Differential trigeminovascular nociceptive responses in the thalamus in the familial hemiplegic migraine 1 knock-in mouse: A Fos protein study

Neurobiology of Disease

Volumn 64, Issue , 2014, Pages 1-7

  Park, JungWook ^a   Moon, HeuiSoo ^a   Akerman, Simon ^a   Holland, Philip R ^a   Lasalandra, Michele P ^a   Andreou, Anna P ^a   Ferrari, Michel D ^c   van den Maagdenberg, Arn M J M ^c   Goadsby, Peter J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Aura; CACNA1A; Familial hemiplegic migraine; Migraine; Trigeminovascular

Indexed keywords

NARATRIPTAN; PROTEIN FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED RESPONSE; FAMILIAL HEMIPLEGIC MIGRAINE; MOUSE; NERVE STIMULATION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPERIOR SAGITTAL SINUS; THALAMUS NUCLEUS; TRIGEMINAL NERVE; WILD TYPE;

AURA; CACNA1A; FAMILIAL HEMIPLEGIC MIGRAINE; MIGRAINE; TRIGEMINOVASCULAR;

ANIMALS; CALCIUM CHANNELS; CEREBELLAR ATAXIA; ELECTRIC STIMULATION; GENE KNOCK-IN TECHNIQUES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIGRAINE DISORDERS; MUTATION, MISSENSE; NEURAL PATHWAYS; NEURONS; NOCICEPTION; PIPERIDINES; PROTO-ONCOGENE PROTEINS C-FOS; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SUPERIOR SAGITTAL SINUS; THALAMIC NUCLEI; TRIGEMINAL CAUDAL NUCLEUS; TRIGEMINAL NUCLEI; TRYPTAMINES;

EID: 84891781328     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.12.004     Document Type: Article

References (71)

1. Akerman S., et al. Voltage-dependent calcium channels are involved in neurogenic dural vasodilation via a pre-synaptic transmitter release mechanism. Br. J. Pharmacol. 2003, 140:558-566.
2. Andersen E., Dafny N. An ascending serornergic pain modulation pathway from the dorsal raphe nucleus to the parafascicularis nucleus of the thalamus. Brain Res. 1983, 269:13-25.
3. Andreou A.P., et al. GABA and valproate modulate trigeminovascular nociceptive transmission in the thalamus. Neurobiol. Dis. 2010, 37:314-323.
4. Andreou A.P., et al. Animal models of headache- from bedside to bench and back to beside. Expert Rev. Neurother. 2010, 10:389-411.
5. Angus-Leppan H., et al. Convergence of afferents from superior sagittal sinus and tooth pulp on cells in the thalamus of the cat. Cephalalgia 1995, 15:191-199.
6. Apkarian A.V., Shi T. Squirrel monkey lateral thalamus. I. Somatic nociresponsive neurons and their relation to spinothalamic terminals. J. Neurosci. 1994, 14:6779-6795.
7. Barnes N.M., Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999, 38:1083-1152.
8. Benjamin L., et al. Hypothalamic activation after stimulation of the superior sagittal sinus in the cat: a Fos study. Neurobiol. Dis. 2004, 16:500-505.
9. Bergerot A., et al. Animal models of migraine. Looking at the component parts of a complex disorder. Eur. J. Neurosci. 2006, 24:1517-1534.
10. Bullitt E. Expression of c-fos-like protein as a marker for neuronal-activity following noxious-stimulation in the rat. J. Comp. Neurol. 1990, 296:517-530.
11. 2+ channel activity and inhibitory synaptic transmission. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:2590-2595.
12. 2+ channelopathy. Neuron 2004, 43:387-400.
13. Craig A.D. Pain mechanisms: labeled lines versus convergence in central processing. Annu. Rev. Neurosci. 2003, 26:1-30.
14. Craig A.D., Zhang E.T. Retrograde analyses of spinothalamic projections in the macaque monkey: input to posterolateral thalamus. J. Comp. Neurol. 2006, 499:953-964.
15. Craig A.D., et al. A thalamic nucleus specific for pain and temperature sensation. Nature 1994, 372:770-773.
16. DaSilva A.F., et al. Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine. Neuroreport 2007, 18:301-305.
17. Davidson S., et al. Termination zones of functionally characterized spinothalamic tract neurons within the primate posterior thalamus. J. Neurophysiol. 2008, 100:2026-2037.
18. Davis K.D., Dostrovsky J.O. Properties of feline thalamic neurons activated by stimulation of the middle meningeal artery and sagittal sinus. Brain Res. 1988, 454:89-100.
19. Eikermann-Haerter K., et al. Enhanced subcortical spreading depression in familial hemiplegic migraine type 1 mutant mice. J. Neurosci. 2011, 31:5755-5763.
20. Goadsby P.J. Calcitonin gene-related peptide antagonists as treatments of migraine and other primary headaches. Drugs 2005, 65:2557-2567.
21. Goadsby P.J., et al. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann. Neurol. 1990, 28:183-187.
22. Goadsby P.J., et al. Migraine- current understanding and treatment. N. Engl. J. Med. 2002, 346:257-270.
23. Goadsby P.J., et al. Neurobiology of migraine. Neuroscience 2009, 161:327-341.
24. Hadjikhani N., et al. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4687-4692.
25. Hammond D.L., et al. Morphine suppresses Fos protein-like immunoreactivity in the spinal cord and nucleus tractus solitarii evoked by a noxious visceral stimulus in the rat. J. Comp. Neurol. 1992, 315:244-253.
26. Hansen J.M., et al. Familial hemiplegic migraine type 2 does not share hypersensitivity to nitric oxide with common types of migraine. Cephalalgia 2008, 28:367-375.
27. Hansen J.M., et al. Calcitonin gene-related peptide does not cause the familial hemiplegic migraine phenotype. Neurology 2008, 71:841-847.
28. Hansen J.M., et al. Familial hemiplegic migraine type 1 shows no hypersensitivity to nitric oxide. Cephalalgia 2008, 28:496-505.
29. Headache Classification Committee of the International Headache Society The international classification of headache disorders (second edition). Cephalalgia 2004, 24:1-160.
30. Hoskin K.L., Goadsby P.J. Exposure and isolation of the superior sagittal sinus elicits Fos in the trigeminal nucleus caudalis and dorsal horn of the cervical spinal cord: how long should you wait?. Brain Res. 1999, 824:133-135.
31. Hoskin K.L., et al. Stimulation of the middle meningeal artery leads to Fos expression in the trigeminocervical nucleus: a comparative study of monkey and cat. J. Anat. 1999, 194:579-588.
32. Hoskin K.L., et al. Fos expression in the midbrain periaqueductal grey after trigeminovascular stimulation. J. Anat. 2001, 197:29-35.
33. Ishijima B., et al. Nociceptive neurons in the human thalamus. Confin. Neurol. 1975, 37:99-106.
34. Iversen H.K., Olesen J. Headache induced by a nitric oxide donor (nitroglycerin) responds to sumatriptan- a human model for development of migraine drugs. Cephalalgia 1996, 16:412-418.
35. Iversen H.K., et al. Intravenous nitroglycerin as an experimental headache model. Basic characteristics. Pain 1989, 38:17-24.
36. Jones B.E., Yang T.Z. The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J. Comp. Neurol. 1985, 242:56-92.
37. Kaube H., et al. Intravenous acetylsalicylic acid inhibits central trigeminal neurons in the dorsal horn of the upper cervical spinal cord in the cat. Headache 1993, 33:541-550.
38. Klapper J., et al. Triptans in the treatment of basilar migraine and migraine with prolonged aura. Headache 2001, 41:981-984.
39. Kline P. The Handbook of Physiological Testing 1999, Routledge, London.
40. Lassen L.H., et al. CGRP may play a causative role in migraine. Cephalalgia 2002, 22:54-61.
41. Lenz F.A., et al. Thermal and pain sensations evoked by microstimulation in the area of human ventrocaudal nucleus. J. Neurophysiol. 1993, 70:200-212.
42. Levy D., et al. Disruption of communication between peripheral and central trigeminovascular neurons mediates the antimigraine action of 5HT 1B/1D receptor agonists. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:4274-4279.
43. 1F receptor immunoreactivity (IR) in the rat trigeminocervical complex (TCC) new therapeutic possibilities for the triptans. Cephalalgia 2004, 24:148.
44. Mathew R., et al. Immunohistochemical characterization of calcitonin gene-related peptide in the trigeminal system of the familial hemiplegic migraine 1 knock-in mouse. Cephalalgia 2011, 31:1368-1380.
45. Mintz I.M., et al. Calcium control of transmitter release at a cerebellar synapse. Neuron 1995, 15:675-688.
46. Moon H.S., et al. Altered responses in the descending modulatory system of transgenic mice with a CACNA1A mutation. Headache 2010, 50:6-7.
47. Morgan J.I., Curran T. Stimulus-transcription coupling in neurons: role of cellular immediate-early genes. Trends Neurosci. 1989, 12:459-462.
48. Noseda R., et al. A neural mechanism for exacerbation of headache by light. Nat. Neurosci. 2010, 13:239-245.
49. Ohara S., Lenz F.A. Medial lateral extent of thermal and pain sensations evoked by microstimulation in somatic sensory nuclei of human thalamus. J. Neurophysiol. 2003, 90:2367-2377.
50. 2+ channel gene CACNL1A4. Cell 1996, 87:543-552.
51. Park J.W., et al. Blunted trigeminovascular nociceptive responses in mice with the CACNA1A mutation. Headache 2010, 50:61.
52. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2003, Academic Press, London.
53. Pearse D.D., et al. Jun, Fos and Krox in the thalamus after C-fiber stimulation: coincident-input-dependent expression, expression across somatotopic boundaries, and nucleolar translocation. Neuroscience 2001, 107:143-159.
54. Royce G.J., et al. Subcortical projections to the centromedian and parafascicular thalamic nuclei in the cat. J. Comp. Neurol. 1991, 306:129-155.
55. Shields K.G., Goadsby P.J. Serotonin receptors modulate trigeminovascular responses in ventroposteromedial nucleus of thalamus: a migraine target?. Neurobiol. Dis. 2006, 23:491-501.
56. Shields K.G., et al. Calcium channels modulate nociceptive transmission in the trigeminal nucleus of the cat. Neuroscience 2005, 135:203-212.
57. Siegel S. Non-Parametric Statistics for the Behavioural Sciences 1956, McGraw-Hill, Kogakusha, Tokyo.
58. Sprenger T., Goadsby P.J. What has functional neuroimaging done for primary headache. . .and for the clinical neurologist?. J. Clin. Neurosci. 2010, 17:547-553.
59. 1B/1D agonists inhibits trigeminal cell firing in the cat. Brain 1997, 120:2171-2177.
60. Summ O., et al. Modulation of nocioceptive transmission with calcitonin gene-related peptide receptor antagonists in the thalamus. Brain 2010, 133:2540-2548.
61. 2+ channels. J. Neurosci. 1999, 19:890-899.
62. Thomsen L.L., et al. A population-based study of familial hemiplegic migraine suggests revised diagnostic criteria. Brain 2002, 125:1379-1391.
63. V2.1 current density in neurons. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13284-13289.
64. Tottene 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, 61:762-773.
65. van den Maagdenberg A.M.J.M., et al. A Cacna1a knock-in migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41:701-710.
66. Vertes R.P., Martin G.F. Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. J. Comp. Neurol. 1988, 275:511-541.
67. Weigel R., Krauss J.K. Center median-parafascicular complex and pain control. Review from a neurosurgical perspective. Stereotact. Funct. Neurosurg. 2004, 82:115-126.
68. Weiss N., et al. The S218L familial hemiplegic migraine mutation promotes deinhibition of Ca(v)2.1 calcium channels during direct G-protein regulation. Pflugers Arch. 2008, 457:315-326.
69. Westenbroek R.E., et al. Immunochemical identification and subcellular distribution of the alpha(1a) subunits of brain calcium channels. J. Neurosci. 1995, 15:6403-6418.
70. Xiao Y., et al. Release of glutamate and CGRP from trigeminal ganglion neurons: role of calcium channels and 5-HT1 receptor signalling. Mol. Pain 2008, 4:12.
71. Zagami A.S., Lambert G.A. Stimulation of cranial vessels excites nociceptive neurones in several thalamic nuclei of the cat. Exp. Brain Res. 1990, 81:552-566.