Testosterone and nerve growth factor have distinct but interacting effects on structure and neurotransmitter expression of adult pelvic ganglion cells in vitro

• Published in: Neuroscience Vol. 108; no. 2; pp. 331 - 340
• Main Authors: Meusburger, S.M, Keast, J.R
• Format: Journal Article
• Language: English
• Published: Oxford Elsevier Ltd 01.01.2001; Elsevier
• Subjects: Acetylcholine - metabolism; androgen; Animals; Biological and medical sciences; Cell Differentiation - drug effects; Cell Differentiation - physiology; Cell Size - drug effects; Cell Size - physiology; Cells, Cultured; Choline O-Acetyltransferase - metabolism; Drug Interactions - physiology; Fundamental and applied biological sciences. Psychology; Ganglia, Autonomic - drug effects; Ganglia, Autonomic - growth & development; Ganglia, Autonomic - metabolism; Hypogastric Plexus - drug effects; Hypogastric Plexus - growth & development; Hypogastric Plexus - metabolism; Male; Nerve Growth Factor - metabolism; Nerve Growth Factor - pharmacology; Neurites - drug effects; Neurites - metabolism; Neurites - ultrastructure; Neurons - cytology; Neurons - drug effects; Neurons - metabolism; neuropeptide; Neuropeptide Y - metabolism; Neurotransmitter Agents - biosynthesis; Neurotransmitter Agents - metabolism; neurotrophic; Norepinephrine - metabolism; parasympathetic; Peripheral nervous system. Autonomic nervous system. Neuromuscular transmission. Ganglionic transmission. Electric organ; Rats; Rats, Wistar; steroid; Testosterone - metabolism; Testosterone - pharmacology; Tyrosine 3-Monooxygenase - metabolism; urogenital; Vasoactive Intestinal Peptide - metabolism; Vertebrates: nervous system and sense organs; neurotrophic; androgen; neuropeptide; HEPES, N-(2-hydroxyethyl)piperazine- N′-(2-ethanesulphonic acid); NGF, nerve growth factor; ChAT, choline acetyltransferase; NPY, neuropeptide Y; VIP, vasoactive intestinal peptide; urogenital; ER, oestrogen receptor; PBS, phosphate-buffered saline; parasympathetic; TH, tyrosine hydroxylase; EDTA, ethylenediaminetetraacetate; steroid; Androgen; Rat; Rodentia; Nerve growth factor; Gene expression; In vitro; Neuropeptide; Testosterone; Vertebrata; Mammalia; Pelvic ganglion; Neurotransmitter; Testicular hormone; Sex steroid hormone; Parasympathetic nervous system
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/S0306-4522(01)00420-1

Circulating testosterone has potent effects on the structure and function of many pelvic ganglion cells in adult rats in vivo. However not all androgen-sensitive pelvic neurones possess androgen receptors and testosterone effects may therefore be indirect, by an action on the target organs. Here we have examined if testosterone influences neuronal structure in vitro in pelvic ganglion cells cultured from adult male rats. We have also used multiple label immunofluorescence to monitor the expression of transmitter-synthesising enzymes and peptides under various culture conditions. Testosterone was a more potent stimulant of noradrenergic soma growth in culture than nerve growth factor. Whereas nerve growth factor increased the number, branching and length of neurites, testosterone stimulated growth of a small number of very short processes, each of which bore numerous short protrusions. Testosterone also impeded the longer neurite growth induced by nerve growth factor. Many pelvic ganglion cells altered their expression of transmitters/neuropeptides under different culture conditions. In particular, under control conditions or during nerve growth factor treatment, vasoactive intestinal peptide was up-regulated in noradrenergic and cholinergic neurones; testosterone impeded this up-regulation in noradrenergic neurones. Choline acetyltransferase immunoreactivity could only be visualised when nerve growth factor was present in the cultures, and cholinergic neurones showed less neurite outgrowth than noradrenergic neurones under all culture conditions. Nerve growth factor did not stimulate levels of this enzyme as strongly if testosterone was present. This study has shown that testosterone has potent effects on the structure of many pelvic ganglion cells in vitro. It is possible that these effects are mediated indirectly, e.g. by stimulating glial-derived substances, however our results suggest that the effects are not mediated by nerve growth factor. The results also show that testosterone influences some of the actions of nerve growth factor, suggesting that there may be complex interactions between steroid signalling and neurotrophic factors in maintaining neuronal structure and function in vivo.