Skip to main content
Top
Published in: Seminars in Immunopathology 3/2018

01-05-2018 | Review

Neurogenic inflammation and its role in migraine

Author: Roshni Ramachandran

Published in: Seminars in Immunopathology | Issue 3/2018

Login to get access

Abstract

The etiology of migraine pain involves sensitized meningeal afferents that densely innervate the dural vasculature. These afferents, with their cell bodies located in the trigeminal ganglion, project to the nucleus caudalis, which in turn transmits signals to higher brain centers. Factors such as chronic stress, diet, hormonal fluctuations, or events like cortical spreading depression can generate a state of “sterile inflammation” in the intracranial meninges resulting in the sensitization and activation of trigeminal meningeal nociceptors. This sterile inflammatory phenotype also referred to as neurogenic inflammation is characterized by the release of neuropeptides (such as substance P, calcitonin gene related peptide) from the trigeminal innervation. This release leads to vasodilation, plasma extravasation secondary to capillary leakage, edema, and mast cell degranulation. Although neurogenic inflammation has been observed and extensively studied in peripheral tissues, its role has been primarily investigated in the genesis and maintenance of migraine pain. While some aspects of neurogenic inflammation has been disregarded in the occurrence of migraine pain, targeted analysis of factors have opened up the possibilities of a dialogue between the neurons and immune cells in driving such a sterile neuroinflammatory state in migraine pathophysiology.
Literature
3.
go back to reference Russell MB, Rasmussen BK, Thorvaldsen P, Olesen J (1995) Prevalence and sex-ratio of the subtypes of migraine. Int J Epidemiol 24:612–618PubMedCrossRef Russell MB, Rasmussen BK, Thorvaldsen P, Olesen J (1995) Prevalence and sex-ratio of the subtypes of migraine. Int J Epidemiol 24:612–618PubMedCrossRef
8.
go back to reference McNaughton FL, Feindel WH (1997) Innervation of intracranial structures: a reappraisal. In: Physiological Aspects of Clinical Neurology, Oxford: Blackwell Scientific Publications, England, pp 270–293 McNaughton FL, Feindel WH (1997) Innervation of intracranial structures: a reappraisal. In: Physiological Aspects of Clinical Neurology, Oxford: Blackwell Scientific Publications, England, pp 270–293
10.
go back to reference Andres KH, Düring Von M, Muszynski K, Schmidt RF (1987) Nerve fibres and their terminals of the dura mater encephali of the rat. Anat Embryol 175:289–301PubMedCrossRef Andres KH, Düring Von M, Muszynski K, Schmidt RF (1987) Nerve fibres and their terminals of the dura mater encephali of the rat. Anat Embryol 175:289–301PubMedCrossRef
11.
go back to reference Arnold F (1831) Der Kopftheil des vegetativen Nervensystems beim Menschen: in anatomischer und physiologischer Hinsicht Arnold F (1831) Der Kopftheil des vegetativen Nervensystems beim Menschen: in anatomischer und physiologischer Hinsicht
13.
go back to reference Grzybowski JL (1931) Innervation de la dure—mére cranienne chez l’homme. Arch Anat Histol Embryol 14:387–428 Grzybowski JL (1931) Innervation de la dure—mére cranienne chez l’homme. Arch Anat Histol Embryol 14:387–428
15.
go back to reference Steiger HJ, Meakin CJ (1984) The meningeal representation in the trigeminal ganglion—an experimental study in the cat. Headache 24:305–309PubMedCrossRef Steiger HJ, Meakin CJ (1984) The meningeal representation in the trigeminal ganglion—an experimental study in the cat. Headache 24:305–309PubMedCrossRef
17.
go back to reference Uddman R, Hara H, Edvinsson L (1989) Neuronal pathways to the rat middle meningeal artery revealed by retrograde tracing and immunocytochemistry. J Auton Nerv Syst 26:69–75PubMedCrossRef Uddman R, Hara H, Edvinsson L (1989) Neuronal pathways to the rat middle meningeal artery revealed by retrograde tracing and immunocytochemistry. J Auton Nerv Syst 26:69–75PubMedCrossRef
22.
go back to reference Messlinger K, Hanesch U, Baumgärtel M et al (1993) Innervation of the dura mater encephali of cat and rat: ultrastructure and calcitonin gene-related peptide-like and substance P-like immunoreactivity. Anat Embryol 188:219–237PubMedCrossRef Messlinger K, Hanesch U, Baumgärtel M et al (1993) Innervation of the dura mater encephali of cat and rat: ultrastructure and calcitonin gene-related peptide-like and substance P-like immunoreactivity. Anat Embryol 188:219–237PubMedCrossRef
26.
go back to reference Edvinsson L, Gulbenkian S, Barroso CP et al (1998) Innervation of the human middle meningeal artery: immunohistochemistry, ultrastructure, and role of endothelium for vasomotility. Peptides 19:1213–1225PubMedCrossRef Edvinsson L, Gulbenkian S, Barroso CP et al (1998) Innervation of the human middle meningeal artery: immunohistochemistry, ultrastructure, and role of endothelium for vasomotility. Peptides 19:1213–1225PubMedCrossRef
29.
go back to reference Drummond PD, Lance JW (1992) Pathological sweating and flushing accompanying the trigeminal lacrimal reflex in patients with cluster headache and in patients with a confirmed site of cervical sympathetic deficit. Evidence for parasympathetic cross-innervation. Brain 115(Pt 5):1429–1445PubMedCrossRef Drummond PD, Lance JW (1992) Pathological sweating and flushing accompanying the trigeminal lacrimal reflex in patients with cluster headache and in patients with a confirmed site of cervical sympathetic deficit. Evidence for parasympathetic cross-innervation. Brain 115(Pt 5):1429–1445PubMedCrossRef
30.
go back to reference Drummond PD (1994) Sweating and vascular responses in the face: normal regulation and dysfunction in migraine, cluster headache and harlequin syndrome. Clin Auton Res 4:273–285PubMedCrossRef Drummond PD (1994) Sweating and vascular responses in the face: normal regulation and dysfunction in migraine, cluster headache and harlequin syndrome. Clin Auton Res 4:273–285PubMedCrossRef
33.
go back to reference Keller JT, Saunders MC, Beduk A, Jollis JG (1985) Innervation of the posterior fossa dura of the cat. Brain Res Bull 14:97–102PubMedCrossRef Keller JT, Saunders MC, Beduk A, Jollis JG (1985) Innervation of the posterior fossa dura of the cat. Brain Res Bull 14:97–102PubMedCrossRef
37.
go back to reference Düring Von M, Bauersachs M, Böhmer B et al (1990) Neuropeptide Y- and substance P-like immunoreactive nerve fibers in the rat dura mater encephali. Anat Embryol 182:363–373CrossRef Düring Von M, Bauersachs M, Böhmer B et al (1990) Neuropeptide Y- and substance P-like immunoreactive nerve fibers in the rat dura mater encephali. Anat Embryol 182:363–373CrossRef
40.
go back to reference Dostrovsky JO, Davis KD, Kawakita K (1991) Central mechanisms of vascular headaches. Can J Physiol Pharmacol 69:652–658PubMedCrossRef Dostrovsky JO, Davis KD, Kawakita K (1991) Central mechanisms of vascular headaches. Can J Physiol Pharmacol 69:652–658PubMedCrossRef
42.
go back to reference Bahns E, Ernsberger U, Jänig W, Nelke A (1986) Discharge properties of mechanosensitive afferents supplying the retroperitoneal space. Pflugers Arch 407:519–525PubMedCrossRef Bahns E, Ernsberger U, Jänig W, Nelke A (1986) Discharge properties of mechanosensitive afferents supplying the retroperitoneal space. Pflugers Arch 407:519–525PubMedCrossRef
45.
go back to reference Schepelmann K, Ebersberger A, Pawlak M et al (1999) Response properties of trigeminal brain stem neurons with input from dura mater encephali in the rat. Neuroscience 90:543–554PubMedCrossRef Schepelmann K, Ebersberger A, Pawlak M et al (1999) Response properties of trigeminal brain stem neurons with input from dura mater encephali in the rat. Neuroscience 90:543–554PubMedCrossRef
47.
go back to reference Levine JD (1999) Peripheral mechanisms of inflammatory pain. In: Wall PD, Melzack R (ed) Textbook of Pain. Churchill Livingstone, London, pp 59–84 Levine JD (1999) Peripheral mechanisms of inflammatory pain. In: Wall PD, Melzack R (ed) Textbook of Pain. Churchill Livingstone, London, pp 59–84
48.
go back to reference Lopshire JC, Nicol GD (1998) The cAMP transduction cascade mediates the prostaglandin E2 enhancement of the capsaicin-elicited current in rat sensory neurons: Whole-cell and single-channel studies. J Neurosci 18:6081–6092PubMedCrossRef Lopshire JC, Nicol GD (1998) The cAMP transduction cascade mediates the prostaglandin E2 enhancement of the capsaicin-elicited current in rat sensory neurons: Whole-cell and single-channel studies. J Neurosci 18:6081–6092PubMedCrossRef
49.
go back to reference Pitchford S, Levine JD (1991) Prostaglandins sensitize nociceptors in cell culture. Neurosci Lett 132:105–108PubMedCrossRef Pitchford S, Levine JD (1991) Prostaglandins sensitize nociceptors in cell culture. Neurosci Lett 132:105–108PubMedCrossRef
55.
60.
go back to reference Saito A, Lee TJ (1987) Serotonin as an alternative transmitter in sympathetic nerves of large cerebral arteries of the rabbit. Circ Res 60:220–228PubMedCrossRef Saito A, Lee TJ (1987) Serotonin as an alternative transmitter in sympathetic nerves of large cerebral arteries of the rabbit. Circ Res 60:220–228PubMedCrossRef
64.
go back to reference Reuter U, Bolay H, Jansen-Olesen I et al (2001) Delayed inflammation in rat meninges: implications for migraine pathophysiology. Brain 124:2490–2502PubMedCrossRef Reuter U, Bolay H, Jansen-Olesen I et al (2001) Delayed inflammation in rat meninges: implications for migraine pathophysiology. Brain 124:2490–2502PubMedCrossRef
71.
go back to reference Geppert M, Goda Y, Hammer RE et al (1994) Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79:717–727PubMedCrossRef Geppert M, Goda Y, Hammer RE et al (1994) Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79:717–727PubMedCrossRef
74.
go back to reference Kowalski ML, Sliwinska-Kowalska M, Kaliner MA (1990) Neurogenic inflammation, vascular permeability, and mast cells. II Additional evidence indicating that mast cells are not involved in neurogenic inflammation. J Immunol 145:1214–1221PubMed Kowalski ML, Sliwinska-Kowalska M, Kaliner MA (1990) Neurogenic inflammation, vascular permeability, and mast cells. II Additional evidence indicating that mast cells are not involved in neurogenic inflammation. J Immunol 145:1214–1221PubMed
75.
go back to reference Dimitriadou V, Buzzi MG, Moskowitz MA, Theoharides TC (1991) Trigeminal sensory fiber stimulation induces morphological changes reflecting secretion in rat dura mater mast cells. Neuroscience 44:97–112PubMedCrossRef Dimitriadou V, Buzzi MG, Moskowitz MA, Theoharides TC (1991) Trigeminal sensory fiber stimulation induces morphological changes reflecting secretion in rat dura mater mast cells. Neuroscience 44:97–112PubMedCrossRef
77.
78.
go back to reference Hökfelt T, Millhorn D, Seroogy K et al (1987) Coexistence of peptides with classical neurotransmitters. Experientia 43:768–780PubMedCrossRef Hökfelt T, Millhorn D, Seroogy K et al (1987) Coexistence of peptides with classical neurotransmitters. Experientia 43:768–780PubMedCrossRef
80.
go back to reference Kummer W (1992) Ultrastructure of calcitonin gene-related peptide-immunoreactive nerve fibres in guinea-pig peribronchial ganglia. Regul Pept 37:135–142PubMedCrossRef Kummer W (1992) Ultrastructure of calcitonin gene-related peptide-immunoreactive nerve fibres in guinea-pig peribronchial ganglia. Regul Pept 37:135–142PubMedCrossRef
90.
go back to reference Cui M, Khanijou S, Rubino J, Aoki KR (2004) Subcutaneous administration of botulinum toxin A reduces formalin-induced pain. Pain 107:125–133PubMedCrossRef Cui M, Khanijou S, Rubino J, Aoki KR (2004) Subcutaneous administration of botulinum toxin A reduces formalin-induced pain. Pain 107:125–133PubMedCrossRef
98.
go back to reference Guo A, Vulchanova L, Wang J et al (1999) Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11:946–958PubMedCrossRef Guo A, Vulchanova L, Wang J et al (1999) Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11:946–958PubMedCrossRef
101.
go back to reference Hanko J, Hardebo JE, Kåhrström J et al (1985) Calcitonin gene-related peptide is present in mammalian cerebrovascular nerve fibres and dilates pial and peripheral arteries. Neurosci Lett 57:91–95PubMedCrossRef Hanko J, Hardebo JE, Kåhrström J et al (1985) Calcitonin gene-related peptide is present in mammalian cerebrovascular nerve fibres and dilates pial and peripheral arteries. Neurosci Lett 57:91–95PubMedCrossRef
102.
go back to reference Edwards RM, Stack EJ, Trizna W (1991) Calcitonin gene-related peptide stimulates adenylate cyclase and relaxes intracerebral arterioles. J Pharmacol Exp Ther 257:1020–1024PubMed Edwards RM, Stack EJ, Trizna W (1991) Calcitonin gene-related peptide stimulates adenylate cyclase and relaxes intracerebral arterioles. J Pharmacol Exp Ther 257:1020–1024PubMed
104.
go back to reference Kurosawa M, Messlinger K, Pawlak M, Schmidt RF (1995) Increase of meningeal blood flow after electrical stimulation of rat dura mater encephali: mediation by calcitonin gene-related peptide. Br J Pharmacol 114:1397–1402PubMedPubMedCentralCrossRef Kurosawa M, Messlinger K, Pawlak M, Schmidt RF (1995) Increase of meningeal blood flow after electrical stimulation of rat dura mater encephali: mediation by calcitonin gene-related peptide. Br J Pharmacol 114:1397–1402PubMedPubMedCentralCrossRef
105.
go back to reference Messlinger K, Hanesch U, Kurosawa M et al (1995) Calcitonin gene related peptide released from dural nerve fibers mediates increase of meningeal blood flow in the rat. Can J Physiol Pharmacol 73:1020–1024PubMedCrossRef Messlinger K, Hanesch U, Kurosawa M et al (1995) Calcitonin gene related peptide released from dural nerve fibers mediates increase of meningeal blood flow in the rat. Can J Physiol Pharmacol 73:1020–1024PubMedCrossRef
107.
go back to reference Zagami AS, Goadsby PJ, Edvinsson L (1990) Stimulation of the superior sagittal sinus in the cat causes release of vasoactive peptides. Neuropeptides 16:69–75PubMedCrossRef Zagami AS, Goadsby PJ, Edvinsson L (1990) Stimulation of the superior sagittal sinus in the cat causes release of vasoactive peptides. Neuropeptides 16:69–75PubMedCrossRef
109.
go back to reference Messlinger K, Fischer MJM, Lennerz JK (2011) Neuropeptide effects in the trigeminal system: pathophysiology and clinical relevance in migraine. Keio J Med 60:82–89PubMedCrossRef Messlinger K, Fischer MJM, Lennerz JK (2011) Neuropeptide effects in the trigeminal system: pathophysiology and clinical relevance in migraine. Keio J Med 60:82–89PubMedCrossRef
110.
go back to reference Lassen LH, Haderslev PA, Jacobsen VB et al (2002) CGRP may play a causative role in migraine. Cephalalgia 22:54–61PubMedCrossRef Lassen LH, Haderslev PA, Jacobsen VB et al (2002) CGRP may play a causative role in migraine. Cephalalgia 22:54–61PubMedCrossRef
118.
go back to reference Kruuse C, Thomsen LL, Birk S, Olesen J (2003) Migraine can be induced by sildenafil without changes in middle cerebral artery diameter. Brain 126:241–247PubMedCrossRef Kruuse C, Thomsen LL, Birk S, Olesen J (2003) Migraine can be induced by sildenafil without changes in middle cerebral artery diameter. Brain 126:241–247PubMedCrossRef
120.
go back to reference Markowitz S, Saito K, Moskowitz MA (1987) Neurogenically mediated leakage of plasma protein occurs from blood vessels in dura mater but not brain. J Neurosci 7:4129–4136PubMedCrossRef Markowitz S, Saito K, Moskowitz MA (1987) Neurogenically mediated leakage of plasma protein occurs from blood vessels in dura mater but not brain. J Neurosci 7:4129–4136PubMedCrossRef
121.
go back to reference Alvaro G, Di Fabio R (2007) Neurokinin 1 receptor antagonists—current prospects. Curr Opin Drug Discov Devel 10:613–621PubMed Alvaro G, Di Fabio R (2007) Neurokinin 1 receptor antagonists—current prospects. Curr Opin Drug Discov Devel 10:613–621PubMed
122.
go back to reference Shepherd SL, Williamson DJ, Beer MS et al (1997) Differential effects of 5-HT1B/1D receptor agonists on neurogenic dural plasma extravasation and vasodilation in anaesthetized rats. Neuropharmacology 36:525–533PubMedCrossRef Shepherd SL, Williamson DJ, Beer MS et al (1997) Differential effects of 5-HT1B/1D receptor agonists on neurogenic dural plasma extravasation and vasodilation in anaesthetized rats. Neuropharmacology 36:525–533PubMedCrossRef
123.
go back to reference Buzzi MG, Moskowitz MA (1990) The antimigraine drug, sumatriptan (GR43175), selectively blocks neurogenic plasma extravasation from blood vessels in dura mater. Br J Pharmacol 99:202–206PubMedPubMedCentralCrossRef Buzzi MG, Moskowitz MA (1990) The antimigraine drug, sumatriptan (GR43175), selectively blocks neurogenic plasma extravasation from blood vessels in dura mater. Br J Pharmacol 99:202–206PubMedPubMedCentralCrossRef
124.
go back to reference Moskowitz MA (1992) Neurogenic versus vascular mechanisms of sumatriptan and ergot alkaloids in migraine. Trends Pharmacol Sci 13:307–311PubMedCrossRef Moskowitz MA (1992) Neurogenic versus vascular mechanisms of sumatriptan and ergot alkaloids in migraine. Trends Pharmacol Sci 13:307–311PubMedCrossRef
127.
go back to reference Goldstein DJ, Roon KI, Offen WW et al (2001) Selective seratonin 1F (5-HT(1F)) receptor agonist LY334370 for acute migraine: a randomised controlled trial. Lancet 358:1230–1234PubMedCrossRef Goldstein DJ, Roon KI, Offen WW et al (2001) Selective seratonin 1F (5-HT(1F)) receptor agonist LY334370 for acute migraine: a randomised controlled trial. Lancet 358:1230–1234PubMedCrossRef
128.
go back to reference Petersen LJ, Church MK, Skov PS (1997) Histamine is released in the wheal but not the flare following challenge of human skin in vivo: a microdialysis study. Clin Exp Allergy 27:284–295PubMedCrossRef Petersen LJ, Church MK, Skov PS (1997) Histamine is released in the wheal but not the flare following challenge of human skin in vivo: a microdialysis study. Clin Exp Allergy 27:284–295PubMedCrossRef
129.
go back to reference Petersen LJ (1997) Quantitative measurement of extracellular histamine concentrations in intact human skin in vivo by the microdialysis technique: methodological aspects. Allergy 52:547–555PubMedCrossRef Petersen LJ (1997) Quantitative measurement of extracellular histamine concentrations in intact human skin in vivo by the microdialysis technique: methodological aspects. Allergy 52:547–555PubMedCrossRef
132.
go back to reference Sarchielli P, Di Filippo M, Nardi K, Calabresi P (2007) Sensitization, glutamate, and the link between migraine and fibromyalgia. Curr Pain Headache Rep 11:343–351PubMedCrossRef Sarchielli P, Di Filippo M, Nardi K, Calabresi P (2007) Sensitization, glutamate, and the link between migraine and fibromyalgia. Curr Pain Headache Rep 11:343–351PubMedCrossRef
133.
go back to reference deGroot J, Zhou S, Carlton SM (2000) Peripheral glutamate release in the hindpaw following low and high intensity sciatic stimulation. Neuroreport 11:497–502PubMedCrossRef deGroot J, Zhou S, Carlton SM (2000) Peripheral glutamate release in the hindpaw following low and high intensity sciatic stimulation. Neuroreport 11:497–502PubMedCrossRef
135.
go back to reference Nordlind K, Johansson O, Lidén S, Hökfelt T (1993) Glutamate- and aspartate-like immunoreactivities in human normal and inflamed skin. Virchows Arch B Cell Pathol 64:75–82CrossRef Nordlind K, Johansson O, Lidén S, Hökfelt T (1993) Glutamate- and aspartate-like immunoreactivities in human normal and inflamed skin. Virchows Arch B Cell Pathol 64:75–82CrossRef
136.
go back to reference Warncke T, Stubhaug A, Jørum E (2000) Preinjury treatment with morphine or ketamine inhibits the development of experimentally induced secondary hyperalgesia in man. Pain 86:293–303PubMedCrossRef Warncke T, Stubhaug A, Jørum E (2000) Preinjury treatment with morphine or ketamine inhibits the development of experimentally induced secondary hyperalgesia in man. Pain 86:293–303PubMedCrossRef
137.
go back to reference Cairns BE, Sessle BJ, Hu JW (1998) Evidence that excitatory amino acid receptors within the temporomandibular joint region are involved in the reflex activation of the jaw muscles. J Neurosci 18:8056–8064PubMedCrossRef Cairns BE, Sessle BJ, Hu JW (1998) Evidence that excitatory amino acid receptors within the temporomandibular joint region are involved in the reflex activation of the jaw muscles. J Neurosci 18:8056–8064PubMedCrossRef
138.
go back to reference Davidson EM, Carlton SM (1998) Intraplantar injection of dextrorphan, ketamine or memantine attenuates formalin-induced behaviors. Brain Res 785:136–142PubMedCrossRef Davidson EM, Carlton SM (1998) Intraplantar injection of dextrorphan, ketamine or memantine attenuates formalin-induced behaviors. Brain Res 785:136–142PubMedCrossRef
139.
go back to reference Davidson EM, Coggeshall RE, Carlton SM (1997) Peripheral NMDA and non-NMDA glutamate receptors contribute to nociceptive behaviors in the rat formalin test. Neuroreport 8:941–946PubMedCrossRef Davidson EM, Coggeshall RE, Carlton SM (1997) Peripheral NMDA and non-NMDA glutamate receptors contribute to nociceptive behaviors in the rat formalin test. Neuroreport 8:941–946PubMedCrossRef
140.
go back to reference Jackson DL, Graff CB, Richardson JD, Hargreaves KM (1995) Glutamate participates in the peripheral modulation of thermal hyperalgesia in rats. Eur J Pharmacol 284:321–325PubMedCrossRef Jackson DL, Graff CB, Richardson JD, Hargreaves KM (1995) Glutamate participates in the peripheral modulation of thermal hyperalgesia in rats. Eur J Pharmacol 284:321–325PubMedCrossRef
141.
go back to reference Lawand NB, Willis WD, Westlund KN (1997) Excitatory amino acid receptor involvement in peripheral nociceptive transmission in rats. Eur J Pharmacol 324:169–177PubMedCrossRef Lawand NB, Willis WD, Westlund KN (1997) Excitatory amino acid receptor involvement in peripheral nociceptive transmission in rats. Eur J Pharmacol 324:169–177PubMedCrossRef
142.
go back to reference Carlton SM, Zhou S, Coggeshall RE (1998) Evidence for the interaction of glutamate and NK1 receptors in the periphery. Brain Res 790:160–169PubMedCrossRef Carlton SM, Zhou S, Coggeshall RE (1998) Evidence for the interaction of glutamate and NK1 receptors in the periphery. Brain Res 790:160–169PubMedCrossRef
145.
go back to reference Hu H-J, Bhave G, Gereau RW (2002) Prostaglandin and protein kinase A-dependent modulation of vanilloid receptor function by metabotropic glutamate receptor 5: potential mechanism for thermal hyperalgesia. J Neurosci 22:7444–7452PubMedCrossRef Hu H-J, Bhave G, Gereau RW (2002) Prostaglandin and protein kinase A-dependent modulation of vanilloid receptor function by metabotropic glutamate receptor 5: potential mechanism for thermal hyperalgesia. J Neurosci 22:7444–7452PubMedCrossRef
147.
go back to reference Johnson KW, Phebus LA, Cohen ML (1998) Serotonin in migraine: theories, animal models and emerging therapies. Prog Drug Res 51:219–244PubMedCrossRef Johnson KW, Phebus LA, Cohen ML (1998) Serotonin in migraine: theories, animal models and emerging therapies. Prog Drug Res 51:219–244PubMedCrossRef
148.
go back to reference Durham PL, Sharma RV, Russo AF (1997) Repression of the calcitonin gene-related peptide promoter by 5-HT1 receptor activation. J Neurosci 17:9545–9553PubMedCrossRef Durham PL, Sharma RV, Russo AF (1997) Repression of the calcitonin gene-related peptide promoter by 5-HT1 receptor activation. J Neurosci 17:9545–9553PubMedCrossRef
149.
go back to reference Cutrer FM, Yu XJ, Ayata G et al (1999) Effects of PNU-109,291, a selective 5-HT1D receptor agonist, on electrically induced dural plasma extravasation and capsaicin-evoked c-fos immunoreactivity within trigeminal nucleus caudalis. Neuropharmacology 38:1043–1053PubMedCrossRef Cutrer FM, Yu XJ, Ayata G et al (1999) Effects of PNU-109,291, a selective 5-HT1D receptor agonist, on electrically induced dural plasma extravasation and capsaicin-evoked c-fos immunoreactivity within trigeminal nucleus caudalis. Neuropharmacology 38:1043–1053PubMedCrossRef
150.
152.
go back to reference Lassen LH, Ashina M, Christiansen I et al (1997) Nitric oxide synthase inhibition in migraine. Lancet 349:401–402PubMedCrossRef Lassen LH, Ashina M, Christiansen I et al (1997) Nitric oxide synthase inhibition in migraine. Lancet 349:401–402PubMedCrossRef
155.
go back to reference Dimlich RV, Keller JT, Strauss TA, Fritts MJ (1991) Linear arrays of homogeneous mast cells in the dura mater of the rat. J Neurocytol 20:485–503PubMedCrossRef Dimlich RV, Keller JT, Strauss TA, Fritts MJ (1991) Linear arrays of homogeneous mast cells in the dura mater of the rat. J Neurocytol 20:485–503PubMedCrossRef
156.
go back to reference Sicuteri F, Ricci M, Monfardini R, Ficini M (1957) Experimental headache with endogeneous histamine; first results obtained by 48/80, a histamine-liberator drug, in the cephalic and peripheral circulatory systems of man. Physiol Asp Clin Neurol 11:188–192 Sicuteri F, Ricci M, Monfardini R, Ficini M (1957) Experimental headache with endogeneous histamine; first results obtained by 48/80, a histamine-liberator drug, in the cephalic and peripheral circulatory systems of man. Physiol Asp Clin Neurol 11:188–192
157.
160.
go back to reference Schwartz LB (1987) Mediators of human mast cells and human mast cell subsets. Ann Allergy 58:226–235PubMed Schwartz LB (1987) Mediators of human mast cells and human mast cell subsets. Ann Allergy 58:226–235PubMed
168.
go back to reference Rozniecki JJ, Dimitriadou V, Lambracht-Hall M et al (1999) Morphological and functional demonstration of rat dura mater mast cell-neuron interactions in vitro and in vivo. Brain Res 849:1–15PubMedCrossRef Rozniecki JJ, Dimitriadou V, Lambracht-Hall M et al (1999) Morphological and functional demonstration of rat dura mater mast cell-neuron interactions in vitro and in vivo. Brain Res 849:1–15PubMedCrossRef
170.
go back to reference Tani E, Senba E, Kokumai S et al (1990) Histamine application to the nasal mucosa induces release of calcitonin gene-related peptide and substance P from peripheral terminals of trigeminal ganglion: a morphological study in the guinea pig. Neurosci Lett 112:1–6PubMedCrossRef Tani E, Senba E, Kokumai S et al (1990) Histamine application to the nasal mucosa induces release of calcitonin gene-related peptide and substance P from peripheral terminals of trigeminal ganglion: a morphological study in the guinea pig. Neurosci Lett 112:1–6PubMedCrossRef
192.
go back to reference Hutchinson MR, Northcutt AL, Hiranita T (2012) Opioid activation of toll-like receptor 4 contributes to drug reinforcement. J Neurosci 32(33):11187–200 Hutchinson MR, Northcutt AL, Hiranita T (2012) Opioid activation of toll-like receptor 4 contributes to drug reinforcement. J Neurosci 32(33):11187–200
Metadata
Title
Neurogenic inflammation and its role in migraine
Author
Roshni Ramachandran
Publication date
01-05-2018
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 3/2018
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-018-0676-y

Other articles of this Issue 3/2018

Seminars in Immunopathology 3/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.