Co-treatment with riluzole, a neuroprotective drug, ameliorates the 3-acetylpyridine-induced neurotoxicity in cerebellar Purkinje neurones of rats: Behavioural and electrophysiological evidence

NeuroToxicology

Volumn 30, Issue 3, 2009, Pages 393-402

  Janahmadi, Mahyar ^a   Goudarzi, Iran ^b   Kaffashian, Mohammad Reza ^a   Behzadi, Gila ^a   Fathollahi, Yaqub ^b   Hajizadeh, Sohrab ^b  

^a SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TARBIAT MODARES UNIVERSITY   (Iran)

Author keywords

3 Acetylpyridine; AHP; Cerebellum; Neuroprotection; Neurotoxicity; Post train AHP; Purkinje cells; Riluzole

Indexed keywords

3 ACETYLPYRIDINE; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL; NEUROPROTECTIVE AGENT; NEUROTOXIN; POTASSIUM CHANNEL; RILUZOLE;

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL ACTIVITY; CEREBELLAR ATAXIA; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFECT; HISTOLOGY; HISTOPATHOLOGY; HYPERPOLARIZATION; IN VIVO STUDY; LOCOMOTION; MALE; MOTOR ACTIVITY; NERVE CELL DEGENERATION; NERVE POTENTIAL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PURKINJE CELL; RAT; REGULATORY MECHANISM; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; CEREBELLAR ATAXIA; CEREBELLUM; DRUG INTERACTIONS; MALE; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; NEUROTOXINS; PURKINJE CELLS; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RILUZOLE;

ANIMALIA; RATTUS;

EID: 67349201978     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2009.02.014     Document Type: Article

References (85)

1. Anderson W.A., and Flumerfelt B.A. A light and electron-microscopic study of the effects of 3-acetylpyridine intoxication on the inferior olivary complex and cerebellar cortex. J Comp Neurol 190 1 (1980) 157-174
2. Aubry A., Batini C., Billard J.M., Kado R.T., and Morain P. Tetrodotoxin induced calcium spikes in vitro and in vivo studies of normal and deafferented Purkinje cells. Exp Brain Res 84 2 (1991) 297-302
3. Balaban C.D. Central neurotoxic effects of intraperitoneally administered 3-acetylpyridine, harmaline and niacinamide in Sprague-Dawley and Long-Evans rats: a critical review of central 3-acetylpyridine neurotoxicity. Brain Rev 9 (1985) 21-42
4. Barlow J.B. The cerebellum and adaptive control (2002), Cambridge University Press, New York
5. Batini C., Billard J.M., and Daniel H. Long term modification of cerebellar inhibition after inferior olive degeneration. Exp Brain Res 59 (1985) 404-409
6. Beck H., and Yaari Y. Plasticity of intrinsic neuronal properties in CNS disorders. Nat Rev Neurosci 9 (2008) 357-369
7. Benedetti F., Montarolo P.G., and Rabacchi S. Inferior olive lesion induces long lasting functional modification of Purkinje cells. Exp Brain Res 55 (1984) 368-371
8. Bensimon G., Lacomblez L., and Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis ALS/Riluzole Study Group. N Engl J Med 330 (1994) 585-591
9. Benoit E., and Escande D. Riluzole specifically blocks inactivated Na channels in myelinated nerve fibre. Pflug Arch 419 (1991) 603-609
10. Bezard E., Stutzmann J.M., Imbert C., Boraud T., Boireau A., and Gross C.E. Riluzole delayed appearance of Parkinsonian motor abnormlities in a chronic MPTP monkey model. Eur J Pharmacol 356 (1998) 101-104
11. Billard J.M., and Daniel H. Persistent reduction of Purkinje cell inhibition on neurones of the cerebellar nuclei after climbing fi{ligature}ber deafferentation. Neurosci Lett 88 (1988) 21-26
12. Butterworth R.F. In: Boulton A., Baker G., and Butterworth R. (Eds). Neuromethods: animal models of neurological disease vol. I (1992), Humana Clifton, NJ 275-294
13. Campos-Torres A., Touret M., Vidal P.-P., Barnum S., and deWaele C. The differential response of astrocytes within the vestibular and cochlear nuclei following unilateral labyrinthectomy or vestibular afferent activity blockade by transtympanic tetrodotoxin injection in the rat. Neuroscience 130 (2005) 853-865
14. Cao Y.-J., Dreixler J.C., Couey J.J., and Houamed K.M. Modulation of recombinant and native neuronal SK channels by the neuroprotective drug riluzole. Eur J Pharmacol 449 (2002) 47-54
15. Cerminara N.L., and Rawson J.A. Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. J Neurosci 24 (2004) 4510-4517
16. Cheramy A., Barbeito L., GodeheuG, and Glowinski J. Riluzole inhibits the release of glutamate in the caudate nucleus of the cat in vivo. Neurosci Lett 147 (1992) 209-212
17. + channel expression and function in rat Purkinje neurons. J Neurosci 22 (2002) 4456-4467
18. Colin F., Manil J., and Desclin J.C. The olivocerebellar system. I. Delayed and slow inhibitory effects: an overlooked salient feature of cerebellar climbing fi{ligature}bers. Brain Res 187 (1980) 3-27
19. Dahhaoui M., Stelz T., and Caston J. Effects of lesion of the inferior olivary complex by 3-acetylpyridine on learning and memory in the rat. J Comp Physiol 171 (1992) 657-664
20. Davidson M., Zemishlany Z., Mohs R.C., Horvath T.B., Powchik P., Blass J.P., et al. 4-Aminopyridine in the treatment of Alzheimer's disease. Biol Psychiatry 23 5 (1988) 485-490
21. Desclin J.C., and Escubi J. Effects of 3-acetylpyridine on the central nervous system of the rat, as demonstrated by silver methods. Brain Res 77 (1974) 349-364
22. Desclin J.C., and Colin F. The olivocerebellar system. II. Some ultrastructural correlates of inferior olive destruction in the rat. Brain Res 187 (1980) 29-46
23. De Zeeuw C.I., Hansel C., Bian F., Koekkoek S.K., Van Alphen A.M., Linden D.J., et al. Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibule-ocular reflex. Neuron 20 (1998) 495-508
24. Deutsch A.Y., Elsworth J.D., Roth R.H., and Goldstein M. 3-Acetylpyridine results in degeneration of the extrapyramidal and cerebellar motor systems: loss of the dorsolateral striatal dopamine innervation. Brain Res 527 (1990) 96-102
25. Doble A. The role of excitotoxicity in neurodegenerative disease: implications for therapy. Pharmacol Ther 81 (1999) 163-221
26. + channels to rat Purkinje neuron function. J Physiol 548 (2003) 53-69
27. + current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol 493 (1996) 83-97
28. Fernandez A.M., de la Vega A.G., and Torres-Aleman I. Insulin-like growth factor I restores motor coordination in a rat model of cerebellar ataxia. Proc Natl Acad Sci 95 3 (1998) 1253-1258
29. Gasbarri A., Pompili A., Pacitti C., and Cicirata F. Comparative effects of lesions to the ponto-cerebellar and olivo-cerebellar pathways on motor and spatial learning in the rat. Neuroscience 116 (2003) 1131-1140
30. Glickstein M. Mossy-fiber sensory input to the cerebellum. Prog Brain Res 114 (1997) 251-259
31. Gollisch T., and Herz A.V.M. Input-driven components of spike-frequency adaptation can be unmasked in vivo. J Neurosci 24 34 (2004) 7435-7444
32. Grunnet M., Jespersen T., Angelo K., Frokjaer-Jensen C., Klaerke D.A., Olesen S.P., et al. Pharmacological modulation of SK3 channels. Neuropharmacology 40 (2001) 879-887
33. Guyot M.C., Palfi S., Stutzmann J.M., Maziere M., Hantraye P., and Brouillet E. Riluzole protects from motor deficits and striatal degeneration produced by systemic 3-nitropropionic acid intoxication in rats. Neuroscience 81 (1997) 141-149
34. + channels in the modulation of 4-aminopyridine-induced burst firing in rat cerebellar Purkinje cells. Brain Res 1156 (2007) 59-66
35. + (BK) channels regulate the spike configuration in the burst firing of cerebellar Purkinje neurons. Brain Res 1212 (2008) 1-8
36. Hallworth N.E., Wilson C.J., and Bevan M.D. Apamin sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. J Neurosci 23 (2003) 7525-7542
37. Hausser M., and Clark B.A. Tonic synaptic inhibition modulates nervous system neurons. Annu Rev Physiol 58 (1997) 329-348
38. Herbert T., Drapeau P., Pradier L., and Dunn R.J. Block of the rat brain IIA sodium channel alpha subunit by the neuroprotective drug riluzole. Mol Pharmacol 45 (1994) 1055-1060
39. Hoebeek F.E., Stahl J.S., van Alphen A.M., Schonewille M., and Luo C. Increased noise level of Purkinje cell activities minimizes impact of their modulation during sensorimotor control. Neuron 45 (2005) 953-965
40. Huang C.S., Song J.H., Nagata K., Yeh J.Z., and Narahashi T. Effects of the neuroprotective agent riluzole on the high voltage-activated calcium channels of rat dorsal root ganglion neurons. J Pharmacol Exp Ther 282 (1997) 1280-1290
41. Hubert T., and Doble A. Ibotenic acid stimulates D-(3H) aspartate release from cultured cerebellar granule cells. Neurosci Lett 96 (1989) 345-350
42. Ito M. The cerebellum and neural control (1984), Raven Press, New York
43. + channel in cultured rat cerebellar Purkinje neurons. Eur J Neurosci 11 (1999) 735-739
44. Jankovic J., and Hunter C. A double-blind, placebo-controlled and longitudinal study of riluzole in early Parkinson's disease. Parkinson Relat Disord 8 (2002) 271-276
45. Jehle T., Bauer J., Blauth E., Hummel A., Darstein M., Freiman T.M., et al. Effects of riluzole on electrically evoked neurotransmitter release. Br J Pharmacol 130 6 (2000) 1227-1234
46. Kado R.T., Batini C., and Morain P. Cerebellar Purkinje cells: membrane property changes on partial deafferentation. In: Mecanisms underlying long lasting changes in neuronal properties: fact and perspectives. Gif lectures in neurobiology. J Physiol (Paris) 83 (1989) 172-180
47. Kanthasamy A.G., Yun R.J., Nguyen B., and Truong D.D. Effect of riluzole on the neurological and neuropathological changes in an animal model of cardiac arrest-induced movement disorder. JPET 288 3 (1999) 1340-1348
48. + channels in rat brain: targeting to axons and nerve terminals. J Neurosci 16 (1996) 955-963
49. Lacomblez L., Bensimon G., Leigh P.N., Guillet P., and Meininger V. Dose-ranging study of riluzole in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis/Riluzole Study Group II. Lancet 347 (1996) 1425-1431
50. Lang-Lazdunski L., Heurteaux C., Mignon A., Mantz J., Widmann C., Desmonts J., et al. Ischemic spinal cord injury induced by aortic cross-clamping: prevention by riluzole. Eur J Cardiothorac Surg 18 (2000) 174-181
51. + channels. Annu Rev Physiol 51 (1989) 385-399
52. Llinás R., Walton K., Hillman D.E., and Sotelo C. Inferior olive: its role in motor learning. Science 190 (1975) 1230-1231
53. Lopiano L., and Savio T. Inferior olive lesion induces long-term mod-ifications of cerebellar inhibition of Deiters nuclei. Neurosci Res 4 (1986) 51-61
54. Malgouris C., Bardot F., Daniel M., Pellis F., Rataud J., Uzan A., et al. Riluzole, a novel antiglutamate, prevents memory loss and hippocampal neuronal damage in ischemic gerbils. J Neurosci 9 11 (1989) 3720-3727
55. Martin D., Thompson M.A., and Nadler J.V. The neuroprotective agent riluzole inhibits release of glutamate and aspartate from slices of hippocampal area CA1. Eur J Pharmacol 250 (1993) 473-476
56. McKay B.E., Engbers J.D.T., Mehaffey W.H., Gordon G.R.J., Molineux M.L., Bains J.S., et al. Climbing fiber discharge regulates cerebellar function by controlling the intrinsic characteristics of Purkinje cell output. J Neurolphysiol 97 (2007) 2590-2604
57. McKee P., Fuller G.N., and Stevens D.L. Riluzole in amyotrophic lateral sclerosis. N Engl J Med 331 4 (1994) 273-274
58. Montarolo P.G., Palestini M., and Strata P. The inhibitory effect of the olivocerebellar input on the cerebellar Purkinje cells in the rat. J Physiol (Lond) 332 (1982) 187-202
59. Morain P., Kado R.T., and Batini C. Electrophysiological effect of partial deafferentation in the rat cerebellar Purkinje cell. Exp Brain Res Ser 17 (1989) 231-234
60. Murphy M.G., and O'Leary J.L. Neurological deficit in cats with lesions of the olivocerebellar system. Arch Neurol 24 (1971) 145-157
61. Noh K.-M., Hwang J.-Y., Shin H.-C., and Koh J.-Y. A novel neuroprotective mechanism of riluzole: direct inhibition of protein kinase C. Neurobiol Dis 7 4 (2000) 375-383
62. Obinu M.C., Reibaud M., Blanchard V., Moussaoui S., and Imperato A. Neuroprotective effect of riluzole in a primate model of Parkinson's disease: behavioural and histological evidence. Mov Disord 17 (2002) 13-19
63. O'Hearn E., and Mollier M.K. The olivocerebellar projection mediates ibogaine-induced degeneration of Purkinje cells: a model of indirect, trance-synaptic excitotoxicity. J Neurosci 17 22 (1997) 8828-8841
64. Roman I.M., and Bean B.P. Ionic currents underlying spontaneous action potentials n isolated cerebellar Purkinje neurons. J Neurosci 19 (1999) 1663-1674
65. Rossi F., Cantino D., and Strata P. Morphology of Purkinje cell axon terminals in intracerebellar nuclei following inferior olive lesion. Neuroscience 22 1 (1987) 99-112
66. Sacco T., Bruno A., Wanke E., and Tempia F. Functional roles of an ERG current isolated in cerebellar Purkinje neurons. J Neurophysiol 90 (2003) 1817-1828
67. + channel deficiency. PNAS 101 (2004) 9474-9478
68. Seoane A., Apps R., Balbuena E., Herrero L., and Llorens J. Differential effects of trans-crotononitrile and 3-acetylpyridine on inferior olive integrity and behavioural performance in the rat. Eur J Neurosci 22 (2005) 880-894
69. Simpson J.I., Wylie D.R., and De Zeeuw C.I. On climbing fiber signals and their consequence(s). Behav Brain Sci 19 3 (1996) 384-398
70. Siniscalchi A., Bonci A., Mercuri N.B., and Bernardi G. Effects of riluzole on rat cortical neurones: an in vitro electrophysiological study. Br J Pharmacol 120 (1997) 225-230
71. Stefani A., Spadoni F., and Bernardi G. Differential inhibition by riluzole, lamotrigine, and phenytoin of sodium and calcium currents in cortical neurons: implications for neuroprotective strategies. Exp Neurol 147 (1997) 115-122
72. Stefoski D., Davis F.A., Fitzsimmons W.E., Luskin S.S., Rush J., and Parkhurst G.W. 4-Aminopyridine in multiple sclerosis: prolonged administration. Neurology 41 9 (1991) 1344-1348
73. + channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol Cell Neurosci 15 (2000) 476-493
74. Stone T.W. Neuropharmacology of quinolinic and kynurenic acids. Pharmacol Rev 45 (1993) 309-379
75. Strupp M., Kalla R., Dichgans M., Freilinger T., Glasauer S., and Brandt T. Treatment of episodic ataxia type 2 with the potassium channel blocker 4-aminopyridine. Neurology 62 9 (2004) 1623-1625
76. Strupp M., Zwergala A., and Brandta T. Episodic ataxia type 2. Neurotherapeutics 4 2 (2007) 267-273
77. Stutzmann J.M., Wahl F., Pratt J., Mary V., Reibaud M., Tecoult E., et al. Neuroprotective profile of riluzole in vivo models of acute neurodegenerative diseases. CNS Drugs Rev 3 (1997) 83-101
78. Torres-Aleman I., Barrios V., Lledo A., and Berciano J. The insulin-like growth factor system in cerebellar degeneration. Ann Neurol 39 (1996) 335-342
79. Vergara C., Latorre R., Marrion N.V., and Adelman J.P. Calcium-activated potassium channels. Curr Opin Neurobiol 8 (1998) 321-329
80. Walter J.T., Alvina K., Womack M.D., Chevez C., and Khodakhah K. Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 9 (2006) 389-397
81. Ca channels in cultured differentiated human skeletal muscle cells. Life Sci 82 (2008) 1-20
82. Weisz C.J., Raike R.S., Soria-Jasso L.E., and Hess E.J. Potassium channel blockers inhibit the triggers of attacks in the calcium channel mouse mutant tottering. J Neurosci 25 16 (2005) 4141-4145
83. Wu S.N., and Li H.F. Characterization of riluzole-induced stimulation of large-conductance calcium-activated potassium channels in rat pituitary GH3 cells. J Investig Med 47 (1999) 484-495
84. Wu S.N., Wu A.Z., and Lin M.W. Pharmacological roles of the large-conductance calcium-activated potassium channel. Curr Top Med Chem 6 10 (2006) 1025-1030
85. Yoon K.W., Covey D.F., and Rothman S.M. Multiple mechanisms of picrotoxin block of GABA-induced currents in rat hippocampal neurons. J Physiol 464 (1993) 423-439