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Cover ArticleResearch Articles, Development/Plasticity/Repair

Dynamic Changes in Ultrastructure of the Primary Cilium in Migrating Neuroblasts in the Postnatal Brain

Mami Matsumoto, Masato Sawada, Diego García-González, Vicente Herranz-Pérez, Takashi Ogino, Huy Bang Nguyen, Truc Quynh Thai, Keishi Narita, Natsuko Kumamoto, Shinya Ugawa, Yumiko Saito, Sen Takeda, Naoko Kaneko, Konstantin Khodosevich, Hannah Monyer, José Manuel García-Verdugo, Nobuhiko Ohno and Kazunobu Sawamoto
Journal of Neuroscience 11 December 2019, 39 (50) 9967-9988; DOI: https://doi.org/10.1523/JNEUROSCI.1503-19.2019
Mami Matsumoto
1Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
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Masato Sawada
1Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
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Diego García-González
2Department of Clinical Neurobiology, Medical Faculty of Heidelberg University and German Cancer Research Center, 69120 Heidelberg, Germany,
3Biotech Research & Innovation Centre, University of Copenhagen, 2200 Copenhagen, Denmark,
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Vicente Herranz-Pérez
4Laboratory of Comparative Neurobiology, Cavanilles Institute, University of Valencia, CIBERNED, 46980, Valencia, Spain,
5Predepartamental Unit of Medicine, Faculty of Health Sciences, Universitat Jaume I, 12071 Castelló de la Plana, Spain,
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Takashi Ogino
1Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
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Huy Bang Nguyen
6Division of Neurobiology and Bioinformatics, National Institute for Physiological Sciences, Okazaki 444-8787, Japan,
7Department of Anatomy, Faculty of Medicine, University of Medicine and Pharmacy at Ho Chi Minh City, Ho Chi Minh City 70000, Vietnam,
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Truc Quynh Thai
6Division of Neurobiology and Bioinformatics, National Institute for Physiological Sciences, Okazaki 444-8787, Japan,
8Department of Histology-Embryology-Genetics, Faculty of Basic Medical Sciences, Pham Ngoc Thach University of Medicine, Ho Chi Minh City 70000, Vietnam,
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Keishi Narita
9Department of Anatomy and Cell Biology, Faculty of Medicine, University of Yamanashi, Chuo 409-3898, Japan,
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Natsuko Kumamoto
10Department of Anatomy and Neuroscience, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
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Shinya Ugawa
10Department of Anatomy and Neuroscience, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
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Yumiko Saito
11Graduate School of Integrated Sciences for Life, Hiroshima University, Hiroshima 739-8521, Japan,
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Sen Takeda
9Department of Anatomy and Cell Biology, Faculty of Medicine, University of Yamanashi, Chuo 409-3898, Japan,
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Naoko Kaneko
1Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
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Konstantin Khodosevich
3Biotech Research & Innovation Centre, University of Copenhagen, 2200 Copenhagen, Denmark,
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Hannah Monyer
2Department of Clinical Neurobiology, Medical Faculty of Heidelberg University and German Cancer Research Center, 69120 Heidelberg, Germany,
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José Manuel García-Verdugo
4Laboratory of Comparative Neurobiology, Cavanilles Institute, University of Valencia, CIBERNED, 46980, Valencia, Spain,
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Nobuhiko Ohno
6Division of Neurobiology and Bioinformatics, National Institute for Physiological Sciences, Okazaki 444-8787, Japan,
12Department of Anatomy, Division of Histology and Cell Biology, Jichi Medical University, School of Medicine, Shimotsuke 329-0498, Japan, and
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Kazunobu Sawamoto
1Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
13Division of Neural Development and Regeneration, National Institute for Physiological Sciences, Okazaki 444-8585, Japan
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Article Information

DOI 
https://doi.org/10.1523/JNEUROSCI.1503-19.2019
PubMed 
31685650
Published By 
Society for Neuroscience
History 
  • Received June 16, 2019
  • Revision received October 8, 2019
  • Accepted October 24, 2019
  • First published November 4, 2019.
  • Version of record published December 11, 2019.
Copyright & Usage 
Copyright © 2019 the authors

Author Information

  1. Mami Matsumoto1,*,
  2. Masato Sawada1,*,
  3. Diego García-González2,3,
  4. Vicente Herranz-Pérez4,5,
  5. Takashi Ogino1,
  6. Huy Bang Nguyen6,7,
  7. Truc Quynh Thai6,8,
  8. Keishi Narita9,
  9. Natsuko Kumamoto10,
  10. Shinya Ugawa10,
  11. Yumiko Saito11,
  12. Sen Takeda9,
  13. Naoko Kaneko1,
  14. Konstantin Khodosevich3,
  15. Hannah Monyer2,
  16. José Manuel García-Verdugo4,
  17. Nobuhiko Ohno6,12, and
  18. Kazunobu Sawamoto1,13
  1. 1Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
  2. 2Department of Clinical Neurobiology, Medical Faculty of Heidelberg University and German Cancer Research Center, 69120 Heidelberg, Germany,
  3. 3Biotech Research & Innovation Centre, University of Copenhagen, 2200 Copenhagen, Denmark,
  4. 4Laboratory of Comparative Neurobiology, Cavanilles Institute, University of Valencia, CIBERNED, 46980, Valencia, Spain,
  5. 5Predepartamental Unit of Medicine, Faculty of Health Sciences, Universitat Jaume I, 12071 Castelló de la Plana, Spain,
  6. 6Division of Neurobiology and Bioinformatics, National Institute for Physiological Sciences, Okazaki 444-8787, Japan,
  7. 7Department of Anatomy, Faculty of Medicine, University of Medicine and Pharmacy at Ho Chi Minh City, Ho Chi Minh City 70000, Vietnam,
  8. 8Department of Histology-Embryology-Genetics, Faculty of Basic Medical Sciences, Pham Ngoc Thach University of Medicine, Ho Chi Minh City 70000, Vietnam,
  9. 9Department of Anatomy and Cell Biology, Faculty of Medicine, University of Yamanashi, Chuo 409-3898, Japan,
  10. 10Department of Anatomy and Neuroscience, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan,
  11. 11Graduate School of Integrated Sciences for Life, Hiroshima University, Hiroshima 739-8521, Japan,
  12. 12Department of Anatomy, Division of Histology and Cell Biology, Jichi Medical University, School of Medicine, Shimotsuke 329-0498, Japan, and
  13. 13Division of Neural Development and Regeneration, National Institute for Physiological Sciences, Okazaki 444-8585, Japan
View Full Text

Author contributions

  1. Author contributions: M.M., M.S., D.G.-G., V.H.-P., K.N., N. Kumamoto, S.U., Y.S., S.T., N. Kaneko, K.K., H.M., J.M.G.-V., N.O., and K.S. designed research; M.M., M.S., D.G.-G., V.H.-P., T.O., H.B.N., T.Q.T., K.K., and N.O. performed research; M.M., D.G.-G., V.H.-P., T.O., N. Kaneko, H.M., J.M.G.-V., N.O., and K.S. analyzed data; M.M., M.S., D.G.-G., K.K., and K.S. wrote the paper; K.N., N. Kumamoto, S.U., Y.S., and S.T. contributed unpublished reagents/analytic tools.

  2. ↵*M.M. and M.S. contributed equally to this work.

Disclosures

    • Received June 16, 2019.
    • Revision received October 8, 2019.
    • Accepted October 24, 2019.
  • This work was supported by Japan Agency for Medical Research and Development Research Grants JP19bm0704033 to K.S., JP19gm1210007 to K.S., and JP19jm0210060 to M.S., N. Kaneko, and K.S.; Japan Society for the Promotion of Science KAKENHI 26250019, 15H01384, 15H01217, 16H06280, 17H01392, 17H05512, 17H05750, 19H04757, 19H04785, and 18KK0213 to K.S., 26830014 and 18K14823 to M.S., and 16J00373 to M.M.; Japan Society for the Promotion of Science Program for Advancing Strategic International Networks to Accelerate the Circulation of Talented Researchers S2704 to M.S., V.H-P., N. Kaneko, J.M.G-V., and K.S.; Bilateral Open Partnership Joint Research Projects to K.S.; Grant-in-Aid for Research at Nagoya City University to K.S.; Cooperative Study Programs of National Institute for Physiological Sciences to K.S.; the Mitsubishi Foundation to K.S.; the Canon Foundation to K.S.; the Takeda Science Foundation to K.S. and M.S.; Spanish Ministry of Science, Innovation and Universities PCI2018-093062 to V.H-P. and J.M.G-V.; and Independent Research Fund Denmark 8020-00083B to K.K. M.M. was supported by a Japan Society for the Promotion of Science Fellowship. We thank Joseph G. Gleeson, Masahiro Yamaguchi, Hiroyuki Miyoshi, Joshua J. Breunig, Kozo Kaibuchi, Tatsunori Seki, and Shaoyu Ge for materials; Hisashi Oishi, Hiroshi Takase, Mikio Furuse, Shigeyuki Magi, and Kagayaki Kato for technical support; and Yoichi Kato, Yusuke Hirabayashi, and Sawamoto laboratory members for discussions.

  • The authors declare no competing financial interests.

  • Correspondence should be addressed to Kazunobu Sawamoto at sawamoto{at}med.nagoya-cu.ac.jp

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Dynamic Changes in Ultrastructure of the Primary Cilium in Migrating Neuroblasts in the Postnatal Brain
Mami Matsumoto, Masato Sawada, Diego García-González, Vicente Herranz-Pérez, Takashi Ogino, Huy Bang Nguyen, Truc Quynh Thai, Keishi Narita, Natsuko Kumamoto, Shinya Ugawa, Yumiko Saito, Sen Takeda, Naoko Kaneko, Konstantin Khodosevich, Hannah Monyer, José Manuel García-Verdugo, Nobuhiko Ohno, Kazunobu Sawamoto
Journal of Neuroscience 11 December 2019, 39 (50) 9967-9988; DOI: 10.1523/JNEUROSCI.1503-19.2019

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Dynamic Changes in Ultrastructure of the Primary Cilium in Migrating Neuroblasts in the Postnatal Brain
Mami Matsumoto, Masato Sawada, Diego García-González, Vicente Herranz-Pérez, Takashi Ogino, Huy Bang Nguyen, Truc Quynh Thai, Keishi Narita, Natsuko Kumamoto, Shinya Ugawa, Yumiko Saito, Sen Takeda, Naoko Kaneko, Konstantin Khodosevich, Hannah Monyer, José Manuel García-Verdugo, Nobuhiko Ohno, Kazunobu Sawamoto
Journal of Neuroscience 11 December 2019, 39 (50) 9967-9988; DOI: 10.1523/JNEUROSCI.1503-19.2019
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Keywords

  • electron microscopy
  • live imaging
  • neuronal migration
  • olfactory bulb
  • primary cilium
  • rostral migratory stream

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