EFHC1 interacts with microtubules to regulate cell division and cortical development

Nature Neuroscience

Volumn 12, Issue 10, 2009, Pages 1266-1274

  De Nijs, Laurence ^a   Léon, Christine ^a   Nguyen, Laurent ^a   Loturco, Joseph J ^b   Delgado Escueta, Antonio V ^c   Grisar, Thierry ^a   Lakaye, Bernard ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; PROTEIN EFHC1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; LOCOMOTION; MICROTUBULE; MITOSIS SPINDLE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CALCIUM-BINDING PROTEINS; CELL DIVISION; CELL LINE, TRANSFORMED; CELL MOVEMENT; CEREBRAL CORTEX; ELECTROPORATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FEMALE; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOPRECIPITATION; IN SITU NICK-END LABELING; MICROTUBULES; MUTATION; NEUROGLIA; NEURONS; PREGNANCY; PROTEIN BINDING; RATS; RATS, WISTAR; RNA INTERFERENCE; TRANSFECTION;

EID: 70349554367     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2390     Document Type: Article

References (50)

1. Delgado-Escueta, A.V. et al. Mapping and positional cloning of common idiopathic generalized epilepsies: juvenile myoclonus epilepsy and childhood absence epilepsy. Adv. Neurol. 79, 351-374 (1999).
2. Delgado-Escueta, A.V. & Enrile-Bacsal, F. Juvenile myoclonic epilepsy of Janz. Neurology 34, 285-294 (1984).
3. Meencke, H.J. & Janz, D. Neuropathological fndings in primary generalized epilepsy: a study of eight cases. Epilepsia 25, 8-21 (1984).
4. Woermann, F.G., Free, S.L., Koepp, M.J., Sisodiya, S.M. & Duncan, J.S. Abnormal cerebral structure in juvenile myoclonic epilepsy demonstrated with voxel-based analysis of MRI. Brain 122, 2101-2108 (1999).
5. Delgado-Escueta, A.V. Advances in genetics of juvenile myoclonic epilepsies. Epilepsy Curr. 7, 61-67 (2007).
6. Cossette, P. et al. Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy. Nat. Genet. 31, 184-189 (2002).
7. Haug, K. et al. Mutations in CLCN2 encoding a voltage-gated chloride channel are associated with idiopathic generalized epilepsies. Nat. Genet. 33, 527-532 (2003).
8. Suzuki, T. et al. Mutations in EFHC1 cause juvenile myoclonic epilepsy. Nat. Genet. 36, 842-849 (2004).
9. Annesi, F. et al. Mutational analysis of EFHC1 gene in Italian families with juvenile myoclonic epilepsy. Epilepsia 48, 1686-1690 (2007).
10. Ma, S. et al. Mutations in the GABRA1 and EFHC1 genes are rare in familial juvenile myoclonic epilepsy. Epilepsy Res. 71, 129-134 (2006).
11. Stogmann, E. et al. Idiopathic generalized epilepsy phenotypes associated with different EFHC1 mutations. Neurology 67, 2029-2031 (2006). (Pubitemid 44967383)
12. Medina, M.T. et al. Novel mutations in Myoclonin1/EFHC1 in sporadic and familial juvenile myoclonic epilepsy. Neurology 70, 2137-2144 (2008).
13. Ikeda, T. et al. The mouse ortholog of EFHC1 implicated in juvenile myoclonic epilepsy is an axonemal protein widely conserved among organisms with motile cilia and fagella. FEBS Lett. 579, 819-822 (2005).
14. Suzuki, T. et al. Sequential expression of Efhc1/myoclonin1 in choroid plexus and ependymal cell cilia. Biochem. Biophys. Res. Commun. 367, 226-233 (2008).
15. King, S.M. Axonemal protoflament ribbons, DM10 domains and the link to juvenile myoclonic epilepsy. Cell Motil. Cytoskeleton 63, 245-253 (2006).
16. de Nijs, L. et al. EFHC1, a protein mutated in juvenile myoclonic epilepsy, associates with the mitotic spindle through its N-terminus. Exp. Cell Res. 312, 2872-2879 (2006).
17. Grisar, T. et al. Some genetic and biochemical aspects of myoclonus. Neurophysiol. Clin. 36, 271-279 (2006).
18. Gupta, A., Tsai, L.H. & Wynshaw-Boris, A. Life is a journey: a genetic look at neocortical development. Nat. Rev. Genet. 3, 342-355 (2002).
19. LoTurco, J.J. & Bai, J. The multipolar stage and disruptions in neuronal migration. Trends Neurosci. 29, 407-413 (2006).
20. Shu, T. et al. Doublecortin-like kinase controls neurogenesis by regulating mitotic spindles and M phase progression. Neuron 49, 25-39 (2006).
21. Nadarajah, B. & Parnavelas, J.G. Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci. 3, 423-432 (2002). (Pubitemid 135711798)
22. Hand, R. et al. Phosphorylation of Neurogenin2 specifes the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48, 45-62 (2005).
23. Heng, J.I. et al. Neurogenin 2 controls cortical neuron migration through regulation of Rnd2. Nature 455, 114-118 (2008).
24. Saffn, J.M. et al. ASAP, a human microtubule-associated protein required for bipolar spindle assembly and cytokinesis. Proc. Natl. Acad. Sci. USA 102, 11302-11307 (2005).
25. Aonuma, M. et al. Microtubule bundle formation and cell death induced by the human CLASP/Orbit N-terminal fragment. Cell Struct. Funct. 30, 7-13 (2005).
26. Martínez-López, M.J. et al. Mouse neuron navigator 1, a novel microtubule-associated protein involved in neuronal migration. Mol. Cell. Neurosci. 28, 599-612 (2005).
27. Faulkner, N.E. et al. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol. 2, 784-791 (2000).
28. Wakefeld, J.G., Stephens, D.J. & Tavare, J.M. A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. J. Cell Sci. 116, 637-646 (2003).
29. Ohnuma, S. & Harris, W.A. Neurogenesis and the cell cycle. Neuron 40, 199-208 (2003).
30. Noctor, S.C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specifc phases. Nat. Neurosci. 7, 136-144 (2004).
31. Feng, Y. & Walsh, C.A. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44, 279-293 (2004).
32. Pontious, A., Kowalczyk, T., Englund, C. & Hevner, R.F. Role of intermediate progenitor cells in cerebral cortex development. Dev. Neurosci. 30, 24-32 (2008).
33. Kowalczyk, T. et al. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex published online, doi:10.1093/cercor/bhn260 (23 January 2009).
34. Roegiers, F. & Jan, Y.N. Asymmetric cell division. Curr. Opin. Cell Biol. 16, 195-205 (2004).
35. Yamashita, Y.M., Jones, D.L. & Fuller, M.T. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 301, 1547-1550 (2003).
36. Noctor, S.C., Flint, A.C., Weissman, T.A., Dammerman, R.S. & Kriegstein, A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714-720 (2001).
37. Rakic, P. Mode of cell migration to the superfcial layers of fetal monkey neocortex. J. Comp. Neurol. 145, 61-83 (1972).
38. Halfter, W., Dong, S., Yip, Y.P., Willem, M. & Mayer, U. A critical function of the pial basement membrane in cortical histogenesis. J. Neurosci. 22, 6029-6040 (2002).
39. Hartfuss, E. et al. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130, 4597-4609 (2003).
40. Tanaka, T. et al. Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell Biol. 165, 709-721 (2004).
41. Tsai, L.H. & Gleeson, J.G. Nucleokinesis in neuronal migration. Neuron 46, 383-388 (2005).
42. Yingling, J. et al. Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132, 474-486 (2008).
43. Tsai, J.W., Chen, Y., Kriegstein, A.R. & Vallee, R.B. LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J. Cell Biol. 170, 935-945 (2005).
44. Shu, T. et al. Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron 44, 263-277 (2004).
45. Suzuki, T. et al. Efhc1 defciency causes spontaneous myoclonus and increased seizure susceptibility. Hum. Mol. Genet. 18, 1099-1109 (2009).
46. Corbo, J.C. et al. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J. Neurosci. 22, 7548-7557 (2002).
47. Bai, J. et al. RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat. Neurosci. 6, 1277-1283 (2003).
48. Ramos, R.L., Bai, J. & LoTurco, J.J. Heterotopia formation in rat, but not mouse, neocortex after RNA interference knockdown of DCX. Cereb. Cortex 16, 1323-1331 (2006).
49. Young-Pearse, T.L. et al. A critical function for beta-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. J. Neurosci. 27, 14459-14469 (2007).
50. Nguyen, L. et al. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 20, 1511-1524 (2006).doi:10.1038/ nn.2390doi:10.1038/nn.2390