RRC ID 36287
Author Hatori R, Ando T, Sasamura T, Nakazawa N, Nakamura M, Taniguchi K, Hozumi S, Kikuta J, Ishii M, Matsuno K.
Title Left-right asymmetry is formed in individual cells by intrinsic cell chirality.
Journal Mech. Dev.
Abstract Many animals show left-right (LR) asymmetric morphology. The mechanisms of LR asymmetric development are evolutionarily divergent, and they remain elusive in invertebrates. Various organs in Drosophila melanogaster show stereotypic LR asymmetry, including the embryonic gut. The Drosophila embryonic hindgut twists 90° left-handedly, thereby generating directional LR asymmetry. We recently revealed that the hindgut epithelial cell is chiral in shape and other properties; this is termed planar cell chirality (PCC). We previously showed by computer modeling that PCC is sufficient to induce the hindgut rotation. In addition, both the PCC and the direction of hindgut twisting are reversed in Myosin31DF (Myo31DF) mutants. Myo31DF encodes Drosophila MyosinID, an actin-based motor protein, whose molecular functions in LR asymmetric development are largely unknown. Here, to understand how PCC directs the asymmetric cell-shape, we analyzed PCC in genetic mosaics composed of cells homozygous for mutant Myo31DF, some of which also overexpressed wild-type Myo31DF. Wild-type cell-shape chirality only formed in the Myo31DF-overexpressing cells, suggesting that cell-shape chirality was established in each cell and reflects intrinsic PCC. A computer model recapitulating the development of this genetic mosaic suggested that mechanical interactions between cells are required for the cell-shape behavior seen in vivo. Our mosaic analysis also suggested that during hindgut rotation in vivo, wild-type Myo31DF suppresses the elongation of cell boundaries, supporting the idea that cell-shape chirality is an intrinsic property determined in each cell. However, the amount and distribution of F-actin and Myosin II, which are known to help generate the contraction force on cell boundaries, did not show differences between Myo31DF mutant cells and wild-type cells, suggesting that the static amount and distribution of these proteins are not involved in the suppression of cell-boundary elongation. Taken together, our results suggest that cell-shape chirality is intrinsically formed in each cell, and that mechanical force from intercellular interactions contributes to its formation and/or maintenance.
Volume 133
Pages 146-62
Published 2014-8
DOI 10.1016/j.mod.2014.04.002
PII S0925-4773(14)00024-0
PMID 24800645
MeSH Animals Animals, Genetically Modified Body Patterning / genetics Body Patterning / physiology* Cell Polarity / genetics Cell Polarity / physiology* Cell Shape / genetics Cell Shape / physiology Computer Simulation Digestive System / cytology Digestive System / embryology Drosophila Proteins / genetics Drosophila Proteins / physiology* Drosophila melanogaster / cytology* Drosophila melanogaster / embryology* Drosophila melanogaster / genetics Genes, Insect Mechanotransduction, Cellular / genetics Models, Biological Mosaicism Mutation Myosin Type I / genetics Myosin Type I / physiology*
IF 1.9
Times Cited 9
WOS Category DEVELOPMENTAL BIOLOGY
Resource
Drosophila