TY - JOUR
T1 - Dynamic changes in ultrastructure of the primary cilium in migrating neuroblasts in the postnatal brain
AU - Matsumoto, Mami
AU - Sawada, Masato
AU - García-González, Diego
AU - Herranz-Pérez, Vicente
AU - Ogino, Takashi
AU - Nguyen, Huy Bang
AU - Thai, Truc Quynh
AU - Narita, Keishi
AU - Kumamoto, Natsuko
AU - Ugawa, Shinya
AU - Saito, Yumiko
AU - Takeda, Sen
AU - Kaneko, Naoko
AU - Khodosevich, Konstantin
AU - Monyer, Hannah
AU - García-Verdugo, José Manuel
AU - Ohno, Nobuhiko
AU - Sawamoto, Kazunobu
N1 - Publisher Copyright:
Copyright © 2019 the authors
PY - 2019/12/11
Y1 - 2019/12/11
N2 - New neurons, referred to as neuroblasts, are continuously generated in the ventricular-subventricular zone of the brain throughout an animal’s life. These neuroblasts are characterized by their unique potential for proliferation, formation of chain-like cell aggregates, and long-distance and high-speed migration through the rostral migratory stream (RMS) toward the olfactory bulb (OB), where they decelerate and differentiate into mature interneurons. The dynamic changes of ultrastructural features in postnatal-born neuroblasts during migration are not yet fully understood. Here we report the presence of a primary cilium, and its ultrastructural morphology and spatiotemporal dynamics, in migrating neuroblasts in the postnatal RMS and OB. The primary cilium was observed in migrating neuroblasts in the postnatal RMS and OB in male and female mice and zebrafish, and a male rhesus monkey. Inhibition of intraflagellar transport molecules in migrating neuroblasts impaired their ciliogenesis and rostral migration toward the OB. Serial section transmission electron microscopy revealed that each migrating neuroblast possesses either a pair of centrioles or a basal body with an immature or mature primary cilium. Using immunohistochemistry, live imaging, and serial block-face scanning electron microscopy, we demonstrate that the localization and orientation of the primary cilium are altered depending on the mitotic state, saltatory migration, and deceleration of neuroblasts. Together, our results highlight a close mutual relationship between spatiotemporal regulation of the primary cilium and efficient chain migration of neuroblasts in the postnatal brain.
AB - New neurons, referred to as neuroblasts, are continuously generated in the ventricular-subventricular zone of the brain throughout an animal’s life. These neuroblasts are characterized by their unique potential for proliferation, formation of chain-like cell aggregates, and long-distance and high-speed migration through the rostral migratory stream (RMS) toward the olfactory bulb (OB), where they decelerate and differentiate into mature interneurons. The dynamic changes of ultrastructural features in postnatal-born neuroblasts during migration are not yet fully understood. Here we report the presence of a primary cilium, and its ultrastructural morphology and spatiotemporal dynamics, in migrating neuroblasts in the postnatal RMS and OB. The primary cilium was observed in migrating neuroblasts in the postnatal RMS and OB in male and female mice and zebrafish, and a male rhesus monkey. Inhibition of intraflagellar transport molecules in migrating neuroblasts impaired their ciliogenesis and rostral migration toward the OB. Serial section transmission electron microscopy revealed that each migrating neuroblast possesses either a pair of centrioles or a basal body with an immature or mature primary cilium. Using immunohistochemistry, live imaging, and serial block-face scanning electron microscopy, we demonstrate that the localization and orientation of the primary cilium are altered depending on the mitotic state, saltatory migration, and deceleration of neuroblasts. Together, our results highlight a close mutual relationship between spatiotemporal regulation of the primary cilium and efficient chain migration of neuroblasts in the postnatal brain.
KW - Electron microscopy
KW - Live imaging
KW - Neuronal migration
KW - Olfactory bulb
KW - Primary cilium
KW - Rostral migratory stream
UR - https://www.scopus.com/pages/publications/85076448264
UR - https://www.scopus.com/pages/publications/85076448264#tab=citedBy
U2 - 10.1523/JNEUROSCI.1503-19.2019
DO - 10.1523/JNEUROSCI.1503-19.2019
M3 - Article
C2 - 31685650
AN - SCOPUS:85076448264
SN - 0270-6474
VL - 39
SP - 9967
EP - 9988
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 50
ER -