Dynamics and mechanical stability of the developing dorsoventral organizer of the wing imaginal disc

PLoS Computational Biology

Volumn 7, Issue 9, 2011, Pages

  Canela Xandri, Oriol ^a   Sagués, Francesc ^a   Casademunt, Jaume ^a   Buceta, Javier ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; CLONE CELLS; DIGITAL STORAGE; DYNAMICS; MECHANICAL STABILITY; MECHANISMS;

CELL CYCLE; CELL SEGREGATIONS; CELLULAR DOMAIN; CELLULAR POPULATIONS; CONTROL-CELL; DROSOPHILLA; IN-SILICO; PACKING PROPERTIES; SILICO EXPERIMENTS; VERTEX MODEL;

CELL PROLIFERATION;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIVISION; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; COMPUTER MODEL; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; DYNAMICS; LIMB DEVELOPMENT; NONHUMAN; WING IMAGINAL DISC DORSOVENTRAL ORGANIZER DEVELOPMENT; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; BIOMECHANICS; CELL COMMUNICATION; COMPUTER SIMULATION; CYTOLOGY; FORELIMB; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMAGINAL DISC; MORPHOGENESIS; MUTATION; PHYSIOLOGY;

ANIMALS; BIOMECHANICS; BODY PATTERNING; CELL COMMUNICATION; CELL CYCLE; CELL PROLIFERATION; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; CYTOSKELETON; DROSOPHILA; IMAGINAL DISCS; MODELS, BIOLOGICAL; MUTATION; WING;

EID: 80053452529     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002153     Document Type: Article

References (72)

1. Carroll SB, (1998) From pattern to gene, from gene to pattern. Int J Dev Biol 42: 305-309.
2. McNeill H, (2000) Sticking together and sorting things out: adhesion as a force in development. Nat Rev Genet 1: 100-108.
3. Lawrence P, Struhl G, (1996) Morphogens, compartments, and pattern: Lessons from drosophila? Cell 85: 951-961.
4. Vincent JP, (1998) Compartment boundaries: where, why and how? Int J Dev Biol 42: 311-315.
5. Cavodeassi F, Corral RDD, Campuzano S, Domínguez M, (1999) Compartments and organizing boundaries in the drosophila eye: the role of the homeodomain iroquois proteins. Development 126: 4933-4942.
6. Morata G, (2001) How drosophila appendages develop. Nat Rev Mol Cell Biol 2: 89-97.
7. Resino J, Salama-Cohen P, García-Bellido A, (2002) Determining the role of patterned cell proliferation in the shape and size of the drosophila wing. Proc Natl Acad Sci U S A 99: 7502-7507.
8. Simmonds A, Brook W, Cohen S, Belle J, (1995) Distinguishable functions for engrailed and invected in anterior-posterior patterning in the drosophila wing. Nature 376: 424-427.
9. Diaz-Benjumea F, Cohen S, (1993) Interaction between dorsal and ventral cells in the imaginal disc directs wing development in drosophila. Cell 75: 741-752.
10. Blair SS, (2001) Cell lineage: compartments and capricious. Curr Biol 11: R1017-R1021.
11. Rodriguez I, Basler K, (1997) Control of compartmental affinity boundaries by hedgehog. Nature 389: 614-618.
12. Lecuit T, Lenne PF, (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8: 633-644.
13. Garcia-Bellido A, Ripoll P, Morata G, (1973) Developmental compartmentalization of wing disk of drosophila. Nature New Biol 245: 251-253.
14. Blair SS, (2003) Lineage compartments in drosophila. Curr Biol 13: R548-R551.
15. González-Gaitán M, Capdevila MP, García-Bellido A, (1994) Cell proliferation patterns in the wing imaginal disc of drosophila. Mech Dev 46: 183-200.
16. Dahmann C, Basler K, (1999) Compartment boundaries: at the edge of development. Trends Genet 15: 320-326.
17. Irvine KD, Rauskolb C, (2001) Boundaries in development: formation and function. Annu Rev Cell Dev Biol 17: 189-214.
18. Tepass U, Godt D, Winklbauer R, (2002) Cell sorting in animal development: signalling and adhesive mechanisms in the formation of tissue boundaries. Curr Opin Genet Dev 12: 572-582.
19. Blair SS, (2003) Developmental biology: boundary lines. Nature 424: 379-381.
20. Neumann C, Cohen S, (1997) Long-range action of wingless organizes the dorsal-ventral axis of the drosophila wing. Development 124: 871-880.
21. Wolpert L, (1969) Positional information and spatial pattern of cellular differentiation. J Theor Biol 25: 1-47.
22. Zecca M, Basler K, Struhl G, (1996) Direct and long-range action of a wingless morphogen gradient. Cell 87: 833-844.
23. Nellen D, Burke R, Struhl G, Basler K, (1996) Direct and long-range action of a dpp morphogen gradient. Cell 85: 357-368.
24. Crozatier M, Glise B, Vincent A, (2004) Patterns in evolution: veins of the drosophila wing. Trends Genet 20: 498-505.
25. Affolter M, Basler K, (2007) The decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet 8: 663-674.
26. Micchelli CA, Rulifson EJ, Blair SS, (1997) The function and regulation of cut expression on the wing margin of drosophila: Notch, wingless and a dominant negative role for delta and serrate. Development 124: 1485-1495.
27. Buceta J, Herranz H, Canela-Xandri O, Reigada R, Sagués F, et al. (2007) Robustness and stability of the gene regulatory network involved in dv boundary formation in the drosophila wing. PLoS ONE 2: e602.
28. Major RJ, Irvine KD, (2005) Inuence of notch on dorsoventral compartmentalization and actin organization in the drosophila wing. Development 132: 3823-3833.
29. Major RJ, Irvine KD, (2006) Localization and requirement for myosin ii at the dorsal-ventral compartment boundary of the drosophila wing. Dev Dyn 235: 3051-3058.
30. Giraldez AJ, Cohen SM, (2003) Wingless and notch signaling provide cell survival cues and control cell proliferation during wing development. Development 130: 6533-6543.
31. Herranz H, Milán M, (2006) Notch and afinity boundaries in drosophila. Bioessays 28: 113-116.
32. Monier B, Pélissier-Monier A, Brand AH, Sanson B, (2010) An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in drosophila embryos. Nat Cell Biol 12: 60-65 sup pp 1-9.
33. Canela-Xandri O, Sagués F, Reigada R, Buceta J, (2008) A spatial toggle switch drives boundary formation in development. Biophys J 95: 5111-5120.
34. Tabata T, Schwartz C, Gustavson E, Ali Z, Kornberg T, (1995) Creating a drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development 121: 3359-3369.
35. de Celis J, Garcia-Bellido A, Bray S, (1996) Activation and function of notch at the dorsal-ventral boundary of the wing imaginal disc. Development 122: 359-369.
36. Micchelli CA, Blair SS, (1999) Dorsoventral lineage restriction in wing imaginal discs requires notch. Nature 401: 473-476.
37. Becam I, Milán M, (2008) A permissive role of notch in maintaining the dv affinity boundary of the drosophila wing. Dev Biol 322: 190-198.
38. Koelzer S, Klein T, (2006) Regulation of expression of vg and establishment of the dorsoventral compartment boundary in the wing imaginal disc by suppressor of hairless. Dev Biol 289: 77-90.
39. Landsberg KP, Farhadifar R, Ranft J, Umetsu D, Widmann TJ, et al. (2009) Increased cell bond tension governs cell sorting at the drosophila anteroposterior compartment boundary. Curr Biol 19: 1950-1955.
40. Gong Y, Mo C, Fraser SE, (2004) Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430: 689-693.
41. Baena-López LA, Baonza A, García-Bellido A, (2005) The orientation of cell divisions determines the shape of drosophila organs. Curr Biol 15: 1640-1644.
42. Théry M, Racine V, Pépin A, Piel M, Chen Y, et al. (2005) The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol 7: 947-953.
43. Bittig T, Wartlick O, Kicheva A, González-Gaitán M, Jülicher F, (2008) Dynamics of anisotropic tissue growth. New J Phys 10: 063001.
44. Taylor J, Adler PN, (2008) Cell rearrangement and cell division during the tissue level morphogenesis of evaginating drosophila imaginal discs. Dev Biol 313: 739-751.
45. Aigouy B, Farhadifar R, Staple DB, Sagner A, Röper JC, et al. (2010) Cell ow reorients the axis of planar polarity in the wing epithelium of drosophila. Cell 142: 773-86.
46. Graner F, Glazier J, (1992) Simulation of biological cell sorting using a two-dimensional extended potts model. Phys Rev Lett 69: 2013-2016.
47. 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 Theor Biol 226: 439-453.
48. Aegerter-Wilmsen T, Aegerter CM, Hafen E, Basler K, (2007) Model for the regulation of size in the wing imaginal disc of drosophila. Mech Dev 124: 318-326.
49. Hufnagel L, Teleman AA, Rouault H, Cohen SM, Shraiman BI, (2007) On the mechanism of wing size determination in y development. Proc Natl Acad Sci U S A 104: 3835-3840.
50. Farhadifar R, Röper JC, Aigouy B, Eaton S, Jülicher F, (2007) The inuence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol 17: 2095-2104.
51. Nagai T, Honda H, (2009) Computer simulation of wound closure in epithelial tissues: Cell-basallamina adhesion. Phys Rev E 80: 061903.
52. Aegerter-Wilmsen T, Smith AC, Christen AJ, Aegerter CM, Hafen E, et al. (2010) Exploring the effects of mechanical feedback on epithelial topology. Development 137: 499-506.
53. Weliky M, Oster G, (1990) The mechanical basis of cell rearrangement. I. Epithelial morphogenesis during Fundulus epiboly. Development 109: 373-386.
54. Nagai T, Honda H, (2001) A dynamic cell model for the formation of epithelial tissues. Philos Mag Part B 81: 699-719.
55. Milán M, Campuzano S, García-Bellido A, (1996) Cell cycling and patterned cell proliferation in the wing primordium of drosophila. Proc Natl Acad Sci USA 93: 640-5.
56. Martín FA, Herrera SC, Morata G, (2009) Cell competition, growth and size control in the Drosophila wing imaginal disc. Development 136: 3747-3756.
57. O'Keefe DD, Thomas JB, (2001) Drosophila wing development in the absence of dorsal identity. Development 128: 703-710.
58. Sakaue-Sawano A, Kurokawa H, Morimura T, Hanyu A, Hama H, et al. (2008) Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132: 487-498.
59. Cohen M, Georgiou M, Stevenson NL, Miodownik M, Baum B, (2010) Dynamic filopodia transmit intermittent delta-notch signaling to drive pattern refinement during lateral inhibition. Dev Cell 19: 78-89.
60. Stavans J, (1993) The evolution of cellular structures. Rep Prog Phys 56: 733-789.
61. Smith J, Martin L, (1973) Do cells cycle? Proc Natl Acad Sci U S A 70: 1263-1267.
62. Shields R, (1978) Further evidence for a random transition in the cell cycle. Nature 273: 755-758.
63. Théry M, Bornens M, (2006) Cell shape and cell division. Curr Opin Cell Biol 18: 648-657.
64. Gibson WT, Veldhuis JH, Rubinstein B, Cartwright HN, Perrimon N, et al. (2011) Control of the mitotic cleavage plane by local epithelial topology. Cell 144: 427-38.
65. Minc N, Burgess D, Chang F, (2011) Influence of cell geometry on division-plane positioning. Cell 144: 414-26.
66. Johnston LA, Edgar BA, (1998) Wingless and notch regulate cell-cycle arrest in the developing drosophila wing. Nature 394: 82-84.
67. Herranz H, Pérez L, Martín FA, Milán M, (2008) A wingless and notch double-repression mechanism regulates g1-s transition in the drosophila wing. EMBO J 27: 1633-1645.
68. Dubatolova T, Omelyanchuk L, (2004) Analysis of cell proliferation in drosophila wing imaginal discs using mosaic clones. Heredity 92: 299-305.
69. Kicheva A, Pantazis P, Bollenbach T, Kalaidzidis Y, Bittig T, et al. (2007) Kinetics of morphogen gradient formation. Science 315: 521-525.
70. Cohen B, McGuffin ME, Pfeie C, Segal D, Cohen SM, (1992) apterous, a gene required for imaginal disc development in drosophila encodes a member of the lim family of developmental regulatory proteins. Genes Dev 6: 715-29.
71. Axelrod JD, Matsuno K, Artavanis-Tsakonas S, Perrimon N, (1996) Interaction between Wingless and Notch signaling pathways mediated by dishevelled. Science 271: 1826-1832.
72. Blair SS, (1993) Mechanisms of compartment formation: evidence that non-proliferating cells do not play a critical role in defining the d/v lineage restriction in the developing wing of drosophila. Development 119: 339-51.