Arachidonic acid inhibition of L-type calcium (Ca V 1.3b) channels varies with accessory Ca Vβ subunits

Journal of General Physiology

Volumn 133, Issue 4, 2009, Pages 387-403

  Mandy, L Roberts Crowley ^a   Rittenhouse, Ann R ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; BARIUM ION; CALCIUM CHANNEL L TYPE; CALCIUM ION; MUSCARINIC M1 RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL; ALPHA1D (CAV1.3) L-TYPE CALCIUM CHANNEL, HUMAN; CALCIUM CHANNEL BLOCKING AGENT; MUSCARINIC RECEPTOR; PROTEIN SUBUNIT;

ALPHA CHAIN; ARTICLE; BETA CHAIN; CALCIUM CHANNEL PORE FORMING BETA SUBUNIT; CHANNEL GATING; CONTROLLED STUDY; HUMAN; HUMAN CELL; KINETICS; MEMBRANE CURRENT; MEMBRANE POTENTIAL; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMISTRY; COMPARATIVE STUDY; METABOLISM; PHYSIOLOGY; PROTEIN SUBUNIT;

ARACHIDONIC ACID; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CELL LINE; HUMANS; PROTEIN SUBUNITS; RECEPTORS, MUSCARINIC;

EID: 64549155659     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200810047     Document Type: Article

References (81)

1. Arias, J.M., J. Murbartian, I. Vitko, J.H. Lee, and E. Perez-Reyes. 2005. Transfer of beta subunit regulation from high to low voltagegated Ca2+ channels. FEBS Lett. 579: 3907 - 3912.
2. Axelrod, J., R.M. Burch, and C.L. Jelsema. 1988. Receptor-mediated activation of phospholipase A2 via GTP-binding proteins: arachidonic acid and its metabolites as second messengers. Trends Neurosci. 11: 117 - 123.
3. Banihashemi, B., and P.R. Albert. 2002. Dopamine-D2S receptor inhibition of calcium influx, adenylyl cyclase, and mitogen-activated protein kinase in pituitary cells: distinct Galpha and Gbetagamma requirements. Mol. Endocrinol. 16: 2393 - 2404.
4. Bannister, R.A., K. Melliti, and B.A. Adams. 2002. Reconstituted slow muscarinic inhibition of neuronal (Ca(v)1.2c) L-type Ca2+ channels. Biophys. J. 83: 3256 - 3267.
5. 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.
6. Bean, B.P. 1989. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature. 340: 153 - 156.
7. Bell, D.C., A.J. Butcher, N.S. Berrow, K.M. Page, P.F. Brust, A. Nesterova, K.A. Stauderman, G.R. Seabrook, B. Nurnberg, and A.C. Dolphin. 2001. Biophysical properties, pharmacology, and modulation of human, neuronal L-type (alpha(1D), Ca(V)1.3) voltage-dependent calcium currents. J. Neurophysiol. 85: 816 - 827.
8. 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.
9. Brandt, A., J. Striessnig, and T. Moser. 2003. CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. J. Neurosci. 23: 10832 - 10840.
10. Brandt, A., D. Khimich, and T. Moser. 2005. Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J. Neurosci. 25: 11577 - 11585.
11. Bringmann, A., S. Schopf, F. Faude, and A. Reichenbach. 2001. Arachidonic acid-induced inhibition of Ca2+ channel currents in retinal glial (Muller) cells. Graefes Arch. Clin. Exp. Ophthalmol. 239: 859 - 864.
12. Cardenas, C.G., L.P. Del Mar, and R.S. Scroggs. 1997. Two parallel signaling pathways couple 5HT1A receptors to N- and L-type calcium channels in C-like rat dorsal root ganglion cells. J. Neurophysiol. 77: 3284 - 3296.
13. Catterall, W.A. 2000. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol. 16: 521 - 555.
14. Catterall, W.A., E. Perez-Reyes, T.P. Snutch, and J. Striessnig. 2005. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev. 57: 411 - 425.
15. Chavis, P., H. Shinozaki, J. Bockaert, and L. Fagni. 1994. The metabotropic glutamate receptor types 2/3 inhibit L-type calcium channels via a pertussis toxin-sensitive G-protein in cultured cerebellar granule cells. J. Neurosci. 14: 7067 - 7076.
16. 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.
17. Clarke, A.L., S. Petrou, J.V. Walsh Jr., and J.J. Singer. 2002. Modulation of BK(Ca) channel activity by fatty acids: structural requirements and mechanism of action. Am. J. Physiol. Cell Physiol. 283: C1441 - C1453.
18. Colecraft, H.M., B. Alseikhan, S.X. Takahashi, D. Chaudhuri, S. Mittman, V. Yegnasubramanian, R.S. Alvania, D.C. Johns, E. Marban, and D.T. Yue. 2002. Novel functional properties of Ca(2+) channel beta subunits revealed by their expression in adult rat heart cells. J. Physiol. 541: 435 - 452.
19. Day, M., P.A. Olson, J. Platzer, J. Striessnig, and D.J. Surmeier. 2002. Stimulation of 5-HT(2) receptors in prefrontal pyramidal neurons inhibits Ca(v)1.2 L type Ca(2+) currents via a PLCbeta/IP3/calcineurin signaling cascade. J. Neurophysiol. 87: 2490 - 2504.
20. Denson, D.D., X. Wang, R.T. Worrell, and D.C. Eaton. 2000. Effects of fatty acids on BK channels in GH(3) cells. Am. J. Physiol. Cell Physiol. 279: C1211 - C1219.
21. Frazier, C.J., J.R. Serrano, E.G. George, X. Yu, A. Viswanathan, E. Perez-Reyes, and S.W. Jones. 2001. Gating kinetics of the α 1I Ttype calcium channel. J. Gen. Physiol. 118: 457 - 470.
22. Gamper, N., V. Reznikov, Y. Yamada, J. Yang, and M.S. Shapiro. 2004. Phosphatidylinositol 4,5-bisphosphate signals underlie receptorspecific Gq/11-mediated modulation of N-type Ca2+ channels. J. Neurosci. 24: 10980 - 10992.
23. Gao, L., L.A. Blair, G.D. Salinas, L.A. Needleman, and J. Marshall. 2006. Insulin-like growth factor-1 modulation of CaV1.3 calcium channels depends on Ca2+ release from IP3-sensitive stores and calcium/calmodulin kinase II phosphorylation of the alpha1 subunit EF hand. J. Neurosci. 26: 6259 - 6268.
24. Grunnet, M., and W.A. Kaufmann. 2004. Coassembly of big conductance Ca2+-activated K+ channels and L-type voltage-gated Ca2+ channels in rat brain. J. Biol. Chem. 279: 36445 - 36453.
25. Hell, J.W., R.E. Westenbroek, C. Warner, M.K. Ahlijanian, W. Prystay, M.M. Gilbert, T.P. Snutch, and W.A. Catterall. 1993. Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits. J. Cell Biol. 123: 949 - 962.
26. Hering, S. 2002. beta-Subunits: fine tuning of Ca(2+) channel block. Trends Pharmacol. Sci. 23: 509 - 513.
27. Hering, S., S. Berjukow, S. Sokolov, R. Marksteiner, R.G. Weiss, R. Kraus, and E.N. Timin. 2000. Molecular determinants of inactivation in voltage-gated Ca2+ channels. J. Physiol. 528: 237 - 249.
28. Jarrahian, A., and C.J. Hillard. 1997. Arachidonylethanolamide (anandamide) binds with low affinity to dihydropyridine binding sites in brain membranes. Prostaglandins Leukot. Essent. Fatty Acids. 57: 551 - 554.
29. Jones, S.W., and K.S. Elmslie. 1997. Transmitter modulation of neuronal calcium channels. J. Membr. Biol. 155: 1 - 10.
30. Kobrinsky, E., K.J. Kepplinger, A. Yu, J.B. Harry, H. Kahr, C. Romanin, D.R. Abernethy, and N.M. Soldatov. 2004. Voltage-gated rearrangements associated with differential beta-subunit modulation of the L-type Ca(2+) channel inactivation. Biophys. J. 87: 844 - 857.
31. Koschak, A., D. Reimer, I. Huber, M. Grabner, H. Glossmann, J. Engel, and J. Striessnig. 2001. alpha 1D (Cav1.3) subunits can form l-type Ca2+ channels activating at negative voltages. J. Biol. Chem. 276: 22100 - 22106.
32. Lazarewicz, J.W., E. Salinska, and J.T. Wroblewski. 1992. NMDA receptor- mediated arachidonic acid release in neurons: role in signal transduction and pathological aspects. Adv. Exp. Med. Biol. 318: 73 - 89.
33. 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.
34. Lipton, P. 1999. Ischemic cell death in brain neurons. Physiol. Rev. 79: 1431 - 1568.
35. Liu, G., N. Dilmac, N. Hilliard, and G.H. Hockerman. 2003. Ca v 1.3 is preferentially coupled to glucose-stimulated insulin secretion in the pancreatic beta-cell line INS-1. J. Pharmacol. Exp. Ther. 305: 271 - 278.
36. Liu, L., and A.R. Rittenhouse. 2000. Effects of arachidonic acid on unitary calcium currents in rat sympathetic neurons. J. Physiol. 525: 391 - 404.
37. Liu, L., 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.
38. 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.
39. 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.
40. Lopez, G.A., Y.N. Jan, and L.Y. Jan. 1994. Evidence that the S6 segment of the Shaker voltage-gated K+ channel comprises part of the pore. Nature. 367: 179 - 182.
41. Mangoni, M.E., B. Couette, E. Bourinet, J. Platzer, D. Reimer, J. Striessnig, and J. Nargeot. 2003. Functional role of L-type Cav1.3 Ca2+ channels in cardiac pacemaker activity. Proc. Natl. Acad. Sci. USA. 100: 5543 - 5548.
42. Marks, T.N., and S.W. Jones. 1992. Calcium currents in the A7r5 smooth muscle-derived cell line. An allosteric model for calcium channel activation and dihydropyridine agonist action. J. Gen. Physiol. 99: 367 - 390.
43. McEnery, M.W., C.L. Vance, C.M. Begg, W.L. Lee, Y. Choi, and S.J. Dubel. 1998. Differential expression and association of calcium channel subunits in development and disease. J. Bioenerg. Biomembr. 30: 409 - 418.
44. Meves, H. 2008. Arachidonic acid and ion channels: an update. Br. J. Pharmacol. 155: 4 - 16.
45. Michailidis, I.E., Y. Zhang, and J. Yang. 2007. The lipid connectionregulation of voltage-gated Ca(2+) channels by phosphoinositides. Pflugers Arch. 455: 147 - 155.
46. Ogielska, E.M., W.N. Zagotta, T. Hoshi, S.H. Heinemann, J. Haab, and R.W. Aldrich. 1995. Cooperative subunit interactions in C-type inactivation of K channels. Biophys. J. 69: 2449 - 2457.
47. Oliver, D., 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.
48. Olson, P.A., T. Tkatch, S. Hernandez-Lopez, S. Ulrich, E. Ilijic, E. Mugnaini, H. Zhang, I. Bezprozvanny, and D.J. Surmeier. 2005. G-protein-coupled receptor modulation of striatal CaV1.3 Ltype Ca2+ channels is dependent on a Shank-binding domain. J. Neurosci. 25: 1050 - 1062.
49. Oz, M., A. Alptekin, Y. Tchugunova, and M. Dinc. 2005. Effects of saturated long-chain N-acylethanolamines on voltage-dependent Ca2+ fluxes in rabbit T-tubule membranes. Arch. Biochem. Biophys. 434: 344 - 351.
50. Patil, P.G., D.L. Brody, and D.T. Yue. 1998. Preferential closed-state inactivation of neuronal calcium channels. Neuron. 20: 1027 - 1038.
51. Pemberton, K.E., and S.V. Jones. 1997. Inhibition of the L-type calcium channel by the five muscarinic receptors (m1-m5) expressed in NIH 3T3 cells. Pflugers Arch. 433: 505 - 514.
52. 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.
53. Petit-Jacques, J., and H.C. Hartzell. 1996. Effect of arachidonic acid on the L-type calcium current in frog cardiac myocytes. J. Physiol. 493: 67 - 81.
54. Pike, L.J. 2003. Lipid rafts: bringing order to chaos. J. Lipid Res. 44: 655 - 667.
55. Platzer, J., J. Engel, A. Schrott-Fischer, K. Stephan, S. Bova, H. Chen, H. Zheng, and J. Striessnig. 2000. Congenital deafness and sinoatrial node dysfunction in mice lacking class D L-type Ca2+ channels. Cell. 102: 89 - 97.
56. Qin, N., D. Platano, R. Olcese, J.L. Costantin, E. Stefani, and L. Birnbaumer. 1998. Unique regulatory properties of the type 2a Ca2+ channel beta subunit caused by palmitoylation. Proc. Natl. Acad. Sci. USA. 95: 4690 - 4695.
57. Restituito, S., T. Cens, C. Barrere, S. Geib, S. Galas, M. De Waard, and P. Charnet. 2000. The [beta]2a subunit is a molecular groom for the Ca2+ channel inactivation gate. J. Neurosci. 20: 9046 - 9052.
58. Safa, P., J. Boulter, and T.G. Hales. 2001. Functional properties of Cav1.3 (alpha1D) L-type Ca2+ channel splice variants expressed by rat brain and neuroendocrine GH3 cells. J. Biol. Chem. 276: 38727 - 38737.
59. Scholze, A., T.D. Plant, A.C. Dolphin, and B. Nurnberg. 2001. Functional expression and characterization of a voltage-gated CaV1.3 (alpha1D) calcium channel subunit from an insulinsecreting cell line. Mol. Endocrinol. 15: 1211 - 1221.
60. Serrano, J.R., E. Perez-Reyes, and S.W. Jones. 1999. State-dependent inactivation of the α 1G T-type calcium channel. J. Gen. Physiol. 114: 185 - 201.
61. Shimada, T., 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.
62. Shimasue, K., T. Urushidani, M. Hagiwara, and T. Nagao. 1996. Effects of anandamide and arachidonic acid on specific binding of (+) -PN200-110, diltiazem and (-) -desmethoxyverapamil to Ltype Ca2+ channel. Eur. J. Pharmacol. 296: 347 - 350.
63. Singer, D., M. Biel, I. Lotan, V. Flockerzi, F. Hofmann, and N. Dascal. 1991. The roles of the subunits in the function of the calcium channel. Science. 253: 1553 - 1557.
64. Sinnegger, M.J., Z. Wang, M. Grabner, S. Hering, J. Striessnig, H. Glossmann, and J. Mitterdorfer. 1997. Nine L-type amino acid residues confer full 1,4-dihydropyridine sensitivity to the neuronal calcium channel alpha1A subunit. Role of L-type Met1188. J. Biol. Chem. 272: 27686 - 27693.
65. Stotz, S.C., S.E. Jarvis, and G.W. Zamponi. 2004. Functional roles of cytoplasmic loops and pore lining transmembrane helices in the voltage-dependent inactivation of HVA calcium channels. J. Physiol. 554: 263 - 273.
66. Sun, X., D. Zhou, P. Zhang, E.G. Moczydlowski, and G.G. Haddad. 2007. Beta-subunit-dependent modulation of hSlo BK current by arachidonic acid. J. Neurophysiol. 97: 62 - 69.
67. Takahashi, S.X., J. Miriyala, and H.M. Colecraft. 2004. Membraneassociated guanylate kinase-like properties of beta-subunits required for modulation of voltage-dependent Ca2+ channels. Proc. Natl. Acad. Sci. USA. 101: 7193 - 7198.
68. 2+ channel α 1G. J. Gen. Physiol. 124: 225 - 238.
69. Tang, X., E.M. Edwards, B.B. Holmes, J.R. Falck, and W.B. Campbell. 2006. Role of phospholipase C and diacylglyceride lipase pathway in arachidonic acid release and acetylcholine-induced vascular relaxation in rabbit aorta. Am. J. Physiol. Heart Circ. Physiol. 290: H37 - H45.
70. Tucker, S.J., and T. Baukrowitz. 2008. How highly charged anionic lipids bind and regulate ion channels. J. Gen. Physiol. 131: 431 - 438.
71. Vellani, V., 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.
72. Vilin, Y.Y., N. Makita, A.L. George Jr., and P.C. Ruben. 1999. Structural determinants of slow inactivation in human cardiac and skeletal muscle sodium channels. Biophys. J. 77: 1384 - 1393.
73. Wappl, E., J. Mitterdorfer, H. Glossmann, and J. Striessnig. 2001. Mechanism of dihydropyridine interaction with critical binding residues of L-type Ca2+ channel alpha 1 subunits. J. Biol. Chem. 276: 12730 - 12735.
74. Wikstrom, M.A., S. Grillner, and A. El Manira. 1999. Inhibition of N- and L-type Ca2+ currents by dopamine in lamprey spinal motoneurons. Neuroreport. 10: 3179 - 3183.
75. Wu, L., 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.
76. Xiao, Y.F., A.M. Gomez, J.P. Morgan, W.J. Lederer, and A. Leaf. 1997. Suppression of voltage-gated L-type Ca2+ currents by polyunsaturated fatty acids in adult and neonatal rat ventricular myocytes. Proc. Natl. Acad. Sci. USA. 94: 4182 - 4187.
77. Xu, W., and D. Lipscombe. 2001. Neuronal Ca(V)1.3alpha(1) Ltype channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J. Neurosci. 21: 5944 - 5951.
78. Yamaguchi, S., B.S. Zhorov, K. Yoshioka, T. Nagao, H. Ichijo, and S. Adachi-Akahane. 2003. Key roles of Phe1112 and Ser1115 in the pore-forming IIIS5-S6 linker of L-type Ca2+ channel alpha1C subunit (CaV 1.2) in binding of dihydropyridines and action of Ca2+ channel agonists. Mol. Pharmacol. 64: 235 - 248.
79. Yehuda, S., S. Rabinovitz, R.L. Carasso, and D.I. Mostofsky. 1998. Fatty acids and brain peptides. Peptides. 19: 407 - 419.
80. Zhang, H., Y. Fu, C. Altier, J. Platzer, D.J. Surmeier, and I. Bezprozvanny. 2006. Ca1.2 and CaV1.3 neuronal L-type calcium channels: differential targeting and signaling to pCREB. Eur. J. Neurosci. 23: 2297 - 2310.
81. Zhang, Y., 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.