Multi-cellular rosettes in the mouse visceral endoderm facilitate the ordered migration of anterior visceral endoderm cells

PLoS Biology

Volumn 10, Issue 2, 2012, Pages

  Trichas, Georgios ^a   Smith, Aaron M ^a   White, Natalia ^a   Wilkins, Vivienne ^a   Watanabe, Tomoko ^a   Moore, Abigail ^a   Joyce, Bradley ^a   Sugnaseelan, Jacintha ^a   Rodriguez, Tristan A ^b   Kay, David ^a   Baker, Ruth E ^a   Maini, Philip K ^a   Srinivas, Shankar ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ZO1;

ANIMAL CELL; ANIMAL TISSUE; ANTERIOR VISCERAL ENDODERM CELL; ARTICLE; BRANCHING MORPHOGENESIS; CELL CYCLE ARREST; CELL FUNCTION; CELL JUNCTION; CELL MIGRATION; CELL MOTION; CELL POLARITY; CONTROLLED STUDY; ECTODERM; EMBRYO; ENDODERM; EPITHELIUM CELL; FEMALE; HOMOZYGOSITY; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; MOUSE; NONHUMAN; ROSETTE FORMATION; ROSETTE FORMING CELL; SIGNAL TRANSDUCTION; SIMULATION; VISCOSITY; ALGORITHM; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; C57BL MOUSE; CBA MOUSE; COMPUTER SIMULATION; CYTOLOGY; EMBRYO CULTURE; PHYSIOLOGY; POLARIZATION MICROSCOPY; TIME LAPSE IMAGING;

ALGORITHMS; ANIMALS; CELL MOVEMENT; CELL POLARITY; COMPUTER SIMULATION; EMBRYO CULTURE TECHNIQUES; EMBRYO, MAMMALIAN; ENDODERM; EPITHELIAL CELLS; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICROSCOPY, POLARIZATION; MODELS, BIOLOGICAL; TIME-LAPSE IMAGING;

EID: 84857468671     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001256     Document Type: Article

References (41)

1. Affolter M, Zeller R, Caussinus E, (2009) Tissue remodelling through branching morphogenesis. Nat Rev Mol Cell Biol 10: 831-842.
2. Costantini F, Kopan R, (2010) Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev Cell 18: 698-712.
3. Miller R. K, McCrea P. D, (2010) Wnt to build a tube: contributions of Wnt signaling to epithelial tubulogenesis. Dev Dyn 239: 77-93.
4. Sawyer J. M, Harrell J. R, Shemer G, Sullivan-Brown J, Roh-Johnson M, et al. (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341: 5-19.
5. Streit A, (2007) The preplacodal region: an ectodermal domain with multipotential progenitors that contribute to sense organs and cranial sensory ganglia. Int J Dev Biol 51: 447-461.
6. Arnold S. J, Robertson E. J, (2009) Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10: 91-103.
7. Rossant J, Tam P. P, (2009) Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136: 701-713.
8. Srinivas S, (2006) The anterior visceral endoderm-turning heads. Genesis 44: 565-572.
9. Beddington R. S, Robertson E. J, (1999) Axis development and early asymmetry in mammals. Cell 96: 195-209.
10. Thomas P. Q, Brown A, Beddington R. S, (1998) Hex: a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors. Development 125: 85-94.
11. Belo J. A, Bouwmeester T, Leyns L, Kertesz N, Gallo M, et al. (1997) Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech Dev 68: 45-57.
12. Yamamoto M, Saijoh Y, Perea-Gomez A, Shawlot W, Behringer R. R, et al. (2004) Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428: 387-392.
13. Srinivas S, Rodriguez T, Clements M, Smith J. C, Beddington R. S, (2004) Active cell migration drives the unilateral movements of the anterior visceral endoderm. Development 131: 1157-1164.
14. Perea-Gomez A, Rhinn M, Ang S. L, (2001) Role of the anterior visceral endoderm in restricting posterior signals in the mouse embryo. Int J Dev Biol 45: 311-320.
15. Norris D. P, Brennan J, Bikoff E. K, Robertson E. J, (2002) The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 129: 3455-3468.
16. Ding J, Yang L, Yan Y. T, Chen A, Desai N, et al. (1998) Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature 395: 702-707.
17. Kimura-Yoshida C, Nakano H, Okamura D, Nakao K, Yonemura S, et al. (2005) Canonical Wnt signaling and its antagonist regulate anterior-posterior axis polarization by guiding cell migration in mouse visceral endoderm. Dev Cell 9: 639-650.
18. Stuckey D. W, Clements M, Di-Gregorio A, Senner C. E, Le Tissier P, et al. (2011) Coordination of cell proliferation and anterior-posterior axis establishment in the mouse embryo. Development 138: 1521-1530.
19. Migeotte I, Omelchenko T, Hall A, Anderson K. V, (2010) Rac1-dependent collective cell migration is required for specification of the anterior-posterior body axis of the mouse. PLoS Biol 8: e1000442 doi:10.1371/journal.pbio.1000442.
20. Trichas G, Joyce B, Crompton L. A, Wilkins V, Clements M, et al. (2011) Nodal dependent differential localisation of dishevelled-2 demarcates regions of differing cell behaviour in the visceral endoderm. PLoS Biol 9: e1001019 doi:10.1371/journal.pbio.1001019.
21. Axelrod J. D, (2009) Progress and challenges in understanding planar cell polarity signaling. Semin Cell Dev Biol 20: 964-971.
22. Keller R, (2006) Mechanisms of elongation in embryogenesis. Development 133: 2291-2302.
23. Zallen J. A, (2007) Planar polarity and tissue morphogenesis. Cell 129: 1051-1063.
24. Bertet C, Sulak L, Lecuit T, (2004) Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429: 667-671.
25. Blankenship J. T, Backovic S. T, Sanny J. S, Weitz O, Zallen J. A, (2006) Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev Cell 11: 459-470.
26. Zallen J. A, Zallen R, (2004) Cell-pattern disordering during convergent extension in Drosophila. J Phys Condens Matter 16: S5073.
27. Honda H, (1978) Description of cellular patterns by Dirichlet domains: the two-dimensional case. J Theor Biol 72: 523-543.
28. Gibson M. C, Patel A. B, Nagpal R, Perrimon N, (2006) The emergence of geometric order in proliferating metazoan epithelia. Nature 442: 1038-1041.
29. Rauzi M, Verant P, Lecuit T, Lenne P. F, (2008) Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat Cell Biol 10: 1401-1410.
30. Aegerter-Wilmsen T, Smith A. C, Christen A. J, Aegerter C. M, Hafen E, et al. (2010) Exploring the effects of mechanical feedback on epithelial topology. Development 137: 499-506.
31. Weliky M, Oster G, (1990) The mechanical basis of cell rearrangement. I. Epithelial morphogenesis during Fundulus epiboly. Development 109: 373-386.
32. Farhadifar R, Roper J. C, Aigouy B, Eaton S, Julicher F, (2007) The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol 17: 2095-2104.
33. Hufnagel L, Teleman A. A, Rouault H, Cohen S. M, Shraiman B. I, (2007) On the mechanism of wing size determination in fly development. Proc Natl Acad Sci U S A 104: 3835-3840.
34. Landsberg K. P, Farhadifar R, Ranft J, Umetsu D, Widmann T. J, et al. (2009) Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr Biol 19: 1950-1955.
35. Rodriguez T. A, Casey E. S, Harland R. M, Smith J. C, Beddington R. S, (2001) Distinct enhancer elements control Hex expression during gastrulation and early organogenesis. Dev Biol 234: 304-316.
36. Smith A. M, Baker R. E, Kay D, Maini P. K, (2011) Incorporating chemical signalling factors into cell-based models of growing epithelial tissues. J Math Biol E-pub ahead of print 07 Sep 2011. doi:10.1007/s00285-011-0464-y.
37. Graner F, Glazier J. A, (1992) Simulation of biological cell sorting using a 2-dimensional extended potts-model. Phys Rev Lett 69: 2013-2016.
38. Meineke F. A, Potten C. S, Loeffler M, (2001) Cell migration and organization in the intestinal crypt using a lattice-free model. Cell Prolif 34: 253-266.
39. Keller P. J, Stelzer E. H, (2008) Quantitative in vivo imaging of entire embryos with digital scanned laser light sheet fluorescence microscopy. Curr Opin Neurobiol 18: 624-632.
40. Huisken J, Stainier D. Y, (2009) Selective plane illumination microscopy techniques in developmental biology. Development 136: 1963-1975.
41. Honda H, Tanemura M, Nagai T, (2004) A three-dimensional vertex dynamics cell model of space-filling polyhedra simulating cell behavior in a cell aggregate. J Theoret Biol 226: 439-453.