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Surface mechanics mediate pattern formation in the developing retina

Abstract

Pattern formation of biological structures involves organizing different types of cells into a spatial configuration. In this study, we investigate the physical basis of biological patterning of the Drosophila retina in vivo. We demonstrate that E- and N-cadherins mediate apical adhesion between retina epithelial cells. Differential expression of N-cadherin within a sub-group of retinal cells (cone cells) causes them to form an overall shape that minimizes their surface contact with surrounding cells. The cells within this group, in both normal and experimentally manipulated conditions, pack together in the same way as soap bubbles do. The shaping of the cone cell group and packing of its components precisely imitate the physical tendency for surfaces to be minimized. Thus, simple patterned expression of N-cadherin results in a complex spatial pattern of cells owing to cellular surface mechanics.

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Figure 1: Pattern formation in different tissues.
Figure 2: Configuration of cone cells precisely correlates with soap bubble configurations.
Figure 3: DE- and DN-cadherins are required for apical adhesion of retinal cells.
Figure 4: DN-cadherin is required for cone cell patterning.
Figure 5: Misexpression of cadherins leads to patterning defects.

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Acknowledgements

We thank T. Uemura, H. Oda, U. Tepass, G. Thomas, B. Dickson, P. Garrity, the Bloomington Drosophila Stock Center and the Developmental Studies Hybridoma Bank for fly strains and/or antibodies. We also thank K. Saigo for use of facilities. We thank M. Steinberg and R. Matsuda for critical input. We acknowledge G. Beitel, A. Dudley, J. Widom and E. Sontheimer for greatly improving the manuscript. T.H. was supported by a research fellowship from the Japan Society for the Promotion of Science for Young Scientists. This work was also supported by the NIH.

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Correspondence to Takashi Hayashi or Richard W. Carthew.

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Hayashi, T., Carthew, R. Surface mechanics mediate pattern formation in the developing retina. Nature 431, 647–652 (2004). https://doi.org/10.1038/nature02952

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