Down syndrome cognitive phenotypes modeled in mice trisomic for all HSA 21 homologues

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Belichenko, Pavel V ^a   Kleschevnikov, Alexander M ^a   Becker, Ann ^a   Wagner, Grant E ^a   Lysenko, Larisa V ^a   Yu, Y Eugene ^b   Mobley, William C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; PICROTOXIN;

ADULT; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CHROMOSOME 10; CHROMOSOME 16; CHROMOSOME 17; CHROMOSOME 21; CHROMOSOME DUPLICATION; COGNITION; COMPULSION; CONTROLLED STUDY; DENTATE GYRUS; DOWN SYNDROME; EXPERIMENTAL STUDY; GENETIC MODEL; GENOMICS; GENOTYPE PHENOTYPE CORRELATION; INTELLECTUAL IMPAIRMENT; LOCOMOTION; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MOUSE; MURINE MODEL; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; STEREOTYPY; SYNTENY; TRISOMY 21; WORKING MEMORY; Y-MAZE TEST; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; PATHOPHYSIOLOGY; PSYCHOLOGY; TRISOMY;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DOWN SYNDROME; LOCOMOTION; MICE; PHENOTYPE; TRISOMY;

EID: 84941978800     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134861     Document Type: Article

References (118)

1. Lejeune J, Turpin R, Gautier M. [Chromosomic diagnosis of mongolism]. Arch Fr Pediatr. 1959;16:962-963. PMID: 14415503
2. Galdzicki Z, Siarey RJ. Understanding mental retardation in Down's syndrome using trisomy 16 mouse models. Genes Brain Behav. 2003;2:167-178. PMID: 12931790
3. Belichenko PV, Kleschevnikov AM, Salehi A, Epstein CJ, Mobley WC. Synaptic and cognitive abnormalities in mouse models of Down syndrome: exploring genotype-phenotype relationships. J Comp Neurol. 2007;504:329-345. PMID: 17663443
4. Lana-Elola E, Watson-Scales SD, Fisher EM, Tybulewicz VL. Down syndrome: searching for the genetic culprits. Dis Model Mech. 2011;4:586-595. doi: 10.1242/dmm.008078 PMID: 21878459
5. Kleschevnikov AM, Belichenko PV, Salehi A, Wu C. Discoveries in Down syndrome: moving basic science to clinical care. Prog Brain Res. 2012;197:199-221. doi: 10.1016/B978-0-444-54299-1.00010-8 PMID: 22541294
6. Ruparelia A, Pearn ML, Mobley WC. Aging and intellectual disability: insights from mouse models of Down syndrome. Dev Disabil Res Rev. 2013;18:43-50. doi: 10.1002/ddrr.1127 PMID: 23949828
7. Liu C, Belichenko PV, Zhang L, Fu D, Kleschevnikov AM, Baldini A, et al. Mouse models for Down syndrome-associated developmental cognitive disabilities. Dev Neurosci. 2011;33:404-413. doi: 10.1159/000329422 PMID: 21865664
8. Popov VI, Kleschevnikov AM, Klimenko OA, Stewart MG, Belichenko PV. Three-dimensional synaptic ultrastructure in the dentate gyrus and hippocampal area CA3 in the Ts65Dn mouse model of Down syndrome. J Comp Neurol. 2011;519:1338-1354. doi: 10.1002/cne.22573 PMID: 21452200
9. Salehi A, Delcroix JD, Belichenko PV, Zhan K, Wu C, Valletta JS, et al. Increased App expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron. 2006;51:29-42. PMID: 16815330
10. Zhang L, Fu D, Belichenko PV, Liu C, Kleschevnikov AM, Pao A, et al. Genetic analysis of Down syndrome facilitated by mouse chromosome engineering. Bioeng Bugs. 2012;3:8-12. doi: 10.4161/bbug.3.1.17696 PMID: 22126738
11. Dierssen M, Fillat C, Crnic L, Arbones M, Florez J, Estivill X. Murine models for Down syndrome. Physiol Behav. 2001;73:859-871. PMID: 11566219
12. Das I, Reeves RH. The use of mouse models to understand and improve cognitive deficits in Down syndrome. Dis Model Mech. 2011;4:596-606. doi: 10.1242/dmm.007716 PMID: 21816951
13. Belichenko PV, Kleschevnikov AM, Masliah E, Wu C, Takimoto-Kimura R, Salehi A, et al. Excitatoryinhibitory relationship in the fascia dentata in the Ts65Dn mouse model of Down syndrome. J Comp Neurol. 2009;512:453-466. doi: 10.1002/cne.21895 PMID: 19034952
14. Davisson MT, Schmidt C, Reeves RH, Irving NG, Akeson EC, Harris BS, et al. Segmental trisomy as a mouse model for Down syndrome. Prog Clin Biol Res. 1993;384:117-133. PMID: 8115398
15. O'Doherty A, Ruf S, Mulligan C, Hildreth V, Errington ML, Cooke S, et al. An aneuploid mouse strain carrying human chromosome 21 with Down syndrome phenotypes. Science. 2005;309:2033-2037. PMID: 16179473
16. Pereira PL, Magnol L, Sahun I, Brault V, Duchon A, Prandini P, et al. A new mouse model for the trisomy of the Abcg1-U2af1 region reveals the complexity of the combinatorial genetic code of down syndrome. Hum Mol Genet. 2009;18:4756-4769. doi: 10.1093/hmg/ddp438 PMID: 19783846
17. Sago H, Carlson EJ, Smith DJ, Kilbridge J, Rubin EM, Mobley WC, et al. Ts1Cje, a partial trisomy 16 mouse model for Down syndrome, exhibits learning and behavioral abnormalities. Proc Natl Acad Sci USA. 1998;95:6256-6261. PMID: 9600952
18. Olson LE, Richtsmeier JT, Leszl J, Reeves RH. A chromosome 21 critical region does not cause specific Down syndrome phenotypes. Science. 2004;306:687-690. PMID: 15499018
19. Escorihuela RM, Fernandez-Teruel A, Vallina IF, Baamonde C, Lumbreras MA, Dierssen M, et al. A behavioral assessment of Ts65Dn mice: a putative Down syndrome model. Neurosci Lett. 1995;199:143-146. PMID: 8584244
20. Escorihuela RM, Vallina IF, Martinez-Cue C, Baamonde C, Dierssen M, Tobena A, et al. Impaired short- and long-term memory in Ts65Dn mice, a model for Down syndrome. Neurosci Lett. 1998;247:171-174. PMID: 9655620
21. Olson LE, Roper RJ, Sengstaken CL, Peterson EA, Aquino V, Galdzicki Z, et al. Trisomy for the Down syndrome 'critical region' is necessary but not sufficient for brain phenotypes of trisomic mice. Hum Mol Genet. 2007;16:774-782. PMID: 17339268
22. Stasko MR, Costa AC. Experimental parameters affecting the Morris water maze performance of a mouse model of Down syndrome. Behav Brain Res. 2004;154:1-17. PMID: 15302106
23. Braudeau J, Delatour B, Duchon A, Pereira PL, Dauphinot L, De Chaumont F, et al. Specific targeting of the GABA-A receptor alpha5 subtype by a selective inverse agonist restores cognitive deficits in Down syndrome mice. J Psychopharmacol. 2011;25:1030-1042. doi: 10.1177/0269881111405366 PMID: 21693554
24. Rueda N, Llorens-Martin M, Florez J, Valdizan E, Banerjee P, Trejo JL, et al. Memantine normalizes several phenotypic features in the Ts65Dn mouse model of Down syndrome. J Alzheimers Dis. 2010;21:277-290. doi: 10.3233/JAD-2010-100240 PMID: 20421694
25. Faizi M, Bader PL, Tun C, Encarnacion A, Kleschevnikov A, Belichenko P, et al. Comprehensive behavioral phenotyping of Ts65Dn mouse model of Down syndrome: activation of beta1-adrenergic receptor by xamoterol as a potential cognitive enhancer. Neurobiol Dis. 2011;43:397-413. doi: 10. 1016/j.nbd.2011.04.011 PMID: 21527343
26. Kleschevnikov AM, Belichenko PV, Faizi M, Jacobs LF, Htun K, Shamloo M, et al. Deficits in cognition and synaptic plasticity in a mouse model of Down syndrome ameliorated by GABAB receptor antagonists. J Neurosci. 2012;32:9217-9227. doi: 10.1523/JNEUROSCI.1673-12.2012 PMID: 22764230
27. Costa AC, Scott-McKean JJ, Stasko MR. Acute injections of the NMDA receptor antagonist memantine rescue performance deficits of the Ts65Dn mouse model of Down syndrome on a fear conditioning test. Neuropsychopharmacology. 2008;33:1624-1632. PMID: 17700645
28. Hyde LA, Frisone DF, Crnic LS. Ts65Dn mice, a model for Down syndrome, have deficits in context discrimination learning suggesting impaired hippocampal function. Behav Brain Res. 2001;118:53-60. PMID: 11163633
29. Lockrow J, Boger H, Bimonte-Nelson H, Granholm AC. Effects of long-term memantine on memory and neuropathology in Ts65Dn mice, a model for Down syndrome. Behav Brain Res. 2011;221:610-622. doi: 10.1016/j.bbr.2010.03.036 PMID: 20363261
30. Fernandez F, Morishita W, Zuniga E, Nguyen J, Blank M, Malenka RC, et al. Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat Neurosci. 2007;10:411-413. PMID: 17322876
31. Demas GE, Nelson RJ, Krueger BK, Yarowsky PJ. Impaired spatial working and reference memory in segmental trisomy (Ts65Dn) mice. Behav Brain Res. 1998;90:199-201. PMID: 9521551
32. Demas GE, Nelson RJ, Krueger BK, Yarowsky PJ. Spatial memory deficits in segmental trisomic Ts65Dn mice. Behav Brain Res. 1996;82:85-92. PMID: 9021073
33. Hunter CL, Bimonte HA, Granholm AC. Behavioral comparison of 4 and 6 month-old Ts65Dn mice: age-related impairments in working and reference memory. Behav Brain Res. 2003;138:121-131. PMID: 12527443
34. Siarey RJ, Stoll J, Rapoport SI, Galdzicki Z. Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down Syndrome. Neuropharmacology. 1997;36:1549-1554. PMID: 9517425
35. Costa AC, Grybko MJ. Deficits in hippocampal CA1 LTP induced by TBS but not HFS in the Ts65Dn mouse: a model of Down syndrome. Neurosci Lett. 2005;382:317-322. PMID: 15925111
36. Garcia-Cerro S, Martinez P, Vidal V, Corrales A, Florez J, Vidal R, et al. Overexpression of Dyrk1A is implicated in several cognitive, electrophysiological and neuromorphological alterations found in a mouse model of Down syndrome. PLoS One. 2014;9:e106572. doi: 10.1371/journal.pone.0106572 PMID: 25188425
37. Lysenko LV, Kim J, Henry C, Tyrtyshnaia A, Kohnz RA, Madamba F, et al. Monoacylglycerol lipase inhibitor JZL184 improves behavior and neural properties in Ts65Dn mice, a model of Down syndrome. PLoS One. 2014;9:e114521. doi: 10.1371/journal.pone.0114521 PMID: 25474204
38. Kleschevnikov AM, Belichenko PV, Villar AJ, Epstein CJ, Malenka RC, Mobley WC. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J Neurosci. 2004;24:8153-8160. PMID: 15371516
39. Di Filippo M, Tozzi A, Ghiglieri V, Picconi B, Costa C, Cipriani S, et al. Impaired plasticity at specific subset of striatal synapses in the Ts65Dn mouse model of Down syndrome. Biol Psychiatry. 2010;67:666-671. doi: 10.1016/j.biopsych.2009.08.018 PMID: 19818432
40. Cooper JD, Salehi A, Delcroix JD, Howe CL, Belichenko PV, Chua-Couzens J, et al. Failed retrograde transport of NGF in a mouse model of Down's syndrome: reversal of cholinergic neurodegenerative phenotypes following NGF infusion. Proc Natl Acad Sci USA. 2001;98:10439-10444. PMID: 11504920
41. Salehi A, Faizi M, Colas D, Valletta J, Laguna J, Takimoto-Kimura R, et al. Restoration of norepinephrinemodulated contextual memory in a mouse model of Down syndrome. Sci Transl Med. 2009;1:7ra17. doi: 10.1126/scitranslmed.3000258 PMID: 20368182
42. Yu T, Liu C, Belichenko P, Clapcote SJ, Li S, Pao A, et al. Effects of individual segmental trisomies of human chromosome 21 syntenic regions on hippocampal long-term potentiation and cognitive behaviors in mice. Brain Res. 2010;1366:162-171. doi: 10.1016/j.brainres.2010.09.107 PMID: 20932954
43. Yu T, Li ZY, Jia ZP, Clapcote SJ, Liu CH, Li SM, et al. A mouse model of Down syndrome trisomic for all human chromosome 21 syntenic regions. Human Molecular Genetics. 2010;19:2780-2791. doi: 10.1093/hmg/ddq179 PMID: 20442137
44. Zhang L, Meng K, Jiang X, Liu C, Pao A, Belichenko PV, et al. Human chromosome 21 orthologous region on mouse chromosome 17 is a major determinant of Down syndrome-related developmental cognitive deficits. Hum Mol Genet. 2014;23:578-589. doi: 10.1093/hmg/ddt446 PMID: 24041763
45. Belichenko NP, Belichenko PV, Kleschevnikov AM, Salehi A, Reeves RH, Mobley WC. The "Down syndrome critical region" is sufficient in the mouse model to confer behavioral, neurophysiological, and synaptic phenotypes characteristic of Down syndrome. J Neurosci. 2009;29:5938-5948. doi: 10.1523/JNEUROSCI.1547-09.2009 PMID: 19420260
46. Kleschevnikov AM, Belichenko PV, Gall J, George L, Nosheny R, Maloney MT, et al. Increased efficiency of the GABAA and GABAB receptor-mediated neurotransmission in the Ts65Dn mouse model of Down syndrome. Neurobiol Dis. 2012;45:683-691. doi: 10.1016/j.nbd.2011.10.009 PMID: 22062771
47. Deacon RM. Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nat Protoc. 2006;1:122-124. PMID: 17406223
48. Thomas A, Burant A, Bui N, Graham D, Yuva-Paylor LA, Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl). 2009;204:361-373.
49. Bevins RA, Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat Protoc. 2006;1:1306-1311. PMID: 17406415
50. Niesman IR, Schilling JM, Shapiro LA, Kellerhals SE, Bonds JA, Kleschevnikov AM, et al. Traumatic brain injury enhances neuroinflammation and lesion volume in caveolin deficient mice. J Neuroinflammation. 2014;11:39. doi: 10.1186/1742-2094-11-39 PMID: 24593993
51. Cronk CE. Growth of children with Down's syndrome: birth to age 3 years. Pediatrics. 1978;61:564-568. PMID: 149290
52. De Asua DR, Parra P, Costa R, Moldenhauer F, Suarez C. Evaluation of the impact of abdominal obesity on glucose and lipid metabolism disorders in adults with Down syndrome. Research in Developmental Disabilities. 2014;35:2942-2949. doi: 10.1016/j.ridd.2014.07.038 PMID: 25108610
53. Simon P, Dupuis R, Costentin J. Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res. 1994;61:59-64. PMID: 7913324
54. 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;360:263-280. PMID: 2147289
55. Belichenko PV, Masliah E, Kleschevnikov AM, Villar AJ, Epstein CJ, Salehi A, et al. Synaptic structural abnormalities in the Ts65Dn mouse model of Down Syndrome. J Comp Neurol. 2004;480:281-298. PMID: 15515178
56. Fuchs C, Ciani E, Guidi S, Trazzi S, Bartesaghi R. Early-occurring proliferation defects in peripheral tissues of the Ts65Dn mouse model of Down syndrome are associated with patched1 over expression. Lab Invest. 2012;92:1648-1660. doi: 10.1038/labinvest.2012.117 PMID: 22890555
57. Olson LE, Mohan S. Bone density phenotypes in mice aneuploid for the Down syndrome critical region. Am J Med Genet A. 2011;155 A: 2436-2445. doi: 10.1002/ajmg.a.34203 PMID: 21915988
58. Costa AC, Walsh K, Davisson MT. Motor dysfunction in a mouse model for Down syndrome. Physiol Behav. 1999;68:211-220. PMID: 10627083
59. Galante M, Jani H, Vanes L, Daniel H, Fisher EM, Tybulewicz VL, et al. Impairments in motor coordination without major changes in cerebellar plasticity in the Tc1 mouse model of Down syndrome. Hum Mol Genet. 2009;18:1449-1463. doi: 10.1093/hmg/ddp055 PMID: 19181682
60. Martinez-Cue C, Rueda N, Garcia E, Davisson MT, Schmidt C, Florez J. Behavioral, cognitive and biochemical responses to different environmental conditions in male Ts65Dn mice, a model of Down syndrome. Behav Brain Res. 2005;163:174-185. PMID: 15941601
61. Turner CA, Presti MF, Newman HA, Bugenhagen P, Crnic L, Lewis MH. Spontaneous stereotypy in an animal model of Down syndrome: Ts65Dn mice. Behav Genet. 2001;31:393-400. PMID: 11720125
62. Driscoll LL, Carroll JC, Moon J, Crnic LS, Levitsky DA, Strupp BJ. Impaired sustained attention and error-induced stereotypy in the aged Ts65Dn mouse: a mouse model of Down syndrome and Alzheimer's disease. Behav Neurosci. 2004;118:1196-1205. PMID: 15598129
63. Reeves RH, Irving NG, Moran TH, Wohn A, Kitt C, Sisodia SS, et al. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat Genet. 1995;11:177-184. PMID: 7550346
64. Sago H, Carlson EJ, Smith DJ, Rubin EM, Crnic LS, Huang TT, et al. Genetic dissection of region associated with behavioral abnormalities in mouse models for Down syndrome. Pediatr Res. 2000;48:606-613. PMID: 11044479
65. Morice E, Andreae LC, Cooke SF, Vanes L, Fisher EM, Tybulewicz VL, et al. Preservation of longterm memory and synaptic plasticity despite short-term impairments in the Tc1 mouse model of Down syndrome. Learn Mem. 2008;15:492-500. doi: 10.1101/lm.969608 PMID: 18626093
66. Smith GK, Kesner RP, Korenberg JR. Dentate gyrus mediates cognitive function in the Ts65Dn/DnJ mouse model of Down syndrome. Hippocampus. 2014;24:354-362. doi: 10.1002/hipo.22229 PMID: 24339224
67. Fernandez F, Garner CC. Object recognition memory is conserved in Ts1Cje, a mouse model of Down syndrome. Neurosci Lett. 2007;421:137-141. PMID: 17566652
68. Siarey RJ, Villar AJ, Epstein CJ, Galdzicki Z. Abnormal synaptic plasticity in the Ts1Cje segmental trisomy 16 mouse model of Down syndrome. Neuropharmacology. 2005;49:122-128. PMID: 15992587
69. Haw CM, Barnes TRE, Clark K, Crichton P, Kohen D. Movement disorder in Down's syndrome: A possible marker of the severity of mental handicap. Movement Disorders. 1996;11:395-403. PMID: 8813219
70. Woods-Kettelberger A, Kongsamut S, Smith CP, Winslow JT, Corbett R. Animal models with potential applications for screening compounds for the treatment of obsessive-compulsive disorder. Expert Opin Investig Drugs. 1997;6:1369-1381. PMID: 15989507
71. Londei T, Valentini AM, Leone VG. Investigative burying by laboratory mice may involve nonfunctional, compulsive, behaviour. Behav Brain Res. 1998;94:249-254. PMID: 9722276
72. Gathercole SE, Alloway TP. Practitioner review: Short-term and working memory impairments in neurodevelopmental disorders: diagnosis and remedial support. Journal of Child Psychology and Psychiatry. 2006;47:4-15. PMID: 16405635
73. Jarrold C, Baddeley AD, Phillips C. Down syndrome and the phonological loop: the evidence for, and importance of, a specific verbal short-term memory deficit. Downs Syndr Res Pract. 1999;6:61-75. PMID: 11276981
74. Carlesimo GA, Marotta L, Vicari S. Long-term memory in mental retardation: evidence for a specific impairment in subjects with Down's syndrome. Neuropsychologia. 1997;35:71-79. PMID: 8981379
75. Vicari S, Bellucci S, Carlesimo GA. Implicit and explicit memory: a functional dissociation in persons with Down syndrome. Neuropsychologia. 2000;38:240-251. PMID: 10678691
76. Dierssen M. Down syndrome: the brain in trisomic mode. Nat Rev Neurosci. 2012;13:844-858. doi: 10.1038/nrn3314 PMID: 23165261
77. Roper RJ, Reeves RH. Understanding the basis for Down syndrome phenotypes. PLoS Genet. 2006;2:e50. PMID: 16596169
78. Pritchard MA, Kola I. The "gene dosage effect" hypothesis versus the "amplified developmental instability" hypothesis in Down syndrome. J Neural Transm Suppl. 1999;57:293-303. PMID: 10666684
79. Rachidi M, Lopes C. Mental retardation in Down syndrome: from gene dosage imbalance to molecular and cellular mechanisms. Neurosci Res. 2007;59:349-369. PMID: 17897742
80. Haydar TF, Blue ME, Molliver ME, Krueger BK, Yarowsky PJ. Consequences of trisomy 16 for mouse brain development: corticogenesis in a model of Down syndrome. J Neurosci. 1996;16:6175-6182. PMID: 8815899
81. Lacey-Casem ML, Oster-Granite ML. The neuropathology of the trisomy 16 mouse. Crit Rev Neurobiol. 1994;8:293-322. PMID: 7850875
82. Galdzicki Z, Siarey R, Pearce R, Stoll J, Rapoport SI. On the cause of mental retardation in Down syndrome: extrapolation from full and segmental trisomy 16 mouse models. Brain Res Brain Res Rev. 2001;35:115-145. PMID: 11336779
83. Holtzman DM, Bayney RM, Li YW, Khosrovi H, Berger CN, Epstein CJ, et al. Dysregulation of gene expression in mouse trisomy 16, an animal model of Down syndrome. EMBO J. 1992;11:619-627. PMID: 1371464
84. Duchon A, Raveau M, Chevalier C, Nalesso V, Sharp AJ, Herault Y. Identification of the translocation breakpoints in the Ts65Dn and Ts1Cje mouse lines: relevance for modeling Down syndrome. Mamm Genome. 2011;22:674-684. doi: 10.1007/s00335-011-9356-0 PMID: 21953411
85. Reinholdt LG, Ding Y, Gilbert GJ, Czechanski A, Solzak JP, Roper RJ, et al. Molecular characterization of the translocation breakpoints in the Down syndrome mouse model Ts65Dn. Mamm Genome. 2011;22:685-691. doi: 10.1007/s00335-011-9357-z PMID: 21953412
86. Gribble SM, Wiseman FK, Clayton S, Prigmore E, Langley E, Yang FT, et al. Massively Parallel Sequencing Reveals the Complex Structure of an Irradiated Human Chromosome on a Mouse Background in the Tc1 Model of Down Syndrome. PLoS One. 2013;8.
87. Levkovitz Y, Avignone E, Groner Y, Segal M. Upregulation of GABA neurotransmission suppresses hippocampal excitability and prevents long-term potentiation in transgenic superoxide dismutaseoverexpressing mice. J Neurosci. 1999;19:10977-10984. PMID: 10594078
88. Cooper A, Grigoryan G, Guy-David L, Tsoory MM, Chen A, Reuveny E. Trisomy of the G proteincoupled K+ channel gene, Kcnj6, affects reward mechanisms, cognitive functions, and synaptic plasticity in mice. Proc Natl Acad Sci USA. 2012;109:2642-2647. doi: 10.1073/pnas.1109099109 PMID: 22308328
89. Souchet B, Guedj F, Sahun I, Duchon A, Daubigney F, Badel A, et al. Excitation/inhibition balance and learning are modified by Dyrk1a gene dosage. Neurobiol Dis. 2014;69:65-75. doi: 10.1016/j. nbd.2014.04.016 PMID: 24801365
90. Sahun I, Marechal D, Pereira PL, Nalesso V, Gruart A, Garcia JM, et al. Cognition and hippocampal plasticity in the mouse is altered by monosomy of a genomic region implicated in Down syndrome. Genetics. 2014;197:899-912. doi: 10.1534/genetics.114.165241 PMID: 24752061
91. Mouton-Liger F, Sahun I, Collin T, Lopes Pereira P, Masini D, Thomas S, et al. Developmental molecular and functional cerebellar alterations induced by PCP4/PEP19 overexpression: implications for Down syndrome. Neurobiol Dis. 2014;63:92-106. doi: 10.1016/j.nbd.2013.11.016 PMID: 24291518
92. Dierssen M, Arque G, McDonald J, Andreu N, Martinez-Cue C, Florez J, et al. Behavioral Characterization of a Mouse Model Overexpressing DSCR1/RCAN1. PLoS One. 2011;6.
93. Azkona G, Amador-Arjona A, Obradors-Tarrago C, Varea E, Arque G, Pinacho R, et al. Characterization of a mouse model overexpressing beta-site APP-cleaving enzyme 2 reveals a new role for BACE2. Genes Brain Behav. 2010;9:160-172. doi: 10.1111/j.1601-183X.2009.00538.x PMID: 19840121
94. Gardiner K. Gene-dosage effects in Down syndrome and trisomic mouse models. Genome Biol. 2004;5:244. PMID: 15461808
95. Lalo E, Vercueil L, Bougerol T, Jouk PS, Debu B. Late event-related potentials and movement complexity in young adults with Down syndrome. Neurophysiologie Clinique-Clinical Neurophysiology. 2005;35:81-91. PMID: 16087071
96. Lauteslager PEM. Motor development in young children with Down syndrome. Physical and Motor Development in Mental Retardation. 1995;40:75-98.
97. Capone G, Goyal P, Ares W, Lannigan E. Neurobehavioral disorders in children, adolescents, and young adults with Down syndrome. American Journal of Medical Genetics Part C-Seminars in Medical Genetics. 2006;142 C: 158-172.
98. Ekstein S, Glick B, Weill M, Kay B, Berger I. Down syndrome and attention-deficit/hyperactivity disorder (ADHD). J Child Neurol. 2011;26:1290-1295. doi: 10.1177/0883073811405201 PMID: 21628698
99. Altafaj X, Dierssen M, Baamonde C, Marti E, Visa J, Guimera J, et al. Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Human Molecular Genetics. 2001;10:1915-1923. PMID: 11555628
100. Lott IT. Neurological phenotypes for Down syndrome across the life span. Prog Brain Res. 2012;197:101-121. doi: 10.1016/B978-0-444-54299-1.00006-6 PMID: 22541290
101. Evans DW, Gray FL. Compulsive-like behavior in individuals with Down syndrome: its relation to mental age level, adaptive and maladaptive behavior. Child Dev. 2000;71:288-300. PMID: 10834464
102. Prasher VP, Day S. Brief report: obsessive-compulsive disorder in adults with Down's Syndrome. J Autism Dev Disord. 1995;25:453-458. PMID: 7592255
103. Myers BA, Pueschel SM. Psychiatric disorders in persons with Down syndrome. J Nerv Ment Dis. 1991;179:609-613. PMID: 1833506
104. Douglass HM, Moffitt TE, Dar R, McGee R, Silva P. Obsessive-compulsive disorder in a birth cohort of 18-year-olds: prevalence and predictors. J Am Acad Child Adolesc Psychiatry. 1995;34:1424-1431. PMID: 8543509
105. Zohar AH. The epidemiology of obsessive-compulsive disorder in children and adolescents. Child Adolesc Psychiatr Clin N Am. 1999;8:445-460. PMID: 10442225
106. Nicolas LB, Kolb Y, Prinssen EP. A combined marble burying-locomotor activity test in mice: a practical screening test with sensitivity to different classes of anxiolytics and antidepressants. Eur J Pharmacol. 2006;547:106-115. PMID: 16934246
107. Njunge K, Handley SL. Evaluation of Marble-Burying Behavior as a Model of Anxiety. Pharmacology Biochemistry and Behavior. 1991;38:63-67.
108. Kerins G, Petrovic K, Bruder MB, Gruman C. Medical conditions and medication use in adults with Down syndrome: a descriptive analysis. Downs Syndr Res Pract. 2008;12:141-147. doi: 10.3104/reports.2009 PMID: 19026287
109. Somers JM, Goldner EM, Waraich P, Hsu L. Prevalence and incidence studies of anxiety disorders: a systematic review of the literature. Can J Psychiatry. 2006;51:100-113. PMID: 16989109
110. Baddeley A, Jarrold C. Working memory and Down syndrome. J Intellect Disabil Res. 2007;51:925-931. PMID: 17990999
111. Lanfranchi S, Jerman O, Vianello R. Working memory and cognitive skills in individuals with Down syndrome. Child Neuropsychol. 2009;15:397-416. doi: 10.1080/09297040902740652 PMID: 19274603
112. Whitney KN, Wenger GR. Working memory in the aged Ts65Dn mouse, a model for Down syndrome. Behav Brain Res. 2012;232:202-209. doi: 10.1016/j.bbr.2012.03.042 PMID: 22503781
113. Cramer N, Galdzicki Z. From abnormal hippocampal synaptic plasticity in down syndrome mouse models to cognitive disability in down syndrome. Neural Plast. 2012;2012:101542. doi: 10.1155/2012/101542 PMID: 22848844
114. Potier MC, Braudeau J, Dauphinot L, Delatour B. Reducing GABAergic inhibition restores cognitive functions in a mouse model of Down syndrome. CNS Neurol Disord Drug Targets. 2014;13:8-15. PMID: 24152333
115. Kaur G, Sharma A, Xu W, Gerum S, Alldred MJ, Subbanna S, et al. Glutamatergic transmission aberration: a major cause of behavioral deficits in a murine model of Down's syndrome. J Neurosci. 2014;34:5099-5106. doi: 10.1523/JNEUROSCI.5338-13.2014 PMID: 24719089
116. De S, Babu MM. Genomic neighbourhood and the regulation of gene expression. Curr Opin Cell Biol. 2010;22:326-333. doi: 10.1016/j.ceb.2010.04.004 PMID: 20493676
117. Deitz SL, Roper RJ. Trisomic and allelic differences influence phenotypic variability during development of Down syndrome mice. Genetics. 2011;189:1487-1495. doi: 10.1534/genetics.111.131391 PMID: 21926299
118. Aldridge K, Reeves RH, Olson LE, Richtsmeier JT. Differential effects of trisomy on brain shape and volume in related aneuploid mouse models. Am J Med Genet A. 2007;143A: 1060-1070. PMID: 17431903