Excitation/inhibition balance and learning are modified by Dyrk1a gene dosage

Neurobiology of Disease

Volumn 69, Issue , 2014, Pages 65-75

  Souchet, Benoit ^a   Guedj, Fayçal ^a   Sahún, Ignasi ^b,c   Duchon, Arnaud ^d   Daubigney, Fabrice ^a   Badel, Anne ^a   Yanagawa, Yuchio ^e   Barallobre, Maria Jose ^f   Dierssen, Mara ^b,c   Yu, Eugene ^g   Herault, Yann ^d   Arbones, Mariona ^c,f   Janel, Nathalie ^a   Créau, Nicole ^a   Delabar, Jean Maurice ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^d INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^e GUNMA UNIVERSITY   (Japan)

^f UNIVERSITY OF BARCELONA   (Spain)

^g ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Down syndrome; DYRK1A; Excitation; Inhibition

Indexed keywords

GLUTAMATE DECARBOXYLASE 67; DYRK KINASE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DENSITY; COPY NUMBER VARIATION; DYRK1A GENE; EXCITATION; GABAERGIC TRANSMISSION; GENE DOSAGE; GENE OVEREXPRESSION; GENE TARGETING; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INHIBITION (PSYCHOLOGY); INTRACELLULAR SIGNALING; LEARNING; MALE; MAZE TEST; MEMORY; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PARTIAL TRISOMY; PRIORITY JOURNAL; ROTAROD TEST; SYNAPTOGENESIS; UPREGULATION; ANIMAL; C57BL MOUSE; DISEASE MODEL; DOWN SYNDROME; GENETICS; HUMAN; METABOLISM; MOTOR ACTIVITY; NERVE CELL; NERVE CELL INHIBITION; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SEIZURE; SYNAPSE; TRANSGENIC MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; GENE DOSAGE; HUMANS; LEARNING; MALE; MEMORY; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SEIZURES; SYNAPSES;

EID: 84902007612     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.04.016     Document Type: Article

References (63)

1. Ahn K.J., et al. DYRK1A BAC transgenic mice show altered synaptic plasticity with learning and memory defects. Neurobiol. Dis. 2006, 22:463-472.
2. Altafaj X., et al. Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum. Mol. Genet. 2001, 10:1915-1923.
3. Arque G., et al. Impaired spatial learning strategies and novel object recognition in mice haploinsufficient for the dual specificity tyrosine-regulated kinase-1A (Dyrk1A). PLoS One 2008, 3:e2575.
4. Begenisic T., et al. Environmental enrichment decreases GABAergic inhibition and improves cognitive abilities, synaptic plasticity, and visual functions in a mouse model of Down syndrome. Front. Cell. Neurosci. 2011, 5:29.
5. Belichenko N.P., et al. 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.
6. Belichenko P.V., et al. Excitatory-inhibitory relationship in the fascia dentata in the Ts65Dn mouse model of Down syndrome. J. Comp. Neurol. 2009, 512:453-466.
7. Best T.K., et al. Dysfunctional hippocampal inhibition in the Ts65Dn mouse model of Down syndrome. Exp. Neurol. 2012, 233:749-757.
8. Braudeau J., 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.
9. Chakrabarti L., et al. Olig1 and Olig2 triplication causes developmental brain defects in Down syndrome. Nat. Neurosci. 2010, 13:927-934.
10. Costa A.C., et al. 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.
11. Courcet J.B., et al. The DYRK1A gene is a cause of syndromic intellectual disability with severe microcephaly and epilepsy. J. Med. Genet. 2012, 49:731-736.
12. Cramer N.P., et al. GABAB-GIRK2-mediated signaling in Down syndrome. Adv. Pharmacol. 2010, 58:397-426.
13. Créau N. Molecular and cellular alterations in Down syndrome: toward the identification of targets for therapeutics. Neural Plast. 2012, 2012:171639.
14. Davisson M.T., et al. Segmental trisomy as a mouse model for Down syndrome. Prog. Clin. Biol. Res. 1993, 384:117-133.
15. De la Torre R., et al. Epigallocatechin-3-gallate, a DYRK1A inhibitor, rescues cognitive deficits in Down syndrome mouse models and in humans. Mol. Nutr. Food Res. 2014, 58:278-288.
16. Delabar J.M., et al. Molecular mapping of twenty-four features of Down syndrome on chromosome 21. Eur. J. Hum. Genet. 1993, 1:114-124.
17. Dowjat W.K., et al. Trisomy-driven overexpression of DYRK1A kinase in the brain of subjects with Down syndrome. Neurosci. Lett. 2007, 413:77-81.
18. Escorihuela R.M., et al. A behavioral assessment of Ts65Dn mice: a putative Down syndrome model. Neurosci. Lett. 1995, 199:143-146.
19. Faizi M., 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.
20. Fernandez F., et al. Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat. Neurosci. 2007, 10:411-413.
21. Fotaki V., et al. Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice. Mol. Cell. Biol. 2002, 22:6636-6647.
22. Guedj F., et al. Green tea polyphenols rescue of brain defects induced by overexpression of DYRK1A. PLoS One 2009, 4:e4606.
23. Guedj F., et al. DYRK1A: a master regulatory protein controlling brain growth. Neurobiol. Dis. 2012, 46:190-203.
24. Heinen M., et al. Adult-onset fluoxetine treatment does not improve behavioral impairments and may have adverse effects on the Ts65Dn mouse model of Down syndrome. Neural Plast. 2012, 2012:467251.
25. Kalueff A.V. Mapping convulsants' binding to the GABA-A receptor chloride ionophore: a proposed model for channel binding sites. Neurochem. Int. 2007, 50:61-68.
26. Kleschevnikov A.M., et al. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J. Neurosci. 2004, 24:8153-8160.
27. Kleschevnikov A.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.
28. Kleschevnikov A.M., 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.
29. Krumm N., et al. A de novo convergence of autism genetics and molecular neuroscience. Trends Neurosci. 2014, 37:95-105.
30. Lau C.G., Murthy V.N. Activity-dependent regulation of inhibition via GAD67. J. Neurosci. 2012, 32:8521-8531.
31. Li Z., et al. Duplication of the entire 22.9Mb human chromosome 21 syntenic region on mouse chromosome 16 causes cardiovascular and gastrointestinal abnormalities. Hum. Mol. Genet. 2007, 16:1359-1366.
32. Lockrow J., et al. Effects of long-term memantine on memory and neuropathology in Ts65Dn mice, a model for Down syndrome. Behav. Brain Res. 2011, 221:610-622.
33. Martinez-Cue C., et al. Reducing GABAA alpha5 receptor-mediated inhibition rescues functional and neuromorphological deficits in a mouse model of Down syndrome. J. Neurosci. 2013, 33:3953-3966.
34. Medina A.E., et al. Sex differences in sensitivity to seizures elicited by pentylenetetrazol in mice. Pharmacol. Biochem. Behav. 2001, 68:591-596.
35. Möhler H. Cognitive enhancement by pharmacological and behavioral interventions: the murine Down syndrome model. Biochem. Pharmacol. 2012, 84:994-999.
36. Moller R.S., et al. Truncation of the Down syndrome candidate gene DYRK1A in two unrelated patients with microcephaly. Am. J. Hum. Genet. 2008, 82:1165-1170.
37. Oegema R., et al. Distinctive phenotypic abnormalities associated with submicroscopic 21q22 deletion including DYRK1A. Mol. Syndromol. 2010, 1:113-120.
38. Olson L.E., 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.
39. O'Roak B.J., et al. Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science 2012, 338:1619-1622.
40. Perez-Cremades D., et al. Alteration of inhibitory circuits in the somatosensory cortex of Ts65Dn mice, a model for Down's syndrome. J. Neural Transm. 2010, 117:445-455.
41. Potier M.C., et al. Reducing GABAergic inhibition restores cognitive functions in a mouse model of Down syndrome. CNS Neurol. Disord. Drug Targets 2014 Feb, 13(1):8-15.
42. Rahmani Z., et al. Critical role of the D21S55 region on chromosome 21 in the pathogenesis of Down syndrome. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:5958-5962.
43. Reeves R.H., et al. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat. Genet. 1995, 11:177-184.
44. Reinholdt L.G., et al. Molecular characterization of the translocation breakpoints in the Down syndrome mouse model Ts65Dn. Mamm. Genome 2011, 22:685-691.
45. Rogers D.C., et al. SHIRPA, a protocol for behavioral assessment: validation for longitudinal study of neurological dysfunction in mice. Neurosci. Lett. 2001, 306:89-92.
46. Ronan A., et al. Familial 4.3Mb duplication of 21q22 sheds new light on the Down syndrome critical region. J. Med. Genet. 2007, 44:448-451.
47. Rubenstein J.L., Merzenich M.M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003, 2:255-267.
48. Rueda N., et al. Memantine normalizes several phenotypic features in the Ts65Dn mouse model of Down syndrome. J. Alzheimers Dis. 2010, 21:277-290.
49. Sahara S., et al. The fraction of cortical GABAergic neurons is constant from near the start of cortical neurogenesis to adulthood. J. Neurosci. 2012, 32:4755-4761.
50. Siarey R.J., et al. Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down Syndrome. Neuropharmacology 1997, 36:1549-1554.
51. Siddiqui A., et al. Molecular responses of the Ts65Dn and Ts1Cje mouse models of Down syndrome to MK-801. Genes Brain Behav. 2008, 7:810-820.
52. Singer H.S., Minzer K. Neurobiology of Tourette's syndrome: concepts of neuroanatomic localization and neurochemical abnormalities. Brain Dev. 2003, 25(Suppl. 1):S70-S84.
53. Smith D.J., et al. Functional screening of 2Mb of human chromosome 21q22.2 in transgenic mice implicates minibrain in learning defects associated with Down syndrome. Nat. Genet. 1997, 16:28-36.
54. Sun Q., Turrigiano G.G. PSD-95 and PSD-93 play critical but distinct roles in synaptic scaling up and down. J. Neurosci. 2011, 31:6800-6808.
55. Tamamaki N., et al. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol. 2003, 467:60-79.
56. Tejedor F., et al. minibrain: a new protein kinase family involved in postembryonic neurogenesis in Drosophila. Neuron 1995, 14:287-301.
57. Thomazeau A., et al. Prefrontal deficits in a murine model overexpressing the down syndrome candidate gene dyrk1a. J. Neurosci. 2014, 34:1138-1147.
58. Turner C.P., et al. Postnatal exposure to MK801 induces selective changes in GAD67 or parvalbumin. Exp. Brain Res. 2010, 201:479-488.
59. van Bon B.W., et al. Intragenic deletion in DYRK1A leads to mental retardation and primary microcephaly. Clin. Genet. 2011, 79:296-299.
60. Vidal V., et al. Lack of behavioral and cognitive effects of chronic ethosuximide and gabapentin treatment in the Ts65Dn mouse model of Down syndrome. Neuroscience 2012, 220:158-168.
61. Voronov S.V., et al. Synaptojanin 1-linked phosphoinositide dyshomeostasis and cognitive deficits in mouse models of Down's syndrome. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:9415-9420.
62. Wassef A., et al. GABA and schizophrenia: a review of basic science and clinical studies. J. Clin. Psychopharmacol. 2003, 23:601-640.
63. Yu T., 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.