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

Barbara Schamberger; Ricardo Ziege; Karine Anselme; Martine Ben Amar; Michał Bykowski; André P.G. Castro; Amaia Cipitria; Rhoslyn A. Coles; Rumiana Dimova; Michaela Eder; Sebastian Ehrig; Luis M. Escudero; Myfanwy E. Evans; Paulo R. Fernandes; Peter Fratzl; Liesbet Geris; Notburga Gierlinger; Edouard Hannezo; Aleš Iglič; Jacob J.K. Kirkensgaard; Philip Kollmannsberger; Łucja Kowalewska; Nicholas A. Kurniawan; Ioannis Papantoniou; Laurent Pieuchot; Tiago H.V. Pires; Lars D. Renner; Andrew O. Sageman-Furnas; Gerd E. Schröder-Turk; Anupam Sengupta; Vikas R. Sharma; Antonio Tagua; Caterina Tomba; Xavier Trepat; Sarah L. Waters; Edwina F. Yeo; Andreas Roschger; Cécile M. Bidan; John W.C. Dunlop

doi:10.1002/adma.202206110

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

Barbara Schamberger
, Ricardo Ziege
, Karine Anselme
, Martine Ben Amar
, Michał Bykowski
, André P.G. Castro
, Amaia Cipitria
, Rhoslyn A. Coles
, Rumiana Dimova
, Michaela Eder
, Sebastian Ehrig
, Luis M. Escudero
, Myfanwy E. Evans
, Paulo R. Fernandes
, Peter Fratzl
, Liesbet Geris
, Notburga Gierlinger
, Edouard Hannezo
, Aleš Iglič
, Jacob J.K. Kirkensgaard

Philip Kollmannsberger, Łucja Kowalewska, Nicholas A. Kurniawan, Ioannis Papantoniou, Laurent Pieuchot, Tiago H.V. Pires, Lars D. Renner, Andrew O. Sageman-Furnas, Gerd E. Schröder-Turk, Anupam Sengupta, Vikas R. Sharma, Antonio Tagua, Caterina Tomba, Xavier Trepat, Sarah L. Waters, Edwina F. Yeo, Andreas Roschger (Corresponding author), Cécile M. Bidan (Corresponding author), John W.C. Dunlop (Corresponding author)

Research output: Contribution to journal › Review article › peer-review

139 Citations (Scopus)

181 Downloads (Pure)

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.

Original language	English
Article number	2206110
Number of pages	23
Journal	Advanced Materials
Volume	35
Issue number	13
DOIs	https://doi.org/10.1002/adma.202206110
Publication status	Published - 29 Mar 2023

Funding

B.S. and A.R. contributed equally to this work. A.P.G.C. and P.R.F. acknowledge the funding from Fundação para a Ciência e Tecnologia (Portugal), through IDMEC, under LAETA project UIDB/50022/2020. T.H.V.P. acknowledges the funding from Fundação para a Ciência e Tecnologia (Portugal), through Ph.D. Grant 2020.04417.BD. A.S. acknowledges that this work was partially supported by the ATTRACT Investigator Grant (no. A17/MS/11572821/MBRACE, to A.S.) from the Luxembourg National Research Fund. The author thanks Gerardo Ceada for his help in the graphical representations. N.A.K. acknowledges support from the European Research Council (grant 851960) and the Gravitation Program “Materials Driven Regeneration,” funded by the Netherlands Organization for Scientific Research (024.003.013). M.B.A. acknowledges support from the French National Research Agency (grant ANR‐201‐8‐CE1‐3‐0008 for the project “Epimorph”). G.E.S.T. acknowledges funding by the Australian Research Council through project DP200102593. A.C. acknowledges the funding from the Deutsche Forschungsgemeinschaft (DFG) Emmy Noether Grant CI 203/‐2 1, the Spanish Ministry of Science and Innovation (PID2021‐123013O‐BI00) and the IKERBASQUE Basque Foundation for Science. B.S. and A.R. contributed equally to this work. A.P.G.C. and P.R.F. acknowledge the funding from Fundação para a Ciência e Tecnologia (Portugal), through IDMEC, under LAETA project UIDB/50022/2020. T.H.V.P. acknowledges the funding from Fundação para a Ciência e Tecnologia (Portugal), through Ph.D. Grant 2020.04417.BD. A.S. acknowledges that this work was partially supported by the ATTRACT Investigator Grant (no. A17/MS/11572821/MBRACE, to A.S.) from the Luxembourg National Research Fund. The author thanks Gerardo Ceada for his help in the graphical representations. N.A.K. acknowledges support from the European Research Council (grant 851960) and the Gravitation Program “Materials Driven Regeneration,” funded by the Netherlands Organization for Scientific Research (024.003.013). M.B.A. acknowledges support from the French National Research Agency (grant ANR-201-8-CE1-3-0008 for the project “Epimorph”). G.E.S.T. acknowledges funding by the Australian Research Council through project DP200102593. A.C. acknowledges the funding from the Deutsche Forschungsgemeinschaft (DFG) Emmy Noether Grant CI 203/-2 1, the Spanish Ministry of Science and Innovation (PID2021-123013O-BI00) and the IKERBASQUE Basque Foundation for Science.

Funders	Funder number
European Union's Horizon 2020 - Research and Innovation Framework Programme	851960
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	024.003.013

Keywords

biological systems
mechanotransduction
morphogenesis
surface curvature
Morphogenesis
Cell Membrane
Mechanical Phenomena

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Schamberger, B., Ziege, R., Anselme, K., Ben Amar, M., Bykowski, M., Castro, A. P. G., Cipitria, A., Coles, R. A., Dimova, R., Eder, M., Ehrig, S., Escudero, L. M., Evans, M. E., Fernandes, P. R., Fratzl, P., Geris, L., Gierlinger, N., Hannezo, E., Iglič, A., ... Dunlop, J. W. C. (2023). Curvature in Biological Systems: Its Quantification, Emergence, and Implications across the Scales. Advanced Materials, 35(13), Article 2206110. https://doi.org/10.1002/adma.202206110

@article{39eb45ad63434cf49ad95e929177d35d,

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

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, Morphogenesis, Cell Membrane, Mechanical Phenomena",

author = "Barbara Schamberger and Ricardo Ziege and Karine Anselme and \{Ben Amar\}, Martine and Micha{\l} Bykowski and Castro, \{Andr{\'e} P.G.\} and Amaia Cipitria and Coles, \{Rhoslyn A.\} and Rumiana Dimova and Michaela Eder and Sebastian Ehrig and Escudero, \{Luis M.\} and Evans, \{Myfanwy E.\} and Fernandes, \{Paulo R.\} and Peter Fratzl and Liesbet Geris and Notburga Gierlinger and Edouard Hannezo and Ale{\v s} Igli{\v c} and Kirkensgaard, \{Jacob J.K.\} and Philip Kollmannsberger and {\L}ucja Kowalewska and Kurniawan, \{Nicholas A.\} and Ioannis Papantoniou and Laurent Pieuchot and Pires, \{Tiago H.V.\} and Renner, \{Lars D.\} and Sageman-Furnas, \{Andrew O.\} and Schr{\"o}der-Turk, \{Gerd E.\} and Anupam Sengupta and Sharma, \{Vikas R.\} and Antonio Tagua and Caterina Tomba and Xavier Trepat and Waters, \{Sarah L.\} and Yeo, \{Edwina F.\} and Andreas Roschger and Bidan, \{C{\'e}cile M.\} and Dunlop, \{John W.C.\}",

note = "Publisher Copyright: {\textcopyright} 2023 The Authors. Advanced Materials published by Wiley-VCH GmbH.",

year = "2023",

month = mar,

day = "29",

doi = "10.1002/adma.202206110",

language = "English",

volume = "35",

journal = "Advanced Materials",

issn = "0935-9648",

publisher = "Wiley-Blackwell",

number = "13",

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Schamberger, B, Ziege, R, Anselme, K, Ben Amar, M, Bykowski, M, Castro, APG, Cipitria, A, Coles, RA, Dimova, R, Eder, M, Ehrig, S, Escudero, LM, Evans, ME, Fernandes, PR, Fratzl, P, Geris, L, Gierlinger, N, Hannezo, E, Iglič, A, Kirkensgaard, JJK, Kollmannsberger, P, Kowalewska, Ł, Kurniawan, NA, Papantoniou, I, Pieuchot, L, Pires, THV, Renner, LD, Sageman-Furnas, AO, Schröder-Turk, GE, Sengupta, A, Sharma, VR, Tagua, A, Tomba, C, Trepat, X, Waters, SL, Yeo, EF, Roschger, A, Bidan, CM & Dunlop, JWC 2023, 'Curvature in Biological Systems: Its Quantification, Emergence, and Implications across the Scales', Advanced Materials, vol. 35, no. 13, 2206110. https://doi.org/10.1002/adma.202206110

TY - JOUR

T1 - Curvature in Biological Systems

T2 - Its Quantification, Emergence, and Implications across the Scales

AU - Schamberger, Barbara

AU - Ziege, Ricardo

AU - Anselme, Karine

AU - Ben Amar, Martine

AU - Bykowski, Michał

AU - Castro, André P.G.

AU - Cipitria, Amaia

AU - Coles, Rhoslyn A.

AU - Dimova, Rumiana

AU - Eder, Michaela

AU - Ehrig, Sebastian

AU - Escudero, Luis M.

AU - Evans, Myfanwy E.

AU - Fernandes, Paulo R.

AU - Fratzl, Peter

AU - Geris, Liesbet

AU - Gierlinger, Notburga

AU - Hannezo, Edouard

AU - Iglič, Aleš

AU - Kirkensgaard, Jacob J.K.

AU - Kollmannsberger, Philip

AU - Kowalewska, Łucja

AU - Kurniawan, Nicholas A.

AU - Papantoniou, Ioannis

AU - Pieuchot, Laurent

AU - Pires, Tiago H.V.

AU - Renner, Lars D.

AU - Sageman-Furnas, Andrew O.

AU - Schröder-Turk, Gerd E.

AU - Sengupta, Anupam

AU - Sharma, Vikas R.

AU - Tagua, Antonio

AU - Tomba, Caterina

AU - Trepat, Xavier

AU - Waters, Sarah L.

AU - Yeo, Edwina F.

AU - Roschger, Andreas

AU - Bidan, Cécile M.

AU - Dunlop, John W.C.

PY - 2023/3/29

Y1 - 2023/3/29

N2 - 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.

AB - 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.

KW - biological systems

KW - mechanotransduction

KW - morphogenesis

KW - surface curvature

KW - Morphogenesis

KW - Cell Membrane

KW - Mechanical Phenomena

UR - https://www.scopus.com/pages/publications/85148379457

U2 - 10.1002/adma.202206110

DO - 10.1002/adma.202206110

M3 - Review article

C2 - 36461812

AN - SCOPUS:85148379457

SN - 0935-9648

VL - 35

JO - Advanced Materials

JF - Advanced Materials

IS - 13

M1 - 2206110

ER -

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

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