrations with uterine activity in pregnant rhesus monkeys. J Clin Endocrinol & Metab 1991; 73: 804-810.
34. Ichikawa S, Ichinose H, Nagatsu T. Multiple mRNAs of monkey tyrosine hydroxylase. Biochem Biophys Res Commun 1990; 173:1331-1336.
35. Mayerhofer A, Russell LD, Grothe C, Rudolf M, Gratzl M. Presence and localization of a basic fibroblast growth factor-like protein in rodent testes. Endocrinology 1991; 129:921-924.
36. Dissen GA, Hill DF, Costa ME, Dees WL, Lara HE, Ojeda SR. A role for trkA nerve growth factor receptors in mammalian ovulation. Endocrinology 1996; 137:198-209.
37. Savage RM, Danilchik MV. Dynamics of germ plasm localization and its inhibition by ultraviolet irradiation in early cleavage Xenopus embryos. Dev Biol 1993; 157:371-382.
38. de la Torre JC. Standardization of the sucrose-potassium phosphateglyoxylic acid histofluorescence method for tissue monoamines. Neurosci Lett 1980; 17:339-340.
39. Russell L, Burguet S. Ultrastructure of Leydig cells as revealed by secondary tissue treatment with a ferrocyanide-osmium mixture. Tissue & Cell 1977; 9:751-766.
40. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156-159.
41. Lara HE, Hill DF, Katz KH, Ojeda SR. The gene encoding nerve growth factor is expressed in the immature rat ovary: effect of denervation and hormonal treatment. Endocrinology 1990; 126:357-363.
42. Ojeda SR, Hill DF, Katz KH. The genes encoding nerve growth factor and its receptor are expressed in the developing female rat hypothalamus. Mol Brain Res 1991; 9:47-55.
43. Ma YJ, Costa ME, Ojeda SR. Developmental expression of the genes encoding transforming growth factor alpha (TGFα) and its receptor in the hypothalamus of female rhesus macaques. Neuroendocrinology 1994; 60:346-359.
44. O'Malley KL, Anhalt MJ, Martin BM, Kelsoe JR, Winfield SL, Ginns EI. Isolation and characterization of the human tyrosine hydroxylase gene: identification of 5′ alternative splice sites responsible for multiple mRNAs. Biochemistry 1987; 26:6910-6914.
45. Ichinose H, Ohye T, Fujita K, Yoshida M, Ueda S, Nagatsu T. Increased heterogeneity of tyrosine hydroxylase in humans. Biochem Biophys Res Commun 1993; 195:158-165.
46. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 1977; 74:5463-5467.
47. Burnstock G. Autonomic neuromuscular junctions: current developments and future directions. J Anat 1986; 146:1-30.
48. Prince FP. Ultrastructural evidence of indirect and direct autonomic innervation of human Leydig cells: comparison of neonatal, childhood and pubertal ages. Cell Tissue Res 1992; 269:383-390.
49. van Campenhout E. Les relation nerveuses de la glande interstitielle des glandes genitales des mammiferes. Rev Can Biol 1949; 8:374-429.
50. Nistal M, Paniagua R, Asuncion-Abaurrea M. Varicose axons bearing "synaptic" vesicles on the basal lamina of the human seminiferous tubules. Cell Tissue Res 1982; 226:75-82.
51. Miyake K, Yamamoto M, Mitsuya H. Pharmacological and histological evidence for adrenergic innervation of the myoid cells in the rat seminiferous tubule. Tohoku J Exp Med 1986; 149:79-87.
52. Zieher LM, Debeljuk L, Iturriza F, Mancini RE. Biogenic amine concentration in testes of rats at different ages. Endocrinology 1971; 88: 351-354.
53. Davidoff MS, Schulze W, Middendorf R, Holstein AF. The Leydig cell of the human testis - a new member of the diffuse neuroendocrine system. Cell Tissue Res 1993; 271:429-439.
54. Middendorf R, Davidoff M, Holstein AF. Neuroendocrine marker substances in human Leydig cells - changes by disturbances of testicular function. Andrologia 1993; 25:257-262.
55. Schultea TD, Dees WL, Ojeda SR. Postnatal development of sympathetic and sensory innervation of the rhesus monkey ovary. Biol Reprod 1992; 47:760-767.
56. Lauder JM. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 1993; 16:233-240.
57. Ayer-LeLievre C, Olson L, Ebendal T, Hallböök F, Persson H. Nerve growth factor mRNA and protein in the testis and epididymis of mouse and rat. Proc Natl Acad Sci USA 1988; 85:2628-2632.
58. Seidl K, Holstein AF. Evidence for the presence of nerve growth factor (NGF) and NGF receptors in human testis. Cell Tissue Res 1990; 261: 549-554.
59. Ip NY, Ibañez CF, Nye SH, McClain J, Jones PF, Gies DR, Belluscio L, Le Beau MM, Espinosa III R, Squinto SP, Persson H, Yancopoulos GD. Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution, and receptor specificity. Proc Natl Acad Sci USA 1992; 89:3060-3064.
60. Ledley FD, DiLella AG, Kwok SCM, Woo SLC. Homology between phenylalanine and tyrosine hydroxylases reveals common structural and functional domains. Biochemistry 1985; 24.3389-3394.
61. Grima B, Lamouroux A, Boni C, Julien J-F, Javoy-Agid F, Mallet J. A single human gene encoding multiple tyrosine hydroxylases with different predicted functional characteristics. Nature 1987; 326:707-711.
62. Nagatsu T. The human tyrosine hydroxylase gene. Cell Mol Neurobiol 1989; 9:313-321.
63. Mayerhofer A, Dissen GA, Pau KYF, Ojeda SR. Novel tyrosine hydroxylase mRNA forms in rhesus monkey testis and ovary. Soc Neurosci Abstr 1994; 20:11.
64. Cattaneo R. Different types of messenger RNA editing. Annu Rev Genet 1991; 25:71-88.
65. Adler BK, Hajduk SL. Mechanisms and origins of RNA editing. Curr Opin Genet Dev 1994; 4:316-322.
66. Pigeon D, Ferrara P, Gros F, Thibault J. Rat pheochromocytoma tyrosine hydroxylase is phosphorylated on serine 40 by an associated protein kinase. J Biol Chem 1987; 262:6155-6158.
67. Campbell DG, Hardie DG, Vulliet PR. Identification of four phosphorylation sites in the N-terminal region of tyrosine hydroxylase. J Biol Chem 1986; 261:10489-10492.