Connexin 39.9 protein is necessary for coordinated activation of slow-twitch muscle and normal behavior in zebrafish

Hiromi Hirata, Hua Wen, Yu Kawakami, Yuriko Naganawa, Kazutoyo Ogino, Kenta Yamada, Louis Saint-Amant, Sean E. Low, Wilson W. Cui, Weibin Zhou, Shawn M. Sprague, Kazuhide Asakawa, Akira Muto, Koichi Kawakami, John Y. Kuwada

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

In many tissues and organs, connexin proteins assemble between neighboring cells to form gap junctions. These gap junctions facilitate direct intercellular communication between adjoining cells, allowing for the transmission of both chemical and electrical signals. In rodents, gap junctions are found in differentiating myoblasts and are important for myogenesis. Although gap junctions were once believed to be absent from differentiated skeletal muscle in mammals, recent studies in teleosts revealed that differentiated muscle does express connexins and is electrically coupled, at least at the larval stage. These findings raised questions regarding the functional significance of gap junctions in differentiated muscle. Our analysis of gap junctions in muscle began with the isolation of a zebrafish motor mutant that displayed weak coiling at day 1 of development, a behavior known to be driven by slow-twitch muscle (slow muscle). We identified a missense mutation in the gene encoding Connexin 39.9. In situ hybridization found connexin 39.9 to be expressed by slow muscle. Paired muscle recordings uncovered that wild-type slow muscles are electrically coupled, whereas mutant slow muscles are not. The further examination of cellular activity revealed aberrant, arrhythmic touch-evoked Ca 2+ transients in mutant slow muscle and a reduction in the number of muscle fibers contracting in response to touch in mutants. These results indicate that Connexin 39.9 facilitates the spreading of neuronal inputs, which is irregular during motor development, beyond the muscle cells and that gap junctions play an essential role in the efficient recruitment of slow muscle fibers.

Original languageEnglish (US)
Pages (from-to)1080-1089
Number of pages10
JournalJournal of Biological Chemistry
Volume287
Issue number2
DOIs
StatePublished - Jan 6 2012

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Connexins
Zebrafish
Muscle
Gap Junctions
Chemical activation
Muscles
Proteins
Touch
Slow-Twitch Muscle Fibers
Intercellular Junctions
Muscle Development
Myoblasts
Missense Mutation
Muscle Cells
Gene encoding
Mammals
In Situ Hybridization
Fibers
Rodentia
Skeletal Muscle

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

Connexin 39.9 protein is necessary for coordinated activation of slow-twitch muscle and normal behavior in zebrafish. / Hirata, Hiromi; Wen, Hua; Kawakami, Yu; Naganawa, Yuriko; Ogino, Kazutoyo; Yamada, Kenta; Saint-Amant, Louis; Low, Sean E.; Cui, Wilson W.; Zhou, Weibin; Sprague, Shawn M.; Asakawa, Kazuhide; Muto, Akira; Kawakami, Koichi; Kuwada, John Y.

In: Journal of Biological Chemistry, Vol. 287, No. 2, 06.01.2012, p. 1080-1089.

Research output: Contribution to journalArticle

Hirata, H, Wen, H, Kawakami, Y, Naganawa, Y, Ogino, K, Yamada, K, Saint-Amant, L, Low, SE, Cui, WW, Zhou, W, Sprague, SM, Asakawa, K, Muto, A, Kawakami, K & Kuwada, JY 2012, 'Connexin 39.9 protein is necessary for coordinated activation of slow-twitch muscle and normal behavior in zebrafish', Journal of Biological Chemistry, vol. 287, no. 2, pp. 1080-1089. https://doi.org/10.1074/jbc.M111.308205
Hirata, Hiromi ; Wen, Hua ; Kawakami, Yu ; Naganawa, Yuriko ; Ogino, Kazutoyo ; Yamada, Kenta ; Saint-Amant, Louis ; Low, Sean E. ; Cui, Wilson W. ; Zhou, Weibin ; Sprague, Shawn M. ; Asakawa, Kazuhide ; Muto, Akira ; Kawakami, Koichi ; Kuwada, John Y. / Connexin 39.9 protein is necessary for coordinated activation of slow-twitch muscle and normal behavior in zebrafish. In: Journal of Biological Chemistry. 2012 ; Vol. 287, No. 2. pp. 1080-1089.
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