CaMKII locally encodes L-type channel activity to signal to nuclear CREB in excitation - transcription coupling

Journal of Cell Biology

Volumn 183, Issue 5, 2008, Pages 849-863

  Wheeler, Damian G ^a   Barrett, Curtis F ^a,c   Groth, Rachel D ^a   Safa, Parsa ^a,b   Tsien, Richard W ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOLECULAR DEVICES CORPORATION   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BETA ACTIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL L TYPE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CAMK2A PROTEIN, RAT; CAMK2B PROTEIN, HUMAN; CREB1 PROTEIN, RAT; PROTEIN KINASE INHIBITOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL COMMUNICATION; CELL NUCLEUS; CHANNEL GATING; CONTROLLED STUDY; EXCITATION TRANSCRIPTION COUPLING; MEMBRANE DEPOLARIZATION; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; STIMULUS RESPONSE; ANIMAL; CELL CULTURE; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; METABOLISM; NERVE CELL; NEWBORN; PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SUPERIOR CERVICAL GANGLION; TIME;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL MEMBRANE; CELL NUCLEUS; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; MEMBRANE POTENTIALS; NEURONS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUPERIOR CERVICAL GANGLION; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 58149302821     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200805048     Document Type: Article

References (107)

1. Adams, P.R., and D.A. Brown. 1973. Action of -aminobutyric acid (GABA) on rat sympathetic ganglion cells. Br. J. Pharmacol. 47: 639P-640P.
2. Almers, W. 1978. Gating currents and charge movements in excitable membranes. Rev. Physiol. Biochem. Pharmacol. 82: 96-190.
3. Altamirano, J., and D.M. Bers. 2007. Voltage dependence of cardiac excitation-contraction coupling: unitary Ca2+ current amplitude and open channel probability. Circ. Res. 101: 590-597.
4. Armstrong, C.M., F.M. Bezanilla, and P. Horowicz. 1972. Twitches in the presence of ethylene glycol bis(-aminoethyl ether)-N, N' -tetracetic acid. Biochim. Biophys. Acta. 267: 605-608.
5. Artalejo, C.R., S. Rossie, R.L. Perlman, and A.P. Fox. 1992. Voltage-dependent phosphorylation may recruit Ca2+ current facilitation in chromaffi n cells. Nature. 358: 63-66.
6. Augustine, G.J. 2001. How does calcium trigger neurotransmitter release? Curr. Opin. Neurobiol. 11: 320-326.
7. Augustine, G.J., M.P. Charlton, and S.J. Smith. 1985. Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J. Physiol. 367: 163-181.
8. Augustine, G.J., F. Santamaria, and K. Tanaka. 2003. Local calcium signaling in neurons. Neuron. 40: 331-346.
9. Beam, K.G., and C. Franzini-Armstrong. 1997. Functional and structural approaches to the study of excitation-contraction coupling. Methods Cell Biol. 52: 283-306.
10. Berridge, M.J. 1998. Neuronal calcium signaling. Neuron. 21: 13-26.
11. Bers, D.M. 2002. Cardiac excitation-contraction coupling. Nature. 415: 198-205.
12. Bers, D.M., and T. Guo. 2005. Calcium signaling in cardiac ventricular myocytes. Ann. NY Acad. Sci. 1047: 86-98.
13. Bito, H., K. Deisseroth, and R.W. Tsien. 1996. CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell. 87: 1203-1214.
14. Bollmann, J.H., B. Sakmann, and J.G. Borst. 2000. Calcium sensitivity of glutamate release in a calyx-type terminal. Science. 289: 953-957.
15. 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.
16. Burgoyne, R.D. 2007. Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat. Rev. Neurosci. 8: 182-193.
17. Cannell, M.B., H. Cheng, and W.J. Lederer. 1995. The control of calcium release in heart muscle. Science. 268: 1045-1049.
18. Carlezon, W.A. Jr., R.S. Duman, and E.J. Nestler. 2005. The many faces of CREB. Trends Neurosci. 28: 436-445.
19. Chad, J.E., and R. Eckert. 1984. Calcium domains associated with individual channels can account for anomalous voltage relations of CA-dependent responses. Biophys. J. 45: 993-999.
20. Chapman, R.A., and J. Tunstall. 1981. The tension-depolarization relationship of frog atrial trabeculae as determined by potassium contractures. J. Physiol. 310: 97-115.
21. Chow, F., and A. Means. 2007. The calcium/calmodulin-dependent protein kinase cascades. In Calcium: A Matter of Life or death. Vol. 41. J. Krebs and M. Michalak, editors. Elselvier B.V., Amsterdam. 345-364.
22. Chow, R.H. 1991. Cadmium block of squid calcium currents. Macroscopic data and a kinetic model. J. Gen. Physiol. 98: 751-770.
23. De Crescenzo, V., K.E. Fogarty, R. Zhuge, R.A. Tuft, L.M. Lifshitz, J. Carmichael, K.D. Bellve, S.P. Baker, S. Zissimopoulos, F.A. Lai, et al. 2006. Dihydropyridine receptors and type 1 ryanodine receptors constitute the molecular machinery for voltage-induced Ca2+ release in nerve terminals. J. Neurosci. 26: 7565-7574.
24. De Koninck, P., and H. Schulman. 1998. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science. 279: 227-230.
25. Deisseroth, K., H. Bito, and R.W. Tsien. 1996. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron. 16: 89-101.
26. Deisseroth, K., E.K. Heist, and R.W. Tsien. 1998. Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature. 392: 198-202.
27. Deisseroth, K., P.G. Mermelstein, H. Xia, and R.W. Tsien. 2003. Signaling from synapse to nucleus: the logic behind the mechanisms. Curr. Opin. Neurobiol. 13: 354-365.
28. Dodge, F.A. Jr., and R. Rahamimoff. 1967. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193: 419-432.
29. Dolmetsch, R. 2003. Excitation-transcription coupling: signaling by ion channels to the nucleus. Sci. STKE. 2003: PE4.
30. Dolmetsch, R.E., U. Pajvani, K. Fife, J.M. Spotts, and M.E. Greenberg. 2001. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science. 294: 333-339.
31. Dupont, G., G. Houart, and P. De Koninck. 2003. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations: a simple model. Cell Calcium. 34: 485-497.
32. Ellinor, P.T., J. Yang, W.A. Sather, J.F. Zhang, and R.W. Tsien. 1995. Ca2+ channel selectivity at a single locus for high-affi nity Ca2+ interactions. Neuron. 15: 1121-1132.
33. Erickson, M.G., B.A. Alseikhan, B.Z. Peterson, and D.T. Yue. 2001. Preassociation of calmodulin with voltage-gated Ca(2+) channels revealed by FRET in single living cells. Neuron. 31: 973-985.
34. Franzini-Armstrong, C., and F. Protasi. 1997. Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol. Rev. 77: 699-729.
35. Greenberg, M.E., E.B. Ziff, and L.A. Greene. 1986. Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science. 234: 80-83.
36. Guatimosim, S., K. Dilly, L.F. Santana, M. Saleet Jafri, E.A. Sobie, and W.J. Lederer. 2002. Local Ca(2+) signaling and EC coupling in heart: Ca(2+) sparks and the regulation of the [Ca(2+)](i) transient. J. Mol. Cell. Cardiol. 34: 941-950.
37. Hagiwara, S., and K. Takahashi. 1967. Surface density of calcium ions and calcium spikes in the barnacle muscle fi ber membrane. J. Gen. Physiol. 50: 583-601.
38. Hanson, P.I., and H. Schulman. 1992. Neuronal Ca2+/calmodulin-dependent protein kinases. Annu. Rev. Biochem. 61: 559-601.
39. Hardingham, G.E., F.J. Arnold, and H. Bading. 2001. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 4: 261-267.
40. Hawrot, E., and P.H. Patterson. 1979. Long-term culture of dissociated sympathetic neurons. Methods Enzymol. 58: 574-584.
41. Hegle, A.P., D.D. Marble, and G.F. Wilson. 2006. A voltage-driven switch for ion-independent signaling by ether-a-go-go K+ channels. Proc. Natl. Acad. Sci. USA. 103: 2886-2891.
42. Henkart, M. 1980. Identifi cation and function of intracellular calcium stores in axons and cell bodies of neurons. Fed. Proc. 39: 2783-2789.
43. Hille, B. 1994. Modulation of ion-channel function by G-protein-coupled receptors. Trends Neurosci. 17: 531-536.
44. Hille, B. 2001. Ion Channels of Excitable Membranes. Sinauer, Sunderland, MA. 814 pp.
45. Hirning, L.D., A.P. Fox, E.W. McCleskey, B.M. Olivera, S.A. Thayer, R.J. Miller, and R.W. Tsien. 1988. Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons. Science. 239: 57-61.
46. Hodgkin, A.L., and P. Horowicz. 1960. Potassium contractures in single muscle fibres. J. Physiol. 153: 386-403.
47. Hoshi, T., J. Rothlein, and S.J. Smith. 1984. Facilitation of Ca2+-channel currents in bovine adrenal chromaffi n cells. Proc. Natl. Acad. Sci. USA. 81: 5871-5875.
48. 2+ signals for facilitation. J. Cell Biol. 171: 537-547.
49. Kaczmarek, L.K. 2006. Non-conducting functions of voltage-gated ion channels. Nat. Rev. Neurosci. 7: 761-771.
50. Katz, B., and R. Miledi. 1967. A study of synaptic transmission in the absence of nerve impulses. J. Physiol. 192: 407-436.
51. Kavalali, E.T., and M.R. Plummer. 1994. Selective potentiation of a novel calcium channel in rat hippocampal neurones. J. Physiol. 480: 475-484.
52. Klingauf, J., and E. Neher. 1997. Modeling buffered Ca2+ diffusion near the membrane: implications for secretion in neuroendocrine cells. Biophys. J. 72: 674-690.
53. Kobrinsky, E., E. Schwartz, D.R. Abernethy, and N.M. Soldatov. 2003. Voltagegated mobility of the Ca2+ channel cytoplasmic tails and its regulatory role. J. Biol. Chem. 278: 5021-5028.
54. Koschak, A., G.J. Obermair, F. Pivotto, M.J. Sinnegger-Brauns, J. Striessnig, and D. Pietrobon. 2007. Molecular nature of anomalous L-type calcium channels in mouse cerebellar granule cells. J. Neurosci. 27: 3855-3863.
55. Kunze, D.L., and D. Rampe. 1992. Characterization of the effects of a new Ca2+ channel activator, FPL 64176, in GH3 cells. Mol. Pharmacol. 42: 666-670.
56. 2+. Voltage and concentration dependence of calcium entry into the pore. J. Gen. Physiol. 88: 321-347.
57. Lee, T.S., R. Karl, S. Moosmang, P. Lenhardt, N. Klugbauer, F. Hofmann, T. Kleppisch, and A. Welling. 2006. Calmodulin kinase II is involved in voltage-dependent facilitation of the L-type Cav1.2 calcium channel: identification of the phosphorylation sites. J. Biol. Chem. 281: 25560-25567.
58. Lencesova, L., A. O'Neill, W.G. Resneck, R.J. Bloch, and M.P. Blaustein. 2004. Plasma membrane-cytoskeleton-endoplasmic reticulum complexes in neurons and astrocytes. J. Biol. Chem. 279: 2885-2893.
59. 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.
60. Liu, L., 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.
61. Llinas, R., I.Z. Steinberg, and K. Walton. 1981. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33: 323-351.
62. Lonze, B.E., and D.D. Ginty. 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron. 35: 605-623.
63. Lopez-Lopez, J.R., P.S. Shacklock, C.W. Balke, and W.G. Wier. 1995. Local calcium transients triggered by single L-type calcium channel currents in cardiac cells. Science. 268: 1042-1045.
64. Mager, D.E., E. Kobrinsky, A. Masoudieh, A. Maltsev, D.R. Abernethy, and N.M. Soldatov. 2007. Analysis of functional signaling domains from fl uorescence imaging and the two-dimensional continuous wavelet transform. Biophys. J. 93: 2900-2910.
65. Mains, R.E., and P.H. Patterson. 1973. Primary cultures of dissociated sympathetic neurons. I. Establishment of long-term growth in culture and studies of differentiated properties. J. Cell Biol. 59: 329-345.
66. Mintz, I.M., B.L. Sabatini, and W.G. Regehr. 1995. Calcium control of transmitter release at a cerebellar synapse. Neuron. 15: 675-688.
67. Morgan, J.I., and T. Curran. 1986. Role of ion fl ux in the control of c-fos expression. Nature. 322: 552-555.
68. Mori, M.X., M.G. Erickson, and D.T. Yue. 2004. Functional stoichiometry and local enrichment of calmodulin interacting with Ca2+ channels. Science. 304: 432-435.
69. Murata, Y., H. Iwasaki, M. Sasaki, K. Inaba, and Y. Okamura. 2005. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature. 435: 1239-1243.
70. Murphy, T.H., P.F. Worley, and J.M. Baraban. 1991. L-type voltage-sensitive calcium channels mediate synaptic activation of immediate early genes. Neuron. 7: 625-635.
71. O'Lague, P.H., K. Obata, P. Claude, E.J. Furshpan, and D.D. Potter. 1974. Evidence for cholinergic synapses between dissociated rat sympathetic neurons in cell culture. Proc. Natl. Acad. Sci. USA. 71: 3602-3606.
72. O'Lague, P.H., E.J. Furshpan, and D.D. Potter. 1978. Studies on rat sympathetic neurons developing in cell culture. II. Synaptic mechanisms. Dev. Biol. 67: 404-423.
73. Pietrobon, D., and P. Hess. 1990. Novel mechanism of voltage-dependent gating in L-type calcium channels. Nature. 346: 651-655.
74. Pitt, G.S., R.D. Zuhlke, A. Hudmon, H. Schulman, H. Reuter, and R.W. Tsien. 2001. Molecular basis of calmodulin tethering and Ca2+-dependent inactivation of L-type Ca2+ channels. J. Biol. Chem. 276: 30794-30802.
75. Rios, E., and G. Brum. 1987. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature. 325: 717-720.
76. Sakagami, H., A. Kamata, H. Nishimura, J. Kasahara, Y. Owada, Y. Takeuchi, M. Watanabe, K. Fukunaga, and H. Kondo. 2005. Prominent expression and activity-dependent nuclear translocation of Ca2+/calmodulindependent protein kinase Idelta in hippocampal neurons. Eur. J. Neurosci. 22: 2697-2707.
77. Santana, L.F., H. Cheng, A.M. Gomez, M.B. Cannell, and W.J. Lederer. 1996. Relation between the sarcolemmal Ca2+ current and Ca2+ sparks and local control theories for cardiac excitation-contraction coupling. Circ. Res. 78: 166-171.
78. Sather, W.A., and E.W. McCleskey. 2003. Permeation and selectivity in calcium channels. Annu. Rev. Physiol. 65: 133-159.
79. Schneggenburger, R., and E. Neher. 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature. 406: 889-893.
80. Schneggenburger, R., and E. Neher. 2005. Presynaptic calcium and control of vesicle fusion. Curr. Opin. Neurobiol. 15: 266-274.
81. Schneider, M.F. 1994. Control of calcium release in functioning skeletal muscle fibers. Annu. Rev. Physiol. 56: 463-484.
82. Schneider, M.F., and W.K. Chandler. 1973. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature. 242: 244-246.
83. Shahrezaei, V., A. Cao, and K.R. Delaney. 2006. Ca2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction. J. Neurosci. 26: 13240-13249.
84. Simon, S.M., and R.R. Llinas. 1985. Compartmentalization of the submembrane calcium activity during calcium infl ux and its signifi cance in transmitter release. Biophys. J. 48: 485-498.
85. Soderling, T.R. 1999. The Ca-calmodulin-dependent protein kinase cascade. Trends Biochem. Sci. 24: 232-236.
86. Stern, M.D. 1992. Theory of excitation-contraction coupling in cardiac muscle. Biophys. J. 63: 497-517.
87. Sternberg, S. 1983. Biomedical image processing. Computer. 16: 22-34.
88. Sudhof, T.C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27: 509-547.
89. Sugita, R., H. Mochizuki, T. Ito, H. Yokokura, R. Kobayashi, and H. Hidaka. 1994. Ca2+/calmodulin-dependent protein kinase kinase cascade. Biochem. Biophys. Res. Commun. 203: 694-701.
90. Takeda, H., Y. Kitaoka, Y. Hayashi, T. Kumai, Y. Munemasa, H. Fujino, S. Kobayashi, and S. Ueno. 2007. Calcium/calmodulin-dependent protein kinase II regulates the phosphorylation of CREB in NMDA-induced retinal neurotoxicity. Brain Res. 1184: 306-315.
91. Thiagarajan, T.C., E.S. Piedras-Renteria, and R.W. Tsien. 2002. alpha- and beta CaMKII. Inverse regulation by neuronal activity and opposing effects on synaptic strength. Neuron. 36: 1103-1114.
92. Vizard, T.N., G.W. O'Keeffe, H. Gutierrez, C.H. Kos, D. Riccardi, and A.M. Davies. 2008. Regulation of axonal and dendritic growth by the extracellular calcium-sensing receptor. Nat. Neurosci. 11: 285-291.
93. Wakamori, M., M. Strobeck, T. Niidome, T. Teramoto, K. Imoto, and Y. Mori. 1998. Functional characterization of ion permeation pathway in the N-type Ca2+ channel. J. Neurophysiol. 79: 622-634.
94. Wang, S.Q., L.S. Song, E.G. Lakatta, and H. Cheng. 2001. Ca2+ signalling between single L-type Ca2+ channels and ryanodine receptors in heart cells. Nature. 410: 592-596.
95. Weick, J.P., R.D. Groth, A.L. Isaksen, and P.G. Mermelstein. 2003. Interactions with PDZ proteins are required for L-type calcium channels to activate cAMP response element-binding protein-dependent gene expression. J. Neurosci. 23: 3446-3456.
96. West, A.E., E.C. Griffith, and M.E. Greenberg. 2002. Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3: 921-931.
97. Wheeler, D.G., and E. Cooper. 2001. Depolarization strongly induces human cytomegalovirus major immediate-early promoter/enhancer activity in neurons. J. Biol. Chem. 276: 31978-31985.
98. Wheeler, D.G., C.F. Barrett, and R.W. Tsien. 2006. L-type calcium channel ligands block nicotine-induced signaling to CREB by inhibiting nicotinic receptors. Neuropharmacology. 51: 27-36.
99. Wiznerowicz, M., and D. Trono. 2003. Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J. Virol. 77: 8957-8961.
100. Wu, L.G., and P. Saggau. 1994. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J. Neurosci. 14: 645-654.
101. Xiao, R.P., H. Cheng, W.J. Lederer, T. Suzuki, and E.G. Lakatta. 1994. Dual regulation of Ca2+/calmodulin-dependent kinase II activity by membrane voltage and by calcium influx. Proc. Natl. Acad. Sci. USA. 91: 9659-9663.
102. Xu, W., and D. Lipscombe. 2001. Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J. Neurosci. 21: 5944-5951.
103. Yang, J., P.T. Ellinor, W.A. Sather, J.F. Zhang, and R.W. Tsien. 1993. Molecular determinants of Ca2+ selectivity and ion permeation in L-type Ca2+ channels. Nature. 366: 158-161.
104. Yuan, W., and D.M. Bers. 1994. Ca-dependent facilitation of cardiac Ca current is due to Ca-calmodulin-dependent protein kinase. Am. J. Physiol. 267: H982-H993.
105. Zhang, H., A. Maximov, Y. Fu, F. Xu, T.S. Tang, T. Tkatch, D.J. Surmeier, and I. Bezprozvanny. 2005. Association of CaV1.3 L-type calcium channels with Shank. J. Neurosci. 25: 1037-1049.
106. Zhao, R., L. Liu, and A.R. Rittenhouse. 2007. Ca2+ infl ux through both L- and N-type Ca2+ channels increases c-fos expression by electrical stimulation of sympathetic neurons. Eur. J. Neurosci. 25: 1127-1135.
107. Zuhlke, R.D., G.S. Pitt, K. Deisseroth, R.W. Tsien, and H. Reuter. 1999. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature. 399: 159-162.