SUN1/2 and Syne/Nesprin-1/2 Complexes Connect Centrosome to the Nucleus during Neurogenesis and Neuronal Migration in Mice

Nuclear movement is critical during neurogenesis and neuronal migration, which are fundamental for mammalian brain development. Although dynein, Lis1, and other cytoplasmic proteins are known for their roles in connecting microtubules to the nucleus during interkinetic nuclear migration (INM) and nu...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2009-10, Vol.64 (2), p.173-187
Main Authors: Zhang, Xiaochang, Lei, Kai, Yuan, Xiaobing, Wu, Xiaohui, Zhuang, Yuan, Xu, Tian, Xu, Rener, Han, Min
Format: Article
Language:English
Subjects:
Animals
Behavior, Animal - physiology
Brain
Brain - cytology
Bromodeoxyuridine - metabolism
Cell adhesion & migration
Cell Movement - genetics
Cell Movement - physiology
Cell Nucleus - metabolism
Cell Proliferation
CELLBIO
Cells, Cultured
Centrosome - metabolism
Colleges & universities
Cytoskeletal Proteins
DEVBIO
Dyneins - metabolism
Electroporation - methods
Exploratory Behavior - physiology
Female
Membrane Proteins - deficiency
Membrane Proteins - metabolism
Mice
Mice, Inbred C57BL
Mice, Transgenic
Microtubule-Associated Proteins - deficiency
Microtubule-Associated Proteins - metabolism
Nerve Tissue Proteins - deficiency
Nerve Tissue Proteins - metabolism
Neurogenesis
Neurogenesis - genetics
Neurogenesis - physiology
Neurons
Neurons - cytology
Neurons - ultrastructure
Nuclear Proteins - deficiency
Nuclear Proteins - metabolism
Pregnancy
Protein Interaction Mapping - methods
Protein Structure, Tertiary - genetics
Protein Transport - physiology
Proteins
Telomere-Binding Proteins - deficiency
Telomere-Binding Proteins - metabolism
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Summary:Nuclear movement is critical during neurogenesis and neuronal migration, which are fundamental for mammalian brain development. Although dynein, Lis1, and other cytoplasmic proteins are known for their roles in connecting microtubules to the nucleus during interkinetic nuclear migration (INM) and nucleokinesis, the factors connecting dynein/Lis1 to the nuclear envelope (NE) remain to be determined. We report here that the SUN-domain proteins SUN1 and SUN2 and the KASH-domain proteins Syne-1/Nesprin-1 and Syne-2/Nesprin-2 play critical roles in neurogenesis and neuronal migration in mice. We show that SUN1 and SUN2 redundantly form complexes with Syne-2 to mediate the centrosome-nucleus coupling during both INM and radial neuronal migration in the cerebral cortex. Syne-2 is connected to the centrosome through interactions with both dynein/dynactin and kinesin complexes. Syne-2 mutants also display severe defects in learning and memory. These results fill an important gap in our understanding of the mechanism of nuclear movement during brain development.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2009.08.018