Localization and age-related changes of nitric oxide- and ANP-mediated cyclic-GMP synthesis in rat cervical spinal cord: An immunocytochemical study

Brain Research

Volumn 857, Issue 1-2, 2000, Pages 219-234

  Vles, J S H ^a   De Louw, A J ^a   Steinbusch, H ^a   Markerink Van Ittersum, M ^b   Steinbusch, H W M ^b   Blanco, C E ^a   Axer, H ^c   Troost, J ^a   De Vente, J ^b  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Acetylcholine; cGMP; Colocalization; GABA; Nitric oxide; Rat; Spinal cord

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ATRIAL NATRIURETIC FACTOR; CYCLIC GMP; GLUTAMATE TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITROPRUSSIDE SODIUM; PARVALBUMIN; SEROTONIN; TYROSINE 3 MONOOXYGENASE;

AGE; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL MEMBRANE; CERVICAL SPINAL CORD; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; GRAY MATTER; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; RAT; WHITE MATTER;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ATRIAL NATRIURETIC FACTOR; CERVICAL VERTEBRAE; CYCLIC GMP; NITRIC OXIDE; RATS; RATS, INBRED LEW; SPINAL CORD;

EID: 0033969896     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)02434-8     Document Type: Article

References (68)

1. 3H -D-aspartate in the dorsal horn of the rat spinal cord J. Comp. Neurol. 314:1991;114-124.
2. Bredt D.S., Glatt C.E., Hwang P.M., Fotuhi M., Dawson T.M., Snyder S.H. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of mammalian CNS together with NADPH diaphorase. Neuron. 7:1991;615-624.
3. Brüning G., Mayer B. Prenatal development of nitric oxide synthase in the mouse spinal cord. Neurosci. Lett. 202:1996;189-192.
4. Clowry G.J., McHanwell S. Expression of nitric oxide synthase by motor neurons in the spinal cord of the mutant mouse wobbler. Neurosci. Lett. 215:1996;177-180.
5. De Vente J., Hopkins D.A., Markerink-van Ittersum M., Emson P.C., Schmidt H.H.H.W., Steinbusch H.W.M. Distribution of nitric oxide synthase and nitric oxide-receptive, cyclic GMP-producing structures in the rat brain. Neuroscience. 87:1998;207-241.
6. De Vente J., Hopkins D.A., Markerink-van Ittersum M., Steinbusch H.W.M. Nitric oxide-mediated cGMP production in the islands of Calleja in the rat. Brain Res. 789:1998;175-178.
7. De Vente J., Manshanden C.G., Sikking R.A., Ramaekers F.C.S., Steinbusch H.W.M. A functional parameter to study heterogeneity of glial cells in rat brain slices: cyclic guanosine monophosphate production in atrial natriuretic factor (ANF)-responsive cells. Glia. 3:1990;43-54.
8. De Vente J., Steinbusch H.W.M. On the stimulation of soluble and particulate guanylate cyclase in the rat brain and the involvement of nitric oxide as studied by cGMP immunocytochemistry. Acta Histochem. 92:1992;13-38.
9. Dun N.J., Dun S.L., Förstermann U., Tseng L.F. Nitric oxide synthase immunoreactivity in rat spinal cord. Neurosci. Lett. 47:1992;217-220.
10. Dun N.J., Dun S.L., Wu S.Y., Förstermann U., Schmidt H.H.H.W., Tseng L.F. Nitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrelmonkey spinal cord. Neuroscience. 54:1993;845-857.
11. East S.J., Batchelor A.M., Garthwaite J. Selective blockade of N-methyl-D-aspartate receptor function by the nitric oxide donor, nitroprusside. Eur. J. Pharmacol. 209:1991;119-121.
12. Estevez A.G., Spear N., Thompson A.J., Cornwell T.L., Radi R., Barbeito L., Beckman J.S. Nitric oxide-dependent production of cGMP supports the survival of rat embryonic motor neurons cultured with brain-derived neurotrophic factor. J. Neurosci. 18:1998;3708-3714.
13. Ewer J., Truman J. Increases in cyclic 3′,5-guanosine monophosphate (cGMP) occur at ecdysis in an evolutionarily conserved crustacean cardioactive peptide-immunoreactive insect neuronal network. J. Comp. Neurol. 370:1996;330-341.
14. Feelisch M. The use of nitric oxide donors in pharmacological studies. N. S. Arch. Pharmacol. 358:1998;113-122.
15. Furuta A., Rothstein J.D., Martin L.J. Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J. Neurosci. 17:1997;8363-8375.
16. Garry M.G., Durnett Richardson J., Hargreaves K.M. Carrageenan-induced inflammation alters the content of i-cGMP and i-cAMP in the dorsal horn of the spinal cord. Brain Res. 646:1994;135-139.
17. Garthwaite J. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:1991;6-67.
18. Garthwaite J., Boulton C.L. Nitric oxide signalling in the central nervous system. Annu. Rev. Physiol. 57:1995;683-707.
19. Getting S.J., Segieth J., Ahmad S., Biggs C.S., Whitton P.S. Biphasic modulation of GABA release by nitric oxide in the hippocampus of freely moving rats in vivo. Brain Res. 717:1996;196-199.
20. Harteneck C., Koesling D., Söling A., Schulz G., Böhme E. Expression of soluble guanylyl cyclase catalytic activity requires two enzyme subunits. FEBS Lett. 272:1990;221-223.
21. Herbison A.E., Simonian S.X., Norris P.J., Emson P.C. Relationship of neuronal nitric oxide synthase immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J. Neuroendocrinol. 8:1996;73-82.
22. Hope B.T., Michael G.J., Knigge K.M., Vincent S.R. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl Acad. Sci. U.S.A. 88:1991;2811-2814.
23. Ichikawa T., Ajiki K., Matsuura J., Misawa H. Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: in situ hybridization histochemistry and immunohistochemistry. J. Chem. Neuroanat. 13:1997;23-39.
24. Ignarro L.J. Regulation of cytosolic guanylyl cyclase by porphyrins and metalloporphyrins. Adv. Pharmacol. 26:1994;35-65.
25. Inglis F.M., Furia F., Zuckerman K.E., Strittmatter S.M., Kalb R.G. The role of nitric oxide and NMDA receptors in the development of motor neuron dendrites. J. Neurosci. 18:1998;10493-10501.
26. Inoue T., Mashimo T., Shibata M., Shibuta S., Yoshiya I. Rapid development of nitric oxide-induced hyperalgesia depends on an alternate to the cGMP-mediated pathway in the rat neuropathic pain model. Brain Res. 792:1998;263-270.
27. Kalb R.G., Agostini J. Molecular evidence for nitric oxide-mediated motor neuron development. Neuroscience. 57:1993;1-8.
28. Kanda K. Expression of neuronal nitric oxide synthase in spinal motoneurons in aged rats. Neurosci. Lett. 219:1996;41-44.
29. Kurihara T., Yoshioka K. The excitatory and inhibitory modulation of primary afferent fibre-evoked responses of ventral roots in the neonatal rat spinal cord exerted by nitric oxide. Br. J. Pharmacol. 118:1996;1743-1753.
30. Laing I., Todd A.J., Heizmann C.W., Schmidt H.H.H.W. Subpopulations of GABAergic neurons in laminae I-III of rat spinal dorsal horn defined by coexistence with classical transmitters, peptides, nitric oxide synthase or parvalbumin. Neuroscience. 61:1994;123-132.
31. Liuzzi F.J., Wu W.T., Scofille S.A., Schinco F.P. Development of nitric oxide synthase expression in the superficial dorsal horn of the rat spinal cord. Exp. Neurol. 121:1993;275-278.
32. Malcangio M., Bowery N.G. GABA and its receptors in the spinal cord. Trends Pharmacol. Sci. 17:1996;457-462.
33. Mantyh C.R., Kruger L., Brecha N.C., Mantyh P.W. Localization of specific binding sites for atrial natriuretic factor in the central nervous system of rat, guinea, cat and human. Brain Res. 412:1987;329-342.
34. Markerink-van Ittersum M., Steinbusch H.W.M., De Vente J. Region-specific developmental patterns of atrial natriuretic factor- and nitric oxide-activated guanylyl cyclase in the postnatal frontal rat brain. Neuroscience. 78:1997;571-587.
35. Morris R., Southam E., Gittins S.R., De Vente J., Garthwaite J. The NO-cGMP pathway in neonatal rat dorsal horn. Eur. J. Neurosci. 6:1994;876-879.
36. Murad F. Regulation of cytosolic guanylyl cyclase by nitric oxide: the NO-cyclic GMP signal transduction system. Adv. Pharmacol. 26:1994;19-33.
37. Murad F., Mittal C.K., Arnold W.P., Katsuki S., Kimura H. Guanylate cyclase: activation by azide, nitro-compounds, nitric oxide, and hydroxyl radical and inhibition by hemoglobin and myoglobin. Adv. Cyclic Nucleotide Res. 9:1978;145-158.
38. Quirion R., Dalpé M., De Lean A., Gutkowska J., Cantin M., Genest J. Atrial natriuretic factor binding sites in brain and related structures. Peptides. 5:1984;1167-1172.
39. A receptor function in the rat cerebral cortex and cerebellar granule cells. Neuroscience. 74:1996;99-105.
40. Saito S., Kidd G.J., Trapp B.D., Dawson T.M., Bredt D.S., Wilson D.A., Traystman R.J., Snyder S.H., Hanley D.F. Rat spinal cord neurons contain nitric oxide synthase. Neuroscience. 59:1994;447-456.
41. Salter M., Strijbos P. The nitric oxide cyclic GMP pathway is required for nociceptive signalling at specific loci within the somatosensory pathway. Neuroscience. 73:1996;649-655.
42. Saper C.B., Hurley K.M., Moga M.M., Holmes H.R., Adams S.A., Leahy K.M., Needleman P. Brain natriuretic peptides: differential localization of a new family of neuropeptides. Neurosci. Lett. 96:1989;29-34.
43. Schmidt H.H.H.W. NO, CO and OH. Endogenous soluble guanylyl cyclase-activating factors. FEBS Lett. 307:1992;102-107.
44. Schmidt H.H.H.W., Gagne G.D., Nakane M., Pollock J.S., Miller M.F., Murad F. Mapping of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH-diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J. Histochem. Cytochem. 40:1992;1439-1456.
45. G-monomethyl-L-arginine, an inhibitor of nitric oxide synthase, increases extracellular GABA in the striatum of the freely moving rat. NeuroReport. 6:1995;1298-1300.
46. Shibuki K., Okada D. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature. 349:1991;326-328.
47. Shuttleworth C.W., Xue C., Ward S.M., De Vente J., Sanders K.M. Immunohistochemical localization of 3′,5-cyclic guanosine monophosphate in the canine proximal colon: responses to nitric oxide and electrical stimulation of enteric inhibitory neurons. Neuroscience. 56:1993;513-522.
48. J.B. Siegan, A.T. Hama, Alterations in rat spinal cord cGMP by peripheral nerve injury and adrenal medullary transplantation, Neurosci. Lett., 215, 49-52.
49. Simonnet G., Legendre M.A.P., Gabrion J., Vincent J.D. Characteristics and specific localization of receptors for atrial natriuretic peptides at non-neuronal cells in cultured mouse spinal cord cells. Neuroscience. 29:1989;189-199.
50. Sorg O., Horn T.F.W., Yu N., Gruol D.L., Bloom F.E. Inhibition of astrocyte glutamate uptake by reactive oxygen species: role of antioxydant enzymes. Mol. Med. 3:1997;431-440.
51. Southam E., Garthwaite J. Comparative effects of some nitric oxide donors on cyclic GMP levels in rat cerebellar slices. Neurosci. Lett. 130:1991;107-111.
52. Southam E., Garthwaite J. The nitric oxide-cyclic GMP signalling pathway in rat brain. Neuropharmacology. 32:1993;1267-1277.
53. Soyguder Z., Schmidt H.H.H.W., Morris R. Postnatal development of nitric oxide synthase type 1 expression in the lumbar spinal cord of the rat: a comparison with the induction of c-fos in response to peripheral application of mustard oil. Neurosci. Lett. 180:1994;188-192.
54. Spike R.C., Todd A.J., Johnston H.M. Coexistence of NADPH diaphorase with GABA, glycine, and acetylcholine in rat spinal cord. J. Comp. Neurol. 335:1993;320-333.
55. Tanaka J., Markerink-van Ittersum M., Steinbusch H.W.M., De Vente J. Nitric oxide-mediated cGMP synthesis in oligodendrocytes in the developing rat brain. Glia. 19:1997;286-297.
56. Tang F.R., Tan C.K., Ling E.A. The distribution of NADPH-d in the central grey region (laminaX) of rat upper thoracic spinal cord. J. Neurocytol. 24:1995;735-743.
57. Truman J.W., De Vente J., Ball E.E. Nitric oxide-sensitive guanylate cyclase is generally associated with the synaptogenesis phase of neuronal development in insects. Development. 122:1996;3949-3958.
58. Ueda S., Minamino N., Sudoh T., Kangawa K., Matsuo H. Regional distribution of immunoreactive brain natriuretic peptide in parcine brain and spinal cord. Biochem. Biophys. Res. Commun. 155:1988;733-739.
59. Valtschanoff J.G., Weinberg R.J., Rustioni A., Schmidt H.H.H.W. Nitric oxide synthase and GABA colocalize in lamina II of rat spinal cord. Neurosci. Lett. 148:1992;6-10.
60. Vincent S.R., Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience. 45:1992;755-784.
61. Vizzard M.A., Erdman S.L., Förstermann U., De Groat W.C. Ontogeny of nitric oxide synthase in the lumbosacral spinal cord of the neonatal rat. Dev. Brain Res. 81:1994;201-217.
62. Vizzard M.A., Erickson K., De Groat W.C. Localization of NADPH diaphorase in the thoracolumbar and sacrococcygeal spinal cord of the dog. J. Auton. Nerv. Syst. 64:1997;128-142.
63. Wedel B.J., Garbers D.L. New Insights on the functions of the guanylyl cyclase receptors. FEBS Lett. 410:1997;29-33.
64. Wetts R., Phelps P.E., Vaughn J.E. Transient and continuous expression of NADPH diaphorase in different neuronal populations of developing rat spinal cord. Dev. Dyn. 202:1995;215-228.
65. Wu S.Y., Dun S.L., Förstermann U., Dun N.J. Nitric oxide and excitatory postsynaptic currents in immature rat sympathetic preganglionic neurons in vitro. Neuroscience. 79:1997;237-245.
66. Wu W., Li L. Inhibition of nitric oxide synthase reduces motoneuron death due to spinal root avulsion. Neurosci. Lett. 153:1993;121-124.
67. Young H.M., McConalogue K., Furness J.B., De Vente J. Nitric oxide targets in the guinea-pig intestine identified by induction of cyclic GMP immunoreactivity. Neuroscience. 55:1993;583-596.
68. Zamir N., Skofitsch G., Eskay R.L., Jacobowitz D.M. Distribution of immunoreactive atrial natriuretic peptides in the central nervous system of the rat. Brain Res. 365:1986;105-111.