Impaired motor function in mice with cell-specific knockout of sodium channel Scn8a (NaV1.6) in cerebellar Purkinje neurons and granule cells

Journal of Neurophysiology

Volumn 96, Issue 2, 2006, Pages 785-793

  Levin, Stephen I ^a   Khaliq, Zayd M ^b   Aman, Teresa K ^b   Grieco, Tina M ^b   Kearney, Jennifer A ^a   Raman, Indira M ^b   Meisler, Miriam H ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ATAXIA; CEREBELLUM; CONTROLLED STUDY; EXON; EXPERIMENTAL MODEL; GENE; GENE EXPRESSION; GRANULE CELL; HISTOLOGY; LOCOMOTION; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; MUTATION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCN8A GENE; SOUTHERN BLOTTING; SYNAPSE; TREMOR;

ACTION POTENTIALS; ALLELES; ANIMALS; ATAXIA; BLOTTING, SOUTHERN; CEREBELLUM; CYTOPLASMIC GRANULES; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; EXONS; MICE; MICE, KNOCKOUT; MUTATION; NERVE FIBERS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PSYCHOMOTOR PERFORMANCE; PURKINJE CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SODIUM CHANNELS; SYNAPSES;

EID: 33746613637     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01193.2005     Document Type: Article

References (54)

1. Afshari FS, Ptak K, Khaliq ZM, Grieco TM, Slater NT, McCrimmon DR, and Raman IM. Resurgent Na currents in four classes of neurons of the cerebellum. J Neurophysiol 92: 2831-2843, 2004.
2. Aller MI, Jones A, Merlo D, Paterlini M, Meyer AH, Amtmann U, Brickley S, Jolin HE, McKenzie AN, Monyer H, Farrant M, and Wisden W. Cerebellar granule cell Cre recombinase expression. Genesis 36: 97-103, 2003.
3. Altman J and Bayer SA. Development of the Cerebellar System: In Relation to its Evolution, structure, and Functions. Boca Raton, FL: CRC, 1997.
4. Aman TK and Raman IM. Differential regulation of Na channel availability by long-lived inactivated states in Purkinje and cerebellar nuclear neurons. Soc Neurosci Abstr 151.6, 2005.
5. Barski JJ, Dethleffsen K, and Meyer M. Cre recombinase expression in cerebellar Purkinje cells. Genesis 28: 93-98, 2000.
6. Boiko T, Rasband MN, Levinson SR, Caldwell JH, Mandel G, Trimmer JS, and Matthews G. Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron 30: 91-104, 2001.
7. Boiko T, Van Wart A, Caldwell JH, Levinson SR, Trimmer JS, and Matthews G. Functional specialization of the axon initial segment by isoform-specific sodium channel targeting. J Neurosci 23: 2306-2313, 2003.
8. Burgess DL, Kohrman DC, Galt J, Plummer NW, Jones JM, Spear B, and Meisler MH. Mutation of a new sodium channel gene, Scn8a, in the mouse mutant "motor endplate disease." Nat Genet 10: 461-465, 1995.
9. Caldwell JH, Schaller KL, Lasher RS, Peles E, and Levinson SR. Sodium channel Na(v)1.6 is localized at nodes of ranvier, dendrites, and synapses. Proc Natl Acad Sci USA 97: 5616-5620, 2000.
10. Chadderton P, Margrie TW, and Hausser M. Integration of quanta in cerebellar granule cells during sensory processing. Nature 428: 856-860, 2004.
11. Clark HB, Burright EN, Yunis WS, Larson S, Wilcox C, Hartman B, Matilla A, Zoghbi HY, and Orr HT. Purkinje cell expression of a mutant allele of SCA1 in transgenic mice leads to disparate effects on motor behaviors, followed by a progressive cerebellar dysfunction and histological alterations. J Neurosci 17: 7385-7395, 1997.
12. Crawley JN. What's Wrong With My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice. New York: Wiley-Liss, 2000.
13. Dick DJ, Boakes RJ, and Harris JB. A cerebellar abnormality in the mouse with motor end-plate disease. Neuropathol Appl Neurobiol 11: 141-147, 1985.
14. Dick DJ, Boakes RJ, Candy JM, Harris JB, and Cullen MJ. Cerebellar structure and function in the murine mutant "jolting." J Neurol Sci 76: 255-267, 1986.
15. Do MTH and Bean BP. Sodium currents in subthalamic nucleus neurons from Nav1.6-null mice. J Neurophysiol 92: 726-733, 2004.
16. Drews VL, Lieberman AP, and Meisler MH. Multiple transcripts of sodium channel SCN8A [Na(V)1.6] with alternative 5′- and 3′-untranslated regions and initial characterization of the SCN8A promoter. Genomics 85: 245-257, 2005.
17. Garin N, Hornung JP, and Escher G. Distribution of postsynaptic GABA(A) receptor aggregates in the deep cerebellar nuclei of normal and mutant mice. J Comp Neurol 447: 210-217, 2002.
18. Golowasch J, Abbott LF, and Marder E. Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis. J Neurosci 19: RC33, 1999.
19. Grieco TM, Afshari FS, and Raman IM. A role for phosphorylation in the maintenance of resurgent sodium current in cerebellar purkinje neurons. J Neurosci 22: 3100-3107, 2002.
20. Grieco TM and Raman IM. Production of resurgent current in NaV1.6-null Purkinje neurons by slowing sodium channel inactivation with beta-pompilidotoxin. J Neurosci 24: 35-42, 2004.
21. Grusser-Cornehls U and Baurle J. Mutant mice as a model for cerebellar ataxia. Prog Neurobiol 63: 489-540, 2001.
22. Hamann M, Meisler MH, and Richter A. Motor disturbances in mice with deficiency of the sodium channel gene Scn8a show features of human dystonia. Exp Neurol 2003.
23. Harris JB, Boakes RJ, and Court JA. Physiological and biochemical studies on the cerebellar cortex of the murine mutants "jolting" and "motor endplate disease." J Neurol Sci 110: 186-194, 1992.
24. Hartmann MJ and Bower JM. Tactile responses in the granule cell layer of cerebellar folium crus IIa of freely behaving rats. J Neurosci 21: 3549-3563, 2001.
25. Herculano-Houzel S and Lent R. Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J Neurosci 25: 2518-2521, 2005.
26. Ito M. Mechanisms of motor learning in the cerebellum. Brain Research 886:237-245, 2000.
27. Kearney JA, Buchner DA, De Haan G, Adamska M, Levin SI, Furay AR, Albin RL, Jones JM, Montal M, Stevens MJ, Sprunger LK, and Meisler MH. Molecular and pathological effects of a modifier gene on deficiency of the sodium channel Scn8a [Na(v)1.6]. Hum Mol Genet 11: 2765-2775, 2002.
28. Khaliq ZM, Gouwens NW, and Raman IM. The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J Neurosci 23: 4899-4912, 2003.
29. Khaliq ZM and Raman IM. Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J Neurosci 25: 454-463, 2005.
30. Khaliq ZM and Raman IM. Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J Neurosci 26: 1935-1944, 2006.
31. Kreitzer AC and Regehr WG. Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21: RC174, 2001.
32. Levin SI and Meisler MH. Floxed allele for conditional inactivation of the voltage-gated sodium channel Scn8a [Na(v)1.6]. Genesis 39: 234-239, 2004.
33. 2+ transients. Neuron 15: 407-415, 1995.
34. Linnemann C, Sultan F, Pedroarena CM, Schwarz C, and Thier P. Lurcher mice exhibit potentiation of GABA(A)-receptor-mediated conductance in cerebellar nuclei neurons in close temporal relationship to Purkinje cell death. J Neurophysiol 91: 1102-1107, 2004.
35. McCormick DA, Steinmetz JE, and Thompson RF. Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Res 359: 120-130, 1985.
36. Medina JF and Mauk MD. Simulations of cerebellar motor learning: computational analysis of plasticity at the mossy fiber to deep nucleus synapse. J Neurosci 19: 7140-7151, 1999.
37. Medina JF, Nores WL, and Mauk MD. Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416: 330-333, 2002.
38. Meisler MH and Kearney JA. Sodium channel mutations in epilepsy and other neurological disorders. J Clin Invest 115: 2010-2017, 2005.
39. Meisler MH, Plummer NW, Burgess DL, Buchner DA, and Sprunger LK. Allelic mutations of the sodium channel SCN8A reveal multiple cellular and physiological functions. Genetica 122: 37-45, 2004.
40. Planells-Cases R, Caprini M, Zhang J, Rockenstein EM, Rivera RR, Murre C, Masliah E, and Montal M. Neuronal death and perinatal lethality in voltage-gated sodium channel alpha(II)-deficient mice. Biophys J 78: 2878-2891, 2000.
41. Raman IM and Bean BP. Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17: 4517-4526, 1997.
42. Raman IM and Bean BP. Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys J 80: 729-737, 2001.
43. Raman IM, Sprunger LK, Meisler MH, and Bean BP. Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19: 881-891, 1997.
44. Regan LJ. Voltage-dependent calcium currents in Purkinje cells from rat cerebellar vermis. J Neurosci 11: 2259-2269, 1991.
45. Schaller KL and Caldwell JH. Developmental and regional expression of sodium channel isoform NaCh6 in the rat central nervous system. J Comp Neurol 420: 84-97, 2000.
46. Schaller KL and Caldwell JH. Expression and distribution of voltage-gated sodium channels in the cerebellum. Cerebellum 2: 2-9, 2003.
47. Shakkottai VG, Chou CH, Oddo S, Sailer CA, Knaus HG, Gutman GA, Barish ME, LaFerla FM, and Chandy KG. Enhanced neuronal excitability in the absence of neurodegeneration induces cerebellar ataxia. J Clin Invest 113: 582-590, 2004.
48. Smith MR, Smith RD, Plummer NW, Meisler MH, and Goldin AL. Functional analysis of the mouse Scn8a sodium channel. J Neurosci 18: 6093-6102, 1998.
49. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71, 1999.
50. Sprunger LK, Escayg A, Tallaksen-Greene S, Albin RL, and Meisler MH. Dystonia associated with mutation of the neuronal sodium channel Scn8a and identification of the modifier locus Scnm1 on mouse chromosome 3. Hum Mol Genet 8: 471-479, 1999.
51. Thompson RF. The neurobiology of learning and memory. Science 233: 941-947, 1986.
52. Walter JT, Alvina K, Womack MD, Chevez C, and Khodakhah K. Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 9: 389-397, 2006.
53. Yu FH, Mantegazza M, Westenbroek RE, Robbins CA, Spain WJ, Burton KA, McKnight GS, Scheuer T, and Catterall WA. Deletion of the NaV1.1 channel: a mouse model for severe myoclonic epilepsy of infancy. Soc Neurosci Abstr 479.5, 2004.
54. Zhao L, Bakke M, Krimkevich Y, Cushman LJ, Parlow AF, Camper SA, and Parker KL. Steroidogenic factor 1 (SF1) is essential for pituitary gonadotrope function. Development 128: 147-154, 2001.