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PMID: 1280832 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies.

Verge VM, Xu Z, Xu XJ, Wiesenfeld-Hallin Z, Hökfelt T

Abstract

Using in situ hybridization, we studied nitric oxide (NO) synthase (EC 1.14.23.-) mRNA in lumbar dorsal root ganglia after peripheral transection of the sciatic nerve in rats. The effect of the NO synthase inhibitor N omega-nitro-L-arginine methyl ester on the nociceptive flexor reflex was also studied in axotomized rats. Nerve section induced a dramatic increase in number of NO synthase mRNA-positive cells in the ipsilateral dorsal root ganglia. In some of these cells the peptides galanin and/or vasoactive intestinal polypeptide and/or neuropeptide Y were also strongly up-regulated. Intravenous administration of nitro-L-arginine methyl ester blocked spinal hyperexcitability at much lower dosages in axotomized than in normal animals. The results suggest involvement of NO in the function of lumbar sensory neurons, especially after axotomy, perhaps preferentially at peripheral sites.

MeSH Terms
Amino Acid Oxidoreductases/genetics Animals Ganglia, Spinal/enzymology Gene Expression In Situ Hybridization Male Nerve Regeneration Neuronal Plasticity Nitric Oxide/metabolism Nitric Oxide Synthase Peripheral Nerves/physiology RNA, Messenger/genetics Rats Rats, Sprague-Dawley Vasoactive Intestinal Peptide/genetics
Chemicals
RNA, Messenger Nitric Oxide Vasoactive Intestinal Peptide Nitric Oxide Synthase Amino Acid Oxidoreductases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Verge V M
Department of Histology and Neurobiology, Karolinska Institute, Stockholm, Sweden.
Xu Z
Xu X J
Wiesenfeld-Hallin Z
Hökfelt T
References (33)
33 references, click to expand
  1. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme.
    Proc Natl Acad Sci U S A. 1990 Jan;87(2):682-5 PMID: 1689048
  2. Neuronal NADPH diaphorase is a nitric oxide synthase.
    Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2811-4 PMID: 1707173
  3. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical.
    Circ Res. 1987 Dec;61(6):866-79 PMID: 2890446
  4. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase.
    Nature. 1991 Jun 27;351(6329):714-8 PMID: 1712077
  5. Biological roles of nitric oxide.
    Sci Am. 1992 May;266(5):68-71, 74-7 PMID: 1373517
  6. Increased neuropeptide Y (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy.
    Neurosci Lett. 1991 Apr 1;124(2):200-3 PMID: 1712437
  7. Localization of nitric oxide synthase indicating a neural role for nitric oxide.
    Nature. 1990 Oct 25;347(6295):768-70 PMID: 1700301
  8. Vasoactive intestinal polypeptide (VIP) increases in the spinal cord after peripheral axotomy of the sciatic nerve originate from primary afferent neurons.
    Brain Res. 1986 Apr 30;372(1):37-44 PMID: 3708358
  9. Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry.
    Histochemistry. 1992 Aug;98(1):39-49 PMID: 1429016
  10. Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide.
    Science. 1985 Sep 13;229(4718):1094-7 PMID: 2994212
  11. Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy.
    Neurosci Lett. 1987 Dec 29;83(3):217-20 PMID: 2450311
  12. Vasoactive intestinal peptide: a neurotrophic releasing agent and an astroglial mitogen.
    J Neurosci Res. 1990 Mar;25(3):386-94 PMID: 2325164
  13. Transferrin Receptor Expression and Iron Uptake in the Injured and Regenerating Rat Sciatic Nerve.
    Eur J Neurosci. 1991;3(10):919-927 PMID: 12106249
  14. Electrophysiological evidence for a role of nitric oxide in prolonged chemical nociception in the rat.
    Neuropharmacology. 1992 Mar;31(3):251-8 PMID: 1630593
  15. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine.
    Nature. 1980 Nov 27;288(5789):373-6 PMID: 6253831
  16. Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat.
    J Comp Neurol. 1991 Apr 15;306(3):382-92 PMID: 1864999
  17. Nucleotide sequence divergence and functional constraint in VIP precursor mRNA evolution between human and rat.
    FEBS Lett. 1985 Apr 8;183(1):55-9 PMID: 3838518
  18. Nitric oxide may act as a messenger between dorsal root ganglion neurones and their satellite cells.
    Neurosci Lett. 1992 Mar 16;137(1):29-32 PMID: 1378218
  19. Axoplasmic transport block reduces ectopic impulse generation in injured peripheral nerves.
    Pain. 1983 May;16(1):73-85 PMID: 6191267
  20. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum.
    Proc Natl Acad Sci U S A. 1989 Nov;86(22):9030-3 PMID: 2573074
  21. Histochemical mapping of nitric oxide synthase in the rat brain.
    Neuroscience. 1992;46(4):755-84 PMID: 1371855
  22. NMDA receptor activation induces nitric oxide synthesis from arginine in rat brain slices.
    Eur J Pharmacol. 1989 Oct 17;172(4-5):413-6 PMID: 2555211
  23. Ongoing activity in peripheral nerves: the physiology and pharmacology of impulses originating from a neuroma.
    Exp Neurol. 1974 Jun;43(3):580-93 PMID: 4827166
  24. Galanin-mediated control of pain: enhanced role after nerve injury.
    Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3334-7 PMID: 1373497
  25. The fine localization of dehydrogenases in the nervous system.
    Z Zellforch Microsk Anat Histochem. 1961;2:266-82 PMID: 13776456
  26. Structure and expression of the rat neuropeptide Y gene.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):2068-72 PMID: 3031663
  27. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor.
    Nature. 1987 Jun 11-17;327(6122):524-6 PMID: 3495737
  28. Muscle but not cutaneous C-afferent input produces prolonged increases in the excitability of the flexion reflex in the rat.
    J Physiol. 1984 Nov;356:443-58 PMID: 6520794
  29. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues.
    Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7797-801 PMID: 1715581
  30. Isolation and characterization of a complementary DNA (galanin) clone from estrogen-induced pituitary tumor messenger RNA.
    J Biol Chem. 1987 Dec 15;262(35):16755-8 PMID: 2445750
  31. Sensory afferent impulses originate from dorsal root ganglia as well as from the periphery in normal and nerve injured rats.
    Pain. 1983 Dec;17(4):321-39 PMID: 6664680
  32. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase.
    Neuron. 1991 Oct;7(4):615-24 PMID: 1718335
  33. Substance P: depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons.
    Brain Res. 1979 May 25;168(2):247-59 PMID: 221070
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1992-12-01
Pages
11617-21
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC50604
Subset
IM
Grants
PHS HHS · 43230 · United States
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