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 & Luis M. Escudero
Nature Communications volume 9, Article number: 2960 (2018)
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.
Acknowledgements
M.D.M.-B. and A.V.-E. work was funded by the Ministerio Español de Ciencia y Tecnología (grants numbers BFU2013-48988-C2-1-P and BFU2016-80797 to M.D.M.-B.). A.V.-E. is supported by a FPI studentship (BES-2014-068850) from the Ministerio de Economía y Competitividad. S.S. is supported by grant of the MICINN/FEDER to J.C.-G. Hombría (BFU2016-76528-P). F.C. work is funded by Spanish Government Grant BFU2014-55918 and BBVA Foundation Personal Grant IN[16]_BBM_BAS_0078. J.B. acknowledges core funding by Lehigh University. L.M.E. and P.G.-G. are supported by the Ramón y Cajal program (PI13/01347); L.M.E., A.M., and C.G. work is funded by the Ministry of Economy, Industry, and Competitiveness grant BFU2016-74975-P co-funded by FEDER funds. P.V.-M. is supported by a contract co-funded by the Asociación Fundación Española contra el Cáncer and the Seville University. A.M.C. is supported by Fundación Pública Andaluza Progreso y Salud (Consejería de Salud), ref. PI-0033-2014. C.F. and A.T. is supported by a contract from Sistema Nacional de Garantía Juvenil and Programa Operativo de Empleo Juvenil 2014–2020. We are thankful to Dr. Nicolas Gompel for the picture of the Cetoniidae: Protaetia (Potosia) speciose to illustrate the term “scutoid”. We thank Dr. Paco Martín, Dr. José López-Barneo, Dr. Alberto Pascual, Dr. Colin Adrain and Dr. Matthew Freeman for helpful comments and corrections to the manuscript.
Author information
Author notes
These authors contributed equally: Pedro Gómez-Gálvez, Pablo Vicente-Munuera.
Affiliations
Departamento de Biología Celular, Universidad de Sevilla and Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla, 41013, Seville, Spain
Pedro Gómez-Gálvez, Pablo Vicente-Munuera, Antonio Tagua, Cristina Forja, Ana M. Castro, Marta Letrán, Marina Bermúdez-Gallardo, Óscar Serrano-Pérez-Higueras & Luis M. Escudero
CABD, CSIC/JA/UPO, Campus Universidad Pablo de Olavide, 41013, Seville, Spain
Andrea Valencia-Expósito, Sol Sotillos & María D. Martín-Bermudo
Departamento de Matemática Aplicada I, Universidad de Sevilla, 41012, Seville, Spain
Clara Grima & Alberto Márquez
Centro de Biología Molecular Severo Ochoa and CIBER de Enfermedades Raras. C/ Nicolás Cabrera 1, 28049, Madrid, Spain
Florencia Cavodeassi
St. George’s, University of London, Cranmer Terrace, SW17 0RE, London, UK
Florencia Cavodeassi
Bioengineering Department, Lehigh University, Bethlehem, PA, 18018, USA
Javier Buceta
Chemical and Biomolecular Engineering Department, Lehigh University, Bethlehem, PA, 18018, USA
Javier Buceta
Contributions
L.M.E. designed the study with help from A.M., C.G., and J.B. P.G.-G. and P.V.-M. wrote the software for the mathematical model and performed analyses. A.T., C.F., A.M.C., M.L., A.V.-E., M.B.-G., O.S.-P.-H., F.C., S.S., and M.D.M.-B., collaborated in the obtaining, measurement of parameters and analysis of the confocal images. All authors participated in the interpretation of results, discussions, and the development of the project. J.B. and L.M.E. wrote the manuscript with input from all authors.
Competing interests
The authors declare no competing interests.
Corresponding authors
Correspondence to Javier Buceta or Luis M. Escudero.
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