Journal
JOURNAL OF CELL SCIENCE
Volume 130, Issue 4, Pages 712-724Publisher
COMPANY BIOLOGISTS LTD
DOI: 10.1242/jcs.193003
Keywords
Drosophila; Spectraplakin; Short stop; Dorsal closure; Microtubule; Actin
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Funding
- Janos Bolyai Research Fellowship of the Magyar Tudomanyos Akademia (Hungarian Academy of Sciences)
- National Research, Development and Innovation Office [NKFI-K117010, OTKA-K108538, GINOP-2.3.2-15-2016-00001]
- Medical Research Council [MC_UP_1201/11]
- MRC [MC_UP_1201/11] Funding Source: UKRI
- Medical Research Council [MC_UP_1201/11] Funding Source: researchfish
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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.
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