Developing Neonatal Rat Sympathetic and Sensory Neurons Differ in Their Regulation of 5-HT3 Receptor Expression

Overview

Journal J Neurosci

Specialty Neurology

Date 1997 Sep 1

PMID 9254675

Citations 8

Authors

M Rosenberg

B Pie

E Cooper

Affiliations

Soon will be listed here.

Abstract

Serotonin 5-HT3 receptors (5-HT3Rs) are ligand-gated ion channels expressed by many peripheral neurons and are involved in several physiological processes. To learn more about the developmental regulation of 5-HT3R expression, we investigated rat sympathetic and vagal sensory neurons. We found that sympathetic and sensory neurons differ in their regulation of 5-HT3R expression during early postnatal life and as these neurons develop in culture. In SCG neurons 5-HT3R transcript levels are low at postnatal day 1 (P1) and increase 7.5-fold by P21; this increase occurs even after elimination of preganglionic innervation. In comparison, 5-HT3R mRNA levels in P1 nodose neurons are over 14-fold greater than in P1 SCG and change little by P21. We show that 5-HT3R transcript levels in nodose neurons depend on intact target innervation and drop by 60% after axotomy. When P1 SCG neurons develop in culture, we observed a significant increase in 5-HT3R expression: after 7 d in culture, transcript levels increase ninefold versus a threefold increase for neurons developing for 7 d in vivo. In contrast, 5-HT3R mRNA levels in cultured nodose neurons drop by 70% within 24 hr; however, this drop is transient. After 2 d, transcript levels begin to increase, and after 7 d, they are above initial values. We show that this delayed increase in 5-HT3R expression depends on neurotrophins. In both nodose and sympathetic neurons we found that the changes in 5-HT3R gene expression correlate directly with the appearance of 5-HT-evoked current densities.

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References

De Koninck P, Carbonetto S, Cooper E . NGF induces neonatal rat sensory neurons to extend dendrites in culture after removal of satellite cells. J Neurosci. 1993; 13(2):577-85. PMC: 6576645. View

Greenshaw A . Behavioural pharmacology of 5-HT3 receptor antagonists: a critical update on therapeutic potential. Trends Pharmacol Sci. 1993; 14(7):265-70. DOI: 10.1016/0165-6147(93)90128-7. View

Hawrot E, Patterson P . Long-term culture of dissociated sympathetic neurons. Methods Enzymol. 1979; 58:574-84. DOI: 10.1016/s0076-6879(79)58174-9. View

McFarlane S, Cooper E . Postnatal development of voltage-gated K currents on rat sympathetic neurons. J Neurophysiol. 1992; 67(5):1291-300. DOI: 10.1152/jn.1992.67.5.1291. View

Smolen A, Raisman G . Synapse formation in the rat superior cervical ganglion during normal development and after neonatal deafferentation. Brain Res. 1980; 181(2):315-23. DOI: 10.1016/0006-8993(80)90615-0. View

De Koninck P, Cooper E . Differential regulation of neuronal nicotinic ACh receptor subunit genes in cultured neonatal rat sympathetic neurons: specific induction of alpha 7 by membrane depolarization through a Ca2+/calmodulin-dependent kinase pathway. J Neurosci. 1995; 15(12):7966-78. PMC: 6577970. View

Miquel M, Emerit M, Gingrich J, Nosjean A, Hamon M, El Mestikawy S . Developmental changes in the differential expression of two serotonin 5-HT3 receptor splice variants in the rat. J Neurochem. 1995; 65(2):475-83. DOI: 10.1046/j.1471-4159.1995.65020475.x. View

Yang J, Mathie A, Hille B . 5-HT3 receptor channels in dissociated rat superior cervical ganglion neurons. J Physiol. 1992; 448:237-56. PMC: 1176197. DOI: 10.1113/jphysiol.1992.sp019039. View

Jackson M, Yakel J . The 5-HT3 receptor channel. Annu Rev Physiol. 1995; 57:447-68. DOI: 10.1146/annurev.ph.57.030195.002311. View

10.

Krieg P, Melton D . In vitro RNA synthesis with SP6 RNA polymerase. Methods Enzymol. 1987; 155:397-415. DOI: 10.1016/0076-6879(87)55027-3. View

11.

Mandelzys A, Cooper E . Effects of ganglionic satellite cells and NGF on the expression of nicotinic acetylcholine currents by rat sensory neurons. J Neurophysiol. 1992; 67(5):1213-21. DOI: 10.1152/jn.1992.67.5.1213. View

12.

Mandelzys A, Pie B, Deneris E, Cooper E . The developmental increase in ACh current densities on rat sympathetic neurons correlates with changes in nicotinic ACh receptor alpha-subunit gene expression and occurs independent of innervation. J Neurosci. 1994; 14(4):2357-64. PMC: 6577148. View

13.

Maricq A, Peterson A, Brake A, Myers R, Julius D . Primary structure and functional expression of the 5HT3 receptor, a serotonin-gated ion channel. Science. 1991; 254(5030):432-7. DOI: 10.1126/science.1718042. View

14.

Jacob M, Berg D . Effects of preganglionic denervation and postganglionic axotomy on acetylcholine receptors in the chick ciliary ganglion. J Cell Biol. 1987; 105(4):1847-54. PMC: 2114658. DOI: 10.1083/jcb.105.4.1847. View

15.

Litman P, Barg J, Rindzoonski L, Ginzburg I . Subcellular localization of tau mRNA in differentiating neuronal cell culture: implications for neuronal polarity. Neuron. 1993; 10(4):627-38. DOI: 10.1016/0896-6273(93)90165-n. View

16.

Heumann R, Lindholm D, Bandtlow C, Meyer M, Radeke M, Misko T . Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci U S A. 1987; 84(23):8735-9. PMC: 299621. DOI: 10.1073/pnas.84.23.8735. View

17.

Donoghue S, Garcia M, Jordan D, Spyer K . Identification and brain-stem projections of aortic baroreceptor afferent neurones in nodose ganglia of cats and rabbits. J Physiol. 1982; 322:337-52. PMC: 1249673. DOI: 10.1113/jphysiol.1982.sp014040. View

18.

Apud J . The 5-HT3 receptor in mammalian brain: a new target for the development of psychotropic drugs?. Neuropsychopharmacology. 1993; 8(2):117-30. DOI: 10.1038/npp.1993.13. View

19.

Herdegen T, Zimmermann M . Expression of c-Jun and JunD transcription factors represent specific changes in neuronal gene expression following axotomy. Prog Brain Res. 1994; 103:153-71. DOI: 10.1016/s0079-6123(08)61135-8. View

20.

Mandelzys A, De Koninck P, Cooper E . Agonist and toxin sensitivities of ACh-evoked currents on neurons expressing multiple nicotinic ACh receptor subunits. J Neurophysiol. 1995; 74(3):1212-21. DOI: 10.1152/jn.1995.74.3.1212. View