title: Distinct intracellular Ca2+dynamics regulate apical constriction and differentially contribute to neural tube closure.
abstract: Early in the development of the central nervous system, progenitor cells undergo a shape change, called apical constriction, that triggers the neural plate to form a tubular structure. How apical constriction in the neural plate is controlled and how it contributes to tissue morphogenesis are not fully understood. In this study, we show that intracellular calcium ions (Ca2+) are required forXenopusneural tube formation and that there are two types of Ca2+-concentration changes, a single-cell and a multicellular wave-like fluctuation, in the developing neural plate. Quantitative imaging analyses revealed that transient increases in Ca2+concentration induced cortical F-actin remodeling, apical constriction and accelerations of the closing movement of the neural plate. We also show that extracellular ATP and N-cadherin (cdh2) participate in the Ca2+-induced apical constriction. Furthermore, our mathematical model suggests that the effect of Ca2+fluctuations on tissue morphogenesis is independent of fluctuation frequency and that fluctuations affecting individual cells are more efficient than those at the multicellular level. We propose that distinct Ca2+signaling patterns differentially modulate apical constriction for efficient epithelial folding and that this mechanism has a broad range of physiological outcomes.
authors.affiliation: Division of Morphogenesis, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8585, Japan msuzuki@nibb.ac.jp nueno@nibb.ac.jp.|Department of Basic Biology, School of Life Science, the Graduate University of Advanced Studies, Hayama, Kanagawa 240-0193 Japan.
authors.forename: Makoto
authors.identifier: 0000-0002-5494-6593
authors.initials: M
authors.lastname: Suzuki
authors.affiliation: Department of Basic Biology, School of Life Science, the Graduate University of Advanced Studies, Hayama, Kanagawa 240-0193 Japan.|Division of Developmental Genetics, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan.|Department of Biodesign Research, Okazaki Institute for Integrative Bioscience, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan.
authors.forename: Masanao
authors.initials: M
authors.lastname: Sato
authors.affiliation: Department of Basic Biology, School of Life Science, the Graduate University of Advanced Studies, Hayama, Kanagawa 240-0193 Japan.|Division of Embryology, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan.
authors.forename: Hiroshi
authors.initials: H
authors.lastname: Koyama
authors.affiliation: Division of Morphogenesis, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8585, Japan.|Department of Basic Biology, School of Life Science, the Graduate University of Advanced Studies, Hayama, Kanagawa 240-0193 Japan.
authors.forename: Yusuke
authors.initials: Y
authors.lastname: Hara
authors.affiliation: Division of Morphogenesis, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8585, Japan.|Department of Basic Biology, School of Life Science, the Graduate University of Advanced Studies, Hayama, Kanagawa 240-0193 Japan.
authors.forename: Kentaro
authors.initials: K
authors.lastname: Hayashi
authors.affiliation: Division of Morphogenesis, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8585, Japan.
authors.forename: Naoko
authors.initials: N
authors.lastname: Yasue
authors.affiliation: Department of Functional Biology, Graduate School of Biostudies, Kyoto University, Sakyo-ku, Kyoto 606-8501, Japan.
authors.forename: Hiromi
authors.initials: H
authors.lastname: Imamura
authors.affiliation: Department of Basic Biology, School of Life Science, the Graduate University of Advanced Studies, Hayama, Kanagawa 240-0193 Japan.|Division of Embryology, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan.
authors.forename: Toshihiko
authors.initials: T
authors.lastname: Fujimori
authors.affiliation: Department of Biomolecular Science and Engineering, The Institute of Scientific and Industrial Research, Osaka University, Ibaraki, Osaka 567-0047, Japan.
authors.forename: Takeharu
authors.initials: T
authors.lastname: Nagai
authors.affiliation: Department of Chemistry, University of Alberta, Edmonton, Alberta, Canada T6G 2G2.
authors.forename: Robert E
authors.initials: RE
authors.lastname: Campbell
authors.affiliation: Division of Morphogenesis, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi 444-8585, Japan msuzuki@nibb.ac.jp nueno@nibb.ac.jp.|Department of Basic Biology, School of Life Science, the Graduate University of Advanced Studies, Hayama, Kanagawa 240-0193 Japan.
authors.forename: Naoto
authors.initials: N
authors.lastname: Ueno
mesh_terms: D000199:Actins / Q000378:metabolism; D000255:Adenosine Triphosphate / Q000378:metabolism; D000818:Animals; D002118:Calcium / Q000378:metabolism*; D016764:Cell Polarity; D005110:Extracellular Space / Q000378:metabolism; D021621:Imaging, Three-Dimensional; D042541:Intracellular Space / Q000378:metabolism*; D016014:Linear Models; D008954:Models, Biological; D009024:Morphogenesis; D054258:Neural Plate / Q000166:cytology / Q000378:metabolism; D054259:Neural Tube / Q000166:cytology* / Q000378:metabolism*; D014982:Xenopus laevis / Q000196:embryology*
chemical_list: D000199:Actins; D000255:Adenosine Triphosphate; D002118:Calcium
keywords: Actomyosin; Apical constriction; Ca2+; Epithelial remodeling; Neural tube closure