N-type voltage gated calcium channels mediate excitatory synaptic transmission in the anterior cingulate cortex of adult mice

Molecular Pain

Volumn 9, Issue 1, 2013, Pages

  Kang, SukJae J ^a   Liu, Ming Gang ^a,b   Shi, Tian Yao ^b,c   Zhao, Ming Gao ^c   Kaang, Bong Kiun ^a   Zhuo, Min ^a,b,d  

^a Seoul National University   (South Korea)

^b UNIVERSITY OF TORONTO   (Canada)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; 2 CHLOROADENOSINE; BACLOFEN; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALCIUM CHANNEL R TYPE; CALCIUM CHANNEL T TYPE; CARBACHOL; GLUTAMIC ACID; OMEGA CONOTOXIN GVIA; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BRAIN REGION; EXCITATORY POSTSYNAPTIC POTENTIAL; MALE; MOLECULAR MECHANICS; MOUSE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION;

2-CHLOROADENOSINE; ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, N-TYPE; CARBACHOL; GYRUS CINGULI; MALE; MICE; MICE, INBRED C57BL; OMEGA-CONOTOXIN GVIA; SYNAPTIC TRANSMISSION;

EID: 84887322980     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-9-58     Document Type: Article

References (65)

1. Wright CE, Angus JA. Effects of N-, P- and Q-type neuronal calcium channel antagonists on mammalian peripheral neurotransmission. Br J Pharmacol 1996, 119(1):49-56. 10.1111/j.1476-5381.1996.tb15676.x, 1915745, 8872356.
2. Takahashi T, Momiyama A. Different types of calcium channels mediate central synaptic transmission. Nature 1993, 366(6451):156-158. 10.1038/366156a0, 7901765.
3. Regehr WG, Mintz IM. Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses. Neuron 1994, 12(3):605-613. 10.1016/0896-6273(94)90216-X, 8155322.
4. Wheeler DB, Randall A, Tsien RW. Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 1994, 264(5155):107-111. 10.1126/science.7832825, 7832825.
5. Castillo PE, Weisskopf MG, Nicoll RA. The role of Ca2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron 1994, 12(2):261-269. 10.1016/0896-6273(94)90269-0, 8110457.
6. Luebke JI, Dunlap K, Turner TJ. Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron 1993, 11(5):895-902. 10.1016/0896-6273(93)90119-C, 7902110.
7. Dunlap K, Luebke JI, Turner TJ. Exocytotic Ca2+ channels in mammalian central neurons. Trends Neurosci 1995, 18(2):89-98. 10.1016/0166-2236(95)93882-X, 7537420.
8. Olivera BM, Miljanich GP, Ramachandran J, Adams ME. Calcium channel diversity and neurotransmitter release: the omega-conotoxins and omega-agatoxins. Annu Rev Biochem 1994, 63:823-867. 10.1146/annurev.bi.63.070194.004135, 7979255.
9. Catterall WA, Few AP. Calcium channel regulation and presynaptic plasticity. Neuron 2008, 59(6):882-901. 10.1016/j.neuron.2008.09.005, 18817729.
10. Cao YQ, Tsien RW. Different relationship of N- and P/Q-type Ca2+ channels to channel-interacting slots in controlling neurotransmission at cultured hippocampal synapses. J Neurosci 2010, 30(13):4536-4546. 10.1523/JNEUROSCI.5161-09.2010, 20357104.
11. Gribkoff VK. The role of voltage-gated calcium channels in pain and nociception. Semin Cell Dev Biol 2006, 17(5):555-564. 10.1016/j.semcdb.2006.09.002, 17141538.
12. Cao YQ. Voltage-gated calcium channels and pain. Pain 2006, 126(1-3):5-9.
13. Park J, Luo ZD. Calcium channel functions in pain processing. Channels (Austin) 2010, 4(6):510-517. 3052250, 21150297.
14. Zamponi GW, Lewis RJ, Todorovic SM, Arneric SP, Snutch TP. Role of voltage-gated calcium channels in ascending pain pathways. Brain Res Rev 2009, 60(1):84-89. 10.1016/j.brainresrev.2008.12.021, 2692704, 19162069.
15. Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron 2006, 52(1):77-92. 10.1016/j.neuron.2006.09.021, 1810425, 17015228.
16. Dogrul A, Gardell LR, Ossipov MH, Tulunay FC, Lai J, Porreca F. Reversal of experimental neuropathic pain by T-type calcium channel blockers. Pain 2003, 105(1-2):159-168.
17. Brittain JM, Duarte DB, Wilson SM, Zhu W, Ballard C, Johnson PL, Liu N, Xiong W, Ripsch MS, Wang Y, et al. Suppression of inflammatory and neuropathic pain by uncoupling CRMP-2 from the presynaptic Ca2+ channel complex. Nat Med 2011, 17(7):822-829. 10.1038/nm.2345, 3219927, 21642979.
18. Adams DJ, Callaghan B, Berecki G. Analgesic conotoxins: block and G protein-coupled receptor modulation of N-type (Ca(V) 2.2) calcium channels. Br J Pharmacol 2012, 166(2):486-500. 10.1111/j.1476-5381.2011.01781.x, 3417482, 22091786.
19. Atanassoff PG, Hartmannsgruber MW, Thrasher J, Wermeling D, Longton W, Gaeta R, Singh T, Mayo M, McGuire D, Luther RR. Ziconotide, a new N-type calcium channel blocker, administered intrathecally for acute postoperative pain. Reg Anesth Pain Med 2000, 25(3):274-278.
20. Perret D, Luo ZD. Targeting voltage-gated calcium channels for neuropathic pain management. Neurotherapeutics 2009, 6(4):679-692. 10.1016/j.nurt.2009.07.006, 2755636, 19789072.
21. Staats PS, Yearwood T, Charapata SG, Presley RW, Wallace MS, Byas-Smith M, Fisher R, Bryce DA, Mangieri EA, Luther RR, et al. Intrathecal ziconotide in the treatment of refractory pain in patients with cancer or AIDS: a randomized controlled trial. JAMA 2004, 291(1):63-70. 10.1001/jama.291.1.63, 14709577.
22. Vogt BA. Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 2005, 6(7):533-544. 2659949, 15995724.
23. Zhuo M. Cortical excitation and chronic pain. Trends Neurosci 2008, 31(4):199-207. 10.1016/j.tins.2008.01.003, 18329111.
24. Li XY, Ko HG, Chen T, Descalzi G, Koga K, Wang H, Kim SS, Shang Y, Kwak C, Park SW, et al. Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. Science 2010, 330(6009):1400-1404. 10.1126/science.1191792, 21127255.
25. Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, Steenland HW, Zhuo M. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci 2008, 28(29):7445-7453. 10.1523/JNEUROSCI.1812-08.2008, 18632948.
26. Yen CP, Kuan CY, Sheehan J, Kung SS, Wang CC, Liu CK, Kwan AL. Impact of bilateral anterior cingulotomy on neurocognitive function in patients with intractable pain. J Clin Neurosci 2009, 16(2):214-219. 10.1016/j.jocn.2008.04.008, 19101146.
27. Yen CP, Kung SS, Su YF, Lin WC, Howng SL, Kwan AL. Stereotactic bilateral anterior cingulotomy for intractable pain. J Clin Neurosci 2005, 12(8):886-890. 10.1016/j.jocn.2004.11.018, 16326270.
28. Johansen JP, Fields HL, Manning BH. The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci U S A 2001, 98(14):8077-8082. 10.1073/pnas.141218998, 35470, 11416168.
29. Zhuo M. Molecular mechanisms of pain in the anterior cingulate cortex. J Neurosci Res 2006, 84(5):927-933. 10.1002/jnr.21003, 16862566.
30. Kang SJ, Liu MG, Chen T, Ko HG, Baek GC, Lee HR, Lee K, Collingridge GL, Kaang BK, Zhuo M. Plasticity of metabotropic glutamate receptor-dependent long-term depression in the anterior cingulate cortex after amputation. J Neurosci 2012, 32(33):11318-11329. 10.1523/JNEUROSCI.0146-12.2012, 22895715.
31. Liu MG, Kang SJ, Shi TY, Koga K, Zhang MM, Collingridge GL, Kaang BK, Zhuo M. Long-term potentiation of synaptic transmission in the adult mouse insular cortex: multielectrode array recordings. J Neurophysiol 2013, 110(2):505-521. 10.1152/jn.01104.2012, 23636718.
32. Liu MG, Koga K, Guo YY, Kang SJ, Collingridge GL, Kaang BK, Zhao MG, Zhuo M. Long-term depression of synaptic transmission in the adult mouse insular cortex in vitro. Eur J Neurosci 2013, 38(8):3128-3145. 10.1111/ejn.12330, 23930740.
33. Oka H, Shimono K, Ogawa R, Sugihara H, Taketani M. A new planar multielectrode array for extracellular recording: application to hippocampal acute slice. J Neurosci Methods 1999, 93(1):61-67. 10.1016/S0165-0270(99)00113-2, 10598865.
34. Zhao MG, Ko SW, Wu LJ, Toyoda H, Xu H, Quan J, Li J, Jia Y, Ren M, Xu ZC, et al. Enhanced presynaptic neurotransmitter release in the anterior cingulate cortex of mice with chronic pain. J Neurosci 2006, 26(35):8923-8930. 10.1523/JNEUROSCI.2103-06.2006, 16943548.
35. Toyoda H, Zhao MG, Xu H, Wu LJ, Ren M, Zhuo M. Requirement of extracellular signal-regulated kinase/mitogen-activated protein kinase for long-term potentiation in adult mouse anterior cingulate cortex. Mol Pain 2007, 3:36. 10.1186/1744-8069-3-36, 2245920, 18053155.
36. Wu LJ, Ko SW, Toyoda H, Zhao MG, Xu H, Vadakkan KI, Ren M, Knifed E, Shum F, Quan J, et al. Increased anxiety-like behavior and enhanced synaptic efficacy in the amygdala of GluR5 knockout mice. PLoS One 2007, 2(1):e167. 10.1371/journal.pone.0000167, 1766473, 17245443.
37. Wu LJ, Zhang XH, Fukushima H, Zhang F, Wang H, Toyoda H, Li BM, Kida S, Zhuo M. Genetic enhancement of trace fear memory and cingulate potentiation in mice overexpressing Ca2+/calmodulin-dependent protein kinase IV. Eur J Neurosci 2008, 27(8):1923-1932. 10.1111/j.1460-9568.2008.06183.x, 18412613.
38. Gasparini S, Kasyanov AM, Pietrobon D, Voronin LL, Cherubini E. Presynaptic R-type calcium channels contribute to fast excitatory synaptic transmission in the rat hippocampus. J Neurosci 2001, 21(22):8715-8721.
39. Gross RA, Macdonald RL, Ryan-Jastrow T. 2-Chloroadenosine reduces the N calcium current of cultured mouse sensory neurones in a pertussis toxin-sensitive manner. J Physiol 1989, 411:585-595. 1190543, 2614735.
40. Lester RA, Jahr CE. Quisqualate receptor-mediated depression of calcium currents in hippocampal neurons. Neuron 1990, 4(5):741-749. 10.1016/0896-6273(90)90200-Y, 1971515.
41. Mintz IM, Bean BP. GABAB receptor inhibition of P-type Ca2+ channels in central neurons. Neuron 1993, 10(5):889-898. 10.1016/0896-6273(93)90204-5, 8388225.
42. Catterall WA. Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 2011, 3(8):a003947. 10.1101/cshperspect.a003947, 3140680, 21746798.
43. McGivern JG, McDonough SI. Voltage-gated calcium channels as targets for the treatment of chronic pain. Curr Drug Targets CNS Neurol Disord 2004, 3(6):457-478. 10.2174/1568007043336743, 15578964.
44. Yaksh TL. Calcium channels as therapeutic targets in neuropathic pain. J Pain 2006, 7(1 Suppl 1):S13-30.
45. Jun K, Piedras-Renteria ES, Smith SM, Wheeler DB, Lee SB, Lee TG, Chin H, Adams ME, Scheller RH, Tsien RW, et al. Ablation of P/Q-type Ca(2+) channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the alpha(1A)-subunit. Proc Natl Acad Sci U S A 1999, 96(26):15245-15250. 10.1073/pnas.96.26.15245, 24805, 10611370.
46. Rajakulendran S, Kaski D, Hanna MG. Neuronal P/Q-type calcium channel dysfunction in inherited disorders of the CNS. Nat Rev Neurol 2012, 8(2):86-96. 10.1038/nrneurol.2011.228, 22249839.
47. Tottene A, Conti R, Fabbro A, Vecchia D, Shapovalova M, Santello M, van den Maagdenberg AM, Ferrari MD, Pietrobon D. Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron 2009, 61(5):762-773. 10.1016/j.neuron.2009.01.027, 19285472.
48. Tottene A, Fellin T, Pagnutti S, Luvisetto S, Striessnig J, Fletcher C, Pietrobon D. Familial hemiplegic migraine mutations increase Ca(2+) influx through single human CaV2.1 channels and decrease maximal CaV2.1 current density in neurons. Proc Natl Acad Sci U S A 2002, 99(20):13284-13289. 10.1073/pnas.192242399, 130625, 12235360.
49. Mato S, Lafourcade M, Robbe D, Bakiri Y, Manzoni OJ. Role of the cyclic-AMP/PKA cascade and of P/Q-type Ca++ channels in endocannabinoid-mediated long-term depression in the nucleus accumbens. Neuropharmacology 2008, 54(1):87-94. 10.1016/j.neuropharm.2007.04.014, 17606273.
50. Wei F, Li P, Zhuo M. Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J Neurosci 1999, 19(21):9346-9354.
51. Harvey J, Palmer MJ, Irving AJ, Clarke VR, Collingridge GL. NMDA receptor dependence of mGlu-mediated depression of synaptic transmission in the CA1 region of the rat hippocampus. Br J Pharmacol 1996, 119(6):1239-1247. 10.1111/j.1476-5381.1996.tb16028.x, 1915892, 8937729.
52. Vignes M, Clarke VR, Davies CH, Chambers A, Jane DE, Watkins JC, Collingridge GL. Pharmacological evidence for an involvement of group II and group III mGluRs in the presynaptic regulation of excitatory synaptic responses in the CA1 region of rat hippocampal slices. Neuropharmacology 1995, 34(8):973-982. 10.1016/0028-3908(95)00093-L, 8532178.
53. Kamiya H, Shinozaki H, Yamamoto C. Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J Physiol 1996, 493(Pt 2):447-455. 1158929, 8782108.
54. Burke JP, Hablitz JJ. Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex. J Neurosci 1994, 14(8):5120-5130.
55. Glaum SR, Slater NT, Rossi DJ, Miller RJ. Role of metabotropic glutamate (ACPD) receptors at the parallel fiber-Purkinje cell synapse. J Neurophysiol 1992, 68(4):1453-1462.
56. Calabresi P, Pisani A, Mercuri NB, Bernardi G. Heterogeneity of metabotropic glutamate receptors in the striatum: electrophysiological evidence. Eur J Neurosci 1993, 5(10):1370-1377. 10.1111/j.1460-9568.1993.tb00923.x, 8275236.
57. Swartz KJ, Bean BP. Inhibition of calcium channels in rat CA3 pyramidal neurons by a metabotropic glutamate receptor. J Neurosci 1992, 12(11):4358-4371.
58. Swartz KJ, Merritt A, Bean BP, Lovinger DM. Protein kinase C modulates glutamate receptor inhibition of Ca2+ channels and synaptic transmission. Nature 1993, 361(6408):165-168. 10.1038/361165a0, 8380626.
59. Sahara Y, Westbrook GL. Modulation of calcium currents by a metabotropic glutamate receptor involves fast and slow kinetic components in cultured hippocampal neurons. J Neurosci 1993, 13(7):3041-3050.
60. Sayer RJ, Schwindt PC, Crill WE. Metabotropic glutamate receptor-mediated suppression of L-type calcium current in acutely isolated neocortical neurons. J Neurophysiol 1992, 68(3):833-842.
61. Choi S, Lovinger DM. Metabotropic glutamate receptor modulation of voltage-gated Ca2+ channels involves multiple receptor subtypes in cortical neurons. J Neurosci 1996, 16(1):36-45.
62. Anwyl R. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 1999, 29(1):83-120. 10.1016/S0165-0173(98)00050-2, 9974152.
63. Stefani A, Pisani A, Mercuri NB, Calabresi P. The modulation of calcium currents by the activation of mGluRs. Functional implications. Mol Neurobiol 1996, 13(1):81-95. 10.1007/BF02740753, 8892337.
64. Conn PJ, Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 1997, 37:205-237. 10.1146/annurev.pharmtox.37.1.205, 9131252.
65. Schoepp DD, Jane DE, Monn JA. Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 1999, 38(10):1431-1476. 10.1016/S0028-3908(99)00092-1, 10530808.