Protective effects of 4-aminopyridine in experimental optic neuritis and multiple sclerosis.

Chronic disability in multiple sclerosis is linked to neuroaxonal degeneration. 4-aminopyridine (4-AP) is used and licensed as a symptomatic treatment to ameliorate ambulatory disability in multiple sclerosis. The presumed mode of action is via blockade of axonal voltage gated potassium channels, thereby enhancing conduction in demyelinated axons. In this study, we provide evidence that in addition to those symptomatic effects, 4-AP can prevent neuroaxonal loss in the CNS. Using in vivo optical coherence tomography imaging, visual function testing and histologic assessment, we observed a reduction in retinal neurodegeneration with 4-AP in models of experimental optic neuritis and optic nerve crush. These effects were not related to an anti-inflammatory mode of action or a direct impact on retinal ganglion cells. Rather, histology and in vitro experiments indicated 4-AP stabilization of myelin and oligodendrocyte precursor cells associated with increased nuclear translocation of the nuclear factor of activated T cells. In experimental optic neuritis, 4-AP potentiated the effects of immunomodulatory treatment with fingolimod. As extended release 4-AP is already licensed for symptomatic multiple sclerosis treatment, we performed a retrospective, multicentre optical coherence tomography study to longitudinally compare retinal neurodegeneration between 52 patients on continuous 4-AP therapy and 51 matched controls. In line with the experimental data, during concurrent 4-AP therapy, degeneration of the macular retinal nerve fibre layer was reduced over 2 years. These results indicate disease-modifying effects of 4-AP beyond symptomatic therapy and provide support for the design of a prospective clinical study using visual function and retinal structure as outcome parameters.

[1]  Michael Dietrich,et al.  Using Optical Coherence Tomography and Optokinetic Response As Structural and Functional Visual System Readouts in Mice and Rats. , 2019, Journal of visualized experiments : JoVE.

[2]  S. Saidha,et al.  The International Multiple Sclerosis Visual System Consortium: Advancing Visual System Research in Multiple Sclerosis , 2018, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[3]  S. Kusunoki,et al.  4-Aminopyridine ameliorates relapsing remitting experimental autoimmune encephalomyelitis in SJL/J mice , 2018, Journal of Neuroimmunology.

[4]  X. Montalban,et al.  Restoring Axonal Function with 4-Aminopyridine: Clinical Efficacy in Multiple Sclerosis and Beyond , 2018, CNS Drugs.

[5]  H. Hartung,et al.  Early alpha-lipoic acid therapy protects from degeneration of the inner retinal layers and vision loss in an experimental autoimmune encephalomyelitis-optic neuritis model , 2018, Journal of Neuroinflammation.

[6]  H. Schöler,et al.  Nfat/calcineurin signaling promotes oligodendrocyte differentiation and myelination by transcription factor network tuning , 2018, Nature Communications.

[7]  P. Brugger,et al.  Positive effects of fampridine on cognition, fatigue and depression in patients with multiple sclerosis over 2 years , 2018, Journal of Neurology.

[8]  A. Lovett-racke,et al.  Suppression of Inflammatory Demyelinaton and Axon Degeneration through Inhibiting Kv3 Channels , 2017, Front. Mol. Neurosci..

[9]  H. Hartung,et al.  Iron‐sulfur glutaredoxin 2 protects oligodendrocytes against damage induced by nitric oxide release from activated microglia , 2017, Glia.

[10]  F. Paul,et al.  Optical coherence tomography for the diagnosis and monitoring of idiopathic intracranial hypertension , 2017, Journal of Neurology.

[11]  C. Heesen,et al.  Pattern of gray matter volumes related to retinal thickness and its association with cognitive function in relapsing–remitting MS , 2016, Brain and behavior.

[12]  M. Noble,et al.  4‐Aminopyridine promotes functional recovery and remyelination in acute peripheral nerve injury , 2016, EMBO molecular medicine.

[13]  Andrés Cruz-Herranz,et al.  Whole-body positional manipulators for ocular imaging of anaesthetised mice and rats: a do-it-yourself guide , 2016, BMJ Open Ophthalmology.

[14]  Pablo Villoslada,et al.  The APOSTEL recommendations for reporting quantitative optical coherence tomography studies , 2016, Neurology.

[15]  C. Gasperini,et al.  Prolonged-release fampridine and walking and balance in MS: randomised controlled MOBILE trial , 2016, Multiple sclerosis.

[16]  Jerry L Prince,et al.  Applying an Open-Source Segmentation Algorithm to Different OCT Devices in Multiple Sclerosis Patients and Healthy Controls: Implications for Clinical Trials , 2015, Multiple sclerosis international.

[17]  F. Bethoux,et al.  Long-term safety and efficacy of dalfampridine for walking impairment in patients with multiple sclerosis: Results of open-label extensions of two Phase 3 clinical trials , 2015, Multiple sclerosis.

[18]  H. Wiendl,et al.  4-Aminopyridine ameliorates mobility but not disease course in an animal model of multiple sclerosis , 2013, Experimental Neurology.

[19]  A. Conger,et al.  Effect of 4-aminopyridine on vision in multiple sclerosis patients with optic neuropathy , 2013, Neurology.

[20]  Axel Petzold,et al.  The OSCAR-IB Consensus Criteria for Retinal OCT Quality Assessment , 2012, PloS one.

[21]  A. Schnitzler,et al.  Optical Coherence Tomography in Parkinsonian Syndromes , 2012, PloS one.

[22]  D. Centonze,et al.  Oral fingolimod rescues the functional deficits of synapses in experimental autoimmune encephalomyelitis , 2012, British journal of pharmacology.

[23]  Amy Conger,et al.  The Impact of Utilizing Different Optical Coherence Tomography Devices for Clinical Purposes and in Multiple Sclerosis Trials , 2011, PloS one.

[24]  M. Esiri,et al.  Acid-sensing ion channel 1 is involved in both axonal injury and demyelination in multiple sclerosis and its animal model. , 2011, Brain : a journal of neurology.

[25]  Jeffrey A. Cohen,et al.  Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria , 2011, Annals of neurology.

[26]  D. Herr,et al.  FTY720 (fingolimod) efficacy in an animal model of multiple sclerosis requires astrocyte sphingosine 1-phosphate receptor 1 (S1P1) modulation , 2010, Proceedings of the National Academy of Sciences.

[27]  H. Hartung,et al.  Activation of CXCR7 receptor promotes oligodendroglial cell maturation , 2010, Annals of neurology.

[28]  L. Krupp,et al.  A phase 3 trial of extended release oral dalfampridine in multiple sclerosis , 2010, Annals of neurology.

[29]  D. Fischer,et al.  A Method for Preparing Primary Retinal Cell Cultures for Evaluating the Neuroprotective and Neuritogenic Effect of Factors on Axotomized Mature CNS Neurons , 2010, Current protocols in neuroscience.

[30]  D. Fischer,et al.  Neuroprotective and Axon Growth-Promoting Effects following Inflammatory Stimulation on Mature Retinal Ganglion Cells in Mice Depend on Ciliary Neurotrophic Factor and Leukemia Inhibitory Factor , 2009, The Journal of Neuroscience.

[31]  De-Pei Li,et al.  Aminopyridines Potentiate Synaptic and Neuromuscular Transmission by Targeting the Voltage-activated Calcium Channel β Subunit*♦ , 2009, The Journal of Biological Chemistry.

[32]  L. Krupp,et al.  Sustained-release oral fampridine in multiple sclerosis: a randomised, double-blind, controlled trial , 2009, The Lancet.

[33]  A. Cross,et al.  Fampridine-SR in multiple sclerosis: a randomized, double-blind, placebo-controlled, dose-ranging study , 2007, Multiple sclerosis.

[34]  R. Douglas,et al.  Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. , 2004, Investigative ophthalmology & visual science.

[35]  Lin Chen,et al.  Transcriptional regulation by calcium, calcineurin, and NFAT. , 2003, Genes & development.

[36]  O. McManus,et al.  Identification of a new class of inhibitors of the voltage-gated potassium channel, Kv1.3, with immunosuppressant properties. , 2002, Biochemistry.

[37]  C. Polman,et al.  4-Aminopyridine in patients with multiple sclerosis: dosage and serum level related to efficacy and safety. , 1993, Clinical neuropharmacology.

[38]  S. Thanos,et al.  Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo , 1993, Brain Research.

[39]  H. Korn,et al.  Mechanism of 4-aminopyridine action on voltage-gated potassium channels in lymphocytes , 1992, The Journal of general physiology.

[40]  D. Nicholls,et al.  Repetitive Action Potentials in Isolated Nerve Terminals in the Presence of 4‐Aminopyridine: Effects on Cytosolic Free Ca2+ and Glutamate Release , 1989, Journal of neurochemistry.

[41]  G. Gibson,et al.  Changes in cytosolic free calcium with 1,2,3,4-tetrahydro-5-aminoacridine, 4-aminopyridine and 3,4-diaminopyridine. , 1988, Biochemical pharmacology.

[42]  T A Sears,et al.  The effects of 4‐aminopyridine and tetraethylammonium ions on normal and demyelinated mammalian nerve fibres. , 1981, The Journal of physiology.

[43]  Francesco Viola,et al.  The loss of macular ganglion cells begins from the early stages of disease and correlates with brain atrophy in multiple sclerosis patients , 2019, Multiple sclerosis.

[44]  D. Reich,et al.  Multiple Sclerosis , 2018, The New England journal of medicine.

[45]  Andrew M. Johnson,et al.  The effect of Fampridine-SR on cognitive fatigue in a randomized double-blind crossover trial in patients with MS. , 2017, Multiple sclerosis and related disorders.