Deficits in cognition and synaptic plasticity in a mouse model of down syndrome ameliorated by GABA B receptor antagonists

Journal of Neuroscience

Volumn 32, Issue 27, 2012, Pages 9217-9227

  Kleschevnikov, Alexander M ^a,d   Belichenko, Pavel V ^a,d   Faizi, Mehrdad ^b   Jacobs, Lucia F ^c   Htun, Khin ^b   Shamloo, Mehrdad ^b   Mobley, William C ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; [3 (3, 4 DICHLOROBENZYLAMINO) PROPYL] (DIETHOXYMETHYL) PHOSPHINIC ACID; BENZYL [3 [[1 (3, 4 DICHLOROPHENYL) ETHYL] AMINO] 2 HYDROXYPROPYL] PHOSPHINIC ACID; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONDITIONING; CONTROLLED STUDY; DOWN SYNDROME; ELECTROPHYSIOLOGY; EVOKED RESPONSE; FEAR; HIPPOCAMPUS; LOCOMOTION; LONG TERM MEMORY; LONG TERM POTENTIATION; MAZE TEST; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OBJECT RELATION; PRIORITY JOURNAL; RECOGNITION; SHORT TERM MEMORY; WESTERN BLOTTING; WORKING MEMORY;

ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; FEMALE; GABA-B RECEPTOR ANTAGONISTS; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; SYNAPTIC TRANSMISSION;

EID: 84863475944     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1673-12.2012     Document Type: Article

References (86)

1. Andre P, Ferrat T, Steinman M, Olpe HR (1992) Increased acetylcholine and quisqualate responsiveness after blockade of GABAB receptors. Eur J Pharmacol 218:137-143.
2. Barker GR, Warburton EC (2011) When is the hippocampus involved in recognition memory? J Neurosci 31:10721-10731.
3. Begenisic T, Spolidoro M, Braschi C, Baroncelli L, Milanese M, Pietra G, Fabbri ME, Bonanno G, Cioni G, Maffei L, Sale A (2011) Environmental enrichment decreases GABAergic inhibition and improves cognitive abilities, synaptic plasticity, and visual functions in a mouse model of Down syndrome. Front Cell Neurosci 5:29.
4. Belichenko NP, Belichenko PV, Kleschevnikov AM, Salehi A, Reeves RH, Mobley WC (2009) The "Down syndrome critical region" is sufficient in the mouse model to confer behavioral, neurophysiological, and synaptic phenotypes characteristic of Down syndrome. J Neurosci 29:5938-5948.
5. Belichenko PV, Masliah E, Kleschevnikov AM, Villar AJ, Epstein CJ, Salehi A, Mobley WC (2004) Synaptic structural abnormalities in the Ts65Dn mouse model of Down Syndrome. J Comp Neurol 480:281-298.
6. Belichenko PV, Kleschevnikov AM, Salehi A, Epstein CJ, Mobley WC (2007) Synaptic and cognitive abnormalities in mouse models of Down syndrome: exploring genotype-phenotype relationships. J Comp Neurol 504:329-345.
7. Belichenko PV, Kleschevnikov AM, Masliah E, Wu C, Takimoto-Kimura R, Salehi A, Mobley WC (2009) Excitatory-inhibitory relationship in the fascia dentata in the Ts65Dn mouse model of Down syndrome. J Comp Neurol 512:453-466.
8. Bennett GW, Ballard TM, Watson CD, Fone KC (1997) Effect of neuropeptides on cognitive function. Exp Gerontol 32:451-469.
9. Best TK, Siarey RJ, Galdzicki Z (2007) Ts65Dn, a mouse model of Down syndrome, exhibits increased GABAB-induced potassium current. J Neurophysiol 97:892-900.
10. Best TK, Cramer NP, Chakrabarti L, Haydar TF, Galdzicki Z (2012) Dysfunctional hippocampal inhibition in the Ts65Dn mouse model of Down syndrome. Exp Neurol 233:749-757.
11. Bevins RA, Besheer J (2006) Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory. Nat Protoc 1:1306-1311.
12. Bowes C, Li T, Frankel WN, Danciger M, Coffin JM, Applebury ML, Farber DB (1993) Localization of a retroviral element within the rd gene coding for the beta subunit of cGMP phosphodiesterase. Proc Natl Acad Sci U S A 90:2955-2959.
13. Braudeau J, Dauphinot L, Duchon A, Loistron A, Dodd RH, Hérault Y, Delatour B, Potier MC (2011a) Chronic treatment with a promnesiant GABA-A alpha5-selective inverse agonist increases immediate early genes expression during memory processing in mice and rectifies their expression levels in a Down syndrome mouse model. Adv Pharmacol Sci 2011:153218.
14. Braudeau J, Delatour B, Duchon A, Pereira PL, Dauphinot L, de Chaumont F, Olivo-Marin JC, Dodd RH, Hérault Y, Potier MC (2011b) Specific targeting of the GABA-A receptor alpha5 subtype by a selective inverse agonist restores cognitive deficits in Down syndrome mice. J Psychopharmacol 25:1030-1042.
15. Carlesimo GA, Marotta L, Vicari S (1997) Long-term memory in mental retardation: evidence for a specific impairment in subjects with Down's syndrome. Neuropsychologia 35:71-79.
16. Chakrabarti L, Best TK, Cramer NP, Carney RS, Isaac JT, Galdzicki Z, Haydar TF (2010) Olig1 and Olig2 triplication causes developmental brain defects in Down syndrome. Nat Neurosci 13: 1927-1934.
17. Chalifoux JR, Carter AG (2010) GABAB receptors modulate NMDA receptor calcium signals in dendritic spines. Neuron 66:101-113.
18. Charles KJ, Evans ML, Robbins MJ, Calver AR, Leslie RA, Pangalos MN (2001) Comparative immunohistochemical localisation of GABA(B1a), GABA(B1b) and GABA(B2) subunits in rat brain, spinal cord and dorsal root ganglion. Neuroscience 106:447-467.
19. Colombo G, Melis S, Brunetti G, Serra S, Vacca G, Carai MA, Gessa GL (2001) GABA(B) receptor inhibition causes locomotor stimulation in mice. Eur J Pharmacol 433:101-104.
20. Contestabile A, Benfenati F, Gasparini L (2010) Communication breaks Down: from neurodevelopment defects to cognitive disabilities in Down syndrome. Prog Neurobiol 91:1-22.
21. Cooper A, Grigoryan G, Guy-David L, Tsoory MM, Chen A, Reuveny E (2012) Trisomy of the G protein-coupled K channel gene, Kcnj6, affects reward mechanisms, cognitive functions, and synaptic plasticity in mice. Proc Natl Acad Sci U S A 109:2642-2647.
22. Costa AC, Grybko MJ (2005) Deficits in hippocampal CA1 LTP induced by TBS but not HFS in the Ts65Dn mouse: a model of Down syndrome. Neurosci Lett 382:317-322.
23. Costa AC, Scott-McKean JJ, Stasko MR (2008) 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 33:1624-1632.
24. Cramer NP, Best TK, Stoffel M, Siarey RJ, Galdzicki Z (2010) GABABGIRK2-mediated signaling in Down syndrome. Adv Pharmacol 58:397-426.
25. Davisson MT, Schmidt C, Reeves RH, Irving NG, Akeson EC, Harris BS, Bronson RT (1993) Segmental trisomy as a mouse model for Down syndrome. Prog Clin Biol Res 384:117-133.
26. Dierssen M, Fillat C, Crnic L, Arbonés M, Flórez J, Estivill X (2001) Murine models for Down syndrome. Physiol Behav 73:859-871.
27. Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, Bertolino A, Zaitsev E, Gold B, Goldman D, Dean M, Lu B, Weinberger DR (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112:257-269.
28. Faizi M, Bader PL, Tun C, Encarnacion A, Kleschevnikov A, Belichenko P, Saw N, Priestley M, Tsien RW, Mobley WC, Shamloo M (2011) Comprehensive behavioral phenotyping of Ts65Dn mouse model of down syndrome: activation of beta(1)-adrenergic receptor by xamoterol as a potential cognitive enhancer. Neurobiol Dis 43:397-413.
29. Fernandez F, Garner CC (2007a) Object recognition memory is conserved in Ts1Cje, a mouse model of Down syndrome. Neurosci Lett 421:137-141.
30. Fernandez F, Garner CC (2007b) Over-inhibition: a model for developmental intellectual disability. Trends Neurosci 30:497-503.
31. Fernandez F, Morishita W, Zuniga E, Nguyen J, Blank M, Malenka RC, Garner CC (2007) Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat Neurosci 10:411-413.
32. Froestl W, Gallagher M, Jenkins H, Madrid A, Melcher T, Teichman S, Mondadori CG, Pearlman R (2004) SGS742: the first GABA(B) receptor antagonist in clinical trials. Biochem Pharmacol 68:1479-1487.
33. Galdzicki Z, Siarey RJ (2003) Understanding mental retardation in Down's syndrome using trisomy 16 mouse models. Genes Brain Behav 2:167-178.
34. Gardiner K, Herault Y, Lott IT, Antonarakis SE, Reeves RH, Dierssen M (2010) Down syndrome: from understanding the neurobiology to therapy. J Neurosci 30:14943-14945.
35. Getova D, Bowery NG (1998) The modulatory effects of high affinity GABA(B) receptor antagonists in an active avoidance learning paradigm in rats. Psychopharmacology (Berl) 137:369-373.
36. Getova DP, Bowery NG (2001) Effects of high-affinity GABAB receptor antagonists on active and passive avoidance responding in rodents with gamma-hydroxybutyrolactone-induced absence syndrome. Psychopharmacology (Berl) 157:89-95.
37. Gotti S, Caricati E, Panzica G (2011) Alterations of brain circuits in Down syndrome murine models. J Chem Neuroanat 42:317-326.
38. Hanson JE, Blank M, Valenzuela RA, Garner CC, Madison DV (2007) The functional nature of synaptic circuitry is altered in area CA3 of the hippocampus in a mouse model of Down's syndrome. J Physiol 579:53-67.
39. Harashima C, Jacobowitz DM, Witta J, Borke RC, Best TK, Siarey RJ, Galdzicki Z (2006) Abnormal expression of the G-protein-activated inwardly rectifying potassium channel 2 (GIRK2) in hippocampus, frontal cortex, and substantia nigra of Ts65Dn mouse: a model of Down syndrome. J Comp Neurol 494:815-833.
40. Haydar TF, Reeves RH (2012) Trisomy 21 and early brain development. Trends Neurosci 35:81-91.
41. Heese K, Otten U, Mathivet P, Raiteri M, Marescaux C, Bernasconi R (2000) GABA(B) receptor antagonists elevate both mRNA and protein levels of the neurotrophins nerve growth factor (NGF) and brain-derived neurotrophic factor (BDNF) but not neurotrophin-3 (NT-3) in brain and spinal cord of rats. Neuropharmacology 39:449-462.
42. Helm KA, Haberman RP, Dean SL, Hoyt EC, Melcher T, Lund PK, Gallagher M (2005) GABAB receptor antagonist SGS742 improves spatial memory and reduces protein binding to the cAMP response element (CRE) in the hippocampus. Neuropharmacology 48:956-964.
43. Holtzman DM, Santucci D, Kilbridge J, Chua-Couzens J, Fontana DJ, Daniels SE, Johnson RM, Chen K, Sun Y, Carlson E, Alleva E, Epstein CJ, Mobley WC (1996) Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc Natl Acad Sci U S A 93:13333-13338.
44. Hyde LA, Frisone DF, Crnic LS (2001) Ts65Dn mice, a model for Down syndrome, have deficits in context discrimination learning suggesting impaired hippocampal function. Behav Brain Res 118:53-60.
45. Incerti M, Toso L, Vink J, Roberson R, Nold C, Abebe D, Spong CY (2011) Prevention of learning deficit in a Down syndrome model. Obstet Gynecol 117:354-361.
46. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16:147-154.
47. Kleschevnikov AM, Belichenko PV, Villar AJ, Epstein CJ, Malenka RC, Mobley WC (2004) Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J Neurosci 24:8153-8160.
48. Kleschevnikov AM, Van Volkinburg J, Zhan K, Mobley WC (2005) Expression of GIRK2 and related proteins after chronic administrations of Prozac in Ts65Dn mice, a genetic model of Down syndrome. Soc Neurosci Abstr 31:115.7.
49. Kleschevnikov AM, Belichenko PV, Gall J, George L, Nosheny R, Maloney MT, Salehi A, Mobley WC (2012a) Increased efficiency of the GABAA and GABAB receptor-mediated neurotransmission in the Ts65Dn mouse model of Down syndrome. Neurobiol Dis 45:683-691.
50. Kleschevnikov AM, Belichenko PV, Salehi A, Wu C (2012b) Discoveries in Down syndrome: moving basic science to clinical care. Prog Brain Res 197:199-221.
51. Kluge C, Stoppel C, Szinyei C, Stork O, Pape HC (2008) Role of the somatostatin system in contextual fear memory and hippocampal synaptic plasticity. Learn Mem 15:252-260.
52. Kulik A, Vida I, Luján R, Haas CA, López-Bendito G, Shigemoto R, Frotscher M (2003) Subcellular localization of metabotropic GABA(B) receptor subunits GABA(B1a/b) and GABA(B2) in the rat hippocampus. J Neurosci 23:11026-11035.
53. Kulik A, Vida I, Fukazawa Y, Guetg N, Kasugai Y, Marker CL, Rigato F, Bettler B, Wickman K, Frotscher M, Shigemoto R (2006) Compartmentdependent colocalization of Kir3.2-containing K channels and GABAB receptors in hippocampal pyramidal cells. J Neurosci 26:4289-4297.
54. Liu C, Belichenko PV, Zhang L, Fu D, Kleschevnikov AM, Baldini A, Antonarakis SE, Mobley WC, Yu YE (2011) Mouse models for Down syndrome-associated developmental cognitive disabilities. Dev Neurosci 33:404-413.
55. Lott IT, Dierssen M (2010) Cognitive deficits and associated neurological complications in individuals with Down's syndrome. Lancet Neurol 9:623-633.
56. Luscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA (1997) G proteincoupled inwardly rectifying K channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19:687-695.
57. Margeta-Mitrovic M, Mitrovic I, Riley RC, Jan LY, Basbaum AI (1999) Immunohistochemical localization of GABA(B) receptors in the rat central nervous system. J Comp Neurol 405:299-321.
58. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317:94-99.
59. Mitra A, Blank M, Madison DV (2012) Developmentally altered inhibition in Ts65Dn, a mouse model of Down syndrome. Brain Res 1440:1-8.
60. Mondadori C, Jaekel J, Preiswerk G (1993) CGP 36742: the first orally active GABAB blocker improves the cognitive performance of mice, rats, and rhesus monkeys. Behav Neural Biol 60:62-68.
61. Moore CS, Roper RJ (2007) The power of comparative and developmental studies for mouse models of Down syndrome. Mamm Genome 18:431-443.
62. Morrisett RA, Mott DD, Lewis DV, Swartzwelder HS, Wilson WA (1991) GABAB-receptor-mediated inhibition of the N-methyl-D-aspartate component of synaptic transmission in the rat hippocampus. J Neurosci 11:203-209.
63. Mott DD, Lewis DV (1991) Facilitation of the induction of long-term potentiation by GABAB receptors. Science 252:1718-1720.
64. Murer G, Adelbrecht C, Lauritzen I, Lesage F, Lazdunski M, Agid Y, Raisman Vozari R (1997) An immunocytochemical study on the distribution of two G-protein-gated inward rectifier potassium channels (GIRK2 and GIRK4) in the adult rat brain. Neuroscience 80:345-357.
65. Nadel L (2003) Down's syndrome: a genetic disorder in biobehavioral perspective. Genes Brain Behav 2:156-166.
66. Nagahara AH, Tuszynski MH (2011) Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat Rev Drug Discov 10:209-219.
67. Nyitrai G, Kékesi KA, Emri Z, Szárics E, Juhász G, Kardos J (2003) GABA(B) receptor antagonist CGP-36742 enhances somatostatin release in the rat hippocampus in vivo and in vitro. Eur J Pharmacol 478:111-119.
68. Olpe HR, Steinmann MW, Ferrat T, Pozza MF, Greiner K, Brugger F, Froestl W, Mickel SJ, Bittiger H (1993) The actions of orally active GABAB receptor antagonists on GABAergic transmission in vivo and in vitro. Eur J Pharmacol 233:179-186.
69. Olson LE, Roper RJ, Sengstaken CL, Peterson EA, Aquino V, Galdzicki Z, Siarey R, Pletnikov M, Moran TH, Reeves RH (2007) Trisomy for the Down syndrome 'critical region' is necessary but not sufficient for brain phenotypes of trisomic mice. Hum Mol Genet 16:774-782.
70. Pérez-Cremades D, Hernández S, Blasco-Ibáñez JM, Crespo C, Nacher J, Varea E (2010) Alteration of inhibitory circuits in the somatosensory cortex of Ts65Dn mice, a model for Down's syndrome. J Neural Transm 117:445-455.
71. Popov VI, Kleschevnikov AM, Klimenko OA, Stewart MG, Belichenko PV (2011) Three-dimensional synaptic ultrastructure in the dentate gyrus and hippocampal area CA3 in the Ts65Dn mouse model of down syndrome. J Comp Neurol 519:1338-1354.
72. Pozza MF, Manuel NA, Steinmann M, Froestl W, Davies CH (1999) Comparison of antagonist potencies at preand post-synaptic GABA(B) receptors at inhibitory synapses in the CA1 region of the rat hippocampus. Br J Pharmacol 127:211-219.
73. Reeves RH (2006) Down syndrome mouse models are looking up. Trends Mol Med 12:237-240.
74. Rueda N, Flórez J, Martínez-Cué C (2008) Chronic pentylenetetrazole but not donepezil treatment rescues spatial cognition in Ts65Dn mice, a model for Down syndrome. Neurosci Lett 433:22-27.
75. Sago H, Carlson EJ, Smith DJ, Rubin EM, Crnic LS, Huang TT, Epstein CJ (2000) Genetic dissection of region associated with behavioral abnormalities in mouse models for Down syndrome. Pediatr Res 48:606-613.
76. Salehi A, Faizi M, Belichenko PV, Mobley WC (2007) Using mouse models to explore genotype-phenotype relationship in Down syndrome. Ment Retard Dev Disabil Res Rev 13:207-214.
77. Salehi A, Faizi M, Colas D, Valletta J, Laguna J, Takimoto-Kimura R, Kleschevnikov A, Wagner SL, Aizen P, Shamloo M, Mobley WC (2009) Restoration of norepinephrine-modulated contextual memory in a mouse model of Down syndrome. SciTransl Med 1:7ra17.
78. Shichiri M, Yoshida Y, Ishida N, Hagihara Y, Iwahashi H, Tamai H, Niki E (2011) alpha-Tocopherol suppresses lipid peroxidation and behavioral and cognitive impairments in the Ts65Dn mouse model of Down syndrome. Free Radic Biol Med 50:1801-1811.
79. Siarey RJ, Stoll J, Rapoport SI, Galdzicki Z (1997) Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down Syndrome. Neuropharmacology 36:1549-1554.
80. Squire LR, Wixted JT, Clark RE (2007) Recognition memory and the medial temporal lobe: a new perspective. Nat Rev Neurosci 8:872-883.
81. Stäubli U, Scafidi J, Chun D (1999) GABAB receptor antagonism: facilitatory effects on memory parallel those on LTP induced by TBS but not HFS. J Neurosci 19:4609-4615
82. Sturgeon X, Gardiner KJ (2011) Transcript catalogs of human chromosome 21 and orthologous chimpanzee and mouse regions. Mamm Genome 22:261-271.
83. Sylvester PE (1983) The hippocampus in Down's syndrome. J Ment Defic Res 27:227-236.
84. Vicari S (2001) Implicit versus explicit memory function in children with Down and Williams syndrome. Downs Syndr Res Pract 7:35-40.
85. Yu T, Liu C, Belichenko P, Clapcote SJ, Li S, Pao A, Kleschevnikov A, Bechard AR, Asrar S, Chen R, Fan N, Zhou Z, Jia Z, Chen C, Roder JC, Liu B, Baldini A, Mobley WC, Yu YE (2010) Effects of individual segmental trisomies of human chromosome 21 syntenic regions on hippocampal long-term potentiation and cognitive behaviors in mice. Brain Res 1366:162-171.
86. Zhang L, Fu D, Belichenko PV, Liu C, Kleschevnikov AM, Pao A, Liang P, Clapcote SJ, Mobley WC, Yu YE (2012) Genetic analysis of Down syndrome facilitated by mouse chromosome engineering. Bioeng Bugs 3:8-12.