Spatiotemporal remodeling of extracellular matrix orients epithelial sheet folding

23. K. V. Iyer, R. Piscitello-Gómez, J. Paijmans, F. Jülicher, S. Eaton, Epithelial viscoelasticity is

regulated by mechanosensitive E-cadherin turnover. Curr. Biol. 29, 578–591.e5 (2019).

24. J. A. Croker, S. L. Ziegenhorn, R. A. Holmgren, Regulation of the Drosophila transcription

factor, Cubitus interruptus, by two conserved domains. Dev. Biol. 291, 368–381 (2006).

26. A. Proag, B. Monier, M. Suzanne, Physical and functional cell-matrix uncoupling in a developing tissue under tension. Development 146, dev172577 (2019).

27. M. A. Sturtevant, E. Bier, Analysis of the genetic hierarchy guiding wing vein development

in Drosophila. Development 121, 785–801 (1995).

REFERENCES AND NOTES

1. C. M. Nelson, On buckling morphogenesis. J. Biomech. Eng. 138, 021005 (2016).

2. C. Collinet, T. Lecuit, Programmed and self-organized flow of information during morphogenesis. Nat. Rev. Mol. Cell Biol. 22, 245–265 (2021).

3. C. H. Waddington, The genetic control of wing development in Drosophila. J. Genet. 41,

75–113 (1940).

4. D. Fristrom, M. Wilcox, J. Fristrom, The distribution of PS integrins, laminin A and F-actin

during key stages in Drosophila wing development. Development 117, 509–523 (1993).

5. F. Roch, C. R. Alonso, M. Akam, Drosophila miniature and dusky encode ZP proteins required for cytoskeletal reorganisation during wing morphogenesis. J. Cell Sci. 116,

1199–1207 (2003).

6. M. C. Diaz de la Loza, B. J. Thompson, Forces shaping the Drosophila wing. Mech. Dev. 144,

23–32 (2017).

7. T. Lecuit, P.-F. Lenne, Cell surface mechanics and the control of cell shape, tissue patterns

and morphogenesis. Nat. Rev. Mol. Cell Biol. 8, 633–644 (2007).

8. C.-P. Heisenberg, Y. Bellaïche, Forces in tissue morphogenesis and patterning. Cell 153,

948–962 (2013).

9. E. Caussinus, O. Kanca, M. Affolter, Fluorescent fusion protein knockout mediated by antiGFP nanobody. Nat. Struct. Mol. Biol. 19, 117–121 (2012).

10. R. P. Ray, A. Matamoro-Vidal, P. S. Ribeiro, N. Tapon, D. Houle, I. Salazar-Ciudad,

B. J. Thompson, Patterned anchorage to the apical extracellular matrix defines tissue shape

in the developing appendages of Drosophila. Dev. Cell 34, 310–322 (2015).

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

functions in sensory organ development. J. Cell Biol. 187, 219–231 (2009).

29. A. Tsuboi, S. Ohsawa, D. Umetsu, Y. Sando, E. Kuranaga, T. Igaki, K. Fujimoto, Competition

for space is controlled by apoptosis-induced change of local epithelial topology. Curr. Biol.

28, 2115–2128.e5 (2018).

30. W. Draper, J. Liphardt, Origins of chemoreceptor curvature sorting in Escherichia coli. Nat.

Commun. 8, 14838 (2017).

31. T. Kondo, S. Hayashi, Mitotic cell rounding accelerates epithelial invagination. Nature 494,

125–129 (2013).

32. J. Bischof, R. K. Maeda, M. Hediger, F. Karch, K. Basler, An optimized transgenesis system for

Drosophila using germ-line-specific ϕC31 integrases. Proc. Natl. Acad. Sci. U.S.A. 104,

3312–3317 (2007).

33. K. J. T. T. Venken, Y. He, R. A. Hoskins, H. J. Bellen, P[acman]: A BAC transgenic platform for

targeted insertion of large DNA fragments in D. melanogaster. Science 314,

1747–1751 (2006).

34. B. Aigouy, D. Umetsu, S. Eaton, Segmentation and Quantitative Analysis of Epithelial

Tissues, in Methods in molecular biology (2016); http://link.springer.com/10.1007/978-14939-6371-3_13, pp. 227–239.

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

segmentation of epithelia using deep learning. Development 147, dev194589 (2020).

36. S. E. McGuire, P. T. Le, A. J. Osborn, K. Matsumoto, R. L. Davis, Spatiotemporal rescue of

memory dysfunction in Drosophila. Science 302, 1765–1768 (2003).

11. R. Etournay, M. Popović, M. Merkel, A. Nandi, C. Blasse, B. Aigouy, H. Brandl, G. Myers,

G. Salbreux, F. Jülicher, S. Eaton, Interplay of cell dynamics and epithelial tension during

morphogenesis of the Drosophila pupal wing. eLife 4, e07090 (2015).

37. A.-K. Classen, B. Aigouy, A. Giangrande, S. Eaton, Imaging Drosophila Pupal Wing Morphogenesis, in Methods in molecular biology (Clifton, N.J.) (2008); http://link.springer.com/10.

1007/978-1-59745-583-1_16, vol. 420, pp. 265–275.

12. W.-C. Chu, S. Hayashi, Mechano-chemical enforcement of tendon apical ECM into nanofilaments during Drosophila flight muscle development. Curr. Biol. 31,

1366–1378.e7 (2021).

38. B. Ewen-Campen, D. Yang-Zhou, V. R. Fernandes, D. P. González, L.-P. Liu, R. Tao, X. Ren,

J. Sun, Y. Hu, J. Zirin, S. E. Mohr, J.-Q. Ni, N. Perrimon, Optimized strategy for in vivo Cas9activation in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 114, 9409–9414 (2017).

13. S. J. Smith, L. A. Davidson, M. Rebeiz, Evolutionary expansion of apical extracellular matrix

is required for the elongation of cells in a novel structure. eLife 9, e55965 (2020).

14. C. M. Lye, H. W. Naylor, B. Sanson, Subcellular localisations of the CPTI collection of YFPtagged proteins in Drosophila embryos. Development 141, 4006–4017 (2014).

15. N. Lowe, J. S. Rees, J. Roote, E. Ryder, I. M. Armean, G. Johnson, E. Drummond, H. Spriggs,

J. Drummond, J. P. Magbanua, H. Naylor, B. Sanson, R. Bastock, S. Huelsmann, V. Trovisco,

M. Landgraf, S. Knowles-Barley, J. D. Armstrong, H. White-Cooper, C. Hansen, R. G. Phillips,

K. S. Lilley, S. Russell, D. St Johnston, Analysis of the expression patterns, subcellular localisations and interaction partners of Drosophila proteins using a pigP protein trap library.

Development 141, 3994–4005 (2014).

16. L. F. Appel, M. Prout, R. Abu-Shumays, A. Hammonds, J. C. Garbe, D. Fristrom, J. Fristrom,

The Drosophila Stubble-stubbloid gene encodes an apparent transmembrane serine protease required for epithelial morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 90,

4937–4941 (1993).

Tsuboi et al., Sci. Adv. 9, eadh2154 (2023)

1 September 2023

Acknowledgments: We thank the Kyoto and Bloomington Drosophila Stock Centers, the

Vienna Drosophila Resource Center, M. Suzanne, R. A. Holmgren, T. Tabata, S. Ohsawa, Y. Hattori,

K. Sugimura, and D. Umetsu for fly stocks; M. Hirohata, K. Ikeguchi, M. Miki, and A. Nakata for

assistance with data analysis and experiments; H. Wada for the TPIV; W. Draper for the code to

calculate curvature; B. Aigouy for the Tissue Analyzer and EPySeg; KULIC, K. Takakura, and

H. Yukinaga for imaging with a MP microscope; S. Hayashi, T. Uemura, T. Usui, T. Harumoto,

M. S. Kitazawa, S. Tsugawa, and D. Umetsu for comments on the manuscript; and members of

the Kondo, Uemura, and Fujimoto laboratories for discussions. A.T. was a JSPS Research Fellow.

Funding: This work was supported by JSPS KAKENHI 19J00764 (to A.T.), 21H05779 (to A.T.),

17H06386 (to K.F.), and 16H06280 “ABiS”; a grant from the NIPPON Genetics (to A.T.); The

Keihanshin Consortium for Fostering the Next Generation of Global Leaders in Research (KCONNEX) established by the program of Building of Consortia for the Development of Human

Resources in Science and Technology, MEXT (to T.K.); and Japan Science and Technology

13 of 14

Downloaded from https://www.science.org on September 03, 2023

25. H. Tanimoto, S. Itoh, P. ten Dijke, T. Tabata, Hedgehog creates a gradient of DPP activity in

Drosophila wing imaginal discs. Mol. Cell 5, 59–71 (2000).

Other Supplementary Material for this

manuscript includes the following:

Movies S1 to S14

S C I E N C E A D VA N C E S | R E S E A R C H A R T I C L E

Agency JPMJCR2121 (to K.F.). Author contributions: Conceptualization: A.T., K.F., and T.K.

Formal analysis: A.T. Investigation: A.T. Funding acquisition: A.T., K.F., and T.K. Project

administration: A.T. Supervision: T.K. Writing—original draft: A.T. and T.K. Writing—review and

editing: K.F. Competing interests: The authors declare that they have no competing interests.

Data and materials availability: All data needed to evaluate the conclusions in the paper are

present in the paper and/or the Supplementary Materials.

Submitted 16 February 2023

Accepted 1 August 2023

Published 1 September 2023

10.1126/sciadv.adh2154

Downloaded from https://www.science.org on September 03, 2023

Tsuboi et al., Sci. Adv. 9, eadh2154 (2023)

1 September 2023

14 of 14

Spatiotemporal remodeling of extracellular matrix orients epithelial sheet folding

Alice Tsuboi, Koichi Fujimoto, and Takefumi Kondo

Sci. Adv., 9 (35), eadh2154.

DOI: 10.1126/sciadv.adh2154

Use of this article is subject to the Terms of service

Science Advances (ISSN ) is published by the American Association for the Advancement of Science. 1200 New York Avenue NW,

Washington, DC 20005. The title Science Advances is a registered trademark of AAAS.

Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim

to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

Downloaded from https://www.science.org on September 03, 2023

View the article online

https://www.science.org/doi/10.1126/sciadv.adh2154

Permissions

https://www.science.org/help/reprints-and-permissions

...