A hyperexcitability phenotype in mouse trigeminal sensory neurons expressing the R192Q Cacna1a missense mutation of familial hemiplegic migraine type-1

Neuroscience

Volumn 266, Issue , 2014, Pages 244-254

  Hullugundi, S K ^a,c   Ansuini, A ^a   Ferrari, M D ^b   van den Maagdenberg, A M J M ^b   Nistri, A ^a  

^a SISSA   (Italy)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Bldg 142   (United States)

Author keywords

ATP; Capsaicin; P2X3 receptors; Purinergic; TRPV1 receptors

Indexed keywords

5 [[(3 PHENOXYBENZYL)(1,2,3,4 TETRAHYDRO 1 NAPHTHYL)AMINO]CARBONYL]TRIMELLITIC ACID; ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; CAPSAICIN; PURINERGIC P2X3 RECEPTOR; CALCIUM CHANNEL N TYPE; VOLTAGE-DEPENDENT CALCIUM CHANNEL (P-Q TYPE);

ACTION POTENTIAL; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CACNA1A GENE; CONTROLLED STUDY; EVOKED BRAIN STEM RESPONSE; FAMILIAL HEMIPLEGIC MIGRAINE; FAMILIAL HEMIPLEGIC MIGRAINE TYPE 1; GENE; GENE EXPRESSION REGULATION; LATENT PERIOD; MISSENSE MUTATION; MOLECULAR INTERACTION; MOUSE; MUTATIONAL ANALYSIS; NEUROPATHOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPIC VARIATION; PRIORITY JOURNAL; SATELLITE CELL; SENSORY NERVE CELL; TRIGEMINUS GANGLION; UPREGULATION; WHOLE CELL PATCH CLAMP; ANIMAL; CELL CULTURE; CEREBELLAR ATAXIA; DISEASE MODEL; GENE TARGETING; GENETICS; MIGRAINE; PATCH CLAMP TECHNIQUE; PHENOTYPE; PHYSIOLOGY;

ANIMALS; CALCIUM CHANNELS, N-TYPE; CELLS, CULTURED; CEREBELLAR ATAXIA; DISEASE MODELS, ANIMAL; GENE KNOCK-IN TECHNIQUES; MICE; MIGRAINE DISORDERS; MUTATION, MISSENSE; PATCH-CLAMP TECHNIQUES; PHENOTYPE; SENSORY RECEPTOR CELLS; TRIGEMINAL GANGLION;

EID: 84896278507     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.02.020     Document Type: Article

References (48)

1. Andres-Enguix I., Shang L., Stansfeld P.J., Morahan J.M., Sansom M.S., Lafrenière R.G., Roy B., Griffiths L.R., Rouleau G.A., Ebers G.C., Cader Z.M., Tucker S.J. Functional analysis of missense variants in the TRESK (KCNK18) K channel. Sci Rep 2012, 2:237.
2. Barclay J., Patel S., Dorn G., Wotherspoon G., Moffatt S., Eunson L., Abdel'al S., Natt F., Hall J., Winter J., Bevan S., Wishart W., Fox A., Ganju P. Functional downregulation of P2X3 receptor subunit in rat sensory neurons reveals a significant role in chronic neuropathic and inflammatory pain. J Neurosci 2002, 22:8139-8147.
3. 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.
4. Bradbury E.J., Burnstock G., McMahon S.B. The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 1998, 12:256-268.
5. + currents generates distinct firing patterns in different subtypes of adult mouse trigeminal ganglion neurons. J Physiol 2008, 586:5101-5118.
6. v2.1 knock-in mice: implications for basic mechanisms of migraine pain. J Neurosci 2011, 31:3638-3649.
7. Chanda M.L., Tuttle A.H., Baran I., Atlin C., Guindi D., Hathaway G., Israelian N., Levenstadt J., Low D., Macrae L., O'Shea L., Silver A., Zendegui E., Mariette Lenselink A., Spijker S., Ferrari M.D., van den Maagdenberg A.M., Mogil J.S. Behavioral evidence for photophobia and stress-related ipsilateral head pain in transgenic Cacna1a mutant mice. Pain 2013, 154:1254-1262.
8. V2.1 into lipid rafts in cerebellum: implications for localization and function. J Neurosci 2006, 26:8748-8757.
9. Docherty R.J., Yeats J.C., Piper A.S. Capsazepine block of voltage-activated calcium channels in adult rat dorsal root ganglion neurones in culture. Br J Pharmacol 1997, 12:1461-1467.
10. Eikermann-Haerter K., Dileköz E., Kudo C., Savitz S.I., Waeber C., Baum M.J., Ferrari M.D., van den Maagdenberg A.M., Moskowitz M.A., Ayata C. Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J Clin Invest 2009, 119:99-109.
11. Fabbretti E., Nistri A. Regulation of P2X3 receptor structure and function. CNS Neurol Disord Drug Targets 2012, 11:687-698.
12. V2.1 calcium current and excitability in a Cacna1a mouse model of migraine. J Physiol 2011, 589:5879-5895.
13. Franceschini A., Nair A., Bele T., van den Maagdenberg A.M., 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.
14. +-channel activators in Cacna1a(S218L) mutant mice. J Neurosci 2012, 32:15533-15546.
15. 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, 37:83-90.
16. Gnanasekaran A., Sundukova M., van den Maagdenberg A.M., Fabbretti E., Nistri A. Lipid rafts control P2X3 receptor distribution and function in trigeminal sensory neurons of a transgenic migraine mouse model. Mol Pain 2011, 7:77.
17. Goadsby P.J., Lipton R.B., Ferrari M.D. Migraine-current understanding and treatment. N Engl J Med 2002, 24(346):257-270.
18. Goldstein S.A., Bayliss D.A., Kim D., Lesage F., Plant L.D., Rajan S. International Union of Pharmacology. LV. Nomenclature and molecular relationships of two-P potassium channels. Pharmacol Rev 2005, 57:527-540.
19. Head B.P., Patel H.H., Insel P.A. Interaction of membrane/lipid rafts with the cytoskeleton: Impact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling. Biochim Biophys Acta 2014, 1838:532-545.
20. Ho T.W., Edvinsson L., Goadsby P.J. CGRP and its receptors provide new insights into migraine pathophysiology. Nat Rev Neurol 2010, 6:573-582.
21. Hullugundi S.K., Ferrari M.D., van den Maagdenberg A.M., Nistri A. The mechanism of functional up-regulation of P2X3 receptors of trigeminal sensory neurons in a genetic mouse model of familial hemiplegic migraine type 1 (FHM-1). PLoS One 2013, 8:e60677.
22. International Headache Society The International Classification of Headache Disorders: 2nd edition. Cephalalgia 2004, 24(Suppl. 1):9-160.
23. Iwashita T., Shimizu T., Shibata M., Toriumi H., Ebine T., Funakubo M., Suzuki N. Activation of extracellular signal-regulated kinase in the trigeminal ganglion following both treatment of the dura mater with capsaicin and cortical spreading depression. Neurosci Res 2013, 77:110-119.
24. Jarvis M.F., Khakh B.S. ATP-gated P2X cation-channels. Neuropharmacology 2009, 56:208-215.
25. Jarvis M.F., Burgard E.C., McGaraughty S., Honore P., Lynch K., Brennan T.J., Subieta A., Van Biesen T., Cartmell J., Bianchi B., Niforatos W., Kage K., Yu H., Mikusa J., Wismer C.T., Zhu C.Z., Chu K., Lee C.H., Stewart A.O., Polakowski J., Cox B.F., Kowaluk E., Williams M., Sullivan J., Faltynek C. A-317491, a novel potent and selective non-nucleotide antagonist of P2X3 and P2X2/3 receptors, reduces chronic inflammatory and neuropathic pain in the rat. Proc Natl Acad Sci U S A 2002, 99:17179-17184.
26. Kaja S., van de Ven R.C., Broos L.A., Veldman H., van Dijk J.G., Verschuuren J.J., Frants R.R., Ferrari M.D., van den Maagdenberg A.M., Plomp J.J. Gene dosage-dependent transmitter release changes at neuromuscular synapses of CACNA1A R192Q knockin mice are non-progressive and do not lead to morphological changes or muscle weakness. Neuroscience 2005, 135:81-95.
27. Kuenzi F.M., Dale N. Effect of capsaicin and analogues on potassium and calcium currents and vanilloid receptors in Xenopus embryo spinal neurones. Br J Pharmacol 1996, 119:81-90.
28. Lafrenière R.G., Cader M.Z., Poulin J.F., Andres-Enguix I., Simoneau M., Gupta N., Boisvert K., Lafrenière F., McLaughlan S., Dubé M.P., Marcinkiewicz M.M., Ramagopalan S., Ansorge O., Brais B., Sequeiros J., Pereira-Monteiro J.M., Griffiths L.R., Tucker S.J., Ebers G., Rouleau G.A. A dominant-negative mutation in the TRESK potassium channel is linked to familial migraine with aura. Nat Med 2010, 16:1157-1160.
29. Lambert G.A., Davis J.B., Appleby J.M., Chizh B.A., Hoskin K.L., Zagami A.S. The effects of the TRPV1 receptor antagonist SB-705498 on trigeminovascular sensitisation and neurotransmission. Naunyn Schmiedebergs Arch Pharmacol 2009, 380:311-325.
30. Lauritzen M. Pathophysiology of the migraine aura; the spreading depression theory. Brain 1994, 117:199-210.
31. + channel mutation. J Neurosci 2013, 33:12810-12824.
32. Meents J.E., Neeb L., Reuter U. TRPV1 in migraine pathophysiology. Trends Mol Med 2010, 16:153-159.
33. V2.1 channel mutation R192Q enhances ATP-gated P2X3 receptor activity of mouse sensory ganglion neurons mediating trigeminal pain. Mol Pain 2010, 6:48.
34. O'Neill J., Brock C., Olesen A.E., Andresen T., Nilsson M., Dickenson A.H. Unravelling the mystery of capsaicin: a tool to understand and treat pain. Pharmacol Rev 2012, 64:939-971.
35. 2+ channel gene CACNL1A4. Cell 1996, 87:543-552.
36. Orio P., Madrid R., de la Peña E., Parra A., Meseguer V., Bayliss D.A., Belmonte C., Viana F. Characteristics and physiological role of hyperpolarization activated currents in mouse cold thermoreceptors. J Physiol 2009, 587:1961-1976.
37. Platkiewicz J., Brette R. A threshold equation for action potential initiation. PLoS Comput Biol 2010, 6:e1000850.
38. Pristerà A., Baker M.D., Okuse K. Association between tetrodotoxin resistant channels and lipid rafts regulates sensory neuron excitability. PLoS One 2012, 7(8):e40079. [Erratum in: PLoS One 8(5)].
39. v2.2) voltage-gated calcium channel membrane microdomains: lipid raft association and clustering. Cell Calcium 2010, 48:183-194.
40. Sekerli M., Negro C.D., Lee R., Butera R.J. Estimating action potential thresholds from neuronal time-series: new metrics and evaluation of methodologies. IEEE Trans Biomed Eng 2004, 51:1665-1672.
41. Sessle B.J. Neural mechanisms and pathways in craniofacial pain. Can J Neurol Sci 1999, 26(Suppl. 3):S7-S11.
42. Simonetti M., Fabbro A., D'Arco M., Zweyer M., Nistri A., Giniatullin R., Fabbretti E. 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.
43. Sokolova E., Skorinkin A., Moiseev I., Agrachev A., Nistri A., Giniatullin R. Experimental and modeling studies of desensitization of P2X3 receptors. Mol Pharmacol 2006, 70:373-382.
44. 3 receptors. Pain 2009, 143:26-36.
45. Szoke E., Börzsei R., Tóth D.M., Lengl O., Helyes Z., Sándor Z., Szolcsányi J. Effect of lipid raft disruption on TRPV1 receptor activation of trigeminal sensory neurons and transfected cell line. Eur J Pharmacol 2010, 628:67-74.
46. v2.1 knockin migraine mice. Neuron 2009, 61:762-773.
47. V2.1 voltage activated calcium channels and synaptic transmission in familial hemiplegic migraine pathogenesis. J Physiol 2012, 106:12-22.
48. van den Maagdenberg A.M., Pietrobon D., Pizzorusso T., Kaja S., Broos L.A., Cesetti T., van de Ven R.C., Tottene A., van der Kaa J., Plomp J.J., Frants R.R., Ferrari M.D. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41:701-710.