Riluzole exerts transient modulating effects on cortical and axonal hyperexcitability in ALS

References

• Bensimon G, Lacomblez L, Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med. 1994;330:585–91.
   PubMed Web of Science ®Google Scholar
• Lacomblez L, Bensimon G, Leigh PN, Guillet P, Meininger V. Dose-ranging study of riluzole in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis/Riluzole Study Group II. Lancet. 1996;347:1425–31.
   PubMed Web of Science ®Google Scholar
• Miller RG, Mitchell JD, Moore DH. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst Rev. 2012;3:Cd001447.
   PubMed Web of Science ®Google Scholar
• Cheah BC, Vucic S, Krishnan AV, Kiernan MC. Riluzole, neuroprotection and amyotrophic lateral sclerosis. Curr Med Chem. 2010;17:1942–199.
   PubMed Web of Science ®Google Scholar
• Azbill RD, Mu X, Springer JE. Riluzole increases high-affinity glutamate uptake in rat spinal cord synaptosomes. Brain Res. 2000;871:175–80.
   PubMed Web of Science ®Google Scholar
• Dunlop J, Beal McIlvain H, She Y, Howland DS. Impaired Spinal Cord Glutamate Transport Capacity and Reduced Sensitivity to Riluzole in a Transgenic Superoxide Dismutase Mutant Rat Model of Amyotrophic Lateral Sclerosis. J Neurosci. 2003;23:1688–96.
   PubMed Web of Science ®Google Scholar
• Wang SJ, Wang KY, Wang WC. Mechanisms underlying the riluzole inhibition of glutamate release from rat cerebral cortex nerve terminals (synaptosomes). Neuroscience. 2004;125:191–201.
   PubMed Web of Science ®Google Scholar
• Eisen A, Kim S, Pant B. Amyotrophic lateral sclerosis (ALS): a phylogenetic disease of the corticomotoneuron? Muscle Nerve. 1992;15:219–24.
   PubMed Web of Science ®Google Scholar
• Vucic S, Kiernan MC. Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain. 2006;129:2436–46.
   PubMed Web of Science ®Google Scholar
• Vucic S, Kiernan MC. Up-regulation of persistent sodium conductances in familial ALS. J Neurol Neurosurg Psychiatry. 2010;81:222–7.
   PubMed Web of Science ®Google Scholar
• Vucic S, Nicholson GA, Kiernan MC. Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain. 2008;131:1540–50.
   PubMed Web of Science ®Google Scholar
• Vucic S, Rothstein JD, Kiernan MC. Advances in treating amyotrophic lateral sclerosis: insights from pathophysiological studies. Trends Neurosci. 2014;37:433–42.
   PubMed Web of Science ®Google Scholar
• Menon P, Geevasinga N, Yiannikas C, Howells J, Kiernan MC, Vucic S. Sensitivity and specificity of threshold tracking transcranial magnetic stimulation for diagnosis of amyotrophic lateral sclerosis: a prospective study. The Lancet Neurology. 2015;14:478–84.
   PubMed Web of Science ®Google Scholar
• Vucic S, Lin CS-Y, Cheah BC, et al. Riluzole exerts central and peripheral modulating effects in amyotrophic lateral sclerosis. Brain. 2013;136:1361–70.
   PubMed Web of Science ®Google Scholar
• Benoit E, Escande D. Riluzole specifically blocks inactivated Na channels in myelinated nerve fibre. Pflugers Arch. 1991;419:603–9.
   PubMed Web of Science ®Google Scholar
• Urbani A, Belluzzi O. Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur J Neurosci. 2000;12:3567–74.
   PubMed Web of Science ®Google Scholar
• Wang Y-J, Lin M-W, Lin A-A, Wu S-N. Riluzole-induced block of voltage-gated Na + current and activation of BKCa channels in cultured differentiated human skeletal muscle cells. Life Sciences. 2008;82:11–20.
   PubMed Web of Science ®Google Scholar
• Stys PK. General mechanisms of axonal damage and its prevention. J Neurol Sci. 2005;233:3–13.
   PubMed Web of Science ®Google Scholar
• Stys PK. Sodium channel blockers as neuroprotectants in neuroinflammatory disease: a double-edged sword. Ann Neurol. 2007;62:3–5.
   PubMed Web of Science ®Google Scholar
• Burke D, Kiernan MC, Bostock H. Excitability of human axons. Clin Neurophysiol. 2001;112:1575–85.
   PubMed Web of Science ®Google Scholar
• de Carvalho M, Dengler R, Eisen A, et al. Electrodiagnostic criteria for diagnosis of ALS. Clin Neurophysiol. 2008;119:497–503.
   PubMed Web of Science ®Google Scholar
• Cedarbaum JM, Stambler N, Malta E, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci. 1999;169:13–21.
   PubMed Web of Science ®Google Scholar
• Vucic S, Howells J, Trevillion L, Kiernan MC. Assessment of cortical excitability using threshold tracking techniques. Muscle Nerve. 2006;33:477–86.
   PubMed Web of Science ®Google Scholar
• Fisher RJ, Nakamura Y, Bestmann S, Rothwell JC, Bostock H. Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking. Exp Brain Res. 2002;143:240–8.
   PubMed Web of Science ®Google Scholar
• Cantello R, Gianelli M, Civardi C, Mutani R. Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology. 1992;42:1951–9.
   PubMed Web of Science ®Google Scholar
• Mills KR, Murray NM. Electrical stimulation over the human vertebral column: which neural elements are excited? Electroencephalogr Clin Neurophysiol. 1986;63:582–9.
   PubMedGoogle Scholar
• de Carvalho M, Swash M. Nerve conduction studies in amyotrophic lateral sclerosis. Muscle Nerve. 2000;23:344–52.
   PubMed Web of Science ®Google Scholar
• Schwenkreis P, Liepert J, Witscher K, et al. Riluzole suppresses motor cortex facilitation in correlation to its plasma level. A study using transcranial magnetic stimulation. Exp Brain Res. 2000;135:293–9.
   PubMed Web of Science ®Google Scholar
• Schwenkreis P, Witscher K, Janssen F, et al. Influence of the N-methyl-D-aspartate antagonist memantine on human motor cortex excitability. Neurosci Lett. 1999;270:137–40.
   PubMed Web of Science ®Google Scholar
• Ziemann U, Reis J, Schwenkreis P, et al. TMS and drugs revisited 2014. Clin Neurophysiol. 2015;126:1847–68.
   PubMed Web of Science ®Google Scholar
• Vucic S, Ziemann U, Eisen A, Hallett M, Kiernan MC. Transcranial magnetic stimulation and amyotrophic lateral sclerosis: pathophysiological insights. J Neurol Neurosurg Psychiatry. 2013;84:1161–70.
   PubMed Web of Science ®Google Scholar
• Walhout R, Westeneng H-J, Verstraete E, et al. Cortical thickness in ALS: towards a marker for upper motor neuron involvement. J Neurol Neurosurg Psychiatry. 2015; 86:288–94
   PubMed Web of Science ®Google Scholar
• Grosskreutz J, Kaufmann J, Fradrich J, Dengler R, Heinze H-J, Peschel T. Widespread sensorimotor and frontal cortical atrophy in amyotrophic lateral sclerosis. BMC Neurol. 2006;6:17.
   PubMed Web of Science ®Google Scholar
• Verstraete E, Veldink JH, Hendrikse J, Schelhaas HJ, van den Heuvel MP, van den Berg LH. Structural MRI reveals cortical thinning in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2012;83:383–8.
   PubMed Web of Science ®Google Scholar
• Chiò A, Pagani M, Agosta F, Calvo A, Cistaro A, Filippi M. Neuroimaging in amyotrophic lateral sclerosis: insights into structural and functional changes. Lancet Neurol. 2014;13:1228–40.
   PubMed Web of Science ®Google Scholar
• Mancuso R, Navarro X. Amyotrophic lateral sclerosis: current perspectives from basic research to the clinic. Prog Neurobiol. 2015;133:1–26.
   PubMed Web of Science ®Google Scholar
• Vucic S, Cheah BC, Yiannikas C, Kiernan MC. Cortical excitability distinguishes ALS from mimic disorders. Clin Neurophysiol. 2011;122:1860–6.
   PubMed Web of Science ®Google Scholar
• Bruno R, Vivier N, Montay G, et al. Population pharmacokinetics of riluzole in patients with amyotrophic lateral sclerosis. Clin Pharmacol Ther. 1997;62:518–26.
   PubMed Web of Science ®Google Scholar
• Sanderink G-J, Bournique B, Stevens J, Petry M, Martinet M. Involvement of Human CYP1A Isoenzymes in the Metabolism and Drug Interactions of Riluzole In Vitro. J Pharmacol Exp Ther. 1997;282:1465–72.
   PubMed Web of Science ®Google Scholar
• Stefan K, Kunesch E, Benecke R, Classen J. Effects of riluzole on cortical excitability in patients with amyotrophic lateral sclerosis. Ann Neurol. 2001;49:536–9.
   PubMed Web of Science ®Google Scholar
• Nihei K, McKee AC, Kowall NW. Patterns of neuronal degeneration in the motor cortex of amyotrophic lateral sclerosis patients. Acta Neuropathologica. 1993;86:55–64.
   PubMed Web of Science ®Google Scholar
• Neumann M, Sampathu DM, Kwong LK, et al. Ubiquitinated TDP-43 in Frontotemporal Lobar Degeneration and Amyotrophic Lateral Sclerosis. Science. 2006;314:130–3.
   PubMed Web of Science ®Google Scholar
• Al-Sarraj S, King A, Troakes C, et al. P62 positive, TDP-43 negative, neuronal cytoplasmic and intranuclear inclusions in the cerebellum and hippocampus define the pathology of C9orf72-linked FTLD and MND/ALS. Acta Neuropathologica. 2011;122:691–702.
   PubMed Web of Science ®Google Scholar
• Ziemann U, Rothwell JC, Ridding MC. Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol (Lond). 1996;496:873–81.
   Google Scholar
• Ilic TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol (Lond). 2002;545:153–67.
   Google Scholar
• Pieri M, Carunchio I, Curcio L, Mercuri NB, Zona C. Increased persistent sodium current determines cortical hyperexcitability in a genetic model of amyotrophic lateral sclerosis. Exp Neurol. 2009;215:368–79.
   PubMed Web of Science ®Google Scholar
• Hebert T, Drapeau P, Pradier L, Dunn RJ. Block of the rat brain IIA sodium channel alpha subunit by the neuroprotective drug riluzole. Mol Pharmacol. 1994;45:1055–60.
   PubMed Web of Science ®Google Scholar
• Song J-H, Huang C-S, Nagata K, Yeh JZ, Narahashi T. Differential Action of Riluzole on Tetrodotoxin-Sensitive and Tetrodotoxin-Resistant Sodium Channels. J Pharmacol Exp Ther. 1997;282:707–14.
   PubMed Web of Science ®Google Scholar
• Kiernan MC, Cikurel K, Bostock H. Effects of temperature on the excitability properties of human motor axons. Brain. 2001;124:816–25.
   PubMed Web of Science ®Google Scholar
• Ziemann U. TMS and drugs. Clin Neurophysiol. 2004:1717–29.
   PubMed Web of Science ®Google Scholar
• Menon P, Geevasinga N, Yiannikas C, Howells J, Kiernan M, Vucic S. The sensitivity and specificity of threshold-tracking transcranial magnetic stimulation for the diagnosis of amyotrophic lateral sclerosis: a prospective study. Lancet Neurol. 2015;14:478–84.
   PubMed Web of Science ®Google Scholar