Release of calcitonin gene-related peptide from the jugular--nodose ganglion complex in rats--A new model to examine the role of cardiac peptidergic and nitrergic innervation
[en] Objective: Afferent information from the heart and the lung is conveyed to the brainstem by primary afferent fibers originating from vagal sensory neurons (jugular–nodose ganglion complex, JNC). The present study was made to evaluate if release of the sensory neuropeptide calcitonin gene-related peptide (CGRP) from the JNC can be used as a model for future studies on changes in neuropeptide release under pathological conditions of the heart.
Methods: Freshly isolated rat JNC’s were passed through a series of solutions based on oxygenated synthetic interstitial fluid (SIF). Substances such as the TRPV1 receptor agonist capsaicin and the nitric oxide (NO) donor sodium nitroprusside (SNP) were added as excitatory test stimuli. The eluates were processed using an enzyme immuno-assay (EIA) for measurement of CGRP concentrations. Immunohistochemistry was used to visualize CGRP containing and NO producing neurons in the JNC.
Results: Both SNP and capsaicin caused significant increases in CGRP release. CGRP-immunoreactive neurons (somata) were preferentially found in the jugular ganglion, whereas neurons immunoreactive for neuronal NO synthase were mostly localized in the nodose ganglion.
Conclusion: The present study demonstrates an easily reproducible model for measuring stimulated CGRP release from vagal afferents arising from the JNC. Nitric oxide produced by vagal afferents may stimulate CGRP release upon afferent activation.
Koulchitsky, Stanislav ; Université de Liège > Département des sciences biomédicales et précliniques > Pharmacologie
Dieterle, Anne
Neuhuber, Winfried L.
Weyand, Michael
Messlinger, Karl
Language :
English
Title :
Release of calcitonin gene-related peptide from the jugular--nodose ganglion complex in rats--A new model to examine the role of cardiac peptidergic and nitrergic innervation
Bellamy J., Bowen E.J., Russo A.F., and Durham P.L. Nitric oxide regulation of calcitonin gene-related peptide gene expression in rat trigeminal ganglia neurons. Eur. J. Neurosci. 23 (2006) 2057-2066
Berthoud H.R., and Neuhuber W.L. Functional and chemical anatomy of the afferent vagal system. Auton. Neurosci. 85 (2000) 1-17
Biella G., Panara C., Pecile A., and Sotgiu M.L. Facilitatory role of calcitonin gene-related peptide (CGRP) on excitation induced by substance P (SP) and noxious stimuli in rat spinal dorsal horn neurons. An iontophoretic study in vivo. Brain Res. 559 (1991) 352-356
Bretag A.H. Synthetic interstitial fluid for isolated mammalian tissue. Life Sci. 8 (1969) 319-329
Cadieux A., Springall D.R., Mulderry P.K., Rodrigo J., Ghatei M.A., Terenghi G., Bloom S.R., and Polak J.M. Occurrence, distribution and ontogeny of CGRP immunoreactivity in the rat lower respiratory tract: effect of capsaicin treatment and surgical denervations. Neuroscience 19 (1986) 605-627
Dun N.J., Dun S.L., Chiba T., and Forstermann U. Nitric oxide synthase-immunoreactive vagal afferent fibers in rat superior cervical ganglia. Neuroscience 65 (1995) 231-239
Durham P.L., Cady R., and Cady R. Regulation of calcitonin gene-related peptide secretion from trigeminal nerve cells by botulinum toxin type A: implications for migraine therapy. Headache 44 (2004) 35-42
Ferrari R., Panzali A.F., Poole-Wilson P.A., and Anand I.S. Plasma CGRP-like immunoreactivity in treated and untreated congestive heart failure. Lancet 338 (1991) 1084
Fischer M.J., Reeh P.W., and Sauer S.K. Proton-induced calcitonin gene-related peptide release from rat sciatic nerve axons, in vitro, involving TRPV1. Eur. J. Neurosci. 18 (2003) 803-810
Franco-Cereceda A., Henke H., Lundberg J.M., Petermann J.B., Hökfelt T., and Fischer J.A. Calcitonin gene-related peptide (CGRP) in capsaicin-sensitive substance P-immunoreactive sensory neurons in animals and man: distribution and release by capsaicin. Peptides 8 (1987) 399-410
Franco-Cereceda A., and Liska J. Potential of calcitonin gene-related peptide in coronary heart disease. Pharmacology 60 (2000) 1-8
Fukuda T., Ichikawa H., Terayama R., Yamaai T., Kuboki T., and Sugimoto T. ASIC3-immunoreactive neurons in the rat vagal and glossopharyngeal sensory ganglia. Brain Res. 1081 (2006) 150-155
Gray D.W., and Marshall I. Nitric oxide synthesis inhibitors attenuate calcitonin gene-related peptide endothelium-dependent vasorelaxation in rat aorta. Eur. J. Pharmacol. 212 (1992) 37-42
Grundy D. Neuroanatomy of visceral nociception: vagal and splanchnic afferent. Gut 51 Suppl 1 (2002) i2-i5
Helke C.J., and Hill K.M. Immunohistochemical study of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat. Neuroscience 26 (1988) 539-551
Helke C.J., and Niederer A.J. Studies on the coexistence of substance P with other putative transmitters in the nodose and petrosal ganglia. Synapse 5 (1990) 144-151
Holzer P., Wachter C., Heinemann A., Jocic M., Lippe I.T., and Herbert M.K. Diverse interactions of calcitonin gene related peptide and nitric oxide in the gastric and cutaneous microcirculation. Can. J. Physiol. Pharmacol. 73 (1995) 991-994
Hughes S.R., and Brain S.D. Nitric oxide-dependent release of vasodilator quantities of calcitonin gene-related peptide from capsaicin-sensitive nerves in rabbit skin. Br. J. Pharmacol. 111 (1994) 425-430
Kessler F., Habelt C., Averbeck B., Reeh P.W., and Kress M. Heat-induced release of CGRP from isolated rat skin and effects of bradykinin and the protein kinase C activator PMA. Pain 83 (1999) 289-295
Mair J., Lechleitner P., Längle T., Wiedermann C., Dienstl F., and Saria A. Plasma CGRP in acute myocardial infarction. Lancet 335 (1990) 168
Mayer B., John M., Heinzel B., Werner E.R., Wachter H., Schultz G., and Böhme E. Brain nitric oxide synthase is a biopterin- and flavin-containing multi-functional oxido-reductase. FEBS Lett. 288 (1991) 187-191
Meller S.T., and Gebhart G.F. A critical review of the afferent pathways and the potential chemical mediators involved in cardiac pain. Neuroscience 48 (1992) 501-524
Menard D.P., van Rossum D., Kar S., Jolicoeur F.B., Jhamandas K., and Quirion R. Tolerance to the antinociceptive properties of morphine in the rat spinal cord: alteration of calcitonin gene-related peptide-like immunostaining and receptor binding sites. J. Pharmacol. Exp. Ther. 273 (1995) 887-894
Meng J., Wang J., Lawrence G., and Dolly J.O. Synaptobrevin I mediates exocytosis of CGRP from sensory neurons and inhibition by botulinum toxins reflects their anti-nociceptive potential. J. Cell Sci. 120 (2007) 2864-2874
Mitchell J.A., Williams F.M., Williams T.J., and Larkin S.W. Role of nitric oxide in the dilator actions of capsaicin-sensitive nerves in the rabbit coronary circulation. Neuropeptides 31 (1997) 333-338
Morris R., Southam E., Braid D.J., and Garthwaite J. Nitric oxide may act as a messenger between dorsal root ganglion neurones and their satellite cells. Neurosci. Lett. 137 (1992) 29-32
Mulderry P.K., Ghatei M.A., Rodrigo J., Allen J.M., Rosenfeld M.G., Polak J.M., and Bloom S.R. Calcitonin gene-related peptide in cardiovascular tissues of the rat. Neuroscience 14 (1985) 947-954
Natura G., von Banchet G.S., and Schaible H.G. Calcitonin gene-related peptide enhances TTX-resistant sodium currents in cultured dorsal root ganglion neurons from adult rats. Pain 116 (2005) 194-204
Nozdrachev A.D., and Polyakov E.L. Anatomy of the Rat (Laboratory Animals) (2001), St. Petersburg, Russia 464 pp
Petruska J.C., Napaporn J., Johnson R.D., and Cooper B.Y. Chemical responsiveness and histochemical phenotype of electrophysiologically classified cells of the adult rat dorsal root ganglion. Neuroscience 115 (2002) 15-30
Plato M., Kummer W., and Haberberger R.V. Structural and neurochemical comparison of vagal and spinal afferent neurons projecting to the rat lung. Neurosci. Lett. 395 (2006) 215-219
Raddino R., Pela G., Manca C., Barbagallo M., D'Aloia A., Passeri M., and Visioli O. Mechanism of action of human calcitonin gene-related peptide in rabbit heart and in human mammary arteries. J. Cardiovasc. Pharmacol. 29 (1997) 463-470
Saito A., and Goto K. Depletion of calcitonin gene-related peptide (CGRP) by capsaicin in cerebral arteries. J. Pharmacobiodyn. 9 (1986) 613-619
Saito A., Kimura S., and Goto K. Calcitonin gene-related peptide as potential neurotransmitter in guinea pig right atrium. Am. J. Physiol. 250 (1986) H693-H698
Sauer S.K., Reeh P.W., and Bove G.M. Noxious heat-induced CGRP release from rat sciatic nerve axons in vitro. Eur. J. Neurosci. 14 (2001) 1203-1208
Springall D.R., Cadieux A., Oliveira H., Su H., Royston D., and Polak J.M. Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J. Auton. Nerv. Syst. 20 (1987) 155-166
Strecker T., Dux M., and Messlinger K. Nitric oxide releases calcitonin-gene-related peptide from rat dura mater encephali promoting increases in meningeal blood flow. J. Vasc. Res. 39 (2002) 489-496
Strecker T., Reeh P.W., Weyand M., and Messlinger K. Release of calcitonin gene-related peptide from the isolated mouse heart: methodological validation of a new model. Neuropeptides 40 (2006) 107-113
Sugiyama A., Kobayashi M., Tsujimoto G., Motomura S., and Hashimoto K. The first demonstration of CGRP-immunoreactive fibers in canine hearts: coronary vasodilator, inotropic and chronotropic effects of CGRP in canine isolated, blood-perfused heart preparations. Jpn. J. Pharmacol. 50 (1989) 421-427
van Rossum D., Hanisch U.K., and Quirion R. Neuroanatomical localization, pharmacological characterization and functions of CGRP, related peptides and their receptors. Neurosci. Biobehav. Rev. 21 (1997) 649-678
Wank M., and Neuhuber W.L. Local differences in vagal afferent innervation of the rat esophagus are reflected by neurochemical differences at the level of the sensory ganglia and by different brainstem projections. J. Comp. Neurol. 435 (2001) 41-59
Yu S., Undem B.J., and Kollarik M. Vagal afferent nerves with nociceptive properties in guinea-pig oesophagus. J. Physiol. 563 (2005) 831-842
Zhang Z., Winborn C.S., Marquez de Prado B., and Russo A.F. Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J. Neurosci. 27 (2007) 2693-2703
Zhuo H., Ichikawa H., and Helke C.J. Neurochemistry of the nodose ganglion. Prog. Neurobiol. 52 (1997) 79-107
