Peripheral sensitization in migraine - Role for P2X purinergic receptors in the dura-vascular sensory pathway

Drug Development Research

Volumn 68, Issue 6, 2007, Pages 321-328

  Jennings, Ernest A ^a   Cho, Hyun Jung ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

ATP; Migraine; P2X; Pain; Trigeminal

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PURINERGIC P2X RECEPTOR; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y RECEPTOR;

DURA MATER; HUMAN; MAST CELL; MIGRAINE; MUSCLE SPINDLE AFFERENT NERVE; NERVE CELL EXCITABILITY; NEUROTRANSMITTER RELEASE; NOCICEPTION; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; SENSITIZATION; TRIGEMINAL NERVE;

EID: 38149029131     PISSN: 02724391     EISSN: 10982299     Source Type: Journal    
DOI: 10.1002/ddr.20195     Document Type: Review

References (81)

1. Ahn AH, Basbaum AI. 2005. Where do triptans act in the treatment of migraine? Pain 115:1-4.
2. Ali H, Leung KB, Pearce FL, Hayes NA, Foreman JC. 1986. Comparison of the histamine-releasing action of substance P on mast cells and basophils from different species and tissues. Int Arch Allergy Appl Immunol 79:413-418.
3. 3 receptor expression differs from dorsal root ganglion and is modulated by deep tissue inflammation. Pain 117:280-291.
4. Amir R, Devor M. 2000. Functional cross-excitation between afferent A- and C-neurons in dorsal root ganglia. Neuroscience 95:189-195.
5. Bereiter DA, Hirata H, Hu JW. 2000. Trigeminal subnucleus caudalis: beyond homologies with the spinal dorsal horn. Pain 88:221-224.
6. Blandini F, Rinaldi L, Tassorelli C, Sances G, Motta M, Samuele A, Fancellu R, Nappi G, Leon A. 2006. Peripheral levels of BDNF and NGF in primary headaches. Cephalalgia 26:136-142.
7. Bleehen T. 1978. The effects of adenine nucleotides on cutaneous afferent nerve activity. Br J Pharmacol 62:573-577.
8. Bleehen T, Keele CA. 1977. Observations on the algogenic actions of adenosine compounds on the human blister base preparation. Pain 3:367-377.
9. Bo X, Karoon P, Nori SL, Bardini M, Burnstock G. 1998. P2X purinoceptors in postmortem human cerebral arteries. J Cardiovase Pharmacol 31:794-799.
10. 3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 12:256-268.
11. Bulanova E, Budagian V, Orinska Z, Hein M, Petersen F, Thon L, Adam D, Bulfone-Paus S. 2005. Extracellular ATP induces cytokine expression and apoptosis through P2X7 receptor in murine mast cells. J Immunol 174:3880-3890.
12. Burnstock G. 1981. Pathophysiology of migraine: a new hypothesis. Lancet 1:1397-1399.
13. Burnstock G. 1996. A unifying purinergic hypothesis for the initiation of pain. Lancet 347:1604-1605.
14. Burnstock G. 2000. P2X receptors in sensory neurones. Br J Anaesth 84:476-488.
15. Burnstock G. 2006. Purinergic P2 receptors as targets for novel analgesics. Pharmacol Ther 110:433-454.
16. Burstein R, Yamamura H, Malick A, Strassman AM. 1998. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J Neurophysiol 79:964-982.
17. Burstein R, Cutrer MF, Yarnitsky D. 2000. The development of cutaneous allodynia during a migraine attack clinical evidence for the sequential recruitment of spinal and supraspinal nociceptive neurons in migraine. Brain 123(Pt 8):1703-1709.
18. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN. 1995. A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377:428-431.
19. Chiang CY, Park SJ, Kwan CL, Hu JW, Sessle BJ. 1998. NMDA receptor mechanisms contribute to neuroplasticity induced in caudalis nociceptive neurons by tooth pulp stimulation. J Neurophysiol 80:2621-2631.
20. Chiang CY, Zhang S, Xie YF, Hu JW, Dostrovsky JO, Salter MW, Sessle BJ. 2005. Endogenous ATP involvement in mustard-oil-induced central sensitization in trigeminal subnucleus caudalis (medullary dorsal horn). J Neurophysiol 94:1751-1760.
21. 2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol 567(Pt 2):621-639.
22. 3 receptors of nociceptive trigeminal ganglion neurons. J Neurosci 27:8190-8201.
23. Dodick D, Silberstein S. 2006. Central sensitization theory of migraine: clinical implications. Headache 46(Suppl 4):S182-S191.
24. Egan TM, Khakh BS. 2004. Contribution of calcium ions to P2X channel responses. J Neurosci 24:3413-3420.
25. 3 receptors of trigeminal sensory neurons by calcitonin gene-related peptide. J Neurosci 26:6163-6171.
26. Ferrari MD, Goadsby PJ, Roon KI, Lipton RB. 2002. Triptans (serotonin, 5-HT1B/1D agonists) in migraine: detailed results and methods of a meta-analysis of 53 trials. Cephalalgia 22:633-658.
27. Gallai V, Sarchielli P, Floridi A, Franceschini M, Codini M, Glioti G, Trequattrini A, Palumbo R. 1995, Vasoactive peptide levels in the plasma of young migraine patients with and without aura assessed both interictally and ictally. Cephalalgia 15:384-390.
28. Goadsby PJ, Edvinsson L, Ekman R. 1988. Release of vasoactive peptides in the extracerebral circulation of humans and the cat during activation of the trigeminovascular system. Ann Neurol 23:193-196.
29. Goadsby PJ, Edvinsson L, Ekman R. 1990. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann Neurol 28:183-817.
30. Goldstein DJ, Wang O, Saper JR, Stoltz R, Silberstein SD, Mathew NT. 1997. Ineffectiveness of neurokinin-1 antagonist in acute migraine: a crossover study. Cephalalgia 17:785-790.
31. Goldstein DJ, Roon KI, Offen WW, Ramadan NM, Phebus LA, Johnson KW, Schaus JM, Ferrari MD. 2001. Selective serotonin 1F (5-HT1F) receptor agonist LY334370 for acute migraine: a randomised controlled trial. Lancet 358:1230-1234.
32. Hansson E. 2006. Could chronic pain and spread of pain sensation be induced and maintained by glial activation? Acta Physiol (OxF) 187:321-327.
33. Headache Classification Committee of the International Headache Society. 1988. Classification and diagnostic criteria for headache disorders, cranial neuralgias and facial pain. Cephalalgia 8(Suppl 7):1-96.
34. Heatley RV, Denburg JA, Bayer N, Bienenstock J. 1982. Increased plasma histamine levels in migraine patients. Clin Allergy 12:145-149.
35. Henry P, Michel P, Brochet B, Dartigues JF, Tison S, Salamon R. 1992. A nationwide survey of migraine in France: prevalence and clinical features in adults. GRIM. Cephalalgia 12:229-237.
36. Humphrey PP, Goadsby PJ. 1994. The mode of action of sumatriptan is vascular? A debate. Cephalalgia 14:401-410.
37. Humphrey PP, Feniuk W, Perren MJ, Beresford IJ, Skingle M, Whalley ET. 1990. Serotonin and migraine. Ann NY Acad Sci 600:587-598.
38. Ikeda H, Tsuda M, Inoue K, Murase K. 2007. Long-term potentiation of neuronal excitation by neuron-glia interactions in the rat spinal dorsal horn. Eur J Neurosci 25:1297-1306.
39. Jennings EA, Christie MJ, Sessle BJ. 2006. ATP potentiates neurotransmission in the rat trigeminal subnucleus caudalis. NeuroReport 17:1507-1510.
40. Jennings EA, Ryan RM, Christie MJ. 2004. Effects of sumatriptan on rat medullary dorsal horn neurons. Pain 111:30-37.
41. Jennings EA, Sessle BJ. 2007. The adenosine tri-phosphate (ATP)-induced increase in neurotransmission is N-methyl-D-aspartate (NMDA) receptor-dependent. Soc Neurosci Abs 37:721.13.
42. Khakh BS. 2001. Molecular physiology of P2X receptors and ATP signalling at synapses. Nat Rev Neurosci 2:1651-1674.
43. Kruuse C, Thomsen LL, Birk S, Olesen J. 2003. Migraine can be induced by sildenafil without changes in middle cerebral artery diameter. Brain 126(Pt 1):241-247.
44. Lassen LH, Haderslev PA, Jacobsen VB, Iversen HK, Sperling B, Olesen J. 2002. CGRP may play a causative role in migraine. Cephalalgia 22:54-61.
45. Lazarov NE. 2002. Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus. Prog Neurobiol 66:19-59.
46. Levy D, Burstein R, Kainz V, Jakubowski M, Strassman AM. 2007. Mast cell degranulation activates a pain pathway underlying migraine headache. Pain 130:166-176.
47. Levy D, Burstein R, Strassman AM. 2006. Mast cell involvement in the pathophysiology of migraine headache: a hypothesis. Headache 46(Suppl 1):S13-S18.
48. Lewis CJ, Ennion SJ, Evans RJ. 2000. P2 purinoceptor-mediated control of rat cerebral (pial) microvasculature; contribution of P2X and P2Y receptors. J Physiol 527(Pt 2):315-324.
49. Limmroth V, May A, Auerbach P, Wosnitza G, Eppe T, Diener HC. 1996. Changes in cerebral blood flow velocity after treatment with sumatriptan or placebo and implications for the pathophysiology of migraine. J Neurol Sci 138:60-65.
50. Lipton RB, Scher AI, Kolodner K, Liberman J, Steiner TJ, Stewart WF. 2002. Migraine in the United States: epidemiology and patterns of health care use. Neurology 58:885-894.
51. Liu XJ, Salter MW. 2005. Purines and pain mechanisms: recent developments. Curr Opin Invest Drugs 6:65-75.
52. Mayberg M, Langer RS, Zervas NT, Moskowitz MA. 1981. Perivascular meningeal projections from cat trigeminal ganglia: possible pathway for vascular headaches in man. Science 213:228-230.
53. McGaraughty S, Chu KL, Namovic MT, Donnelly-Roberts DL, Harris RR, Zhang XF, Shieh CC, Wismer CT, Zhu CZ, Gauvin DM, Fabiyi AC, Honore P, Gregg RJ, Kort ME, Nelson DW, Carroll WA, Marsh K, Faltyner CR, Jarvis MF. 2007. P2X7-related modulation of pathological nociception in rats. Neuroscience 146:1817-1828.
54. Moskowitz MA. 1992. Neurogenic versus vascular mechanisms of sumatriptan and ergot alkaloids in migraine. Trends Pharmacol Sci 13:307-311.
55. Nakagawa T, Wakamatsu K, Zhang N, Maeda S, Minami M, Satoh M, Kaneko S. 2007. Intrathecal administration of ATP produces long-lasting allodynia in rats: differential mechanisms in the phase of the induction and maintenance. Neuroscience 147:445-455.
56. Nicol GD, Vasko MR. 2007. Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks? Mol Interv 7:26-41.
57. North RA. 2002. Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067.
58. 3 receptors and peripheral pain mechanisms. J Physiol 554:301-308.
59. Olesen J, Diener HC, Husstedt IW, Goadsby PJ, Hall D, Meier U, Pollentier S, Lesko LM. 2004. Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N Engl J Med 350:1104-1110.
60. Peroutka SJ. 2005. Neurogenic inflammation and migraine: implications for the therapeutics. Mol Interv 5:304-311.
61. Piotrowski W, Foreman JC. 1986. Some effects of calcitonin gene-related peptide in human skin and on histamine release. Br J Dermatol 114:37-46.
62. Qu Y, Franchi L, Nunez G, Dubyak GR. 2007. Nonclassical IL-1beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J Immunol 179:1913-1925.
63. Roon KI, Olesen J, Diener HC, Ellis P, Hettiarachchi J, Poole PH, Christianssen I, Kleinermans D, Kok JG, Ferrari MD. 2000. No acute antimigraine efficacy of CP-122,288, a highly potent inhibitor of neurogenic inflammation: results of two randomized, double-blind, placebo-controlled clinical trials. Ann Neurol 47: 238-241.
64. 3 purinoceptors in sensory ganglia of the mouse during embryonic and postnatal development. Histochem Cell Biol 122:539-551.
65. Russell MB, Rasmussen BK, Thorvaldsen P, Olesen J. 1995. Prevalence and sex-ratio of the subtypes of migraine. Int J Epidemiol 24:612-618.
66. Sarchielli P, Alberti A, Codini M, Floridi A, Gallai V. 2000. Nitric oxide metabolites, prostaglandins and trigeminal vasoactive peptides in internal jugular vein blood during spontaneous migraine attacks. Cephalalgia 20:907-918.
67. Sarchielli P, Gallai V. 2004. Nerve growth factor and chronic daily headache: a potential implication for therapy. Expert Rev Neurother 4:115-127.
68. Sessle BJ. 2000. Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 11:57-91.
69. Sessle BJ. 2005. Orofacial Pain. In: Merskey H, Loeser JD, Dubner R, editors. The paths of pain: 1975-2005, Seattle, WA: IASP Press. p 131-150.
70. 3 receptors in rat trigeminal ganglion neurons. Neuroscience 144:208-216.
71. Stewart WF, Lipton RB, Celentano DD, Reed ML. 1992. Prevalence of migraine headache in the United States. Relation to age, income, race, and other sociodemographic factors. JAMA 267:64-69.
72. Storer RJ, Akerman S, Goadsby PJ. 2004. Calcitonin gene-related peptide (CGRP) modulates nociceptive trigeminovascular transmission in the cat. Br J Pharmacol 142:1171-1181.
73. Strassman AM, Raymond SA, Burstein R. 1996. Sensitization of meningeal sensory neurons and the origin of headaches. Nature 384:560-564.
74. Thalakoti S, Patil VV, Damodaram S, Vause CV, Langford LE, Freeman SE, Durham PL. 2007. Neuron-glia signaling in trigeminal ganglion: implications for migraine pathology. Headache 47:1008-1023.
75. Theoharides TC, Donelan J, Kandere-Grzybowska K, Konstantinidou A. 2005. The role of mast cells in migraine pathophysiology. Brain Res Brain Res Rev 49:65-76.
76. Tvedskov JF, Lipka K, Ashina M, Iversen HK, Schifter S, Olesen J. 2005. No increase of calcitonin gene-related peptide in jugular blood during migraine. Ann Neurol 58:561-568.
77. Woolf CJ, Salter MW. 2000. Neuronal plasticity: increasing the gain in pain. Science 288:1765-1769.
78. Xie YF, Zhang S, Chiang CY, Hu JW, Dostrovsky JO, Sessle BJ. 2007. Involvement of glia in central sensitization in trigeminal subnucleus caudalis (medullary dorsal horn). Brain Behav Immun 21:634-641.
79. Zagami AS, Goadsby PJ, Edvinsson L. 1990. Stimulation of the superior sagittal sinus in the cat causes release of vasoactive peptides. Neuropeptides 16:69-75.
80. Zhang XC, Strassman AM, Burstein R, Levy D. 2007. Sensitization and activation of intracranial meningeal nociceptors by mast cell mediators. J Pharmacol Exp Ther 322:806-812.
81. 2 release in isolated rat dura mater. Pain 97: 259-265.