AMPA glutamate receptors are required for sensory-organ formation and morphogenesis in the basal chordate

Shinobu Hirai, Kohji Hotta, Yoshihiro Kubo, Atsuo Nishino, Shigeo Okabe, Yasushi Okamura, Haruo Okado

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

AMPA-type glutamate receptors (GluAs) mediate fast excitatory transmission in the vertebrate central nervous system (CNS), and their function has been extensively studied in the mature mammalian brain. However, GluA expression begins very early in developing embryos, suggesting that they may also have unidentified developmental roles. Here, we identify developmental roles for GluAs in the ascidian Ciona intestinalis. Mammals express Ca2+-permeable GluAs (Ca-P GluAs) and Ca2+-impermeable GluAs (Ca-I GluAs) by combining subunits derived from four genes. In contrast, ascidians have a single gluA gene. Taking advantage of the simple genomic GluA organization in ascidians, we knocked down (KD) GluAs in Ciona and observed severe impairments in formation of the ocellus, a photoreceptive organ used during the swimming stage, and in resorption of the tail and body axis rotation during metamorphosis to the adult stage. These defects could be rescued by injection of KD-resistant GluAs. GluA KD phenotypes could also be reproduced by expressing a GluA mutant that dominantly inhibits glutamate-evoked currents. These results suggest that, in addition to their role in synaptic communication in mature animals, GluAs also have critical developmental functions.

Original languageEnglish
Pages (from-to)3939-3944
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number15
DOIs
Publication statusPublished - 2017 Apr 11

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Chordata
Urochordata
AMPA Receptors
Glutamate Receptors
Morphogenesis
Ciona intestinalis
Genes
Vertebrates
Tail
Glutamic Acid
Mammals
Embryonic Structures
Central Nervous System
Communication
Phenotype
Injections
Brain

Keywords

  • AMPA-type glutamate receptor
  • Ascidian
  • Development
  • Morphogeneis

ASJC Scopus subject areas

  • General

Cite this

AMPA glutamate receptors are required for sensory-organ formation and morphogenesis in the basal chordate. / Hirai, Shinobu; Hotta, Kohji; Kubo, Yoshihiro; Nishino, Atsuo; Okabe, Shigeo; Okamura, Yasushi; Okado, Haruo.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 15, 11.04.2017, p. 3939-3944.

Research output: Contribution to journalArticle

Hirai, Shinobu ; Hotta, Kohji ; Kubo, Yoshihiro ; Nishino, Atsuo ; Okabe, Shigeo ; Okamura, Yasushi ; Okado, Haruo. / AMPA glutamate receptors are required for sensory-organ formation and morphogenesis in the basal chordate. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 15. pp. 3939-3944.
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