Network dysfunction in α-synuclein transgenic mice and human Lewy body dementia

Annals of Clinical and Translational Neurology

Volumn 2, Issue 11, 2015, Pages 1012-1028

  Morris, Meaghan ^a,b   Sanchez, Pascal E ^a   Verret, Laure ^a,c,d   Beagle, Alexander J ^c   Guo, Weikun ^a   Dubal, Dena ^c   Ranasinghe, Kamalini G ^c   Koyama, Akihiko ^a,e   Ho, Kaitlyn ^a   Yu, Gui Qiu ^a   Vossel, Keith A ^a,c   Mucke, Lennart ^a,c  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e EISAI INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CALBINDIN;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DIFFUSE LEWY BODY DISEASE; ELECTROENCEPHALOGRAPHY; EPILEPTIC DISCHARGE; FEMALE; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INCIDENCE; MALE; MOUSE; MYOCLONUS; NERVE CELL NETWORK; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEIZURE; SPIKE WAVE; TRANSGENIC MOUSE; WESTERN BLOTTING;

EID: 84995676930     PISSN: None     EISSN: 23289503     Source Type: Journal    
DOI: 10.1002/acn3.257     Document Type: Article

References (62)

1. McKeith IG, Dickson DW, Lowe J, et al. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 2005;65:1863–1872.
2. Andersson M, Hansson O, Minthon L, et al. Electroencephalogram variability in dementia with lewy bodies, Alzheimer's disease and controls. Dement Geriatr Cogn Disord 2008;26:284–290.
3. Bonanni L, Thomas A, Tiraboschi P, et al. EEG comparisons in early Alzheimer's disease, dementia with Lewy bodies and Parkinson's disease with dementia patients with a 2-year follow-up. Brain 2008;131(Pt 3):690–705.
4. Almkvist O, Jelic V, Amberla K, et al. Responder characteristics to a single oral dose of cholinesterase inhibitor: a double-blind placebo-controlled study with tacrine in Alzheimer patients. Dement Geriatr Cogn Disord 2001;12:22–32.
5. Adler G, Brassen S, Chwalek K, et al. Prediction of treatment response to rivastigmine in Alzheimer's dementia. J Neurol Neurosurg Psychiatry 2004;75:292–294.
6. Lippa CF, Smith TW, Perry E. Dementia with Lewy bodies: choline acetyltransferase parallels nucleus basalis pathology. J Neural Transm 1999;106:525–535.
7. McKeith IG. Spectrum of Parkinson's disease, Parkinson's dementia, and Lewy body dementia. Neurol Clin 2000;18:865–902.
8. Perry EK, Irving D, Kerwin JM, et al. Cholinergic transmitter and neurotrophic activities in Lewy body dementia: similarity to Parkinson's and distinction from Alzheimer disease. Alzheimer Dis Assoc Disord 1993;7:69–79.
9. Possin KL, Kang GA, Guo C, et al. Rivastigmine is associated with restoration of left frontal brain activity in Parkinson's disease. Mov Disord 2013;28:1384–1390.
10. Nemani VM, Lu W, Berge V, et al. Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 2010;65:66–79.
11. Bendor JT, Logan TP, Edwards RH. The function of alpha-synuclein. Neuron 2013;79:1044–1066.
12. Chesselet MF, Richter F, Zhu C, et al. A progressive mouse model of Parkinson's disease: the Thy1-aSyn (“Line 61”) mice. Neurotherapeutics 2012;9:297–314.
13. Magen I, Fleming SM, Zhu C, et al. Cognitive deficits in a mouse model of pre-manifest Parkinson's disease. Eur J Neurosci 2012;35:870–882.
14. Sales-Carbonell C, Rueda-Orozco PE, Soria-Gomez E, et al. Striatal GABAergic and cortical glutamatergic neurons mediate contrasting effects of cannabinoids on cortical network synchrony. Proc Natl Acad Sci USA 2013;110:719–724.
15. Fisher RS, van Emde Boas W, Blume W, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005;46:470–472.
16. Rothman K, Greenland S. Modern epidemiology. 3rd ed. Philadelphia: Lippincott Williams & Wilkins, 2008.
17. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Neurobiol Aging 1997;18(4 Suppl):S1–S2.
18. Rockenstein E, Mallory M, Hashimoto M, et al. Differential neuropathological alterations in transgenic mice expressing α-synuclein from the PDGF-B and Thy-1 promoters. J Neurosci Res 2002;68:568–578.
19. 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 2000;20:4050–4058.
20. Dawson HN, Ferreira A, Eyster MV, et al. Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 2001;114:1179–1187.
21. Kinney GG, Patino P, Mermet-Bouvier Y, et al. Cognition-enhancing drugs increase stimulated hippocampal theta rhythm amplitude in the urethane-anesthetized rat. J Pharmacol Exp Ther 1999;291:99–106.
22. Verret L, Mann EO, Hang GB, et al. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012;149:708–721.
23. Palop JJ, Mucke L, Roberson ED. Quantifying biomarkers of cognitive dysfunction and neuronal network hyperexcitability in mouse models of Alzheimer's disease: depletion of calcium-dependent proteins and inhibitory hippocampal remodeling. Methods Mol Biol 2011;670:245–262.
24. Miller JJ, Baimbridge KG. Biochemical and immunohistochemical correlates of kindling-induced epilepsy: role of calcium binding protein. Brain Res 1983;278:322–326.
25. Marksteiner J, Ortler M, Bellmann R, Sperk G. Neuropeptide Y biosynthesis is markedly induced in mossy fibers during temporal lobe epilepsy of the rat. Neurosci Lett 1990;112:143–148.
26. Palop JJ, Chin J, Roberson ED, et al. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007;55:697–711.
27. Winston SM, Hayward MD, Nestler EJ, Duman RS. Chronic electroconvulsive seizures down-regulate expression of the immediate-early genes c-fos and c-jun in rat cerebral cortex. J Neurochem 1990;54:1920–1925.
28. Roberson ED, Halabisky B, Yoo JW, et al. Amyloid-β/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. J Neurosci 2011;31:700–711.
29. Sanchez PE, Zhu L, Verret L, et al. Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer's disease model. Proc Natl Acad Sci USA 2012;109:E2895–E2903.
30. Roberson ED, Scearce-Levie K, Palop JJ, et al. Reducing endogenous tau ameliorates amyloid β-induced deficits in an Alzheimer's disease mouse model. Science 2007;316:750–754.
31. Ittner LM, Ke YD, Delerue F, et al. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010;142:387–397.
32. Devos SL, Goncharoff DK, Chen G, et al. Antisense reduction of tau in adult mice protects against seizures. J Neurosci 2013;33:12887–12897.
33. Holth JK, Bomben VC, Reed JG, et al. Tau loss attenuates neuronal network hyperexcitability in mouse and Drosophila genetic models of epilepsy. J Neurosci 2013;33:1651–1659.
34. Gheyara AL, Ponnusamy R, Djukic B, et al. Tau reduction prevents disease in a mouse model of Dravet syndrome. Ann Neurol 2014;76:443–456.
35. Buzsaki G, Bickford RG, Ponomareff G, et al. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci 1988;8:4007–4026.
36. Riekkinen P Jr, Riekkinen M, Sirvio J, et al. Loss of cholinergic neurons in the nucleus basalis induces neocortical electroencephalographic and passive avoidance deficits. Neuroscience 1992;47:823–831.
37. Dong H, Yuede CM, Coughlan CA, et al. Effects of donepezil on amyloid-beta and synapse density in the Tg2576 mouse model of Alzheimer's disease. Brain Res 2009;1303:169–178.
38. Weiner MF, Hynan LS, Parikh B, et al. Can Alzheimer's disease and dementias with Lewy bodies be distinguished clinically? J Geriatr Psychiatry Neurol 2003;16:245–250.
39. Caviness JN, Adler CH, Caselli RJ, Hernandez JL. Electrophysiology of the myoclonus in dementia with Lewy bodies. Neurology 2003;60:523–524.
40. 28K immunoreactivity from dentate granule cells in human temporal lobe epilepsy. Neuroscience 1997;76:377–385.
41. Palop JJ, Jones B, Kekonius L, et al. Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci USA 2003;100:9572–9577.
42. Bandopadhyay R, Liu JY, Sisodiya SM, Thom M. A comparative study of the dentate gyrus in hippocampal sclerosis in epilepsy and dementia. Neuropathol Appl Neurobiol 2014;40:177–190.
43. Caviness JN, Adler CH, Beach TG, et al. Small-amplitude cortical myoclonus in Parkinson's disease: physiology and clinical observations. Mov Disord 2002;17:657–662.
44. Kojovic M, Cordivari C, Bhatia K. Myoclonic disorders: a practical approach for diagnosis and treatment. Ther Adv Neurol Disord 2011;4:47–62.
45. Louis ED, Klatka LA, Liu Y, Fahn S. Comparison of extrapyramidal features in 31 pathologically confirmed cases of diffuse Lewy body disease and 34 pathologically confirmed cases of Parkinson's disease. Neurology 1997;48:376–380.
46. Caviness JN, Alving LI, Maraganore DM, et al. The incidence and prevalence of myoclonus in Olmsted County, Minnesota. Mayo Clin Proc 1999;74:565–569.
47. Forsgren L, Bucht G, Eriksson S, Bergmark L. Incidence and clinical characterization of unprovoked seizures in adults: a prospective population-based study. Epilepsia 1996;37:224–229.
48. McDowell KA, Shin D, Roos KP, Chesselet MF. Sleep dysfunction and EEG alterations in mice overexpressing alpha-synuclein. J Parkinsons Dis 2014;4:531–539.
49. Rockenstein E, Nuber S, Overk CR, et al. Accumulation of oligomer-prone alpha-synuclein exacerbates synaptic and neuronal degeneration in vivo. Brain 2014;137(Pt 5):1496–1513.
50. Pillai J, Sperling MR. Interictal EEG and the diagnosis of epilepsy. Epilepsia 2006;47(Suppl 1):14–22.
51. Vossel KA, Beagle AJ, Rabinovici GD, et al. Seizures and epileptiform activity in the early stages of Alzheimer disease. JAMA Neurol 2013;70:1158–1166.
52. Brown P, Steiger MJ, Thompson PD, et al. Effectiveness of piracetam in cortical myoclonus. Mov Disord 1993;8:63–68.
53. Ikeda A, Shibasaki H, Tashiro K, et al. Clinical trial of piracetam in patients with myoclonus: nationwide multiinstitution study in Japan. The Myoclonus/Piracetam Study Group. Mov Disord 1996;11:691–700.
54. Frucht SJ, Louis ED, Chuang C, Fahn S. A pilot tolerability and efficacy study of levetiracetam in patients with chronic myoclonus. Neurology 2001;57:1112–1114.
55. Caviness JN, Lue LF, Beach TG, et al. Parkinson's disease, cortical dysfunction, and alpha-synuclein. Mov Disord 2011;26:1436–1442.
56. Kotsopoulos IA, van Merode T, Kessels FG, et al. Systematic review and meta-analysis of incidence studies of epilepsy and unprovoked seizures. Epilepsia 2002;43:1402–1409.
57. Masliah E, Rockenstein E, Veinbergs I, et al. β-Amyloid peptides enhance α-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease. Proc Natl Acad Sci USA 2001;98:12245–12250.
58. Del Ser T, Hachinski V, Merskey H, Munoz DG. Clinical and pathologic features of two groups of patients with dementia with Lewy bodies: effect of coexisting Alzheimer-type lesion load. Alzheimer Dis Assoc Disord 2001;15:31–44.
59. Merdes AR, Hansen LA, Jeste DV, et al. Influence of Alzheimer pathology on clinical diagnostic accuracy in dementia with Lewy bodies. Neurology 2003;60:1586–1590.
60. Hamilton RL. Lewy bodies in Alzheimer's disease: a neuropathological review of 145 cases using a-synuclein immunohistochemistry. Brain Pathol 2000;10:378–384.
61. Briel RCG, McKeith IG, Barker WA, et al. EEG findings in dementia with Lewy bodies and Alzheimer's disease. J Neurol Neurosurg Psychiatry 1999;66:401–403.
62. Bakker A, Krauss GL, Albert MS, et al. Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 2012;74:467–474.