Prefrontal deficits in a murine model overexpressing the down syndrome candidate gene Dyrk1A

Journal of Neuroscience

Volumn 34, Issue 4, 2014, Pages 1138-1147

  Thomazeau, Aurore ^a,b,c   Lassalle, Olivier ^a,b,c   Iafrati, Jillian ^a,b,c   Souchet, Benoit ^d   Guedj, Fayçal ^d   Janel, Nathalie ^d   Chavis, Pascale ^a,b,c   Delabar, Jean ^d   Manzoni, Olivier J ^a,b,c  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Down syndrome; Dyrk1a; Green tea; NMDAR; Prefrontal cortex; Synaptic plasticity

Indexed keywords

DOWN SYNDROME; DYRK1A; GREEN TEA; NMDAR; PREFRONTAL CORTEX; SYNAPTIC PLASTICITY;

ANIMALS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; DOWN SYNDROME; MALE; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; PYRAMIDAL CELLS;

EID: 84892755214     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2852-13.2014     Document Type: Article

References (41)

1. Altafaj X, Martín ED, Ortiz-Abalia J, Valderrama A, Lao-Peregrín C, Dierssen M, Fillat C (2013) Normalization of Dyrk1A expression by AAV2/1-shDyrk1A attenuates hippocampal-dependent defects in the Ts65Dn mouse model of Down syndrome. Neurobiol Dis 52:117-127. CrossRef Medline
2. Bagni C, Greenough WT (2005) From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome. Nat Rev Neurosci 6:376-387. CrossRef Medline
3. BeckerW (2011) Recent insights into the function of DYRK1A. FEBS J 278: 222. CrossRef Medline
4. Belichenko NP, Belichenko PV, Kleschevnikov AM, Salehi A, Reeves RH, MobleyWC (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. CrossRef Medline
5. Benavides-Piccione R, Dierssen M, Ballesteros-Yáñez I, Martínez de Lagrán M, Arbonés ML, Fotaki V, DeFelipe J, Elston GN (2005) Alterations in the phenotype of neocortical pyramidal cells in the Dyrk1A+/-mouse. Neurobiol Dis 20:115-122. CrossRef Medline
6. Busquets-Garcia A, Gomis-González M, Guegan T, Agustín-Pavón C, Pastor A, Mato S, Pérez-Samartín A, Matute C, de la Torre R, Dierssen M, Maldonado R, Ozaita A (2013) Targeting the endocannabinoid system in the treatment of fragile X syndrome. Nat Med 19:603-607. CrossRef Medline
7. Chavis P, Westbrook G (2001) Integrins mediate functional pre-and postsynaptic maturation at a hippocampal synapse. Nature 411:317-321. CrossRef Medline
8. 2+-dependent intracellular signaling. J Neurophysiol 97:2448-2464. CrossRef Medline
9. Daoudal G, Hanada Y, Debanne D (2002) Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 99:14512-14517. CrossRef Medline
10. De la Torre R, De Sola S, Pons M, Duchon A, Martinez de Lagran M, Farre M, Fito M, Benejam B, Langohr K, Rodriguez J, Pujadas M, Bizot JC, Cuenca A, Janel N, Catuara S, Covas MI, Blehaut H, Herault Y, Delabar JM, DierssenM (2013) Epigallocatechin-3-gallate, aDYRK1Ainhibitor, rescues cognitive deficits in Down syndrome mouse models and in humans. Mol Nutr Food Res. Advance online publication. Retrieved Sept. 14, 2013. doi: 10.1002/mnfr.201300325. CrossRef Medline
11. Delabar JM, Theophile D, Rahmani Z, Chettouh Z, Blouin JL, Prieur M, Noel B, SinetPM (1993) Molecular mapping of twenty-four features ofDown syndrome on chromosome 21. Eur J Hum Genet 1:114-124. Medline
12. Di Filippo M, Tozzi A, Ghiglieri V, Picconi B, Costa C, Cipriani S, Tantucci M, Belcastro V, Calabresi P (2010) Impaired plasticity at specific subset of striatal synapses in the Ts65Dn mouse model of Down Syndrome. Biol Psychiatry 67:666-671. CrossRef Medline
13. Feng W, Zhang M (2009) Organization and dynamics of PDZ-domainrelated supramodules in the postsynaptic density. Nat Rev Neurosci 10: 87-99. CrossRef Medline
14. 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. CrossRef Medline
15. Garner CC, Wetmore DZ (2012) Synaptic pathology of down syndrome. Adv Exp Med Biol 970:451-468. CrossRef Medline
16. Goldman-Rakic PS (1990) Cellular and circuit basis of working memory in prefrontal cortex of nonhuman primates. Prog Brain Res 85:325-335; discussion 335-336. Medline
17. Goto Y, Yang CR, Otani S (2010) Functional and dysfunctional synaptic plasticity in prefrontal cortex: roles in psychiatric disorders. Biol Psychiatry 67:199-207. CrossRef Medline
18. 2+/calmodulin-dependent protein kinase II in cultured prefrontal cortical neurons. Mol Pharmacol 69:813-822. CrossRef Medline
19. Guedj F, Sébrié C, Rivals I, Ledru A, Paly E, Bizot JC, Smith D, Rubin E, Gillet B, Arbones M, Delabar JM (2009) Green tea polyphenols rescue of brain defects induced by overexpression of DYRK1A. PLoS One 4:e4606. CrossRef Medline
20. Guedj F, Pereira PL, Najas S, Barallobre MJ, Chabert C, Souchet B, Sebrie C, Verney C, Herault Y, Arbones M, Delabar JM (2012) DYRK1A: a master regulatory protein controlling brain growth. Neurobiol Dis 46:190-203. CrossRef Medline
21. Hill MN, Hillard CJ, Bambico FR, Patel S, Gorzalka BB, GobbiG (2009) The therapeutic potential of the endocannabinoid system for the development of a novel class of antidepressants. Trends Pharmacol Sci 30:484-493. CrossRef Medline
22. Hirsch JC, Crepel F (1990) Use-dependent changes in synaptic efficacy in rat prefrontal neurons in vitro. J Physiol 427:31-49. Medline
23. Iafrati J, Orejarena MJ, Lassalle O, Bouamrane L, Chavis P (2013) Reelin, an extracellular matrix protein linked to early onset psychiatric diseases, drives postnatal development of the prefrontal cortex via GluN2BNMDARs and the mTOR pathway. Mol Psychiatry. Advance online publication. Retrieved Oct. 22, 2031. doi: 10.1038/mp.2013.148. CrossRef Medline
24. Jung KM, Sepers M, Henstridge CM, Lassalle O, Neuhofer D, Martin H, Ginger M, Frick A, DiPatrizio NV, Mackie K, Katona I, Piomelli D, Manzoni OJ (2012) Uncoupling of the endocannabinoid signalling complex in a mouse model of fragile X syndrome. Nat Commun 3:1080. CrossRef Medline
25. Kasanetz F, Manzoni OJ (2009) Maturation of excitatory synaptic transmission of the rat nucleus accumbens from juvenile to adult. J Neurophysiol 101:2516-2527. CrossRef Medline
26. Lafourcade M, Elezgarai I, Mato S, Bakiri Y, Grandes P, Manzoni OJ (2007) Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. PLoS One 2:e709. CrossRef Medline
27. Lafourcade M, Larrieu T, Mato S, Duffaud A, Sepers M, Matias I, De Smedt-Peyrusse V, Labrousse VF, Bretillon L, Matute C, Rodríguez-Puertas R, Layé S, Manzoni OJ (2011) Nutritional omega-3 deficiency abolishes endocannabinoid-mediated neuronal functions. Nat Neurosci 14:345-350. CrossRef Medline
28. Lanfranchi S, Jerman O, Dal Pont E, Alberti A, Vianello R (2010) Executive function in adolescents with Down Syndrome. J Intellect Disabil Res 54: 308-319. CrossRef Medline
29. Lepagnol-Bestel AM, Zvara A, Maussion G, Quignon F, Ngimbous B, Ramoz N, Imbeaud S, Loe-Mie Y, Benihoud K, Agier N, Salin PA, Cardona A, Khung-Savatovsky S, Kallunki P, Delabar JM, Puskas LG, Delacroix H, Aggerbeck L, Delezoide AL, Delattre O, et al. (2009) DYRK1A interacts with the REST/NRSF-SWI/SNF chromatin remodelling complex to deregulate gene clusters involved in the neuronal phenotypic traits of Down syndrome. Hum Mol Genet 18:1405-1414. CrossRef Medline
30. Lisman J, Yasuda R, Raghavachari S (2012) Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 13:169-182. CrossRef Medline
31. Lledo PM, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, Nicoll RA (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci U S A 92:11175-11179. CrossRef Medline
32. Marrs WR, Blankman JL, Horne EA, Thomazeau A, Lin YH, Coy J, Bodor AL, Muccioli GG, Hu SS, Woodruff G, Fung S, Lafourcade M, Alexander JP, Long JZ, Li W, Xu C, Möller T, Mackie K, Manzoni OJ, Cravatt BF, et al. (2010) The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors. Nat Neurosci 13:951-957. CrossRef Medline
33. Martinez de Lagran M, Benavides-Piccione R, Ballesteros-Yañez I, Calvo M, Morales M, Fillat C, Defelipe J, Ramakers GJ, Dierssen M (2012) Dyrk1A influences neuronal morphogenesis through regulation of cytoskeletal dynamics in mammalian cortical neurons. Cereb Cortex 22:2867-2877. CrossRef Medline
34. Pennington BF, Moon J, Edgin J, Stedron J, Nadel L (2003) The neuropsychology of Down syndrome: evidence for hippocampal dysfunction. Child Dev 74:75-93. CrossRef Medline
35. Penzes P, Cahill ME, Jones KA, VanLeeuwen JE, WoolfreyKM (2011) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14: 285-293. CrossRef Medline
36. Puente N, Cui Y, Lassalle O, Lafourcade M, Georges F, Venance L, Grandes P, Manzoni OJ (2011) Polymodal activation of the endocannabinoid system in the extended amygdala. Nat Neurosci 14:1542-1547. CrossRef Medline
37. 2+ channels in metabotropic glutamate receptor 2/3-dependent presynaptic long-term depression at nucleus accumbens synapses. J Neurosci 22:4346-4356. Medline
38. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ (2002b) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci U S A 99:8384-8388. CrossRef Medline
39. Sanhueza M, Lisman J (2013) The CaMKII/NMDAR complex as a molecular memory. Mol Brain 6:10. CrossRef Medline
40. Seamans JK, Floresco SB, Phillips AG (1995) Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav Neurosci 109:1063-1073. CrossRef Medline
41. Stein V, House DR, Bredt DS, Nicoll RA (2003) Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J Neurosci 23:5503-5506. Medline