Unified quantitative characterization of epithelial tissue development

eLife

Volumn 4, Issue DECEMBER2015, 2015, Pages

  Guirao, Boris ^a   Rigaud, Stéphane U ^a   Bosveld, Floris ^a   Bailles, Anaïs ^a,f   López Gay, Jesús ^a   Ishihara, Shuji ^b   Sugimura, Kaoru ^c,d   Graner, François ^e   Bellaïche, Yohanns ^a  

^a INSTITUT CURIE   (France)

^b MEIJI UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e UNIVERSITÉ PARIS DIDEROT   (France)

^f AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIVISION; CELL SHAPE; COMPUTER SIMULATION; DORSAL REGION; DROSOPHILA; EPITHELIUM; HISTOGENESIS; INSECT CELL CULTURE; MECHANICAL STRESS; MORPHOGENESIS; NONHUMAN; ORGAN CULTURE; QUANTITATIVE ANALYSIS; QUANTITATIVE STUDY; THORAX; TISSUE GROWTH; WING; ANIMAL; BIOLOGICAL MODEL; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING;

ANIMALS; COMPUTER SIMULATION; DROSOPHILA; EPITHELIUM; MODELS, BIOLOGICAL;

EID: 84979532625     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08519     Document Type: Article

References (66)

1. Aigouy B, Farhadifar R, Staple DB, Sagner A, Röper JC, Jülicher F, Eaton S. 2010. Cell flow reorients the axis of planar polarity in the wing epithelium of drosophila. Cell 142:773–786. doi: 10.1016/j.cell.2010.07.042
2. Akaike H. 1980. Likelihood and the Bayes procedure (chapter 3). Bernardo J. M, De Groot M. H, Lindley D. V, Smith A. F. M eds Bayesian Statistics. Valencia, Spain: University Press; 143–203.
3. Aliee M, Röper JC, Landsberg KP, Pentzold C, Widmann TJ, Jülicher F, Dahmann C. 2012. Physical mechanisms shaping the drosophila dorsoventral compartment boundary. Current Biology 22:967–976. doi: 10.1016/j.cub.2012.03.070
4. Antunes M, Pereira T, Cordeiro JV, Almeida L, Jacinto A. 2013. Coordinated waves of actomyosin flow and apical cell constriction immediately after wounding. Journal of Cell Biology 202:365–379. doi: 10.1083/jcb.201211039
5. Aubouy M, Jiang Y, Glazier JA, Graner F. 2003. A texture tensor to quantify deformations. Granular Matter 5: 67–70. doi: 10.1007/s10035-003-0126-x
6. Baena-López LA, Baonza A, García-Bellido A. 2005. The orientation of cell divisions determines the shape of drosophila organs. Current Biology 15:1640–1644. doi: 10.1016/j.cub.2005.07.062
7. Bambardekar K, Clément R, Blanc O, Chardès C, Lenne PF. 2015. Direct laser manipulation reveals the mechanics of cell contacts in vivo. Proceedings of the National Academy of Sciences of the United States of America 112:1416–1421. doi: 10.1073/pnas.1418732112
8. Bardet PL, Guirao B, Paoletti C, Serman F, Léopold V, Bosveld F, Goya Y, Mirouse V, Graner F, Bellaïche Y. 2013. PTEN controls junction lengthening and stability during cell rearrangement in epithelial tissue. Developmental Cell 25:534–546. doi: 10.1016/j.devcel.2013.04.020
9. Batchelor GK. 1970. The stress system in a suspension of force-free particles. Journal of Fluid Mechanics 41:545–570. doi: 10.1017/S0022112070000745
10. Blanchard GB, Kabla AJ, Schultz NL, Butler LC, Sanson B, Gorfinkiel N, Mahadevan L, Adams RJ. 2009. Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation. Nature Methods 6:458–464. doi: 10.1038/nmeth.1327
11. Bosveld F, Bonnet I, Guirao B, Tlili S, Wang Z, Petitalot A, Marchand R, Bardet PL, Marcq P, Graner F, et al. 2012. Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway. Science 336: 724–727. doi: 10.1126/science.1221071
12. Boulanger J, Kervrann C, Bouthemy P, Elbau P, Sibarita JB, Salamero J. 2010. Patch-based nonlocal functional for denoising fluorescence microscopy image sequences. IEEE Transactions on Medical Imaging 29:442–454. doi: 10.1109/TMI.2009.2033991
13. Brodland GW, Conte V, Cranston PG, Veldhuis J, Narasimhan S, Hutson MS, Jacinto A, Ulrich F, Baum B, Miodownik M. 2010. Video force microscopy reveals the mechanics of ventral furrow invagination in drosophila. Proceedings of the National Academy of Sciences of the United States of America 107:22111–22116. doi: 10.1073/pnas.1006591107
14. Brodland GW, Veldhuis JH, Kim S, Perrone M, Mashburn D, Hutson MS. 2014. Cell FIT: a cellular force-inference toolkit using curvilinear cell boundaries. PloS One 9:e99116. doi: 10.1371/journal.pone.0099116
15. Butler LC, Blanchard GB, Kabla AJ, Lawrence NJ, Welchman DP, Mahadevan L, Adams RJ, Sanson B. 2009. Cell shape changes indicate a role for extrinsic tensile forces in drosophila germ-band extension. Nature Cell Biology 11:859–864. doi: 10.1038/ncb1894
16. Campinho P, Behrndt M, Ranft J, Risler T, Minc N, Heisenberg CP. 2013. Tension-oriented cell divisions limit anisotropic tissue tension in epithelial spreading during zebrafish epiboly. Nature Cell Biology 15:1405–1414. doi: 10.1038/ncb2869
17. Cheddadi I, Saramito P, Dollet B, Raufaste C, Graner F. 2011. Understanding and predicting viscous, elastic, plastic flows. European Physical Journal E 34:1–15. doi: 10.1140/epje/i2011-11001-4
18. Chiou KK, Hufnagel L, Shraiman BI. 2012. Mechanical stress inference for two dimensional cell arrays. PLoS Computational Biology 8:e1002512. doi: 10.1371/journal.pcbi.1002512
19. Classen AK, Aigouy B, Giangrande A, Eaton S. 2008. Imaging drosophila pupal wing morphogenesis. Methods in Molecular Biology 420:265–275. doi: 10.1007/978-1-59745-583-1_16
20. David NB, Martin CA, Segalen M, Rosenfeld F, Schweisguth F, Bellaïche Y. 2005. Drosophila ric-8 regulates galphai cortical localization to promote galphai-dependent planar orientation of the mitotic spindle during asymmetric cell division. Nature Cell Biology 7:1083–1090. doi: 10.1038/ncb1319
21. Economou AD, Brock LJ, Cobourne MT, Green JB. 2013. Whole population cell analysis of a landmark-rich mammalian epithelium reveals multiple elongation mechanisms. Development 140:4740–4750. doi: 10.1242/dev.096545
22. Etournay R, Popović M, Merkel M, Nandi A, Blasse C, Aigouy B, Brandl H, Myers G, Salbreux G, Jü licher F, et al. 2015. Interplay of cell dynamics and epithelial tension during morphogenesis of the drosophila pupal wing. eLife 4. doi: 10.7554/eLife.07090
23. Fink J, Carpi N, Betz T, Bétard A, Chebah M, Azioune A, Bornens M, Sykes C, Fetler L, Cuvelier D, et al. 2011. External forces control mitotic spindle positioning. Nature Cell Biology 13:771–778. doi: 10.1038/ncb2269
24. Gho M, Bellaïche Y, Schweisguth F. 1999. Revisiting the drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development 126:3573–3584.
25. Gibson WT, Veldhuis JH, Rubinstein B, Cartwright HN, Perrimon N, Brodland GW, Nagpal R, Gibson MC. 2011. Control of the mitotic cleavage plane by local epithelial topology. Cell 144:427–438. doi: 10.1016/j.cell.2010.12.035
26. Glazier JA, Graner F. 1993. Simulation of the differential adhesion driven rearrangement of biological cells. Physical Review E 47:2128–2154. doi: 10.1103/PhysRevE.47.2128
27. Graner F, Dollet B, Raufaste C, Marmottant P. 2008. Discrete rearranging disordered patterns, part I: robust statistical tools in two or three dimensions. European Physical Journal E 25:349–369. doi: 10.1140/epje/i2007-10298-8
28. Graner F, Glazier JA. 1992. Simulation of biological cell sorting using a two-dimensional extended Potts model. Physical Review Letters 69:2013–2016. doi: 10.1103/PhysRevLett.69.2013
29. Grosshans J, Wieschaus E. 2000. A genetic link between morphogenesis and cell division during formation of the ventral furrow in drosophila. Cell 101:523–531. doi: 10.1016/S0092-8674(00)80862-4
30. Guillot C, Lecuit T. 2013. Mechanics of epithelial tissue homeostasis and morphogenesis. Science 340:1185–1189. doi: 10.1126/science.1235249
31. Heisenberg CP, Bellaïche Y. 2013. Forces in tissue morphogenesis and patterning. Cell 153:948–962. doi: 10.1016/j.cell.2013.05.008
32. Heller E, Kumar KV, Grill SW, Fuchs E. 2014. Forces generated by cell intercalation tow epidermal sheets in mammalian tissue morphogenesis. Developmental Cell 28:617–632. doi: 10.1016/j.devcel.2014.02.011
33. Huang J, Zhou W, Dong W, Watson AM, Hong Y. 2009. From the cover: directed, efficient, and versatile modifications of the drosophila genome by genomic engineering. Proceedings of the National Academy of Sciences of the United States of America 106:8284–8289. doi: 10.1073/pnas.0900641106
34. Ishihara S, Sugimura K, Cox SJ, Bonnet I, Bellaïche Y, Graner F. 2013. Comparative study of non-invasive force and stress inference methods in tissue. European Physical Journal E 36:1–13. doi: 10.1140/epje/i2013-13045-8
35. Ishihara S, Sugimura K. 2012. Bayesian inference of force dynamics during morphogenesis. Journal of Theoretical Biology 313:201–211. doi: 10.1016/j.jtbi.2012.08.017
36. Kaipio J, Somersalo E. 2006. Statistical and computational inverse problems. Springer 160.
37. Keller PJ. 2013. Imaging morphogenesis: technological advances and biological insights. Science 340:1234168. doi: 10.1126/science.1234168
38. Khan Z, Wang YC, Wieschaus EF, Kaschube M. 2014. Quantitative 4D analyses of epithelial folding during drosophila gastrulation. Development 141:2895–2900. doi: 10.1242/dev.107730
39. Krzic U, Gunther S, Saunders TE, Streichan SJ, Hufnagel L. 2012. Multiview light-sheet microscope for rapid in toto imaging. Nature Methods 9:730–733. doi: 10.1038/nmeth.2064
40. Lau K, Tao H, Liu H, Wen J, Sturgeon K, Sorfazlian N, Lazic S, Burrows JT, Wong MD, Li D, et al. 2015. Anisotropic stress orients remodelling of mammalian limb bud ectoderm. Nature Cell Biology 17:569–579. doi: 10.1038/ncb3156
41. Lecuit T, Lenne PF, Munro E. 2011. Force generation, transmission, and integration during cell and tissue morphogenesis. Annual Review of Cell and Developmental Biology 27:157–184. doi: 10.1146/annurev-cellbio-100109-104027
42. Legoff L, Rouault H, Lecuit T. 2013. A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing drosophila wing disc. Development 140:4051–4059. doi: 10.1242/dev.090878
43. Malvern LE. 1969. Introduction to the Mechanics of a Continuous Medium. New Jersey: Prentice-Hall, Inc.
44. Mao Y, Tournier AL, Bates PA, Gale JE, Tapon N, Thompson BJ. 2011. Planar polarization of the atypical myosin dachs orients cell divisions in drosophila. Genes & Development 25:131–136. doi: 10.1101/gad.610511
45. Mao Y, Tournier AL, Hoppe A, Kester L, Thompson BJ, Tapon N. 2013. Differential proliferation rates generate patterns of mechanical tension that orient tissue growth. EMBO Journal 32:2790–2803. doi: 10.1038/emboj.2013.197
46. Marinari E, Mehonic A, Curran S, Gale J, Duke T, Baum B. 2012. Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 484:542–545. doi: 10.1038/nature10984
47. Marée AFM, Grieneisen VA, Hogeweg P. 2007. The Cellular Potts Model and biophysical properties of cells, tissues and morphogenesis. Anderson Alexander RA, Chaplain Mark AJ, Rejniak Katarzyna A, Single Cell-Based Models in Biology and Medicine. Basel: Birkhä user 107–136. doi: 10.1007/978-3-7643-8123-3_5
48. Mata J, Curado S, Ephrussi A, Rørth P. 2000. Tribbles coordinates mitosis and morphogenesis in drosophila by regulating string/CDC25 proteolysis. Cell 101:511–522. doi: 10.1016/S0092-8674(00)80861-2
49. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 2003. Spatiotemporal rescue of memory dysfunction in drosophila. Science 302:1765–1768. doi: 10.1126/science.1089035
50. Monier B, Gettings M, Gay G, Mangeat T, Schott S, Guarner A, Suzanne M. 2015. Apico-basal forces exerted by apoptotic cells drive epithelium folding. Nature 518:245–248. doi: 10.1038/nature14152
51. Mummery-Widmer JL, Yamazaki M, Stoeger T, Novatchkova M, Bhalerao S, Chen D, Dietzl G, Dickson BJ, Knoblich JA. 2009. Genome-wide analysis of notch signalling in drosophila by transgenic RNAi. Nature 458: 987–992. doi: 10.1038/nature07936
52. Oda H, Tsukita S. 2001. Real-time imaging of cell-cell adherens junctions reveals that drosophila mesoderm invagination begins with two phases of apical constriction of cells. Journal of Cell Science 114:493–501.
53. Olguín P, Glavic A, Mlodzik M. 2011. Intertissue mechanical stress affects frizzled-mediated planar cell polarity in the drosophila notum epidermis. Current Biology 21:236–242. doi: 10.1016/j.cub.2011.01.001
54. Quesada-Hernández E, Caneparo L, Schneider S, Winkler S, Liebling M, Fraser SE, Heisenberg CP. 2010. Stereotypical cell division orientation controls neural rod midline formation in zebrafish. Current Biology 20: 1966–1972. doi: 10.1016/j.cub.2010.10.009
55. Rael M, Willert CE, Wereley ST, Kompenhans J. 2007. Particle Image Velocimetry - a Practical Guide. Springer.
56. Ranft J, Basan M, Elgeti J, Joanny JF, Prost J, Jü licher F. 2010. Fluidization of tissues by cell division and apoptosis. Proceedings of the National Academy of Sciences of the United States of America 107:20863–20868. doi: 10.1073/pnas.1011086107
57. Rauzi M, Lenne PF. 2011. Cortical forces in cell shape changes and tissue morphogenesis. Current Topics in Developmental Biology 95:93–144. doi: 10.1016/B978-0-12-385065-2.00004-9
58. Rauzi M, Verant P, Lecuit T, Lenne PF. 2008. Nature and anisotropy of cortical forces orienting drosophila tissue morphogenesis. Nature Cell Biology 10:1401–1410. doi: 10.1038/ncb1798
59. Rozbicki E, Chuai M, Karjalainen AI, Song F, Sang HM, Martin R, Knölker HJ, MacDonald MP, Weijer CJ. 2015. Myosin-II-mediated cell shape changes and cell intercalation contribute to primitive streak formation. Nature Cell Biology 17:397–408. doi: 10.1038/ncb3138
60. Saburi S, Hester I, Fischer E, Pontoglio M, Eremina V, Gessler M, Quaggin SE, Harrison R, Mount R, McNeill H. 2008. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nature Genetics 40:1010–1015. doi: 10.1038/ng.179
61. Seher TC, Leptin M. 2000. Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during drosophila gastrulation. Current Biology 10:623–629. doi: 10.1016/S0960-9822(00)00502-9
62. Sugimura K, Ishihara S. 2013. The mechanical anisotropy in a tissue promotes ordering in hexagonal cell packing. Development 140:4091–4101. doi: 10.1242/dev.094060
63. Tlili S, Gay C, Graner F, Marcq P, Molino F, Saramito P. 2015. Colloquium: mechanical formalisms for tissue dynamics. European Physical Journal E 38:33. doi: 10.1140/epje/i2015-15033-4
64. Tomer R, Khairy K, Amat F, Keller PJ. 2012. Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy. Nature Methods 9:755–763. doi: 10.1038/nmeth.2062
65. Wyatt TPJ, Harris AR, Lam M, Cheng Q, Bellis J, Dimitracopoulos A, Kabla AJ, Charras GT, Baum B. 2015. Emergence of homeostatic epithelial packing and stress dissipation through divisions oriented along the long cell axis. Proceedings of the National Academy of Sciences of the United States of America 112:5726–5731. doi: 10.1073/pnas.1420585112
66. Zulueta-Coarasa T, Tamada M, Lee EJ, Fernandez-Gonzalez R. 2014. Automated multidimensional image analysis reveals a role for Abl in embryonic wound repair. Development 141:2901–2911. doi: 10.1242/dev.106898