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Expression of peptides, nitric oxide synthase and NPY receptor in trigeminal and nodose ganglia after nerve lesions

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Abstract

Using immunohistochemistry and in situ hybridization, the expression of galanin (GAL)/galanin message associated peptide (GMAP)-, neuropeptide Y (NPY)-, vasoactive intestinal polypeptide (VIP)/peptide histidine isoleucine (PHI)- and nitric oxide synthase (NOS)-like immunoreactivities and mRNAs, and NPY receptor mRNA was studied in normal trigeminal and nodose ganglia and 14 and 42 days after peripheral axotomy. In normal trigeminal ganglia about 11% of the counted neuron profiles contained GAL mRNA, 4% NOS mRNA, 5% NPY mRNA, 7% VIP mRNA, and 19% NPY receptor mRNA. Peptide mRNA- and NPY receptor mRNA-positive neuron profiles were small in size. Fourteen days after axotomy a marked increase in the number of GAL mRNA- (34% of counted neuron profiles), NPY mRNA- (54%) and VIP mRNA- (31%) positive neuron profiles, and a moderate increase in the number of NOS mRNA- (22%) positive neuron profiles were observed in the ipsilateral trigeminal ganglia. The GAL/GMAP, VIP- and NOS-positive profiles were mainly small, the NPY-positive ones mostly large. NPY receptor mRNA was expressed in some large neurons. In normal nodose ganglia, about 3% of the counted neuron profiles contained GAL mRNA, 3% NPY mRNA, 17% NOS mRNA and less than 1% VIP mRNA. Fourteen days after peripheral axotomy, a marked increase in the number of GAL mRNA- (78% of counted neuron profiles), NOS mRNA- (37%) and VIP- (46%) mRNA-positive neuron profiles was seen in the ipsilateral nodose ganglia. The number of NPY-positive (23%) neurons was moderately increased, mainly in small neuron profiles. There were no NPY receptor mRNA-positive neurons, either in normal nodose ganglia or in nodose ganglia ipsilateral to the axotomy. In contralateral nodose ganglia the number of GAL- and NPY-positive neuron profiles was slightly increased, and VIP cells showed a moderate increase. Immunohistochemical analysis revealed parallel changes in expression of peptides and NOS in both trigeminal and nodose ganglia, demonstrating that the changes in mRNA levels are translated into protein. Finally, although not quantified, similar upregulations of peptide and NOS mRNA levels were observed in both ganglia 42 days after nerve injury provided that regeneration was not allowed, suggesting that the changes are long lasting. The present results show that the effect of axotomy on peptide and NOS expression in the trigeminal and nodose ganglia is similar to that previously shown for lumbar dorsal root ganglia. However, no mRNA for the NPY Y1 receptor could be detected in the vagal system. In general the mechanism(s) for and the purpose(s) of the messenger regulation in response to axotomy may be similar in these different sensory systems (dorsal root, trigeminal and nodose ganglia).

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References

  • Aimi Y, Fujimura M, Vincent SR, Kimura H (1991) Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat. J Comp Neurol 306:382–392

    Google Scholar 

  • Bamber BA, Masters BA, Hoyle GW, Brinster RL, Palmiter RD (1994) Leukemia inhibitory factor induces neurotransmitter switching in transgenic mice. Proc Natl Acad Sci USA 91:7839–7843

    Google Scholar 

  • Banner LR, Patterson PH (1994) Major changes in the expression of the mRNAs for cholinergic differentiation factor/leukemia inhibitory factor and its receptor after injury to adult peripheral nerves and ganglia. Proc Natl Acad Sci USA 91:7109–7113

    Google Scholar 

  • Bredt DS, Hwang PH, Glatt C, Lowenstein C, Reed RR, Snyder SH (1991) Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 1991:714–718

    Google Scholar 

  • Ceccatelli S, Hulting A-L, Zhang X, Gustafsson L, Villar M, Hökfelt T (1993) Nitric oxide synthase in the rat anterior pituitary gland and the role of nitric oxide in regulation of luteinizing hormone secretion. Proc Natl Acad Sci USA 90:11292–11296

    Google Scholar 

  • Christensson-Nylander I, Herrera-Marschitz M, Staines W, Hökfelt T, Terenius L, Ungerstedt U, Cuello C, Oertel WH, Goldstein M (1986) Striato-nigral dynorphin and substance P pathways in the rat. Exp Brain Res 64:169–192

    Google Scholar 

  • Coons AH (1958) Fluorescent antibody methods. In: Danielli JF (ed) General cytochemical methods. Academic Press, New York, pp 399–422

    Google Scholar 

  • Dagerlind Å, Friberg K, Bean AJ, Hökfelt T (1992) Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry 98:39–49

    Google Scholar 

  • Eva C, Keinänen K, Monyer H, Seeburg P, Sprengel R (1990) Molecular cloning of a novel G protein-coupled receptor that may belong to the neuropeptide receptor family. FEBS Lett 271:81–84

    Google Scholar 

  • Fahrenkrug J, Pedersen JH (1984) Development and validation of a specific radioimmunoassay for PHI in plasma. Clin Chim Acta 143:183–192

    Google Scholar 

  • Fiallos-Estrada CE, Kummer W, Mayer B, Bravo R, Zimmermann M, Herdegen T (1993) Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and c-JUN co-expression in rat dorsal root ganglion neurons following sciatic nerve transection. Neurosci Lett 150:169–173

    Google Scholar 

  • Fitzgerald M, Wall PD, Goedert M, Emson PC (1985) Nerve growth factor counteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Res 332:131–141

    Google Scholar 

  • Freidin M, Kessler JA (1991) Cytokine regulation of substance P expression in sympathetic neurons. Proc Natl Acad Sci USA 88:3200–3203

    Google Scholar 

  • Fukada K (1985) Purification and partial characterization of a cholinergic neuronal differentiation factor. Proc Natl Acad Sci USA 82:8795–8799

    Google Scholar 

  • Grundy D (1992) Extrinsic reflex pathways in the upper gastrointestinal tract and their central processing. In: Holle GE, Wood JD (eds) Advances in the innervation of the gastrointestinal tract. Elsevier, Amsterdam, pp 539–545

    Google Scholar 

  • Heike CJ, Hill KM (1988) Immunohistochemical study of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat. Neuroscience 26:539–551

    Google Scholar 

  • Heike CJ, Niederer AJ (1990) Studies on the coexistence of substance P with other putative transmitters in the nodose and petrosal ganglia. Synapse 5:144–151

    Google Scholar 

  • Heike CJ, Rabchevsky A (1991) Axotomy alters putative neurotransmitters in visceral sensory neurons of the nodose and petrosal ganglia. Brain Res 551:44–51

    Google Scholar 

  • Herzog H, Hort YJ, Ball HJ, Hayes G, Shine J, Selbie LA (1992) Cloned human neuropeptide Y receptor couples to two different second messenger systems. Proc Natl Acad Sci USA 89:5794–5798

    Google Scholar 

  • Hökfelt T, Wiesenfeld-Hallin Z, Villar MJ, Melander T (1987) Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci Lett 83:217–220

    Google Scholar 

  • Hökfelt T, Åman K, Arvidsson U, Bedecs K, Ceccatelli S, Hulting A, Langel Ü, Meister B, Pieribone V, Bartfai T (1992) Galanin message-associated peptide (GMAP)- and galanin-like immunoreactivities: overlapping and differential distributions in Ihe rat Neurosci Lett 142:139–142

    Google Scholar 

  • Hökfelt T, Zhang X, Wiesenfeld-Hallin Z (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17:22–30

    Google Scholar 

  • Jessell T, Tsunoo A, Kanazawa I, Otsuka M (1979) Substance P: depletion in the dorsal horn of the rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain Res 168:247–259

    Google Scholar 

  • Johnson DG, de C Nougueira Araujo GM (1981) A simple method of reducing the fading of immunofluorescence during microscopy. J Immunol Methods 43:349–350

    Article  CAS  PubMed  Google Scholar 

  • Kashiba H, Senba E, Kawai Y, Ueda Y, Tohyama M (1992a) Axonal blockade induces the expression of vasoactive intestinal polypeptide and galanin in rat dorsal root ganglion neurons. Brain Res 577:19–28

    Google Scholar 

  • Kashiba H, Senba E, Ueda Y, Tohyama M (1992b) Co-localized but target-unrelated expression of vasoactive intestinal polypeptide and galanin in rat dorsal root ganglion neurons after peripheral nerve crush injury. Brain Res 582:47–57

    Google Scholar 

  • Katz DM, Black IB (1986) Expression and regulation of catecholaminergic traits in primary sensory neurons: relationship to target innervation in vivo. J Neurosci 6:983–989

    Google Scholar 

  • Katz DM, Karten HJ (1980) Substance P in the vagal sensory ganglia: localization in cell bodies and pericellular arborizations. J Comp Neurol 193:549–564

    Google Scholar 

  • Katz DM, Markey KA, Goldstein M, Black IB (1983) Expression of catecholaminergic characteristics by primary sensory neurons in the normal adult rat in vivo. Proc Natl Acad Sci USA 80:3526–3530

    Google Scholar 

  • Kessler JA, Black IB (1980) Nerve growth factor stimulates the development of substance P in sensory ganglia. Proc Natl Acad Sci USA 77:649–652

    Google Scholar 

  • Larhammar D, Ericsson A, Persson H (1987) Structure and expression of the rat neuropeptide Y gene. Proc Natl Acad Sci USA 84:2068–2072

    Google Scholar 

  • Larhammar D, Blomqvist AG, Yee F, Jazin E, Yoo H, Wahlestedt C (1992) Cloning and functional expression of a human neuropeptide Y/peptide YY receptor of the Y1 type. J Biol Chem 267:10935–10938

    Google Scholar 

  • Lindsay RM, Harmar AJ (1989) Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337:362–364

    Google Scholar 

  • Lindsay RM, Lockett C, Sternberg J, Winter J (1989) Neuropeptide expression in cultures of adult sensory neurons: modulation of substance P and calcitonin gene-related peptide levels by nerve growth factor. Neuroscience 33:53–65

    Google Scholar 

  • Lundberg JM, Hökfelt T, Nilsson G, Terenius L, Rehfeld J, Elde R, Said S (1978) Peptide neurons in the vagus, splanchnic and sciatic nerves. Acta Physiol Scand 104:499–501

    Google Scholar 

  • Mantyh PW, Hunt SP (1984) Neuropeptides are present in projection neurones at all levels in visceral and taste pathways: from periphery to sensory cortex. Brain Res 299:297–311

    Google Scholar 

  • McGregor GP, Gibson SJ, Sabate IM, Blank MA, Christofides ND, Wall PD, Polak JM, Bloom SR (1984) Effect of peripheral nerve section and nerve crush on spinal cord neuropeptides in the rat: increased VIP and PHI in the dorsal horn. Neuroscience 13:207–216

    Google Scholar 

  • Mulderry PK (1994) Neuropeptide expression by newborn and adult rat sensory neurons in culture: Effects of nerve growth factor and other neurotrophic factors. Neuroscience 59:673–688

    Google Scholar 

  • Nawa H, Patterson PH (1990) Separation and partial characterization of neuropeptide-inducing factors in heart cell conditioned medium. Neuron 4:269–277

    Google Scholar 

  • Nawa H, Nakanishi S, Patterson PH (1991) Recombinant cholinergic differentiation factor (leukemia inhibitory factor) regulates sympathetic neuron phenotype by alterations in the size and amounts of neuropeptide mRNAs. J Neurochem 56:2147–2150

    Google Scholar 

  • Nielsch V, Bisby MA, Keen P (1987) Effect of cutting or crushing the rat sciatic nerve on synthesis of substance P by isolated L5 dorsal root ganglia. Neuropeptides 10:137–145

    Google Scholar 

  • Nishizawa M, Hayakawa Y, Yanaihara N, Okamoto H (1985) Nucleotide sequence divergence and functional constraint in VIP precursor mRNA evolution between human and rat. FEBS Lett 183:55–59

    Google Scholar 

  • Noguchi K, Senba E, Morita Y, Sato M, Tohyama M (1989) Prepro-VIP preprotachykinin mRNAs in the rat dorsal root ganglion cells following peripheral axotomy. Mol Brain Res 6:327–330

    Google Scholar 

  • Noguchi K, De Leon M, Nahin RL, Senba E, Ruda MA (1993) Quantification of axotomy-induced alteration of neuropeptide mRNAs in dorsal root ganglion neurons with special reference to neuropeptide Y mRNA and the effects of neonatal capsaicin treatment. J Neurosci 35:54–66

    Google Scholar 

  • Noguchi K, Dubner R, DeLeon M, Senba E, Ruda MA (1994) Axotomy induces preprotachykinin gene expression in a subpopulation of dorsal root ganglion neurons. J Neurosci Res 37:596–603

    Google Scholar 

  • Noguchi K, Kawai Y, Fukuoka T, Senba E, Miki K (1995) Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effects on dorsal column nucleus neurons. J Neurosci 15:7633–7643

    Google Scholar 

  • Otten U, Goedert M, Mayer N, Lembeck F (1980) Requirement of nerve growth factor for development of substance P-containing sensory neurons. Nature 287:158–159

    Google Scholar 

  • Paintal AS (1973) Vagal sensory receptors and their reflex effects. Physiol Rev 53:159–227

    Google Scholar 

  • Patterson PH (1994) Leukemia inhibitory factor, a cytokine at the interface between neurobiology and immunology. Proc Natl Acad Sci USA 91:7833–7835

    Google Scholar 

  • Pease PC (1962) Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat Rec 142:342

    Google Scholar 

  • Platt JL, Michael AF (1983) Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J Histochem Cytochem 31:840–842

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rao MS, Sun Y, Escary JL, Perreau J, Tresser S, Patterson PH, Zigmond RE, Brulet P, Landis SC (1993) Leukemia inhibitory factor mediates an injury response but not a target-directed developmental transmitter switch in sympathetic neurons. Neuron 11:1175–1185

    Google Scholar 

  • Riveros-Moreno V, Beddell C, Moncada S (1993) Nitric oxide synthase. Structural studies using anti-peptide antibodies. Eur J Biochem 215:801–808

    Google Scholar 

  • Schalling M (1990) In situ hybridization studies on regulatory molecules in neural and endocrine tissue with special reference to expression of coexisting peptides: Karolinska Institute, Stockholm

    Google Scholar 

  • Shadiack AM, Hart RP, Carlson C, Jonakait GM (1993) Interleukin-1 induces substance P in sympathetic ganglia through the induction of leukemia inhibitory factor. J Neurosci 13:2601–2609

    Google Scholar 

  • Shehab SAS, Atkinson ME (1984) Sciatic nerve section has variable effects on primary afferent neuropeptides. J Anat 139:725

    Google Scholar 

  • Shehab SAS, Atkinson ME (1986a) Vasoactive intestinal polypeptide (VIP) increases in the spinal cord after peripheral axotomy of the sciatic nerve originate from primary afferent neurons. Brain Res 372:37–44

    Google Scholar 

  • Shehab SAS, Atkinson ME (1986b) Vasoactive intestinal polypeptide increases in areas of the dorsal horn of the spinal cord from which other neuropeptides are depleted following peripheral axotomy. Exp Brain Res 62:422–430

    Google Scholar 

  • Verge VMK, Xu Z, Xu X-J, Wiesenfeld-Hallin Z, Hökfelt T (1992) Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc Natl Acad Sci USA 89:11617–11621

    Google Scholar 

  • Verge VMK, Richardson PM, Wisenfeld-Hallin Z, Hökfelt T (1995) Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. J Neurosci 15:2081–2096

    Google Scholar 

  • Villar MJ, Cortes R, Theodorsson E, Wiesenfeld-Hallin Z, Schalling M, Fahrenkrug J, Emson PC, Hökfelt T (1989) Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33:587–604

    Google Scholar 

  • Villar MJ, Wiesenfeld-Hallin Z, Xu XJ, Theodorsson E, Emson PC, Hökfelt T (1991) Further studies on galanin-, substance P, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord: effects of dorsal rhizotomies and sciatic nerve lesions. Exp Neurol 112:29–39

    Google Scholar 

  • Vrontakis ME, Peden LM, Duckworth ML, Friesen HG (1987) Isolation and characterization of a complementary DNA (galanin) clone from estrogen-induced pituitary tumor messenger RNA. J Biol Chem 262:16755–16758

    Google Scholar 

  • Wakisaka S, Kajander KC, Bennett GJ (1991) Increased neuropeptide (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci Lett 124:200–203

    Google Scholar 

  • Wakisaka S, Kajander KC, Bennett GJ (1992) Effects of peripheral nerve injuries and tissue inflammation on the levels of neuropeptide Y-like immunoreactivity in rat primary afferent neurons. Brain Res 598:349–352

    Google Scholar 

  • Wakisaka S, Takikita S, Sasaki Y, Kato J, Tabata MJ, Kurisu K (1993) Cell size-specific appearance of neuropeptide Y in the trigeminal ganglion following peripheral axotomy of different branches of the mandibular nerve of the rat. Brain Res 620:347–350

    Google Scholar 

  • Wank SA, Pisegna JR, Weerth AD (1992) Brain and gastrointestinal cholecystokinin receptor family: structure and functional expression. Proc Natl Acad Sci USA 89:8691–8695

    Google Scholar 

  • Wiesenfeld-Hallin Z, Bartfai T, Hökfelt T (1992) Galanin in sensory neurons in the spinal cord. Front Neuroendocrinol 13:319–343

    Google Scholar 

  • Xu X-J, Wiesenfeld-Hallin Z, Villar MJ, Fahrenkrug J, Hökfelt T (1990) On the role of galanin, substance P and other neuropeptides in primary sensory neurons of the rat: studies on spinal reflex excitability and peripheral axotomy. Eur J Neurosci 2:733–743

    Google Scholar 

  • Yamamori T, Fukada K, Aebersold R, Korsching S, Fann MJ, Patterson PH (1989) The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science 246:1412–1416

    Google Scholar 

  • Young IWS (1990) In situ hybridization histochemistry. In: Björklund A, Hökfelt T, Wouterlood FG, van den Pool AN (eds) Handbook of chemical neuroanatomy, vol 8, Analysis of neuronal microcircuits and synaptic interactions. Elsevier, Amsterdam, pp 481–512

    Google Scholar 

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

    Google Scholar 

  • Zhang X, Dagerlind Å, Elde RP, Castel M-N, Broberger C, Wiesenfeld-Halin Z, Hökfelt T (1993a) Marked increase in cholecystokinin B receptor messenger RNA levels in rat dorsal root ganglia after peripheral axotomy. Neuroscience 57:227–233

    Google Scholar 

  • Zhang X, Meister B, Elde R, Verge VMK, Terenius L, Hökfelt T (1993b) Large calibre primary afferent neurons projecting to the gracile nucleus express neuropeptide Y after sciatic nerve lesions: an immunohistochemical and in situ hybridization study in rats. Eur J Neurosci 5:1510–1519

    Google Scholar 

  • Zhang X, Verge V, Wiesenfeld-Hallin Z, Ju G, Bredt D, Snyder SH, Hökfelt T (1993c) Nitric oxid synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J Comp Neurol 335:563–575

    Google Scholar 

  • Zhang X, Wiesenfeld-Hallin Z, Hökfelt T (1994) Effect of peripheral axotomy on expression of neuropeptide Y (Y1) receptor mRNA in rat lumbar dorsal root ganglia. Eur J Neurosci, 6:43–57

    Google Scholar 

  • Zhang Q, Ji R-R, Lindsay R, Hökfelt T (1995a) Effect of growth factors on substance P mRNA expression in axotomized dorsal root ganglia. Neuroreport 6:1309–1312

    Google Scholar 

  • Zhang Q, Ji R-R, Zhang Y-T, Sundler F, Hannibal J, Fahrenkrug J, Hökfelt T (1995b) Expression of pituitary adenylate cyclaseactivating polypeptide in dorsal root ganglia following axotomy: time course and coexistence. Brain Res 705:149–158

    Google Scholar 

  • Zhang X, Bean AJ, Wiesenfeld-Hallin Z, Xu X-J, Hökfelt T (1995c) Ultrastructural studies on peptides in the dorsal horn of the rat spinal cord. III. Effects of peripheral axotomy with special reference to galanin. Neuroscience 64:893–915

    Google Scholar 

  • Zhuo H, Lewin AC, Phillips ET, Sinclair CM, Heike CJ (1995) Inhibition of axoplasmic transport in the rat vagus nerve alters the numbers of neuropeptide and tyrosine hydroxylase messenger RNA-containing and immunoreactive visceral afferent neurons of the nodose ganglion. Neuroscience 66:175–187

    Google Scholar 

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Authors and Affiliations

  1. Department of Neuroscience/Histology, Karolinska Institute, Box 60400, S-17177, Stockholm, Sweden

    Xu Zhang, Ru-Rong Ji, Jan Arvidsson & Tomas Hökfelt

  2. Department of Pharmacology, Karolinska Institute, Stockholm, Sweden

    Jan M. Lundberg

  3. Department of Neurochemistry and Neurotoxicology, Stockholm University, Stockholm, Sweden

    Tamas Bartfai & Katarina Bedecs

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  1. Xu Zhang
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  2. Ru-Rong Ji
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  3. Jan Arvidsson
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During the final part of this study Dr. Jan Arvidsson tragically died from a cerebral insult.

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Zhang, X., Ji, RR., Arvidsson, J. et al. Expression of peptides, nitric oxide synthase and NPY receptor in trigeminal and nodose ganglia after nerve lesions. Exp Brain Res 111, 393–404 (1996). https://doi.org/10.1007/BF00228728

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