Riluzole does not improve lifespan or motor function in three ALS mouse models

References

• Petrov D, Mansfield C, Moussy A, Hermine O. ALS clinical trials review: 20 years of failure. Are we any closer to registering a new treatment? Front Aging Neurosci. 2017;9:68. [Review].
   PubMed Web of Science ®Google Scholar
• Martin D, Thompson MA, Nadler JV. The neuroprotective agent riluzole inhibits release of glutamate and aspartate from slices of hippocampal area CA1. Eur J Pharmacol. 1993;250:473–6.
   PubMed Web of Science ®Google Scholar
• Albo F, Pieri M, Zona C. Modulation of AMPA receptors in spinal motor neurons by the neuroprotective agent riluzole. J Neurosci Res. 2004;78:200–7.
   PubMed Web of Science ®Google Scholar
• He Y, Zorumski CF, Mennerick S. Contribution of presynaptic Na(+) channel inactivation to paired-pulse synaptic depression in cultured hippocampal neurons. J Neurophysiol. 2002;87:925–36.
   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
• Lamanauskas N, Nistri A. Riluzole blocks persistent Na + and Ca2+ currents and modulates release of glutamate via presynaptic NMDA receptors on neonatal rat hypoglossal motoneurons in vitro. Eur J Neurosci. 2008;27:2501–14.
   PubMed Web of Science ®Google Scholar
• Daniel B, Green O, Viskind O, Gruzman A. Riluzole increases the rate of glucose transport in L6 myotubes and NSC-34 motor neuron-like cells via AMPK pathway activation. Amyotroph Lateral Scler Frontotemporal Degener. 2013;14:434–43.
   PubMed Web of Science ®Google Scholar
• Mizuta I, Ohta M, Ohta K, Nishimura M, Mizuta E, Kuno S. Riluzole stimulates nerve growth factor, brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor synthesis in cultured mouse astrocytes. Neurosci Lett. 2001;310:117–20.
   PubMed Web of Science ®Google Scholar
• Bellingham MC. A review of the neural mechanisms of action and clinical efficiency of riluzole in treating amyotrophic lateral sclerosis: what have we learned in the last decade? CNS Neurosci Ther. 2011;17:4–31. [Review].
   PubMed Web of Science ®Google Scholar
• 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
• Bensimon G, Lacomblez L, Delumeau JC, Bejuit R, Truffinet P, Meininger V. A study of riluzole in the treatment of advanced stage or elderly patients with amyotrophic lateral sclerosis. J Neurol. 2002;249:609–15.
   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;Mar 14; (3):CD001447.
   PubMed Web of Science ®Google Scholar
• Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science. 1994;264:1772–5.
   PubMed Web of Science ®Google Scholar
• Wegorzewska I, Bell S, Cairns NJ, Miller TM, Baloh RH. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci USA. 2009;106:18809–14.
   PubMed Web of Science ®Google Scholar
• Shelkovnikova TA, Peters OM, Deykin AV, Connor-Robson N, Robinson H, Ustyugov AA, et al. Fused in sarcoma (FUS) protein lacking nuclear localization signal (NLS) and major RNA binding motifs triggers proteinopathy and severe motor phenotype in transgenic mice. J Biol Chem. 2013;288:25266–74.
   PubMed Web of Science ®Google Scholar
• Ludolph AC, Bendotti C, Blaugrund E, Chio A, Greensmith L, Loeffler JP, et al. Guidelines for preclinical animal research in ALS/MND: A consensus meeting. Amyotroph Lateral Scler. 2010;11:38–45.
   PubMed Web of Science ®Google Scholar
• Gurney ME, Cutting FB, Zhai P, Doble A, Taylor CP, Andrus PK, et al. Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral sclerosis. Ann Neurol. 1996;39:147–57.
   PubMed Web of Science ®Google Scholar
• Scott S, Kranz JE, Cole J, Lincecum JM, Thompson K, Kelly N, et alet al. Design, power, and interpretation of studies in the standard murine model of ALS. Amyotroph Lateral Scler. 2008;9:4–15.
   PubMed Web of Science ®Google Scholar
• Colovic M, Zennaro E, Caccia S. Liquid chromatographic assay for riluzole in mouse plasma and central nervous system tissues. J Chromatogr B Analyt Technol Biomed Life Sci. 2004;803:305–9.
   PubMed Web of Science ®Google Scholar
• Groeneveld GJ, van Kan HJ, Torano JS, Veldink JH, Guchelaar HJ, Wokke JH, et al. Inter- and intraindividual variability of riluzole serum concentrations in patients with ALS. J Neurol Sci. 2001;191:121–5.
   PubMed Web of Science ®Google Scholar
• Taylor JP, Brown RH, Jr., Cleveland DW. Decoding ALS: from genes to mechanism. Nature 2016;539:197–206.
   PubMed Web of Science ®Google Scholar
• Esmaeili MA, Panahi M, Yadav S, Hennings L, Kiaei M. Premature death of TDP-43 (A315T) transgenic mice due to gastrointestinal complications prior to development of full neurological symptoms of amyotrophic lateral sclerosis. Int J Exp Pathol. 2013;94:56–64.
   PubMed Web of Science ®Google Scholar
• Herdewyn S, Cirillo C, Van Den Bosch L, Robberecht W, Vanden Berghe P, Van Damme P. Prevention of intestinal obstruction reveals progressive neurodegeneration in mutant TDP-43 (A315T) mice. Mol Neurodegeneration. 2014;9:24.
   PubMed Web of Science ®Google Scholar
• Coughlan KS, Halang L, Woods I, Prehn JH. A high-fat jelly diet restores bioenergetic balance and extends lifespan in the presence of motor dysfunction and lumbar spinal cord motor neuron loss in TDP-43A315T mutant C57BL6/J mice. Dis Model Mech. 2016;9:1029–37.
   PubMed Web of Science ®Google Scholar
• Hatzipetros T, Bogdanik LP, Tassinari VR, Kidd JD, Moreno AJ, Davis C, et al. C57BL/6J congenic Prp-TDP43A315T mice develop progressive neurodegeneration in the myenteric plexus of the colon without exhibiting key features of ALS. Brain Res. 2014;1584:59–72.
   PubMed Web of Science ®Google Scholar
• Chio A, Restagno G, Brunetti M, Ossola I, Calvo A, Mora G, et al. Two Italian kindreds with familial amyotrophic lateral sclerosis due to FUS mutation. Neurobiol Aging. 2009;30:1272–5.
   PubMed Web of Science ®Google Scholar
• Gurney ME, Fleck TJ, Himes CS, Hall ED. Riluzole preserves motor function in a transgenic model of familial amyotrophic lateral sclerosis. Neurology. 1998;50:62–6.
   PubMed Web of Science ®Google Scholar
• Snow RJ, Turnbull J, da Silva S, Jiang F, Tarnopolsky MA. Creatine supplementation and riluzole treatment provide similar beneficial effects in copper, zinc superoxide dismutase (G93A) transgenic mice. Neuroscience. 2003;119:661–7.
   PubMed Web of Science ®Google Scholar
• Waibel S, Reuter A, Malessa S, Blaugrund E, Ludolph AC. Rasagiline alone and in combination with riluzole prolongs survival in an ALS mouse model. J Neurol. 2004;251:1080–4.
   PubMed Web of Science ®Google Scholar
• Del Signore SJ, Amante DJ, Kim J, Stack EC, Goodrich S, Cormier K, et al. Combined riluzole and sodium phenylbutyrate therapy in transgenic amyotrophic lateral sclerosis mice. Amyotroph Lateral Scler. 2009;10:85–94.
   PubMed Web of Science ®Google Scholar
• Perrin S. Preclinical research: Make mouse studies work. Nature. 2014;507:423–5.
   PubMed Web of Science ®Google Scholar
• Yoshida H, Yanai H, Namiki Y, Fukatsu-Sasaki K, Furutani N, Tada N. Neuroprotective effects of edaravone: a novel free radical scavenger in cerebrovascular injury. CNS Drug Rev. 2006;12:9–20.
   PubMedGoogle Scholar
• Ito H, Wate R, Zhang J, Ohnishi S, Kaneko S, Nakano S, et al. Treatment with edaravone, initiated at symptom onset, slows motor decline and decreases SOD1 deposition in ALS mice. Exp Neurol. 2008;213:448–55.
   PubMed Web of Science ®Google Scholar
• Aoki M, Warita H, Mizuno H, Suzuki N, Yuki S, Itoyama Y. Feasibility study for functional test battery of SOD transgenic rat (H46R) and evaluation of edaravone, a free radical scavenger. Brain Res. 2011;1382:321–5. [Evaluation Studies].
   PubMed Web of Science ®Google Scholar
• Yoshino H, Kimura A. Investigation of the therapeutic effects of edaravone, a free radical scavenger, on amyotrophic lateral sclerosis (Phase II study). Amyotroph Lateral Scler. 2006;7:241–5.
   PubMed Web of Science ®Google Scholar
• Abe K, Itoyama Y, Sobue G, Tsuji S, Aoki M, Doyu M, et al. Confirmatory double-blind, parallel-group, placebo-controlled study of efficacy and safety of edaravone (MCI-186) in amyotrophic lateral sclerosis patients. Amyotroph Lateral Scler Frontotemporal Degener. 2014;15:610–7.
   PubMed Web of Science ®Google Scholar
• Tanaka M, Sakata T, Palumbo J, Akimoto M. A 24-week, phase III, double-blind, parallel-group study of edaravone (MCI-186) for treatment of amyotrophic lateral sclerosis (ALS) (P3.189). Neurology 2016;86(Suppl P3):189.
   Google Scholar
• Tanaka M, Sakata T, Palumbo J, Akimoto M. A double-blind, parallel-group, placebo-controlled, 24-week, exploratory study of edaravone (MCI-186) for the treatment of advanced amyotrophic lateral sclerosis (ALS) (P3.191). Neurology 2016;86(Suppl P3):191.
   Web of Science ®Google Scholar
• Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 2006;314:130–3.
   PubMed Web of Science ®Google Scholar
• Shelkovnikova TA, Robinson HK, Connor-Robson N, Buchman VL. Recruitment into stress granules prevents irreversible aggregation of FUS protein mislocalized to the cytoplasm. Cell Cycle. 2013;12:3194–202.
   PubMed Web of Science ®Google Scholar