Curvature in Biological Systems: Its Quantification, Emergence, and Implications across the Scales

Barbara Schamberger¹, Ricardo Ziege², Karine Anselme^{3

4}, Martine Ben Amar⁵, Michał Bykowski⁶, André P G Castro^{7

8}, Amaia Cipitria^{3

9

10}, Rhoslyn A Coles¹¹, Rumiana Dimova¹², Michaela Eder², Sebastian Ehrig^{13

14}, Luis M Escudero^{15

16}, Myfanwy E Evans¹⁷, Paulo R Fernandes⁷, Peter Fratzl², Liesbet Geris¹⁸, Notburga Gierlinger¹⁹, Edouard Hannezo²⁰, Aleš Iglič²¹, Jacob J K Kirkensgaard^{22

23}, Philip Kollmannsberger²⁴, Łucja Kowalewska⁶, Nicholas A Kurniawan²⁵, Ioannis Papantoniou^{26

27

28}, Laurent Pieuchot^{3

4}, Tiago H V Pires⁷, Lars D Renner²⁹, Andrew O Sageman-Furnas³⁰, Gerd E Schröder-Turk^{31

32}, Anupam Sengupta³³, Vikas R Sharma¹, Antonio Tagua^{15

16}, Caterina Tomba³⁴, Xavier Trepat^{35

36}, Sarah L Waters³⁷, Edwina F Yeo³⁷, Andreas Roschger¹, Cécile M Bidan², John W C Dunlop¹

Affiliations

¹ Department of the Chemistry and Physics of Materials, Paris-Lodron University of Salzburg, 5020, Salzburg, Austria.
² Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476, Potsdam, Germany.
³ IS2M (CNRS - UMR 7361), Université de Haute-Alsace, F-68100, Mulhouse, France.
⁴ Université de Strasbourg, F-67081, Strasbourg, France.
⁵ Department of Physics, Laboratoire de Physique de l'Ecole Normale Supérieure, 24 rue Lhomond, 75005, Paris, France.
⁶ Department of Plant Anatomy and Cytology, Faculty of Biology, University of Warsaw, 02-096, Warsaw, Poland.
⁷ IDMEC, Instituto Superior Técnico, Universidade de Lisboa, 1049-001, Lisboa, Portugal.
⁸ ESTS, Instituto Politécnico de Setúbal, 2914-761, Setúbal, Portugal.
⁹ Group of Bioengineering in Regeneration and Cancer, Biodonostia Health Research Institute, 20014, San Sebastian, Spain.
¹⁰ IKERBASQUE, Basque Foundation for Science, 48009, Bilbao, Spain.
¹¹ Cluster of Excellence, Matters of Activity, Humboldt-Universität zu Berlin, 10178, Berlin, Germany.
¹² Department of Theory and Bio-Systems, Max Planck Institute of Colloids and Interfaces, 14476, Potsdam, Germany.
¹³ Max Delbrück Center for Molecular Medicine, 13125, Berlin, Germany.
¹⁴ Berlin Institute for Medical Systems Biology, 10115, Berlin, Germany.
¹⁵ Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013, Seville, Spain.
¹⁶ Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), 28031, Madrid, Spain.
¹⁷ Institute for Mathematics, University of Potsdam, 14476, Potsdam, Germany.
¹⁸ Biomechanics Research Unit, GIGA In Silico Medicine, University of Liège, 4000, Liège, Belgium.
¹⁹ Institute of Biophysics, Department of Nanobiotechnology, University of Natural Resources and Life Sciences Vienna (Boku), 1190, Vienna, Austria.
²⁰ Institute of Science and Technology Austria, 3400, Klosterneuburg, Austria.
²¹ Laboratory of Physics, Faculty of Electrical engineering, University of Ljubljana, Tržaška 25, SI-1000, Ljubljana, Slovenia.
²² Condensed Matter Physics, Niels Bohr Institute, University of Copenhagen, Universitetsparken 5, 2100, København Ø, Denmark.
²³ Ingredients and Dairy Technology, Department of Food Science, University of Copenhagen, Rolighedsvej 26, 1958, Frederiksberg, Denmark.
²⁴ Center for Computational and Theoretical Biology, University of Würzburg, 97074, Würzburg, Germany.
²⁵ Department of Biomedical Engineering and Institute for Complex Molecular Systems, Eindhoven University of Technology, 5600 MB, Eindhoven, The Netherlands.
²⁶ Prometheus Division of Skeletal Tissue Engineering, KU Leuven, O&N1, Herestraat 49, PB 813, 3000, Leuven, Belgium.
²⁷ Skeletal Biology and Engineering Research Center, Department of Development and Regeneration, KU Leuven, O&N1, Herestraat 49, PB 813, 3000, Leuven, Belgium.
²⁸ Institute of Chemical Engineering Sciences, Foundation for Research and Technology (FORTH), Stadiou Str., 26504, Patras, Greece.
²⁹ Leibniz Institute of Polymer Research and the Max Bergmann Center of Biomaterials, 01069, Dresden, Germany.
³⁰ Department of Mathematics, North Carolina State University, Raleigh, NC, 27695, USA.
³¹ School of Physics, Chemistry and Mathematics, Murdoch University, 90 South St, Murdoch, WA, 6150, Australia.
³² Department of Materials Physics, Research School of Physics, The Australian National University, Canberra, ACT, 2600, Australia.
³³ Physics of Living Matter, Department of Physics and Materials Science, University of Luxembourg, L-1511, Luxembourg City, Grand Duchy of Luxembourg.
³⁴ Univ Lyon, CNRS, INSA Lyon, Ecole Centrale de Lyon, Université Claude Bernard Lyon 1, CPE Lyon, INL, UMR5270, 69622, Villeurbanne, France.
³⁵ ICREA at the Institute for Bioengineering of Catalonia, The Barcelona Institute for Science and Technology, 08028, Barcelona, Spain.
³⁶ Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), 08028, Barcelona, Spain.
³⁷ Mathematical Institute, University of Oxford, OX2 6GG, Oxford, UK.

PMID: 36461812
DOI: 10.1002/adma.202206110

Free article

Review

Curvature in Biological Systems: Its Quantification, Emergence, and Implications across the Scales

Barbara Schamberger et al. Adv Mater. 2023 Mar.

Free article

. 2023 Mar;35(13):e2206110.

doi: 10.1002/adma.202206110. Epub 2023 Feb 15.

Authors

Affiliations

¹ Department of the Chemistry and Physics of Materials, Paris-Lodron University of Salzburg, 5020, Salzburg, Austria.
² Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476, Potsdam, Germany.
³ IS2M (CNRS - UMR 7361), Université de Haute-Alsace, F-68100, Mulhouse, France.
⁴ Université de Strasbourg, F-67081, Strasbourg, France.
⁵ Department of Physics, Laboratoire de Physique de l'Ecole Normale Supérieure, 24 rue Lhomond, 75005, Paris, France.
⁶ Department of Plant Anatomy and Cytology, Faculty of Biology, University of Warsaw, 02-096, Warsaw, Poland.
⁷ IDMEC, Instituto Superior Técnico, Universidade de Lisboa, 1049-001, Lisboa, Portugal.
⁸ ESTS, Instituto Politécnico de Setúbal, 2914-761, Setúbal, Portugal.
⁹ Group of Bioengineering in Regeneration and Cancer, Biodonostia Health Research Institute, 20014, San Sebastian, Spain.
¹⁰ IKERBASQUE, Basque Foundation for Science, 48009, Bilbao, Spain.
¹¹ Cluster of Excellence, Matters of Activity, Humboldt-Universität zu Berlin, 10178, Berlin, Germany.
¹² Department of Theory and Bio-Systems, Max Planck Institute of Colloids and Interfaces, 14476, Potsdam, Germany.
¹³ Max Delbrück Center for Molecular Medicine, 13125, Berlin, Germany.
¹⁴ Berlin Institute for Medical Systems Biology, 10115, Berlin, Germany.
¹⁵ Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013, Seville, Spain.
¹⁶ Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), 28031, Madrid, Spain.
¹⁷ Institute for Mathematics, University of Potsdam, 14476, Potsdam, Germany.
¹⁸ Biomechanics Research Unit, GIGA In Silico Medicine, University of Liège, 4000, Liège, Belgium.
¹⁹ Institute of Biophysics, Department of Nanobiotechnology, University of Natural Resources and Life Sciences Vienna (Boku), 1190, Vienna, Austria.
²⁰ Institute of Science and Technology Austria, 3400, Klosterneuburg, Austria.
²¹ Laboratory of Physics, Faculty of Electrical engineering, University of Ljubljana, Tržaška 25, SI-1000, Ljubljana, Slovenia.
²² Condensed Matter Physics, Niels Bohr Institute, University of Copenhagen, Universitetsparken 5, 2100, København Ø, Denmark.
²³ Ingredients and Dairy Technology, Department of Food Science, University of Copenhagen, Rolighedsvej 26, 1958, Frederiksberg, Denmark.
²⁴ Center for Computational and Theoretical Biology, University of Würzburg, 97074, Würzburg, Germany.
²⁵ Department of Biomedical Engineering and Institute for Complex Molecular Systems, Eindhoven University of Technology, 5600 MB, Eindhoven, The Netherlands.
²⁶ Prometheus Division of Skeletal Tissue Engineering, KU Leuven, O&N1, Herestraat 49, PB 813, 3000, Leuven, Belgium.
²⁷ Skeletal Biology and Engineering Research Center, Department of Development and Regeneration, KU Leuven, O&N1, Herestraat 49, PB 813, 3000, Leuven, Belgium.
²⁸ Institute of Chemical Engineering Sciences, Foundation for Research and Technology (FORTH), Stadiou Str., 26504, Patras, Greece.
²⁹ Leibniz Institute of Polymer Research and the Max Bergmann Center of Biomaterials, 01069, Dresden, Germany.
³⁰ Department of Mathematics, North Carolina State University, Raleigh, NC, 27695, USA.
³¹ School of Physics, Chemistry and Mathematics, Murdoch University, 90 South St, Murdoch, WA, 6150, Australia.
³² Department of Materials Physics, Research School of Physics, The Australian National University, Canberra, ACT, 2600, Australia.
³³ Physics of Living Matter, Department of Physics and Materials Science, University of Luxembourg, L-1511, Luxembourg City, Grand Duchy of Luxembourg.
³⁴ Univ Lyon, CNRS, INSA Lyon, Ecole Centrale de Lyon, Université Claude Bernard Lyon 1, CPE Lyon, INL, UMR5270, 69622, Villeurbanne, France.
³⁵ ICREA at the Institute for Bioengineering of Catalonia, The Barcelona Institute for Science and Technology, 08028, Barcelona, Spain.
³⁶ Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), 08028, Barcelona, Spain.
³⁷ Mathematical Institute, University of Oxford, OX2 6GG, Oxford, UK.

PMID: 36461812
DOI: 10.1002/adma.202206110

Abstract

Surface curvature both emerges from, and influences the behavior of, living objects at length scales ranging from cell membranes to single cells to tissues and organs. The relevance of surface curvature in biology is supported by numerous experimental and theoretical investigations in recent years. In this review, first, a brief introduction to the key ideas of surface curvature in the context of biological systems is given and the challenges that arise when measuring surface curvature are discussed. Giving an overview of the emergence of curvature in biological systems, its significance at different length scales becomes apparent. On the other hand, summarizing current findings also shows that both single cells and entire cell sheets, tissues or organisms respond to curvature by modulating their shape and their migration behavior. Finally, the interplay between the distribution of morphogens or micro-organisms and the emergence of curvature across length scales is addressed with examples demonstrating these key mechanistic principles of morphogenesis. Overall, this review highlights that curved interfaces are not merely a passive by-product of the chemical, biological, and mechanical processes but that curvature acts also as a signal that co-determines these processes.

Keywords: biological systems; mechanotransduction; morphogenesis; surface curvature.

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References

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Curvature in Biological Systems: Its Quantification, Emergence, and Implications across the Scales

Affiliations

Curvature in Biological Systems: Its Quantification, Emergence, and Implications across the Scales

Authors

Affiliations

Abstract

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources