Cav1.2 and Cav1.3 L-type calcium channels operate in a similar voltage range but show different coupling to Ca2+-dependent conductances in hippocampal neurons

American Journal of Physiology - Cell Physiology

Volumn 306, Issue 12, 2014, Pages

  Hasreiter, Julia ^a   Goldnagl, Lena ^a   Böhm, Stefan ^a   Kubista, Helmut ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Dihydropyridine; Gene deletion; Knockout; Voltage gated calcium channel

Indexed keywords

CALCIUM; CALCIUM CHANNEL CAV1.2; CALCIUM CHANNEL CAV1.3; CALCIUM CHANNEL L TYPE; DIHYDROPYRIDINE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; CACNA1D PROTEIN, MOUSE; CAV1.2 PROTEIN, MOUSE;

AFTERDEPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CONDUCTANCE; CALCIUM TRANSPORT; CONTROLLED STUDY; DEPOLARIZATION; EMBRYO; HIPPOCAMPAL NEURONAL CULTURE; HYPERPOLARIZATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; WILD TYPE; ANIMAL; GENE DELETION; GENETICS; HIPPOCAMPUS; KNOCK OUT; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; RAT; VOLTAGE-GATED CALCIUM CHANNEL;

DIHYDROPYRIDINE; GENE DELETION; KNOCKOUT; VOLTAGE-GATED CALCIUM CHANNEL;

ANIMALS; CALCIUM CHANNELS, L-TYPE; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; NEURONS; RATS;

EID: 84902687762     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00329.2013     Document Type: Article

References (76)

1. Amano H, Amano T, Matsubayashi H, Ishihara K, Serikawa T, Sasa M. Enhanced calcium influx in hippocampal CA3 neurons of spontaneously epileptic rats. Epilepsia 42: 345-350, 2001.
2. Anekonda TS, Quinn JF, Harris C, Frahler K, Wadsworth TL, Woltjer RL. L-type voltage-gated calcium channel blockade with isradipine as a therapeutic strategy for Alzheimer's disease. Neurobiol Dis 41: 62-70, 2011.
3. Barad M. Later developments: molecular keys to age-related memory impairment. Alzheimer Dis Assoc Disord 17: 168-176, 2003.
4. Bouhadfane M, Tazerart S, Moqrich A, Vinay L, Brocard F. Sodiummediated plateau potentials in lumbar motoneurons of neonatal rats. J Neurosci 33: 15626-15641, 2013.
5. Cai X, Liang CW, Muralidharan S, Kao JP, Tang CM, Thompson SM. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44: 351-364, 2004.
6. Carlin KP, Jones KE, Jiang Z, Jordan LM, Brownstone RM. Dendritic L-type calcium currents in mouse spinal motoneurons: implications for bistability. Eur J Neurosci 12: 1635-1646, 2000.
7. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, Tkatch T, Meredith GE, Surmeier DJ. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 447: 1081-1086, 2007.
8. 2+ channels. Neuroscience 120: 435-442, 2003.
9. Dao DT, Mahon PB, Cai X, Kovacsics CE, Blackwell RA, Arad M, Shi J, Zandi PP, O'Donnell P; Bipolar Genome Study (BiGS) Consortium, Knowles JA, Weissman MM, Coryell W, Scheftner WA, Lawson WB, Levinson DF, Thompson SM, Potash JB, Gould TD. Mood disorder susceptibility gene CACNA1C modifies mood-related behaviors in mice and interacts with sex to influence behavior in mice and diagnosis in humans. Biol Psychiatry 68: 801-810, 2010.
10. 2+ channels in neural stem/progenitor cell differentiation. Eur J Neurosci 23: 935-944, 2006.
11. Davis SE, Bauer EP. L-type voltage-gated calcium channels in the basolateral amygdala are necessary for fear extinction. J Neurosci 32: 13582-13586, 2012.
12. Dovzhenok A, Kuznetsov AS. Exploring neuronal bistability at the depolarization block. PLoS One 7: e42811, 2012.
13. Dunmyre JR, Del Negro CA, Rubin JE. Interactions of persistent sodium and calcium-activated nonspecific cationic currents yield dynamically distinct bursting regimes in a model of respiratory neurons. J Comput Neurosci 31: 305-328, 2011.
14. 2+ channel alpha2delta subunit. J Neurosci 17: 6884-6891, 1997.
15. 2+ channels after cocaine withdrawal. Synapse 63: 690-697, 2009.
16. Fossat P, Sibon I, Le Masson G, Landry M, Nagy F. L-type calcium channels and NMDA receptors: a determinant duo for short-term nociceptive plasticity. Eur J Neurosci 25: 127-135, 2007.
17. Gamelli AE, McKinney BC, White JA, Murphy GG. Deletion of the L-type calcium channel Cav1.3 but not Cav12 results in a diminished sAHP in mouse CA1 pyramidal neurons. Hippocampus 21: 133-141, 2011.
18. Geier P, Lagler M, Boehm S, Kubista H. Dynamic interplay of excitatory and inhibitory coupling modes of neuronal L-type calcium channels. Am J Physiol Cell Physiol 300: C937-C949, 2011.
19. Gomez JP, Fares N, Potreau D. Effects of Bay K 8644 on L-type calcium current from newborn rat cardiomyocytes in primary culture. J Mol Cell Cardiol 28: 2217-2229, 1996.
20. Haase H, Alvarez J, Petzhold D, Doller A, Behlke J, Erdmann J, Hetzer R, Regitz-Zagrosek V, Vassort G, Morano I. Ahnak is critical for cardiac Cav1.2 calcium channel function and its beta-adrenergic regulation. FASEB J 19: 1969-1977, 2005.
21. Haj-Dahmane S, Andrade R. Calcium-activated cation nonselective current contributes to the fast afterdepolarization in rat prefrontal cortex neurons. J Neurophysiol 78: 1983-1989, 1997.
22. Hasuo H, Phelan KD, Twery MJ, Gallagher JP. A calcium-dependent slow afterdepolarization recorded in rat dorsolateral septal nucleus neurons in vitro. J Neurophysiol 64: 1838-1846, 1990.
23. 2+-activated monovalent selective cation channel. Curr Biol 13: 1153-1158, 2003.
24. 2+ channels. J Biol Chem 279: 55211-55217, 2004.
25. 2+ channels in ACC. Nat Neurosci 13: 482-488, 2010.
26. 2+ channels in the lateral superior olive: functional analysis in wild-type, Cav1.3-/-, and Cav12DHP-/-mice. J Neurophysiol 108: 365-379, 2012.
27. Kalmbach BE, Chitwood RA, Dembrow NC, Johnston D. Dendritic generation of mGLUR-mediated slow afterdepolarization in layer 5 neurons of prefrontal cortex. J Neurosci 33: 13518-13532, 2013.
28. Kang S, Cooper G, Dunne SF, Dusel B, Luan CH, Surmeier DJ, Silverman RB. Cav1.3-selective L-type calcium channel antagonists as potential new therapeutics for Parkinson's disease. Nat Commun 3: 1146, 2012.
29. 2+ channels Cav1.3 and Cav12 by 1,4-dihydropyrimidines and 4H-pyrans as dihydropyridine mimics. Bioorg Med Chem 21: 4365-4373, 2013.
30. Köhling R, Straub H, Speckmann EJ. Differential involvement of L-type calcium channels in epileptogenesis of rat hippocampal slices during ontogenesis. Neurobiol Dis 7: 471-482, 2000.
31. 2+ channels activating at negative voltages. J Biol Chem 276: 22100-22106, 2001.
32. Lacinová L. Voltage-dependent calcium channels. Gen Physiol Biophys 24, Suppl 1: 1-78, 2005.
33. Lacinova L, Moosmang S, Langwieser N, Hofmann F, Kleppisch T. Cav1.2 calcium channels modulate the spiking pattern of hippocampal pyramidal cells. Life Sci 82: 41-49, 2008.
34. Langwieser N, Christel CJ, Kleppisch T, Hofmann F, Wotjak CT, Moosmang S. Homeostatic switch in hebbian plasticity and fear learning after sustained loss of Cav1.2 calcium channels. J Neurosci 30: 8367-8375, 2010.
35. Lee CR, Tepper JM. A calcium-activated nonselective cation conductance underlies the plateau potential in rat substantia nigra GABAergic neurons. J Neurosci 27: 6531-6541, 2007.
36. Liao P, Soong TW. Cav1.2 channelopathies: from arrhythmias to autism, bipolar disorder, and immunodeficiency. Pflügers Arch 460: 353-359, 2010.
37. Liebmann L, Karst H, Sidiropoulou K, van Gemert N, Meijer OC, Poirazi P, Joëls M. Differential effects of corticosterone on the slow afterhyperpolarization in the basolateral amygdala and CA1 region: possible role of calcium channel subunits. J Neurophysiol 99: 958-968, 2008.
38. 2+ channels in NMDA receptor-independent synaptic plasticity and spatial memory. J Neurosci 25: 9883-9982, 2005.
39. Morisset V, Nagy F. Ionic basis for plateau potentials in deep dorsal horn neurons of the rat spinal cord. J Neurosci 19: 7309-7316, 1999.
40. Moyer JR Jr, Thompson LT, Black JP, Disterhoft JF. Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age-and concentration-dependent manner. J Neurophysiol 68: 2100-2109, 1992.
41. Mrejeru A, Wei A, Ramirez JM. Calcium-activated nonselective cation currents are involved in generation of tonic and bursting activity in dopamine neurons of the substantia nigra pars compacta. J Physiol 589: 2497-2514, 2011.
42. Pedersen SF, Owsianik G, Nilius B. TRP channels: an overview. Cell Calcium 38: 233-252, 2005.
43. Perrier JF, Mejia-Gervacio S, Hounsgaard J. Facilitation of plateau potentials in turtle motoneurones by a pathway dependent on calcium and calmodulin. J Physiol 528: 107-113, 2000.
44. Petersson ME, Fransén E. Long-lasting small-amplitude TRP-mediated dendritic depolarizations in CA1 pyramidal neurons are intrinsically stable and originate from distal tuft regions. Eur J Neurosci 36: 2917-2925, 2012.
45. 2+-dependent slow afterdepolarization in nigral dopamine neurons. J Neurophysiol 81: 977-984, 1999.
46. 2+ channels. Cell 102: 89-97, 2000.
47. Radzicki D, Yau HJ, Pollema-Mays SL, Mlsna L, Cho K, Koh S, Martina M. Temperature-sensitive Cav1.2 calcium channels support intrinsic firing of pyramidal neurons and provide a target for the treatment of febrile seizures. J Neurosci 33: 9920-9931, 2013.
48. Roberts CB, O'Boyle MP, Suter KJ. Dendrites determine the contribution of after depolarization potentials (ADPs) to generation of repetitive action potentials in hypothalamic gonadotropin releasing-hormone (GnRH) neurons. J Comput Neurosci 26: 39-53, 2009.
49. Rubi L, Schandl U, Lagler M, Geier P, Spies D, Gupta KD, Boehm S, Kubista H. Raised activity of L-type calcium channels renders neurons prone to form paroxysmal depolarization shifts. Neuromolecular Med 15: 476-492, 2013.
50. 2+ channels mediate cocaine-induced GluA1 trafficking in the nucleus accumbens, a long-term adaptation dependent on ventral tegmental area Cav1.3 channels. J Neurosci 31: 13562-13575, 2011.
51. Seoane A, Massey PV, Keen H, Bashir ZI, Brown MW. L-type voltage-dependent calcium channel antagonists impair perirhinal longterm recognition memory and plasticity processes. J Neurosci 29: 9534-9544, 2009.
52. 2+ channels responsible for plateau potentials in motoneurons from the lumbar spinal cord of the turtle. Eur J Neurosci 18: 258-266, 2003.
53. Singer D, Biel M, Lotan I, Flockerzi V, Hofmann F, Dascal N. The roles of the subunits in the function of the calcium channel. Science 253: 1553-1557, 1991.
54. 2+ channels. J Clin Invest 113: 1430-1439, 2004.
55. Speckmann EJ, Walden J. Anti-epileptic effects of organic calcium channel, blockers in animal experiments. In: Epilepsy: Models, Mechanism and Concepts, edited by Schwartzkroin PA. Cambridge, UK: Cambridge Univ. Press, 1993, p. 462-486.
56. Speckmann EJ, Walden J, Bingmann D. Functional implication of calcium ions in epileptic seizures. Antiepileptic effects of organic calcium antagonists. Arzneimittelforschung 39: 149-156, 1989.
57. Staley K, Hellier JL, Dudek FE. Do interictal spikes drive epileptogenesis? Neuroscientist 11: 272-276, 2005.
58. Staley KJ, White A, Dudek FE. Interictal spikes: harbingers or causes of epilepsy? Neurosci Lett 497: 247-250, 2011.
59. Straub H, Köhling R, Frieler A, Grigat M, Speckmann EJ. Contribution of L-type calcium channels to epileptiform activity in hippocampal and neocortical slices of guinea-pigs. Neuroscience 95: 63-72, 2000.
60. 2+ channel isoforms for brain function. Biochem Soc Trans 34: 903-909, 2006.
61. Surmeier DJ, Schumacker PT. Calcium, bioenergetics, and neuronal vulnerability in Parkinson's disease. J Biol Chem 288: 10736-10741, 2013.
62. Tomlinson WJ, Stea A, Bourinet E, Charnet P, Nargeot J, Snutch TP. Functional properties of a neuronal class C L-type calcium channel. Neuropharmacology 32: 1117-1126, 1993.
63. 2+-activated cation conductance in myenteric AH neurons. Neuroscience 115: 375-393, 2002.
64. 2+ channel alpha 1 subunits. J Biol Chem 276: 12730-12735, 2001.
65. 2+ signaling to control CREB-dependent gene expression. Cell 149: 1112-1124, 2012.
66. White JA, McKinney BC, John MC, Powers PA, Kamp TJ, Murphy GG. Conditional forebrain deletion of the L-type calcium channel Cav1.2 disrupts remote spatial memories in mice. Learn Mem 15: 1-5, 2008.
67. Williams ME, Feldman DH, McCue AF, Brenner R, Velicelebi G, Ellis SB, Harpold MM. Structure and functional expression of alpha 1, alpha 2, and beta subunits of a novel human neuronal calcium channel subtype. Neuron 8: 71-84, 1992.
68. Wu WW, Chan CS, Disterhoft JF. Slow afterhyperpolarization governs the development of NMDA receptor-dependent afterdepolarization in CA1 pyramidal neurons during synaptic stimulation. J Neurophysiol 92: 2346-2356, 2004.
69. 2+ current. Brain Res 812: 133-141, 1998.
70. Xu W, Lipscombe D. Neuronal Cav1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21: 5944-5951, 2001.
71. Yagami T, Kohma H, Yamamoto Y. L-type voltage-dependent calcium channels as therapeutic targets for neurodegenerative diseases. Curr Med Chem 19: 4816-4827, 2012.
72. Yamamoto R, Ueta Y, Kato N. Dopamine induces a slow afterdepolarization in lateral amygdala neurons. J Neurophysiol 98: 984-992, 2007.
73. Yasuda T, Chen L, Barr W, McRory JE, Lewis RJ, Adams DJ, Zamponi GW. Auxiliary subunit regulation of high-voltage activated calcium channels expressed in mammalian cells. Eur J Neurosci 20: 1-13, 2004.
74. Zhang H, Fu Y, Altier C, Platzer J, Surmeier DJ, Bezprozvanny I. Cav1.2 and Cav1.3 neuronal L-type calcium channels: differential targeting and signaling to pCREB. Eur J Neurosci 23: 2297-2310, 2006.
75. Zhang Z, Reboreda A, Alonso A, Barker PA, Séguéla P. TRPC channels underlie cholinergic plateau potentials and persistent activity in entorhinal cortex. Hippocampus 21: 386-397, 2011.
76. Zhou Z, Xiong W, Masurkar AV, Chen WR, Shepherd GM. Dendritic calcium plateau potentials modulate input-output properties of juxtaglomerular cells in the rat olfactory bulb. J Neurophysiol 96: 2354-2363, 2006.