Tangential migration of neuronal precursors of glutamatergic neurons in the adult mammalian brain

In a classic model of mammalian brain formation, precursors of principal glutamatergic neurons migrate radially along radial glia fibers whereas GABAergic interneuron precursors migrate tangentially. These migration modes have significant implications for brain function. Here we used clonal lineage...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 112; no. 30; pp. 9484 - 9489
Main Authors Sun, Gerald J., Zhou, Yi, Stadel, Ryan P., Moss, Jonathan, Yong, Jing Hui A., Ito, Shiori, Kawasaki, Nicholas K., Phan, Alexander T., Oh, Justin H., Modak, Nikhil, Reed, Randall R., Toni, Nicolas, Song, Hongjun, Ming, Guo-li
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 28.07.2015
National Acad Sciences
Subjects
Adults
Animals
Biological Sciences
Brain
Brain - metabolism
Brain Mapping - methods
Cell Movement
Dentate Gyrus - physiology
Female
Genetics
Glutamine - chemistry
Green Fluorescent Proteins - metabolism
Hippocampus - physiology
Imaging, Three-Dimensional
Mammals
Mice
Mice, Inbred C57BL
Mice, Transgenic
Microscopy, Confocal
Microscopy, Fluorescence
Models, Neurological
Morphology
Neural Stem Cells - cytology
Neurogenesis - physiology
Neurons
Neurons - cytology
Neurons - physiology
migration
adult neurogenesis
vascular niche
lineage tracing
hippocampus
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Summary:In a classic model of mammalian brain formation, precursors of principal glutamatergic neurons migrate radially along radial glia fibers whereas GABAergic interneuron precursors migrate tangentially. These migration modes have significant implications for brain function. Here we used clonal lineage tracing of active radial glia-like neural stem cells in the adult mouse dentate gyrus and made the surprising discovery that proliferating neuronal precursors of glutamatergic granule neurons exhibit significant tangential migration along blood vessels, followed by limited radial migration. Genetic birthdating and morphological and molecular analyses pinpointed the neuroblast stage as the main developmental window when tangential migration occurs.We also developed a partial “wholemount” dentate gyrus preparation and observed a dense plexus of capillaries, with which only neuroblasts, among the entire population of progenitors, are directly associated. Together, these results provide insight into neuronal migration in the adult mammalian nervous system.
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Edited by Fred H. Gage, Salk Institute for Biological Studies, San Diego, CA, and approved June 23, 2015 (received for review May 2, 2015)
Author contributions: G.J.S., Y.Z., H.S., and G.-l.M. designed research; G.J.S., Y.Z., R.P.S., J.M., J.H.A.Y., S.I., N.K.K., A.T.P., J.H.O., N.M., and N.T. performed research; R.R.R. contributed new reagents/analytic tools; G.J.S., Y.Z., J.M., J.H.A.Y., S.I., N.K.K., A.T.P., J.H.O., N.M., and N.T. analyzed data; and G.J.S., Y.Z., H.S., and G.-l.M. wrote the paper.
1G.J.S., Y.Z., and R.P.S. contributed equally to this work.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1508545112