Impaired hippocampal plasticity and altered neurogenesis in adult Ube3a maternal deficient mouse model for Angelman syndrome

Experimental Neurology

Volumn 220, Issue 2, 2009, Pages 341-348

  Mardirossian, Sandrine ^a   Rampon, Claire ^b   Salvert, Denise ^a   Fort, Patrice ^a   Sarda, Nicole ^a  

^a UNIVERSITÉ LYON 1   (France)

^b Université Paul Sabatier   (France)

Author keywords

Angelman syndrome; BrdU; Doublecortin; Hippocampal plasticity; Immediate early genes; Ki67; NeuN; Neurogenesis; Ube3a maternal deficiency

Indexed keywords

BRAIN PROTEIN; BROXURIDINE; DOUBLECORTIN; KI 67 ANTIGEN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN ARC; PROTEIN C FOS; PROTEIN UBE3A; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; GENE DELETION; GENE EXPRESSION; GRANULE CELL; HAPPY PUPPET SYNDROME; HIPPOCAMPUS; IMMEDIATE EARLY GENE; IMMUNOHISTOCHEMISTRY; LEARNING; MEMORY; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL;

ANGELMAN SYNDROME; ANIMALS; ANTIMETABOLITES; BROMODEOXYURIDINE; CELL PROLIFERATION; CELL SURVIVAL; GENES, FOS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; NEUROPEPTIDES; UBIQUITIN-PROTEIN LIGASES;

EID: 71549116102     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.08.035     Document Type: Article

References (72)

1. Aimone J.B., Willes J., and Gage F.H. Potential role for adult neurogenesis in the encoding of time in new memories. Nat. Neurosci. 9 (2006) 723-727
2. Albrecht U., Sutcliffe J.S., Cattanach B.M., Beechey C.V., Armstong D., Eichele G., and Beaudet A.L. Imprinted expression of the murine Angelman syndrome gene, Ube3a, in hippocampal and Purkinje neurons. Nat. Genet. 17 (1997) 75-78
3. Bramham C.R., Worley P.F., Moore M.J., and Guzowski J.F. The immediate early gene arc/arg 3.: regulation, mechanisms and function. J. Neurosci. 28 (2008) 11760-11767
4. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., and Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467 (2003) 1-10
5. Bruel-Jungerman E., Rampon C., and Laroche S. Adult neurogenesis, synaptic plasticity and memory: facts and hypotheses. Rev. Neurosci. 18 (2007) 93-114
6. Cantero J.L., Atienza M., Stickgold R., Kahana M.J., Madsen J.R., and Kocsis B. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 23 (2003) 10897-10903
7. Cheron G., Servais L., Wagstaff J., and Dan A. Fast cerebellar oscillation associated with ataxia in a mouse model of Angelman syndrome. Neuroscience 130 (2005) 631-637
8. Cheron G., Servais L., and Dan B. Cerebellar network plasticity: from genes to fast oscillation. Neuroscience 153 (2008) 1-19
9. Clark S., Schwalbe J., Stasko M.R., Yarowsky P.J., and Costa A.C.S. Fluoxetine rescues deficient neurogenesis in hippocampus of the Ts65Dn mouse model for Down syndrome. Exp. Neurol. 200 (2006) 256-261
10. Clayton-Smith J., and Laan L. Angelman syndrome: a review of the clinical and genetics aspects. J. Med. Genet. 40 (2003) 87-95
11. Colas D., Wagstaff J., Fort P., Salvert D., and Sarda N. Sleep disturbances in Ube3a maternal-deficient mice modelling Angelman syndrome. Neurobiol. Dis. 20 (2005) 471-478
12. Cole A.J., Saffen D.W., Baraban J.M., and Worley P.F. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340 (1989) 474-476
13. Cooper-Kuhn C.M., and Kuhn H.G. Is it all DNA repair? Methodological considerations for detecting neurogenesis in the adult brain. Brain. Res. Dev. 134 (2002) 13-21
14. Couillard-Despres S., Winner B., Schaubeck S., Aignier R., Vroemen M., Weider N., Bogdahn U., Winkler J., Kuhn H.G., and Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21 (2005) 1-14
15. Dan B., and Boyd S.G. Angelman syndrome reviewed from a neurophysiological perspective. The UBE3A-GABRB3 hypothesis. Neuropediatrics 34 (2003) 169-176
16. Dan B., Boyd S.G., and Cheron G. From genomic imprinting to developmental physiology: identifying stepping stones. Curr. Pharmacogenom. 2 (2004) 3
17. Dan B., Servais L., Boyd S.G., Wagstaff J., and Cheron G. From electrophysiology to chromatin: a bottom-up approach to Angelman syndrome. Ann. N. Y. Acad. Sci. 1030 (2004) 599-611
18. Dan B., Boyd S.G., Pelc K., and Cheron G. Lamotrigine effect on GABA transmission in Angelman syndrome?. Epilepsia 48 (2007) 1634
19. Dayer A.G., Ford A.A., Cleaver K.M., Yassaee M., and Cameron H.A. Short-term and long-term survival of new neurons in the dentate gyrus. J. Comp. Neurol. 460 (2003) 563-572
20. Dindot S.T., Antalffy B.A., Bhattacharjee M.B., and Beaudet A.L. The Angelman syndrome ubiquitin ligase localizes to the synapse and nucleus, and maternal deficiency results in abnormal dendritic spine morphology. Hum. Mol. Genet. 17 (2008) 111-118
21. Fleischmann A., Hvalby O., Jensen V., Strekalova T., Zacher C., Layer L.E., Kvello A., Reschke M., Spanagel R., Sprengel R., Wagner E.F., and Gass P. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J. Neurosci. 23 (2003) 9116-9122
22. Ge S., Goh E.L., Sailor K.A., Kitabatake Y., Ming G.L., and Song H. GABA regulates synaptic plasticity integration of newly generated neurons in the adult brain. Nature 439 (2006) 589-593
23. Ge S., Pradhan A., Ming G.L., and Song H. GABA sets the tempo for activity-dependent adult neurogenesis. Trends. Neurosci. 30 (2007) 1-8
24. Ge S., Sailor K.A., Ming G.L., and Song H. Synaptic integration and plasticity of new neurons in the adult hippocampus. J. Physiol. 586 (2008) 3759-3765
25. Guzman-Marin R., Bashir T., Suntsova N., Szymusiak R., and McGinty D. Hippocampal neurogenesis reduced by sleep fragmentation in the adult rat. Neuroscience 148 (2007) 325-333
26. Guzman-Marin R., Suntsova N., Bashir T., Nienhuis R., Szymusiak R., and McGinty D. Rapid eye movement sleep deprivation contributes to reduction of neurogenesis in the hippocampal dentate gyrus of the adult rat. Sleep 31 (2008) 167-175
27. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., and Barnes C.A. Inhibition of activity-dependent Arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J. Neurosci. 20 (2000) 3993-4001
28. Guzowski J.F., Setlow B., Wagner E.K., and McGaugh J.L. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 21 (2001) 5089-5098
29. Hansel C., de Jeu M., Belmaguenai A., Houtman S.H., Buitendijk G.H., Andreev D., De Zeeuw C.I., and Elgersman Y. alphaCaMKII is essential for cerebellar LTD and motor learning. Neuron 51 (2006) 835-843
30. Heck D.H., Zhao Y., Roy S., LeDoux M.S., and Reiter L.T. Analysis of cerebellar function in Ube3a-deficient mice reveals novel genotype-specific behaviours. Hum. Mol. Genet. 17 (2008) 2181-2189
31. Heine V.M., Maslam S., Joels M., and Lucassen P.J. Prominent decline of newborn cell proliferation, differentiation and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol. Aging. 25 (2004) 361-375
32. Jessberger S., and Kempermann G. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur. J. Neurosci. 18 (2003) 2712-2727
33. Jessberger S., Römer B., Babu H., and Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp. Neurol. 196 (2005) 342-351
34. Jiang Y.H., Armstrong D., Albrecht U., Atkins C.M., Noebels J.L., Eichele G., Sweatt J.D., and Beaudet A.L. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 21 (1998) 799-811
35. Kee N., Sivalingam S., Boonstra R., and Wojtowicz J.M. The utility of Ki67 and BrdU as proliferative markers of adult neurogenesis. J. Neurosci. Methods. 115 (2002) 97-105
36. Kee N., Teixeira C.M., Wang A.H., and Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci 10 (2007) 355-362
37. Kempermann G., Gast D., Kronenberg G., Yamaguchi A., and Gage F.H. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130 (2003) 391-399
38. Kempermann G., Wiskott L., and Gage F.H. Functional significance of adult neurogenesis. Curr. Opin. Neurobiol. 14 (2004) 186-191
39. Kempermann G., Jessberger S., Steiner B., and Kronenberg G. Milestones of neural development in the adult neurogenesis. Trends. Neurosci. 27 (2004) 447-452
40. Kishino T., Lalande M., and Wagstaff J. UBE3A/E6-AP mutations cause Angelman syndrome. Nat. Genet. 15 (1997) 70-73
41. Kubik S., Miyashita T., and Guzowski J.F. Using immediate early genes to map hippocampal subregional functions. Learn. Mem. 14 (2007) 758-770
42. Lam B.Y., Zhang W., Enticknap N., Haggis E., Cader M.Z., and Chawla S. Inverse rezgulation of plasticity-related immediate realy genes by calcineurin in hippocampal neurons. J. Biol. Chem. 284 (2009) 12562-12571
43. Lossie A.C., Whitney M.M., Amidon D., Dong H.J., Chen P., Theriaque D., Hutson A., Nicholls R.D., Zori R.T., Williams C.A., and Driscoll D.J. Distinct phenotypes distinguish the molecular classes of Angelman syndrome. J. Med. Genet. 12 (2001) 834-845
44. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., Gilbert D.J., Jenkins N.A., Lanahan A.A., and Worley P.F. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14 (1995) 433-435
45. Matsura T., Sutcliffe J.S., Fang P., Galjaard R.J., Jiang Y., Benton C.S., Romens J.M., and Beaudet A.L. Do novo truncating mutations in E6-AP ubiquitin-protein ligase gene (UBE3A) in Angelman syndrome. Nat. Genet. 15 (1997) 74-77
46. McCaugh J.L. Memory: a century of consolidation. Science 287 (2000) 248-251
47. Ming G.L., and Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28 (2005) 223-250
48. Miura K., Kishino T., Li E., Webber H., Dikkes P., Holmes G.L., and Wagstaff J. Neurobehavioral and electroencephalographic abnormalities in Ube3a maternal-deficient mice. Neurobiol. Dis. 9 (2002) 149-159
49. Morris R.G.M., Garrud P., Rawlins J.N.P., and O'Keefe J. Place navigation is impaired in rats with hippocampal lesions. Nature 297 (1982) 681-683
50. Munoz-Cabello B., Rufo-Campos M., Madruga-Garrido M., Blanco-Martinez B., Ruiz-Del Portal L., and Candau Fernandez-Mensaque R. Epileptic seizures in Angelman syndrome. Rev. Neurol. 47 (2008) 113-118
51. Ogata K., and Kosaka T. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113 (2002) 221-233
52. Overstreet-Wadiche L.S., Bensen A.L., and Westbrook G.L. Delayed development of adult granule cells in dentate gyrus. J. Neurosci. 26 (2006) 2326-2334
53. Parent J.M., and Murphy G.G. Mechanisms and functional significance of aberrant seizure-induced hippocampal neurogenesis. Epilepsia 5 (2008) 19-25
54. Pelc K., Cheron G., Boyd S.G., and Dan B. Are there distinctive sleep problems in Angelman syndrome?. Sleep. Med. 9 (2008) 434-441
55. Pelc K., Cheron G., and Dan B. Behavior and neuropsychiatric manifestations in Angelman syndrome. Neuropsychiatr. Dis. Treat. 4 (2008) 577-584
56. Pelc K., Boyd S.G., Cheron G., and Dan B. Epilepsy in Angelman syndrome. Seizure 17 (2008) 211-217
57. Ramirez-Amaya V., Marrone D.F., Gage F.H., Worley P.F., and Barnes C.A. Integration of new neurons into functional neural networks. J. Neurosci. 26 (2006) 12237-12241
58. Rao M.S., and Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Europ. J. Neurosci. 19 (2004) 234-246
59. Riedel G., Micheau J., Lam A.G.M., Roloff E.V.L., Martin S.J., Bridge H., de Hots L., Poeschel B., McCulloch J., and Morris R.G.M. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat. Neurosci. 2 (1999) 898-905
60. Rouguelle C., Glatt H., and Lalande M. The Angelman syndrome candidate gene, UBE3A/E6-AP is imprinted in brain. Nat. Genet. 17 (1997) 14-15
61. Roybon L., Hjalt T., Stott S., Guillemot F., Li J.Y., and Brundin P. Neurogenin2 directs granule neuroblast production and amplification while NeuroD1 specifies neuronal fate during hippocampal neurogenesis. Plos One 4 (2009) 4779-4806
62. Silva A.J., Stevens C.F., Tonegawa S., and Wang Y. Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257 (1992) 201-206
63. Silva A.J., Paylor R., Wehner J.M., and Tonegawa S. Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257 (1992) 206-211
64. Traub R.D., Middleton S.J., Knöpfel T., and Whittington M.A. Model of very fast ( > 75 Hz) network oscillations generated by electrical coupling between the proximal axons of cerebellar Purkinje cells. Eur. J. Neurosci. 28 (2008) 1603-1616
65. Trouche S., Bontempi B., Roullet P., and Rampon C. Recruitment of adult-generated neurons into functional hippocampal networks contributes to updating and strengthening of spatial of spatial memory. Proc. Natl. Acad. Sci. U S A. 106 (2009) 5919-5924
66. Van Woerden G.M., Harris K.D., Hojiati M.R., Gustin R.M., Qui S., de Avila Freire R., Jiang Y.H., Elgersma Y., and Weeber E.J. Rescue of neurological deficits in a mouse model for Angelman syndrome by reduction of alpha CaMKII inhibitory phosphorylation. Nat. Neurosci. 10 (2007) 280-282
67. Verret L., Jankowsky J.L., Xu G.M., Borchelt D.R., and Rampon C. Alzheimer's-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hippocampal neurogenesis. J. Neurosci. 27 (2007) 6771-6780
68. Weeber E.J., Jiang Y.H., Elgersma Y., Varga A.W., Carrasquillo Y., Brown S.E., Christian J.M., Mimikjoo B., Silva A., Beaudet A.L., and Sweatt J.D. Derangements of hippocampal calcium-calmodulin-dependent protein kinase II in a mouse model for Angelman mental retardation syndrome. J. Neurosci. 23 (2003) 2634-2644
69. Williams C.A. Neurological aspects of Angelman syndrome. Brain. Dev. 27 (2005) 88-94
70. Williams C.A., Beaudet A.L., Clayton-Smith J., Knoll J.H., Kyllerman M., Laan L.A., Magenis R.E., Moncla A., Schinzel A.A., Summers J.A., et al. Angelman syndrome 2005: update consensus for diagnostic criteria. Am. J. Med. Genet. 17 (2006) 75-78
71. Yamasaki K., Joh K., Phta T., Masazaki H., Ishimaru H., Mukai T., Niikawa N., Ogawa M., Wagstaff J., and Kishino T. Neurons but no glial cells show reciprocal imprinting of sense and antisense transcripts of Ube3a. Hum. Mol. Genet. 12 (2003) 837-847
72. Zhao C., Teng E.M., Summers Jr. R.G., Ming G.L., and Gage F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 26 (2006) 3-11