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The Journal of Neuroscience, March 15, 1999, 19(6):1912-1921

Cloning and Expression of a Novel Member of the Low Voltage-Activated T-Type Calcium Channel Family

Jung-Ha Lee1, Asif N. Daud1, Leanne L. Cribbs1, Antonio E. Lacerda2, Alexei Pereverzev3, Udo Klöckner4, Toni Schneider3, and Edward Perez-Reyes1

1 Department of Physiology, Loyola University Medical Center, Maywood, Illinois 60153, 2 Rammelkamp Center for Research and Education, MetroHealth Medical Center, Cleveland, Ohio 44109, and Departments of 3 Physiology and 4 Vegetative Physiology, University of Cologne, D50931 Cologne, Germany

Low voltage-activated Ca2+ channels play important roles in pacing neuronal firing and producing network oscillations, such as those that occur during sleep and epilepsy. Here we describe the cloning and expression of the third member of the T-type family, alpha 1I or CavT.3, from rat brain. Northern analysis indicated that it is predominantly expressed in brain. Expression of the cloned channel in either Xenopus oocytes or stably transfected human embryonic kidney-293 cells revealed novel gating properties. We compared these electrophysiological properties to those of the cloned T-type channels alpha 1G and alpha 1H and to the high voltage-activated channels formed by alpha 1Ebeta 3. The alpha 1I channels opened after small depolarizations of the membrane similar to alpha 1G and alpha 1H but at more depolarized potentials. The kinetics of activation and inactivation were dramatically slower, which allows the channel to act as a Ca2+ injector. In oocytes, the kinetics were even slower, suggesting that components of the expression system modulate its gating properties. Steady-state inactivation occurred at higher potentials than any of the other T channels, endowing the channel with a substantial window current. The alpha 1I channel could still be classified as T-type by virtue of its criss-crossing kinetics, its slow deactivation (tail current), and its small (11 pS) conductance in 110 mM Ba2+ solutions. Based on its brain distribution and novel gating properties, we suggest that alpha 1I plays important roles in determining the electroresponsiveness of neurons, and hence, may be a novel drug target.

Key words: molecular cloning; calcium channel; CNS; thalamus; anticonvulsant; epilepsy


Copyright © 1999 Society for Neuroscience  0270-6474/99/1961912-10$05.00/0


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J. Physiol., April 1, 2002; 540(1): 3 - 14.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
P. Mariot, K. Vanoverberghe, N. Lalevee, M. F. Rossier, and N. Prevarskaya
Overexpression of an alpha 1H (Cav3.2) T-type Calcium Channel during Neuroendocrine Differentiation of Human Prostate Cancer Cells
J. Biol. Chem., March 22, 2002; 277(13): 10824 - 10833.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
S. S. Sidach and I. M. Mintz
Kurtoxin, A Gating Modifier of Neuronal High- and Low-Threshold Ca Channels
J. Neurosci., March 15, 2002; 22(6): 2023 - 2034.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
S. J. Slaght, N. Leresche, J.-M. Deniau, V. Crunelli, and S. Charpier
Activity of Thalamic Reticular Neurons during Spontaneous Genetically Determined Spike and Wave Discharges
J. Neurosci., March 15, 2002; 22(6): 2323 - 2334.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
C. Berthier, A. Monteil, P. Lory, and C. Strube
{alpha}1H mRNA in single skeletal muscle fibres accounts for T-type calcium current transient expression during fetal development in mice
J. Physiol., March 15, 2002; 539(3): 681 - 691.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
G. Michels, J. Matthes, R. Handrock, U. Kuchinke, F. Groner, L. L. Cribbs, A. Pereverzev, T. Schneider, E. Perez-Reyes, and S. Herzig
Single-Channel Pharmacology of Mibefradil in Human Native T-Type and Recombinant Cav3.2 Calcium Channels
Mol. Pharmacol., March 1, 2002; 61(3): 682 - 694.
[Abstract] [Full Text] [PDF]


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Protein Eng Des SelHome page
G. Barreiro, C. R. W. Guimaraes, and R. B. de Alencastro
A molecular dynamics study of an L-type calcium channel model
Protein Eng. Des. Sel., February 1, 2002; 15(2): 109 - 122.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
C. M. Santi, F. S. Cayabyab, K. G. Sutton, J. E. McRory, J. Mezeyova, K. S. Hamming, D. Parker, A. Stea, and T. P. Snutch
Differential Inhibition of T-Type Calcium Channels by Neuroleptics
J. Neurosci., January 15, 2002; 22(2): 396 - 403.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
K. Talavera, M. Staes, A. Janssens, N. Klugbauer, G. Droogmans, F. Hofmann, and B. Nilius
Aspartate Residues of the Glu-Glu-Asp-Asp (EEDD) Pore Locus Control Selectivity and Permeation of the T-type Ca2+ Channel alpha 1G
J. Biol. Chem., November 30, 2001; 276(49): 45628 - 45635.
[Abstract] [Full Text] [PDF]


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JGPHome page
C. J. Frazier, J. R. Serrano, E. G. George, X. Yu, A. Viswanathan, E. Perez-Reyes, and S. W. Jones
Gating Kinetics of the {alpha}1i T-Type Calcium Channel
J. Gen. Physiol., November 1, 2001; 118(5): 457 - 470.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
J. C. Gomora, A. N. Daud, M. Weiergraber, and E. Perez-Reyes
Block of Cloned Human T-Type Calcium Channels by Succinimide Antiepileptic Drugs
Mol. Pharmacol., November 1, 2001; 60(5): 1121 - 1132.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
O. Lesouhaitier, A. Chiappe, and M. F. Rossier
Aldosterone Increases T-Type Calcium Currents in Human Adrenocarcinoma (H295R) Cells by Inducing Channel Expression
Endocrinology, October 1, 2001; 142(10): 4320 - 4330.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
S. M. Todorovic, V. Jevtovic-Todorovic, S. Mennerick, E. Perez-Reyes, and C. F. Zorumski
Cav3.2 Channel Is a Molecular Substrate for Inhibition of T-Type Calcium Currents in Rat Sensory Neurons by Nitrous Oxide
Mol. Pharmacol., September 1, 2001; 60(3): 603 - 610.
[Abstract] [Full Text] [PDF]


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Mol. Endocrinol.Home page
A. Scholze, T. D. Plant, A. C. Dolphin, and B. Nurnberg
Functional Expression and Characterization of a Voltage-Gated CaV1.3 ({{alpha}}1D) Calcium Channel Subunit from an Insulin-Secreting Cell Line
Mol. Endocrinol., July 1, 2001; 15(7): 1211 - 1221.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
P J Green, R Warre, P D Hayes, N C L McNaughton, A D Medhurst, M Pangalos, D M Duckworth, and A D Randall
Kinetic modification of the {alpha}1I subunit-mediated T-type Ca2+ channel by a human neuronal Ca2+ channel {gamma} subunit
J. Physiol., June 1, 2001; 533(2): 467 - 478.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
H.-y. Jung, N. P. Staff, and N. Spruston
Action Potential Bursting in Subicular Pyramidal Neurons Is Driven by a Calcium Tail Current
J. Neurosci., May 15, 2001; 21(10): 3312 - 3321.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
S. Brevi, M. de Curtis, and J. Magistretti
Pharmacological and Biophysical Characterization of Voltage-Gated Calcium Currents in the Endopiriform Nucleus of the Guinea Pig
J Neurophysiol, May 1, 2001; 85(5): 2076 - 2087.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
L. L. Cribbs, B. L. Martin, E. A. Schroder, B. B. Keller, B. P. Delisle, and J. Satin
Identification of the T-Type Calcium Channel (CaV3.1d) in Developing Mouse Heart
Circ. Res., March 2, 2001; 88(4): 403 - 407.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Cell Physiol.Home page
A. D. Schrier, H. Wang, E. M. Talley, E. Perez-Reyes, and P. Q. Barrett
{alpha}1H T-type Ca2+ channel is the predominant subtype expressed in bovine and rat zona glomerulosa
Am J Physiol Cell Physiol, February 1, 2001; 280(2): C265 - C272.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
M. Staes, K. Talavera, N. Klugbauer, J. Prenen, L. Lacinova, G. Droogmans, F. Hofmann, and B. Nilius
The amino side of the C-terminus determines fast inactivation of the T-type calcium channel {alpha}1G
J. Physiol., January 1, 2001; 530(1): 35 - 45.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Cell Physiol.Home page
M. Tateyama, S. Zong, T. Tanabe, and R. Ochi
Properties of voltage-gated Ca2+ channels in rabbit ventricular myocytes expressing Ca2+ channel {alpha}1E cDNA
Am J Physiol Cell Physiol, January 1, 2001; 280(1): C175 - C182.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
S. M. Wilson, P. T. Toth, S. B. Oh, S. E. Gillard, S. Volsen, D. Ren, L. H. Philipson, E. C. Lee, C. F. Fletcher, L. Tessarollo, et al.
The Status of Voltage-Dependent Calcium Channels in alpha 1E Knock-Out Mice
J. Neurosci., December 1, 2000; 20(23): 8566 - 8571.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Cell Physiol.Home page
P. Q. Barrett, H.-K. Lu, R. Colbran, A. Czernik, and J. J. Pancrazio
Stimulation of unitary T-type Ca2+ channel currents by calmodulin-dependent protein kinase II
Am J Physiol Cell Physiol, December 1, 2000; 279(6): C1694 - C1703.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
R. C. Foehring, P. G. Mermelstein, W.-J. Song, S. Ulrich, and D. J. Surmeier
Unique Properties of R-Type Calcium Currents in Neocortical and Neostriatal Neurons
J Neurophysiol, November 1, 2000; 84(5): 2225 - 2236.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
V. Leuranguer, A. Monteil, E. Bourinet, G. Dayanithi, and J. Nargeot
T-type calcium currents in rat cardiomyocytes during postnatal development: contribution to hormone secretion
Am J Physiol Heart Circ Physiol, November 1, 2000; 279(5): H2540 - H2548.
[Abstract] [Full Text] [PDF]


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J. Pharmacol. Exp. Ther.Home page
R. L. Martin, J.-H. Lee, L. L. Cribbs, E. Perez-Reyes, and D. A. Hanck
Mibefradil Block of Cloned T-Type Calcium Channels
J. Pharmacol. Exp. Ther., October 1, 2000; 295(1): 302 - 308.
[Abstract] [Full Text]


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Mol Hum ReprodHome page
W.-Y. Son, J.-H. Lee, J.-H. Lee, and C.-T. Han
Acrosome reaction of human spermatozoa is mainly mediated by {alpha}1H T-type calcium channels
Mol. Hum. Reprod., October 1, 2000; 6(10): 893 - 897.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
S. Sokolov, R. G Weiss, E. N Timin, and S. Hering
Modulation of slow inactivation in class A Ca2+ channels by {beta}-subunits
J. Physiol., September 15, 2000; 527(3): 445 - 454.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
Y. Mori, M. Wakamori, S.-i. Oda, C. F. Fletcher, N. Sekiguchi, E. Mori, N. G. Copeland, N. A. Jenkins, K. Matsushita, Z. Matsuyama, et al.
Reduced Voltage Sensitivity of Activation of P/Q-Type Ca2+ Channels is Associated with the Ataxic Mouse Mutation Rolling Nagoya (tgrol)
J. Neurosci., August 1, 2000; 20(15): 5654 - 5662.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
S. M. Todorovic, E. Perez-Reyes, and C. J. Lingle
Anticonvulsants But Not General Anesthetics Have Differential Blocking Effects on Different T-Type Current Variants
Mol. Pharmacol., July 1, 2000; 58(1): 98 - 108.
[Abstract] [Full Text]


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Proc. Natl. Acad. Sci. USAHome page
P. Bijlenga, J.-H. Liu, E. Espinos, C.-A. Haenggeli, J. Fischer-Lougheed, C. R. Bader, and L. Bernheim
T-type alpha 1H Ca2+ channels are involved in Ca2+ signaling during terminal differentiation (fusion) of human myoblasts
PNAS, June 20, 2000; 97(13): 7627 - 7632.
[Abstract] [Full Text] [PDF]


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J. Histochem. Cytochem.Home page
M. Weiergräber, A. Pereverzev, R. Vajna, M. Henry, M. Schramm, W. Nastainczyk, H. Grabsch, and T. Schneider
Immunodetection of {alpha}1E Voltage-gated Ca2+ Channel in Chromogranin-positive Muscle Cells of Rat Heart, and in Distal Tubules of Human Kidney
J. Histochem. Cytochem., June 1, 2000; 48(6): 807 - 820.
[Abstract] [Full Text]


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J. Neurophysiol.Home page
C. Beurrier, B. Bioulac, and C. Hammond
Slowly Inactivating Sodium Current (INaP) Underlies Single-Spike Activity in Rat Subthalamic Neurons
J Neurophysiol, April 1, 2000; 83(4): 1951 - 1957.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
J. Nargeot
A Tale of Two (Calcium) Channels
Circ. Res., March 31, 2000; 86(6): 613 - 615.
[Full Text] [PDF]


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Circ. Res.Home page
J. F. Heubach, A. Kohler, E. Wettwer, and U. Ravens
T-Type and Tetrodotoxin-Sensitive Ca2+ Currents Coexist in Guinea Pig Ventricular Myocytes and Are Both Blocked by Mibefradil
Circ. Res., March 31, 2000; 86(6): 628 - 635.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
J. Satin and L. L. Cribbs
Identification of a T-Type Ca2+ Channel Isoform in Murine Atrial Myocytes (AT-1 Cells)
Circ. Res., March 31, 2000; 86(6): 636 - 642.
[Abstract] [Full Text] [PDF]



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