Gender-specific perturbations in modulatory inputs to motoneurons in a mouse model of amyotrophic lateral sclerosis

Neuroscience

Volumn 226, Issue , 2012, Pages 313-323

  Herron, L R ^a   Miles, G B ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

Plasticity; Spinal cord; Synapse

Indexed keywords

MUSCARINIC M1 RECEPTOR; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV2.1; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN STEM; CELL LOSS; CONTROLLED STUDY; DENDRITE; FEMALE; GENOTYPE; GLIA CELL; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOTONEURON; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SOMATOSENSORY SYSTEM; SPINAL CORD; SYMPTOMATOLOGY;

AGING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, NEWBORN; CELL COUNT; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MOTOR NEURONS; MUTATION; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; SEX CHARACTERISTICS; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 84867432434     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.031     Document Type: Article

References (78)

1. Alexander G.M., Erwin K.L., Byers N., Deitch J.S., Augelli B.J., Blankenhorn E.P., Heiman-Patterson T.D. Effect of transgene copy number on survival in the G93A SOD1 transgenic mouse model of ALS. Brain Res Mol Brain Res 2004, 130:7-15.
2. Amendola J., Durand J. Morphological differences between wild-type and transgenic superoxide dismutase 1 lumbar motoneurons in postnatal mice. J Comp Neurol 2008, 511:329-341.
3. Anneser J.M., Cookson M.R., Ince P.G., Shaw P.J., Borasio G.D. Glial cells of the spinal cord and subcortical white matter up-regulate neuronal nitric oxide synthase in sporadic amyotrophic lateral sclerosis. Exp Neurol 2001, 171:418-421.
4. Apostolova I., Irintchev A., Schachner M. Tenascin-R restricts posttraumatic remodeling of motoneuron innervation and functional recovery after spinal cord injury in adult mice. J Neurosci 2006, 26:7849-7859.
5. Avossa D., Grandolfo M., Mazzarol F., Zatta M., Ballerini L. Early signs of motoneuron vulnerability in a disease model system: Characterization of transverse slice cultures of spinal cord isolated from embryonic ALS mice. Neuroscience 2006, 138:1179-1194.
6. Beers D.R., Henkel J.S., Xiao Q., Zhao W., Wang J., Yen A.A., Siklos L., McKercher S.R., Appel S.H. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2006, 103:16021-16026.
7. Bendotti C., Calvaresi N., Chiveri L., Prelle A., Moggio M., Braga M., Silani V., De Biasi S. Early vacuolization and mitochondrial damage in motor neurons of FALS mice are not associated with apoptosis or with changes in cytochrome oxidase histochemical reactivity. J Neurol Sci 2001, 191:25-33.
8. Bento-Abreu A., Van Damme P., Van Den Bosch L., Robberecht W. The neurobiology of amyotrophic lateral sclerosis. Eur J Neurosci 2010, 31:2247-2265.
9. Boillee S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., Kollias G., Cleveland D.W. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
10. Bories C., Amendola J., Lamotte d'Incamps B., Durand J. Early electrophysiological abnormalities in lumbar motoneurons in a transgenic mouse model of amyotrophic lateral sclerosis. Eur J Neurosci 2007, 25:451-459.
11. Brownstone R.M., Bui T.V. Spinal interneurons providing input to the final common path during locomotion. Prog Brain Res 2010, 187:81-95.
12. Carunchio I., Mollinari C., Pieri M., Merlo D., Zona C. GAB(A) receptors present higher affinity and modified subunit composition in spinal motor neurons from a genetic model of amyotrophic lateral sclerosis. Eur J Neurosci 2008, 28:1275-1285.
13. Catania M.V., Aronica E., Yankaya B., Troost D. Increased expression of neuronal nitric oxide synthase spliced variants in reactive astrocytes of amyotrophic lateral sclerosis human spinal cord. J Neurosci 2001, 21:RC148.
14. Chang Q., Martin L.J. Glycinergic innervation of motoneurons is deficient in amyotrophic lateral sclerosis mice. a quantitative confocal analysis. Am J Pathol 2009, 174:574-585.
15. Chang Q., Martin L.J. Glycine receptor channels in spinal motoneurons are abnormal in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurosci 2011, 31:2815-2827.
16. Clement A.M., Nguyen M.D., Roberts E.A., Garcia M.L., Boillee S., Rule M., McMahon A.P., Doucette W., Siwek D., Ferrante R.J., Brown R.H., Julien J.P., Goldstein L.S., Cleveland D.W. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 2003, 302:113-117.
17. Conradi S., Skoglund S. Observations on the ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the cat during postnatal development. Acta Physiol Scand Suppl 1969, 333:5-52.
18. Cudkowicz M.E., Pastusza K.A., Sapp P.C., Mathews R.K., Leahy J., Pasinelli P., Francis J.W., Jiang D., Andersen J.K., Brown R.H. Survival in transgenic ALS mice does not vary with CNS glutathione peroxidase activity. Neurology 2002, 59:729-734.
19. Di Giorgio F.P., Carrasco M.A., Siao M.C., Maniatis T., Eggan K. Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 2007, 10:608-614.
20. ElBasiouny S.M., Amendola J., Durand J., Heckman C.J. Evidence from computer simulations for alterations in the membrane biophysical properties and dendritic processing of synaptic inputs in mutant superoxide dismutase-1 motoneurons. J Neurosci 2010, 30:5544-5558.
21. Fornai F., Longone P., Cafaro L., Kastsiuchenka O., Ferrucci M., Manca M.L., Lazzeri G., Spalloni A., Bellio N., Lenzi P., Modugno N., Siciliano G., Isidoro C., Murri L., Ruggieri S., Paparelli A. Lithium delays progression of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2008, 105:2052-2057.
22. Frey D., Schneider C., Xu L., Borg J., Spooren W., Caroni P. Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 2000, 20:2534-2542.
23. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 2009, 10:507-518.
24. 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., et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264:1772-1775.
25. Hayworth C.R., Gonzalez-Lima F. Pre-symptomatic detection of chronic motor deficits and genotype prediction in congenic B6.SOD1(G93A) ALS mouse model. Neuroscience 2009, 164:975-985.
26. Heiman-Patterson T.D., Deitch J.S., Blankenhorn E.P., Erwin K.L., Perreault M.J., Alexander B.K., Byers N., Toman I., Alexander G.M. Background and gender effects on survival in the TgN(SOD1-G93A)1Gur mouse model of ALS. J Neurol Sci 2005, 236:1-7.
27. Hellstrom J., Arvidsson U., Elde R., Cullheim S., Meister B. Differential expression of nerve terminal protein isoforms in VAChT-containing varicosities of the spinal cord ventral horn. J Comp Neurol 1999, 411:578-590.
28. Hellstrom J., Oliveira A.L., Meister B., Cullheim S. Large cholinergic nerve terminals on subsets of motoneurons and their relation to muscarinic receptor type 2. J Comp Neurol 2003, 460:476-486.
29. Hossaini M., Cano S.C., van Dis V., Haasdijk E.D., Hoogenraad C.C., Holstege J.C., Jaarsma D. Spinal inhibitory interneuron pathology follows motor neuron degeneration independent of glial mutant superoxide dismutase 1 expression in SOD1-ALS mice. J Neuropathol Exp Neurol 2011, 70:662-677.
30. Ikemoto A., Nakamura S., Akiguchi I., Hirano A. Differential expression between synaptic vesicle proteins and presynaptic plasma membrane proteins in the anterior horn of amyotrophic lateral sclerosis. Acta Neuropathol 2002, 103:179-187.
31. Ilieva H., Polymenidou M., Cleveland D.W. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J Cell Biol 2009, 187:761-772.
32. Ince P.G., Slade J., Chinnery R.M., McKenzie J., Royston C., Roberts G.W., Shaw P.J. Quantitative study of synaptophysin immunoreactivity of cerebral cortex and spinal cord in motor neuron disease. J Neuropathol Exp Neurol 1995, 54:673-679.
33. Jaarsma D., Teuling E., Haasdijk E.D., De Zeeuw C.I., Hoogenraad C.C. Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J Neurosci 2008, 28:2075-2088.
34. Jakovcevski I., Wu J., Karl N., Leshchyns'ka I., Sytnyk V., Chen J., Irintchev A., Schachner M. Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. J Neurosci 2007, 27:7222-7233.
35. Jiang M., Schuster J.E., Fu R., Siddique T., Heckman C.J. Progressive changes in synaptic inputs to motoneurons in adult sacral spinal cord of a mouse model of amyotrophic lateral sclerosis. J Neurosci 2009, 29:15031-15038.
36. Kanning K.C., Kaplan A., Henderson C.E. Motor neuron diversity in development and disease. Annu Rev Neurosci 2010, 33:409-440.
37. 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.
38. Kuo J.J., Schonewille M., Siddique T., Schults A.N., Fu R., Bar 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.
39. 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.
40. Li W., Ochalski P.A., Brimijoin S., Jordan L.M., Nagy J.I. C-terminals on motoneurons: electron microscope localization of cholinergic markers in adult rats and antibody-induced depletion in neonates. Neuroscience 1995, 65:879-891.
41. Lino M.M., Schneider C., Caroni P. Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J Neurosci 2002, 22:4825-4832.
42. Martin L.J., Liu Z., Chen K., Price A.C., Pan Y., Swaby J.A., Golden W.C. Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice. mechanisms of mitochondriopathy and cell death. J Comp Neurol 2007, 500:20-46.
43. Matsumoto A. Androgen stimulates neuronal plasticity in the perineal motoneurons of aged male rats. J Comp Neurol 2001, 430:389-395.
44. Matsumoto S., Goto S., Kusaka H., Ito H., Imai T. Synaptic pathology of spinal anterior horn cells in amyotrophic lateral sclerosis: an immunohistochemical study. J Neurol Sci 1994, 125:180-185.
45. Matsumoto A., Micevych P.E., Arnold A.P. Androgen regulates synaptic input to motoneurons of the adult rat spinal cord. J Neurosci 1998, 8:4168-4176.
46. McCombe P.A., Henderson R.D. Effects of gender in amyotrophic lateral sclerosis. Gend Med: official journal of the partnership for gender-specific medicine at Columbia University 2010, 7:557-570.
47. Mehanna A., Jakovcevski I., Acar A., Xiao M., Loers G., Rougon G., Irintchev A., Schachner M. Polysialic acid glycomimetic promotes functional recovery and plasticity after spinal cord injury in mice. Mol Ther J Am Soc Gene Ther 2010, 18:34-43.
48. Miles G.B., Hartley R., Todd A.J., Brownstone R.M. Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc Natl Acad Sci USA 2007, 104:2448-2453.
49. Militello A., Vitello G., Lunetta C., Toscano A., Maiorana G., Piccoli T., La Bella V. The serum level of free testosterone is reduced in amyotrophic lateral sclerosis. J Neurol Sci 2002, 195:67-70.
50. Morrison B.M., Janssen W.G., Gordon J.W., Morrison J.H. Time course of neuropathology in the spinal cord of G86R superoxide dismutase transgenic mice. J Comp Neurol 1998, 391:64-77.
51. Muennich E.A., Fyffe R.E. Focal aggregation of voltage-gated, Kv2.1 subunit-containing, potassium channels at synaptic sites in rat spinal motoneurones. J Physiol 2004, 554:673-685.
52. Nagai M., Re D.B., Nagata T., Chalazonitis A., Jessell T.M., Wichterle H., Przedborski S. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 2007, 10:615-622.
53. Nagao M., Misawa H., Kato S., Hirai S. Loss of cholinergic synapses on the spinal motor neurons of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 1998, 57:329-333.
54. Pambo-Pambo A., Durand J., Gueritaud J.P. Early excitability changes in lumbar motoneurons of transgenic SOD1G85R and SOD1G(93A-Low) mice. J Neurophysiol 2009, 102:3627-3642.
55. 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.
56. Pramatarova A., Laganiere J., Roussel J., Brisebois K., Rouleau G.A. Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J Neurosci 2001, 21:3369-3374.
57. Pullen A.H., Athanasiou D. Increase in presynaptic territory of C-terminals on lumbar motoneurons of G93A SOD1 mice during disease progression. Eur J Neurosci 2009, 29:551-561.
58. Quinlan K.A., Schuster J.E., Fu R., Siddique T., Heckman C.J. Altered postnatal maturation of electrical properties in spinal motoneurons in a mouse model of amyotrophic lateral sclerosis. J Physiol 2011, 589:2245-2260.
59. Raoul C., Estevez A.G., Nishimune H., Cleveland D.W., deLapeyriere O., Henderson C.E., Haase G., Pettmann B. Motoneuron death triggered by a specific pathway downstream of Fas. potentiation by ALS-linked SOD1 mutations. Neuron 2002, 35:1067-1083.
60. Raynor E.M., Shefner J.M. Recurrent inhibition is decreased in patients with amyotrophic lateral sclerosis. Neurology 1994, 44:2148-2153.
61. Sasaki S., Iwata M. Synaptic loss in anterior horn neurons in lower motor neuron disease. Acta Neuropathol 1996, 91:416-421.
62. Sasaki S., Maruyama S. Synapse loss in anterior horn neurons in amyotrophic lateral sclerosis. Acta Neuropathol 1994, 88:222-227.
63. Sasaki S., Warita H., Abe K., Iwata M. Neuronal nitric oxide synthase (nNOS) immunoreactivity in the spinal cord of transgenic mice with G93A mutant SOD1 gene. Acta Neuropathol 2002, 103:421-427.
64. Schiffer D., Cordera S., Giordana M.T., Attanasio A., Pezzulo T. Synaptic vesicle proteins, synaptophysin and chromogranin A in amyotrophic lateral sclerosis. J Neurol Sci 1995, 129:68-74.
65. Schutz B. Imbalanced excitatory to inhibitory synaptic input precedes motor neuron degeneration in an animal model of amyotrophic lateral sclerosis. Neurobiol Dis 2005, 20:131-140.
66. Snow R.J., Turnbull J., da Silva S., Jiang F., Tarnopolsky M.A. Creatine supplementation and riluzole treatment provide similar beneficial effects in copper, zinc superoxide dismutase (G93A) transgenic mice. Neuroscience 2003, 119:661-667.
67. Stephens B., Guiloff R.J., Navarrete R., Newman P., Nikhar N., Lewis P. Widespread loss of neuronal populations in the spinal ventral horn in sporadic motor neuron disease. A morphometric study. J Neurol Sci 2006, 244:41-58.
68. Sunico C.R., Dominguez G., Garcia-Verdugo J.M., Osta R., Montero F., Moreno-Lopez B. Reduction in the motoneuron inhibitory/excitatory synaptic ratio in an early-symptomatic mouse model of amyotrophic lateral sclerosis. Brain Pathol 2011, 21:1-15.
69. Tu P.H., Raju P., Robinson K.A., Gurney M.E., Trojanowski J.Q., Lee V.M. Transgenic mice carrying a human mutant superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. Proc Natl Acad Sci USA 1996, 93:3155-3160.
70. Turner B.J., Talbot K. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog Neurobiol 2008, 85:94-134.
71. 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 the adult-onset neurodegenerative disease amyotrophic lateral sclerosis. J Neurosci 2008, 28:10864-10874.
72. Vivekananda U., Manjalay Z.R., Ganesalingam J., Simms J., Shaw C.E., Leigh P.N., Turner M.R., Al-Chalabi A. Low index-to-ring finger length ratio in sporadic ALS supports prenatally defined motor neuronal vulnerability. J Neurol Neurosurg Psychiatry 2011, 82:635-637.
73. Wilson J.M., Rempel J., Brownstone R.M. Postnatal development of cholinergic synapses on mouse spinal motoneurons. J Comp Neurol 2004, 474:13-23.
74. Wooley C.M., Sher R.B., Kale A., Frankel W.N., Cox G.A., Seburn K.L. Gait analysis detects early changes in transgenic SOD1(G93A) mice. Muscle Nerve 2005, 32:43-50.
75. Yamanaka K., Boillee S., Roberts E.A., Garcia M.L., McAlonis-Downes M., Mikse O.R., Cleveland D.W., Goldstein L.S. Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc Natl Acad Sci USA 2008, 105:7594-7599.
76. Zagoraiou L., Akay T., Martin J.F., Brownstone R.M., Jessell T.M., Miles G.B. A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 2009, 64:645-662.
77. Zhao P., Ignacio S., Beattie E.C., Abood M.E. Altered presymptomatic AMPA and cannabinoid receptor trafficking in motor neurons of ALS model mice: implications for excitotoxicity. Eur J Neurosci 2008, 27:572-579.
78. Zona C., Pieri M., Carunchio I. Voltage-dependent sodium channels in spinal cord motor neurons display rapid recovery from fast inactivation in a mouse model of amyotrophic lateral sclerosis. J Neurophysiol 2006, 96:3314-3322.