Aberrant differentiation of glutamatergic cells in neocortex of mouse model for fragile X syndrome

Neurobiology of Disease

Volumn 33, Issue 2, 2009, Pages 250-259

  Tervonen, Topi A ^a   Louhivuori, Verna ^a   Sun, Xiaohong ^a,b   Hokkanen, Marie Estelle ^a   Kratochwil, Claudius F ^a   Zebryk, Pawel ^a,c   Castrén, Eero ^a   Castrén, Maija L ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b CHINA MEDICAL UNIVERSITY   (China)

^c POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

Author keywords

Brain development; BrdU; Differentiation; Fmr1 knockout; Glutamatergic; In utero electroporation; Neural progenitor cell; Tbr1; Tbr2

Indexed keywords

BIOLOGICAL MARKER; FRAGILE X MENTAL RETARDATION PROTEIN; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO CELL; EMBRYO DEVELOPMENT; FEMALE; FRAGILE X SYNDROME; GENE MUTATION; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MITOSIS; MOUSE; NEOCORTEX; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBVENTRICULAR ZONE;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL LINEAGE; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; EXCITATORY AMINO ACID TRANSPORTER 1; FATTY ACID-BINDING PROTEINS; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GLUTAMIC ACID; MESENCHYMAL STEM CELLS; MICE; MICE, KNOCKOUT; MUTATION; NEOCORTEX; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; PYRAMIDAL CELLS; STEM CELLS; T-BOX DOMAIN PROTEINS;

EID: 58149488779     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2008.10.010     Document Type: Article

References (54)

1. Adinolfi S., Ramos A., Martin S.R., Dal Piaz F., Pucci P., Bardoni B., Mandel J.L., and Pastore A. The N-terminus of the fragile X mental retardation protein contains a novel domain involved in dimerization and RNA binding. Biochemistry 42 (2003) 10437-10444
2. Baala L., Briault S., Etchevers H.C., Laumonnier F., Natiq A., Amiel J., Boddaert N., Picard C., Sbiti A., Asermouh A., Attié-Bitach T., Encha-Razavi F., Munnich A., Sefiani A., and Lyonnet S. Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis. Nat. Genet. 39 (2007) 454-456
3. Bagni C., and Greenough W.T. From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome. Nat. Rev. Neurosci. 6 (2005) 376-387
4. Bhattacharyya A., McMillan E., Wallace K., Tubon Jr. T.C., Capowski E.E., and Svendsen C.N. Normal neurogenesis but abnormal gene expression in human fragile X cortical progenitor cells. Stem Cells Dev 17 (2008) 107-117
5. Brown V., Jin P., Ceman S., Darnell J.C., O'Donnell W.T., Tenenbaum S.A., Jin X., Feng Y., Wilkinson K.D., Keene J.D., Darnell R.B., and Warren S.T. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107 (2001) 477-487
6. Bulfone A., Smiga S.M., Shimamura K., Peterson A., Puelles L., and Rubenstein J.L. T-brain-1: a homolog of brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15 (1995) 63-78
7. Bulfone A., Martinez S., Marigo V., Campanella M., Basile A., Quaderi N., Gattuso C., Rubenstein J.L., and Ballabio A. Expression pattern of the Tbr2 (eomesodermin) gene during mouse and chick brain development. Mech. Dev. 84 (1999) 133-138
8. Castrén M. Differentiation of neuronal cells in fragile X syndrome. Cell Cycle 5 (2006) 1528-1530
9. Castrén M., Tervonen T., Kärkkäinen V., Heinonen S., Castrén E., Larsson K., Bakker C.E., Oostra B.A., and Åkerman K. Altered differentiation of neural stem cells in fragile X syndrome. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17834-17839
10. Castrén M., Haapasalo A., Oostra B.A., and Castrén E. Subcellular localization of fragile X mental retardation protein with the I304N mutation in the RNA-binding domain in cultured hippocampal neurons. Cell. Mol. Neurobiol. 21 (2001) 29-38
11. Comery T.A., Harris J.B., Willems P.J., Oostra B.A., Irwin S.A., Weiler I.J., and Greenough W.T. Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 5401-5404
12. Darnell J.C., Fraser C.E., Mostovetsky O., Stefani G., Jones T.A., Eddy S.R., and Darnell R.B. Kissing complex RNAs mediate interaction between the fragile-X mental retardation protein KH2 domain and brain polyribosomes. Genes Dev. 19 (2005) 903-918
13. Darnell J.C., Mostovetsky O., and Darnell R.B. FMRP RNA targets: identification and validation. Genes Brain Behav. 4 (2005) 341-349
14. De Boulle K., Verkerk A.J., Reyniers E., Vits L., Hendrickx J., Van Roy B., Van den Bos F., de Graaff E., Oostra B.A., and Willems P.J. A point mutation in the FMR-1 gene associated with fragile X mental retardation. Nat. Genet. 3 (1993) 31-35
15. de Launoit Y., Baert J.L., Chotteau A., Monte D., Defossez P.A., Coutte L., Pelczar H., and Leenders F. Structure-function relationships of the PEA3 group of ets-related transcription factors. Biochem. Mol. Med. 61 (1997) 127-135
16. D'Hooge R., Nagels G., Franck F., Bakker C.E., Reyniers E., Storm K., Kooy R.F., Oostra B.A., Willems P.J., and De Deyn P.P. Mildly impaired water maze performance in male Fmr1 knockout mice. Neuroscience 76 (1997) 367-376
17. The Dutch-Belgian Fragile X Consortium. Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 78 (1994) 23-33
18. Englund C., Fink A., Lau C., Pham D., Daza R.A., Bulfone A., Kowalczyk T., and Hevner R.F. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25 (2005) 247-251
19. Feng Y., Absher D., Eberhart D.E., Brown V., Malter H.E., and Warren S.T. FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell 1 (1997) 109-118
20. Fukumitsu H., Ohtsuka M., Murai R., Nakamura H., Itoh K., and Furukawa S. Brain-derived neurotrophic factor participates in determination of neuronal laminar fate in the developing mouse cerebral cortex. J. Neurosci. 26 (2006) 13218-13230
21. Galvez R., and Greenough W.T. Sequence of abnormal dendritic spine development in primary somatosensory cortex of a mouse model of the fragile X mental retardation syndrome. Am. J. Med. Genet. A. 135 (2005) 155-160
22. Götz M., and Huttner W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6 (2005) 777-788
23. Hartfuss E., Galli R., Heins N., and Götz M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229 (2001) 15-30
24. Hevner R.F., Shi L., Justice N., Hsueh Y., Sheng M., Smiga S., Bulfone A., Goffinet A.M., Campagnoni A.T., and Rubenstein J.L. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29 (2001) 353-366
25. Hevner R.F., Hodge R.D., Daza R.A., and Englund C. Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci. Res. 55 (2006) 223-233
26. Hienola A., Pekkanen M., Raulo E., Vanttola P., and Rauvala H. HB-GAM inhibits proliferation and enhances differentiation of neural stem cells. Mol. Cell. Neurosci. 26 1 (2004) 75-88
27. Irwin S.A., Patel B., Idupulapati M., Harris J.B., Crisostomo R.A., Larsen B.P., Kooy F., Willems P.J., Cras P., Kozlowski P.B., Swain R.A., Weiler I.J., and Greenough W.T. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am. J. Med. Genet. 98 (2001) 161-167
28. Jacobowitz D.M., and Abbott L.C. Chemoarchitectonic Atlas of the Developing Mouse Brain (1998), CRC Press LLC, Boca Raton, USA
29. Kaufmann W.E., Cohen S., Sun H., and Ho G. Molecular phenotype of fragile X syndrome: FMRP, FXRPs, and protein targets. Microscopy Res. Technique 57 (2002) 135-144
30. Kimura N., Nakashima K., Ueno M., Kiyama H., and Taga T. A novel mammalian T-box-containing gene, Tbr2, expressed in mouse developing brain. Brain Res. Dev. Brain Res. 115 (1999) 183-193
31. Kwon G.S., and Hadjantonakis A.K. Eomes: GFP-a tool for live imaging cells of the trophoblast, primitive streak, and telencephalon in the mouse embryo. Genesis 45 (2007) 208-217
32. Laggerbauer B., Ostareck D., Keidel E.M., Ostareck-Lederer A., and Fischer U. Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum. Mol. Genet. 10 (2001) 329-338
33. Miyashiro K.Y., Beckel-Mitchener A., Purk T.P., Becker K.G., Barret T., Liu L., Carbonetto S., Weiler I.J., Greenough W.T., and Eberwine J. RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron 37 (2003) 417-431
34. Molyneaux B.J., Arlotta P., Menezes J.R., and Macklis J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8 (2007) 427-437
35. Nimchinsky E.A., Oberlander A.M., and Svoboda K. Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci. 21 (2001) 5139-5146
36. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., and Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409 (2001) 714-720
37. Noctor S.C., Martinez-Cerdeno V., Ivic L., and Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7 (2004) 136-144
38. Pacey L.K.K., and Doering L.C. Developmental expression of FMRP in the astrocyte lineage: implications for fragile X syndrome. Glia 55 (2007) 1601-1609
39. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates (2001), Academic Press, San Diego, USA
40. Penagarikano O., Mulle J.G., and Warren S.T. The pathophysiology of fragile X syndrome. Annu. Rev. Genomics Hum. Genet. 8 (2007) 109-129
41. Pfeiffer B.E., and Huber K.M. Fragile X mental retardation protein induces synapse loss through acute postsynaptic translational regulation. J. Neurosci. 27 (2007) 3120-3130
42. Rifé M., Nadal A., Milà M., and Willemsen R. Immunohistochemical FMRP studies in a full mutated female fetus. Am. J. Med. Genet. A (2004)
43. Schaeffer C., Bardoni B., Mandel J.L., Ehresmann B., Ehresmann C., and Moine H. The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J. 20 (2001) 4803-4813
44. Schrier M., Severijnen L.A., Reis S., Rife M., van't Padje S., van Cappellen G., Oostra B.A., and Willemsen R. Transport kinetics of FMRP containing the I304N mutation of severe fragile X syndrome in neurites of living rat PC12 cells. Exp. Neurol. 189 (2004) 343-353
45. Schwartz P.H., Bryant P.J., Fuja T.J., Su H., O'Dowd D.K., and Klassen H. Isolation and characterization of neural progenitor cells from post-mortem human cortex. J. Neurosci. Res. 15;74 6 (2003) 838-851
46. Selby L., Zhang C., and Sun Q.Q. Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein. Neurosci. Lett. 412 (2007) 227-232
47. Tabata H., and Nakajima K. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103 (2001) 865-872
48. Tamanini F., Willemsen R., van Unen L., Bontekoe C., Galjaard H., Oostra B.A., and Hoogeveen A.T. Differential expression of FMR1, FXR1 and FXR2 proteins in human brain and testis. Hum. Mol. Genet. 6 8 (1997) 1315-1322
49. Tuoc T.C., and Stoykova A. Er81 is a downstream target of Pax6 in cortical progenitors. BMC Dev. Biol. 28;8 (2008) 23
50. Van Dam D., D'Hooge R., Hauben E., Reyniers E., Gantois I., Bakker C.E., Oostra B.A., Kooy R.F., and De Deyn P.P. Spatial learning, contextual fear conditioning and conditioned emotional response in Fmr1 knockout mice. Behav. Brain Res. 117 (2000) 127-136
51. Wang H., Ku L., Osterhout D.J., Li W., and Feng Y. Developmentally-programmed FMRP expression in oligodendrocytes: a potential role of FMRP in regulating translation in oligodendroglia progenitors. Hum. Mol. Genet. 13 (2004) 79-89
52. Wang H., Dictenberg J.B., Ku L., Li W., Bassell G.J., and Feng Y. Dynamic association of the fragile X mental retardation protein as a messenger ribonucleoprotein between microtubules and polyribosomes. Mol. Biol. Cell 19 (2008) 105-114
53. Yoneshima H., Yamasaki S., Voelker C.C., Molnar Z., Christophe E., Audinat E., Takemoto M., Nishiwaki M., Tsuji S., Fujita I., and Yamamoto N. Er81 is expressed in a subpopulation of layer 5 neurons in rodent and primate neocortices. Neuroscience 137 (2006) 401-412
54. Zalfa F., Eleuteri B., Dickson K.S., Mercaldo V., De Rubeis S., di Penta A., Tabolacci E., Chiurazzi P., Neri G., Grant S.G., and Bagni C. A new function for the fragile X mental retardation protein in regulation of PSD-95 mRNA stability. Nat. Neurosci. 10 (2007) 578-587