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Development of nNOS-positive preganglionic sympathetic neurons in the rat thoracic spinal cord

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Abstract

To gain a better understanding of the neuroplasticity of sympathetic neurons during postnatal ontogenesis, the distribution of neuronal nitric oxide synthase (nNOS) immunoreactivity was studied in sympathetic preganglionic neurons (SPN) in the spinal cord (Th2 segment) of female Wistar rats at different ages (newborn, 10-, 20-, 30-day-old; 2-, 6-month-old; 3-year-old). In all age groups, the majority of nNOS-immunoreactive (IR) neurons was observed in the nucleus intermediolateralis thoracolumbalis pars principalis. In the first month, the proportion of nNOS-IR neurons decreased significantly from 92 ± 3.4% in newborn to 55 ± 4.6% in 1-month-old, while the number of choline acetyltransferase (ChAT)-IR neurons increased from 74 ± 4.2% to 99 ± 0.3% respectively. Decreasing nNOS expression in the first 10 days of life was also confirmed by western blot analysis. Some nNOS-IR SPN also colocalized calbindin (CB) and cocaine and amphetamine-regulated transcript (CART). The percentage of NOS(+)/CB(−) SPN increased from 23 ± 3.6% in 10-day-old to 36 ± 4.2% in 2-month-old rats. Meanwhile, the proportion of NOS(+)/CART(−) neurons decreased from 82 ± 4.7% in newborn to 53 ± 6.1% in 1-month-old rats. The information provided here will also serve as a basis for future studies investigating the mechanisms of autonomic neuron development.

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References

  • Alkadhi KA, Alzoubi KH, Aleisa AM (2005) Plasticity of synaptic transmission in autonomic ganglia. Prog Neurobiol 75:83–108

    Article  CAS  Google Scholar 

  • Anderson CR (1992) NADPH diaphorase-positive neurons in the rat spinal cord include a subpopulation of autonomic preganglionic neurons. Neurosci Lett 139:280–284

    Article  CAS  Google Scholar 

  • Andressen C, Blumcke I, Celio MR (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181–208

    Article  CAS  Google Scholar 

  • Barber RP, Phelps PE, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1984) The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J Comp Neurol 229:329–346

    Article  CAS  Google Scholar 

  • Cossenza M, Socodato R, Portugal CC, Domith IC, Gladulich LF, Encarnação TG, Calaza KC, Mendonça HR, Campello-Costa P, Paes-de-Carvalho R (2014) Nitric oxide in the nervous system: biochemical, developmental, and neurobiological aspects. Vitam Horm 96:79–125

    Article  CAS  Google Scholar 

  • Dawson TM, Dawson VL (2018) Nitric oxide signaling in neurodegeneration and cell death. Adv Pharmacol 82:57–83

    Article  Google Scholar 

  • Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Synder SH (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci U S A 88:7797–7801

    Article  CAS  Google Scholar 

  • Dun NJ, Dun SL, Kwok EH, Yang J, Chang J (2000) Cocaine- and amphetamine-regulated transcript immunoreactivity in the rat sympathoadrenal axis. Neurosci Lett 283:97–100

    Article  CAS  Google Scholar 

  • Emanuilov AI, Korzina MB, Archakova LI, Novakovskaya SA, Nozdrachev AD, Masliukov PM (2008) Development of the NADPH-diaphorase-positive neurons in the sympathetic ganglia. Ann Anat 190:516–524

    Article  Google Scholar 

  • Fenwick NM, Martin CL, Llewellyn-Smith IJ (2006) Immunoreactivity for cocaine- and amphetamine-regulated transcript in rat sympathetic preganglionic neurons projecting to sympathetic ganglia and the adrenal medulla. J Comp Neurol 495:422–433

    Article  CAS  Google Scholar 

  • Gallo EF, Iadecola C (2011) Neuronal nitric oxide contributes to neuroplasticity-associated protein expression through cGMP, protein kinase G, and extracellular signal-regulated kinase. J Neurosci 31:6947–6955

    Article  CAS  Google Scholar 

  • Gardette R, Listerud MD, Brussaard AB, Role LW (1991) Developmental changes in transmitter sensitivity and synaptic transmission in embryonic chicken sympathetic neurons innervated in vitro. Dev Biol 147:83–95

    Article  CAS  Google Scholar 

  • Gibbs SM (2003) Regulation of neuronal proliferation and differentiation by nitric oxide. Mol Neurobiol 27:107–120

    Article  CAS  Google Scholar 

  • Godfrey EW, Schwarte RC (2010) Nitric oxide and cyclic GMP regulate early events in agrin signaling in skeletal muscle cells. Exp Cell Res 316:1935–1945

    Article  CAS  Google Scholar 

  • Gonsalvez DG, Kerman IA, McAllen RM, Anderson CR (2010) Chemical coding for cardiovascular sympathetic preganglionic neurons in rats. J Neurosci 30:11781–11191

    Article  CAS  Google Scholar 

  • Grkovic I, Anderson CR (1997) Calbindin D28K-immunoreactivity identifies distinct subpopulations of sympathetic pre- and postganglionic neurons in the rat. J Comp Neurol 386:245–259

    Article  CAS  Google Scholar 

  • Heiman MG, Shaham S (2010) Twigs into branches: how a filopodium becomes a dendrite. Curr Opin Neurobiol 20:86–91

    Article  CAS  Google Scholar 

  • Judas M, Sestan N, Kostović I (1999) Nitrinergic neurons in the develo** and adult human telencephalon: transient and permanent patterns of expression in comparison to other mammals. Microsc Res Tech 45:401–419

    Article  CAS  Google Scholar 

  • Masliukov PM, Fateev MM, Nozdrachev AD (2000) Age-dependent changes of electrophysiologic characteristics of the stellate ganglion conducting pathways in kittens. Auton Neurosci 83:12–18

    Article  CAS  Google Scholar 

  • Masliukov PM, Korobkin AA, Nozdrachev AD, Timmermans JP (2012) Calbindin-D28k immunoreactivity in sympathetic ganglionic neurons during development. Auton Neurosci 167:27–33

    Article  CAS  Google Scholar 

  • Masliukov PM, Emanuilov AI, Madalieva LV, Moiseev KY, Bulibin AV, Korzina MB, Porseva VV, Korobkin AA, Smirnova VP (2014) Development of nNOS-positive neurons in the rat sensory and sympathetic ganglia. Neuroscience 256:271–281

    Article  CAS  Google Scholar 

  • Masliukov PM, Emanuilov AI, Moiseev K, Nozdrachev AD, Dobrotvorskaya S, Timmermans JP (2015) Development of non-catecholaminergic sympathetic neurons in para- and prevertebral ganglia of cats. Int J Dev Neurosci 40:76–84

    Article  CAS  Google Scholar 

  • Masliukov PM, Emanuilov AI, Nozdrachev AD (2016) Developmental changes of neurotransmitter properties in sympathetic neurons. Adv Gerontol 29:442–453

    CAS  PubMed  Google Scholar 

  • Masliukov PM, Moiseev K, Budnik AF, Nozdrachev AD, Timmermans JP (2017) Development of calbindin- and calretinin-immunopositive neurons in the enteric ganglia of rats. Cell Mol Neurobiol 37:1257–1267

    Article  CAS  Google Scholar 

  • Meller ST, Gebhart GF (1993) Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52:127–136

    Article  CAS  Google Scholar 

  • Mukhutdinova KA, Kasimov MR, Giniatullin AR, Zakyrjanova GF, Petrov AM (2018) 24S-hydroxycholesterol suppresses neuromuscular transmission in SOD1(G93A) mice: a possible role of NO and lipid rafts. Mol Cell Neurosci 88:308–318

    Article  CAS  Google Scholar 

  • Nikonenko I, Jourdain P, Muller D (2003) Presynaptic remodeling contributes to activity-dependent synaptogenesis. J Neurosci 23:8498–8505

    Article  CAS  Google Scholar 

  • Patel BA, Dai X, Burda JE, Zhao H, Swain GM, Galligan JJ, Bian X (2010) Inhibitory neuromuscular transmission to ileal longitudinal muscle predominates in neonatal guinea pigs. Neurogastroenterol Motil 22:909–918

    Article  CAS  Google Scholar 

  • Petho G, Reeh PW (2012) Sensory and signaling mechanisms of bradykinin eicosanoids platelet-activating factor and nitric oxide in peripheral nociceptors. Physiol Rev 92:1699–1775

    Article  CAS  Google Scholar 

  • Phelps PE, Barber RP, Vaughn JE (1991) Embryonic development of choline acetyltransferase in thoracic spinal motor neurons: somatic and autonomic neurons may be derived from a common cellular group. J Comp Neurol 307:77–86

    Article  CAS  Google Scholar 

  • Porseva VV, Shilkin VV, Strelkov AA, Masliukov PM (2014) Subpopulation of calbindin-immunoreactive interneurons in the dorsal horn of the mice spinal cord. Tsitologiia 56:612–618

    CAS  PubMed  Google Scholar 

  • Porseva VV, Shilkin VV, Krasnov IB, Masliukov PM (2015) Calbindin-D28k immunoreactivity in the mice thoracic spinal cord after space flight. Int J Astrobiol 14:555–562

    Article  CAS  Google Scholar 

  • Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64:51–68

    Article  CAS  Google Scholar 

  • Pyner S, Coote JH (1994) A comparison between the adult rat and neonate rat of the architecture of sympathetic preganglionic neurones projecting to the superior cervical ganglion stellate ganglion and adrenal medulla. J Auton Nerv Syst 48:153–166

    Article  CAS  Google Scholar 

  • Rubin E (1985) Development of the rat superior cervical ganglion: initial stages of synapse formation. J Neurosci 5:697–704

    Article  CAS  Google Scholar 

  • Sanchez-Islas E, Leon-Olea M (2004) Nitric oxide synthase inhibition during synaptic maturation decreases synapsin I immunoreactivity in rat brain. Nitric Oxide 10:141–149

    Article  CAS  Google Scholar 

  • Schmidt HHHW, Gagne GD, Nakane M, Pollock JS, Miller MF, Murad F (1992) Map** of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclases and novel paraneural functions for nitrinergic signal transduction. J Histochem Cytochem 40:1439–1456

    Article  CAS  Google Scholar 

  • Scruggs P, Lai CC, Scruggs JE, Dun NJ (2005) Cocaine- and amphetamine-regulated transcript peptide potentiates spinal glutamatergic sympathoexcitation in anesthetized rats. Regul Pept 127:79–85

    Article  CAS  Google Scholar 

  • Schwaller B (2012) The use of transgenic mouse models to reveal the functions of Ca2+ buffer proteins in excitable cells. Biochim Biophys Acta 1820:1294–1303

    Article  CAS  Google Scholar 

  • Siechen S, Yang S, Chiba A, Saif T (2009) Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals. Proc Natl Acad Sci U S A 106:12611–12616

    Article  CAS  Google Scholar 

  • Smolen A, Raisman G (1980) Synapse formation in the rat superior cervical ganglion during normal development and after neonatal deafferentation. Brain Res 787:315–323

    Article  Google Scholar 

  • Snyder SH (1992) Nitric oxide: first in a new class of neurotransmitters. Science 257:494–496

    Article  CAS  Google Scholar 

  • Southam E, Charles SL, Garthwaite J (1996) The nitric oxide-cyclic GMP pathway and synaptic plasticity in the rat superior cervical ganglion. Br J Pharmacol 119:527–532

    Article  CAS  Google Scholar 

  • Wetts R, Vaughn JE (1994) Choline acetyltransferase and NADPH diaphorase are co-expressed in rat spinal cord neurons. Neuroscience 63:1117–1124

    Article  CAS  Google Scholar 

  • Wetts R, Phelps PE, Vaughn JE (1995) Transient and continuous expression of NADPH diaphorase in different neuronal populations of develo** rat spinal cord. Dev Dyn 202:215–228

    Article  CAS  Google Scholar 

  • Yakovleva OV, Shafigullin MU, Sitdikova GF (2013) The role of nitric oxide in the regulation of neurotransmitter release and processes of exo- and endocytosis of synaptic vesicles in mouse motor nerve endings. Neurochem J 7:103–110

    Article  CAS  Google Scholar 

  • Young HM, Cane KN, Anderson CR (2011) Development of the autonomic nervous system: a comparative view. Auton Neurosci 165:10–27

    Article  CAS  Google Scholar 

  • Zhang P, Yu PC, Tsang AH, Chen Y, Fu AK, Fu WY, Chung KK, Ip NY (2010) S-nitrosylation of cyclin-dependent kinase 5 (cdk5) regulates its kinase activity and dendrite growth during neuronal development. J Neurosci 30:14366–14370

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the RFBR (N 16-04-00538) grant.

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Authors and Affiliations

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

    Konstantin Y. Moiseev & Petr M. Masliukov

  2. Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences, St. Petersburg, Russia

    Irina V. Romanova

  3. I.M. Sechenov First Moscow State Medical University, Moscow, Russia

    Andrey P. Masliukov

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  1. Konstantin Y. Moiseev
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  2. Irina V. Romanova
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  3. Andrey P. Masliukov
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  4. Petr M. Masliukov
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Correspondence to Petr M. Masliukov.

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All animal procedures were approved by the Institutional Animal Care and Use Committee of the Yaroslavl State Medical University and were conducted in accordance with the “Guide for the Care and Use of Laboratory Animals” (NIH Publication No. 85–23, revised 1996) as well as the relevant Guidelines of the Russian Ministry of Health for scientific experimentation on animals.

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Moiseev, K.Y., Romanova, I.V., Masliukov, A.P. et al. Development of nNOS-positive preganglionic sympathetic neurons in the rat thoracic spinal cord. Cell Tissue Res 375, 345–357 (2019). https://doi.org/10.1007/s00441-018-2925-8

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  • DOI: https://doi.org/10.1007/s00441-018-2925-8

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