Skip to main content
SpringerLink
Log in

Postnatal development and distribution of peptide-containing nerves in the genital system of the male rat

An immunohistochemical study

  • Published:
Histochemistry Aims and scope Submit manuscript

Summary

The distribution and relative density of peptide-containing nerves was studied in the rat in order to assess the progression of neuronal changes during the postnatal development of the male genital system from the prepubertal age to adulthood. Testis, caput and cauda epididymis, ductus deferens, seminal vescicles, prostate and penis from 8-, 20-, 38-, and 70-day-old rats were sectioned and were immunostained with antisera to the neuropeptides calcitonin gene-related peptide (CGRP), vasoactive intestinal peptide (VIP) and neuropeptide Y (NPY), and to a general neuronal marker, protein gene product 9.5 (PGP 9.5). The testicular parenchyma and caput epididymis did not show any immunoreactivity. Very scattered CGRP-containing nerves were present in 8-day-old rats; numerous VIP-, CGRP-, and NPY-peptide-containing nerves were observed in the cauda epididymis, ductus deferens, accessory glands and penis of 20-day-old rats. The number of nerves increased in 35-day-old rats while no changes were observed in more adult rats. A parallel increase was seen for the immunostain for PGP 9.5. These data suggest that peptide-containing nerves appear in the genital system after birth and reach a full development before the completion of puberty. Peptide-containing nerves were visible first in the interstitial area and then spread in the muscular coat of the ducts, glands and of the blood vessels. While CGRP- and NPY-containing nerves were distributed in the vicinity of the muscle cells, VIP-containing nerves were also observed in the subepithelial regions, suggesting a possible role of this neuropeptide in the control of epithelial functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allen LG, Wilson FJ, MacDonald GJ (1989) Neuropeptide Y-containing nerves in rat gonads: sex difference and development. Biol Reprod 40:371–378

    Google Scholar 

  • Alm P, Lundberg LM, Wharton J, Polak JM (1988) Ontogenic development of the guinea pig uterine innervation. An immunohistochemical study of different neuronal markers, neuropeptides and S-100 protein. Histochemistry 90:19–24

    Google Scholar 

  • Davies AM, Bandtlow C, Heumann R, Korsching S, Rohrer H, Thoenen H (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353–358

    Google Scholar 

  • Denis-Donini S (1989) Expression of dopaminergic phenotypes in the mouse olfactory bulb induced by the calcitonin gene-related peptide. Nature 339:701–703

    Google Scholar 

  • Dhall U, Cowen T, Haven JA, Burnstock G (1986) Perivascular noradrenergic and peptide-containing nerves show different patterns of changes during development and ageing in the guinea-pig. J Auton Nerv Syst 16:109–126

    Google Scholar 

  • Dixon AF, Kendrick KM, Blank MA, Bloom SR (1984) Effects of tactile and electrical stimuli upon release of vasoactive intestinal polypeptide in the mammalian penis. J Endocrinol 100:249–252

    Google Scholar 

  • Donoso V, Macarena S, St-Pierre S, Huidobro-Toro P (1988) Neuropeptide Y (NPY), an endogenous presynaptic modulator of adrenergic neurotransmission in the rat vas deferens: structural and functional studies. Peptides 9:545–553

    Google Scholar 

  • Doran JF, Jackson P, Kynoch PAM, Thompson RJ (1983) Isolation of PGP 9.5, a new human neuron-specific protein detected by high resolution two dimensional electrophoresis. J Neurochem 40:1542–1547

    Google Scholar 

  • Fahrenkrug J, Palle C, Jorgensen J, Otteson B (1989) Regulatory peptides in the mammalian urogenital system. In: Polak JM (ed) Regulatory peptides. Birkhäuser, Basel, pp 362–381

    Google Scholar 

  • Francavilla S, Moscardelli S, Properzi G, De Matteis MA, Scorza Barcellona P, Natali PG, De Martino C (1987) Postnatal development of epididymis and ductus deferens in the rat. A correlation between the ultrastructure of the epithelium and tubule wall and the fluorescence-microscopic distribution of actin, myosin, fibronectin and basement membrane. Cell Tissue Res 249:257–265

    Google Scholar 

  • Fried GH, Lagercrantz H, Hokfelt T (1978) Improved isolation of small noradrenergic vesicles from rat seminal ducts following castration. A density gradient centrifugation and morphological study. Neuroscience 3:1271–1291

    Google Scholar 

  • Gu J, Islam KN, Polak JM (1983a) Repeated application of first-layer antiserum improves immunoifluorescence staining: a modification of the indirect immunofluorescence staining procedure. Histochem J 15:475–482

    Google Scholar 

  • Gu J, Polak JM, Probert L, Islam KN, Marangos PJ, Mina S, Adrian TE, McGregor GP, O'Shaughnessy DJ, Bloom SR (1983b) Peptidergic innervation of the human male genital tract. J Urology 130:386–391

    Google Scholar 

  • Gulbenkian S, Wharton J, Polak JM (1987) The visualization of cardiovascular innervation in the guinea pig using an antiserum to protein gene product 9.5 (PGP 9.5). J Auton Nerv Syst 18:235–247

    Google Scholar 

  • Haegerstrand A, Jonzon B, Dalsgard CJ, Nilsson J (1989) Vasoactive intestinal polypeptide stimulates cell proliferation and adenylate cyclase activity of cultured human keratinocytes. Proc Natl Acad Sci USA 86:5993–5996

    Google Scholar 

  • Haegerstrand A, Dalsgaard CJ, Jonzon B, Larsson O, Nilsson J (1990) Calcitonin gene-related peptide stimulates proliferation of human endothelial cells. Proc Natl Acad Sci USA 87:3299–3303

    Google Scholar 

  • Hultgardh-Nilsson A, Nilsson J, Jonzon B, Dalsgaard CJ (1988) Growth inhibitory properties of vasoactive intestinal polypeptide. Regul Pept 22:267–274

    Google Scholar 

  • Inyama CO, Wharton J, Davis CJ, Jackson RH, Bloom SR, Polak JM (1987) Distribution of vasoactive intestinal polypeptide binding sites in guinea pig genital tissues. Neurosci Lett 81:111–116

    Google Scholar 

  • Lamano Carvalho TL, Hodson NP, Blank MA, Watson PF, Mulderry PK, Bishop AE, Gu J, Bloom SR, Polak JM (1986) Occurrence, distribution and origin of peptide-containing nerves of guinea-pig and rat male genitalia and the effects of denervation on sperm characteristics. J Anat 149:121–141

    Google Scholar 

  • New HV, Mudge AW (1986) Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis. Nature 323:809–811

    Google Scholar 

  • Orgebin-Crist MC, Danzo BJ, Davies J (1975) Endocrine control of the development and maintenance of sperm fertilizing ability in the epididymis. In: Hamilton DW, Greep RO (eds) Handbook of Physiology, sect. 7. Endocrinology, vol 5. American Physiological Society, Washington DC, pp 319–339

    Google Scholar 

  • Owman Ch, Sjoberg NO, Swedin G (1971) Histochemical and chemical studies on pre- and postnatal development of the different systems of “short” and “long” adrenergic neurons in peripheral organs of the rat. Z Zellforsch Mikrosk Anat 116:319–341

    Google Scholar 

  • Polak JM, Gu J, Mina S, Bloom SE (1981) Vipergic nerves in the penis. Lancet II:217–219

    Google Scholar 

  • Schindelmeiser J, Kutzner M, Bergmann M, Aumuller G, Heck H, Hoffmann K (1988) Influence of long and short photoperiods on the morphology and androgen receptor levels of the epididymis and the ductus deferens of Phodopus sungurus. Andrologia 20:507–515

    Google Scholar 

  • Schindelmeiser J, Rudolf T, Hoffmann K (1989a) Immunohistochemical localization of neuropeptide Y in nerves of the male genital tract of the photoperiodically responsive Djungarian hamster, Phodopus sungorus. Andrologia 21:547–554

    Google Scholar 

  • Schindelmeiser J, Kutzner M, Rolf LH, Hoffmann K (1989b) Photoperiodic influence on the innervation of the ductus epididymidis and ductus deferens of the Djungarian hamster, Phodopus sungorus — electron microscopic and biochemical results. Cell Tissue Res 256:175–181

    Google Scholar 

  • Schleicher GU, Drews U, Stumpf WE, Sar M (1984) Differential distribution of dihydrotestosterone and estradiol binding sites in the epididymis of the mouse. An autoradiographic study. Histochemistry 81:139–147

    Google Scholar 

  • Smith ER, Miller TB, Wilson MW, Appel MC (1984) Effects of vasoactive intestinal pepide on canine prostatic contraction and secretion. Am J Physiol 247:R701-R708

    Google Scholar 

  • Stjarne L, Lundberg JM, Astrand P (1986) Neuropeptide Y — A co-transmitter with noradrenaline and adenosine 5′-triphosphate in the sympathetic nerves of the mouse vas deferens? A biochemical, physiological and electropharmacological study. Neuroscience 18:151–166

    Google Scholar 

  • Stjernquist M, Qwman CH, Sjoberg NO, Sundler F (1987) Coexistence and cooperation between Neuropeptide Y and Norepinephrine in nerve fibers of guinea pig vas deferens and seminal vesicle. Biol Reprod 36:149–155

    Google Scholar 

  • Sun EL, Flickinger CJ (1979) Development of cell types and of regional differences in the postnatal rat epididymis. Am J Anat 154:27–56

    Google Scholar 

  • Virag R, Otteson B, Fahrenkrug J, Levy C, Wagner G (1982) VIP release during penile erection in man. Lancet II:1166–1167

    Google Scholar 

  • Wakade AR, Garcia AG, Kirpekar SM (1975) Effect of castration on the smooth muscle cells of the internal sex organs of the rat: influence of the smooth muscle on the sympathetic neurons innervating the vas deferens, seminal vesicle and coagulating gland. J Pharmacol Exp Ther 193:424–434

    Google Scholar 

  • Zamboni L, De Martino C (1967) Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy. J Cell Biol 35:148 A

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Internal Medicine (Andrology), University of L'Aquila, Via S. Sisto, 1-67100, L'Aquila, Italy

    G. Properzi, G. Cordeschi & S. Francavilla

Authors
  1. G. Properzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Cordeschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Francavilla
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Properzi, G., Cordeschi, G. & Francavilla, S. Postnatal development and distribution of peptide-containing nerves in the genital system of the male rat. Histochemistry 97, 61–68 (1992). https://doi.org/10.1007/BF00271282

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00271282

Keywords

Search

Navigation