Scutoids are a geometrical solution to three-dimensional packing of epithelia

Pedro Gómez-Gálvez, Pablo Vicente-Munuera, Antonio Tagua, Cristina Forja, Ana M. Castro, Marta Letrán, Andrea Valencia-Expósito, Clara Grima, Marina Bermúdez-Gallardo, Óscar Serrano-Pérez-Higueras, Florencia Cavodeassi, Sol Sotillos, María D. Martín-Bermudo, Alberto Márquez, Javier Buceta () and Luis M. Escudero ()
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Pedro Gómez-Gálvez: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla
Pablo Vicente-Munuera: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla
Antonio Tagua: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla
Cristina Forja: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla
Ana M. Castro: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla
Marta Letrán: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla
Andrea Valencia-Expósito: CABD, CSIC/JA/UPO, Campus Universidad Pablo de Olavide
Clara Grima: Universidad de Sevilla
Marina Bermúdez-Gallardo: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla
Óscar Serrano-Pérez-Higueras: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla
Florencia Cavodeassi: Centro de Biología Molecular Severo Ochoa and CIBER de Enfermedades Raras. C/ Nicolás Cabrera 1
Sol Sotillos: CABD, CSIC/JA/UPO, Campus Universidad Pablo de Olavide
María D. Martín-Bermudo: CABD, CSIC/JA/UPO, Campus Universidad Pablo de Olavide
Alberto Márquez: Universidad de Sevilla
Javier Buceta: Lehigh University
Luis M. Escudero: Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla

Nature Communications, 2018, vol. 9, issue 1, 1-14

Abstract: Abstract As animals develop, tissue bending contributes to shape the organs into complex three-dimensional structures. However, the architecture and packing of curved epithelia remains largely unknown. Here we show by means of mathematical modelling that cells in bent epithelia can undergo intercalations along the apico-basal axis. This phenomenon forces cells to have different neighbours in their basal and apical surfaces. As a consequence, epithelial cells adopt a novel shape that we term “scutoid”. The detailed analysis of diverse tissues confirms that generation of apico-basal intercalations between cells is a common feature during morphogenesis. Using biophysical arguments, we propose that scutoids make possible the minimization of the tissue energy and stabilize three-dimensional packing. Hence, we conclude that scutoids are one of nature's solutions to achieve epithelial bending. Our findings pave the way to understand the three-dimensional organization of epithelial organs.

Date: 2018
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DOI: 10.1038/s41467-018-05376-1

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