The Ca2+ channel β subunit determines whether stimulation of Gq-coupled receptors enhances or inhibits N current

Journal of General Physiology

Volumn 134, Issue 5, 2009, Pages 369-384

  Heneghan, John F ^a,b   Mitra Ganguli, Tora ^a,c   Stanish, Lee F ^a,d   Liu, Liwang ^a   Zhao, Rubing ^a   Rittenhouse, Ann R ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; CALCIUM CHANNEL; CALCIUM CHANNEL BETA; CALCIUM CHANNEL BETA1B; CALCIUM CHANNEL BETA2A; CALCIUM CHANNEL BETA3; CALCIUM CHANNEL BETA4; CALCIUM CHANNEL N TYPE; G PROTEIN COUPLED RECEPTOR; M1 RECEPTOR; NEUROKININ 1 RECEPTOR; PALMITIC ACID; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; CALCIUM; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MUSCARINIC M1 RECEPTOR; PROTEIN SUBUNIT;

ARTICLE; CELL STIMULATION; HUMAN; HUMAN CELL; MEMBRANE CURRENT; MODULATION; PALMITOYLATION; PROTEIN EXPRESSION; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL MEMBRANE POTENTIAL; ELECTRIC CONDUCTIVITY; METABOLISM; RAT; SUPERIOR CERVICAL GANGLION;

ANIMALS; CALCIUM; CALCIUM CHANNELS, N-TYPE; CELLS, CULTURED; ELECTRIC CONDUCTIVITY; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HUMANS; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; PROTEIN SUBUNITS; RATS; RECEPTOR, MUSCARINIC M1; SUPERIOR CERVICAL GANGLION;

EID: 70350462762     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200910203     Document Type: Article

References (84)

1. Baekkeskov, S., and J. Kanaani. 2009. Palmitoylation cycles and regulation of protein function (Review). Mol. Membr. Biol. 26:42-54. doi:10.1080/09687680802680108
2. Bannister, R.A., K. Melliti, and B.A. Adams. 2004. Differential modulation of CaV2.3 Ca2+ channels by Galphaq/11-coupled muscarinic receptors. Mol. Pharmacol. 65:381-388. doi:10.1124/mol.65.2.381
3. Barrett, C.F., and A.R. Rittenhouse. 2000. Modulation of N-type calcium channel activity by G-proteins and protein kinase C. J. Gen. Physiol. 115:277-286. doi:10.1085/jgp.115.3.277
4. Barrett, C.F., L. Liu, and A.R. Rittenhouse. 2001. Arachidonic acid reversibly enhances N-type calcium current at an extracellular site. Am. J. Physiol. Cell Physiol. 280:C1306-C1318. (Pubitemid 32433764)
5. Beech, D.J., L. Bernheim, and B. Hille. 1992. Pertussis toxin and voltage dependence distinguish multiple pathways modulating calcium channels of rat sympathetic neurons. Neuron. 8:97-106. doi:10.1016/0896-6273(92)90111-P
6. Bernheim, L., A. Mathie, and B. Hille. 1992. Characterization of muscarinic receptor subtypes inhibiting Ca2+ current and M current in rat sympathetic neurons. Proc. Natl. Acad. Sci. USA. 89:9544-9548. doi:10.1073/pnas.89.20.9544
7. Birnbaumer, L., N. Qin, R. Olcese, E. Tareilus, D. Platano, J. Costantin, and E. Stefani. 1998. Structures and functions of calcium channel beta subunits. J. Bioenerg. Biomembr. 30:357-375. doi:10.1023/A:1021989622656
8. Brosenitsch, T.A., and D.M. Katz. 2001. Physiological patterns of electrical stimulation can induce neuronal gene expression by activating N-type calcium channels. J. Neurosci. 21:2571-2579.
9. Catterall, W.A. 2000. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol. 16:521-555. doi:10.1146/annurev.cellbio.16. 1.521
10. Chemin, J., J. Nargeot, and P. Lory. 2007. Chemical determinants involved in anandamide-induced inhibition of T-type calcium channels. J. Biol. Chem. 282:2314-2323. doi:10.1074/jbc.M610033200
11. Chien, A.J., and M.M. Hosey. 1998. Post-translational modifications of beta subunits of voltage-dependent calcium channels. J. Bioenerg. Biomembr. 30:377-386. doi:10.1023/A:1021941706726
12. Chien, A.J., K.M. Carr, R.E. Shirokov, E. Rios, and M.M. Hosey. 1996. Identification of palmitoylation sites within the L-type calcium channel beta2a subunit and effects on channel function. J. Biol. Chem. 271:26465-26468. doi:10.1074/jbc.271.43.26465
13. Chien, A.J., T. Gao, E. Perez-Reyes, and M.M. Hosey. 1998. Membrane targeting of L-type calcium channels. Role of palmitoylation in the subcellular localization of the beta2a subunit. J. Biol. Chem. 273:23590-23597. doi:10.1074/jbc.273.36.23590
14. Day, N.C., S.G. Volsen, A.L. McCormack, P.J. Craig, W. Smith, R.E. Beattie, P.J. Shaw, S.B. Ellis, M.M. Harpold, and P.G. Ince. 1998. The expression of voltage-dependent calcium channel beta subunits in human hippocampus. Brain Res. Mol. Brain Res. 60:259-269. doi:10.1016/S0169-328X(98) 00186-7
15. Delmas, P., B. Coste, N. Gamper, and M.S. Shapiro. 2005. Phosphoinositide lipid second messengers: new paradigms for calcium channel modulation. Neuron. 47:179-182. doi:10.1016/j.neuron.2005.07.001 (Pubitemid 41019249)
16. Doughman, R.L., A.J. Firestone, and R.A. Anderson. 2003. Phosphatidylinositol phosphate kinases put PI4,5P(2) in its place. J. Membr. Biol. 194:77-89. doi:10.1007/s00232-003-2027-7
17. El-Husseini, A.E.-D., E. Schnell, S. Dakoji, N. Sweeney, Q. Zhou, O. Prange, C. Gauthier-Campbell, A. Aguilera-Moreno, R.A. Nicoll, and D.S. Bredt. 2002. Synaptic strength regulated by palmitate cycling on PSD-95. Cell. 108:849-863. doi:10.1016/S0092-8674(02)00683-9
18. Elmslie, K.S. 2003. Neurotransmitter modulation of neuronal calcium channels. J. Bioenerg. Biomembr. 35:477-489. doi:10.1023/B:JOBB.0000008021. 55853.18
19. Ford, C.P., P.L. Stemkowski, P.E. Light, and P.A. Smith. 2003. Experiments to test the role of phosphatidylinositol 4,5-bisphosphate in neurotransmitter-induced M-channel closure in bullfrog sympathetic neurons. J. Neurosci. 23:4931-4941.
20. Fukata, M., Y. Fukata, H. Adesnik, R.A. Nicoll, and D.S. Bredt. 2004. Identification of PSD-95 palmitoylating enzymes. Neuron. 44:987-996. doi:10.1016/j.neuron.2004.12.005
21. Gamper, N., V. Reznikov, Y. Yamada, J. Yang, and M.S. Shapiro. 2004. Phosphatidylinositol [correction] 4,5-bisphosphate signals underlie receptor-specific Gq/11-mediated modulation of N-type Ca2+ channels. J. Neurosci. 24:10980-10992. doi:10.1523/JNEUROSCI.3869-04.2004 (Pubitemid 39602409)
22. Guo, J.S., and S.R. Ikeda. 2004. Endocannabinoids modulate N-type calcium channels and G-protein-coupled inwardly rectifying potassium channels via CB1 cannabinoid receptors heterologously expressed in mammalian neurons. Mol. Pharmacol. 65:665-674. doi:10.1124/mol.65.3.665
23. Hamilton, J.A., W. Guo, and F. Kamp. 2002. Mechanism of cellular uptake of long-chain fatty acids: do we need cellular proteins? Mol. Cell. Biochem. 239:17-23. doi:10.1023/A:1020542220599
24. Hidalgo, P., G. Gonzalez-Gutierrez, J. Garcia-Olivares, and A. Neely. 2006. The alpha1-beta-subunit interaction that modulates calcium channel activity is reversible and requires a competent alpha-interaction domain. J. Biol. Chem. 281:24104-24110. doi:10.1074/jbc.M605930200
25. Hildebrand, M.E., L.S. David, J. Hamid, K. Mulatz, E. Garcia, G.W. Zamponi, and T.P. Snutch. 2007. Selective inhibition of Cav3.3 T-type calcium channels by Galphaq/11-coupled muscarinic acetylcholine receptors. J. Biol. Chem. 282:21043-21055. doi:10.1074/jbc.M611809200
26. Hurley, J.H., A.L. Cahill, K.P. Currie, and A.P. Fox. 2000. The role of dynamic palmitoylation in Ca2+ channel inactivation. Proc. Natl. Acad. Sci. USA. 97:9293-9298. doi:10.1073/pnas.160589697
27. Kammermeier, P.J., V. Ruiz-Velasco, and S.R. Ikeda. 2000. A voltage-independent calcium current inhibitory pathway activated by muscarinic agonists in rat sympathetic neurons requires both Galpha q/11 and Gbeta gamma. J. Neurosci. 20:5623-5629.
28. Keyser, D.O., and B.E. Alger. 1990. Arachidonic acid modulates hippocampal calcium current via protein kinase C and oxygen radicals. Neuron. 5:545-553. doi:10.1016/0896-6273(90)90092-T
29. Lie, A.A., I. Blümcke, S.G. Volsen, O.D. Wiestler, C.E. Elger, and H. Beck. 1999. Distribution of voltage-dependent calcium channel beta subunits in the hippocampus of patients with temporal lobe epilepsy. Neuroscience. 93:449-456. doi:10.1016/S0306-4522(99)00162-1
30. Lin, Z., C. Harris, and D. Lipscombe. 1996. The molecular identity of Ca channel alpha 1-subunits expressed in rat sympathetic neurons. J. Mol. Neurosci. 7:257-267. doi:10.1007/BF02737063 (Pubitemid 126718465)
31. Lin, Z., S. Haus, J. Edgerton, and D. Lipscombe. 1997. Identification of functionally distinct isoforms of the N-type Ca2+ channel in rat sympathetic ganglia and brain. Neuron. 18:153-166. doi:10.1016/S0896-6273(01)80054-4 (Pubitemid 27053838)
32. Lin, Y.S., S.I. McDonough, and D. Lipscombe. 2004. Alternative splicing in the voltage-sensing region of N-type CaV2.2 channels modulates channel kinetics. J. Neurophysiol. 92:2820-2830. doi:10.1152/jn.00048.2004
33. Liu, L., and A.R. Rittenhouse. 2000. Effects of arachidonic acid on unitary calcium currents in rat sympathetic neurons. J. Physiol. 525:391-404. doi:10.1111/j.1469-7793.2000.00391.x (Pubitemid 30398369)
34. Liu, L., and A.R. Rittenhouse. 2003a. Arachidonic acid mediates muscarinic inhibition and enhancement of N-type Ca2+ current in sympathetic neurons. Proc. Natl. Acad. Sci. USA. 100:295-300. doi:10.1073/pnas.0136826100
35. Liu, L., and A.R. Rittenhouse. 2003b. Pharmacological discrimination between muscarinic receptor signal transduction cascades with bethanechol chloride. Br. J. Pharmacol. 138:1259-1270. doi:10.1038/sj.bjp.0705157 (Pubitemid 36543123)
36. Liu, L.C., C.F. Barrett, and A.R. Rittenhouse. 2001. Arachidonic acid both inhibits and enhances whole cell calcium currents in rat sympathetic neurons. Am. J. Physiol. Cell Physiol. 280:C1293-C1305. (Pubitemid 32433763)
37. Liu, L.P., P.K. Gonzalez, C.F. Barrett, and A.R. Rittenhouse. 2003. The calcium channel ligand FPL 64176 enhances L-type but inhibits N-type neuronal calcium currents. Neuropharmacology. 45:281-292. doi:10.1016/S0028-3908(03) 00153-9
38. Liu, L., M.L. Roberts, and A.R. Rittenhouse. 2004. Phospholipid metabolism is required for M1 muscarinic inhibition of N-type calcium current in sympathetic neurons. Eur. Biophys. J. 33:255-264. doi:10.1007/s00249-003-0387-7 (Pubitemid 39118303)
39. Liu, L., R. Zhao, Y. Bai, L.F. Stanish, J.E. Evans, M.J. Sanderson, J.V. Bonventre, and A.R. Rittenhouse. 2006. M1 muscarinic receptors inhibit L-type Ca2+ current and M-current by divergent signal transduction cascades. J. Neurosci. 26:11588-11598. doi:10.1523/JNEUROSCI.2102-06.2006 (Pubitemid 44772130)
40. Liu, L.J., J.F. Heneghan, T. Mitra-Ganguli, M.L. Roberts-Crowley, and A.R. Rittenhouse. 2007. Role of PIP2 in regulating versus modulating Ca2+ channel activity. J. Physiol. 583:1165-1166; author reply 1167. doi:10.1113/jphysiol.2007.141424
41. Liu, L.J., J.F. Heneghan, G.J. Michael, L.F. Stanish, M. Egertová, and A.R. Rittenhouse. 2008. L- and N-current but not M-current inhibition by M1 muscarinic receptors requires DAG lipase activity. J. Cell. Physiol. 216:91-100. doi:10.1002/jcp.21378
42. Liu, S.J. 2007. Inhibition of L-type Ca2+ channel current and negative inotropy induced by arachidonic acid in adult rat ventricular myocytes. Am. J. Physiol. Cell Physiol. 293:C1594-C1604. doi:10.1152/ajpcell.00284.2007
43. Macdonald, S.G., J.J. Dumas, and N.D. Boyd. 1996. Chemical cross-linking of the substance P (NK-1) receptor to the alpha subunits of the G proteins Gq and G11. Biochemistry. 35:2909-2916. doi:10.1021/bi952351+ (Pubitemid 26086800)
44. Mathie, A., L. Bernheim, and B. Hille. 1992. Inhibition of N- and L-type calcium channels by muscarinic receptor activation in rat sympathetic neurons. Neuron. 8:907-914. doi:10.1016/0896-6273(92)90205-R
45. Melliti, K., U. Meza, and B.A. Adams. 2001. RGS2 blocks slow muscarinic inhibition of N-type Ca(2+) channels reconstituted in a human cell line. J. Physiol. 532:337-347. doi:10.1111/j.1469-7793.2001.0337f.x (Pubitemid 32390392)
46. Meza, U., A. Thapliyal, R.A. Bannister, and B.A. Adams. 2007. Neurokinin 1 receptors trigger overlapping stimulation and inhibition of CaV2.3 (R-type) calcium channels. Mol. Pharmacol. 71:284-293. doi:10.1124/mol.106.028530 (Pubitemid 46020998)
47. Michailidis, I.E., Y. Zhang, and J. Yang. 2007. The lipid connection-regulation of voltage-gated Ca(2+) channels by phosphoinositides. Pflugers Arch. 455:147-155. doi:10.1007/s00424-007-0272-9
48. 2+ current by tachykinin receptor activation. J. Gen. Physiol. 134:385-396.
49. Olcese, R., N. Qin, T. Schneider, A. Neely, X. Wei, E. Stefani, and L. Birnbaumer. 1994. The amino terminus of a calcium channel beta subunit sets rates of channel inactivation independently of the subunit's effect on activation. Neuron. 13:1433-1438. doi:10.1016/0896-6273(94)90428-6
50. Oliver, D.C., C.C. Lien, M. Soom, T. Baukrowitz, P. Jonas, and B. Fakler. 2004. Functional conversion between A-type and delayed rectifier K+ channels by membrane lipids. Science. 304:265-270. doi:10.1126/science.1094113
51. Peralta, E.G., A. Ashkenazi, J.W. Winslow, J. Ramachandran, and D.J. Capon. 1988. Differential regulation of PI hydrolysis and adenylyl cyclase by muscarinic receptor subtypes. Nature. 334:434-437. doi:10.1038/334434a0
52. Perez, J.F., and M.J. Sanderson. 2005. The frequency of calcium oscillations induced by 5-HT, ACH, and KCl determine the contraction of smooth muscle cells of intrapulmonary bronchioles. J. Gen. Physiol. 125:535-553. doi:10.1085/jgp.200409216
53. Petit-Jacques, J.H., and H.C. Hartzell. 1996. Effect of arachidonic acid on the L-type calcium current in frog cardiac myocytes. J. Physiol. 493:67-81. (Pubitemid 26152611)
54. Piomelli, D. 1993. Arachidonic acid in cell signaling. Curr. Opin. Cell Biol. 5:274-280. doi:10.1016/0955-0674(93)90116-8
55. Plummer, M.R., D.E. Logothetis, and P. Hess. 1989. Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons. Neuron. 2:1453-1463. doi:10.1016/0896-6273(89)90191-8
56. Pragnell, M., M. De Waard, Y. Mori, T. Tanabe, T.P. Snutch, and K.P. Campbell. 1994. Calcium channel beta-subunit binds to a conserved motif in the I-II cytoplasmic linker of the alpha 1-subunit. Nature. 368:67-70. doi:10.1038/368067a0 (Pubitemid 2041155)
57. Resh, M.D. 2006. Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci. STKE. doi:10.1126/stke.3592006re14
58. Restituito, S., T. Cens, M. Rousset, and P. Charnet. 2001. Ca(2+) channel inactivation heterogeneity reveals physiological unbinding of auxiliary beta subunits. Biophys. J. 81:89-96. doi:10.1016/S0006-3495(01)75682-2 (Pubitemid 32605954)
59. Rittenhouse, A.R., and R.E. Zigmond. 1999. Role of N- and L-type calcium channels in depolarization-induced activation of tyrosine hydroxylase and release of norepinephrine by sympathetic cell bodies and nerve terminals. J. Neurobiol. 40:137-148. doi:10.1002/(SICI)1097-4695(199908)40:2〈137::AID- NEU1〉3.0.CO;2-A
60. Roberts-Crowley, M.L., and A.R. Rittenhouse. 2009. Arachidonic acid inhibition of L-type calcium (CaV1.3b) channels varies with accessory CaVβ subunits. J. Gen. Physiol. 133:387-403. doi:10.1085/jgp.200810047
61. Roberts-Crowley, M.L., T. Mitra-Ganguli, L. Liu, and A.R. Rittenhouse. 2009. Regulation of voltage-gated Ca2+ channels by lipids. Cell Calcium. 45:589-601. doi:10.1016/j.ceca.2009.03.015
62. Sanderson, M.J., and I. Parker. 2003. Video-rate confocal microscopy. Methods Enzymol. 360:447-481. doi:10.1016/S0076-6879(03)60123-0
63. Scott, V.E., M. De Waard, H. Liu, C.A. Gurnett, D.P. Venzke, V.A. Lennon, and K.P. Campbell. 1996. Beta subunit heterogeneity in N-type Ca2+ channels. J. Biol. Chem. 271:3207-3212. doi:10.1074/jbc.271.6.3207
64. Shapiro, M.S., and B. Hille. 1993. Substance P and somatostatin inhibit calcium channels in rat sympathetic neurons via different G protein pathways. Neuron. 10:11-20. doi:10.1016/0896-6273(93)90237-L
65. Shapiro, M.S., L.P. Wollmuth, and B. Hille. 1994. Modulation of Ca2+ channels by PTX-sensitive G-proteins is blocked by N-ethylmaleimide in rat sympathetic neurons. J. Neurosci. 14:7109-7116. (Pubitemid 24336381)
66. Shimada, T.A., and A.P. Somlyo. 1992. Modulation of voltage-dependent Ca channel current by arachidonic acid and other long-chain fatty acids in rabbit intestinal smooth muscle. J. Gen. Physiol. 100:27-44. doi:10.1085/jgp.100.1.27
67. Spector, A.A. 1975. Fatty acid binding to plasma albumin. J. Lipid Res. 16:165-179.
68. Suh, B.C., and B. Hille. 2002. Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron. 35:507-520. doi:10.1016/S0896-6273(02)00790-0
69. Suh, B.C., and B. Hille. 2005. Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr. Opin. Neurobiol. 15:370-378. doi:10.1016/j.conb.2005.05.005 (Pubitemid 40806451)
70. Suh, B.C., and B. Hille. 2007. Regulation of KCNQ channels by manipulation of phosphoinositides. J. Physiol. 582:911-916. doi:10.1113/ jphysiol.2007.132647
71. Suh, B.C., T. Inoue, T. Meyer, and B. Hille. 2006. Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science. 314:1454-1457. doi:10.1126/science.1131163
72. Tai, C., J.B. Kuzmiski, and B.A. MacVicar. 2006. Muscarinic enhancement of R-type calcium currents in hippocampal CA1 pyramidal neurons. J. Neurosci. 26:6249-6258. doi:10.1523/JNEUROSCI.1009-06.2006
73. Talavera, K., M. Staes, A. Janssens, G. Droogmans, and B. Nilius. 2004. Mechanism of arachidonic acid modulation of the T-type Ca2+ channel α1G. J. Gen. Physiol. 124:225-238. doi:10.1085/jgp.200409050
74. Tanaka, O., H. Sakagami, and H. Kondo. 1995. Localization of mRNAs of voltage-dependent Ca(2+)-channels: four subtypes of alpha 1- and beta-subunits in developing and mature rat brain. Brain Res. Mol. Brain Res. 30:1-16. doi:10.1016/0169-328X(94)00265-G
75. Tencé, M., J. Cordier, J. Premont, and J. Glowinski. 1994. Muscarinic cholinergic agonists stimulate arachidonic acid release from mouse striatal neurons in primary culture. J. Pharmacol. Exp. Ther. 269:646-653. (Pubitemid 24157333)
76. Vellani, V.A., A.M. Reynolds, and P.A. McNaughton. 2000. Modulation of the synaptic Ca2+ current in salamander photoreceptors by polyunsaturated fatty acids and retinoids. J. Physiol. 529:333-344. doi:10.1111/j.1469-7793.2000. 00333.x
77. West, A.E., W.G. Chen, M.B. Dalva, R.E. Dolmetsch, J.M. Kornhauser, A.J. Shaywitz, M.A. Takasu, X. Tao, and M.E. Greenberg. 2001. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. USA. 98:11024-11031. doi:10.1073/pnas.191352298
78. Wisgirda, M.E., and S.E. Dryer. 1994. Functional dependence of Ca(2+)-activated K+ current on L- and N-type Ca2+ channels: differences between chicken sympathetic and parasympathetic neurons suggest different regulatory mechanisms. Proc. Natl. Acad. Sci. USA. 91:2858-2862. doi:10.1073/pnas.91.7.2858
79. Witcher, D.R., M. De Waard, J. Sakamoto, C. Franzini-Armstrong, M. Pragnell, S.D. Kahl, and K.P. Campbell. 1993. Subunit identification and reconstitution of the N-type Ca2+ channel complex purified from brain. Science. 261:486-489. doi:10.1126/science.8392754 (Pubitemid 23276561)
80. Wu, L.C., C.S. Bauer, X.G. Zhen, C. Xie, and J. Yang. 2002. Dual regulation of voltage-gated calcium channels by PtdIns(4,5)P2. Nature. 419:947-952. doi:10.1038/nature01118 (Pubitemid 35339631)
81. Xue, L.D., D.R. Gollapalli, P. Maiti, W.J. Jahng, and R.R. Rando. 2004. A palmitoylation switch mechanism in the regulation of the visual cycle. Cell. 117:761-771. doi:10.1016/j.cell.2004.05.016
82. Yasuda, T., L. Chen, W. Barr, J.E. McRory, R.J. Lewis, D.J. Adams, and G.W. Zamponi. 2004. Auxiliary subunit regulation of high-voltage activated calcium channels expressed in mammalian cells. Eur. J. Neurosci. 20:1-13. doi:10.1111/j.1460-9568.2004.03434.x
83. Zhang, Y.L., L.L. Cribbs, and J. Satin. 2000. Arachidonic acid modulation of alpha1H, a cloned human T-type calcium channel. Am. J. Physiol. Heart Circ. Physiol. 278:H184-H193.
84. Zhao, R., L. Liu, and A.R. Rittenhouse. 2007. Ca2+ influx through both L- and N-type Ca2+ channels increases c-fos expression by electrical stimulation of sympathetic neurons. Eur. J. Neurosci. 25:1127-1135. doi:10.1111/j.1460-9568. 2007.05359.x