International Journal of Oral Biology

  • 제36권2호
  • /
  • Pages.43-50
  • /
  • 2011
  • /
  • 1226-7155(pISSN)
  • /
  • 2287-6618(eISSN)
대한구강생물학회 (The Korean Academy of Oral Biology)
권호 표지

Intracisternal Administration of Voltage Dependent Calcium Channel Blockers Attenuates Orofacial Inflammatory Nociceptive Behavior in Rats

  • Won, Kyoung-A. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Park, Sang-H. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Kim, Bo-K. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Baek, Kyoung-S. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Yoon, Dong-H. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Ahn, Dong-K. (Department of Oral Physiology, School of Dentistry, Kyungpook National University)
  • 투고 : 2011.02.14
  • 심사 : 2011.04.15
  • 발행 : 2011.06.30
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Voltage dependent calcium channel (VDCC), one of the most important regulator of $Ca^{2+}$ concentration in neuron, play an essential role in the central processing of nociceptive information. The present study investigated the antinociceptive effects of L, T or N type VDCC blockers on the formalin-induced orofacial inflammatory pain. Experiments were carried out on adult male Sprague-Dawley rats weighing 220-280 g. Anesthetized rats were individually fixed on a stereotaxic frame and a polyethylene (PE) tube was implanted for intracisternal injection. After 72 hours, 5% formalin ($50 \;{\mu}L$) was applied subcutaneously to the vibrissa pad and nociceptive scratching behavior was recorded for nine successive 5 min intervals. VDCC blockers were administered intracisternally 20 minutes prior to subcutaneous injection of formalin into the orofacial area. The intracisternal administration of 350 or $700{\mu}g$ of verapamil, a blocker of L type VDCC, significantly decreased the number of scratches and duration in the behavioral responses produced by formalin injection. Intracisternal administration of 75 or $150 \;{\mu}g$ of mibefradil, a T type VDCC blocker, or 11 or $22\; {\mu}g$ of cilnidipine, a N type VDCC blocker, also produced significant suppression of the number of scratches and duration of scratching in the first and second phase. Neither intracisternal administration of all VDCC blockers nor vehicle did not affect in motor dysfunction. The present results suggest that central VDCCs play an important role in orofacial nociceptive transmission and a targeted inhibition of the VDCCs is a potentially important treatment approach for inflammatory pain originating in the orofacial area.

키워드

참고문헌

  1. Abbott FV, Franklin KB, Westbrook RF. The formalin test: scoring properties of the first and second phases of the pain response in rats. Pain. 1995;60:91-102. https://doi.org/10.1016/0304-3959(94)00095-V
  2. Ahlijanian MK, Westenbroek RE, Catterall WA. Subunit structure and localization of dihydropyridine-sensitive calcium channels in mammalian brain, spinal cord and retina. Neuron. 1990;4:819-32. https://doi.org/10.1016/0896-6273(90)90135-3
  3. Ahn DK, Lee KR, Lee HJ, Kim SK, Choi HS, Lim EJ, Park JS. Intracisternal administration of chemokines facilitated formalin- induced behavioral responses in the orofacial area of freely moving rats. Brain Res Bull. 2005;66:50-8. https://doi.org/10.1016/j.brainresbull.2005.03.015
  4. Ahn DK, Kim YS, Park JS. Central NO is involved in the antinociceptive action of intracisternal antidepressants in freely moving rats. Neurosci Lett. 1998;243:105-8. https://doi.org/10.1016/S0304-3940(98)00099-8
  5. Altier C, Zamponi GW. Targeting Ca2+ channels to treat pain: T-type versus N-type. Trends Pharmacol Sci. 2004;25:465-70. https://doi.org/10.1016/j.tips.2004.07.004
  6. Barclay JW, Morgan A, Burgoyne RD. Calcium-dependent regulation of exocytosis. Cell Calcium. 2005;38:343-53. https://doi.org/10.1016/j.ceca.2005.06.012
  7. Barton ME, Eberle EL, Shannon HE. The antihyperalgesic effects of the T-type calcium channel blockers ethosuximide, trimethadione, and mibefradil. Eur J Pharmacol. 2005;521: 79-85. https://doi.org/10.1016/j.ejphar.2005.08.017
  8. Carbone E, Lux HD. A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature. 1984; 310:501-2. https://doi.org/10.1038/310501a0
  9. Chen JQ, Chen WH, Deng MC, Li G, Kang Y, Ding ZH, Liang SP. Analgesic effect of huwentoxin-I, a new N-type voltagesensitive calcium channel blocker, on acute visceral pain in rats. Di Yi Jun Yi Da Xue Xue Bao. 2005;25:10-4.
  10. Cheng JK, Lin CS, Chen CC, Yang JR, Chiou LC. Effects of intrathecal injection of T-type calcium channel blockers in the rat formalin test. Behav Pharmacol. 2007;18:1-8. https://doi.org/10.1097/FBP.0b013e3280141375
  11. Choi HS, Ju JS, Lee HJ, Jung CY, Kim BC, Park JS, Ahn DK. Effects of TNF-alpha injected intracisternally on the nociceptive jaw-opening reflex and orofacial formalin test in freely moving rats. Prog Neuropsychopharmacol Biol Psychiatry. 2003a;27:613-8. https://doi.org/10.1016/S0278-5846(03)00049-6
  12. Choi HS, Ju JS, Lee HJ, Kim BC, Park JS, Ahn DK. Effects of intracisternal injection of interleukin-6 on nociceptive jaw opening reflex and orofacial formalin test in freely moving rats. Brain Res Bull. 2003b;59:365-70. https://doi.org/10.1016/S0361-9230(02)00931-0
  13. Choi S, Na HS, Kim J, Lee J, Lee S, Kim D, Park J, Chen CC, Campbell KP, Shin HS. Attenuated pain responses in mice lacking Ca(V)3.2 T-type channels. Genes Brain Behav. 2007; 6:425-31. https://doi.org/10.1111/j.1601-183X.2006.00268.x
  14. Christensen D, Gautron M, Guilbaud G, Kayser V. Combined systemic administration of the glycine/NMDA receptor antagonist, (+)-HA966 and morphine attenuates pain-related behaviour in a rat model of trigeminal neuropathic pain. Pain. 1999;83:433-40. https://doi.org/10.1016/S0304-3959(99)00126-8
  15. Coderre TJ, Melzack R. The role of NMDA receptor-operated calcium channels in persistent nociception after formalininduced tissue injury. J Neurosci. 1992;12:3671-5.
  16. Diaz A, Dickenson AH. Blockade of spinal N- and P-type, but not L-type, calcium channels inhibits the excitability of rat dorsal horn neurones produced by subcutaneous formalin inflammation. Pain. 1997;69:93-100. https://doi.org/10.1016/S0304-3959(96)03271-X
  17. Dunham NW, Miya TS. A note on a simple apparatus for detecting neurological deficit in rats and mice. J Am Pharm Assoc Am Pharm Assoc. 1957;46:208-9. https://doi.org/10.1002/jps.3030460322
  18. Ebersberger A, Portz S, Meissner W, Schaible HG, Richter F. Effects of N-, P/Q- and L-type calcium channel blockers on nociceptive neurones of the trigeminal nucleus with input from the dura. Cephalalgia. 2004;24:250-61. https://doi.org/10.1111/j.1468-2982.2004.00656.x
  19. Fang Z, Hwang JH, Kim JS, Jung SJ, Oh SB. R-type Calcium Channel Isoform in Rat Dorsal Root Ganglion Neurons. Korean J Physiol Pharmacol. 2010;14:45-9. https://doi.org/10.4196/kjpp.2010.14.1.45
  20. Gohil K, Bell JR, Ramachandran J, Miljanich GP. Neuroanatomical distribution of receptors for a novel voltagesensitive calcium channel antagonist, SNX-230 (q-conopeptide MVIIC), Brain Res. 1994;653:258-66. https://doi.org/10.1016/0006-8993(94)90398-0
  21. Gribkoff VK. The role of voltage-gated calcium channels in pain and nociception. Semin Cell Dev Biol. 2006;17:555- 64. https://doi.org/10.1016/j.semcdb.2006.09.002
  22. Gurdal H, Sara Y, Tulunay FC. Effects of calcium channel blockers on formalin-induced nociception and inflammation in rats. Pharmacology. 1992;44:290-6. https://doi.org/10.1159/000138932
  23. Hatakeyama S, Wakamori M, Ino M, Miyamoto N, Takahashi E, Yoshinaga T, Sawada K, Imoto K, Tanaka I, Yoshizawa T, Nishizawa Y, Mori Y, Niidome T, Shoji S. Differential nociceptive responses in mice lacking the alpha(1B) subunit of N-type Ca(2+) channels. Neuroreport. 2001;12:2423-7. https://doi.org/10.1097/00001756-200108080-00027
  24. Heinke B, Balzer E, Sandk hler J. Pre-and postsynaptic contributions of voltage-dependent Ca2+ channels to nociceptive transmission in rat spinal lamina I neurons. Eur J Neurosci. 2004;19:103-11. https://doi.org/10.1046/j.1460-9568.2003.03083.x
  25. Hell JW, Westenbroek RE, Warner C, Ahlijanian MK, Prystay W, Gilbert MM, Snutch TP and Catterall WA. Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel a1 subunits. J Cell Biol. 1993;123:949-62. https://doi.org/10.1083/jcb.123.4.949
  26. Himpens B, Missiaen L, Casteels R. Ca2+ homeostasis in vascular smooth muscle. J Vasc Res. 1995;32:207-19. https://doi.org/10.1159/000159095
  27. Idanpaan-Heikkila JJ, Guilbaud G. Pharmacological studies on a rat model of trigeminal neuropathic pain: baclofen, but not carbamazepine, morphine or tricyclic antidepressants, attenuates the allodynia-like behaviour. Pain. 1999;79:281-90. https://doi.org/10.1016/S0304-3959(98)00172-9
  28. Ikeda H, Heinke B, Ruscheweyh R, Sandkuhler J. Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science. 2003;299:1237-40. https://doi.org/10.1126/science.1080659
  29. Ikeda M, Matsumoto S. Classification of voltage-dependent Ca2+ channels in trigeminal ganglion neurons from neonatal rats. Life Sci. 2003;18:1175-87.
  30. Jiang Z, Rempel J, Li J, Sawchuk MA, Carlin KP, Brownstone RM. Development of L-type calcium channels and a nifedipine-sensitive motor activity in the postnatal mouse spinal cord. Eur J Neurosci. 1999;11:3481-7.
  31. Katoh A, Jindal JA, Raymond JL. Motor deficits in homozygous and heterozygous p/q-type calcium channel mutants. J Neurophysiol. 2007;97:1280-7. https://doi.org/10.1152/jn.00322.2006
  32. Kerr LM, Filloux F, Olivera BM, Jackson H, Wamsley JK. Autoradiographic localization of calcium channels with [125I]omega-Conotoxin in rat brain. Eur J Pharmacol. 1988;146:181-3. https://doi.org/10.1016/0014-2999(88)90501-8
  33. Kim C, Jun K, Lee T, Kim SS, McEnery MW, Chin H, Kim HL, Park JM, Kim DK, Jung SJ, Kim J, Shin HS. Altered nociceptive response in mice deficient in the alpha(1B) subunit of the voltage-dependent calcium channel. Mol Cell Neurosci. 2001;18:235-45. https://doi.org/10.1006/mcne.2001.1013
  34. Koganei H, Shoji M, Iwata S. Suppression of formalin-induced nociception by cilnidipine, a voltage-dependent calcium channel blocker. Biol Pharm Bull. 2009;32:1695-700. https://doi.org/10.1248/bpb.32.1695
  35. Lee MK, Choi BY, Yang GY, Jeon HJ, Kyung HM, Kwon OW, Park HS, Bae YC, Mokha SS, Ahn DK. Low doses of cannabinoids enhance the antinociceptive effects of intracisternally administered mGluRs groups II and III agonists in formalininduced TMJ nociception in rats. Pain. 2008;139:367-75. https://doi.org/10.1016/j.pain.2008.05.005
  36. Levi AJ, Brooksby P, Hancox JC. One hump or two? The triggering of calcium release from the sarcoplasmic reticulum and the voltage dependence of contraction in mammalian cardiac muscle. Cardiovasc Res. 1993;27:1743-57. https://doi.org/10.1093/cvr/27.10.1743
  37. Liang YC, Huang CC, Hsu KS. The synthetic cannabinoids attenuate allodynia and hyperalgesia in a rat model of trigeminal neuropathic pain. Neuropharmacology. 2007;53: 169-77.
  38. Lipscombe D, Helton TD, Xu W. L-type calcium channels: the low down. J Neurophysiol. 2004;92:2633-41. https://doi.org/10.1152/jn.00486.2004
  39. Lux EA. Case report: successful treatment of a patient with trigeminal neuropathy using ziconotide. Anesth Analg. 2010;110:1195-7.
  40. Malmberg AB, Yaksh TL. Voltage-sensitive calcium channels in spinal nociceptive processing: blockade of N- and P-type channels inhibits formalin-induced nociception J Neurosci. 1994;14:4882-90.
  41. Miller RJ. Multiple calcium channels and neuronal function. Science. 1987;235:46-52. https://doi.org/10.1126/science.2432656
  42. Mochida S, Yokoyama CT, Kim DK, Itoh K, Catterall WA. Evidence for a voltage-dependent enhancement of neuro-transmitter release mediated via the synaptic protein interaction site of N-type Ca2+ channels. Proc Natl Acad Sci U S A. 1998;95:14523-8. https://doi.org/10.1073/pnas.95.24.14523
  43. Murakami M, Nakagawasai O, Fujii S, Hosono M, Hozumi S, Esashi A, Taniguchi R, Okamura T, Suzuki T, Sasano H, Yanagisawa T, Tan-no K, Tadano T, Kitamura K, Kisara K. Antinociceptive effect of cilnidipine, a novel N-type calcium channel antagonist. Brain Res. 2000;868:123-7. https://doi.org/10.1016/S0006-8993(00)02295-2
  44. Raboisson P, Dallel R. The orofacial formalin test. Neurosci Biobehav Rev. 2004;28:219-26. https://doi.org/10.1016/j.neubiorev.2003.12.003
  45. Raboisson P, Dallel R, Clavelou P, Sessle BJ, Woda A. Effects of subcutaneous formalin on the activity of trigeminal brain stem nociceptive neurones in the rat. J Neurophysiol. 1995;73:496-505. https://doi.org/10.1152/jn.1995.73.2.496
  46. Rozas G, Guerra MJ, Labandeira-Garcia JL. An automated rotarod method for quantitative drug-free evaluation of overall motor deficits in rat models of parkinsonism. Brain Res Brain Res Protoc. 1997;2:75-84. https://doi.org/10.1016/S1385-299X(97)00034-2
  47. Schmidtko A, Lotsch J, Freynhagen R, Geisslinger G. Ziconotide for treatment of severe chronic pain. Lancet. 2010;375:1569- 77. https://doi.org/10.1016/S0140-6736(10)60354-6
  48. Sluka KA. Blockade of N- and P/O-type calcium channels reduced the secondary heat hyperalgesia induced by acute inflammation. J Pharmacol Exp Ther. 1998;287:232-7.
  49. Snutch TP. Targeting chronic and neuropathic pain: the N-type calcium channel comes of age. NeuroRx. 2005;2:662-70. https://doi.org/10.1602/neurorx.2.4.662
  50. Stirling LC, Forlani G, Baker MD, Wood JN, Matthews EA, Dickenson AH, Nassar MA. Nociceptor-specific gene deletion using heterozygous NaV1.8-Cre recombinase mice. Pain. 2005;113:27-36. https://doi.org/10.1016/j.pain.2004.08.015
  51. Tjolsen A, Berge OG, Hunskaar S, Rosland JH, Hole K. The formalin test: an evaluation of the method. Pain. 1992;51:5- 17. https://doi.org/10.1016/0304-3959(92)90003-T
  52. Wang XM, Zhang ZJ, Bains R, Mokha SS. Effect of antisense knock-down of alpha(2a)- and alpha(2c)-adrenoceptors on the antinociceptive action of clonidine on trigeminal nociception in the rat. Pain. 2002;98:27-35. https://doi.org/10.1016/S0304-3959(01)00464-X
  53. White G, Lovinger DM, Weight FF Transient lowthreshold Ca2+ current triggers burst firing through an afterdepolarizing potential in an adult mammalian neuron. Proc Natl Acad Sci USA. 1989;86:6802-6. https://doi.org/10.1073/pnas.86.17.6802
  54. Xu W, Lipscombe D. Neuronal Ca(v)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci. 2001;21:5944-51.
  55. Yaksh TL, Rudy TA. Chronic catheterization of the spinal subarachnoid space. Physiol Behav. 1976;17:1031-6. https://doi.org/10.1016/0031-9384(76)90029-9
  56. Yang GY, Woo YW, Park MK, Bae YC, Ahn DK, Bonfa E. Intracisternal administration of NR2 antagonists attenuates facial formalin-induced nociceptive behavior in rats. J Orofac Pain. 2010;24:203-11.
  57. Zheng X, Bobich JA. Asequential view of neurotransmitter release. Brain Res Bull. 1998;47:117-28. https://doi.org/10.1016/S0361-9230(98)00040-9