Image-based parameter inference for epithelial mechanics

1.

Lenne P-F, Munro E, Heemskerk I, Warmflash A, Bocanegra-Moreno L, Kishi K, et al. Roadmap for the

multiscale coupling of biochemical and mechanical signals during development. Phys Biol. 2021; 18:

041501. https://doi.org/10.1088/1478-3975/abd0db PMID: 33276350

2.

Chu C-W, Masak G, Yang J, Davidson LA. From biomechanics to mechanobiology: Xenopus provides

direct access to the physical principles that shape the embryo. Curr Opin Genet Dev. 2020; 63: 71–77.

https://doi.org/10.1016/j.gde.2020.05.011 PMID: 32563783

3.

Paci G, Mao Y. Forced into shape: Mechanical forces in Drosophila development and homeostasis.

Semin Cell Dev Biol. 2021. https://doi.org/10.1016/j.semcdb.2021.05.026 PMID: 34092509

4.

Chan CJ, Heisenberg C-P, Hiiragi T. Coordination of Morphogenesis and Cell-Fate Specification in

Development. Curr Biol. 2017; 27: R1024–R1035. https://doi.org/10.1016/j.cub.2017.07.010 PMID:

28950087

5.

Trinh D-C, Alonso-Serra J, Asaoka M, Colin L, Cortes M, Malivert A, et al. How Mechanical Forces

Shape Plant Organs. Curr Biol. 2021; 31: R143–R159. https://doi.org/10.1016/j.cub.2020.12.001

PMID: 33561417

6.

Davidson L, von Dassow M, Zhou J. Multi-scale mechanics from molecules to morphogenesis. Int J Biochem Cell Biol. 2009; 41: 2147–2162. https://doi.org/10.1016/j.biocel.2009.04.015 PMID: 19394436

7.

Petridou NI, Heisenberg C-P. Tissue rheology in embryonic organization. EMBO J. 2019; 38: e102497.

https://doi.org/10.15252/embj.2019102497 PMID: 31512749

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010209 June 23, 2022

21 / 24

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

PLOS COMPUTATIONAL BIOLOGY

Inferring mechanical parameters from image data

8.

Davidson LA. Chapter seven—Embryo Mechanics: Balancing Force Production with Elastic Resistance

During Morphogenesis. In: Labouesse M, editor. Current Topics in Developmental Biology. Academic

Press; 2011. pp. 215–241. https://doi.org/10.1016/B978-0-12-385065-2.00007-4

9.

Wagh K, Ishikawa M, Garcia DA, Stavreva DA, Upadhyaya A, Hager GL. Mechanical Regulation of

Transcription: Recent Advances. Trends Cell Biol. 2021; 31: 457–472. https://doi.org/10.1016/j.tcb.

2021.02.008 PMID: 33712293

10.

Aw WY, Devenport D. Planar cell polarity: global inputs establishing cellular asymmetry. Curr Opin Cell

Biol. 2017; 44: 110–116. https://doi.org/10.1016/j.ceb.2016.08.002 PMID: 27576155

11.

Sugimura K, Lenne P-F, Graner F. Measuring forces and stresses in situ in living tissues. Development.

2016; 143: 186–196. https://doi.org/10.1242/dev.119776 PMID: 26786209

12.

Roca-Cusachs P, Conte V, Trepat X. Quantifying forces in cell biology. Nat Cell Biol. 2017; 19: 742–

751. https://doi.org/10.1038/ncb3564 PMID: 28628082

13.

Go´mez-Gonza´lez M, Latorre E, Arroyo M, Trepat X. Measuring mechanical stress in living tissues. Nat

Rev Phys. 2020; 2: 300–317. https://doi.org/10.1038/s42254-020-0184-6

14.

Fischer LS, Rangarajan S, Sadhanasatish T, Grashoff C. Molecular Force Measurement with Tension

Sensors. Annu Rev Biophys. 2021; 50: 595–616. https://doi.org/10.1146/annurev-biophys-101920064756 PMID: 33710908

15.

Rauzi M, Verant P, Lecuit T, Lenne P-F. Nature and anisotropy of cortical forces orienting Drosophila

tissue morphogenesis. Nat Cell Biol. 2008; 10: 1401–1410. https://doi.org/10.1038/ncb1798 PMID:

18978783

16.

Bosveld F, Bonnet I, Guirao B, Tlili S, Wang Z, Petitalot A, et al. Mechanical Control of Morphogenesis

by Fat/Dachsous/Four-Jointed Planar Cell Polarity Pathway. Science. 2012; 336: 724–727. https://doi.

org/10.1126/science.1221071 PMID: 22499807

17.

Lau K, Tao H, Liu H, Wen J, Sturgeon K, Sorfazlian N, et al. Anisotropic stress orients remodelling of

mammalian limb bud ectoderm. Nat Cell Biol. 2015; 17: 569–579. https://doi.org/10.1038/ncb3156

PMID: 25893915

18.

Bambardekar K, Cle´ment R, Blanc O, Chardès C, Lenne P-F. Direct laser manipulation reveals the

mechanics of cell contacts in vivo. Proc Natl Acad Sci USA. 2015; 112: 1416–1421. https://doi.org/10.

1073/pnas.1418732112 PMID: 25605934

19.

Kong W, Loison O, Chavadimane Shivakumar P, Chan EH, Saadaoui M, Collinet C, et al. Experimental

validation of force inference in epithelia from cell to tissue scale. Sci Rep. 2019; 9: 14647. https://doi.

org/10.1038/s41598-019-50690-3 PMID: 31601854

20.

Davidson L, Keller R. Measuring Mechanical Properties of Embryos and Embryonic Tissues. Methods

in Cell Biology. Academic Press; 2007. pp. 425–439. https://doi.org/10.1016/S0091-679X(07)83018-4

21.

Asaoka Y, Morita H, Furumoto H, Heisenberg C-P, Furutani-Seiki M. Studying YAP-Mediated 3D Morphogenesis Using Fish Embryos and Human Spheroids. In: Hergovich A, editor. The Hippo Pathway:

Methods and Protocols. New York, NY: Springer; 2019. pp. 167–181. https://doi.org/10.1007/978-14939-8910-2_14

22.

Cle´ment R, Dehapiot B, Collinet C, Lecuit T, Lenne P-F. Viscoelastic Dissipation Stabilizes Cell Shape

Changes during Tissue Morphogenesis. Curr Biol. 2017; 27: 3132–3142.e4. https://doi.org/10.1016/j.

cub.2017.09.005 PMID: 28988857

23.

Serwane F, Mongera A, Rowghanian P, Kealhofer DA, Lucio AA, Hockenbery ZM, et al. In vivo quantification of spatially varying mechanical properties in developing tissues. Nat Methods. 2017; 14: 181–

186. https://doi.org/10.1038/nmeth.4101 PMID: 27918540

24.

Prevedel R, Diz-Muñoz A, Ruocco G, Antonacci G. Brillouin microscopy: an emerging tool for mechanobiology. Nat Methods. 2019; 16: 969–977. https://doi.org/10.1038/s41592-019-0543-3 PMID:

31548707

25.

Fletcher AG, Cooper F, Baker RE. Mechanocellular models of epithelial morphogenesis. Philos Trans

R Soc B: Biol Sci. 2017; 372: 20150519. https://doi.org/10.1098/rstb.2015.0519 PMID: 28348253

26.

Loerke D, Blankenship JT. Viscoelastic voyages–Biophysical perspectives on cell intercalation during

Drosophila gastrulation. Semin Cell Dev Biol. 2019. https://doi.org/10.1016/j.semcdb.2019.11.005

PMID: 31784092

27.

Taber LA. Continuum Modeling in Mechanobiology. Springer International Publishing; 2020. https://doi.

org/10.1007/978-3-030-43209-6

28.

Honda H. Geometrical Models for Cells in Tissues. In: Bourne GH, Danielli JF, Jeon KW, editors. International Review of Cytology. Academic Press; 1983. pp. 191–248. https://doi.org/10.1016/S0074-7696

(08)62339-6

29.

Fletcher AG, Osterfield M, Baker RE, Shvartsman SY. Vertex Models of Epithelial Morphogenesis. Biophys J. 2014; 106: 2291–2304. https://doi.org/10.1016/j.bpj.2013.11.4498 PMID: 24896108

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010209 June 23, 2022

22 / 24

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

PLOS COMPUTATIONAL BIOLOGY

Inferring mechanical parameters from image data

30.

Alt S, Ganguly P, Salbreux G. Vertex models: from cell mechanics to tissue morphogenesis. Philos

Trans R Soc B: Biol Sci. 2017; 372: 20150520. https://doi.org/10.1098/rstb.2015.0520 PMID: 28348254

31.

Farhadifar R, Ro¨per J-C, Aigouy B, Eaton S, Ju¨licher F. The Influence of Cell Mechanics, Cell-Cell Interactions, and Proliferation on Epithelial Packing. Curr Biol. 2007; 17: 2095–2104. https://doi.org/10.

1016/j.cub.2007.11.049 PMID: 18082406

32.

Canela-Xandri O, Sague´s F, Casademunt J, Buceta J. Dynamics and Mechanical Stability of the Developing Dorsoventral Organizer of the Wing Imaginal Disc. PLoS Comput Biol. 2011; 7: e1002153.

https://doi.org/10.1371/journal.pcbi.1002153 PMID: 21980267

33.

Mao Y, Tournier AL, Bates PA, Gale JE, Tapon N, Thompson BJ. Planar polarization of the atypical

myosin Dachs orients cell divisions in Drosophila. Genes Dev. 2011; 25: 131–136. https://doi.org/10.

1101/gad.610511 PMID: 21245166

34.

Nestor-Bergmann A, Goddard G, Woolner S, Jensen OE. Relating cell shape and mechanical stress in

a spatially disordered epithelium using a vertex-based model. Math. Med. Biol.: A Journal of the IMA.

2018; 35: i1–i27. https://doi.org/10.1093/imammb/dqx008 PMID: 28992197

35.

Kursawe J, Baker RE, Fletcher AG. Approximate Bayesian computation reveals the importance of

repeated measurements for parameterising cell-based models of growing tissues. J Theor Biol. 2018;

443: 66–81. https://doi.org/10.1016/j.jtbi.2018.01.020 PMID: 29391171

36.

Ishihara S, Sugimura K. Bayesian inference of force dynamics during morphogenesis. J Theor Biol.

2012; 313: 201–211. https://doi.org/10.1016/j.jtbi.2012.08.017 PMID: 22939902

37.

Rauzi M, Lenne P-F, Lecuit T. Planar polarized actomyosin contractile flows control epithelial junction

remodelling. Nature. 2010; 468: 1110–1114. https://doi.org/10.1038/nature09566 PMID: 21068726

38.

Bardet P-L, Guirao B, Paoletti C, Serman F, Le´opold V, Bosveld F, et al. PTEN Controls Junction

Lengthening and Stability during Cell Rearrangement in Epithelial Tissue. Dev Cell. 2013; 25: 534–546.

https://doi.org/10.1016/j.devcel.2013.04.020 PMID: 23707736

39.

Tetley RJ, Blanchard GB, Fletcher AG, Adams RJ, Sanson B. Unipolar distributions of junctional Myosin

II identify cell stripe boundaries that drive cell intercalation throughout Drosophila axis extension. eLife.

2016; 5: e12094. https://doi.org/10.7554/eLife.12094 PMID: 27183005

40.

Lan H, Wang Q, Fernandez-Gonzalez R, Feng JJ. A biomechanical model for cell polarization and intercalation during Drosophila germband extension. Phys Biol. 2015; 12: 056011. https://doi.org/10.1088/

1478-3975/12/5/056011 PMID: 26356256

41.

Siang LC, Fernandez-Gonzalez R, Feng JJ. Modeling cell intercalation during Drosophila germband

extension. Phys Biol. 2018; 15: 066008. https://doi.org/10.1088/1478-3975/aad865 PMID: 30080681

42.

Akaike H. Information theory and an extension of the maximum likelihood principle. 2nd International

Symposium on Information Theory; 1973; Akademiai Kiado, Budapest.

43.

Kirk P, Thorne T, Stumpf MP. Model selection in systems and synthetic biology. Curr Opin Biotechnol.

2013; 24: 767–774. https://doi.org/10.1016/j.copbio.2013.03.012 PMID: 23578462

44.

Hiraiwa T, Wen F-L, Shibata T, Kuranaga E. Mathematical Modeling of Tissue Folding and Asymmetric

Tissue Flow during Epithelial Morphogenesis. Symmetry. 2019; 11: 113. https://doi.org/10.3390/

sym11010113

45.

Aigouy B, Farhadifar R, Staple DB, Sagner A, Ro¨per J-C, Ju¨licher F, et al. Cell Flow Reorients the Axis

of Planar Polarity in the Wing Epithelium of Drosophila. Cell. 2010; 142: 773–786. https://doi.org/10.

1016/j.cell.2010.07.042 PMID: 20813263

46.

Sugimura K, Ishihara S. The mechanical anisotropy in a tissue promotes ordering in hexagonal cell

packing. Development. 2013; 140: 4091–4101. https://doi.org/10.1242/dev.094060 PMID: 24046322

47.

Matamoro-Vidal A, Salazar-Ciudad I, Houle D. Making quantitative morphological variation from basic

developmental processes: Where are we? The case of the Drosophila wing. Dev Dyn. 2015; 244:

1058–1073. https://doi.org/10.1002/dvdy.24255 PMID: 25619644

48.

Etournay R, Popović M, Merkel M, Nandi A, Blasse C, Aigouy B, et al. Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing. eLife. 2015; 4: e07090. https://doi.

org/10.7554/eLife.07090 PMID: 26102528

49.

Ray RP, Matamoro-Vidal A, Ribeiro PS, Tapon N, Houle D, Salazar-Ciudad I, et al. Patterned Anchorage to the Apical Extracellular Matrix Defines Tissue Shape in the Developing Appendages of Drosophila. Dev Cell. 2015; 34: 310–322. https://doi.org/10.1016/j.devcel.2015.06.019 PMID: 26190146

50.

Guirao B, Rigaud SU, Bosveld F, Bailles A, Lo´pez-Gay J, Ishihara S, et al. Unified quantitative characterization of epithelial tissue development. eLife. 2015; 4. https://doi.org/10.7554/eLife.08519 PMID:

26653285

51.

Ishihara S, Sugimura K, Cox SJ, Bonnet I, Bellaïche Y, Graner F. Comparative study of non-invasive

force and stress inference methods in tissue. Eur Phys J E. 2013; 36. https://doi.org/10.1140/epje/

i2013-13045-8 PMID: 23615875

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010209 June 23, 2022

23 / 24

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

PLOS COMPUTATIONAL BIOLOGY

Inferring mechanical parameters from image data

52.

Bertet C, Sulak L, Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation

and axis elongation. Nature. 2004; 429: 667–671. https://doi.org/10.1038/nature02590 PMID:

15190355

53.

Zallen JA, Wieschaus E. Patterned Gene Expression Directs Bipolar Planar Polarity in Drosophila. Dev

Cell. 2004; 6: 343–355. https://doi.org/10.1016/s1534-5807(04)00060-7 PMID: 15030758

54.

Pare´ AC, Vichas A, Fincher CT, Mirman Z, Farrell DL, Mainieri A, et al. A positional Toll receptor code

directs convergent extension in Drosophila. Nature. 2014; 515: 523–527. https://doi.org/10.1038/

nature13953 PMID: 25363762

55.

Agarwal P, Zaidel-Bar R. Principles of Actomyosin Regulation In Vivo. Trends Cell Biol. 2019; 29: 150–

163. https://doi.org/10.1016/j.tcb.2018.09.006 PMID: 30385150

56.

Perez-Vale KZ, Peifer M. Orchestrating morphogenesis: building the body plan by cell shape changes

and movements. Development. 2020; 147. https://doi.org/10.1242/dev.191049 PMID: 32917667

57.

Irvine KD, Wieschaus E. Cell intercalation during Drosophila germband extension and its regulation by

pair-rule segmentation genes. Development. 1994; 120: 827–841. https://doi.org/10.1242/dev.120.4.

827 PMID: 7600960

58.

Farrell DL, Weitz O, Magnasco MO, Zallen JA. SEGGA: a toolset for rapid automated analysis of epithelial cell polarity and dynamics. Development. 2017; 144: 1725–1734. https://doi.org/10.1242/dev.

146837 PMID: 28465336

59.

Samprit C, Ali SH. Analysis of Collinear Data. Regression Analysis by Example. John Wiley & Sons,

Ltd; 2006. pp. 221–258. https://doi.org/10.1002/0470055464.ch9

60.

Royle JA, Dorazio RM. Hierarchical Modeling and Inference in Ecology: The Analysis of Data from Populations, Metapopulations and Communities. Elsevier; 2008.

61.

Mishra N, Heisenberg C-P. Dissecting Organismal Morphogenesis by Bridging Genetics and Biophysics. Annu Rev Genet. 2021; 55: 209–233 https://doi.org/10.1146/annurev-genet-071819-103748 PMID:

34460295

62.

Sugimura K, Bellaïche Y, Graner F, Marcq P, Ishihara S. Robustness of force and stress inference in an

epithelial tissue. 2013 35th Annual International Conference of the IEEE Engineering in Medicine and

Biology Society (EMBC). 2013. pp. 2712–2715. https://doi.org/10.1109/EMBC.2013.6610100

63.

Chiou KK, Hufnagel L, Shraiman BI. Mechanical Stress Inference for Two Dimensional Cell Arrays.

PLoS Comput. Biol. 2012; 8: e1002512. https://doi.org/10.1371/journal.pcbi.1002512 PMID: 22615550

64.

Noll N, Streichan SJ, Shraiman BI. Variational Method for Image-Based Inference of Internal Stress in

Epithelial Tissues. Phys Rev X. 2020; 10: 011072. https://doi.org/10.1103/physrevx.10.011072 PMID:

33767909

65.

Staple DB, Farhadifar R, Ro¨per J-C, Aigouy B, Eaton S, Ju¨licher F. Mechanics and remodelling of cell

packings in epithelia. Eur Phys J E. 2010; 33: 117–127. https://doi.org/10.1140/epje/i2010-10677-0

PMID: 21082210

66.

Royou A, Field C, Sisson JC, Sullivan W, Karess R. Reassessing the Role and Dynamics of Nonmuscle

Myosin II during Furrow Formation in Early Drosophila Embryos. Mol Biol Cell. 2004; 15: 838–850.

https://doi.org/10.1091/mbc.e03-06-0440 PMID: 14657248

67.

Huang J, Zhou W, Dong W, Watson AM, Hong Y. Directed, efficient, and versatile modifications of the

Drosophila genome by genomic engineering. Proc Natl Acad Sci USA. 2009; 106: 8284–8289. https://

doi.org/10.1073/pnas.0900641106

68.

Gergen JP, Butler BA. Isolation of the Drosophila segmentation gene runt and analysis of its expression

during embryogenesis. Genes Dev. 1988; 2: 1179–1193. https://doi.org/10.1101/gad.2.9.1179 PMID:

2847961

69.

Ikawa K, Sugimura K. AIP1 and cofilin ensure a resistance to tissue tension and promote directional cell

rearrangement. Nat Commun. 2018; 9. https://doi.org/10.1038/s41467-018-05605-7 PMID: 30202062

70.

Koto A, Kuranaga E, Miura M. Temporal regulation of Drosophila IAP1 determines caspase functions in

sensory organ development. J Cell Biol. 2009; 187: 219–231. https://doi.org/10.1083/jcb.200905110

PMID: 19822670

71.

Kondo T, Hayashi S. Mitotic cell rounding accelerates epithelial invagination. Nature. 2013; 494: 125–

129. https://doi.org/10.1038/nature11792 PMID: 23334416

72.

Aigouy B, Cortes C, Liu S, Prud’Homme B. EPySeg: a coding-free solution for automated segmentation

of epithelia using deep learning. Development. 2020; 147. https://doi.org/10.1242/dev.194589 PMID:

33268451

73.

Lordereau O. Les mousses bidimensionnelles: de la caracte´risation à la rhe´ologie des mate´riaux he´te´rogènes. These de doctorat, Rennes 1. 2002. Available from: https://www.theses.fr/2002REN10048

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010209 June 23, 2022

24 / 24

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