journal article·2023-03Open access

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

Advanced Materials· Volume 35· Issue 13

Abstract

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.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Advanced Materials and Mechanics · Cellular Mechanics and Interactions · Micro and Nano Robotics

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of the Chemistry and Physics of Materials Paris‐Lodron University of Salzburg 5020 Salzburg Austria

Department of Biomaterials Max Planck Institute of Colloids and Interfaces 14476 Potsdam Germany

IS2M (CNRS ‐ UMR 7361) Université de Haute‐Alsace F‐68100 Mulhouse France

Université de Strasbourg F‐67081 Strasbourg France

Department of Physics Laboratoire de Physique de l'Ecole Normale Supérieure 24 rue Lhomond 75005 Paris France

Department of Plant Anatomy and Cytology Faculty of Biology University of Warsaw 02‐096 Warsaw Poland

IDMEC Instituto Superior Técnico Universidade de Lisboa 1049‐001 Lisboa Portugal

ESTS Instituto Politécnico de Setúbal 2914‐761 Setúbal Portugal

Group of Bioengineering in Regeneration and Cancer Biodonostia Health Research Institute 20014 San Sebastian Spain

IKERBASQUE Basque Foundation for Science 48009 Bilbao Spain

Cluster of Excellence, Matters of Activity Humboldt‐Universität zu Berlin 10178 Berlin Germany

Department of Theory and Bio‐Systems Max Planck Institute of Colloids and Interfaces 14476 Potsdam Germany

Max Delbrück Center for Molecular Medicine 13125 Berlin Germany

Berlin Institute for Medical Systems Biology 10115 Berlin Germany

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

Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED) 28031 Madrid Spain

Institute for Mathematics University of Potsdam 14476 Potsdam Germany

Biomechanics Research Unit GIGA In Silico Medicine University of Liège 4000 Liège Belgium

Institute of Biophysics Department of Nanobiotechnology University of Natural Resources and Life Sciences Vienna (Boku) 1190 Vienna Austria

Institute of Science and Technology Austria 3400 Klosterneuburg Austria

Laboratory of Physics Faculty of Electrical engineering University of Ljubljana Tržaška 25 SI‐1000 Ljubljana Slovenia

Condensed Matter Physics Niels Bohr Institute University of Copenhagen Universitetsparken 5 2100 København Ø Denmark

Ingredients and Dairy Technology Department of Food Science University of Copenhagen Rolighedsvej 26 1958 Frederiksberg Denmark

Center for Computational and Theoretical Biology University of Würzburg 97074 Würzburg Germany

Department of Biomedical Engineering and Institute for Complex Molecular Systems Eindhoven University of Technology 5600 MB Eindhoven The Netherlands

Funding

European Research Council · Agence Nationale de la Recherche · Australian Research Council · Ministerio de Ciencia e Innovación

References (100+)

Show source-provided references
1. 10.1002/adhm.20170115410.1002/adhm.201701154 ↗
2. 10.1016/j.pbiomolbio.2014.06.00910.1016/j.pbiomolbio.2014.06.009 ↗
3. 10.1146/annurev-matsci-062910-10040710.1146/annurev-matsci-062910-100407 ↗
4. 10.1017/CBO978110732585210.1017/CBO9781107325852 ↗
5. 10.1002/adbi.20190008010.1002/adbi.201900080 ↗
6. 10.1038/s41467-018-06494-610.1038/s41467-018-06494-6 ↗
7. 10.1016/j.bpj.2018.01.03910.1016/j.bpj.2018.01.039 ↗
8. 10.1126/sciadv.aao488110.1126/sciadv.aao4881 ↗
9. 10.1038/s41567-021-01374-110.1038/s41567-021-01374-1 ↗
10. 10.1083/jcb.20160400310.1083/jcb.201604003 ↗
11. Hyde S. · 1997
12. 10.1103/RevModPhys.74.95310.1103/RevModPhys.74.953 ↗
13. 10.1098/rsob.19015510.1098/rsob.190155 ↗
14. 10.1016/j.tibtech.2019.01.00610.1016/j.tibtech.2019.01.006 ↗
15. 10.1016/j.biomaterials.2019.11973910.1016/j.biomaterials.2019.119739 ↗
16. 10.1039/c2sm00011c10.1039/c2sm00011c ↗
17. 10.1016/j.actbio.2021.06.01310.1016/j.actbio.2021.06.013 ↗
18. 10.1109/TVCG.2018.286100710.1109/TVCG.2018.2861007 ↗
19. 10.1088/1367-2630/15/8/08302810.1088/1367-2630/15/8/083028 ↗
20. 10.7554/eLife.0586410.7554/eLife.05864 ↗
21. 10.1093/plphys/kiab47610.1093/plphys/kiab476 ↗
22. 10.1146/annurev-neuro-070918-05050910.1146/annurev-neuro-070918-050509 ↗
23. 10.1242/jcs.02382010.1242/jcs.023820 ↗
24. a)K.Crane CS 15‐458/858: Discrete Differential Geometry https://brickisland.net/DDGSpring2019/2019/03/13/steiner-formula-for-surfaces-in-mathbbr3/(accessed: March 2022).
25. 10.1088/1361-6463/aacb9810.1088/1361-6463/aacb98 ↗
26. Tanford C. · 1973
27. Israelachvili J. N. · J. Chem. Soc. · 1976 · 72 · 1525
28. 10.1016/S1937-6448(08)02006-610.1016/S1937-6448(08)02006-6 ↗
29. Evans M. E. · Mitt. Dtsch. Math.‐Ver. · 2014 · 22 · 158
30. do Carmo M. P. · 2016
31. 10.1103/RevModPhys.82.130110.1103/RevModPhys.82.1301 ↗
32. 10.1039/c3sm90111d10.1039/c3sm90111d ↗
33. 10.1038/nphys192010.1038/nphys1920 ↗
34. 10.1038/nature2171810.1038/nature21718 ↗
35. 10.3389/fphy.2020.0018410.3389/fphy.2020.00184 ↗
36. 10.1038/s41563-022-01194-510.1038/s41563-022-01194-5 ↗
37. Kralj‐Iglič V. · Eur. Phys. J. E.: Soft Matter Biol. Phys. · 1999 · 10 · 5
38. Crane K.
39. 10.1017/S096249291300005610.1017/S0962492913000056 ↗
40. Bobenko A. I. · 2008
41. 10.1007/978-3-030-31351-710.1007/978-3-030-31351-7 ↗
42. Sensen C. W. · 2008
43. 10.1007/BFb008450910.1007/BFb0084509 ↗
44. S.Rusinkiewicz trimesh2 https://gfx.cs.princeton.edu/proj/trimesh2/(accessed: March 2020).
45. 10.1145/1276377.127644710.1145/1276377.1276447 ↗
46. 10.1145/2185520.218558110.1145/2185520.2185581 ↗
47. 10.1038/s41592-019-0539-z10.1038/s41592-019-0539-z ↗
48. 10.1006/cviu.1995.101410.1006/cviu.1995.1014 ↗
49. 10.1016/0262-8856(91)90025-K10.1016/0262-8856(91)90025-K ↗
50. 10.1073/pnas.191783811710.1073/pnas.1917838117 ↗
51. 10.1016/j.bpj.2017.11.01510.1016/j.bpj.2017.11.015 ↗
52. 10.1016/j.cag.2019.11.00310.1016/j.cag.2019.11.003 ↗
53. 10.1073/pnas.172232011510.1073/pnas.1722320115 ↗
54. 10.1038/nature0439610.1038/nature04396 ↗
55. 10.1080/09500839.2018.155280610.1080/09500839.2018.1552806 ↗
56. 10.1002/advs.20190064410.1002/advs.201900644 ↗
57. 10.1016/j.celrep.2021.10971510.1016/j.celrep.2021.109715 ↗
58. 10.1038/419579a10.1038/419579a ↗
59. 10.1038/ncomms133610.1038/ncomms1336 ↗
60. 10.1126/science.123884210.1126/science.1238842 ↗
61. 10.1073/pnas.121739111010.1073/pnas.1217391110 ↗
62. 10.1063/1.274393910.1063/1.2743939 ↗
63. 10.1203/PDR.0b013e3181a291d910.1203/PDR.0b013e3181a291d9 ↗
64. 10.1007/s10237-015-0662-410.1007/s10237-015-0662-4 ↗
65. 10.1038/s41586-021-04125-710.1038/s41586-021-04125-7 ↗
66. Laplace P. S. · 1805
67. 10.1038/scientificamerican0776-8210.1038/scientificamerican0776-82 ↗
68. 10.1038/349475a010.1038/349475a0 ↗
69. 10.1016/j.tplants.2010.04.00210.1016/j.tplants.2010.04.002 ↗
70. 10.1126/science.120387410.1126/science.1203874 ↗
71. 10.1007/978-3-319-25979-6_210.1007/978-3-319-25979-6_2 ↗
72. 10.1016/S0006-3495(96)79790-410.1016/S0006-3495(96)79790-4 ↗
73. 10.1051/jphys:0198600470406830010.1051/jphys:01986004704068300 ↗
74. 10.1201/978131515251610.1201/9781315152516 ↗
75. 10.1039/D0SM00499E10.1039/D0SM00499E ↗
76. 10.1083/jcb.20060305510.1083/jcb.200603055 ↗
77. 10.1073/pnas.131634811110.1073/pnas.1316348111 ↗
78. 10.1007/s40843-019-1261-110.1007/s40843-019-1261-1 ↗
79. 10.1007/BF0124813310.1007/BF01248133 ↗
80. 10.1105/tpc.15.0105310.1105/tpc.15.01053 ↗
81. 10.1038/nrm178410.1038/nrm1784 ↗
82. 10.1098/rsif.2008.0372.focus10.1098/rsif.2008.0372.focus ↗
83. 10.1002/jmor.105202010610.1002/jmor.1052020106 ↗
84. 10.1073/pnas.090961610710.1073/pnas.0909616107 ↗
85. 10.1098/rsif.2007.106510.1098/rsif.2007.1065 ↗
86. 10.1016/j.jsb.2011.01.00410.1016/j.jsb.2011.01.004 ↗
87. 10.1016/j.matpr.2014.09.02310.1016/j.matpr.2014.09.023 ↗
88. 10.1039/D0FD00108B10.1039/D0FD00108B ↗
89. 10.1080/10586458.1997.1050434910.1080/10586458.1997.10504349 ↗
90. 10.1083/jcb.20091009910.1083/jcb.200910099 ↗
91. 10.1242/dev.112.3.77510.1242/dev.112.3.775 ↗
92. 10.1242/dev.06786810.1242/dev.067868 ↗
93. 10.1038/s41556-021-00699-610.1038/s41556-021-00699-6 ↗
94. 10.7554/eLife.2268910.7554/eLife.22689 ↗
95. 10.1038/s41467-018-06497-310.1038/s41467-018-06497-3 ↗
96. 10.1016/j.cub.2010.06.07510.1016/j.cub.2010.06.075 ↗
97. 10.1016/j.cub.2021.03.03110.1016/j.cub.2021.03.031 ↗
98. 10.1115/1.403212810.1115/1.4032128 ↗
99. 10.1038/srep0888710.1038/srep08887 ↗
100. 10.1071/FP1105710.1071/FP11057 ↗