Role of calcitonin gene-related peptide and brain natriuretic peptide to modulate the excitability state of trigeminal neurons: relevance to migraine pathology and treatment

References

• Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science. 2000;288(5472):1765–1769.
   PubMed Web of Science ®Google Scholar
• Vos T, Flaxman AD, Naghavi M, et al. Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380(9859):2163–2196.
   PubMed Web of Science ®Google Scholar
• Stovner LJ, Hagen K. Prevalence, burden, and cost of headache disorders. Curr Opin Neurol. 2006;19(3):281–285.
   Web of Science ®Google Scholar
• Olesen J, Gustavsson A, Svensson M, Wittchen HU, Jönsson B, CDBE2010 study group; European Brain Council. The economic cost of brain disorders in Europe. Eur J Neurol. 2012;19(1):155–162.
   PubMed Web of Science ®Google Scholar
• Leonardi M, Steiner TJ, Scher AT, Lipton RB. The global burden of migraine: measuring disability in headache disorders with WHO’s classification of functioning, disability and health (ICF). J Headache Pain. 2005;6(6):429–440.
   PubMedGoogle Scholar
• Lipton RB, Bigal ME, Rush SR, et al. Migraine practice patterns among neurologists. Neurology. 2004;62(11):1926–1931.
   Web of Science ®Google Scholar
• Goadsby PJ, Charbit AR, Andreou AP, Akerman S, Holland PR. Neurobiology of migraine. Neuroscience. 2009;161(2):327–341.
   PubMed Web of Science ®Google Scholar
• Olesen J, Burstein R, Ashina M, Tfelt-Hansen P. Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol. 2009;8(7):679–690.
   PubMed Web of Science ®Google Scholar
• Levy D. Migraine pain and nociceptor activation – where do we stand? Headache. 2010;50(5):909–916.
   Web of Science ®Google Scholar
• Strassman AM, Raymond SA, Burstein R. Sensitization of meningeal sensory neurons and the origin of headaches. Nature. 1996;384(6609):560–564.
   PubMed Web of Science ®Google Scholar
• Levy D, Strassman AM. Distinct sensitizing effects of the cAMP-PKA second messenger cascade on rat dural mechanonociceptors. J Physiol. 2002;538(pt 2):483–493.
   PubMed Web of Science ®Google Scholar
• Davis KD, Meyer RA, Campbell JN. Chemosensitivity and sensitization of nociceptive afferents that innervate the hairy skin of monkey. J Neurophysiol. 1993;69(4):1071–1081.
   Web of Science ®Google Scholar
• Blau JN, Dexter SL. The site of pain origin during migraine attacks. Cephalalgia. 1981;1(3):143–147.
   Web of Science ®Google Scholar
• Rasmussen BK, Jensen R, Olesen J. A population-based analysis of the diagnostic criteria of the international headache society. Cephalalgia. 1991;11(3):129–134.
   Web of Science ®Google Scholar
• Viana F. Chemosensory properties of the trigeminal system. ACS Chem Neurosci. 2011;2(1):38–50.
   PubMed Web of Science ®Google Scholar
• Bigal ME, Walter S, Rapoport AM. Calcitonin gene-related peptide (CGRP) and migraine current understanding and state of development. Headache. 2013;53(8):1230–1244.
   PubMed Web of Science ®Google Scholar
• Russell FA, King R, Smillie S-J, Kodji X, Brain SD. Calcitonin gene-related peptide: physiology and pathophysiology. Physiol Rev. 2014;94(4):1099–1142.
   PubMed Web of Science ®Google Scholar
• Akiyama T, Carstens E. Neural processing of itch. Neuroscience. 2013;250:697–714.
   PubMed Web of Science ®Google Scholar
• Mishra SK, Hoon MA. The cells and circuitry for itch responses in mice. Science. 2013;340(6135):968–971.
   PubMed Web of Science ®Google Scholar
• Yan J, Dussor G. Ion channels and migraine. Headache. 2014;54(4):619–639.
   PubMed Web of Science ®Google Scholar
• Guo A, Vulchanova L, Wang J, Li X, Elde R. Immunocytochemical localization of the vanilloid receptor 1 (VR1):relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci. 1999;11(3):946–958.
   Web of Science ®Google Scholar
• Simonetti M, Fabbro A, D’Arco M, et al. Comparison of P2X and TRPV1 receptors in ganglia or primary culture of trigeminal neurons and their modulation by NGF or serotonin. Mol Pain. 2006;2:11.
   PubMed Web of Science ®Google Scholar
• Holland PR, Akerman S, Andreou AP, Karsan N, Wemmie JA, Goadsby PJ. Acid-sensing ion channel 1: a novel therapeutic target for migraine with aura. Ann Neurol. 2012;72(4):559–563.
   Web of Science ®Google Scholar
• Benemei S, De Cesaris F, Fusi C, Rossi E, Lupi C, Geppetti P. TRPA1 and other TRP channels in migraine. J Headache Pain. 2013;14:71.
   Web of Science ®Google Scholar
• Kelman L. The triggers or precipitants of the acute migraine attack. Cephalalgia. 2007;27(5):394–402.
   PubMed Web of Science ®Google Scholar
• Nassini R, Materazzi S, Vriens J, et al. The “headache tree” via umbellulone and TRPA1 activates the trigeminovascular system. Brain. 2012;135(pt 2):376–390.
   PubMedGoogle Scholar
• Wantke F, Focke M, Hemmer W, et al. Exposure to formaldehyde and phenol during an anatomy dissecting course: sensitizing potency of formaldehyde in medical students. Allergy. 2000;55(1):84–87.
   Web of Science ®Google Scholar
• Irlbacher K, Meyer B-U. Nasally triggered headache. Neurology. 2002; 58(2):294.
   Web of Science ®Google Scholar
• Huang D, Li S, Dhaka A, Story GM, Cao Y-Q. Expression of the transient receptor potential channels TRPV1, TRPA1 and TRPM8 in mouse trigeminal primary afferent neurons innervating the dura. Mol Pain. 2012;8:66.
   Web of Science ®Google Scholar
• Kunkler PE, Ballard CJ, Pellman JJ, Zhang L, Oxford GS, Hurley JH. Intraganglionic signaling as a novel nasal-meningeal pathway for TRPA1-dependent trigeminovascular activation by inhaled environmental irritants. PLoS One. 2014;9(7):e103086.
   Web of Science ®Google Scholar
• Wei X, Edelmayer RM, Yan J, Dussor G. Activation of TRPV4 on dural afferents produces headache-related behavior in a preclinical rat model. Cephalalgia. 2011;31(16):1595–1600.
   Web of Science ®Google Scholar
• Chen Y, Kanju P, Fang Q, et al. TRPV4 is necessary for trigeminal irritant pain and functions as a cellular formalin receptor. Pain. Epub 2014 Oct 2.
   Google Scholar
• Mälkiä A, Morenilla-Palao C, Viana F. The emerging pharmacology of TRPM8 channels: hidden therapeutic potential underneath a cold surface. Curr Pharm Biotechnol. 2011;12(1):54–67.
   Web of Science ®Google Scholar
• Chasman DI, Schürks M, Anttila V, et al. Genome-wide association study reveals three susceptibility loci for common migraine in the general population. Nat Genet. 2011;43(7):695–698.
   PubMed Web of Science ®Google Scholar
• Caterina MJ, Leffler A, Malmberg AB, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 2000; 288(5464):306–313.
   PubMed Web of Science ®Google Scholar
• Davis JB, Gray J, Gunthorpe MJ, et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature. 2000;405(6783):183–187.
   PubMed Web of Science ®Google Scholar
• Gavva NR, Tamir R, Qu Y, et al. AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3-dihydrobenzo[b][1,4] dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties. J Pharmacol Exp Ther. 2005;313(1):474–484.
   PubMed Web of Science ®Google Scholar
• Russo EB. Clinical endocannabinoid deficiency (CECD):can this concept explain therapeutic benefits of cannabis in migraine, fibromyalgia, irritable bowel syndrome and other treatment-resistant conditions? Neuro Endocrinol Lett. 2008;29(2):192–200.
   PubMed Web of Science ®Google Scholar
• Sarchielli P, Pini LA, Coppola F, et al. Endocannabinoids in chronic migraine: CSF findings suggest a system failure. Neuropsychopharmacology. 2007;32(6):1384–1390.
   Web of Science ®Google Scholar
• Akerman S, Kaube H, Goadsby PJ. Anandamide acts as a vasodilator of dural blood vessels in vivo by activating TRPV1 receptors. Br J Pharmacol. 2004;142(8):1354–1360.
   Web of Science ®Google Scholar
• Akerman S, Kaube H, Goadsby PJ. Anandamide is able to inhibit trigeminal neurons using an in vivo model of trigeminovascular-mediated nociception. J Pharmacol Exp Ther. 2004;309(1):56–63.
   Web of Science ®Google Scholar
• Piomelli D. More surprises lying ahead. The endocannabinoids keep us guessing. Neuropharmacology. 2014;76(pt B):228–234.
   PubMedGoogle Scholar
• Burnstock G. The role of adenosine triphosphate in migraine. Biomed Pharmacother. 1989;43(10):727–736.
   Web of Science ®Google Scholar
• Vulchanova L, Riedl MS, Shuster SJ, et al. Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology. 1997;36(9):1229–1242.
   Web of Science ®Google Scholar
• Llewellyn-Smith IJ, Burnstock G. Ultrastructural localization of P2X3 receptors in rat sensory neurons. Neuroreport. 1998;9(11):2545–2550.
   Web of Science ®Google Scholar
• Burnstock G. Purinergic receptors and pain. Curr Pharm Des. 2009; 15(15):1717–1735.
   PubMed Web of Science ®Google Scholar
• Fabbretti E, Nistri A. Regulation of P2X3 receptor structure and function. CNS Neurol Disord Drug Targets. 2012;11(6):687–698.
   Web of Science ®Google Scholar
• Saloman JL, Chung M-K, Ro JY. P2X3 and TRPV1 functionally interact and mediate sensitization of trigeminal sensory neurons. Neuroscience. 2013;232:226–238.
   Web of Science ®Google Scholar
• Yang Z, Cao Y, Wang Y, et al. Behavioural responses and expression of P2X3 receptor in trigeminal ganglion after experimental tooth movement in rats. Arch Oral Biol. 2009;54(1):63–70.
   Web of Science ®Google Scholar
• Oliveira MCG, Parada CA, Veiga MCFA, Rodrigues LR, Barros SP, Tambeli CH. Evidence for the involvement of endogenous ATP and P2X receptors in TMJ pain. Eur J Pain. 2005;9(1):87–93.
   Web of Science ®Google Scholar
• Ford AP. In pursuit of P2X3 antagonists: novel therapeutics for chronic pain and afferent sensitization. Purinergic Signal. 2012;8(Suppl 1):3–26.
   PubMedGoogle Scholar
• Masterson CG, Durham PL. DHE repression of ATP-mediated sensitization of trigeminal ganglion neurons. Headache. 2010;50(9):1424–1439.
   Web of Science ®Google Scholar
• Gribkoff VK, Starrett JE, Dworetzky SI. Maxi-K potassium channels: form, function, and modulation of a class of endogenous regulators of intracellular calcium. Neurosci Rev. 2001;7(2):166–177.
   Google Scholar
• Akerman S, Holland PR, Lasalandra MP, Goadsby PJ. Inhibition of trigeminovascular dural nociceptive afferents by Ca2+-activated K+ (MaxiK/BK(Ca)) channel opening. Pain. 2010;151(1):128–136.
   PubMed Web of Science ®Google Scholar
• Enyedi P, Czirják G. Molecular background of leak K+ currents: two-pore domain potassium channels. Physiol Rev. 2010;90(2):559–605.
   PubMed Web of Science ®Google Scholar
• Lafrenière RG, Cader MZ, Poulin JF, et al. A dominant-negative mutation in the TRESK potassium channel is linked to familial migraine with aura. Nat Med. 2010;16(10):1157–1160.
   PubMed Web of Science ®Google Scholar
• Andres-Enguix I, Shang L, Stansfeld PJ, et al. Functional analysis of missense variants in the TRESK (KCNK18) K channel. Sci Rep. 2012;2:237.
   PubMed Web of Science ®Google Scholar
• Ophoff RA, Terwindt GM, Vergouwe MN, et al. Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell. 1996;87(3):543–552.
   PubMed Web of Science ®Google Scholar
• van denMaagdenberg AM, Pietrobon D, Pizzorusso T, et al. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron. 2004;41(5):701–710.
   Web of Science ®Google Scholar
• Tottene A, Conti R, Fabbro A, et al. Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron. 2009;61(5):762–773.
   Web of Science ®Google Scholar
• Pietrobon D, Moskowitz MA. Pathophysiology of migraine. Annu Rev Physiol. 2013;75:365–391.
   PubMed Web of Science ®Google Scholar
• Franceschini A, Vilotti S, Ferrari MD, van den Maagdenberg AMJM, Nistri A, Fabbretti E. TNFα levels and macrophages expression reflect an inflammatory potential of trigeminal ganglia in a mouse model of familial hemiplegic migraine. PLoS One. 2013;8(1):e52394.
   PubMed Web of Science ®Google Scholar
• Ceruti S, Villa G, Fumagalli M, et al. Calcitonin gene-related peptide-mediated enhancement of purinergic neuron/glia communication by the algogenic factor bradykinin in mouse trigeminal ganglia from wild-type and R192Q Cav2.1 Knock-in mice: implications for basic mechanisms of migraine pain. J Neurosci. 2011;31(10):3638–3649.
   PubMed Web of Science ®Google Scholar
• Franceschini A, Nair A, Bele T, van den Maagdenberg AM, Nistri A, Fabbretti E. Functional crosstalk in culture between macrophages and trigeminal sensory neurons of a mouse genetic model of migraine. BMC Neurosci. 2012;13:143.
   Web of Science ®Google Scholar
• Franceschini A, Hullugundi SK, van den Maagdenberg AMJM, Nistri A, Fabbretti E. Effects of LPS on P2X3 receptors of trigeminal sensory neurons and macrophages from mice expressing the R192Q Cacna1a gene mutation of familial hemiplegic migraine-1. Purinergic Signal. 2013;9(1):7–13.
   Web of Science ®Google Scholar
• Bø SH, Davidsen EM, Gulbrandsen P, et al. Cerebrospinal fluid cytokine levels in migraine, tension-type headache and cervicogenic headache. Cephalalgia. 2009;29(3):365–372.
   PubMed Web of Science ®Google Scholar
• Ishizaki K, Takeshima T, Fukuhara Y, et al. Increased plasma transforming growth factor-beta1 in migraine. Headache. 2005;45(9):1224–1228.
   Web of Science ®Google Scholar
• Tanure MTA, Gomez RS, Hurtado RCL, Teixeira AL, Domingues RB. Increased serum levels of brain-derived neurotropic factor during migraine attacks: a pilot study. J Headache Pain. 2010;11(5):427–430.
   PubMed Web of Science ®Google Scholar
• Steen KH, Reeh PW, Anton F, Handwerker HO. Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J Neurosci. 1992;12(1):86–95.
   Web of Science ®Google Scholar
• Obreja O, Schmelz M, Poole S, Kress M. Interleukin-6 in combination with its soluble IL-6 receptor sensitises rat skin nociceptors to heat, in vivo. Pain. 2002;96(1–2):57–62.
   Web of Science ®Google Scholar
• Sachs D, Cunha FQ, Poole S, Ferreira SH. Tumour necrosis factor-alpha, interleukin-1beta and interleukin-8 induce persistent mechanical nociceptor hypersensitivity. Pain. 2002;96(1–2):89–97.
   Web of Science ®Google Scholar
• Olesen J, Thomsen LL, Iversen H. Nitric oxide is a key molecule in migraine and other vascular headaches. Trends Pharmacol Sci. 1994;15(5):149–153.
   PubMed Web of Science ®Google Scholar
• Belmonte C, Gallar J, Pozo MA, Rebollo I. Excitation by irritant chemical substances of sensory afferent units in the cat’s cornea. J Physiol. 1991;437:709–725.
   PubMed Web of Science ®Google Scholar
• Pozo MA, Gallego R, Gallar J, Belmonte C. Blockade by calcium antagonists of chemical excitation and sensitization of polymodal nociceptors in the cat’s cornea. J Physiol. 1992;450:179–189.
   PubMed Web of Science ®Google Scholar
• Olesen J, Diener HC, Husstedt IW, et al; BIBN 4096 BS Clinical Proof of Concept Study Group. Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N Engl J Med. 2004;350(11):1104–1110.
   PubMed Web of Science ®Google Scholar
• Terenghi G, Polak JM, Ghatei MA, et al. Distribution and origin of calcitonin gene-related peptide (CGRP) immunoreactivity in the sensory innervation of the mammalian eye. J Comp Neurol. 1985;233(4):506–516.
   Web of Science ®Google Scholar
• Alevizaki M, Shiraishi A, Rassool FV, Ferrier GJ, MacIntyre I, Legon S. The calcitonin-like sequence of the beta CGRP gene. FEBS Lett. 1986;206(1):47–52.
   Web of Science ®Google Scholar
• Noguchi K, Senba E, Morita Y, Sato M, Tohyama M. α-CGRP and β-CGRP mRNAs are differentially regulated in the rat spinal cord and dorsal root ganglion. Brain Res. 1990;7(4):299–304.
   Web of Science ®Google Scholar
• Watkins HA, Rathbone DL, Barwell J, Hay DL, Poyner DR. Structure-activity relationships for α-calcitonin gene-related peptide. Br J Pharmacol. 2013;170(7):1308–1322.
   Web of Science ®Google Scholar
• Juaneda C, Dumont Y, Quirion R. The molecular pharmacology of CGRP and related peptide receptor subtypes. Trends Pharmacol Sci. 2000;21(11):432–438.
   PubMed Web of Science ®Google Scholar
• Goadsby PJ, Edvinsson L, Ekman R. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann Neurol. 1990;28(2):183–187.
   PubMed Web of Science ®Google Scholar
• 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(3):901–907.
   Web of Science ®Google Scholar
• Bowen EJ, Schmidt TW, Firm CS, Russo AF, Durham PL. Tumor necrosis factor-α stimulation of calcitonin gene-related peptide expression and secretion from rat trigeminal ganglion neurons. J Neurochem. 2006;96(1):65–77.
   Web of Science ®Google Scholar
• Mason RT, Peterfreund RA, Sawchenko PE, Corrigan AZ, Rivier JE, Vale WW. Release of the predicted calcitonin gene-related peptide from cultured rat trigeminal ganglion cells. Nature. 1984;308(5960):653–655.
   Web of Science ®Google Scholar
• Messlinger K, Fischer MJM, Lennerz JK. Neuropeptide effects in the trigeminal system: pathophysiology and clinical relevance in migraine. Keio J Med. 2011;60(3):82–89.
   PubMedGoogle Scholar
• Giniatullin R, Nistri A, Fabbretti E. Molecular mechanisms of sensitization of pain-transducing P2X3 receptors by the migraine mediators CGRP and NGF. Mol Neurobiol. 2008;37(1):83–90.
   Web of Science ®Google Scholar
• Raddant AC, Russo AF. Calcitonin gene-related peptide in migraine: intersection of peripheral inflammation and central modulation. Expert Rev Mol Med. 2011;13:e36.
   PubMed Web of Science ®Google Scholar
• Vause CV, Durham PL. CGRP stimulation of iNOS and NO release from trigeminal ganglion glial cells involves mitogen-activated protein kinase pathways. J Neurochem. 2009;110(3):811–821.
   Web of Science ®Google Scholar
• Thalakoti S, Patil VV, Damodaram S, et al. Neuron-glia signaling in trigeminal ganglion: implications for migraine pathology. Headache. 2007;47(7):1008–1023; [discussion 24–25].
   PubMed Web of Science ®Google Scholar
• Lennerz JK, Rühle V, Ceppa EP, 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(3):1277–1299.
   PubMed Web of Science ®Google Scholar
• Tso AR, Goadsby PJ. New targets for migraine therapy. Curr Treat Options Neurol. 2014;16(11):318.
   Web of Science ®Google Scholar
• Lassen LH, Haderslev PA, Jacobsen VB, Iversen HK, Sperling B, Olesen J. CGRP may play a causative role in migraine. Cephalalgia. 2002;22(1):54–61.
   PubMed Web of Science ®Google Scholar
• Capuano A, De Corato A, Lisi L, Tringali G, Navarra P, Dello Russo C. Proinflammatory-activated trigeminal satellite cells promote neuronal sensitization: relevance for migraine pathology. Mol Pain. 2009;5:43.
   PubMed Web of Science ®Google Scholar
• Fabbretti E, D’Arco M, Fabbro A, Simonetti M, Nistri A, Giniatullin R. Delayed upregulation of ATP P2X3 receptors of trigeminal sensory neurons by calcitonin gene-related peptide. J Neurosci. 2006;26(23):6163–6171.
   PubMed Web of Science ®Google Scholar
• Greco R, Gasperi V, Maccarrone M, Tassorelli C. The endocannabinoid system and migraine. Exp Neurol. 2010;224(1):85–91.
   PubMed Web of Science ®Google Scholar
• Akerman S, Holland PR, Lasalandra MP, Goadsby PJ. Endocannabinoids in the brainstem modulate dural trigeminovascular nociceptive traffic via CB1 and “triptan” receptors: implications in migraine. J Neurosci. 2013;33(37):14869–14877.
   Web of Science ®Google Scholar
• Cady RJ, Glenn JR, Smith KM, Durham PL. Calcitonin gene-related peptide promotes cellular changes in trigeminal neurons and glia implicated in peripheral and central sensitization. Mol Pain. 2011;7:94.
   Web of Science ®Google Scholar
• Simonetti M, Giniatullin R, Fabbretti E. Mechanisms mediating the enhanced gene transcription of P2X3 receptor by calcitonin gene-related peptide in trigeminal sensory neurons. J Biol Chem. 2008; 283(27):18743–18752.
   PubMed Web of Science ®Google Scholar
• Fischer M, Wille G, Klien S, et al. Brain-derived neurotrophic factor in primary headaches. J Headache Pain. 2012;13(6):469–475.
   PubMed Web of Science ®Google Scholar
• Buldyrev I, Tanner NM, Hsieh H, Dodd EG, Nguyen LT, Balkowiec A. Calcitonin gene-related peptide enhances release of native brain-derived neurotrophic factor from trigeminal ganglion neurons. J Neurochem. 2006;99(5):1338–1350.
   PubMed Web of Science ®Google Scholar
• Nair A, Simonetti M, Birsa N, et al. Familial hemiplegic migraine Ca(v)2.1 channel mutation R192Q enhances ATP-gated P2X3 receptor activity of mouse sensory ganglion neurons mediating trigeminal pain. Mol Pain. 2010;6:48.
   Web of Science ®Google Scholar
• Fioretti B, Catacuzzeno L, Sforna L, et al. Trigeminal ganglion neuron subtype-specific alterations of Ca(V)2.1 calcium current and excitability in a Cacna1a mouse model of migraine. J Physiol. 2011;589(pt 23):5879–5895.
   Web of Science ®Google Scholar
• Moore EL, Salvatore CA. Targeting a family B GPCR/RAMP receptor complex: CGRP receptor antagonists and migraine. Br J Pharmacol. 2012;166(1):66–78.
   PubMed Web of Science ®Google Scholar
• Doods H, Hallermayer G, Wu D, et al. Pharmacological profile of BIBN4096BS, the first selective small molecule CGRP antagonist. Br J Pharmacol. 2000;129(3):420–423.
   PubMed Web of Science ®Google Scholar
• Li J, Wang DH. Development of angiotensin II-induced hypertension: role of CGRP and its receptor. J Hypertens. 2005;23(1):113–118.
   Web of Science ®Google Scholar
• Salvatore CA, Moore EL, Calamari A, et al. Pharmacological properties of MK-3207, a potent and orally active calcitonin gene-related peptide receptor antagonist. J Pharmacol Exp Ther. 2010;333(1):152–160.
   PubMed Web of Science ®Google Scholar
• Diener H-C, Barbanti P, Dahlöf C, Reuter U, Habeck J, Podhorna J. BI 44370 TA, an oral CGRP antagonist for the treatment of acute migraine attacks: results from a phase II study. Cephalalgia. 2011; 31(5):573–584.
   PubMed Web of Science ®Google Scholar
• Luo G, Chen L, Conway CM, et al. Discovery of (5S,6S,9R)-5-amino-6-(2,3-difluorophenyl)-6,7,8,9-tetrahydro-5H-cyclohepta[b]pyridin-9-yl 4-(2-oxo-2,3-dihydro-1H-imidazo[4,5-b]pyridin-1-yl)piperidine-1-carboxylate (BMS-927711):an oral calcitonin gene-related peptide (CGRP) antagonist in clinical trials for treating migraine. J Med Chem. 2012;55(23):10644–10651.
   PubMed Web of Science ®Google Scholar
• Marcus R, Goadsby PJ, Dodick D, Stock D, Manos G, Fischer TZ. BMS-927711 for the acute treatment of migraine: a double-blind, randomized, placebo controlled, dose-ranging trial. Cephalalgia. 2014;34(2):114–125.
   PubMed Web of Science ®Google Scholar
• Benschop RJ, Collins EC, Darling RJ, et al. Development of a novel antibody to calcitonin gene-related peptide for the treatment of osteoarthritis-related pain. Osteoarthritis Cartilage. 2014;22(4):578–585.
   PubMed Web of Science ®Google Scholar
• Dodick DW, Goadsby PJ, Spierings ELH, Scherer JC, Sweeney SP, Grayzel DS. Safety and efficacy of LY2951742, a monoclonal antibody to calcitonin gene-related peptide, for the prevention of migraine: a phase 2, randomised, double-blind, placebo-controlled study. Lancet Neurol. 2014;13(9):885–892.
   PubMed Web of Science ®Google Scholar
• Amgen. A phase 2 study to evaluate the efficacy and safety of AMG 334 in migraine prevention; 2013. Available from: http://clinicaltrials.gov/show/NCT01952574 NLM identifier: NCT01952574. Accessed August 30, 2013.
   Google Scholar
• Bigal ME, Escandon R, Bronson M, et al. Safety and tolerability of LBR-101, a humanized monoclonal antibody that blocks the binding of CGRP to its receptor: results of the phase 1 program. Cephalalgia. 2013;34(7):483–492.
   Web of Science ®Google Scholar
• Petersen KA, Birk S, Lassen LH, et al. The CGRP-antagonist, BIBN4096BS does not affect cerebral or systemic haemodynamics in healthy volunteers. Cephalalgia. 2005;25(2):139–147.
   PubMed Web of Science ®Google Scholar
• Petersen KA, Lassen LH, Birk S, Lesko L, Olesen J. BIBN4096BS antagonizes human alpha-calcitonin gene related peptide-induced headache and extracerebral artery dilatation. Clin Pharmacol Ther. 2005;77(3):202–213.
   PubMed Web of Science ®Google Scholar
• Arulmani U, Schuijt MP, Heiligers JPC, Willems EW, Villalón CM, Saxena PR. Effects of the calcitonin gene-related peptide (CGRP) receptor antagonist BIBN4096BS on alpha-CGRP-induced regional haemodynamic changes in anaesthetised rats. Basic Clin Pharmacol Toxicol. 2004;94(6):291–297.
   PubMed Web of Science ®Google Scholar
• Negro A, Lionetto L, Simmaco M, Martelletti P. CGRP receptor antagonists: an expanding drug class for acute migraine? Expert Opin Investig Drugs. 2012;21(6):807–818.
   PubMed Web of Science ®Google Scholar
• Hewitt DJ, Aurora SK, Dodick DW, et al. Randomized controlled trial of the CGRP receptor antagonist MK-3207 in the acute treatment of migraine. Cephalalgia. 2011;31(6):712–722.
   PubMed Web of Science ®Google Scholar
• Hostetler ED, Joshi AD, Sanabria-Bohórquez S, et al. In vivo quantification of calcitonin gene-related peptide receptor occupancy by telcagepant in rhesus monkey and human brain using the positron emission tomography tracer [11C]MK-4232. J Pharmacol Exp Ther. 2013;347(2):478–486.
   PubMed Web of Science ®Google Scholar
• Sixt M-L, Messlinger K, Fischer MJM. Calcitonin gene-related peptide receptor antagonist olcegepant acts in the spinal trigeminal nucleus. Brain. 2009;132(pt 11):3134–3141.
   Google Scholar
• Asghar MS, Hansen AE, Kapijimpanga T, et al. Dilation by CGRP of middle meningeal artery and reversal by sumatriptan in normal volunteers. Neurology. 2010;75(17):1520–1526.
   PubMed Web of Science ®Google Scholar
• Asghar MS, Hansen AE, Larsson HBW, Olesen J, Ashina M. Effect of CGRP and sumatriptan on the BOLD response in visual cortex. J Headache Pain. 2012;13(2):159–166.
   Web of Science ®Google Scholar
• Dodick DW, Goadsby PJ, Silberstein SD, et al; ALD403 study investigators. Safety and efficacy of ALD403, an antibody to calcitonin gene-related peptide, for the prevention of frequent episodic migraine: a randomised, double-blind, placebo-controlled, exploratory phase 2 trial. Lancet Neurol. 2014;13(11):1100–1107.
   PubMed Web of Science ®Google Scholar
• Leavy O. Therapeutic antibodies: past, present and future. Nat Rev Immunol. 2010;10(5):297.
   PubMed Web of Science ®Google Scholar
• Sela-Culang I, Kunik V, Ofran Y. The structural basis of antibody-antigen recognition. Front Immunol. 2013;4:302.
   PubMed Web of Science ®Google Scholar
• Niebecker R, Kloft C. Safety of therapeutic monoclonal antibodies. Curr Drug Saf. 2010;5(4):275–286.
   PubMedGoogle Scholar
• Ho TW, Connor KM, Zhang Y, et al. Randomized controlled trial of the CGRP receptor antagonist telcagepant for migraine prevention. Neurology. 2014;83(11):958–966.
   PubMed Web of Science ®Google Scholar
• Loo L, Shepherd AJ, Mickle AD, et al. The C-type natriuretic peptide induces thermal hyperalgesia through a noncanonical Gβγ-dependent modulation of TRPV1 channel. J Neurosci. 2012;32(35):11942–11955.
   Web of Science ®Google Scholar
• Zhang FX, Liu XJ, Gong LQ, et al. Inhibition of inflammatory pain by activating B-type natriuretic peptide signal pathway in nociceptive sensory neurons. J Neurosci Off J Soc Neurosci. 2010;30(32):10927–10938.
   Web of Science ®Google Scholar
• Heine S, Michalakis S, Kallenborn-Gerhardt W, et al. CNGA3: a target of spinal nitric oxide/cGMP signaling and modulator of inflammatory pain hypersensitivity. J Neurosci. 2011;31(31):11184–11192.
   Web of Science ®Google Scholar
• Schmidtko A, Gao W, König P, et al. cGMP produced by NO-sensitive guanylyl cyclase essentially contributes to inflammatory and neuropathic pain by using targets different from cGMP-dependent protein kinase I. J Neurosci. 2008;28(34):8568–8576.
   Web of Science ®Google Scholar
• Woodard GE, Rosado JA. Natriuretic peptides in vascular physiology and pathology. Int Rev Cell Mol Biol. 2008;268:59–93.
   PubMed Web of Science ®Google Scholar
• Potter LR, Yoder AR, Flora DR, Antos LK, Dickey DM. Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handb Exp Pharmacol. 2009;191:341–366.
   PubMedGoogle Scholar
• Potter LR. Domain analysis of human transmembrane guanylyl cyclase receptors: implications for regulation. Front Biosci. 2005;10:1205–1220.
   Web of Science ®Google Scholar
• Choudhuri R, Cui L, Yong C, et al. Cortical spreading depression and gene regulation: relevance to migraine. Ann Neurol. 2002;51(4):499–506.
   Web of Science ®Google Scholar
• Uzar E, Evliyaoglu O, Yucel Y, et al. Serum cytokine and pro-brain natriuretic peptide (BNP) levels in patients with migraine. Eur Rev Med Pharmacol Sci. 2011;15(10):1111–1116.
   PubMed Web of Science ®Google Scholar
• Padayatti PS, Pattanaik P, Ma X, van den Akker F. Structural insights into the regulation and the activation mechanism of mammalian guanylyl cyclases. Pharmacol Ther. 2004;104(2):83–99.
   Web of Science ®Google Scholar
• Andrade FA, Restini CBA, Grando MD, Ramalho LNZ, Bendhack LM. Vascular relaxation induced by C-type natriuretic peptide involves the ca2+/NO-synthase/NO pathway. PLoS One. 2014;9(5):e95446.
   Web of Science ®Google Scholar
• D’Souza SP, Davis M, Baxter GF. Autocrine and paracrine actions of natriuretic peptides in the heart. Pharmacol Ther. 2004;101(2):113–129.
   Web of Science ®Google Scholar
• Guo S, Barringer F, Zois NE, Goetze JP, Ashina M. Natriuretic peptides and cerebral hemodynamics. Regul Pept. 2014;192–193:15–23.
   Google Scholar
• Abdelalim EM, Tooyama I. NPR-A regulates self-renewal and pluripotency of embryonic stem cells. Cell Death Dis. 2011;2:e127.
   Web of Science ®Google Scholar
• Vilotti S, Marchenkova A, Ntamati N, Nistri A. B-type natriuretic peptide-induced delayed modulation of TRPV1 and P2X3 receptors of mouse trigeminal sensory neurons. PLoS One. 2013;8(11):e81138.
   Web of Science ®Google Scholar