Intrinsic membrane hyperexcitability of amyotrophic lateral sclerosis patient-derived motor neurons

Cell Reports

Volumn 7, Issue 1, 2014, Pages 1-11

  Wainger, Brian J ^a,b   Kiskinis, Evangelos ^c   Mellin, Cassidy ^a   Wiskow, Ole ^c   Han, Steve S W ^b,c   Sandoe, Jackson ^c   Perez, Numa P ^a   Williams, Luis A ^c   Lee, Seungkyu ^a   Boulting, Gabriella ^c   Berry, James D ^b   Brown, Robert H ^d   Cudkowicz, Merit E ^b   Bean, Bruce P ^e   Eggan, Kevin ^b,c,f   Woolf, Clifford J ^a,e  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Harvard University   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELAYED RECTIFIER POTASSIUM CHANNEL; COPPER ZINC SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; MOTONEURON; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE; NERVE CONDUCTION; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHENOTYPE; PLURIPOTENT STEM CELL; POTASSIUM CURRENT; PRIORITY JOURNAL; ACTION POTENTIAL; CELL CULTURE; CELL DIFFERENTIATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MUTATION; PATHOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; AMYOTROPHIC LATERAL SCLEROSIS; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MOTOR NEURONS; MUTATION; PATCH-CLAMP TECHNIQUES; PHENOTYPE; SUPEROXIDE DISMUTASE;

EID: 84898034713     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.019     Document Type: Article

References (48)

1. Bae J.S., Sawai S., Misawa S., Kanai K., Isose S., Kuwabara S. Differences in excitability properties of FDI and ADM motor axons. Muscle Nerve 2009, 39:350-354.
2. Blair I.P., Williams K.L., Warraich S.T., Durnall J.C., Thoeng A.D., Manavis J., Blumbergs P.C., Vucic S., Kiernan M.C., Nicholson G.A. FUS mutations in amyotrophic lateral sclerosis: clinical, pathological, neurophysiological and genetic analysis. J.Neurol. Neurosurg. Psychiatry 2010, 81:639-645.
3. Bock C., Kiskinis E., Verstappen G., Gu H., Boulting G., Smith Z.D., Ziller M., Croft G.F., Amoroso M.W., Oakley D.H., et al. Reference Maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 2011, 144:439-452.
4. Boehler M.D., Wheeler B.C., Brewer G.J. Added astroglia promote greater synapse density and higher activity in neuronal networks. Neuron Glia Biol. 2007, 3:127-140.
5. Bostock H., Sharief M.K., Reid G., Murray N.M. Axonal ion channel dysfunction in amyotrophic lateral sclerosis. Brain 1995, 118:217-225.
6. Boulting G.L., Kiskinis E., Croft G.F., Amoroso M.W., Oakley D.H., Wainger B.J., Williams D.J., Kahler D.J., Yamaki M., Davidow L., et al. A functionally characterized test set of human induced pluripotent stem cells. Nat. Biotechnol. 2011, 29:279-286.
7. Brown D.A., Passmore G.M. Neural KCNQ (Kv7) channels. Br. J. Pharmacol. 2009, 156:1185-1195.
8. Chambers S.M., Fasano C.A., Papapetrou E.P., Tomishima M., Sadelain M., Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 2009, 27:275-280.
9. Chan C.S., Guzman J.N., Ilijic E., Mercer J.N., Rick C., Tkatch T., Meredith G.E., Surmeier D.J. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 2007, 447:1081-1086.
10. Cleveland D.W., Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2001, 2:806-819.
11. Cohen M.R., Kohn A. Measuring and interpreting neuronal correlations. Nat. Neurosci. 2011, 14:811-819.
12. Figueroa-Romero C., Hur J., Bender D.E., Delaney C.E., Cataldo M.D., Smith A.L., Yung R., Ruden D.M., Callaghan B.C., Feldman E.L. Identification of epigenetically altered genes in sporadic amyotrophic lateral sclerosis. PLoS ONE 2012, 7:e52672.
13. Fritz E., Izaurieta P., Weiss A., Mir F.R., Rojas P., Gonzalez D., Rojas F., Brown R.H., Madrid R., van Zundert B. Mutant SOD1-expressing astrocytes release toxic factors that trigger motoneuron death by inducing hyperexcitability. J.Neurophysiol. 2013, 109:2803-2814.
14. Gogliotti R.G., Quinlan K.A., Barlow C.B., Heier C.R., Heckman C.J., Didonato C.J. Motor neuron rescue in spinal muscular atrophy mice demonstrates that sensory-motor defects are a consequence, not a cause, of motor neuron dysfunction. J.Neurosci. 2012, 32:3818-3829.
15. Hanson M.G., Landmesser L.T. Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 2004, 43:687-701.
16. Imlach W.L., Beck E.S., Choi B.J., Lotti F., Pellizzoni L., McCabe B.D. SMN is required for sensory-motor circuit function in Drosophila. Cell 2012, 151:427-439.
17. Ince P.G., Highley J.R., Kirby J., Wharton S.B., Takahashi H., Strong M.J., Shaw P.J. Molecular pathology and genetic advances in amyotrophic lateral sclerosis: an emerging molecular pathway and the significance of glial pathology. Acta Neuropathol. 2011, 122:657-671.
18. Kanai K., Kuwabara S., Misawa S., Tamura N., Ogawara K., Nakata M., Sawai S., Hattori T., Bostock H. Altered axonal excitability properties in amyotrophic lateral sclerosis: impaired potassium channel function related to disease stage. Brain 2006, 129:953-962.
19. Kanai K., Shibuya K., Sato Y., Misawa S., Nasu S., Sekiguchi Y., Mitsuma S., Isose S., Fujimaki Y., Ohmori S., et al. Motor axonal excitability properties are strong predictors for survival in amyotrophic lateral sclerosis. J.Neurol. Neurosurg. Psychiatry 2012, 83:734-738.
20. Kiernan M.C., Vucic S., Cheah B.C., Turner M.R., Eisen A., Hardiman O., Burrell J.R., Zoing M.C. Amyotrophic lateral sclerosis. Lancet 2011, 377:942-955.
21. Kiskinis E., Sandoe J., Williams L.A., Boulting G.L., Moccia R., Wainger B.J., Han S., Peng T., Thams S., Mikkilineni S., et al. Pathways disrupted in human ALS motor neurons identified through genetic correction of mutant SOD1. Cell Stem Cell 2014, 14. Published online April 3, 2014. 10.1016/j.stem.2014.03.004.
22. Kuo J.J., Schonewille M., Siddique T., Schults A.N., Fu R., Bär P.R., Anelli R., Heckman C.J., Kroese A.B. Hyperexcitability of cultured spinal motoneurons from presymptomatic ALS mice. J.Neurophysiol. 2004, 91:571-575.
23. Kuo J.J., Siddique T., Fu R., Heckman C.J. Increased persistent Na(+) current and its effect on excitability in motoneurones cultured from mutant SOD1 mice. J.Physiol. 2005, 563:843-854.
24. Marchetto M.C., Muotri A.R., Mu Y., Smith A.M., Cezar G.G., Gage F.H. Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 2008, 3:649-657.
25. Mentis G.Z., Blivis D., Liu W., Drobac E., Crowder M.E., Kong L., Alvarez F.J., Sumner C.J., O'Donovan M.J. Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron 2011, 69:453-467.
26. Mills K.R., Nithi K.A. Corticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis. Muscle Nerve 1997, 20:1137-1141.
27. Nakata M., Kuwabara S., Kanai K., Misawa S., Tamura N., Sawai S., Hattori T., Bostock H. Distal excitability changes in motor axons in amyotrophic lateral sclerosis. Clin. Neurophysiol. 2006, 117:1444-1448.
28. Pasinelli P., Brown R.H. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 2006, 7:710-723.
29. Pieri M., Albo F., Gaetti C., Spalloni A., Bengtson C.P., Longone P., Cavalcanti S., Zona C. Altered excitability of motor neurons in a transgenic mouse model of familial amyotrophic lateral sclerosis. Neurosci. Lett. 2003, 351:153-156.
30. Porter R.J., Partiot A., Sachdeo R., Nohria V., Alves W.M. Randomized, multicenter, dose-ranging trial of retigabine for partial-onset seizures. Neurology 2007, 68:1197-1204. 205 Study Group.
31. Robberecht W., Philips T. The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 2013, 14:248-264.
32. Sandoe J., Eggan K. Opportunities and challenges of pluripotent stem cell neurodegenerative disease models. Nat. Neurosci. 2013, 16:780-789.
33. Sareen D., O'Rourke J.G., Meera P., Muhammad A.K., Grant S., Simpkinson M., Bell S., Carmona S., Ornelas L., Sahabian A., Gendron T., Petrucelli L., Baughn M., Ravits J., Harms M.B., Rigo F., Bennett C.F., Otis T.S., Svendsen C.N., Baloh R.H. Targeting RNA foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci. Transl. Med. 2013, 5:208ra149.
34. Saxena S., Caroni P. Selective neuronal vulnerability in neurodegenerative diseases: from stressor thresholds to degeneration. Neuron 2011, 71:35-48.
35. Saxena S., Roselli F., Singh K., Leptien K., Julien J.P., Gros-Louis F., Caroni P. Neuroprotection through excitability and mTOR required in ALS motoneurons to delay disease and extend survival. Neuron 2013, 80:80-96.
36. Sesti F., Liu S., Cai S.Q. Oxidation of potassium channels by ROS: a general mechanism of aging and neurodegeneration?. Trends Cell Biol. 2010, 20:45-51.
37. Shibuya K., Misawa S., Arai K., Nakata M., Kanai K., Yoshiyama Y., Ito K., Isose S., Noto Y., Nasu S., et al. Markedly reduced axonal potassium channel expression in human sporadic amyotrophic lateral sclerosis: an immunohistochemical study. Exp. Neurol. 2011, 232:149-153.
38. Sun W., Maffie J.K., Lin L., Petralia R.S., Rudy B., Hoffman D.A. DPP6 establishes the A-type K(+) current gradient critical for the regulation of dendritic excitability in CA1 hippocampal neurons. Neuron 2011, 71:1102-1115.
39. Tamura N., Kuwabara S., Misawa S., Kanai K., Nakata M., Sawai S., Hattori T. Increased nodal persistent Na+ currents in human neuropathy and motor neuron disease estimated by latent addition. Clin. Neurophysiol. 2006, 117:2451-2458.
40. Urbani A., Belluzzi O. Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur. J. Neurosci. 2000, 12:3567-3574.
41. van Es M.A., van Vught P.W., Blauw H.M., Franke L., Saris C.G., Van den Bosch L., de Jong S.W., de Jong V., Baas F., van't Slot R., et al. Genetic variation in DPP6 is associated with susceptibility to amyotrophic lateral sclerosis. Nat. Genet. 2008, 40:29-31.
42. van Es M.A., van Vught P.W., van Kempen G., Blauw H.M., Veldink J.H., van den Berg L.H. Dpp6 is associated with susceptibility to progressive spinal muscular atrophy. Neurology 2009, 72:1184-1185.
43. van Zundert B., Peuscher M.H., Hynynen M., Chen A., Neve R.L., Brown R.H., Constantine-Paton M., Bellingham M.C. Neonatal neuronal circuitry shows hyperexcitable disturbance in a mouse model of theadult-onset neurodegenerative disease amyotrophic lateral sclerosis. J.Neurosci. 2008, 28:10864-10874.
44. Vucic S., Kiernan M.C. Axonal excitability properties in amyotrophic lateral sclerosis. Clin. Neurophysiol. 2006, 117:1458-1466.
45. Vucic S., Kiernan M.C. Upregulation of persistent sodium conductances in familial ALS. J.Neurol. Neurosurg. Psychiatry 2010, 81:222-227.
46. Waters M.F., Minassian N.A., Stevanin G., Figueroa K.P., Bannister J.P., Nolte D., Mock A.F., Evidente V.G., Fee D.B., Müller U., et al. Mutations in voltage-gated potassium channel KCNC3 cause degenerative and developmental central nervous system phenotypes. Nat. Genet. 2006, 38:447-451.
47. Wickenden A.D., Yu W., Zou A., Jegla T., Wagoner P.K. Retigabine, a novel anti-convulsant, enhances activation of KCNQ2/Q3 potassium channels. Mol. Pharmacol. 2000, 58:591-600.
48. Williams K.L., Fifita J.A., Vucic S., Durnall J.C., Kiernan M.C., Blair I.P., Nicholson G.A. Pathophysiological insights into ALS with C9ORF72 expansions. J.Neurol. Neurosurg. Psychiatry 2013, 84:931-935.