Functional compensation by other voltage-gated Ca2+ channels in mouse basal forebrain neurons with CaV2.1 mutations

Brain Research

Volumn 1140, Issue 1, 2007, Pages 105-119

  Etheredge, Jason A ^a   Murchison, David ^a   Abbott, Louise C ^b   Griffith, William H ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Tottering Leaner Calcium current Basal forebrain Cholinergic RT PCR

Indexed keywords

BARIUM; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CHOLINE ACETYLTRANSFERASE; MESSENGER RNA; VOLTAGE GATED CALCIUM CHANNEL;

ABSENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHOLINERGIC SYSTEM; FEMALE; FOREBRAIN; GENE EXPRESSION REGULATION; GENE MUTATION; GENOTYPE; MALE; MEMBRANE CURRENT; MOTOR CONTROL; MOTOR PERFORMANCE; MOUSE; MOUSE STRAIN; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PURKINJE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WILD TYPE;

ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CALCIUM CHANNELS, N-TYPE; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; ION CHANNEL GATING; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; MICE, TRANSGENIC; MUTATION; NEURONS; PATCH-CLAMP TECHNIQUES; PROSENCEPHALON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

MUS;

EID: 33847641509     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2005.11.007     Document Type: Article

References (104)

1. Applied Biosystems Prism® 7700 sequence detection system, User Bulletin 2. User's manual (1997), The Perkin-Elmer Corporation, Foster City CA 1-36
2. Aosaki T., and Kasai H. Characterization of two kinds of high voltage-activated Ca-channel currents in chick sensory neurones. Differential sensitivity to dihydropyridines and ω-conotoxin GVIA. Pfluegers Arch. 414 (1989) 150-156
3. Arikkath J., and Campbell K.P. Auxiliary subunits: essential components of the voltage-gated calcium channel complex. Curr. Opin. Neurobiol. 13 (2003) 298-307
4. Bean B.P. Classes of calcium channels in vertebrate cells. Annu. Rev. Physiol. 51 (1989) 367-384
5. Berridge M.J. Neuronal calcium signaling. Neuron 21 (1998) 13-26
6. 2+ channel activity and coordinate regulation of subunit mRNA in single neurons of rat hippocampal 'zipper' slices. Epilepsy Res. 43 (2001) 211-226
7. Brashear H.R., Zaborszky L., and Heimer L. Distribution of GABAergic and cholinergic neurons in the rat diagonal band. Neuroscience 17 (1986) 439-451
8. Caddick S.J., Wang C., Fletcher C.F., Jenkins N.A., Copeland N.G., and Hosford D.A. Excitatory but not inhibitory synaptic transmission is reduced in lethargic (Cacnb4(lh)) and tottering (Cacna1atg) mouse thalami. J. Neurophysiol. 81 (1999) 2066-2074
9. 2+ channel activity and inhibitory synaptic transmission. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 2590-2595
10. Campbell D.B., and Hess E.J. L-type calcium channels contribute to the tottering mouse dystonic episodes. Mol. Pharmacol. 55 (1999) 23-31
11. Campbell L.W., Hao S.-Y., Thibault O., Blalock E.M., and Landfield P.W. Aging changes in voltage gated calcium currents in hippocampal CA1 neurons. J. Neurosci. 16 (1996) 6286-6295
12. 2+ channels and their role in neurotransmitter release. Cell Calcium 24 (1998) 307-323
13. Catterall W.A. Structure and function of voltage-gated ion channels. Annu. Rev. Cell Dev. Biol. 16 (2000) 521-555
14. Catterall W.A., Striessnig J., Snutch T.P., and Perez-Reyes E. International union of pharmacology. international union of pharmacology. XL, Compendium of voltage-gated ion channels: calcium channels. Pharmacol. Rev. 55 (2003) 579-581
15. Choi D.W. Excitotoxic cell death. J. Neurobiol. 23 (1992) 1261-1276
16. Chung Y.H., Shin C.M., Kim M.J., Shin D.H., Yoo Y.B., and Cha C.I. Differential alterations in the distribution of voltage-gated calcium channels in aged rat cerebellum. Brain Res. 903 (2001) 247-252
17. Clapham D.E. Calcium signaling. Cell 80 (1995) 259-268
18. V1.2 during aging. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 16018-16023
19. De Waard M., Liu H., Walker D., Scott V.E.S., Gurnett C.A., and Campbell K.P. Direct binding of G-protein complex to voltage-dependent calcium channels. Nature 385 (1997) 446-450
20. Doering C.J., and Zamponi G.W. Molecular pharmacology of high voltage-activated calcium channels. J. Bioenerg. Biomembr. 35 (2003) 491-505
21. Dolphin A.C. Mechanisms of modulation of voltage-dependent calcium channels by G-proteins. J. Physiol. 506 (1998) 3-11
22. Dove L.S., Abbott L.C., and Griffith W.H. Whole-cell and single-channel analysis of P-type calcium currents in cerebellar Purkinje cells of leaner mutant mice. J. Neurosci. 18 (1998) 7687-7699
23. Dove L.S., Nahm S.S., Murchison D., Abbott L.C., and Griffith W.H. Altered calcium homeostasis in cerebellar Purkinje cells of leaner mutant mice. J. Neurophysiol. 84 (2000) 513-524
24. 2+ channels in mammalian central neurons. Trends Neurosci. 18 (1995) 89-98
25. Duque A., Balatoni B., Detari L., and Zaborszky L. EEG correlation of the discharge properties of identified neurons in the basal forebrain. J. Neurophysiol. 84 (2000) 1627-1635
26. Ertel E.A., Campbell K.P., Harpold M.M., Hofmann F., Mori Y., Perez-Reyes E., Schwartz A., Snutch T.P., Tanabe T., Birnbaumer L., Tsien R.W., and Catterall W.A. Nomenclature of voltage-gated calcium channels. Neuron 25 (2000) 533-535
27. Everitt B.J., and Robbins T.W. Central cholinergic systems and cognition. Annu. Rev. Psychol. 48 (1997) 649-684
28. Fletcher C.F., Lutz C.M., O'Sullivan T.N., Shaughnessy Jr. J.D., Hawkes R., Frankel W.N., Copeland N.G., and Jenkins N.A. Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell 87 (1996) 607-617
29. 2+ channelopathies. J. Bioenerg. Biomembr. 35 (2003) 697-718
30. Gibson G.E., and Peterson C. Calcium and the aging nervous system. Neurobiol. Aging 8 (1987) 329-343
31. Ginty D.D. Calcium regulation of gene expression: isn't that spatial. Neuron 18 (1997) 183-186
32. Griffith W.H. Membrane properties of cell types within guinea pig basal forebrain nuclei in vitro. J. Neurophysiol. 59 (1988) 1590-1612
33. Griffith W.H., Taylor L., and Davis M.J. Whole-cell and single-channel calcium currents in guinea pig basal forebrain neurons. J. Neurophysiol. 71 (1994) 2359-2376
34. Griffith W.H., Jasek M.C., Bain S.H., and Murchison D. Modification of ion channels and calcium homeostasis of basal forebrain neurons during aging. Behav. Brain Res. 115 (2000) 219-233
35. Gritti I., Mainville L., Mancia M., and Jones B.E. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J. Comp. Neurol. 383 (1997) 163-177
36. Han, S.H., 2002. Molecular and functional diversity of basal forebrain neurons during aging, Dissertation, Texas A and M University.
37. Han S.H., McCool B.A., Murchison D., Nahm S.S., Parrish A.R., and Griffith W.H. Single-cell RT-PCR detects shifts in mRNA expression profiles of basal forebrain neurons during aging. Mol. Brain Res. 98 (2002) 67-80
38. Han S.H., Murchison D., and Griffith W.H. Low voltage-activated calcium and fast tetrodotoxin-resistant sodium currents define subtypes of cholinergic and noncholinergic neurons in rat basal forebrain. Mol. Brain Res. 134 (2005) 226-238
39. Heintz N., and Zoghbi H.Y. Insights from mouse models into the molecular basis of neurodegeneration. Annu. Rev. Physiol. 62 (2000) 779-802
40. Hell J.W., Westenbroek R.E., Warner C., Ahlijanian M.K., Prystay W., Gilbert M.M., Snutch T.P., and Catterall W.A. Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits. J. Cell Biol. 123 (1993) 949-962
41. 2+ channel subunit mRNA expression in the hippocampus of aged F344 rats. Neurobiol. Aging 19 (1998) 581-587
42. 2+ channels. Neuron 9 (1992) 69-77
43. Iwamoto M., Hagishita T., Shoji-Kasai Y., Ando S., and Tanaka Y. Age-related changes in the levels of voltage-dependent calcium channels and other synaptic proteins in rat brain cortices. Neurosci. Lett. 366 (2004) 277-281
44. Jen J., and Geschwind D.H. Ataxia and calcium channels: what a headache. Arch. Neurol. 58 (2001) 179-180
45. 1A subunit. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 15245-15250
46. Karst H., Nair S., Velzing E., Rumpff-van Essen L., Slagter E., Shinnick-Gallagher P., and Joels M. Glucocorticoids alter calcium conductances and calcium channel subunit expression in basolateral amygdala neurons. Eur. J. Neurosci. 16 (2002) 1083-1089
47. 2+ for drug development: chronic nicotine treatment upregulates L-type high voltage-gated calcium channels. J. Pharmacol. Sci. 97 (2005) 344-347
48. Katsura M., Mohri Y., Shuto K., Hai-Du Y., Amano T., Tsujimura A., Sasa M., and Ohkuma S. Up-regulation of L-type voltage-dependent calcium channels after long term exposure to nicotine in cerebral cortical neurons. J. Biol. Chem. 277 (2002) 7979-7988
49. Khachaturian Z.S. Calcium hypothesis of Alzheimer's disease and brain aging. Ann. N. Y. Acad. Sci. 747 (1994) 1-11
50. Landfield P.W. Increased calcium-current hypothesis of brain aging. Neurobiol. Aging 8 (1987) 346-347
51. Lau F.C., Abbott L.C., Rhyu I.J., Kim D.S., and Chin H. Expression of calcium channel alpha1A mRNA and protein in the leaner mouse (tgla/tgla) cerebellum. Mol. Brain Res. 59 (1998) 93-99
52. Lipscombe D., Helton T.D., and Xu W. L-type calcium channels: the low down. J. Neurophysiol. 92 (2004) 2633-2641
53. 2+-channels. Eur. J. Neurosci. 15 (2002) 13-18
54. Lorenzon N.M., Lutz C.M., Frankel W.N., and Beam K.G. Altered calcium channel currents in Purkinje cells of the neurological mutant mouse leaner. J. Neurosci. 18 (1998) 4482-4489
55. Manns I.D., Alonso A., and Jones B.E. Discharge properties of juxtacellularly labeled and immunohistochemically identified cholinergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J. Neurosci. 20 (2000) 9252-9263
56. 2+ channels in hippocampal neurons. Nature 395 (1998) 900-905
57. Matsushita K., Wakamori M., Rhyu I.J., Arii T., Oda S., Mori Y., and Imoto K. Bidirectional alterations in cerebellar synaptic transmission of tottering and rolling Ca2+ channel mutant mice. J. Neurosci. 22 (2002) 4388-4398
58. McDonough S.I., Swartz K.J., Mintz I.M., Boland L.M., and Bean B.P. Inhibition of calcium channels in rat central and peripheral neurons by omega-conotoxin MVIIC. J. Neurosci. 16 (1996) 2612-2623
59. McRory J.E., Santi C.M., Hamming K.S., Mezeyova J., Sutton K.G., Baillie D.L., Stea A., and Snutch T.P. Molecular and functional characterization of a family of rat brain T-type calcium channels. J. Biol. Chem. 276 (2001) 3999-4011
60. Mintz I.M., Adams M.E., and Bean B.P. P-type calcium channels in central and peripheral neurons. Neuron 9 (1992) 85-95
61. Mermelstein P.G., Bito H., Deisseroth K., and Tsien R.W. Critical dependence of cAMP response element-binding protein phosphorylation on L-type calcium channels supports a selective response to EPSPs in preference to action potentials. J. Neurosci. 20 (2000) 266-273
62. Mori Y., Friedrich T., Kim M.S., Mikami A., Nakai J., Ruth P., Bosse E., Hofmann F., Flockerzi V., Furuichi T., et al. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature 350 (1991) 398-402
63. Morris N.P., Harris S.J., and Henderson Z. Parvalbumin-immunoreactive, fast-spiking neurons in the medial septum/diagonal band complex of the rat: intracellular recordings in vitro. Neuroscience 92 (1999) 589-600
64. Moyer Jr. J.R., and Disterhoft J.F. Nimodipine decreases calcium action potentials in rabbit hippocampal CA1 neurons in an age-dependent and concentration-dependent manner. Hippocampus 4 (1994) 11-17
65. Murchison D., and Griffith W.H. Low-voltage activated calcium currents increase in basal forebrain neurons from aged rats. J. Neurophysiol. 74 (1995) 876-887
66. Murchison D., and Griffith W.H. High-voltage-activated calcium currents in basal forebrain neurons during aging. J. Neurophysiol. 76 (1996) 158-174
67. Murchison D., and Griffith W.H. Increased calcium buffering in basal forebrain neurons during aging. J. Neurophysiol. 80 (1998) 350-364
68. 2+ signaling functions in Purkinje neurons in the leaner mutant mouse. Cerebellum 1 (2002) 119-127
69. Nahm S.S., Jung K.Y., Enger M.K., Griffith W.H., and Abbott L.C. Differential expression of T-type calcium channels in P/Q-type calcium channel mutant mice with ataxia and absence epilepsy. J. Neurobiol. 62 (2005) 352-360
70. 1D subunit in postnatal pancreatic β cell generation. J. Clin. Invest. 108 (2001) 1015-1022
71. 2+ channels. J. Neurosci. 18 (1998) 3171-3179
72. Olson P.A., Tkatch T., Hernandez-Lopez S., Ulrich S., Ilijic E., Mugnaini E., Zhang H., Bezprozvanny I., and Surmeier D.J. G-protein-coupled receptor modulation of striatal CaV1.3 L-type Ca2+ channels is dependent on a Shank-binding domain. J. Neurosci. 25 (2005) 1050-1062
73. 2+ channel gene CACNL1A4. Cell 87 (1996) 543-552
74. Palmer A.M. Pharmacotherapy for Alzheimer's disease: progress and prospects. Trends Neurosci. 23 (2002) 426-433
75. Panula P., Revuelta A.V., Cheney D.L., Wu J.Y., and Costa E. An immunohistochemical study on the location of GABAergic neurons in rat septum. J. Comp. Neurol. 222 (1984) 69-80
76. Perez-Reyes E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol. Rev. 83 (2003) 117-161
77. 2+-dependent inactivation of L-type calcium channels. Neuron 22 (1999) 549-558
78. Pietrobon D. Calcium channels and channelopathies of the central nervous system. Mol. Neurobiol. 25 (2002) 31-50
79. 2+ channel subunit mutations. J. Neurosci. 20 (2000) 163-170
80. Rasmusson D.D. The role of acetylcholine in cortical synaptic plasticity. Behav. Brain Res. 115 (2000) 205-218
81. Rizzuto R., and Pozzan T. When calcium goes wrong: genetic alterations of a ubiquitous signaling route. Nat. Genet. 34 (2003) 135-141
82. Sarter M., and Bruno J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95 (2000) 933-952
83. Schjott J.M., Hsu S.C., and Plummer M.R. The neuronal beta 4 subunit increases the unitary conductance of L-type voltage-gated calcium channels in PC12 cells. J. Biol. Chem. 278 (2003) 33936-33942
84. Shinnick-Gallagher P., McKernan M.G., Xie J., and Zinebi F. L-type voltage-gated calcium channels are involved in the in vivo and in vitro expression of fear conditioning. Ann. N. Y. Acad. Sci. 985 (2003) 135-149
85. + current in mouse neocortical pyramidal neurons. J. Neurosci. 23 (2003) 3639-3648
86. Talley E.M., Cribbs L.L., Lee J.H., Daud A., Perez-Reyes E., and Bayliss D.A. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J. Neurosci. 19 (1999) 1895-1911
87. Terwindt G.M., Ophoff R.A., Haan J., Frants R.R., and Ferrari M.D. Familial hemiplegic migraine: a clinical comparison of families linked and unlinked to chromosome 19. Cephalgia 16 (1996) 153-155
88. Thibault O., and Landfield P.W. Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272 (1996) 1017-1020
89. i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J. Neurosci. 21 (2001) 9744-9756
90. Tkatch T., Baranauskas G., and Surmeier D.J. Basal forebrain neurons adjacent to the globus pallidus co-express GABAergic and cholinergic marker mRNAs. Neuroreport 9 (1998) 1935-1939
91. 2+ regulation and gene expression in normal brain aging. Trends Neurosci. 27 (2004) 614-620
92. 2+ channels. Trends Pharmacol. Sci. 12 (1991) 349-354
93. V1.3) of L-type calcium channels in the hippocampus of aged rats. Mol. Brain Res. 107 (2002) 120-127
94. V1.3) in area CA1 of the hippocampus and both are ameliorated by chronic nimodipine treatment. Mol. Brain Res. 110 (2003) 193-202
95. Verkhratsky A., and Toescu E.C. Calcium and neuronal aging. Trends Neurosci. 21 (1998) 2-7
96. Wakamori M., Yamazaki K., Matsunodaira H., Teramoto T., Tanaka I., Niidome T., Sawada K., Nishizawa Y., Sekiguchi N., Mori E., Mori Y., and Imoto K. Single tottering mutations responsible for the neuropathic phenotype of the P-type calcium channel. J. Biol. Chem. 273 (1998) 34857-34867
97. Wheeler D.B., Randall A., Sather W.A., and Tsien R.W. Neuronal calcium channels encoded by the alpha 1A subunit and their contribution to excitatory synaptic transmission in the CNS. Prog. Brain Res. 105 (1995) 65-78
98. Whitehouse P.J., Price D.L., Clark A.W., Coyle J.T., and DeLong M.R. Alzheimer's disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann. Neurol. 10 (1981) 122-126
99. Williams S., Souchelnytskyi S., and Danik M. TGFbeta2 mediates rapid inhibition of calcium influx in identified cholinergic basal forebrain neurons. Biochem. Biophys. Res. Commun. 290 (2002) 1321-1327
100. V1.2-deficient mice. J. Biol. Chem. 278 (2003) 40837-40841
101. Zhang Y., Mori M., Burgess D.L., and Noebels J.L. Mutations in high-voltage-activated calcium channel genes stimulate low-voltage-activated currents in mouse thalamic relay neurons. J. Neurosci. 22 (2002) 6362-6371
102. 2+ channel-mutant mouse, tottering. J. Physiol. 547 (2003) 497-507
103. Zhuchenko O., Bailey J., Bonnen P., Ashizawa T., Stockton D.W., Amos C., Dobyns W.B., Subramony S.H., Zoghbi H.Y., and Lee C.C. Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the α1A-voltage-dependent calcium channel. Nat. Genet. 15 (1997) 62-69
104. Zuhlke R.D., Pitt G.S., Deisseroth K., Tsien R.W., and Reuter H. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature 399 (1999) 159-162