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Mechanisms of Action of the 5-HT1B/1D Receptor Agonists

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Mechanisms of Action of the 5-HT1B/1D Receptor Agonists NEUROLOGICAL REVIEW SECTION EDITOR: DAVID E. PLEASURE, MD Mechanisms of Action of the 5-HT1B/1D Receptor Agonists Stewart J. Tepper, MD; Alan M. Rapoport, MD; Fred D. Sheftell, MD ecent studies of the pathophysiology of migraine provide evidence that the headache phase is associated with multiple physiologic actions. These actions include the release of va- soactive neuropeptides by the trigeminovascular system, vasodilation of intracranial ex- tracerebral vessels, and increased nociceptive neurotransmission within the central tri- Rgeminocervical complex. The 5-HT1B/1D receptor agonists, collectively known as triptans, are a major advance in the treatment of migraine. The beneficial effects of the triptans in patients with migraine are related to their multiple mechanisms of action at sites implicated in the pathophysiology of mi- graine. These mechanisms are mediated by 5-HT1B/1D receptors and include vasoconstriction of pain- fully dilated cerebral blood vessels, inhibition of the release of vasoactive neuropeptides by trigemi- nal nerves, and inhibition of nociceptive neurotransmission. The high affinity of the triptans for 5-HT1B/1D receptors and their favorable pharmacologic properties contribute to the beneficial effects of these drugs, including rapid onset of action, effective relief of headache and associated symptoms, and low incidence of adverse effects. Arch Neurol. 2002;59:1084-1088 The pathophysiology of migraine is fairly Increased understanding of the patho- well understood, and evidence supports physiology of migraine has led to the de- contributory roles of both neural and vas- velopment of improved migraine treat- cular mechanisms. The manifestation of ments such as the 5-HT1B/1D receptor headache in migraineurs is probably as- agonists, collectively known as triptans. sociated with activation of the trigemino- The emergence of the triptans has revo- vascular system, followed by the release lutionalized the management of mi- of vasodilatory neuropeptides. Changes in graine by providing options for the highly circulating levels of the neurotransmitter selective stimulation of 5-HT1B/1D recep- serotonin (5-HT) are characteristic of mi- tors, while reducing or eliminating un- graine and may contribute to the patho- wanted activity at other receptor sub- genesis of the disorder. Recent progress in types, thus improving therapeutic understanding the pathophysiology of mi- tolerability. This article focuses on the graine includes the identification of the mechanisms of action of the triptans in re- physiologic roles of vasoactive neuropep- lation to current concepts of the patho- tides associated with migraine and the physiology of migraine and the clinical role characterization of 5-HT receptor sub- of these drugs in the management of pa- types. tients with migraine. From the New England Center for Headache, Stamford, Conn (Drs Tepper, Rapoport, PATHOPHYSIOLOGY OF MIGRAINE and Sheftell); the Department of Neurology, Yale University School of Medicine, New Haven, Conn (Drs Tepper and Rapoport); and the Department of Psychiatry, New York The manifestation of headache in mi- Medical College, Valhalla (Dr Sheftell). Drs Tepper, Rapoport, and Sheftell are consultants for GlaxoSmithKline, Merck, AstraZeneca, and Pharmacia; conduct graineurs has been attributed to activa- research for GlaxoSmithKline, Merck, AstraZeneca, Pharmacia, Allergan, Elan, and tion of the sensory trigeminovascular OrthoMcNeill; and are on the speakers bureau for GlaxoSmithKline, Merck, and system and the subsequent release of va- 1 AstraZeneca. Dr Rapoport is also a consultant for Abbott, Pfizer, Forest Laboratories, soactive neuropeptides. In the geneti- Elan, and Bristol-Myers Squibb. Dr Sheftell is also a consultant for Pfizer. cally susceptible patient, activation of the (REPRINTED) ARCH NEUROL / VOL 59, JULY 2002 WWW.ARCHNEUROL.COM 1084 ©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/27/2021 trigeminovascular system can be initiated by a variety of layed, migraine-like headache several hours after dos- triggers, including stress, certain foods or drugs, odors, ing—a headache not seen when healthy control patients trauma, and changes in sleep habits. The release of va- are given nitroglycerin, which suggests an increased vul- soactive substances from trigeminal nerve terminals in nerability in migraineurs to one or more of the toxic ef- patients with migraine induces inflammatory reactions fects of nitric oxide, including enzyme inhibition and the in meningeal blood vessels, characterized by vasodila- formation of peroxynitrate with lipid peroxidation.9 tion, plasma protein extravasation, and activation of tri- geminovascular afferents.2 Studies in animals support the 5-HT RECEPTORS observation that pain-producing intracranial extracere- bral vessels in the dura mater (peripherally), not the brain, The role of 5-HT in migraine is supported by the obser- are responsible for the generation of headache in pa- vations that urinary and platelet 5-HT levels decrease, and tients with migraine.3 that circulating levels of 5-hydroxyindoleacetic acid (5- Vasoactive neuropeptides found within the trigemi- HIAA), the major metabolite of 5-HT, increase during mi- nal neurons that innervate intracranial blood vessels and graine.10 The ability of 5-HT–depleting and 5-HT– contribute to the manifestation of head pain in mi- releasing agents such as reserpine and fenfluramine to graineurs include calcitonin gene-related peptide (CGRP), induce migraine-like symptoms provides further evi- substance P, and neurokinin A. Calcitonin gene-related dence of the role of serotonin in the pathophysiology of peptide is the most potent vasodilator neurotransmitter migraine.11 Intravenous infusion of 5-HT aborts both re- mapped to the trigeminal system, and its action is endo- serpine-induced and spontaneous headache, but the clini- thelium independent.4 Substance P, a nondecapeptide in- cal use of 5-HT in migraine is precluded by significant volved in nociceptive transmission, has endothelium- untoward effects.11 dependent vasodilatory effects on the cerebrovascular The 5-HT receptors are highly heterogeneous, bed.5 Neurokinin A is a decapeptide with a profile of ac- broadly distributed, and classified into 7 different fami- tion and localization in the trigeminal system that is simi- lies on the basis of their amino acid sequences and other 12 lar to that of substance P but with less potent vasodila- properties. The 5-HT1 receptors are the largest subfam- tory effects and longer-lasting effects on blood vessel ily of 5-HT receptors and typically demonstrate a high 6 permeability. The critical neuropeptide in the genera- affinity for 5-HT. The 5-HT1 receptors are further sub- tion of migraine seems to be CGRP rather than sub- divided according to their physiologic functions, bind- stance P or neurokinin A. ing affinity, and other features. Neurogenic inflammation within the meninges has The cloning of 5-HT1 receptors and the develop- been suggested as a potential model to explain the source ment of 5-HT receptor agonists with specific affinity for of head pain in patients with migraine, but it has been un- 5-HT1 receptor subtypes provided evidence for substan- clear whether neurogenic inflammation occurs during an tial populations of 5-HT1B receptors on vascular endo- acute migraine attack. Studies in animals demonstrate in- thelium and human meningeal blood vessels.6 The mes- creased endothelial permeability and leakage of albumin senger RNA for the 5-HT1B receptor is abundantly into the dura and the retina after high-intensity electrical expressed on neuronal tissues and vascular smooth muscle stimulation of the trigeminal ganglion, but no increased cells, and evidence suggests that this receptor mediates 13 endothelial permeability or protein extravasation has been contraction of vascular smooth muscle. Both the 5-HT1B documented in human retinal or choroidal vessels dur- and 5-HT1D receptors have been localized in human tri- ing migraine attacks or the headache-free interval in mi- geminal ganglia and trigeminal nerves, but only 5-HT1D graineurs.7 These findings suggest that other fundamen- receptors have been detected in trigeminal nerves pro- tal processes, probably in the central nervous system, are jecting peripherally to the dural vasculature and cen- 6,13 key to the pathophysiology of a migraine attack. trally to the brainstem trigeminal nuclei. The 5-HT1D The autonomic nervous system may contribute to receptors are thus localized peripherally to inhibit acti- the pathophysiology of migraine. Hyperfunctioning of vated trigeminal nerves and prevent vasoactive neuro- both the sympathetic and parasympathetic nervous sys- peptide release, and centrally to interrupt pain signal trans- tems has been suspected in patients with migraine, based mission from the blood vessels to sensory neurons located on vasomotor reactions to temperature changes, cardio- in the brainstem.6 vascular responses, and other investigations. The nor- Local application of 5-HT1B/1D receptor agonists in- mal responses of cranial arteries during increased sym- hibits firing activity by second-order trigeminal neu- pathetic activity cast doubt on a major role of sympathetic rons, and this activity is shared by ergonovine, a non- 14 dysfunction in the pathophysiology of migraine, but mild specific 5-HT1 receptor agonist. These observations parasympathetic hypofunction with denervation hyper- support the presence of inhibitory receptors
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