The spinal inhibition of N-type voltage-gated calcium channels selectively prevents scratching behavior in mice

Neuroscience

Volumn 277, Issue , 2014, Pages 794-805

  Maciel, I S ^a   Azevedo, V M ^a   Pereira, T C ^a   Bogo, M R ^a   Souza, A H ^b   Gomez, M V ^b   Campos, M M ^a  

^a PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Mice; N type voltage gated calcium channels; PAR 2; Scratching behavior; Trypsin

Indexed keywords

CALCIUM CHANNEL N TYPE; OMEGA CONOTOXIN MVIIA; OMEGA CONOTOXIN MVIIC; PROTEIN C FOS; TRYPSIN; VOLTAGE GATED CALCIUM CHANNEL; ANTIPRURITIC AGENT; CALCIUM CHANNEL BLOCKING AGENT; PHALPHA1BETA TOXIN, PHONEUTRIA NIGRIVENTER; SPIDER VENOM; CHLOROQUINE; COMPOUND 48-80; NNC 55 0396; PHALPHA1BETA TOXIN; POLYPEPTIDE; SERYLLEUCYLISOLEUCYLGLYCLARGINYLLEUCINE AMIDE PEPTIDE; SNX 482; UNCLASSIFIED DRUG; VERAPAMIL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; MALE; MOLECULAR PATHOLOGY; MOUSE; NERVE CELL EXCITABILITY; NEUROPATHOLOGY; NEUROTRANSMITTER RELEASE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCRATCHING; SKIN PRURITUS; SPINAL CORD; ACUTE DISEASE; ANIMAL; CHRONIC DISEASE; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; PATHOPHYSIOLOGY; PRURITUS; SKIN; TIME; BEHAVIOR CHANGE; CONUS MAGUS; DISEASE CONTROL; DOWN REGULATION; DRUG EFFECT; DRUG SELECTIVITY; DRUG TREATMENT FAILURE; PHONEUTRIA NIGRIVENTER; SCREENING TEST; SKIN EDEMA; SNAIL;

ACUTE DISEASE; ANIMALS; ANTIPRURITICS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, N-TYPE; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MICE; PROTO-ONCOGENE PROTEINS C-FOS; PRURITUS; SKIN; SPIDER VENOMS; SPINAL CORD; TIME FACTORS; TRYPSIN;

EID: 84907033274     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.07.065     Document Type: Article

References (62)

1. Agostini R.M., do Nascimento Pinheiro A.C., Binda N.S., Romano Silva M.A., do Nascimento Cordeiro M., Richardson M., Sena Guimaraes A.L., Gomez M.V. Phoneutria spider toxins block ischemia-induced glutamate release and neuronal death of cell layers of the retina. Retina 2011, 31:1392-1399.
2. Akiyama T., Merrill A.W., Zanotto K., Carstens M.I., Carstens E. Scratching behavior and Fos expression in superficial dorsal horn elicited by protease-activated receptor agonists and other itch mediators in mice. J Pharmacol Exp Ther 2009, 329:945-951.
3. Akiyama T., Tominaga M., Davoodi A., Nagamine M., Blansit K., Horwitz A., Carstens M.I., Carstens E. Roles for substance P and gastrin-releasing peptide as neurotransmitters released by primary afferent pruriceptors. J Neurophysiol 2013, 109:742-748.
4. Akiyama T., Nagamine M., Carstens M.I., Carstens E. Behavioral model of itch, alloknesis, pain and allodynia in the lower hindlimb and correlative responses of lumbar dorsal horn neurons in the mouse. Neuroscience 2014, 266C:38-46.
5. Akiyama T., Tominaga M., Takamori K., Carstens M.I., Carstens E. Roles of glutamate, substance P, and gastrin-releasing peptide as spinal neurotransmitters of histaminergic and nonhistaminergic itch. Pain 2014, 155:80-92.
6. Bautista D.M., Wilson S.R., Hoon M.A. Why we scratch an itch: the molecules, cells and circuits of itch. Nat Neurosci 2014, 17:175-182.
7. Castro-Junior C.J., Milano J., Souza A.H., Silva J.F., Rigo F.K., Dalmolin G., Cordeiro M.N., Richardson M., Barros A.G., Gomez R.S., Silva M.A., Kushmerick C., Ferreira J., Gomez M.V. Phα1β toxin prevents capsaicin-induced nociceptive behavior and mechanical hypersensitivity without acting on TRPV1 channels. Neuropharmacology 2013, 71:237-246.
8. Cevikbas F., Steinhoff M., Ikoma A. Role of spinal neurotransmitter receptors in itch: new insights into therapies and drug development. CNS Neurosci Ther 2011, 17:742-749.
9. Chaplan S.R., Pogrel J.W., Yaksh T.L. Role of voltage-dependent calcium channel subtypes in experimental tactile allodynia. J Pharmacol Exp Ther 1994, 269:1117-1123.
10. 2+ channel-dependent activation of ERK in paraventricular thalamus modulates acid-induced chronic muscle pain. J Neurosci 2010, 30:10360-10368.
11. Costa R., Marotta D.M., Manjavachi M.N., Fernandes E.S., Lima-Garcia J.F., Paszcuk A.F., Quintao N.L., Juliano L., Brain S.D., Calixto J.B. Evidence for the role of neurogenic inflammation components in trypsin-elicited scratching behaviour in mice. Br J Pharmacol 2008, 154:1094-1103.
12. Costa R., Manjavachi M.N., Motta E.M., Marotta D.M., Juliano L., Torres H.A., Pesquero J.B., Calixto J.B. The role of kinin B1 and B2 receptors in the scratching behaviour induced by proteinase-activated receptor-2 agonists in mice. Br J Pharmacol 2010, 159:888-897.
13. Davidson S., Giesler G.J. The multiple pathways for itch and their interactions with pain. Trends Neurosci 2010, 33:550-558.
14. de Souza A.H., Lima M.C., Drewes C.C., da Silva J.F., Torres K.C., Pereira E.M., de Castro Junior C.J., Vieira L.B., Cordeiro M.N., Richardson M., Gomez R.S., Romano-Silva M.A., Ferreira J., Gomez M.V. Antiallodynic effect and side effects of Phalpha1beta, a neurotoxin from the spider Phoneutria nigriventer: comparison with omega-conotoxin MVIIA and morphine. Toxicon 2011, 58:626-633.
15. Dhand A., Aminoff M.J. The neurology of itch. Brain 2014, 137:313-322.
16. Feng Z.P., Hamid J., Doering C., Bosey G.M., Snutch T.P., Zamponi G.W. Residue Gly1326 of the N-type calcium channel alpha 1B subunit controls reversibility of omega-conotoxin GVIA and MVIIA block. J Biol Chem 2001, 276:15728-15735.
17. Frateschi S., Camerer E., Crisante G., Rieser S., Membrez M., Charles R.P., Beermann F., Stehle J.C., Breiden B., Sandhoff K., Rotman S., Haftek M., Wilson A., Ryser S., Steinhoff M., Coughlin S.R., Hummler E. PAR2 absence completely rescues inflammation and ichthyosis caused by altered CAP1/Prss8 expression in mouse skin. Nat Commun 2011, 2:161.
18. 2+]i in spinal cord synaptosomes. Cell Mol Neurobiol 2011, 31:277-283.
19. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985, 260:3440-3450.
20. Han N., Zu J.Y., Chai J. Spinal bombesin-recognized neurones mediate more nonhistaminergic than histaminergic sensation of itch in mice. Clin Exp Dermatol 2012, 37:290-295.
21. Ikoma A., Steinhoff M., Stander S., Yosipovitch G., Schmelz M. The neurobiology of itch. Nat Rev Neurosci 2006, 7:535-547.
22. Inagaki N., Igeta K., Kim J.F., Nagao M., Shiraishi N., Nakamura N., Nagai H. Involvement of unique mechanisms in the induction of scratching behavior in BALB/c mice by compound 48/80. Eur J Pharmacol 2002, 448:175-183.
23. Kini S.P., DeLong L.K., Veledar E., McKenzie-Brown A.M., Schaufele M., Chen S.C. The impact of pruritus on quality of life: the skin equivalent of pain. Arch Dermatol 2011, 147:1153-1156.
24. LaMotte R.H., Dong X., Ringkamp M. Sensory neurons and circuits mediating itch. Nat Rev Neurosci 2014, 15:19-31.
25. Liu T., Ji R.R. Oxidative stress induces itch via activation of transient receptor potential subtype ankyrin 1 in mice. Neurosci Bull 2012, 28:145-154.
26. Liu T., Ji R.R. New insights into the mechanisms of itch: are pain and itch controlled by distinct mechanisms?. Pflugers Arch 2013, 465:1671-1685.
27. Liu Q., Tang Z., Surdenikova L., Kim S., Patel K.N., Kim A., Ru F., Guan Y., Weng H.J., Geng Y., Undem B.J., Kollarik M., Chen Z.F., Anderson D.J., Dong X. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 2009, 139:1353-1365.
28. Liu X.Y., Liu Z.C., Sun Y.G., Ross M., Kim S., Tsai F.F., Li Q.F., Jeffry J., Kim J.Y., Loh H.H., Chen Z.F. Unidirectional cross-activation of GRPR by MOR1D uncouples itch and analgesia induced by opioids. Cell 2011, 147:447-458.
29. Martinez-Gomez J., Lopez-Garcia J.A. Simultaneous assessment of the effects of L-type current modulators on sensory and motor pathways of the mouse spinal cord in vitro. Neuropharmacology 2007, 53:464-471.
30. Matthews E.A., Bee L.A., Stephens G.J., Dickenson A.H. The Cav2.3 calcium channel antagonist SNX-482 reduces dorsal horn neuronal responses in a rat model of chronic neuropathic pain. Eur J Neurosci 2007, 25:3561-3569.
31. Miyamoto T., Nojima H., Shinkado T., Nakahashi T., Kuraishi Y. Itch-associated response induced by experimental dry skin in mice. Jpn J Pharmacol 2002, 88:285-292.
32. Murakami M., Nakagawasai O., Suzuki T., Mobarakeh I.I., Sakurada Y., Murata A., Yamadera F., Miyoshi I., Yanai K., Tan-No K., Sasano H., Tadano T., Iijima T. Antinociceptive effect of different types of calcium channel inhibitors and the distribution of various calcium channel alpha 1 subunits in the dorsal horn of spinal cord in mice. Brain Res 2004, 1024:122-129.
33. Nakano T., Andoh T., Lee J.B., Kuraishi Y. Different dorsal horn neurons responding to histamine and allergic itch stimuli. Neuroreport 2008, 19:723-726.
34. Nojima H., Cuellar J.M., Simons C.T., Carstens M.I., Carstens E. Spinal c-Fos expression associated with spontaneous biting in a mouse model of dry skin pruritus. Neurosci Lett 2004, 361:79-82.
35. Park J., Luo Z.D. Calcium channel functions in pain processing. Channels (Austin) 2010, 4:510-517.
36. Paszcuk A.F., Quintao N.L., Fernandes E.S., Juliano L., Chapman K., Andrade-Gordon P., Campos M.M., Vergnolle N., Calixto J.B. Mechanisms underlying the nociceptive and inflammatory responses induced by trypsin in the mouse paw. Eur J Pharmacol 2008, 581:204-215.
37. Patel K.N., Dong X. An itch to be scratched. Neuron 2010, 68:334-339.
38. Pereira P.J., Lazarotto L.F., Leal P.C., Lopes T.G., Morrone F.B., Campos M.M. Inhibition of phosphatidylinositol-3 kinase gamma reduces pruriceptive, inflammatory, and nociceptive responses induced by trypsin in mice. Pain 2011, 152:2861-2869.
39. Pinheiro A.C., da Silva A.J., Prado M.A., Cordeiro Mdo N., Richardson M., Batista M.C., de Castro Junior C.J., Massensini A.R., Guatimosim C., Romano-Silva M.A., Kushmerick C., Gomez M.V. Phoneutria spider toxins block ischemia-induced glutamate release, neuronal death, and loss of neurotransmission in hippocampus. Hippocampus 2009, 19:1123-1129.
40. Pringos E., Vignes M., Martinez J., Rolland V. Peptide neurotoxins that affect voltage-gated calcium channels: a close-up on omega-agatoxins. Toxins (Basel) 2011, 3:17-42.
41. Quintao N.L., Passos G.F., Medeiros R., Paszcuk A.F., Motta F.L., Pesquero J.B., Campos M.M., Calixto J.B. Neuropathic pain-like behavior after brachial plexus avulsion in mice: the relevance of kinin B1 and B2 receptors. J Neurosci 2008, 28:2856-2863.
42. Rahman W., Dickenson A.H. Voltage gated sodium and calcium channel blockers for the treatment of chronic inflammatory pain. Neurosci Lett 2013, 557:19-26.
43. Rigo F.K., Dalmolin G.D., Trevisan G., Tonello R., Silva M.A., Rossato M.F., Klafke J.Z., Cordeiro Mdo N., Castro Junior C.J., Montijo D., Gomez M.V., Ferreira J. Effect of omega-conotoxin MVIIA and Phalpha1beta on paclitaxel-induced acute and chronic pain. Pharmacol Biochem Behav 2013, 114-115:16-22.
44. Roberson D.P., Gudes S., Sprague J.M., Patoski H.A., Robson V.K., Blasl F., Duan B., Oh S.B., Bean B.P., Ma Q., Binshtok A.M., Woolf C.J. Activity-dependent silencing reveals functionally distinct itch-generating sensory neurons. Nat Neurosci 2013, 16:910-918.
45. Sanford M. Intrathecal ziconotide: a review of its use in patients with chronic pain refractory to other systemic or intrathecal analgesics. CNS Drugs 2013, 27:989-1002.
46. Seyfarth F., Schliemann S., Antonov D., Elsner P. Dry skin, barrier function, and irritant contact dermatitis in the elderly. Clin Dermatol 2011, 29:31-36.
47. Souza A.H., Ferreira J., Cordeiro Mdo N., Vieira L.B., De Castro C.J., Trevisan G., Reis H., Souza I.A., Richardson M., Prado M.A., Prado V.F., Gomez M.V. Analgesic effect in rodents of native and recombinant Ph alpha 1beta toxin, a high-voltage-activated calcium channel blocker isolated from armed spider venom. Pain 2008, 140:115-126.
48. Steinhoff M., Neisius U., Ikoma A., Fartasch M., Heyer G., Skov P.S., Luger T.A., Schmelz M. Proteinase-activated receptor-2 mediates itch: a novel pathway for pruritus in human skin. J Neurosci 2003, 23:6176-6180.
49. 2+ channels. J Neurosci 1997, 17:3002-3013.
50. Sukhtankar D.D., Ko M.C. Physiological function of gastrin-releasing peptide and neuromedin B receptors in regulating itch scratching behavior in the spinal cord of mice. PLoS One 2013, 8:e67422.
51. Sun Y.G., Chen Z.F. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature 2007, 448:700-703.
52. Sun Y.G., Zhao Z.Q., Meng X.L., Yin J., Liu X.Y., Chen Z.F. Cellular basis of itch sensation. Science 2009, 325:1531-1534.
53. Takasusuki T., Yaksh T.L. Regulation of spinal substance p release by intrathecal calcium channel blockade. Anesthesiology 2001, 115:153-164.
54. Todorovic S.M., Jevtovic-Todorovic V. The role of T-type calcium channels in peripheral and central pain processing. CNS Neurol Disord Drug Targets 2006, 5:639-653.
55. Tsukumo Y., Matsumoto Y., Miura H., Yano H., Manabe H. Gabapentin and pregabalin inhibit the itch-associated response induced by the repeated application of oxazolone in mice. J Pharmacol Sci 2011, 115:27-35.
56. Vieira L.B., Kushmerick C., Hildebrand M.E., Garcia E., Stea A., Cordeiro M.N., Richardson M., Gomez M.V., Snutch T.P. Inhibition of high voltage-activated calcium channels by spider toxin PnTx3-6. J Pharmacol Exp Ther 2005, 314:1370-1377.
57. Vink S., Alewood P.F. Targeting voltage-gated calcium channels: developments in peptide and small-molecule inhibitors for the treatment of neuropathic pain. Br J Pharmacol 2012, 167:970-989.
58. Weisshaar E., Dalgard F. Epidemiology of itch: adding to the burden of skin morbidity. Acta Derm Venereol 2009, 89:339-350.
59. Yaksh T.L. Calcium channels as therapeutic targets in neuropathic pain. J Pain 2006, 7:S13-30.
60. Yosipovitch G., Bernhard J.D. Clinical practice. Chronic pruritus. N Engl J Med 2013, 368:1625-1634.
61. Zamponi G.W., Lewis R.J., Todorovic S.M., Arneric S.P., Snutch T.P. Role of voltage-gated calcium channels in ascending pain pathways. Brain Res Rev 2009, 60:84-89.
62. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.