Rescue of synaptic failure and alleviation of learning and memory impairments in a trisomic mouse model of down syndrome

Journal of Neuropathology and Experimental Neurology

Volumn 70, Issue 12, 2011, Pages 1070-1079

  Blanchard, Julie ^a   Bolognin, Silvia ^a   Chohan, Muhammad Omar ^a,b   Rabe, Ausma ^a   Iqbal, Khalid ^a   Grundke Iqbal, Inge ^a  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Ciliary neurotrophic factor peptide; Cognitive impairments; Neurogenesis; Neuronal plasticity; Ts65Dn mice

Indexed keywords

AMINO ACID; NEUROTROPHIC FACTOR; PEPTIDE 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN SYNDROME; FEMALE; HIPPOCAMPUS; IMMEDIATE EARLY GENE; LEARNING DISORDER; MEMORY DISORDER; MOUSE; NERVE CELL PLASTICITY; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; TRISOMY;

ANIMALS; CILIARY NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; DOWN SYNDROME; FEMALE; HIPPOCAMPUS; LEARNING; MEMORY; MICE; NEURONAL PLASTICITY; NEURONS; PEPTIDE FRAGMENTS; SYNAPSES;

EID: 81855191923     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e318236e9ad     Document Type: Article

References (66)

1. Lejeune J, Turpin R, Gautier M. Mongolism; a chromosomal disease (trisomy) [in German]. Bull Acad Natl Med 1959;143:256Y65
2. Brugge KL, Nichols SL, Salmon DP, et al. Cognitive impairment in adults with Down's syndrome: Similarities to early cognitive changes in Alzheimer's disease. Neurology 1994;44:232Y38
3. Chapman RS, Hesketh LJ. Behavioral phenotype of individuals with Down syndrome. Ment Retard Dev Disabil Res Rev 2000;6:84Y95
4. Schmidt-Sidor B, Wisniewski KE, Shepard TH, et al. Brain growth in Down syndrome subjects 15 to 22 weeks of gestational age and birth to 60 months. Clin Neuropathol 1990;9:181Y90
5. Marin-Padilla M. Pyramidal cell abnormalities in the motor cortex of a child with Down's syndrome. A Golgi study. J Comp Neurol 1976;167: 63Y81
6. Becker LE, Armstrong DL, Chan F. Dendritic atrophy in children with Down's syndrome. Ann Neurol 1986;20:520Y26
7. Takashima S, Ieshima A, Nakamura H, et al. Dendrites, dementia and the Down syndrome. Brain Dev 1989;11:131Y33
8. Wisniewski KE. Down syndrome children often have brain with maturation delay, retardation of growth, and cortical dysgenesis. Am J Med Genet Suppl 1990;7:274Y81
9. Zellweger H. Down syndrome. Handbook of Clinical Neurology, Vol. Amsterdam, the Netherlands: North-Holland, 1977:367Y469
10. Sylvester PE. The hippocampus in Down's syndrome. J Ment Defic Res 1983;27:227Y36
11. Ferrer I, Gullotta F. Down's syndrome and Alzheimer's disease: Dendritic spine counts in the hippocampus. Acta Neuropathol 1990;79: 680Y85
12. Pennington BF, Moon J, Edgin J, et al. The neuropsychology of Down syndrome: Evidence for hippocampal dysfunction. Child Dev 2003;74: 75Y93
13. Davisson MT, Schmidt C, Akeson EC. Segmental trisomy of murine chromosome 16: A new model system for studying Down syndrome. Prog Clin Biol Res 1990;360:263Y80
14. Gardiner K, Fortna A, Bechtel L, et al. Mouse models of Down syndrome: How useful can they be? Comparison of the gene content of human chromosome 21 with orthologous mouse genomic regions. Gene 2003;318:137Y47
15. Holtzman DM, Santucci D, Kilbridge J, et al. Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc Natl Acad Sci U S A 1996;93:13333Y38
16. Escorihuela RM, Fernandez-Teruel A, Vallina IF, et al. A behavioral assessment of Ts65Dn mice: A putative Down syndrome model. Neurosci Lett 1995;199:143Y46
17. Escorihuela RM, Vallina IF, Martinez-Cue C, et al. Impaired short- and long-term memory in Ts65Dn mice, a model for Down syndrome. Neurosci Lett 1998;247:171Y74
18. Reeves RH, Irving NG, Moran TH, et al. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat Genet 1995;11: 177Y84
19. Hyde LA, Crnic LS. Age-related deficits in context discrimination learning in Ts65Dn mice that model Down syndrome and Alzheimer's disease. Behav Neurosci 2001;115:1239Y46
20. Belichenko PV, Masliah E, Kleschevnikov AM, et al. Synaptic structural abnormalities in the Ts65Dn mouse model of Down Syndrome. J Comp Neurol 2004;480:281Y98
21. Siarey RJ, Carlson EJ, Epstein CJ, et al. Increased synaptic depression in the Ts65Dn mouse, a model for mental retardation in Down syndrome. Neuropharmacology 1999;38:1917Y20
22. Siarey RJ, Stoll J, Rapoport SI, et al. Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down Syndrome. Neuropharmacology 1997;36:1549Y54
23. Kleschevnikov AM, Belichenko PV, Villar AJ, et al. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J Neurosci 2004;24:8153Y60
24. Haydar TF, Nowakowski RS, Yarowsky PJ, et al. Role of founder cell deficit and delayed neuronogenesis in microencephaly of the trisomy 16 mouse. J Neurosci 2000;20:4156Y64
25. Lorenzi HA, Reeves RH. Hippocampal hypocellularity in the Ts65Dn mouse originates early in development. Brain Res 2006;1104:153Y59
26. Chakrabarti L, Galdzicki Z, Haydar TF. Defects in embryonic neurogenesis and initial synapse formation in the forebrain of the Ts65Dn mouse model of Down syndrome. J Neurosci 2007;27:11483Y95
27. Contestabile A, Fila T, Ceccarelli C, et al. Cell cycle alteration and decreased cell proliferation in the hippocampal dentate gyrus and in the neocortical germinal matrix of fetuses with Down syndrome and in Ts65Dn mice. Hippocampus 2007;17:665Y78
28. Black IB. Trophic regulation of synaptic plasticity. J Neurobiol 1999;41: 108Y18
29. Lu B, Chow A. Neurotrophins and hippocampal synaptic transmission and plasticity. J Neurosci Res 1999;58:76Y87
30. Schinder AF, Poo M. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 2000;23:639Y45
31. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002;25:103Y26
32. Bredt DS, Nicoll RA. AMPA receptor trafficking at excitatory synapses. Neuron 2003;40:361Y79
33. Morris RG, Moser EI, Riedel G, et al. Elements of a neurobiological theory of the hippocampus: The role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 2003;358: 773Y86
34. Collingridge GL, Isaac JT, Wang YT. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 2004;5:952Y62
35. Neves G, Cooke SF, Bliss TV. Synaptic plasticity, memory and the hippocampus: A neural network approach to causality. Nat Rev Neurosci 2008;9:65Y75
36. Aimone JB, Wiles J, Gage FH. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 2006;9:723Y27
37. Leuner B, Gould E, Shors TJ
38. Lledo PM, Alonso M, Grubb MS. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 2006;7:179Y93
39. Abrous DN, Wojtowics JM. Neurogenesis and hippocampal memory system. Adult Neurogenesis, Vol. New York, NY: Cold Spring Harbor Press, 2008
40. Chohan MO, Li B, Blanchard J, et al. Enhancement of dentate gyrus neurogenesis, dendritic and synaptic plasticity and memory by a neurotrophic peptide. Neurobiol Aging 2011;32:1420Y34
41. Morris RG, Garrud P, Rawlins JN, et al. Place navigation impaired in rats with hippocampal lesions. Nature 1982;297:681Y83
42. Kuhn HG, Winkler J, Kempermann G, et al. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 1997;17:5820Y29
43. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991;231:482Y97
44. Bensadoun A, Weinstein D. Assay of proteins in the presence of interfering materials. Anal Biochem 1976;70:241Y50
45. ACTSG. A double-blind placebo-controlled clinical trial of subcutaneous recombinant human ciliary neurotrophic factor (rHCNTF) in amyotrophic lateral sclerosis. ALS CNTF Treatment Study Group. Neurology 1996; 46:1244Y49
46. Windisch M, Gschanes A, Hutter-Paier B. Neurotrophic activities and therapeutic experience with a brain derived peptide preparation. J Neural Transm Suppl 1998;53:289Y98
47. Riedel G, Micheau J, Lam AG, et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci 1999;2:898Y905
48. Pollonini G, Gao V, Rabe A, et al. Abnormal expression of synaptic proteins and neurotrophin-3 in the Down syndrome mouse model Ts65Dn. Neuroscience 2008;156:99Y106
49. Elias GM, Funke L, Stein V, et al. Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 2006;52:307Y20
50. Beique JC, Andrade R. PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J Physiol 2003;546:859Y67
51. Ehrlich I, Malinow R. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J Neurosci 2004;24:916Y27
52. Wiltgen BJ, Royle GA, Gray EE, et al. A role for calcium-permeable AMPA receptors in synaptic plasticity and learning. PLoS One 2010;5
53. Bozon B, Davis S, Laroche S. A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 2003;40:695Y701
54. Donovan MH, Yazdani U, Norris RD, et al. Decreased adult hilppocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol 2006;495:70Y83
55. Lockrow J, Boger H, Bimonte-Nelson H, et al. Effects of long-term memantine on memory and neuropathology in Ts65Dn mice, a model for Down syndrome. Behav Brain Res 2011;221:610Y22
56. Granholm AC, Ford KA, Hyde LA, et al. Estrogen restores cognition and cholinergic phenotype in an animal model of Down syndrome. Physiol Behav 2002;77:371Y85
57. Clark S, Schwalbe J, Stasko MR, et al. Fluoxetine rescues deficient neurogenesis in hippocampus of the Ts65Dn mouse model for Down syndrome. Exp Neurol 2006;200:256Y61
58. Bianchi P, Ciani E, Contestabile A, et al. Lithium restores neurogenesis in the subventricular zone of the Ts65Dn mouse, a model for Down syndrome. Brain Pathol 2010;20:106Y18
59. Chen ZY, Cao L, Wang LM, et al. Development of neurotrophic molecules for treatment of neurodegeneration. Curr Protein Pept Sci 2001;2: 261Y76
60. Demas GE, Nelson RJ, Krueger BK, et al. Spatial memory deficits in segmental trisomic Ts65Dn mice. Behav Brain Res 1996;82:85Y92
61. Quinlan EM, Halpain S. Emergence of activity-dependent, bidirectional control of microtubule-associated protein MAP2 phosphorylation during postnatal development. J Neurosci 1996;16:7627Y37
62. Quinlan EM, Halpain S. Postsynaptic mechanisms for bidirectional control of MAP2 phosphorylation by glutamate receptors. Neuron 1996;16: 357Y68
63. Mirescu C, Gould E. Stress and adult neurogenesis. Hippocampus 2006; 16:233Y38
64. Jessberger S, Clark RE, Broadbent NJ, et al. Dentate gyrusYspecific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 2009;16:147Y54
65. Ekdahl CT, Claasen JH, Bonde S, et al. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 2003;100:13632Y37
66. Verret L, Trouche S, Zerwas M, et al. Hippocampal neurogenesis during normal and pathological aging. Psychoneuroendocrinology 2007; 32(Suppl 1):S26Y30