Expression of L-type calcium channel α1-1.2 and α1-1.3 subunits on rat sacral motoneurons following chronic spinal cord injury

Neuroscience

Volumn 145, Issue 2, 2007, Pages 751-763

  Anelli, R ^a   Sanelli, L ^b   Bennett, D J ^b   Heckman, C J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

3 D image analysis; fluorescence intensity; histochemistry; neurofilament H

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL L TYPE 1.2; CALCIUM CHANNEL L TYPE 1.3; PROTEIN SUBUNIT; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ALPHA CHAIN; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CONTROLLED STUDY; MONOAMINERGIC SYSTEM; NERVE CELL EXCITABILITY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SACRAL SPINAL CORD; SPINAL CORD INJURY; SPINAL CORD MOTONEURON; THORACIC SPINAL CORD; WHITE MATTER;

ANIMALS; BIOGENIC MONOAMINES; CALCIUM CHANNELS; CALCIUM CHANNELS, L-TYPE; CHRONIC DISEASE; EFFERENT PATHWAYS; FEMALE; MEMBRANE POTENTIALS; MOTOR NEURONS; PROTEIN SUBUNITS; RATS; SACRUM; SPINAL CORD INJURIES; UP-REGULATION;

EID: 33847667598     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.12.043     Document Type: Article

References (85)

1. Abe Y., Yamamoto T., Sugiyama Y., Watanabe T., Saito N., Kayama H., and Kumagai T. Apoptotic cells associated with Wallerian degeneration after experimental spinal cord injury: a possible mechanism of oligodendroglial death. J Neurotrauma 16 (1999) 945-952
2. Alaburda A., Perrier J.F., and Hounsgaard J. Mechanisms causing plateau potentials in spinal motoneurones. Adv Exp Med Biol 508 (2002) 219-226
3. Ambalavanar R., and Morris R. Fluoro-Gold injected either subcutaneously or intravascularly results in extensive retrograde labelling of CNS neurones having axons terminating outside the blood-brain barrier. Brain Res 505 (1989) 171-175
4. Anderson C.R., and Edwards S.L. Intraperitoneal injections of Fluorogold reliably labels all sympathetic preganglionic neurons in the rat. J Neurosci Methods 53 (1994) 137-141
5. Anelli R., and Heckman C.J. The calcium binding proteins calbindin, parvalbumin, and calretinin have specific patterns of expression in the gray matter of cat spinal cord. J Neurocytol 34 (2005) 369-385
6. Atlas D., and Melamed E. Direct mapping of beta-adrenergic receptors in the rat central nervous system by a novel fluorescent beta-blocker. Brain Res 150 (1978) 377-385
7. Ballou E.W., Smith W.B., Anelli R., and Heckman C.J. Measuring dendritic distribution of membrane proteins. J Neurosci Methods 156 (2006) 257-266
8. Bar-Peled O., Knudson M., Korsmeyer S.J., and Rothstein J.D. Motor neuron degeneration is attenuated in bax-deficient neurons in vitro. J Neurosci Res 55 (1999) 542-556
9. Beattie M.S., Farooqui A.A., and Bresnahan J.C. Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 17 (2000) 915-925
10. Beattie M.S., Li Q., and Bresnahan J.C. Cell death and plasticity after experimental spinal cord injury. Prog Brain Res 128 (2000) 9-21
11. Bennett D.J., Gorassini M., Fouad K., Sanelli L., Han Y., and Cheng J. Spasticity in rats with sacral spinal cord injury. J Neurotrauma 16 (1999) 69-84
12. Bennett D.J., Li Y., Harvey P.J., and Gorassini M. Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. J Neurophysiol 86 (2001) 1972-1982
13. Bennett D.J., Li Y., and Siu M. Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. J Neurophysiol 86 (2001) 1955-1971
14. Bennett D.J., Sanelli L., Cooke C.L., Harvey P.J., and Gorassini M.A. Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J Neurophysiol 91 (2004) 2247-2258
15. Bose P., Parmer R., Reier P.J., and Thompson F.J. Morphological changes of the soleus motoneuron pool in chronic midthoracic contused rats. Exp Neurol 191 (2005) 13-23
16. Brosenitsch T.A., Salgado-Commissariat D., Kunze D.L., and Katz D.M. A role for L-type calcium channels in developmental regulation of transmitter phenotype in primary sensory neurons. J Neurosci 18 (1998) 1047-1055
17. 2+ channels and anoxic injury in rat CNS white matter. J Neurophysiol 85 (2001) 900-911
18. Campbell D.B., and Hess E.J. L-type calcium channels contribute to the tottering mouse dystonic episodes. Mol Pharmacol 55 (1999) 23-31
19. Carlin K.P., Jones K.E., Jiang Z., Jordan L.M., and Brownstone R.M. Dendritic L-type calcium currents in mouse spinal motoneurons: implications for bistability. Eur J Neurosci 12 (2000) 1635-1646
20. Carriedo S.G., Yin H.Z., and Weiss J.H. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 16 (1996) 4069-4079
21. 2+ channels. Annu Rev Cell Dev Biol 16 (2000) 521-555
22. Catterall W.A., Perez-Reyes E., Snutch T.P., and Striessnig J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 57 (2005) 411-425
23. Chin H., Mock B., Kim H.L., Kim H., and Kozak C.A. The gene for the dihydropyridine-sensitive calcium channel alpha 2 subunit (CCHL2A) maps to the proximal region of mouse chromosome 5. Genomics 13 (1992) 1325-1327
24. Crow J.P., Calingasan N.Y., Chen J., Hill J.L., and Beal M.F. Manganese porphyrin given at symptom onset markedly extends survival of ALS mice. Ann Neurol 58 (2005) 258-265
25. Crowe M.J., Bresnahan J.C., Shuman S.L., Masters J.N., and Beattie M.S. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3 (1997) 73-76
26. Davare M.A., Horne M.C., and Hell J.W. Protein phosphatase 2A is associated with class C L-type calcium channels (Cav1.2) and antagonizes channel phosphorylation by cAMP-dependent protein kinase. J Biol Chem 275 (2000) 39710-39717
27. Day M., Olson P.A., Platzer J., Striessnig J., and Surmeier D.J. 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 (2002) 2490-2504
28. Dobremez E., Bouali-Benazzouz R., Fossat P., Monteils L., Dulluc J., Nagy F., and Landry M. Distribution and regulation of L-type calcium channels in deep dorsal horn neurons after sciatic nerve injury in rats. Eur J Neurosci 21 (2005) 3321-3333
29. Dong H., Fazzaro A., Xiang C., Korsmeyer S.J., Jacquin M.F., and McDonald J.W. Enhanced oligodendrocyte survival after spinal cord injury in Bax-deficient mice and mice with delayed Wallerian degeneration. J Neurosci 23 (2003) 8682-8691
30. Ehlers M.D., and Augustine G.J. Cell signalling. Calmodulin at the channel gate. Nature 399 105 (1999) 107-108
31. 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
32. Gazula V.R., Roberts M., Luzzio C., Jawad A.F., and Kalb R.G. Effects of limb exercise after spinal cord injury on motor neuron dendrite structure. J Comp Neurol 476 (2004) 130-145
33. Gorassini M.A., Knash M.E., Harvey P.J., Bennett D.J., and Yang J.F. Role of motoneurons in the generation of muscle spasms after spinal cord injury. Brain 127 (2004) 2247-2258
34. Gray P.C., Johnson B.D., Westenbroek R.E., Hays L.G., Yates III J.R., Scheuer T., Catterall W.A., and Murphy B.J. Primary structure and function of an A kinase anchoring protein associated with calcium channels. Neuron 20 (1998) 1017-1026
35. Heckmann C.J., Gorassini M.A., and Bennett D.J. Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31 (2005) 135-156
36. Hulme J.T., Lin T.W., Westenbroek R.E., Scheuer T., and Catterall W.A. Beta-adrenergic regulation requires direct anchoring of PKA to cardiac CaV1.2 channels via a leucine zipper interaction with A kinase-anchoring protein 15. Proc Natl Acad Sci U S A 100 (2003) 13093-13098
37. Hultborn H. Plateau potentials and their role in regulating motoneuronal firing. Adv Exp Med Biol 508 (2002) 213-218
38. Jiang Z., Rempel J., Li J., Sawchuk M.A., Carlin K.P., and Brownstone R.M. Development of L-type calcium channels and a nifedipine-sensitive motor activity in the postnatal mouse spinal cord. Eur J Neurosci 11 (1999) 3481-3487
39. 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
40. Kasielke N., Obermair G.J., Kugler G., Grabner M., and Flucher B.E. Cardiac-type EC-coupling in dysgenic myotubes restored with Ca(2+) channel subunit isoforms alpha(1C) and alpha(1D) does not correlate with current density. Biophys J 84 (2003) 3816-3828
41. Kasim S., Egami K., and Jinnah H.A. Self-biting induced by activation of L-type calcium channels in mice: serotonergic influences. Dev Neurosci 24 (2002) 322-327
42. Keane R.W., Kraydieh S., Lotocki G., Bethea J.R., Krajewski S., Reed J.C., and Dietrich W.D. Apoptotic and anti-apoptotic mechanisms following spinal cord injury. J Neuropathol Exp Neurol 60 (2001) 422-429
43. Kitzman P. Alteration in axial motoneuronal morphology in the spinal cord injured spastic rat. Exp Neurol 192 (2005) 100-108
44. 2+ channels in the chicken's cochlea. Proc Natl Acad Sci U S A 94 (1997) 14889-14893
45. 2+ channels activating at negative voltages. J Biol Chem 276 (2001) 22100-22106
46. Kurnellas M.P., Nicot A., Shull G.E., and Elkabes S. Plasma membrane calcium ATPase deficiency causes neuronal pathology in the spinal cord: a potential mechanism for neurodegeneration in multiple sclerosis and spinal cord injury. FASEB J 19 (2005) 298-300
47. Lautrette C., Giraud S., Vermot-Desroches C., Preud'homme J.L., and Jauberteau M.O. Expression of a functional Fas death receptor by human foetal motoneurons. Neuroscience 119 (2003) 377-385
48. Lee R.H., and Heckman C.J. Paradoxical effect of QX-314 on persistent inward currents and bistable behavior in spinal motoneurons in vivo. J Neurophysiol 82 (1999) 2518-2527
49. Leong S.K., and Ling E.A. Labelling neurons with fluorescent dyes administered via intravenous, subcutaneous or intraperitoneal route. J Neurosci Methods 32 (1990) 15-23
50. Li Y., and Bennett D.J. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90 (2003) 857-869
51. Li Y., Gorassini M.A., and Bennett D.J. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91 (2004) 767-783
52. Li Y., Harvey P.J., Li X., and Bennett D.J. Spastic long-lasting reflexes of the chronic spinal rat studied in vitro. J Neurophysiol 91 (2004) 2236-2246
53. Liu X.Z., Xu X.M., Hu R., Du C., Zhang S.X., McDonald J.W., Dong H.X., Wu Y.J., Fan G.S., Jacquin M.F., Hsu C.Y., and Choi D.W. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 17 (1997) 5395-5406
54. Maekawa S., Al-Sarraj S., Kibble M., Landau S., Parnavelas J., Cotter D., Everall I., and Leigh P.N. Cortical selective vulnerability in motor neuron disease: a morphometric study. Brain 127 (2004) 1237-1251
55. Melamed E., Luhar M., and Atlas D. Histochemical labeling of beta-adrenergic receptors in the mouse central nervous system by 9-amino-acridin propranolol. Neurology 28 (1978) 850-853
56. 2+ currents in rat thalamocortical relay neurons by activity and phosphorylation. Eur J Neurosci 15 (2002) 1603-1614
57. 2+ channels. Trends Neurosci 24 (2001) 445-449
58. Newton B.W., and Hamill R.W. Immunohistochemical distribution of serotonin in spinal autonomic nuclei: I. Fiber patterns in the adult rat. J Comp Neurol 279 (1989) 68-81
59. Oh S.B., Piao Z.G., Shin S.S., Ren D., Park K., and Kim J.S. GABAergic and serotonergic modulation of calcium currents in rat trigeminal motoneurons. Biochem Biophys Res Commun 309 (2003) 58-65
60. Park E., Velumian A.A., and Fehlings M.G. The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. J Neurotrauma 21 (2004) 754-774
61. 2+ channels. Brain Res Brain Res Rev 40 (2002) 223-229
62. Perrier J.F., and Hounsgaard J. Development and regulation of response properties in spinal cord motoneurons. Brain Res Bull 53 (2000) 529-535
63. Powers R.K., and Binder M.D. Input-output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143 (2001) 137-263
64. Rekling J.C., Funk G.D., Bayliss D.A., Dong X.W., and Feldman J.L. Synaptic control of motoneuronal excitability. Physiol Rev 80 (2000) 767-852
65. Ren K., and Ruda M.A. A comparative study of the calcium-binding proteins calbindin-D28K, calretinin, calmodulin and parvalbumin in the rat spinal cord. Brain Res Brain Res Rev 19 (1994) 163-179
66. Seino S., Chen L., Seino M., Blondel O., Takeda J., Johnson J.H., and Bell G.I. Cloning of the alpha 1 subunit of a voltage-dependent calcium channel expressed in pancreatic beta cells. Proc Natl Acad Sci U S A 89 (1992) 584-588
67. 2+ channels responsible for plateau potentials in motoneurons from the lumbar spinal cord of the turtle. Eur J Neurosci 18 (2003) 258-266
68. Snutch T.P., Leonard J.P., Gilbert M.M., Lester H.A., and Davidson N. Rat brain expresses a heterogeneous family of calcium channels. Proc Natl Acad Sci U S A 87 (1990) 3391-3395
69. 2+ channels: diversity of form and function. Curr Opin Neurobiol 2 (1992) 247-253
70. Snutch T.P., Tomlinson W.J., Leonard J.P., and Gilbert M.M. Distinct calcium channels are generated by alternative splicing and are differentially expressed in the mammalian CNS. Neuron 7 (1991) 45-57
71. Song X.Q., Wu S.Y., Li C.Y., Wang L.Q., and Wang X.J. [Effect of glia cell line-derived neurotrophic factor on cultured spinal motor neurons from embryonic rat]. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 19 (2003) 490-492
72. 2+ channelopathies. Biochem Biophys Res Commun 322 (2004) 1341-1346
73. Tomlinson W.J., Stea A., Bourinet E., Charnet P., Nargeot J., and Snutch T.P. Functional properties of a neuronal class C L-type calcium channel. Neuropharmacology 32 (1993) 1117-1126
74. Tsang Y.M., Chiong F., Kuznetsov D., Kasarskis E., and Geula C. Motor neurons are rich in non-phosphorylated neurofilaments: cross-species comparison and alterations in ALS. Brain Res 861 (2000) 45-58
75. Vandenberghe W., Robberecht W., and Brorson J.R. AMPA receptor calcium permeability, GluR2 expression, and selective motoneuron vulnerability. J Neurosci 20 (2000) 123-132
76. Vandenberghe W., Van Den Bosch L., and Robberecht W. Glial cells potentiate kainate-induced neuronal death in a motoneuron-enriched spinal coculture system. Brain Res 807 (1998) 1-10
77. Westenbroek R.E., Anderson N.L., and Byers M.R. Altered localization of Cav1.2 (L-type) calcium channels in nerve fibers, Schwann cells, odontoblasts, and fibroblasts of tooth pulp after tooth injury. J Neurosci Res 75 (2004) 371-383
78. 2+ channels in reactive astrocytes after brain injury, hypomyelination, and ischemia. J Neurosci 18 (1998) 2321-2334
79. 2+ channel subtypes on rat spinal motor neurons, interneurons, and nerve terminals. J Neurosci 18 (1998) 6319-6330
80. Williams M.E., Feldman D.H., McCue A.F., Brenner R., Velicelebi G., Ellis S.B., and Harpold M.M. Structure and functional expression of alpha 1, alpha 2, and beta subunits of a novel human neuronal calcium channel subtype. Neuron 8 (1992) 71-84
81. Xu W., and Lipscombe D. Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21 (2001) 5944-5951
82. Yi F.H., Lautrette C., Vermot-Desroches C., Bordessoule D., Couratier P., Wijdenes J., Preud'homme J.L., and Jauberteau M.O. In vitro induction of neuronal apoptosis by anti-Fas antibody-containing sera from amyotrophic lateral sclerosis patients. J Neuroimmunol 109 (2000) 211-220
83. Yong C., Arnold P.M., Zoubine M.N., Citron B.A., Watanabe I., Berman N.E., and Festoff B.W. Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J Neurotrauma 15 (1998) 459-472
84. 2+ channels and their possible counterparts in mammalian CNS neurons. Neuropharmacology 32 (1993) 1075-1088
85. 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