Synaptic scaling up in medium spiny neurons of aged BACHD mice: A slow-progression model of Huntington's disease

Neurobiology of Disease

Volumn 86, Issue , 2016, Pages 131-139

  Rocher, Anne B ^a   Gubellini, Paolo ^b   Merienne, Nicolas ^a,d   Boussicault, Lydie ^a,e   Petit, Fanny ^a   Gipchtein, Pauline ^a   Jan, Caroline ^a   Hantraye, Philippe ^a   Brouillet, Emmanuel ^a   Bonvento, Gilles ^a,c  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

^d LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

AMPAR; Dendritic spine; Homeostatic scaling; Huntington's disease; Medium spiny neuron; Whole cell patch clamp

Indexed keywords

AMPA RECEPTOR; AMPA RECEPTOR SUBUNIT 1; AMPA RECEPTOR SUBUNIT 2; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 88; HUNTINGTIN; MESSENGER RNA; UNCLASSIFIED DRUG; GPR88 PROTEIN, MOUSE; HTT PROTEIN, HUMAN; NERVE PROTEIN; PROTEIN SUBUNIT;

ACTION POTENTIAL AMPLITUDE; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITIC SPINE; FEMALE; GENETIC TRANSCRIPTION; HUNTINGTON CHOREA; MEDIUM SPINY NEURON; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE; ANIMAL; DISEASE COURSE; DISEASE MODEL; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN SUBUNIT; TRANSGENIC MOUSE;

ANIMALS; CORPUS STRIATUM; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HUMANS; HUNTINGTIN PROTEIN; HUNTINGTON DISEASE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; PROTEIN SUBUNITS; RECEPTORS, AMPA; RECEPTORS, G-PROTEIN-COUPLED; SYNAPSES;

EID: 84949035702     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.10.016     Document Type: Article

References (55)

1. Akbarian S., et al. Editing for an AMPA receptor subunit RNA in prefrontal cortex and striatum in Alzheimer's disease, Huntington's disease and schizophrenia. Brain Res. 1995, 699:297-304.
2. Anggono V., et al. PICK1 loss of function occludes homeostatic synaptic scaling. J. Neurosci. 2011, 31:2188-2196.
3. Aoto J., et al. Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 2008, 60:308-320.
4. Arzberger T., et al. Changes of NMDA receptor subunit (NR1, NR2B) and glutamate transporter (GLT1) mRNA expression in Huntington's disease-an in situ hybridization study. J. Neuropathol. Exp. Neurol. 1997, 56:440-454.
5. Azdad K., et al. Homeostatic plasticity of striatal neurons intrinsic excitability following dopamine depletion. PLoS ONE 2009, 4:e6908.
6. Behrens P.F., et al. Impaired glutamate transport and glutamate-glutamine cycling: downstream effects of the Huntington mutation. Brain 2002, 125:1908-1922.
7. Beurrier C., et al. Electrophysiological and behavioral evidence that modulation of metabotropic glutamate receptor 4 with a new agonist reverses experimental Parkinsonism. FASEB J. 2009, 23:3619-3628.
8. Cattaneo E., et al. Normal huntingtin function: an alternative approach to Huntington's disease. Nat. Rev. Neurosci. 2005, 6:919-930.
9. Crimins J.L., et al. Homeostatic responses by surviving cortical pyramidal cells in neurodegenerative tauopathy. Acta Neuropathol. 2011, 122:551-564.
10. Day M., et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat. Neurosci. 2006, 9:251-259.
11. de Chaldee M., et al. Quantitative assessment of transcriptome differences between brain territories. Genome Res. 2003, 13:1646-1653.
12. Faideau M., et al. In vivo expression of polyglutamine-expanded huntingtin by mouse striatal astrocytes impairs glutamate transport: a correlation with Huntington's disease subjects. Hum. Mol. Genet. 2010, 19:3053-3067.
13. Fan M.M., Raymond L.A. N-methyl-d-aspartate (NMDA) receptor function and excitotoxicity in Huntington's disease. Prog. Neurobiol. 2007, 81:272-293.
14. Ferrante R.J., et al. Proliferative and degenerative changes in striatal spiny neurons in Huntington's disease: a combined study using the section-Golgi method and calbindin D28k immunocytochemistry. J. Neurosci. 1991, 11:3877-3887.
15. Gainey M.A., et al. Activity-dependent synaptic GRIP1 accumulation drives synaptic scaling up in response to action potential blockade. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:E3590-E3599.
16. Graveland G.A., et al. Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. Science 1985, 227:770-773.
17. Gray M., et al. Full-length human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice. J. Neurosci. 2008, 28:6182-6195.
18. Hobbs N.Z., et al. Automated quantification of caudate atrophy by local registration of serial MRI: evaluation and application in Huntington's disease. NeuroImage 2009, 47:1659-1665.
19. Hodges A., et al. Regional and cellular gene expression changes in human Huntington's disease brain. Hum. Mol. Genet. 2006, 15:965-977.
20. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 1994, 17:31-108.
21. + permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 1991, 252:851-853.
22. Hu J.H., et al. Homeostatic scaling requires group I mGluR activation mediated by Homer1a. Neuron 2010, 68:1128-1142.
23. Hult S., et al. Mutant huntingtin causes metabolic imbalance by disruption of hypothalamic neurocircuits. Cell Metab. 2011, 13:428-439.
24. Klapstein G.J., et al. Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice. J. Neurophysiol. 2001, 86:2667-2677.
25. Lein E.S., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
26. Levine M.S., et al. Enhanced sensitivity to N-methyl-d-aspartate receptor activation in transgenic and knockin mouse models of Huntington's disease. J. Neurosci. Res. 1999, 58:515-532.
27. Li J.Y., et al. Huntington's disease: a synaptopathy?. Trends Mol. Med. 2003, 9:414-420.
28. Li W., et al. Upregulation of glutamatergic transmission in anterior cingulate cortex in the diabetic rats with neuropathic pain. Neurosci. Lett. 2014, 568:29-34.
29. Lievens J.C., et al. Impaired glutamate uptake in the R6 Huntington's disease transgenic mice. Neurobiol. Dis. 2001, 8:807-821.
30. Mandal M., et al. Impaired alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor trafficking and function by mutant huntingtin. J. Biol. Chem. 2011, 286:33719-33728.
31. Massart R., et al. Striatal GPR88 expression is confined to the whole projection neuron population and is regulated by dopaminergic and glutamatergic afferents. Eur. J. Neurosci. 2009, 30:397-414.
32. Mazarei G., et al. Expression analysis of novel striatal-enriched genes in Huntington disease. Hum. Mol. Genet. 2010, 19:609-622.
33. Mizushima K., et al. A novel G-protein-coupled receptor gene expressed in striatum. Genomics 2000, 69:314-321.
34. Nithianantharajah J., Hannan A.J. Dysregulation of synaptic proteins, dendritic spine abnormalities and pathological plasticity of synapses as experience-dependent mediators of cognitive and psychiatric symptoms in Huntington's disease. Neuroscience 2013, 251:66-74.
35. O'Brien R.J., et al. Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 1998, 21:1067-1078.
36. Peters A., Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Z. Zellforsch. Mikrosk. Anat. 1969, 100:487-506.
37. Pouladi M.A., et al. Marked differences in neurochemistry and aggregates despite similar behavioural and neuropathological features of Huntington disease in the full-length BACHD and YAC128 mice. Hum. Mol. Genet. 2012, 21:2219-2232.
38. Quintana A., et al. Lack of GPR88 enhances medium spiny neuron activity and alters motor- and cue-dependent behaviors. Nat. Neurosci. 2012, 15:1547-1555.
39. Raymond L.A., et al. Pathophysiology of Huntington's disease: time-dependent alterations in synaptic and receptor function. Neuroscience 2011, 198:252-273.
40. Richards P., et al. Dendritic spine loss and neurodegeneration is rescued by Rab11 in models of Huntington's disease. Cell Death Differ. 2011, 18:191-200.
41. Rocher A.B., et al. Significant structural but not physiological changes in cortical neurons of 12-month-old Tg2576 mice. Neurobiol. Dis. 2008, 32:309-318.
42. Rocher A.B., et al. Structural and functional changes in tau mutant mice neurons are not linked to the presence of NFTs. Exp. Neurol. 2010, 223:385-393.
43. Ross C.A., Tabrizi S.J. Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol. 2011, 10:83-98.
44. Shepherd J.D., et al. Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 2006, 52:475-484.
45. Simmons D.A., et al. Up-regulating BDNF with an ampakine rescues synaptic plasticity and memory in Huntington's disease knockin mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4906-4911.
46. Simmons D.A., et al. Brief ampakine treatments slow the progression of Huntington's disease phenotypes in R6/2 mice. Neurobiol. Dis. 2011, 41:436-444.
47. Turrigiano G.G. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 2008, 135:422-435.
48. Turrigiano G.G., et al. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998, 391:892-896.
49. van der Burg J.M., et al. Beyond the brain: widespread pathology in Huntington's disease. Lancet Neurol. 2009, 8:765-774.
50. Vonsattel J.P., DiFiglia M. Huntington disease. J. Neuropathol. Exp. Neurol. 1998, 57:369-384.
51. Wang N., et al. Neuronal targets for reducing mutant huntingtin expression to ameliorate disease in a mouse model of Huntington's disease. Nat. Med. 2014, 20:536-541.
52. Weiss A., et al. Sensitive biochemical aggregate detection reveals aggregation onset before symptom development in cellular and murine models of Huntington's disease. J. Neurochem. 2008, 104:846-858.
53. Wierenga C.J., et al. Postsynaptic expression of homeostatic plasticity at neocortical synapses. J. Neurosci. 2005, 25:2895-2905.
54. Wu L.G., et al. Modes of vesicle retrieval at ribbon synapses, calyx-type synapses, and small central synapses. J. Neurosci. 2007, 27:11793-11802.
55. Xu Q., et al. Synaptic mutant huntingtin inhibits synapsin-1 phosphorylation and causes neurological symptoms. J. Cell Biol. 2013, 202:1123-1138.