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J Cell Sci. 2017 Feb 15;130(4):712-724. doi: 10.1242/jcs.193003. Epub 2017 Jan 6.

The spectraplakin Short stop is an essential microtubule regulator involved in epithelial closure in Drosophila.

Author information

1
Institute of Genetics, Biological Research Centre of the Hungarian Academy of Sciences, Temesvári krt. 62, Szeged 6726, Hungary.
2
Institute of Genetics, Biological Research Centre of the Hungarian Academy of Sciences, Temesvári krt. 62, Szeged 6726, Hungary jankovics.ferenc@brc.mta.hu.
3
Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, Heidelberg 69117, Germany.
4
MRC-Laboratory of Molecular Biology, Cambridge Biomedical Campus, Francis Crick Avenue, Cambridge CB2 0QH, UK.

Abstract

Dorsal closure of the Drosophila embryonic epithelium provides an excellent model system for the in vivo analysis of molecular mechanisms regulating cytoskeletal rearrangements. In this study, we investigated the function of the Drosophila spectraplakin Short stop (Shot), a conserved cytoskeletal structural protein, during closure of the dorsal embryonic epithelium. We show that Shot is essential for the efficient final zippering of the opposing epithelial margins. By using isoform-specific mutant alleles and genetic rescue experiments with truncated Shot variants, we demonstrate that Shot functions as an actin-microtubule cross-linker in mediating zippering. At the leading edge of epithelial cells, Shot regulates protrusion dynamics by promoting filopodia formation. Fluorescence recovery after photobleaching (FRAP) analysis and in vivo imaging of microtubule growth revealed that Shot stabilizes dynamic microtubules. The actin- and microtubule-binding activities of Shot are simultaneously required in the same molecule, indicating that Shot is engaged as a physical crosslinker in this process. We propose that Shot-mediated interactions between microtubules and actin filaments facilitate filopodia formation, which promotes zippering by initiating contact between opposing epithelial cells.

KEYWORDS:

Actin; Dorsal closure; Drosophila; Microtubule; Short stop; Spectraplakin

PMID:
28062848
PMCID:
PMC5339884
DOI:
10.1242/jcs.193003
[Indexed for MEDLINE]
Free PMC Article

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