Neuropeptides
Volume 43, Issue 6 , Pages 483-489 , December 2009

Glyceroltrinitrate facilitates stimulated CGRP release but not gene expression of CGRP or its receptor components in rat trigeminal ganglia

  • Mirjam Eberhardt

      Affiliations

    • Institute of Physiology and Experimental Pathophysiology, Erlangen, Germany
  • ,
  • Lars Neeb

      Affiliations

    • Department of Neurology, Charité Universitätsmedizin Berlin, Germany
  • ,
  • Eva-Maria Vogel

      Affiliations

    • Institute of Experimental and Clinical Pharmacology and Toxicology, Erlangen, Germany
    • Department of Nephrology and Hypertension, Erlangen, Germany
  • ,
  • Gisa Tiegs

      Affiliations

    • Institute of Experimental and Clinical Pharmacology and Toxicology, Erlangen, Germany
    • Division of Experimental Immunology and Hepatology, Center of Internal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
  • ,
  • Uwe Reuter

      Affiliations

    • Department of Neurology, Charité Universitätsmedizin Berlin, Germany
  • ,
  • Karl Messlinger

      Affiliations

    • Institute of Physiology and Experimental Pathophysiology, Erlangen, Germany
  • ,
  • Michael J.M. Fischer

      Affiliations

    • Institute of Physiology and Experimental Pathophysiology, Erlangen, Germany
    • Corresponding Author InformationCorresponding author. Address: Institute of Physiology and Pathophysiology, Universität Erlangen/Nürnberg, Universitätstrasse 17, D-91054 Erlangen, Germany. Tel.: +49 9131 85 22491; fax: +49 9131 85 22497.

Received 8 January 2009 ,Accepted 16 September 2009.

References 

  1. Abd El-Aleem SA, Morales-Aza BM, Donaldson LF. Sensory neuropeptide mRNA up-regulation is bilateral in periodontitis in the rat: a possible neurogenic component to symmetrical periodontal disease. Eur. J. Neurosci. 2004;19:650–658
  2. Ahern GP, Klyachko VA, Jackson MB. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci. 2002;25:510–517
  3. Aimar P, Pasti L, Carmignoto G, Merighi A. Nitric oxide-producing islet cells modulate the release of sensory neuropeptides in the rat substantia gelatinosa. J. Neurosci. 1998;18:10375–10388
  4. Akerman S, Williamson DJ, Kaube H, Goadsby PJ. Nitric oxide synthase inhibitors can antagonize neurogenic and calcitonin gene-related peptide induced dilation of dural meningeal vessels. Br. J. Pharmacol. 2002;137:62–68
  5. Amara SG, Arriza JL, Leff SE, Swanson LW, Evans RM, Rosenfeld MG. Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide. Science. 1985;229:1094–1097
  6. Ambalavanar R, Dessem D, Moutanni A, Yallampalli C, Yallampalli U, Gangula P, et al. Muscle inflammation induces a rapid increase in calcitonin gene-related peptide (CGRP) mRNA that temporally relates to CGRP immunoreactivity and nociceptive behavior. Neuroscience. 2006;143:875–884
  7. Ambalavanar R, Moritani M, Moutanni A, Gangula P, Yallampalli C, Dessem D. Deep tissue inflammation upregulates neuropeptides and evokes nociceptive behaviors which are modulated by a neuropeptide antagonist. Pain. 2006;120:53–68
  8. Ashina M, Bendtsen L, Jensen R, Olesen J. Nitric oxide-induced headache in patients with chronic tension-type headache. Brain. 2000;123(Pt 9):1830–1837
  9. Averbeck B, Reeh PW. Interactions of inflammatory mediators stimulating release of calcitonin gene-related peptide, substance P and prostaglandin E(2) from isolated rat skin. Neuropharmacology. 2001;40:416–423
  10. Bellamy J, Bowen EJ, Russo AF, Durham PL. Nitric oxide regulation of calcitonin gene-related peptide gene expression in rat trigeminal ganglia neurons. Eur. J. Neurosci. 2006;23:2057–2066
  11. Boettger MK, Uceyler N, Zelenka M, Schmitt A, Reif A, Chen Y, et al. Differences in inflammatory pain in nNOS-, iNOS- and eNOS-deficient mice. Eur. J. Pain. 2007;11:810–818
  12. Bretag AH. Synthetic interstitial fluid for isolated mammalian tissue. Life. Sci. 1969;8:319–329
  13. Cadiou H, Studer M, Jones NG, Smith ES, Ballard A, McMahon SB, et al. Modulation of acid-sensing ion channel activity by nitric oxide. J. Neurosci. 2007;27:13251–13260
  14. Doods H, Arndt K, Rudolf K, Just S. CGRP antagonists: unravelling the role of CGRP in migraine. Trends Pharmacol. Sci. 2007;28:580–587
  15. Durham PL, Cady R, Cady R. Regulation of calcitonin gene-related peptide secretion from trigeminal nerve cells by botulinum toxin type A: implications for migraine therapy. Headache. 2004;44:35–42
  16. Eberhardt M, Hoffmann T, Sauer SK, Messlinger K, Reeh PW, Fischer MJ. Calcitonin gene-related peptide release from intact isolated dorsal root and trigeminal ganglia. Neuropeptides. 2008;42:311–317
  17. Ebersberger A, Averbeck B, Messlinger K, Reeh PW. Release of substance P, calcitonin gene-related peptide and prostaglandin E2 from rat dura mater encephali following electrical and chemical stimulation in vitro. Neuroscience. 1999;89:901–907
  18. Edvinsson L. Blockade of CGRP receptors in the intracranial vasculature: a new target in the treatment of headache. Cephalalgia. 2004;24:611–622
  19. Fernihough J, Gentry C, Bevan S, Winter J. Regulation of calcitonin gene-related peptide and TRPV1 in a rat model of osteoarthritis. Neurosci. Lett. 2005;388:75–80
  20. Fischer MJ, Reeh PW. Sensitization to heat through G-protein-coupled receptor pathways in the isolated sciatic mouse nerve. Eur. J. Neurosci. 2007;25:3570–3575
  21. Fischer MJ, Reeh PW, Sauer SK. Proton-induced calcitonin gene-related peptide release from rat sciatic nerve axons, in vitro, involving TRPV1. Eur. J. Neurosci. 2003;18:803–810
  22. Garry MG, Richardson JD, Hargreaves KM. Sodium nitroprusside evokes the release of immunoreactive calcitonin gene-related peptide and substance P from dorsal horn slices via nitric oxide-dependent and nitric oxide-independent mechanisms. J. Neurosci. 1994;14:4329–4337
  23. Gaston BM, Carver J, Doctor A, Palmer LA. S-Nitrosylation signaling in cell biology. Mol. Interventions. 2003;3:253–263
  24. Goadsby PJ. Migraine pathophysiology. Headache. 2005;45(Suppl. 1):S14–S24
  25. Goadsby PJ, Edvinsson L, Ekman R. Release of vasoactive peptides in the extracerebral circulation of humans and the cat during activation of the trigeminovascular system. Ann. Neurol. 1988;23:193–196
  26. Ho TW, Mannix LK, Fan X, Assaid C, Furtek C, Jones CJ, et al. Randomized controlled trial of an oral CGRP receptor antagonist, MK-0974, in acute treatment of migraine. Neurology. 2008;70:1304–1312
  27. Hutchins B, Spears R, Hinton RJ, Harper RP. Calcitonin gene-related peptide and substance P immunoreactivity in rat trigeminal ganglia and brainstem following adjuvant-induced inflammation of the temporomandibular joint. Arch. Oral Biol. 2000;45:335–345
  28. Iadecola C, Pelligrino DA, Moskowitz MA, Lassen NA. Nitric oxide synthase inhibition and cerebrovascular regulation. J. Cereb. Blood Flow Metab. 1994;14:175–192
  29. Jenkins DW, Langmead CJ, Parsons AA, Strijbos PJ. Regulation of calcitonin gene-related peptide release from rat trigeminal nucleus caudalis slices in vitro. Neurosci. Lett. 2004;366:241–244
  30. Koulchitsky S, Fischer MJ, Messlinger K. Calcitonin gene-related peptide receptor inhibition reduces neuronal activity induced by prolonged increase in nitric oxide in the rat spinal trigeminal nucleus. Cephalalgia. 2009;29:408–417
  31. Lai YC, Shaftel SS, Miller JN, Tallents RH, Chang Y, Pinkert CA, et al. Intraarticular induction of interleukin-1beta expression in the adult mouse, with resultant temporomandibular joint pathologic changes, dysfunction, and pain. Arthritis Rheum. 2006;54:1184–1197
  32. Lassen LH, Ashina M, Christiansen I, Ulrich V, Olesen J. Nitric oxide synthase inhibition in migraine. Lancet. 1997;349:401–402
  33. Lennerz JK, Ruhle V, Ceppa EP, Neuhuber WL, Bunnett NW, Grady EF, et al. Calcitonin receptor-like receptor (CLR), receptor activity-modifying protein 1 (RAMP1), and calcitonin gene-related peptide (CGRP) immunoreactivity in the rat trigeminovascular system: differences between peripheral and central CGRP receptor distribution. J. Comp. Neurol. 2008;507:1277–1299
  34. Ma W, Chabot JG, Powell KJ, Jhamandas K, Dickerson IM, Quirion R. Localization and modulation of calcitonin gene-related peptide-receptor component protein-immunoreactive cells in the rat central and peripheral nervous systems. Neuroscience. 2003;120:677–694
  35. McMahon SB, Armanini MP, Ling LH, Phillips HS. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron. 1994;12:1161–1171
  36. Mulder H, Zhang Y, Danielsen N, Sundler F. Islet amyloid polypeptide and calcitonin gene-related peptide expression are upregulated in lumbar dorsal root ganglia after unilateral adjuvant-induced inflammation in the rat paw. Brain Res. Mol. Brain Res. 1997;50:127–135
  37. Ohkuma S, Katsura M. Nitric oxide and peroxynitrite as factors to stimulate neurotransmitter release in the CNS. Prog. Neurobiol. 2001;64:97–108
  38. Olesen J, Thomsen LL, Lassen LH, Olesen IJ. The nitric oxide hypothesis of migraine and other vascular headaches. Cephalalgia. 1995;15:94–100
  39. Olesen J, Diener HC, Husstedt IW, Goadsby PJ, Hall D, Meier U, et al. Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N. Engl. J. Med. 2004;350:1104–1110
  40. Ouyang K, Zheng H, Qin X, Zhang C, Yang D, Wang X, et al. Ca2+ sparks and secretion in dorsal root ganglion neurons. Proc. Natl. Acad. Sci. USA. 2005;102:12259–12264
  41. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45
  42. Pietrobon D, Striessnig J. Neurobiology of migraine. Nat. Rev. Neurosci. 2003;4:386–398
  43. Prast H, Philippu A. Nitric oxide as modulator of neuronal function. Prog. Neurobiol. 2001;64:51–68
  44. Reuter U, Chiarugi A, Bolay H, Moskowitz MA. Nuclear factor-kappaB as a molecular target for migraine therapy. Ann. Neurol. 2002;51:507–516
  45. Sauer SK, Bove GM, Averbeck B, Reeh PW. Rat peripheral nerve components release calcitonin gene-related peptide and prostaglandin E2 in response to noxious stimuli: evidence that nervi nervorum are nociceptors. Neuroscience. 1999;92:319–325
  46. Strecker T, Dux M, Messlinger K. Nitric oxide releases calcitonin-gene-related peptide from rat dura mater encephali promoting increases in meningeal blood flow. J. Vasc. Res. 2002;39:489–496
  47. Thalakoti S, Patil VV, Damodaram S, Vause CV, Langford LE, Freeman SE, et al. Neuron-glia signaling in trigeminal ganglion: implications for migraine pathology. Headache. 2007;47:1008–1023
  48. Ulrich-Lai YM, Flores CM, Harding-Rose CA, Goodis HE, Hargreaves KM. Capsaicin-evoked release of immunoreactive calcitonin gene-related peptide from rat trigeminal ganglion: evidence for intraganglionic neurotransmission. Pain. 2001;91:219–226
  49. Urban MO, Gebhart GF. Supraspinal contributions to hyperalgesia. Proc. Natl. Acad. Sci. USA. 1999;96:7687–7692
  50. Williamson DJ, Hargreaves RJ. Neurogenic inflammation in the context of migraine. Microsc. Res. Tech. 2001;53:167–178
  51. Xu P, Hall AK. Activin acts with nerve growth factor to regulate calcitonin gene-related peptide mRNA in sensory neurons. Neuroscience. 2007;150:665–674
  52. Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, et al. Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat. Chem. Biol. 2006;2:596–607
  53. Zhang Z, Winborn CS, Marquez dP, Russo AF. Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J. Neurosci. 2007;27:2693–2703
  54. Zimmermann M. Pathobiology of neuropathic pain. Eur. J. Pharmacol. 2001;429:23–37

PII: S0143-4179(09)00106-1

doi: 10.1016/j.npep.2009.09.002

Neuropeptides
Volume 43, Issue 6 , Pages 483-489 , December 2009