Nerve excitability changes related to axonal degeneration in amyotrophic lateral sclerosis: Insights from the transgenic SOD1 G127X mouse model

Experimental Neurology

Volumn 233, Issue 1, 2012, Pages 408-420

  Moldovan, Mihai ^a,c   Alvarez, Susana ^a,c   Pinchenko, Volodymyr ^a   Marklund, Stefan ^b   Graffmo, Karin S ^b   Krarup, Christian ^a,c  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UMEÅ UNIVERSITY   (Sweden)

^c Rigshospitalet   (Denmark)

Author keywords

Excitability; Internode; Ion channels; Motor neuron disease; Mouse model; Nerve activity; Node of Ranvier; Regeneration

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPOUND MOTOR ACTION POTENTIAL; CONTROLLED STUDY; DISEASE CLASSIFICATION; EVOKED MUSCLE RESPONSE; F WAVE; HUMAN; HYPERPOLARIZATION; MATHEMATICAL PARAMETERS; MEMBRANE DEPOLARIZATION; MOTONEURON; MOTOR PERFORMANCE; MOTOR UNIT POTENTIAL; MOUSE; MUSCLE STRENGTH; MUTANT; NERVE CONDUCTION; NERVE DEGENERATION; NERVE EXCITABILITY; NERVE FIBER DEGENERATION; NERVE FIBER MEMBRANE CONDUCTANCE; NERVOUS SYSTEM PARAMETERS; NEUROLOGIC EXAMINATION; NONHUMAN; PRIORITY JOURNAL; REFRACTORY PERIOD; STIMULUS RESPONSE SLOPE; THRESHOLD TRACKING; TIBIAL NERVE; TRANSGENIC MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXONS; DIFFERENTIAL THRESHOLD; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; GLYCINE; HUMANS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MOVEMENT; NEURAL CONDUCTION; REACTION TIME; SUPEROXIDE DISMUTASE; TIBIAL NERVE; TIME FACTORS;

EID: 84856222650     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.11.008     Document Type: Article

References (75)

1. Alvarez S., Moldovan M., Krarup C. Acute energy restriction triggers Wallerian degeneration in mouse. Exp. Neurol. 2008, 212:166-178.
2. Andersen P.M., Nilsson P., Ala-Hurula V., Keranen M.L., Tarvainen I., Haltia T., Nilsson L., Binzer M., Forsgren L., Marklund S.L. Amyotrophic lateral sclerosis associated with homozygosity for an Asp90Ala mutation in CuZn-superoxide dismutase. Nat. Genet. 1995, 10:61-66.
3. Andersen P.M., Nilsson P., Keranen M.L., Forsgren L., Hagglund J., Karlsborg M., Ronnevi L.O., Gredal O., Marklund S.L. Phenotypic heterogeneity in motor neuron disease patients with CuZn-superoxide dismutase mutations in Scandinavia. Brain 1997, 120:1723-1737.
4. Argyropoulos C.J., Panayiotopoulos C.P., Scarpalezos S. F- and M-wave conduction velocity in amyotrophic lateral sclerosis. Muscle Nerve 1978, 1:479-485.
5. Baker M.D., Bostock H., Grafe P., Martius P. Function and distribution of three types of rectifying channel in rat spinal root myelinated axons. J. Physiol. 1987, 383:45-67.
6. Barrett E.F., Barrett J.N. Intracellular recording from vertebrate myelinated axons: mechanism of the depolarizing afterpotential. J. Physiol. 1982, 323:117-144.
7. Bechtold D.A., Yue X., Evans R.M., Davies M., Gregson N.A., Smith K.J. Axonal protection in experimental autoimmune neuritis by the sodium channel blocking agent flecainide. Brain 2005, 128:18-28.
8. Beghi E., Logroscino G., Chio A., Hardiman O., Millul A., Mitchell D., Swingler R., Traynor B.J. Amyotrophic lateral sclerosis, physical exercise, trauma and sports: results of a population-based pilot case-control study. Amyotroph. Lateral Scler. 2010, 11:289-292.
9. Böerio D., Greensmith L., Bostock H. Excitability properties of motor axons in the maturing mouse. J. Peripher. Nerv. Syst. 2009, 14:45-53.
10. Böerio D., Kalmar B., Greensmith L., Bostock H. Excitability properties of mouse motor axons in the mutant SOD1(G93A) model of amyotrophic lateral sclerosis. Muscle Nerve 2010, 41:774-784.
11. Bostock H. The strength-duration relationship for excitation of myelinated nerve: computed dependence on membrane parameters. J. Physiol. 1983, 341:59-74.
12. Bostock H., Baker M. Evidence for two types of potassium channel in human motor axons in vivo. Brain Res. 1988, 462:354-358.
13. Bostock H., Rothwell J.C. Latent addition in motor and sensory fibres of human peripheral nerve. J. Physiol. 1997, 498:277-294.
14. Bostock H., Sharief M.K., Reid G., Murray N.M.F. Axonal ion channel dysfunction in amyotrophic lateral sclerosis. Brain 1995, 118:217-225.
15. Bostock H., Cikurel K., Burke D. Threshold tracking techniques in the study of human peripheral nerve. Muscle Nerve 1998, 21:137-158.
16. Burke D., Kiernan M.C., Bostock H. Excitability of human axons. Clin. Neurophysiol. 2001, 112:1575-1585.
17. Carreras I., Yuruker S., Aytan N., Hossain L., Choi J.K., Jenkins B.G., Kowall N.W., Dedeoglu A. Moderate exercise delays the motor performance decline in a transgenic model of ALS. Brain Res. 2010, 1313:192-201.
18. Daube J.R. Estimating the number of motor units in a muscle. J. Clin. Neurophysiol. 1995, 12:585-594.
19. Daube J.R. Motor unit number estimates-from A to Z. J. Neurol. Sci. 2006, 242:23-35.
20. de Carvalho M., Swash M. Nerve conduction studies in amyotrophic lateral sclerosis. Muscle Nerve 2000, 23:344-352.
21. De Vos K.J., Chapman A.L., Tennant M.E., Manser C., Tudor E.L., Lau K.F., Brownlees J., Ackerley S., Shaw P.J., McLoughlin D.M., Shaw C.E., Leigh P.N., Miller C.C., Grierson A.J. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum. Mol. Genet. 2007, 16:2720-2728.
22. Forsberg K., Jonsson P.A., Andersen P.M., Bergemalm D., Graffmo K.S., Hultdin M., Jacobsson J., Rosquist R., Marklund S.L., Brannstrom T. Novel antibodies reveal inclusions containing non-native SOD1 in sporadic ALS patients. PLoS One 2010, 5:e11552.
23. Forsberg K., Andersen P.M., Marklund S.L., Brannstrom T. Glial nuclear aggregates of superoxide dismutase-1 are regularly present in patients with amyotrophic lateral sclerosis. Acta Neuropathol. 2011, 121:623-634.
24. Guo Y.S., Wu D.X., Wu H.R., Wu S.Y., Yang C., Li B., Bu H., Zhang Y.S., Li C.Y. Sensory involvement in the SOD1-G93A mouse model of amyotrophic lateral sclerosis. Exp. Mol. Med. 2009, 41:140-150.
25. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., Alexander D.D., Caliendo J., Hentati A., Kwon Y.W., Deng H.X. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264:1772-1775.
26. Hegedus J., Putman C.T., Tyreman N., Gordon T. Preferential motor unit loss in the SOD1 G93A transgenic mouse model of amyotrophic lateral sclerosis. J. Physiol. 2008, 586:3337-3351.
27. Hegedus J., Jones K.E., Gordon T. Development and use of the incremental twitch subtraction MUNE method in mice. Suppl. Clin. Neurophysiol. 2009, 60:209-217.
28. Hegedus J., Putman C.T., Gordon T. Progressive motor unit loss in the G93A mouse model of amyotrophic lateral sclerosis is unaffected by gender. Muscle Nerve 2009, 39:318-327.
29. Henderson R.D., Ridall P.G., Hutchinson N.M., Pettitt A.N., McCombe P.A. Bayesian statistical MUNE method. Muscle Nerve 2007, 36:206-213.
30. Herold K.F., Nau C., Ouyang W., Hemmings H.C. Isoflurane inhibits the tetrodotoxin-resistant voltage-gated sodium channel Nav1.8. Anesthesiology 2009, 111:591-599.
31. Hockly E., Woodman B., Mahal A., Lewis C.M., Bates G. Standardization and statistical approaches to therapeutic trials in the R6/2 mouse. Brain Res. Bull. 2003, 61:469-479.
32. Horn S., Quasthoff S., Grafe P., Bostock H., Renner R., Schrank B. Abnormal axonal inward rectification in diabetic neuropathy. Muscle Nerve 1996, 19:1268-1275.
33. Jillapalli D., Shefner J.M. Single motor unit variability with threshold stimulation in patients with amyotrophic lateral sclerosis and normal subjects. Muscle Nerve 2004, 30:578-584.
34. Jonsson P.A., Ernhill K., Andersen P.M., Bergemalm D., Brannstrom T., Gredal O., Nilsson P., Marklund S.L. Minute quantities of misfolded mutant superoxide dismutase-1 cause amyotrophic lateral sclerosis. Brain 2004, 127:73-88.
35. Jonsson P.A., Graffmo K.S., Andersen P.M., Brannstrom T., Lindberg M., Oliveberg M., Marklund S.L. Disulphide-reduced superoxide dismutase-1 in CNS of transgenic amyotrophic lateral sclerosis models. Brain 2006, 129:451-464.
36. Kaji R. Physiological and technical basis of peripheral nerve and motoneuron testing. Physiology of ALS and Related Diseases 1997, 15-41. Elsevier Science, Amsterdam. J. Kimura, R. Kaji (Eds.).
37. 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.
38. Kasselman L.J., Shefner J.M., Rutkove S.B. Motor unit number estimation in the rat tail using a modified multipoint stimulation technique. Muscle Nerve 2009, 40:115-121.
39. Kiernan M.C., Bostock H. Effects of membrane polarization and ischaemia on the excitability properties of human motor axons. Brain 2000, 123:2542-2551.
40. Kiernan M.C., Mogyoros I., Burke D. Differences in the recovery of excitability in sensory and motor axons of human median nerve. Brain 1996, 119:1099-1105.
41. Kiernan M.C., Burke D., Andersen K.V., Bostock H. Multiple measures of axonal excitability: a new approach in clinical testing. Muscle Nerve 2000, 23:399-409.
42. Kiernan M.C., Hart I.K., Bostock H. Excitability properties of motor axons in patients with spontaneous motor unit activity. J. Neurol. Neurosurg. Psychiatry 2001, 70:56-64.
43. Kong J., Xu Z. Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J. Neurosci. 1998, 18:3241-3250.
44. Krarup C. Lower motor neuron involvement examined by quantitative electromyography in amyotrophic lateral sclerosis. Clin. Neurophysiol. 2011, 122:414-422.
45. 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.
46. 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, 27:2501-2514.
47. Lehky T.J., Chen C.J., di Prospero N.A., Rhodes L.E., Fischbeck K., Floeter M.K. Standard and modified statistical MUNE evaluations in spinal-bulbar muscular atrophy. Muscle Nerve 2009, 40:809-814.
48. Mahoney D.J., Rodriguez C., Devries M., Yasuda N., Tarnopolsky M.A. Effects of high-intensity endurance exercise training in the G93A mouse model of amyotrophic lateral sclerosis. Muscle Nerve 2004, 29:656-662.
49. Mancuso R., Santos-Nogueira E., Osta R., Navarro X. Electrophysiological analysis of a murine model of motoneuron disease. Clin. Neurophysiol. 2011, 122:1660-1670.
50. McComas A.J., Fawcett P.R., Campbell M.J., Sica R.E.P. Electrophysiological estimation of the number of motor units within a human muscle. J. Neurol. Neurosurg. Psychiatry 1971, 34:121-131.
51. McHanwell S., Biscoe T.J. The sizes of motoneurons supplying hindlimb muscles in the mouse. Proc. R. Soc. Lond. B Biol. Sci. 1981, 213:201-216.
52. Meehan C.F., Moldovan M., Marklund S.L., Graffmo K.S., Nielsen J.B., Hultborn H. Intrinsic properties of lumbar motor neurones in the adult G127insTGGG superoxide dismutase-1 mutant mouse in vivo: evidence for increased persistent inward currents. Acta Physiol. (Oxf.) 2010, 200:361-376.
53. Miller R.G., Mitchell J.D., Lyon M., Moore D.H. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst. Rev. 2007, CD001447.
54. Mogyoros I., Kiernan M.C., Burke D., Bostock H. Strength-duration properties of sensory and motor axons in amyotrophic lateral sclerosis. Brain 1998, 121:851-859.
55. Moldovan M., Krarup C. Mechanisms of hyperpolarization in regenerated mature motor axons in cat. J. Physiol. 2004, 560:807-819.
56. Moldovan M., Krarup C. Persistent abnormalities of membrane excitability in regenerated mature motor axons in cat. J. Physiol. 2004, 560:795-806.
57. Moldovan M., Alvarez S., Krarup C. Motor axon excitability during Wallerian degeneration. Brain 2009, 132:511-523.
58. Moldovan M., Alvarez S., Pinchenko V., Klein D., Nielsen F.C., Wood J.N., Martini R., Krarup C. Na(v)1.8 channelopathy in mutant mice deficient for myelin protein zero is detrimental to motor axons. Brain 2011, 134:585-601.
59. Mori A., Nodera H., Shibuta Y., Okita T., Bostock H., Kaji R. Threshold-dependent effects on peripheral nerve in vivo excitability properties in the rat. Neurosci. Lett. 2010, 468:248-253.
60. Nakata M., Baba H., Kanai K., Hoshi T., Sawai S., Hattori T., Kuwabara S. Changes in Na(+) channel expression and nodal persistent Na(+) currents associated with peripheral nerve regeneration in mice. Muscle Nerve 2008, 37:721-730.
61. Özdinler P.H., Benn S., Yamamoto T.H., Güzel M., Brown R.H., Macklis J.D. Corticospinal motor neurons and related subcerebral projection neurons undergo early and specific neurodegeneration in hSOD1(G93A) transgenic ALS mice. J. Neurosci. 2011, 31:4166-4177.
62. Reaume A.G., Elliott J.L., Hoffman E.K., Kowall N.W., Ferrante R.J., Siwek D.F., Wilcox H.M., Flood D.G., Beal M.F., Brown R.H., Scott R.W., Snider W.D. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 1996, 13:43-47.
63. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
64. Rowlatt C., Chesterman F.C., Sheriff M.U. Lifespan, age changes and tumour incidence in an ageing C57BL mouse colony. Lab. Anim. 1976, 10:419-442.
65. Sawai S., Kanai K., Nakata M., Hiraga A., Misawa S., Isose S., Hattori T., Kuwabara S. Changes in excitability properties associated with axonal regeneration in human neuropathy and mouse Wallerian degeneration. Clin. Neurophysiol. 2008, 119:1097-1105.
66. Scarmeas N., Shih T., Stern Y., Ottman R., Rowland L.P. Premorbid weight, body mass, and varsity athletics in ALS. Neurology 2002, 59:773-775.
67. Schwarz J.R., Glassmeier G., Cooper E.C., Kao T.C., Nodera H., Tabuena D., Kaji R., Bostock H. KCNQ channels mediate IKs, a slow K+ current regulating excitability in the rat node of Ranvier. J. Physiol. 2006, 573:17-34.
68. Shefner J.M., Cudkowicz M., Brown R.H. Motor unit number estimation predicts disease onset and survival in a transgenic mouse model of amyotrophic lateral sclerosis. Muscle Nerve 2006, 34:603-607.
69. Shefner J.M., Cudkowicz M.E., Zhang H., Schoenfeld D., Jillapalli D. Revised statistical motor unit number estimation in the Celecoxib/ALS trial. Muscle Nerve 2007, 35:228-234.
70. Shibuta Y., Nodera H., Mori A., Okita T., Kaji R. Peripheral nerve excitability measures at different target levels: the effects of aging and diabetic neuropathy. J. Clin. Neurophysiol. 2010, 27:350-357.
71. 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.
72. Urbani A., Belluzzi O. Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur. J. Neurosci. 2000, 12:3567-3574.
73. Vucic S., Kiernan M.C. Axonal excitability properties in amyotrophic lateral sclerosis. Clin. Neurophysiol. 2006, 117:1458-1466.
74. Vucic S., Kiernan M.C. Upregulation of persistent sodium conductances in familial ALS. J. Neurol. Neurosurg. Psychiatry 2010, 81:222-227.
75. Yang Q., Kaji R., Hirota N., Kojima Y., Takagi T., Kohara N., Kimura J., Shibasaki H., Bostock H. Effect of maturation on nerve excitability in an experimental model of threshold electrotonus. Muscle Nerve 2000, 23:498-506.