Neonatal neuronal circuitry shows hyperexcitable disturbance in a mouse model of the adult-onset neurodegenerative disease amyotrophic lateral sclerosis

Journal of Neuroscience

Volumn 28, Issue 43, 2008, Pages 10864-10874

  Van Zundert, Brigitte ^a,b,e   Peuscher, Marieke H ^a   Hynynen, Meri ^b   Chen, Adam ^b   Neve, Rachael L ^c   Brown Jr , Robert H ^b   Constantine Paton, Martha ^a   Bellingham, Mark C ^a,d  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c MCLEAN HOSPITAL   (United States)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF CONCEPCIÓN   (Chile)

Author keywords

Action potential; Brainstem; Dendrite; EPSP; Interneuron; IPSP; Locomotor activity; Motor neuron; Sodium channel; Superior colliculus; Synaptic transmission

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; COPPER ZINC SUPEROXIDE DISMUTASE 1; GREEN FLUORESCENT PROTEIN; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; AMINO ACID RECEPTOR STIMULATING AGENT; SOD1 G93A PROTEIN; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DENDRITE; HYPOGLOSSAL NERVE; INTERNEURON; MOTONEURON; MOTOR DYSFUNCTION; MOUSE; NERVE CELL DEGENERATION; NERVE EXCITABILITY; NONHUMAN; PATCH CLAMP; PERINATAL PERIOD; PRIORITY JOURNAL; SUPERIOR COLLICULUS; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; CELL MEMBRANE POTENTIAL; CLASSIFICATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; ELECTROSTIMULATION; FEMALE; GENETICS; HEMISPHERIC DOMINANCE; HUMAN; IN VITRO STUDY; MALE; NERVE CELL; NERVE CELL NETWORK; NERVE TRACT; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION RESPONSE; TRANSGENIC MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; FEMALE; FUNCTIONAL LATERALITY; GAMMA-AMINOBUTYRIC ACID; HUMANS; MALE; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; NERVE NET; NEURAL PATHWAYS; NEURONS; PATCH-CLAMP TECHNIQUES; SUPERIOR COLLICULI; SUPEROXIDE DISMUTASE;

EID: 58149173426     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1340-08.2008     Document Type: Article

References (69)

1. Aamodt SM, Shi J, Colonnese MT, Veras W, Constantine-Paton M (2000) Chronic NMDA exposure accelerates development of GABAergic inhibition in the superior colliculus. J Neurophysiol 83:1580-1591.
2. Alessandri-Haber N, Alcaraz G, Deleuze C, Jullien F, Manrique C, Couraud F, Crest M, Giraud P (2002) Molecular determinants of emerging excitability in rat embryonic motoneurons. J Physiol 541:25-39.
3. Amendola J, Verrier B, Roubertoux P, Durand J (2004) Altered sensorimotor development in a transgenic mouse model of amyotrophic lateral sclerosis. Eur J Neurosci 20:2822-2826.
4. Astman N, Gutnick MJ, Fleidervish IA (1998) Activation of protein kinase C increases neuronal excitability by regulating persistent Na+ current in mouse neocortical slices. J Neurophysiol 80:1547-1551.
5. Banks GB, Kanjhan R, Wiese S, Kneussel M, Wong LM, O'Sullivan G, Sendtner M, Bellingham MC, Betz H, Noakes PG (2005) Glycinergic and GABAergic synaptic activity differentially regulate motoneuron survival and skeletal muscle innervation. J Neurosci 25:1249-1259.
6. Bellingham MC, Berger AJ (1996) Presynaptic depression of excitatory synaptic inputs to rat hypoglossal motoneurons by muscarinic M2 receptors. J Neurophysiol 76:3758-3770.
7. Bendotti C, Calvaresi N, Chiveri L, Prelle A, Moggio M, Braga M, Silani V, De Biasi S (2001) 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 191:25-33.
8. Boillée S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-1392.
9. Brown RH Jr, Robberecht W (2001) Amyotrophic lateral sclerosis: pathogenesis. Semin Neurol 21:131-139.
10. + channels: an unexpected form of cellular plasticity. Nat Rev Neurosci 2:397-407.
11. Carlin KP, Jiang Z, Brownstone RM (2000) Characterization of calcium currents in functionally mature mouse spinal motoneurons. Eur J Neurosci 12:1624-1634.
12. Clarke G, Lumsden CJ, McInnes RR (2001) Inherited neurodegenerative diseases: the one-hit model of neurodegeneration. Hum Mol Genet 10:2269-2275.
13. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillée S, Rule M, Mc-Mahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH Jr, Julien JP, Goldstein LS, Cleveland DW (2003) Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113-117.
14. Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2:806-819.
15. Colonnese MT, Shi J, Constantine-Paton M (2003) Chronic NMDA receptor blockade from birth delays the maturation of NMDA currents, but does not affect AMPA/kainate currents. J Neurophysiol 89:57-68.
16. DeKosky ST, Marek K (2003) Looking backward to move forward: early detection of neurodegenerative disorders. Science 302:830-834.
17. Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, Eggan K (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 10:608-614.
18. Dobbins EG, Feldman JL (1995) Differential innervation of protruder and retractor muscles of the tongue in rat. J Comp Neurol 357:376-394.
19. Facchinetti F, Dawson VL, Dawson TM (1998) Free radicals as mediators of neuronal injury. Cell Mol Neurobiol 18:667-682.
20. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP (1995) Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377:232-236.
21. Goldin AL (1999) Diversity of mammalian voltage-gated sodium channels. Ann N Y Acad Sci 868:38-50.
22. González-Forero D, Portillo F, Sunico CR, Moreno-López B (2004) Nerve injury reduces responses of hypoglossal motoneurones to baseline and chemoreceptor-modulated inspiratory drive in the adult rat. J Physiol 557:991-1011.
23. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng H-X, Chen W, Zhai P, Sufit RL, Siddique T (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264:1772-1775.
24. Hongpaisan J, Winters CA, Andrews SB (2004) Strong calcium entry activates mitochondrial superoxide generation, upregulating kinase signaling in hippocampal neurons. J Neurosci 24:10878-10887.
25. Hu JH, Chernoff K, Pelech S, Krieger C (2003a) Protein kinase and protein phosphatase expression in the central nervous system of G93A mSOD over-expressing mice. J Neurochem 85:422-431.
26. Hu JH, Zhang H, Wagey R, Krieger C, Pelech SL (2003b) Protein kinase and protein phosphatase expression in amyotrophic lateral sclerosis spinal cord. J Neurochem 85:432-442.
27. Inglis FM, Crockett R, Korada S, Abraham WC, Hollmann M, Kalb RG (2002) The AMPA receptor subunit GluR1 regulates dendritic architecture of motor neurons. J Neurosci 22:8042-8051.
28. Ireland MF, Noakes PG, Bellingham MC (2004) P2X7-like receptor sub units enhance excitatory synaptic transmission at central synapses by presynaptic mechanisms. Neuroscience 128:269-280.
29. Kalb RG (1994) Regulation of motor neuron dendrite growth by NMDA receptor activation. Development 120:3063-3071.
30. Kaminski HJ, Richmonds CR, Kusner LL, Mitsumoto H (2002) Differential susceptibility of the ocular motor system to disease. Ann N Y Acad Sci 956:42-54.
31. Knapp LT, Klann E (2000) Superoxide-induced stimulation of protein kinase C via thiol modification and modulation of zinc content. J Biol Chem 275:24136-24145.
32. Kole MHP, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ (2008) Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11:178-186.
33. Kuo JJ, Schonewille M, Siddique T, Schults ANA, Fu RG, Bär PR, Anelli R, Heckman CJ, Kroese ABA (2004) Hyperexcitability of cultured spinal motoneurons from presymptomatic ALS mice. J Neurophysiol 91:571-575.
34. + current and its effect on excitability in motoneurones cultured from mutant SOD1 mice. J Physiol 563:843-854.
35. Li L, Houenou LJ, Wu W, Lei M, Prevette DM, Oppenheim RW (1998) Characterization of spinal motoneuron degeneration following different types of peripheral nerve injury in neonatal and adult mice. J Comp Neurol 396:158-168.
36. Li M, Ona VO, Guégan C, Chen M, Jackson-Lewis V, Andrews LJ, Olszewski AJ, Stieg PE, Lee J-P, Przedborski S, Friedlander RM (2000) Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 288:335-339.
37. Lu W, Constantine-Paton M (2004) Eye opening rapidly induces synaptic potentiation and refinement. Neuron 43:237-249.
38. Maekawa S, Al-Sarraj S, Kibble M, Landau S, Parnavelas J, Cotter D, Everall I, Leigh PN (2004) Cortical selective vulnerability in motor neuron disease: a morphometric study. Brain 127:1237-1251.
39. Mogyoros I, Kiernan MC, Burke D, Bostock H (1998) Strength-duration properties of sensory and motor axons in amyotrophic lateral sclerosis. Brain 121:851-859.
40. Moran LB, Graeber MB (2004) The facial nerve axotomy model. Brain Res Rev 44:154-178.
41. Morrison BM, Janssen WG, Gordon JW, Morrison JH (1998) Time course of neuropathology in the spinal cord of G86R superoxide dismutase transgenic mice. J Comp Neurol 391:64-77.
42. Mulder DW (1982) Clinical limits of amyotrophic lateral sclerosis. Adv Neurol 36:15-22.
43. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:615-622.
44. Neve RL, Neve KA, Nestler EJ, Carlezon WA Jr (2005) Use of herpes virus amplicon vectors to study brain disorders. BioTechniques 39:381-391.
45. Numann R, Catterall WA, Scheuer T (1991) Functional modulation of brain sodium channels by protein kinase C phosphorylation. Science 254:115-118.
46. Núñez-Abades PA, He F, Barrionuevo G, Cameron WE (1994) Morphology of developing rat genioglossal motoneurons studied in vitro: changes in length, branching pattern, and spatial distribution of dendrites. J Comp Neurol 339:401-420.
47. O'Brien JA, Berger AJ (1999) Cotransmission of GABA and glycine to brain stem motoneurons. J Neurophysiol 82:1638-1641.
48. Olson VG, Zabetian CP, Bolanos CA, Edwards S, Barrot M, Eisch AJ, Hughes T, Self DW, Neve RL, Nestler EJ (2005) Regulation of drug reward by cAMP response element-binding protein: evidence for two functionally distinct subregions of the ventral tegmental area. J Neurosci 25:5553-5562.
49. Palop JJ, Chin J, Mucke L (2006) A network dysfunction perspective on neurodegenerative diseases. Nature 443:768-773.
50. Pasinelli P, Brown RH (2006) Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 7:710-723.
51. Porter JD, Goldstein LA, Kasarskis EJ, Brueckner JK, Spear BT (1996) The neuronal voltage-gated sodium channel, Scn8a, is essential for postnatal maturation of spinal, but not oculomotor, motor units. Exp Neurol 139:328-334.
52. Powers RK, Binder MD (2003) Persistent sodium and calcium currents in rat hypoglossal motoneurons. J Neurophysiol 89:615-624.
53. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674.
54. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston SM, Berger R, Tanzi RE, Halperin JJ, Herzfeldt B, Van den Bergh R, et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62.
55. Shi J, Aamodt SM, Constantine-Paton M (1997) Temporal correlations between functional and molecular changes in NMDA receptors and GABA neurotransmission in the superior colliculus. J Neurosci 17:6264-6276.
56. Shi J, Townsend M, Constantine-Paton M (2000) Activity-dependent induction of tonic calcineurin activity mediates a rapid developmental downregulation of NMDA receptor currents. Neuron 28:103-114.
57. Smittkamp SE, Brown JW, Stanford JA (2008) Time-course and characterization of orolingual motor deficits in B6SJL-Tg(SOD1-G93A)1Gur/J mice. Neuroscience 151:613-621.
58. Stephens B, Guiloff RJ, Navarrete R, Newman P, Nikhar N, Lewis P (2006) Widespread loss of neuronal populations in the spinal ventral horn in sporadic motor neuron disease. A morphometric study. J Neurol Sci 244:41-58.
59. Tiraihi T, Rezaie MJ (2004) Synaptic lesions and synaptophysin distribution change in spinal motoneurons at early stages following sciatic nerve transection in neonatal rats. Brain Res Dev Brain Res 148:97-103.
60. Townsend M, Yoshii A, Mishina M, Constantine-Paton M (2003) Developmental loss of miniature N-methyl-D-aspartate receptor currents in NR2A knockout mice. Proc Natl Acad Sci U S A 100:1340-1345.
61. Townsend M, Liu Y, Constantine-Paton M (2004) Retina-driven dephosphorylation of the NR2A subunit correlates with faster NMDA receptor kinetics at developing retinocollicular synapses. J Neurosci 24:11098-11107.
62. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107.
63. Urbani A, Belluzzi O (2000) Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur J Neurosci 12:3567-3574.
64. van Zundert B, Yoshii A, Constantine-Paton M (2004) Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci 27:428-437.
65. 2+, mitochondria and selective motoneuron vulnerability: implications for ALS. Trends Neurosci 28:494-500.
66. Vucic S, Kiernan MC (2006) Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain 129:2436-2446.
67. Vucic S, Nicholson GA, Kiernan MC (2008) Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain 131:1540-1550.
68. Williams K (2001) Ifenprodil, a novel NMDA receptor antagonist: site and mechanism of action. Curr Drug Targets 2:285-298.
69. Xiong G, Mojsilovic-Petrovic J, Pérez CA, Kalb RG (2007) Embryonic motor neuron dendrite growth is stunted by inhibition of nitric oxide-dependent activation of soluble guanylyl cyclase and protein kinase G. Eur J Neurosci 25:1987-1997.