TAG-1-assisted progenitor elongation streamlines nuclear migration to optimize subapical crowding

Nature Neuroscience

Volumn 16, Issue 11, 2013, Pages 1556-1566

  Okamoto, Mayumi ^a   Namba, Takashi ^a   Shinoda, Tomoyasu ^a   Kondo, Takefumi ^b   Watanabe, Tadashi ^c   Inoue, Yasuhiro ^c   Takeuchi, Kosei ^d,e   Enomoto, Yukiko ^a   Ota, Kumiko ^a   Oda, Kanako ^d,f   Wada, Yoshino ^d   Sagou, Ken ^a   Saito, Kanako ^a   Sakakibara, Akira ^a   Kawaguchi, Ayano ^a   Nakajima, Kazunori ^g   Adachi, Taiji ^c   Fujimori, Toshihiko ^h   Ueda, Masahiro ^i,j,k   Hayashi, Shigeo ^b   Kaibuchi, Kozo ^a   Miyata, Takaki ^a   more..

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^e NIIGATA UNIVERSITY   (Japan)

^f Niigata University   (Japan)

^g KEIO UNIVERSITY   (Japan)

^h NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

ⁱ OSAKA UNIVERSITY   (Japan)

^j JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^k RIKEN   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AXONIN 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL CYCLE; CELL MIGRATION; CELL NUCLEUS; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; HISTOGENESIS; MECHANICAL STRESS; MOUSE; NEOCORTEX; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANIMALS; CELL CYCLE; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; CEREBRAL CORTEX; COMPUTER SIMULATION; CONTACTIN 2; EMBRYO, MAMMALIAN; EPITHELIUM; HISTONES; LUMINESCENT PROTEINS; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; ORGAN CULTURE TECHNIQUES; RNA INTERFERENCE; RNA, SMALL INTERFERING; WNT3A PROTEIN;

EID: 84886954165     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3525     Document Type: Article

References (60)

1. Schaper, A. The earliest differentiation in the central nervous system of vertebrates. Science 5, 430-431 (1897
2. Sauer, F.C. Mitosis in the neural tube. J. Comp. Neurol. 62, 377-405 (1935
3. Chenn, A. & McConnell, S.K. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631-641 (1995
4. Taverna, E. & Huttner, W.B. Neural progenitor nuclei in motion. Neuron 67, 906-914 (2010
5. Lui, J.H., Hansen, D.V. & Kriegstein, A.R. Development and evolution of the human neocortex. Cell 146, 18-36 (2011
6. Reiner, O., Sapir, T. & Gerlitz, G. Interkinetic nuclear movement in the ventricular zone of the cortex. J. Mol. Neurosci. 46, 516-526 (2012
7. Sanes, J.R. Analysing cell lineage with a recombinant virus. Trends Neurosci. 12, 21-28 (1989
8. Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727-741 (2001
9. 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
10. Tsai, J-W., Chen, Y., Kriegstein, A. & Vallee, R.B. RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple steps. J. Cell Biol. 170, 935-945 (2005
11. Xie, Z. et al. Cep120 and TACC control interkinetic nuclear migration and neural progenitor pool. Neuron 56, 79-93 (2007
12. Norden, C., Young, S., Link, B.A. & Harris, W.A. Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138, 1195-1208 (2009
13. Tsai, J.W., Lian, W.N., Kemal, S., Kriegstein, A.R. & Vallee, R.B. Kinesin 3 and cytoplasmic dynein mediate interkinetic nuclear migration in neural stem cells. Nat. Neurosci. 13, 1463-1471 (2010
14. Schenk, J., Wilsch-Brauninger, M., Calegari, F. & Huttner, W.B. Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc. Natl. Acad. Sci. USA 106, 16487-16492 (2009
15. Kosodo, Y. et al. Regulation of interkinetic nuclear migration by cell cycle-coupled active and passive mechanisms in the developing brain. EMBO J. 30, 1690-1704 (2011
16. Leung, L., Klopper, A.V., Grill, S.W., Harris, W.A. & Norden, C. Apical migration of nuclei during G2 is a prerequisite for all nuclear motion in zebrafish neuroepithelia. Development 138, 5003-5013 (2011
17. Smart, I.H.M. The operation of ependymal 'choke' in neurogenesis. J. Anat. 99, 941-943 (1965
18. Fietz, S.A. et al. OSVZ progenitors of human and ferret neocortex are epithelial- like and expand by integrin signaling. Nat. Neurosci. 13, 690-699 (2010
19. Hansen, D.V., Lui, J.H., Parker, P.R. & Kriegstein, A.R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464, 554-561 (2010
20. Barkovich, A.J. et al. A developmental and genetic classification for malformations of cortical development: Update 2012. Brain 135, 1348-1369 (2012
21. Götz, M. & Huttner, W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788 (2005
22. Konno, D. et al. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10, 93-101 (2008
23. Postiglione, M.P. et al. Mouse inscrutable induces apical-basal spindle orientation to facilitate intermediate progenitor generation in the developing neocortex. Neuron 72, 269-284 (2011
24. Furley, A.J. et al. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61, 157-170 (1990
25. Abe, T. et al. Establishment of conditional reporter mouse lines at ROSA26 locus for live cell imaging. Genesis 49, 579-590 (2011
26. Miyanaga, Y., Matsuoka, S. & Ueda, M. Single-molecule imaging techniques to visualize chemotactic signaling events on the membrane of living Dictyostelium cells. Methods Mol. Biol. 571, 417-435 (2009
27. Qian, H., Sheetz, M.P. & Elson, E.L. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys. J. 60, 910-921 (1991
28. Kusumi, A., Sako, Y. & Yamamoto, M. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65, 2021-2040 (1993
29. Nishizawa, Y. et al. Survey of the morphogenetic dynamics of the ventricular surface of the developing mouse neocortex. Dev. Dyn. 236, 3061-3070 (2007
30. Shimogori, T. & Ogawa, M. Gene application with in utero electroporation in mouse embryonic brain. Dev. Growth Differ. 50, 499-506 (2008
31. Miyata, T. & Ogawa, M. Twisting of neocortical progenitor cells underlies a spring-like mechanism for daughter cell migration. Curr. Biol. 17, 146-151 (2007
32. Munji, R.N., Choe, Y., Li, G., Siegenthaler, J.A. & Pleasure, S.J. Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J. Neurosci. 31, 1676-1687 (2011
33. Molyneaux, B.J., Arlotta, P., Menezes, J.R. & Macklis, J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437 (2007
34. Bizzoca, A. et al. F3/Contactin acts as a modulator of neurogenesis during cerebral cortex development. Dev. Biol. 365, 133-151 (2012
35. Milev, P., Maurel, P., Haring, M., Margolis, R.K. & Margolis, R.U. TAG-1/Axonin-1 is a high-Affinity ligand of neurocan, phosphacan/protein- Tyrosine phosphatase-ζ/β, and N-CAM. J. Biol. Chem. 271, 15716-15723 (1996
36. Sittaramane, V. et al. The cell adhesion molecule Tag1, transmembrane protein Stbm/Vangl2, and Lamininα1 exhibit genetic interactions during migration of facial branchiomotor neurons in zebrafish. Dev. Biol. 325, 363-373 (2009
37. Fukamauchi, F. et al. TAG-1-deficient mice have marked elevation of adenosine A1 receptors in the hippocampus. Biochem. Biophys. Res. Commun. 281, 220-226 (2001
38. Shitamukai, A., Konno, D. & Matsuzaki, F. Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J. Neurosci. 31, 3683-3695 (2011
39. Marinari, E. et al. Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 484, 542-545 (2012
40. Itoh, Y. et al. Scratch regulates neuronal migration onset via an epithelial-mesenchymal transition-like mechanism. Nat. Neurosci. 16, 416-425 (2013
41. Fitzgerald, M.P., Covio, M. & Lee, K.S. Disturbances in the positioning, proliferation and apoptosis of neural progenitors contribute to subcortical band heterotopia formation. Neuroscience 176, 455-471 (2011
42. Morin, X., Jaouen, F. & Durbec, P. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10, 1440-1448 (2007
43. Chenn, A. & Walsh, C.A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365-369 (2002
44. Inglis-Broadgate, S.L. et al. FGFR3 regulates brain size by controlling progenitor cell proliferation and apoptosis during embryonic development. Dev. Biol. 279, 73-85 (2005
45. Zedević, N. Cellular composition of the telencephalic wall in human embryos. Early Hum. Dev. 32, 131-149 (1993
46. Bayer, S.A. & Altman, J. The Human Brain During the Late First Trimester (CRC Press Taylor & Francis Group, 2006
47. Tsunekawa, Y. et al. Cyclin D2 in the basal process of neural progenitors is linked to non-equivalent cell fates. EMBO J. 31, 1879-1892 (2012
48. Siegenthaler, J.A. et al. Retinoic acid from the meninges regulates cortical neuron generation. Cell 139, 597-609 (2009
49. Rørth, P. Fellow travelers: Emergent properties of collective cell migration. EMBO Rep. 13, 984-991 (2012
50. Heisenberg, C-P. & Bellaïche, Y. Forces in tissue morphogenesis and patterning. Cell 153, 948-962 (2013
51. Kondo, T. & Hayashi, S. Mitotic cell rounding accelerates epithelial invagination. Nature 494, 125-129 (2013
52. Kawabata, I. et al. Electroporation-mediated gene transfer system applied to cultured CNS neurons. Neuroreport 15, 971-975 (2004
53. Sakakibara, A. et al. Dynamics of centrosome translocation and microtubule organization in neocortical neurons during distinct modes of polarization. Cereb. Cortex doi:10.1093/cercor/bhs411 (10 January 2013
54. Nakamuta, S. et al. Local application of neurotrophins specifies axons through inositol 1,4,5-Trisphosphate, calcium, and Ca2+/calmodulin-dependent protein kinases. Sci. Signal. 4, ra76 (2011
55. Sapir, T. et al. Accurate balance of the polarity kinase MARK2/Par-1 is required for proper cortical neuronal migration. J. Neurosci. 28, 5710-5720 (2008
56. Hino, T. et al. Accelerated modification of the zona pellucida is the primary cause of decreased fertilizability of oocyte in the 129 inbred mouse strain. Zygote 19, 315-322 (2011
57. McLean, I.W. & Nakane, P.K. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J. Histochem. Cytochem. 22, 1077-1083 (1974
58. Honda, H., Tanemura, M. & Nagai, T. A three-dimensional vertex dynamics cell model of space-filling polyhedra simulating cell behaviour in a cell aggregate. J. Theor. Biol. 226, 439-453 (2004
59. Eiraku, M. et al. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56 (2011
60. Okuda, S., Inoue, Y., Eiraku, M., Sasai, Y. & Adachi, T. Modeling cell proliferation for simulating three-dimensional tissue morphogenesis based on a reversible network reconnection framework. Biomech. Model Mechanobiol. doi:10.1007/s10237-012-0458-8 (30 November 2012