In vivo 4-aminopyridine treatment alters the neurotoxin 3-acetylpyridine-induced plastic changes in intrinsic electrophysiological properties of rat cerebellar Purkinje neurones

European Journal of Pharmacology

Volumn 642, Issue 1-3, 2010, Pages 56-65

  Goudarzi, Iran ^a,b   Kaffashian, Mohammadreza ^a   Shabani, Mohammad ^c   Haghdoost Yazdi, Hashem ^d   Behzadi, Gila ^a   Janahmadi, Mahyar ^a  

^a SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b DAMGHAN UNIVERSITY   (Iran)

^c KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d QAZVIN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

4 Aminopyridin; Ataxia; Ca2+ spike; Cerebellum; Neuroprotection; Purkinje neurone

Indexed keywords

3 ACETYLPYRIDINE; 4 AMINOPYRIDINE; CALCIUM CHANNEL; CALCIUM ION; 3-ACETYLPYRIDINE; NEUROTOXIN; PYRIDINE DERIVATIVE;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CALCIUM SIGNALING; CEREBELLAR ATAXIA; CONTROLLED STUDY; DRUG MECHANISM; HISTOPATHOLOGY; IN VIVO STUDY; LATENT PERIOD; MALE; MOTOR PERFORMANCE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE POTENTIAL; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; ROTAROD TEST; ANIMAL; ANIMAL BEHAVIOR; ATAXIA; CYTOLOGY; DRUG EFFECTS; DRUG INTERACTION; ELECTROPHYSIOLOGY; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PATHOPHYSIOLOGY; TOXICITY;

4-AMINOPYRIDINE; ANIMALS; ATAXIA; BEHAVIOR, ANIMAL; DRUG INTERACTIONS; ELECTROPHYSIOLOGICAL PROCESSES; MALE; MOTOR ACTIVITY; NEUROTOXINS; PURKINJE CELLS; PYRIDINES; RATS;

EID: 77954623238     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.05.031     Document Type: Article

References (99)

1. Anderson W.A., 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. 1980, 190:157-174.
2. Alviña K., Ellis-Davies G., Khodakhah K. T-type calcium channels mediate rebound firing in intact deep cerebellar neurons. Neuroscience 2009, 158:635-641.
3. Aoyama N., Lee S.M., Moro N., Hovda D.A., Sutton R.L. Duration of ATP reduction affects extent of CA1 cell death in rat models of fluid percussion injury combined with secondary ischemia. Brain Res. 2008, 16(1230):310-319.
4. 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. 1985, 9:21-42.
5. Beck H., Yaari Y. Plasticity of intrinsic neuronal properties in CNS disorders. Nat. Rev. Neurosci. 2008, 9:357-369.
6. Beiswanger C.M., Roscoe-Graessle T.L., Zerbe N., Reuhl K.R., Lowndes H.E. 3-acetylpyridine-induced degeneration in the dorsal root ganglia: involvement of small diameter neurons and influence of axotomy. Neuropath. Appl. Neuro. 2008, 19:164-172.
7. Bever C.T., Leslie J., Camenga D., Panitch H.S., Johnson K.P. Preliminary trial of 3, 4-diaminopyridine in patients with multiple sclerosis. Ann. Neurol. 1990, 27:421-427.
8. Bushell T., Clarke C., Mathie A., Robertson B. Pharmacological characterization of a non-inactivating outward current observed in mouse cerebellar Purkinje neurones. Br. J. Pharmacol. 2002, 135:705-712.
9. Butterworth R.F. Animal models of the cerebellar ataxia. Neuromethods 1992, vol. 21:275-294. Humana Press, New Jersey. A. Boulton, G. Baker, R.F. Butterworth (Eds.).
10. (2+) spikes in Purkinje cells from rat cerebellar slice cultures. J. Physiol. 2002, 540:57-72.
11. Cerminara N.L., Rawson J.A. Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. J. Neurosci. 2004, 24:4510-4517.
12. Chiesa N., Barlow C., Wynshaw-Boris A., Strata P., Tempia F. Atm-deficient mice Purkinje cells show age-dependent defects in calcium spike bursts and calcium currents. Neuroscience 2000, 96:557-583.
13. Coetzee W., Amarillo Y., Chiu J., Chow A., Lau D., McCormack T., Moreno H., Nadal M., Ozaita A., Pountney D., Saganich M., Vega-Saenzde Mierak E., Rudy B. Molecular diversity of K1 channels. Ann NY Acad Sci 1999, 868:233-285.
14. Davidson M., Zemishlany Z., Mohs R.C., Horvath T.B., Powchik P., Blass J.P., Davis K.L. 4-Aminopyridine in the treatment of Alzheimer's disease. Biolo. Psychiat. 1988, 23:485-490.
15. Davis F.A., Stefoski D., Rush J. Orally administered 4aminopyridine improves clinical signs in multiple sclerosis. Ann. Neurol. 1990, 27:186-192.
16. Desclin J.C. Histological evidence supporting the inferior olive as the major source of cerebellar climbing fibers in the rat. Brain Res. 1974, 77:365-384.
17. Desclin J.C., Colin F. The olivocerebellar system. II. Some ultrastructural correlates of inferior olive destruction in the rat. Brain Res. 1980, 187:29-46.
18. Deutch A.Y., Rosin D.L., Goldstein M., Roth R.H. 3-Acetylpyridine-induced degeneration of the nigrostriatal dopamine system: an animal model of olivopontocerebellar atrophy-associated Parkinsonism. Exp. Neurol. 1989, 105:1-9.
19. + channels: electrifying regulators of synaptic terminal excitability. Trends Neurosci. 2004, 7:210-217.
20. + channels to rat Purkinje neuron function. J. Physiol. 2003, 548:53-69.
21. Etzion Y., Grossman Y. Potassium currents modulation of calcium spike firing in dendrites of cerebellar Purkinje cells. Exp. Brain Res. 1998, 122:283-294.
22. 2+ spike firing of cerebellar Purkinje neurons at high pressure. Pflugers Arch. 1999, 437:276-284.
23. Etzion Y., Grossman Y. Highly 4-aminopyridine sensitive delayed rectifier current modulates the excitability of guinea pig cerebellar Purkinje cells. Exp. Brain Res. 2001, 139:419-425.
24. Fernandez A.M., de la Vega A.G., Torres-Aleman I. Insulin-like growth factor I restores motor coordination in a rat model of cerebellar ataxia. Proc. Natl Acad. Sci. 1998, 95:1253-1258.
25. Flores-Hernandez J., Galarraga E., Pineda J.C., Bargas J. Patterns of excitatory and inhibitory synaptic transmission in the rat neostriatum as revealed by 4-AP. J. Neurophysiol. 1994, 72:2246-2256.
26. Gibson G.E., Blass J.P. Oxidative metabolism and acetylcholine synthesis during acetylpyridine treatment. Neurochem. Res. 1985, 10:453-467.
27. Glasauer S., Kalla R., Buttner U., Strupp M., Brandt T. 4-Aminopyridine restores visual ocular motor function in upbeat nystagmus. J. Neurol. Neurosurg. Psychiatry 2005, 76:451-453.
28. Glasauer S., Strupp M., Kalla R., Buttner U., Brandt T. Effect of 4-aminopyridine on upbeat and downbeat nystagmus elucidates the mechanism of downbeat nystagmus. Ann. NY Acad. Sci. 2005, 1039:528-531.
29. + and cell shrinkage a role for PKC upstream of caspase. J. Biol. Chem. 2000, 275:19609-19619.
30. Goshima Y., Miyamae T., Nakamura S., Miki K., Kosaka K., Misu Y. Ventral tegmental injection of nicotine induces locomotor activity and L-DOPA release from nucleus accumbens. Eur. J. Pharmacol. 1996, 309:229-233.
31. Gruol D.L., Franklin C.L. Morphological and physiological differentiation of Purkinje neurones in culture of rat cerebellum. J. Neurosci. 1987, 7:1271-1293.
32. + (BK) channels regulate the spike configuration in the burst firing of cerebellar Purkinje neurons. Brain Res. 2008, 1212:1-8.
33. Haghdoust H., Janahmadi M., Behzadi G. Physiological role of dendrotoxin-sensitive K+ channels in the rat cerebellar Purkinje neurons. Physiol. Res. 2007, 56:807-813.
34. A current with a role in spike timing and locomotor pattern generation. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:5276-5281.
35. Hess B.H., Krewet J.A., Tolber D.L. Olivocerebellar projections are necessary for exogenous trophic factors to delay heredo-Purkinje cell degeneration. Brain Res. 2003, 986:54-62.
36. + currents. J. Pineal Res. 2005, 38:53-61.
37. v channel antagonist, prevents apoptosis of rat cerebellar granule neurons. Neuropharmacoly 2006, 51:737-746.
38. Iwasaki S., Chihara Y., Komuta Y., Ito K., Sahara Y. Low-voltage-activated potassium channels underlie the regulation of intrinsic firing properties of rat vestibular ganglion cells. J. Neurophysiol. 2008, 100:2192-2204.
39. Janahmadi M., Goudarzi I., Kaffashian M.R., Behzadi G., Fathollahi Y., Hajizadeh S. Co-treatment with riluzole, a neuroprotective drug, ameliorates the 3-acetylpyridine-induced neurotoxicity in cerebellar Purkinje neurones of rats: behavioural and electrophysiological evidence. Neurotoxicology 2009, 30:393-402.
40. Jones R.E., Heron J.R., Foster D.H., Sneglar R.S., Mason R.J. Effects of 4-aminopyridine in patients with multiple sclerosis. J. Neurol. Sci. 1983, 60:353-362.
41. Judge S.I.V., Bever C.T. Potassium blockers in multiple sclerosis: neuronal Kv channels and effects of symptomatic treatment. Pharmacol. Theraput. 2006, 111:224-259.
42. Kalla R., Glasauer S., Schautzer F., Lehnen N., Büttner U., Strupp M. 4-Aminopyridine improves downbeat nystagmus, smooth pursuit, and VOR gain. Neurology 2004, 62:1228-1229.
43. Kalla R., Glasauer S., Büttner U., Brandt T., Strupp M. 4-Aminopyridine restores vertical and horizontal neural integrator function in downbeat nystagmus. Brain 2007, 130:2441-2451.
44. Kim J., Hoffman D.A. Potassium channels: newly found players in synaptic plasticity. Neuroscientist 2008, 14:276-286.
45. Kinoshita K., Watanabe Y., Asai H., Matsuoka Y. Metabolic abnormalities caused by 3-acetylpyridine in the cerebral motor regions of rats: partial recovery by thyrotropin-releasing hormone. Jpn J. Pharmacol. 2000, 82:295-300.
46. Kobayashi K., Ikeda Y., Suzuki H. Locomotor activity correlates with modifications of hippocampal mossy fibre synaptic transmission. Eur. J. Neurosci. 2006, 24:1867-1873.
47. + channels. J. Biol. Chem. 2003, 278:32067-32076.
48. Llinás R., Walton K., Hillman D.E., Sotelo C. Inferior olive: its role in motor learning. Science 1975, 190:1230-1231.
49. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. (Lond.) 1980, 305:171-195.
50. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J. Physiol. (Lond.) 1980, 305:197-213.
51. Löhle M., Schrempf W., Wolz M., Reichmann H., Storch A. Potassium channel blocker 4-aminopyridine is effective in interictal cerebellar symptoms in episodic ataxia type 2: a video case report. Mov. Disord. 2008, 23:1314-1316.
52. Lorenzon N.M., Lutz C.M., Frankel W.N., Beam K.G. Altered calcium channel currents in Purkinje cells of the neurological mutant mouse leaner. J. Neurosci. 1998, 18:4482-4489.
53. McKay B.E., Engbers J.D.T., Mehaffey W.H., Gordon G.R.J., Molineux M.L., Bains J.S., Turner R.W. Climbing fiber discharge regulates cerebellar function by controlling the intrinsic characteristics of Purkinje cell output. J. Neurophysiol. 2007, 97:2590-2604.
54. Mehaffey W.H., Fernandez F.R., Doiron B., Turner R.W. Regulation of somatic firing dynamics by backpropagating dendritic spikes. J. Physiol. Paris 2008, 102:181-194.
55. Miall R.C., Keating J.G., Malkmus M., Thach W.T. Simple spike activity predicts occurrence of complex spikes in cerebellar Purkinje cells. Nat. Neurosci. 1998, 1:13-15.
56. 2+ spike firing in the dendrites of cerebellar Purkinje neurons: a modelling study. Brain Res. 2001, 891:106-115.
57. Midtgaard J., Lasser-Ross N., Ross W.N. Spatial distribution of calcium influx in turtle Purkinje cell dendrites in vitro: role of a transient outward current. J. Neurophysiol. 1993, 70:2455-2469.
58. Molineux M.L., Fernandez F.R., Mehaffey W.H., Turner R.W. A-type and T-type currents interact to produce a novel spike latency-voltage relationship in cerebellar stellate cells. J. Neurosci. 2005, 25:10863-10873.
59. Montarolo P.G., Palestini M., Strata P. The inhibitory effect of the olivocerebellar input on the cerebellar Purkinje cells in the rat. J. Physiol. 1982, 332:187-202.
60. Muir G.D., Whishaw I.Q. Red nucleus lesions impair over ground locomotion in rats: a kinetic analysis. Eur. J. Neurosci. 2000, 12:1113-1122.
61. + channel blocker 4-aminopyridine protects against kainite-induced neuronal cell death through activation of NMDA receptors in murine hippocampus. Neuropharmacology 2005, 48:810-821.
62. O'Hearn E., Molliver M.E. The olivocerebellar projection mediates ibogaine-induced degeneration of Purkinje cells: a model of indirect, trans-synaptic excitotoxicity. J. Neurosci. 1997, 17:8828-8841.
63. Otis T.S., Jen J. Blessed are the pacemakers. Nat. Neurosci. 2006, 9:297-298.
64. + spike bursts. Eur. J. Neurosci. 2008, 27:93-103.
65. Pal S., Harynett K.A., Nerbonne J.M., Levitan E.S., Aizemnman E. Meditation of neuronal apoptosis by Kv2.2-encoded potassium channels. J. Neurosci. 2003, 23:4798-4802.
66. Perreault P., Avoli M. Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices. J. Neurophysiol. 1991, 65:771-785.
67. Pong O. Regulation of excitability by potassium channels. Results Probl. Cell Differ. 2007, 44:145-161.
68. Rasband M.N., Trimmer J.S., Schwarz T.L., Levinson S.R., Ellisman M.H., Schachner M., et al. Potassium channel distribution, clustering, and function in remyelinating rat axons. J. Neurosci. 1998, 18:36-47.
69. Sacco T., Tempia F. A-type potassium currents active at subthreshold potentials in mouse cerebellar Purkinje cells. J. Physiol. 2002, 543:505-520.
70. Sakai K., Gash D.M. Effect of bilateral 6-OHDA lesions of the substantia nigra on locomotor activity in the rat. Brain Res. 1994, 633:144-150.
71. + channel deficiency. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9474-9478.
72. Schreurs B.G., Tomsic D., Gusev P.A., Alkon D.L. Dendritic excitability microzones and occluded long-term depression after classical conditioning of the rabbit's nictitating membrane response. J. Neurophysiol. 1997, 77:86-92.
73. 2+-dependent action potential and changes oscillatory firing patterns in rat cerebellar Purkinje cells. Yonsei Med. J. 1999, 40:112-117.
74. Seoane A., Apps R., Balbuene E., Herrero L., Llorens J. Differential effects of trans-crotononitrile and 3-acetylpyridine on the inferior olive integrity and behavioral performance in the rat. Eur. J. Neurosci. 2005, 22:880-894.
75. Shakkottai V.G., Chou C.H., Oddo S., Sailer C.A., Knaus H.G., Gutman G.A., Barish M.E., LaFerla F.M., Chandy K.G. Enhanced neuronal excitability in the absence of neurodegeneration induces cerebellar ataxia. J. Clin. Invest. 2004, 113:582-590.
76. Sherratt R.M., Bostock H., Sears T.A. Effects of 4-aminopyridine on normal and demyelinated mammalian nerve fibres. Nature 1980, 283:570-572.
77. Shimada M., Ozaki H.S., Murakami T.H., Imahayashi T. Effects of 3-acetylpyridine on local cerebral glucose utilization. Neurosci. Res. 1984, 1:357-362.
78. Stone T.W. Neuropharmacology of quinolinic and kynurenic acids. Pharmacol. Rev. 1993, 45:309-379.
79. Strupp M., Kalla R., Dichgans M., Freilinger T., Glasauer S., Brandt T. Treatment of episodic ataxia type 2 with the potassium channel blocker 4-aminopyridine. Neurology 2004, 62:1623-1625.
80. Strupp M., Zwergal A., Brandt T. Episodic ataxia type 2. Neurotherapeutics 2007, 4:267-273.
81. Strupp M., Kalla R., Glasauer S., Wagner J., Hüfner K., Jahn K., Branddt T. Aminopyridines for the treatment of cerebellar and ocular motor disorders. Prog. in Brain Res 2008, 171. C. Kennard, R.J. Leigh (Eds.).
82. Sukin D., Skedros D.G., Beales M., Stratton S.E., Lorden J.F., Oltmans G.A. Temporal sequence of motor disturbances and increased cerebellar glutamic acid decarboxylase activity following 3-acetylpyridine lesions in adult rats. Brain Res. 1987, 426:82-92.
83. Swensen A.M., Bean B.P. Ionic mechanisms of burst firing in dissociated Purkinje neurons. J. Neurosci. 2003, 23:9650-9663.
84. Szalay J., Böti Z., Temesvári P., Bara D. Alterations of the nucleus ruber in 3-acetylpyridine intoxication. A light and electron microscopic study. Exp. Pathol.(Jena). 1979, 17:271-279.
85. Takei T., Kuge Y., Zhao S., Sato M., Strauss H.W., Blankenberg F.G., Tait J.F., Tamaki N. Enhanced apoptotic reaction correlates with suppressed tumor glucose utilization after cytotoxic chemotherapy: use of 99mTc-Annexin V, 18F-FDG, and histologic evaluation. J. Nucl. Med. 2005, 46:794-799.
86. Thesleff S. Aminopyridine and synaptic transmission. Neuroscience 1980, 5:1413-1419.
87. Torres-Aleman I., Barrios V., Lledo A., Berciano J. The insulin-like growth factor system in cerebellar degeneration. Ann. Neurol. 1996, 39:335-342.
88. Walter J.T., Alvina K., Womack M.D., Chevez C., Khodakhah K. Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat. Neurosci. 2006, 9:389-397.
89. Wang Y., Strahlendorf J.C., Strahlendorf H.K. A transient voltage-dependent outward potassium current in mammalian cerebellar Purkinje cells. Brain Res. 1991, 567:153-158.
90. A currents in adult rabbit cerebellar Purkinje cells. Brain Res. 2006, 1096:85-96.
91. Watase K., Barrett C.F., Miyazaki T., Ishiguro T., Ishikawa K., Hu Y., Unno T., Sun Y., Kasai S., Watanabe M., Gomez C.M., Mizusawa H., Tsien R.W., Zoghbi H.Y. Spinocerebellar ataxia type 6 knock in mice develop a progressive neuronal dysfunction with age-dependent accumulation of mutant CaV2.1 channels. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11987-11992.
92. Weisz C.J., Raike R.S., Soria-Jasso L.E., Hess E.J. Potassium channel blockers inhibit the triggers of attacks in the calcium channel mouse mutant tottering. J. Neurosci. 2005, 25:4141-4145.
93. Womack M.D., Khodakhah K. Somatic and dendritic small-conductance calcium-activated potassium channels regulate the output of cerebellar Purkinje neurons. J. Neurosci. 2003, 23:2600-2607.
94. Womack M.D., Khodakhah K. Dendritic control of spontaneous bursting in cerebellar Purkinje cells. J. Neurosci. 2004, 24:3511-3521.
95. + channels in the modulation of 4-aminopyridine-induced burst firing in rat cerebellar Purkinje cells. Brain Res. 2007, 1156:59-66.
96. Yoon K.W., Covey D.F., Rothman S.M. Multiple mechanisms of picrotoxin block of GABA-induced currents in rat hippocampal neurons. J. Physiol. 1993, 464:423-439.
97. Yoshino A., Hovda D.A., Kawamata T., Katayama Y., Becker D.P. Dynamic changes in local cerebral glucose utilization following cerebral concussion in rats: evidence of a hyper- and subsequent hypometabolic state. Brain Res. 1991, 561:106-119.
98. Yu S.P., Farhangrazi Z.S., Ying H.S., Yeh C.H., Choi D.W. Enhancement of outward potassium current may participate in β-amyloid peptide-induced cortical neuronal death. Neurobiol. Dis. 1998, 5:81-88.
99. Zhao Y.M., Sun L.N., Zhou H.Y., Wang X.L. Voltage-dependent potassium channels are involved in glutamate-induced apoptosis of rat hippocampal neurons. Neurosci. Lett. 2006, 398:22-27.