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Immunocytochemical properties of stellate ganglion neurons during early postnatal development

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Abstract

Neurotransmitter features in sympathetic neurons are subject to change during development. To better understand the neuroplasticity of sympathetic neurons during early postnatal ontogenesis, this study was set up to immunocytochemically investigate the development of the catecholaminergic, cholinergic, and peptidergic phenotypes in the stellate ganglion of mice and rats. The present study was performed on Wistar rats and Swiss mice of different ages (newborn, 10-day-old, 20-day-old, 30-day-old, and 60-day-old). To this end, double labeling for tyrosine hydroxylase (TH), choline acetyltransferase (ChAT), vasoactive intestinal (poly)peptide (VIP), neuropeptide Y (NPY), galanin (GAL), and somatostatin (SOM) was applied. The results obtained indicate that the majority of the neurons in the stellate ganglion of both species were TH-positive from birth onward and that a large part of these neurons also contained NPY. The percentage of neurons containing TH and NPY invariably increased with age up to 60 days postnatally. A smaller portion of the stellate ganglion neurons contained other types of neuropeptides and showed a distinct chronological pattern. The proportion of VIP- and ChAT-positive neurons was maximal in 10-day-old animals and then decreased up to 60 days of age, whereas the number of SOM-positive cells in rats significantly decreased from birth onward. In newborn rats, VIP-, ChAT- and SOM-positive neurons were largely TH-positive, while their proportions decreased in 10-day-old and older rats. Accordingly, the largest part of VIP-positive neurons also expressed SOM immunoreactivity at birth, after which the number of neurons containing both peptides diminished. The VIP- and SOM-positive cells did not contain NPY in any of the age groups studied. In rats up to 10 days of life, GAL-immunoreactive (-IR) neurons were scarce, after which their number increased to reach a maximal value in 30-day-old animals and then declined again. The SOM-reactive cells had the smallest size in all rats, while the largest neurons were those containing ChAT. In the mouse stellate ganglion, VIP- and ChAT-IR neurons were larger in comparison to NPY- and TH-IR cells. Our study further revealed some species differences: compared to mice the proportion of neurons containing TH and NPY was higher in rats at all ages under study. Furthermore, no GAL-immunostained neurons were found in mice and the number of SOM-positive cells in mice was limited compared to that observed in rats. In conclusion, the development of neurotransmitter composition is complete in rats and mice by their second month of life. At this age, the percentages of immunopositive cells have become similar to those reported in adult animals.

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References

  • Anderson R, Morris J, Gibbins IL (2001) Neurochemical differentiation of functionally distinct populations of autonomic neurons. J Comp Neurol 429:419–435

    Article  CAS  PubMed  Google Scholar 

  • Asmus SE, Parsons S, Landis SC (2000) Developmental changes in the transmitter properties of sympathetic neurons that innervate the periosteum. J Neurosci 20:1495–1504

    CAS  PubMed  Google Scholar 

  • Baetge G, Schneider KA, Gershon MD (1990) Development and persistence of catecholaminergic neurons in cultured explants of fetal murine vagus nerves and bowel. Development 110:689–701

    CAS  PubMed  Google Scholar 

  • Benarroch EE (1994) Neuropeptides in the sympathetic system: presence, plasticity, modulation and implication. Ann Neurol 36:6–13

    CAS  PubMed  Google Scholar 

  • Bolem P, Fuxe K (1970) Adrenergic and cholinergic nerve terminals in skeletal muscle vessels. Acta Physiol Scand 78:53–59

    Google Scholar 

  • Bulloch AGM (1987) Somatostatin enhances neurite outgrowth and electrical coupling of regenerating neurons in Helisoma. Brain Res 412:6–17

    Article  CAS  PubMed  Google Scholar 

  • Cochard P, Goldstein M, Black IB (1979) Initial development of the noradrenergic phenotype in autonomic neuroblasts of the rat embryo in vivo. Dev Biol 71:109–114

    Google Scholar 

  • Darland DC, Link BA, Nishi R (1995) Activin A and follistatin expression in developing targets of ciliary ganglion neurons suggests a role in regulating neurotransmitter phenotype. Neuron 15:857–866

    Article  CAS  PubMed  Google Scholar 

  • Ernsberger U, Rohrer H (1996) The development of the noradrenergic neurotransmitter phenotype in postganglionic sympathetic neurons. Neurochem Res 21:823–829

    CAS  PubMed  Google Scholar 

  • Ernsberger U, Rohrer H (1999) Development of the cholinergic neurotransmitter phenotype in postganglionic sympathetic neurons. Cell Tissue Res 297:339–361

    Article  CAS  PubMed  Google Scholar 

  • Gabella G (1976) Structure of the autonomic nervous system. Chapman and Hall, London

  • Garcia-Arraras JE, Torres-Avillan I (1999) Developmental expression of galanin-like immunoreactivity by members of the avian sympathoadrenal cell lineage. Cell Tissue Res 295:33–41

    Article  CAS  PubMed  Google Scholar 

  • Gibbins IL (1992) Vasoconstrictor, vasodilatator and pilomotor pathways in sympathetic ganglia of guinea-pigs. Neuroscience 47:657–672

    Article  CAS  PubMed  Google Scholar 

  • Girotti P, Bertorelli R, Fisone G, Land T, Langel Ü, Consolo S, Bartfai T (1993) N-terminal galanin fragments inhibit the hippocampal release of acetylcholine in vivo. Brain Res 612:258–262

    Article  CAS  PubMed  Google Scholar 

  • Goldhawk DE, Meakin SO, Verdi JM (2000) Subpopulations of rat B21 neuroblasts exhibit differential neurotrophin responsiveness during sympathetic development. Dev Biol 218:367–377

    Article  CAS  PubMed  Google Scholar 

  • Guidry G, Landis SC (2000) Absence of cholinergic sympathetic vasodilatation from limb muscle vasculature in rats and mice. Auton Neurosci 82:97–108

    Article  CAS  PubMed  Google Scholar 

  • Haddad C, Armour JA (1991) Ontogeny of canine intrathoracic cardiac nervous system. Am J Physiol 261:R920–R927

    CAS  PubMed  Google Scholar 

  • Heym C, Liu N, Gleich A, Oberst P, Kummer W (1993) Immunohistochemical evidence for different pathways immunoreactive to substance P and calcitonin gene-related peptide (CGRP) in the guinea-pig stellate ganglion. Cell Tissue Res 272:563–574

    CAS  PubMed  Google Scholar 

  • Jobling P, Gibbins IL (1999) Electrophysiological and morphological diversity of mouse sympathetic neurons. J Neurophysiol 82:2747–2764

    CAS  PubMed  Google Scholar 

  • Kessler JA, Adler JE, Black IB (1983) Substance P and somatostatin regulate sympathetic noradrenergic function. Science 221:1059–1061

    CAS  PubMed  Google Scholar 

  • Klimaschewski L, Tran TD, Nobling R, Heym C (1994) Plasticity of postganglionic sympathetic neurons in the rat superior cervical ganglion after axotomy. Microsc Res Tech 29:120–130

    CAS  PubMed  Google Scholar 

  • Klimaschewski L, Kummer W, Heym C (1996) Localization, regulation and function of neurotransmitters and neuromodulators in cervical sympathetic ganglia. Microsc Res Tech 35:44–68

    Article  CAS  PubMed  Google Scholar 

  • Landis SC (1988) Neurotransmitter plasticity in sympathetic neurons and its regulation by environmental factors in vitro and in vivo. In: Björklund A, Hökfelt T, Owman C (eds) Handbook of chemical neuroanatomy. The peripheral nervous system. Elsevier, Amsterdam, pp 65–115

  • Landis SC, Fredieu JR (1986) Coexistence of calcitonin gene-related peptide and vasoactive intestinal peptide in cholinergic sympathetic innervation of rat sweat glands. Brain Res 377:177–181

    Article  CAS  PubMed  Google Scholar 

  • Lindth B, Lundberg JM, Hökfelt T (1989) NPY-, galanin-, VIP/PHI-, CGRP- and substance P-immunoreactive neuronal subpopulations in cat autonomic and sensory ganglia and their projections. Cell Tissue Res 256:259–273

    PubMed  Google Scholar 

  • Lundberg JM, Hökfelt T, Schultzberg M, Uvnäs-Wallenstein K, Köhler C, Said SI (1979) Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat: evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience 4:1539–1559

    Article  CAS  PubMed  Google Scholar 

  • Masliukov PM (2001) Sympathetic neurons of the cat stellate ganglion in postnatal ontogenesis: morphometric analysis. Auton Neurosci 89:48–53

    Article  CAS  PubMed  Google Scholar 

  • Masliukov PM, Pankov VA, Strelkov AA, Masliukova EA, Shilkin VV, Nozdrachev AD (2000) Morphological features of neurons innervating different viscera in the cat stellate ganglion in postnatal ontogenesis. Auton Neurosci 84:169–175

    Article  CAS  PubMed  Google Scholar 

  • Masliukov PM, Shilkin VV, Nozdrachev AD, Timmermans JP (2003) Histochemical features of neurons in the cat stellate ganglion during postnatal ontogenesis. Auton Neourosci 106:84–90

    Article  CAS  Google Scholar 

  • Maxwell GD, Sietz PD, Chenard PH (1984) Development of somatostatin-like immunoreactivity in embryonic sympathetic ganglia. J Neurosci 4:576–584

    CAS  PubMed  Google Scholar 

  • Mohney RP, Siegel RE, Zigmond RE (1994) Galanin and vasoactive intestinal peptide messenger RNAs increase following axotomy of adult sympathetic neurons. J Neurobiol 25:108–118

    CAS  PubMed  Google Scholar 

  • Morales MA, Holmberg K, Xu ZQ, Cozzari C, Hartman BK, Emson P, Goldstein M, Elfvin LG, Hökfelt T (1995) Localization of choline acetyltransferase in rat peripheral sympathetic neurons and its coexistence with nitric oxide synthase and neuropeptides. Proc Natl Acad Sci U S A. 92:11819–11823

    Google Scholar 

  • Morris JL, Grasby DJ, Anderson RL, Gibbins IL (1998) Neurochemical distinction between skeletal muscle vasodilator neurons and pelvic vasodilator neurons in guinea-pigs. J Auton Nerv Syst 71:64–68

    Article  CAS  PubMed  Google Scholar 

  • Morris JL, Anderson RL, Gibbins IL (2001) Neuropeptide Y immunoreactivity in cutaneous sympathetic and sensory neurons during development of the guinea pig. J Comp Neurol 437:321–34

    Article  CAS  PubMed  Google Scholar 

  • Nordström Ö, Melander T, Hökfelt T, Bartfai T, Goldstein M (1987) Evidence for an inhibitory effect of the peptide galanin on dopamine release from the rat median eminence. Neurosci Lett 73:21–26

    Article  PubMed  Google Scholar 

  • Nozdrachev AD (1983) Physiology of the autonomic nervous system, 2nd edn (in Russian). Medizina, Leningrad

  • Phillips JG, Randel WC, Armour JA (1986) Functional anatomy of the major cardiac nerves in cats. Anat Rec 214:362–371

    Google Scholar 

  • Pincus DW, DiCicco-Bloom EM, Black IB (1990) Vasoactive intestinal peptide regulates mitosis, differentiation and survival of cultured sympathetic neuroblasts. Nature 343:564–567

    Article  CAS  PubMed  Google Scholar 

  • Pramanic A, Ögren SO (1993) Galanin stimulates striatal acetylcholine release via a mechanism unrelated to cholinergic receptor stimulation. Regul Pept 45:353–362

    Article  PubMed  Google Scholar 

  • Rao MS, Tyrrell S, Landis SC, Patterson PH (1992) Effects of ciliary neurotrophic factor (CNTF) and depolarization on neuropeptide expression in cultured sympathetic neurons. Dev Biol 150:281–293

    CAS  PubMed  Google Scholar 

  • Reimann W, Schneider F (1993) Galanin receptor activation attenuates norepinephrine release from rat spinal cord slices. Life Sci 52:PL251–PL254

    Article  CAS  PubMed  Google Scholar 

  • Rios R, Stolfi A, Campbell PH, Pickoff AS (1996) Postnatal development of the putative neuropeptide-Y-mediated sympathetic-parasympathetic autonomic interaction. Cardiovasc Res 31:E96–E03

    Article  PubMed  Google Scholar 

  • Roudenok V (2000) Changes in the expression of neuropeptide Y (NPY) during maturation of human sympathetic ganglionic neurons: correlations with tyrosine hydroxylase immunoreactivity. Ann Anat 182:515–519

    CAS  PubMed  Google Scholar 

  • Roudenok V, Kuhnel W (2001) Distribution of vasoactive intestinal polypeptide-, calcitonin gene-related peptide-, somatostatin- and neurofilament-immunoreactivities in sympathetic ganglia of human fetuses and premature neonates. Ann Anat 183:213–216

    CAS  PubMed  Google Scholar 

  • Schäfer MKH, Schütz B, Weihe E, Eiden LE (1997) Target-independent cholinergic differentiation in the rat sympathetic nervous system. Proc Natl Acad Sci U S A 94:4149–4154

    Article  PubMed  Google Scholar 

  • Smith J, Vyas S, Garcia-Arraras JE (1993) Selective modulation of cholinergic properties in cultures of avian embryonic sympathetic ganglia. J Neurosci Res 34:346–356

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by an RFBR grant N 04-04-48364 and an INTAS Fellowship Grant for Young Scientists (M.P.M.).

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Authors and Affiliations

  1. Department of Normal Physiology and Biophysics, Yaroslavl State Medical Academy, Revoliucionnaya 5, 150000, Yaroslavl, Russia

    Petr M. Masliukov

  2. Laboratory of Cell Biology and Histology, Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium

    Jean-Pierre Timmermans

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  1. Petr M. Masliukov
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  2. Jean-Pierre Timmermans
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Correspondence to Petr M. Masliukov.

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Masliukov, P.M., Timmermans, JP. Immunocytochemical properties of stellate ganglion neurons during early postnatal development. Histochem Cell Biol 122, 201–209 (2004). https://doi.org/10.1007/s00418-004-0692-y

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