Myosin-II-mediated cell shape changes and cell intercalation contribute to primitive streak formation

Nature Cell Biology

Volumn 17, Issue 4, 2015, Pages 397-408

  Rozbicki, Emil ^a   Chuai, Manli ^a   Karjalainen, Antti I ^a   Song, Feifei ^b   Sang, Helen M ^b   Martin, René ^c   Knölker, Hans Joachim ^c   Macdonald, Michael P ^a,d   Weijer, Cornelis J ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN I; MYOSIN II; MYOSIN V; PROTEIN INHIBITOR; BLEBBISTATIN; CHLORINATED HYDROCARBON; FUSED HETEROCYCLIC RINGS; PENTABROMOPSEUDILIN; PENTACHLOROPSEUDILIN; PYRROLE DERIVATIVE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANISOTROPY; ARTICLE; CELL FUNCTION; CELL SHAPE; CELL TRANSFORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; GENE SILENCING; HUMAN; HUMAN CELL; MATHEMATICAL COMPUTING; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL MOTION; CELL PROLIFERATION; CHICK EMBRYO; CHICKEN; CYTOLOGY; EMBRYOLOGY; GASTRULATION; GENETICS; HEK293 CELL LINE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PRIMITIVE STREAK; RNA INTERFERENCE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CHICK EMBRYO; CHICKENS; GASTRULATION; HEK293 CELLS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; HYDROCARBONS, CHLORINATED; MYOSIN TYPE I; MYOSIN TYPE II; MYOSIN TYPE V; PHOSPHORYLATION; PRIMITIVE STREAK; PYRROLES; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84925878003     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3138     Document Type: Article

References (70)

1. Stern, C. D. Gastrulation, from Cells to Embryos (Cold Spring Harbor Laboratory Press, 2004).
2. Weinberger, C. & Brick, I. Primary hypoblast development in the chick II. The role of cell division. Roux Arch. Dev. Biol. 191, 127-133 (1982).
3. Stern, C. D. & Downs, K. M. The hypoblast (visceral endoderm): an evo-devo perspective. Development 139, 1059-1069 (2012).
4. Nakaya, Y. & Sheng, G. Epithelial to mesenchymal transition during gastrulation: an embryological view. Dev. Growth Differ. 50, 755-766 (2008).
5. Nakaya, Y., Sukowati, E. W., Wu, Y. & Sheng, G. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat. Cell Biol. 10, 765-775 (2008).
6. Graeper, L. Die Primitiventwicklung des Huehnchens nach stereokinematographischen Untersuchungen kontrolliert durch vitale Farbmarkierung und verglichen mit der Entwicklung anderer Wirbeltiere. Roux Arch. Dev. Biol. 116, 382-429 (1929).
7. Chuai, M. et al. Cell movement during chick primitive streak formation. Dev. Biol. 296, 137-149 (2006).
8. Zamir, E. A., Rongish, B. J. & Little, C. D. The ECM moves during primitive streak formation-computation of ECM versus cellular motion. PLoS Biol. 6, e247 (2008).
9. Voiculescu, O., Bertocchini, F., Wolpert, L., Keller, R. E. & Stern, C. D. The amniote primitive streak is defined by epithelial cell intercalation before gastrulation. Nature 449, 1049-1052 (2007).
10. Chuai, M., Hughes, D. & Weijer, C. J. Collective epithelial and mesenchymal cell migration during gastrulation. Curr. Genomics 13, 267-277 (2012).
11. Cui, C., Yang, X., Chuai, M., Glazier, J. A. & Weijer, C. J. Analysis of tissue flow patterns during primitive streak formation in the chick embryo. Dev. Biol. 284, 37-47 (2005).
12. Sandersius, S. A., Chuai, M., Weijer, C. J. & Newman, T. J. A 'chemotactic dipole' mechanism for large-scale vortex motion during primitive streak formation in the chick embryo. Phys. Biol. 8, 045008 (2011).
13. Wei, Y. & Mikawa, T. Formation of the avian primitive streak from spatially restricted blastoderm: evidence for polarized cell division in the elongating streak. Development 127, 87-96 (2000).
14. Alev, C., Wu, Y., Nakaya, Y. & Sheng, G. Decoupling of amniote gastrulation and streak formation reveals a morphogenetic unity in vertebrate mesoderm induction. Development 140, 2691-2696 (2013).
15. Yanagawa, N., Sakabe, M., Sakata, H., Yamagishi, T. & Nakajima, Y. Nodal signal is required for morphogenetic movements of epiblast layer in the pre-streak chick blastoderm. Dev. Growth Differ. 53, 366-377 (2011).
16. Verveer, P. J. et al. High-resolution three-dimensional imaging of large specimens with light sheet-based microscopy. Nat. Methods 4, 311-313 (2007).
17. Huisken, J., Swoger, J., Del Bene, F., Wittbrodt, J. & Stelzer, E. H. Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305, 1007-1009 (2004).
18. Tomer, R., Khairy, K. & Keller, P. J. Shedding light on the system: studying embryonic development with light sheet microscopy. Curr. Opin. Genet. Dev. 21, 558-565 (2011).
19. Blanchard, G. B. et al. Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation. Nat. Methods 6, 458-464 (2009).
20. Bosveld, F. et al. Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway. Science 336, 724-727 (2012).
21. Allan, C. et al. OMERO: flexible, model-driven data management for experimental biology. Nat. Methods 9, 245-253 (2012).
22. Czirok, A., Rongish, B. J. & Little, C. D. Extracellular matrix dynamics during vertebrate axis formation. Dev. Biol. 268, 111-122 (2004).
23. Amat, F., Myers, E. W. & Keller, P. J. Fast and robust optical flow for time-lapse microscopy using super-voxels. Bioinformatics 29, 373-380 (2013).
24. Downie, J. R. The mechanism of chick blastoderm expansion. J. Embryol. Exp. Morphol. 35, 559-575 (1976).
25. Chapman, S. C., Schubert, F. R., Schoenwolf, G. C. & Lumsden, A. Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Dev. Biol. 245, 187-199 (2002).
26. Chuai, M. & Weijer, C. J. The mechanisms underlying primitive streak formation in the chick embryo. Curr. Top. Dev. Biol. 81, 135-156 (2008).
27. Butler, L. C. et al. Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nat. Cell Biol. 11, 859-864 (2009).
28. Bardet, P. L. et al. PTEN controls junction lengthening and stability during cell rearrangement in epithelial tissue. Dev. Cell 25, 534-546 (2013).
29. Bertet, C., Sulak, L. & Lecuit, T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671 (2004).
30. Blankenship, J. T., Backovic, S. T., Sanny, J. S., Weitz, O. & Zallen, J. A. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 11, 459-470 (2006).
31. Martin, A. C., Gelbart, M., Fernandez-Gonzalez, R., Kaschube, M. & Wieschaus, E. F. Integration of contractile forces during tissue invagination. J. Cell Biol. 188, 735-749 (2010).
32. Zallen, J. A. & Wieschaus, E. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 6, 343-355 (2004).
33. Limouze, J., Straight, A. F., Mitchison, T. & Sellers, J. R. Specificity of blebbistatin, an inhibitor of myosin II. J. Muscle Res. Cell Motil. 25, 337-341 (2004).
34. Simoes Sde, M. et al. Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation. Dev. Cell 19, 377-388 (2010).
35. Levayer, R., Pelissier-Monier, A. & Lecuit, T. Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat. Cell Biol. 13, 529-540 (2011).
36. Warrington, S. J., Strutt, H. & Strutt, D. The Frizzled-dependent planar polarity pathway locally promotes E-cadherin turnover via recruitment of RhoGEF2. Development 140, 1045-1054 (2013).
37. Tamura, M. et al. Development of specific Rho-kinase inhibitors and their clinical application. Biochim. Biophys. Acta 1754, 245-252 (2005).
38. Fedorov, R. et al. The mechanism of pentabromopseudilin inhibition of myosin motor activity. Nat. Struct. Mol. Biol. 16, 80-88 (2009).
39. Bond, L. M., Tumbarello, D. A., Kendrick-Jones, J. & Buss, F. Small-molecule inhibitors of myosin proteins. Future Med. Chem. 5, 41-52 (2013).
40. Chinthalapudi, K. et al. Mechanism and specificity of pentachloropseudilin-mediated inhibition of myosin motor activity. J. Biol. Chem. 286, 29700-29708 (2011).
41. Marinari, E. et al. Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 484, 542-545 (2012).
42. Voiculescu, O., Bodenstein, L., Lau, I. J. & Stern, C. D. Local cell interactions and self-Amplifying individual cell ingression drive amniote gastrulation. eLife 3, e01817 (2014).
43. Fernandez-Gonzalez, R., Simoes Sde, M., Roper, J. C., Eaton, S. & Zallen, J. A. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 17, 736-743 (2009).
44. Ren, Y. et al. Mechanosensing through cooperative interactions between myosin II and the actin crosslinker cortexillin I. Curr. Biol. 19, 1421-1428 (2009).
45. Laakso, J. M., Lewis, J. H., Shuman, H. & Ostap, E. M. Myosin I can act as a molecular force sensor. Science 321, 133-136 (2008).
46. Williams, M., Burdsal, C., Periasamy, A., Lewandoski, M. & Sutherland, A. Mouse primitive streak forms in situ by initiation of epithelial to mesenchymal transition without migration of a cell population. Dev. Dyn. 241, 270-283 (2012).
47. Pouille, P. A., Ahmadi, P., Brunet, A. C. & Farge, E. Mechanical signals trigger Myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci. Signal. 2, ra16 (2009).
48. Zallen, J. A. & Blankenship, J. T. Multicellular dynamics during epithelial elongation. Semin. Cell Dev. Biol. 19, 263-270 (2008).
49. Wagstaff, L. J., Bellett, G., Mogensen, M. M. & Munsterberg, A. Multicellular rosette formation during cell ingression in the avian primitive streak. Dev. Dyn. 237, 91-96 (2008).
50. Keller, R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950-1954 (2002).
51. Honda, H., Nagai, T. & Tanemura, M. Two different mechanisms of planar cell intercalation leading to tissue elongation. Dev. Dyn. 237, 1826-1836 (2008).
52. Dawes-Hoang, R. E. et al. Folded gastrulation, cell shape change and the control of myosin localization. Development 132, 4165-4178 (2005).
53. Kolsch, V., Seher, T., Fernandez-Ballester, G. J., Serrano, L. & Leptin, M. Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 315, 384-386 (2007).
54. Manning, A. J., Peters, K. A., Peifer, M. & Rogers, S. L. Regulation of epithelial morphogenesis by the g protein-coupled receptor mist and its ligand fog. Sci. Signal. 6, ra98 (2013).
55. Niwa, H., Yamamura, K. & Miyazaki, J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199 (1991).
56. Schambach, A. et al. Woodchuck hepatitis virus post-Transcriptional regulatory element deleted from X protein and promoter sequences enhances retroviral vector titer and expression. Gene Ther. 13, 641-645 (2006).
57. McGrew, M. J. et al. Efficient production of germline transgenic chickens using lentiviral vectors. EMBO Rep. 5, 728-733 (2004).
58. Chapman, S. C., Collignon, J., Schoenwolf, G. C. & Lumsden, A. Improved method for chick whole-embryo culture using a filter paper carrier. Dev. Dyn. 220, 284-289 (2001).
59. New, D. A new technique for the cultivation of the Chick embryo in vitro. J. Embryol. Exp. Morphol. 3, 320-331 (1955).
60. Eyal-Giladi, H. & Kochav, S. From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick. I. General morphology. Dev. Biol. 49, 321-337 (1976).
61. Hamburger, V. & Hamilton, H. L. A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92 (1951).
62. Rozbicki, E., Chuai, C. & Weijer, C. J. Liquid culture technique for early chick embryos suitable for long term live imaging. Nat. Protoc. Exch. http://dx.doi.org/10.1038/ protex.2015.012 (2015).
63. Martin, R. et al. Total synthesis of pentabromo-And pentachloropseudilin, and synthetic analogues-Allosteric inhibitors of myosin ATPase. Angew. Chem. Int. Ed. Engl. 48, 8042-8046 (2009).
64. Leslie, N. R., Yang, X., Downes, C. P. & Weijer, C. J. PtdIns(3, 4, 5)P(3)-dependent and-independent roles for PTEN in the control of cell migration. Curr. Biol. 17, 115-125 (2007).
65. Keller, P. J., Schmidt, A. D., Wittbrodt, J. & Stelzer, E. H. Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322, 1065-1069 (2008).
66. Thielicke, W. & Stamhuis, E. J. PIVlab-Towards user-friendly, affordable and accurate digital particle image velocimetry in MATLAB. J. Open Res. Softw. 2, e30 (2014).
67. Heller, E., Kumar, K. V., Grill, S. W. & Fuchs, E. Forces generated by cell intercalation tow epidermal sheets in mammalian tissue morphogenesis. Dev. Cell 28, 617-632 (2014).
68. Meyer, F. Topographic distance and watershed lines. Signal Process. 38, 113-125 (1994).
69. Mulchrone, K. F. & Choudhury, K. R. Fitting an ellipse to an arbitrary shape: implications for strain analysis. J. Struct. Geol. 26, 143-153 (2004).
70. Graner, F., Dollet, B., Raufaste, C. & Marmottant, P. Discrete rearranging disordered patterns, part I: robust statistical tools in two or three dimensions. Eur. Phys. J. E 25, 349-369 (2008).