Cellular and Molecular Life Sciences

, Volume 68, Issue 11, pp 1897–1910 | Cite as

Establishment and maintenance of compartmental boundaries: role of contractile actomyosin barriers

  • Bruno MonierEmail author
  • Anne Pélissier-Monier
  • Bénédicte SansonEmail author


During animal development, tissues and organs are partitioned into compartments that do not intermix. This organizing principle is essential for correct tissue morphogenesis. Given that cell sorting defects during compartmentalization in humans are thought to cause malignant invasion and congenital defects such as cranio-fronto-nasal syndrome, identifying the molecular and cellular mechanisms that keep cells apart at boundaries between compartments is important. In both vertebrates and invertebrates, transcription factors and short-range signalling pathways, such as EPH/Ephrin, Hedgehog, or Notch signalling, govern compartmental cell sorting. However, the mechanisms that mediate cell sorting downstream of these factors have remained elusive for decades. Here, we review recent data gathered in Drosophila that suggest that the generation of cortical tensile forces at compartmental boundaries by the actomyosin cytoskeleton could be a general mechanism that inhibits cell mixing between compartments.


Compartment Boundary Lineage restriction Cell sorting Cell mixing Actin cytoskeleton Nonmuscle Myosin II Drosophila 



After egg laying




Cadherin 99C


Chromophore-assisted laser inactivation


Differential adhesion hypothesis






Filamentous actin




Leucine rich repeat


Second instar larva


Third instar larva


Myosin II Heavy Chain


Myosin II Regulatory Light Chain


Nonmuscle Myosin II










Zona limitans intrathalamica



This work has been supported by ARC (Association pour la Recherche contre le Cancer) and Herchel Smith fellowships to B.M., by an EMBO fellowship to A.P.-M. and by HSFP and Wellcome Trust grants to B.S. A.P.-M. would like to thank Andrea Brand for her support.

Supplementary material

18_2011_668_MOESM1_ESM.tif (5.6 mb)
Supplementary Figure S1: Mechanisms that could implement cell sorting at compartmental boundaries. a Differential adhesion: based on the analogy that liquids such as oil and water are immiscible due to distinct surface tension, it has been suggested that dissociated cells of distinct identities could sort according to their surface tension [1, 2]. It has been proposed that differential surface tension could be conferred by distinct adhesion molecules or by different levels of the same adhesion molecule. This hypothesis was validated in vitro by varying the levels or the nature of cadherins transfected in cultured cells [3]. This theory has been extrapolated to compartmental cell sorting [4–7]: here, the two cell populations express two distinct adhesion molecules: red and blue, respectively. However, one might note that additional parameters might come in the interplay to produce surface tension. In particular, surface tension probably relies on a balance between adhesion at the plasma membrane and contractibility at the cell cortex [8]. In other words, differential expression of adhesion molecules might not be the only strategy to produce differential surface tension between two groups of cells. b Extracellular matrix fence: in a tissue, two compartments could be kept separated by a groove filled with extracellular matrix that would act as a physical fence. c Nonproliferative zone: in a mitotically active epithelium, division of boundary cells could lead to an irregular boundary between two compartments. Inhibition of cell division a few rows of cells on each side of the compartmental boundary could prevent the boundary from being challenged, and thus maintain stable compartmentalization. In the Drosophila wing disc, Notch and Wingless signalling inhibits cell division close to the D/V boundary [9, 10]. d Local orientation of cell division axis: alternatively to c, the mitotic spindle of dividing boundary cells could be oriented so that boundary cells would divide parallel to the boundary. In this case, the progeny of dividing boundary cells would never be found in the opposite compartment, thereby preventing cell mixing. (TIFF 5778 kb)
18_2011_668_MOESM2_ESM.tif (1.7 mb)
Supplementary Figure S2: Cell behavior at morphogen-dependent boundaries. a Compartmentalization can be maintained by morphogen-dependent boundaries. Cell identity (blue) relies on reception of a given morphogen (green), and it changes when cells move too far away from the morphogen source. Stable compartmentalization maintained by morphogen-dependent boundaries does not involve physical segregation of cells. An example of morphogen-dependent boundary can be found in the Drosophila wing disc where the wing/notum boundary relies on reception of EGF signalling [11]. b In the Drosophila embryo at stages 8–11, anterior and posterior compartments are separated by parasegmental boundaries and by posterior-anterior (P-A) boundaries. P-A boundaries, at the level of which the segmental grooves will develop after stage 12, are morphogen-dependent boundaries: engrailed expression in posterior cells relies on reception of the Wingless morphogen secreted by cells of the anterior compartment that face the parasegmental boundary [12–15]. (TIFF 1752 kb)
18_2011_668_MOESM3_ESM.tif (721 kb)
Supplementary Figure S3: A narrow nonproliferative zone at theDrosophilawing disc A/P boundary? Schematization of the pattern of cell proliferation at boundaries in the Drosophila wing pouch showing the broad nonproliferative zone at the D/V boundary. A nonproliferative zone, although narrow, could also form at the A/P boundary in late third instar wing discs. The color-code is similar to the one used in figure 1, green indicates BrdU-positive cells of unknown identity. Schematization is based on the pattern of BrdU incorporation reported in Figure 1b of Johnston and Edgar (1998) [10]. A similar pattern was also reported in Figure 2A of Herranz and coworkers (2008) [9]. In the initial analysis by O’Brochta and Bryant (1985) [16], a nonproliferative zone was not identified at the A/P boundary. High resolution images of the pattern of BrdU incorporation in the more recent reports suggest that such a nonproliferative zone might exist at the A/P boundary after all, although its presence is not discussed by the authors [9, 10]. Additional experiments are required to clarify this situation. (TIFF 721 kb)
18_2011_668_MOESM4_ESM.tif (2.4 mb)
Supplementary Figure S4: Influence of the pattern of Myosin II activation upon groove formation. Top views (top) and cross-section (bottom) of the eye disc epithelium (left) and of the embryonic epithelium (right) showing the pattern of Myosin II activation (green) and the shape of the associated groove. (TIFF 2427 kb)
18_2011_668_MOESM5_ESM.doc (29 kb)
Supplementary material 5 (DOC 29 kb)


  1. 1.
    Garcia-Bellido A (1975) Genetic control of wing disc development in Drosophila. Ciba Found Symp 0:161–182PubMedGoogle Scholar
  2. 2.
    Garcia-Bellido A, Ripoll P, Morata G (1973) Developmental compartmentalisation of the wing disk of Drosophila. Nat New Biol 245:251–253PubMedCrossRefGoogle Scholar
  3. 3.
    Dahmann C, Basler K (1999) Compartment boundaries: at the edge of development. Trends Genet 15:320–326PubMedCrossRefGoogle Scholar
  4. 4.
    Irvine KD, Rauskolb C (2001) Boundaries in development: formation and function. Annu Rev Cell Dev Biol 17:189–214PubMedCrossRefGoogle Scholar
  5. 5.
  6. 6.
    Bryant PJ (1970) Cell lineage relationships in the imaginal wing disc of Drosophila melanogaster. Dev Biol 22:389–411PubMedCrossRefGoogle Scholar
  7. 7.
    Garcia-Bellido A, Ripoll P, Morata G (1976) Developmental compartmentalization in the dorsal mesothoracic disc of Drosophila. Dev Biol 48:132–147PubMedCrossRefGoogle Scholar
  8. 8.
    Lawrence PA (1973) A clonal analysis of segment development in Oncopeltus (Hemiptera). J Embryol Exp Morphol 30:681–699PubMedGoogle Scholar
  9. 9.
    Chen EH, Baker BS (1997) Compartmental organization of the Drosophila genital imaginal discs. Development 124:205–218PubMedGoogle Scholar
  10. 10.
    Vincent JP, O’Farrell PH (1992) The state of engrailed expression is not clonally transmitted during early Drosophila development. Cell 68:923–931PubMedCrossRefGoogle Scholar
  11. 11.
    Altabef M, Clarke JD, Tickle C (1997) Dorso-ventral ectodermal compartments and origin of apical ectodermal ridge in developing chick limb. Development 124:4547–4556PubMedGoogle Scholar
  12. 12.
    Arques CG, Doohan R, Sharpe J, Torres M (2007) Cell tracing reveals a dorsoventral lineage restriction plane in the mouse limb bud mesenchyme. Development 134:3713–3722PubMedCrossRefGoogle Scholar
  13. 13.
    Reintsch WE, Habring-Mueller A, Wang RW, Schohl A, Fagotto F (2005) Beta-catenin controls cell sorting at the notochord-somite boundary independently of cadherin-mediated adhesion. J Cell Biol 170:675–686PubMedCrossRefGoogle Scholar
  14. 14.
    Fraser S, Keynes R, Lumsden A (1990) Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344:431–435PubMedCrossRefGoogle Scholar
  15. 15.
    Inoue T, Tanaka T, Takeichi M, Chisaka O, Nakamura S, Osumi N (2001) Role of cadherins in maintaining the compartment boundary between the cortex and striatum during development. Development 128:561–569PubMedGoogle Scholar
  16. 16.
  17. 17.
  18. 18.
    Langenberg T, Brand M (2005) Lineage restriction maintains a stable organizer cell population at the zebrafish midbrain-hindbrain boundary. Development 132:3209–3216PubMedCrossRefGoogle Scholar
  19. 19.
    Jimenez-Guri E, Udina F, Colas JF, Sharpe J, Padron-Barthe L, Torres M, Pujades C (2010) Clonal analysis in mice underlines the importance of rhombomeric boundaries in cell movement restriction during hindbrain segmentation. PLoS One 5:e10112PubMedCrossRefGoogle Scholar
  20. 20.
    Lawrence PA, Struhl G (1996) Morphogens, compartments, and pattern: lessons from Drosophila? Cell 85:951–961PubMedCrossRefGoogle Scholar
  21. 21.
    Davy A, Bush JO, Soriano P (2006) Inhibition of gap junction communication at ectopic Eph/ephrin boundaries underlies craniofrontonasal syndrome. PLoS Biol 4:1763–1776CrossRefGoogle Scholar
  22. 22.
    Perez-Pomares JM, Foty RA (2006) Tissue fusion and cell sorting in embryonic development and disease: biomedical implications. Bioessays 28:809–821PubMedCrossRefGoogle Scholar
  23. 23.
    Twigg SR, Kan R, Babbs C, Bochukova EG, Robertson SP, Wall SA, Morriss-Kay GM, Wilkie AO (2004) Mutations of ephrin-B1 (EFNB1), a marker of tissue boundary formation, cause craniofrontonasal syndrome. Proc Natl Acad Sci USA 101:8652–8657PubMedCrossRefGoogle Scholar
  24. 24.
    Dahmann C, Basler K (2000) Opposing transcriptional outputs of Hedgehog signaling and Engrailed control compartmental cell sorting at the Drosophila A/P boundary. Cell 100:411–422PubMedCrossRefGoogle Scholar
  25. 25.
    Morata G, Lawrence PA (1975) Control of compartment development by the engrailed gene in Drosophila. Nature 255:614–617PubMedCrossRefGoogle Scholar
  26. 26.
    Blair SS, Ralston A (1997) Smoothened-mediated Hedgehog signalling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila. Development 124:4053–4063PubMedGoogle Scholar
  27. 27.
    Rodriguez I, Basler K (1997) Control of compartmental affinity boundaries by Hedgehog. Nature 389:614–618PubMedCrossRefGoogle Scholar
  28. 28.
    Shen J, Dahmann C (2005) The role of Dpp signaling in maintaining the Drosophila anteroposterior compartment boundary. Dev Biol 279:31–43PubMedCrossRefGoogle Scholar
  29. 29.
    Micchelli CA, Blair SS (1999) Dorsoventral lineage restriction in wing imaginal discs requires Notch. Nature 401:473–476PubMedCrossRefGoogle Scholar
  30. 30.
    Rauskolb C, Correia T, Irvine KD (1999) Fringe-dependent separation of dorsal and ventral cells in the Drosophila wing. Nature 401:476–480PubMedCrossRefGoogle Scholar
  31. 31.
    Milan M, Cohen SM (1999) Notch signaling is not sufficient to define the affinity boundary between dorsal and ventral compartments. Mol Cell 4:1073–1078PubMedCrossRefGoogle Scholar
  32. 32.
    Milan M, Cohen SM (2003) A re-evaluation of the contributions of Apterous and Notch to the dorsoventral lineage restriction boundary in the Drosophila wing. Development 130:553–562PubMedCrossRefGoogle Scholar
  33. 33.
    O’Keefe DD, Thomas JB (2001) Drosophila wing development in the absence of dorsal identity. Development 128:703–710PubMedGoogle Scholar
  34. 34.
    Cheng YC, Amoyel M, Qiu X, Jiang YJ, Xu Q, Wilkinson DG (2004) Notch activation regulates the segregation and differentiation of rhombomere boundary cells in the zebrafish hindbrain. Dev Cell 6:539–550PubMedCrossRefGoogle Scholar
  35. 35.
    Cooke JE, Kemp HA, Moens CB (2005) EphA4 is required for cell adhesion and rhombomere-boundary formation in the zebrafish. Curr Biol 15:536–542PubMedCrossRefGoogle Scholar
  36. 36.
    Mellitzer G, Xu Q, Wilkinson DG (1999) Eph receptors and ephrins restrict cell intermingling and communication. Nature 400:77–81PubMedCrossRefGoogle Scholar
  37. 37.
    Xu Q, Mellitzer G, Robinson V, Wilkinson DG (1999) In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399:267–271PubMedCrossRefGoogle Scholar
  38. 38.
  39. 39.
    Steinberg MS (1970) Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J Exp Zool 173:395–433PubMedCrossRefGoogle Scholar
  40. 40.
    Lawrence PA, Casal J, Struhl G (1999) The Hedgehog morphogen and gradients of cell affinity in the abdomen of Drosophila. Development 126:2441–2449PubMedGoogle Scholar
  41. 41.
    Milan M, Weihe U, Perez L, Cohen SM (2001) The LRR proteins Capricious and Tartan mediate cell interactions during DV boundary formation in the Drosophila wing. Cell 106:785–794PubMedCrossRefGoogle Scholar
  42. 42.
    Schlichting K, Demontis F, Dahmann C (2005) Cadherin Cad99C is regulated by Hedgehog signaling in Drosophila. Dev Biol 279:142–154PubMedCrossRefGoogle Scholar
  43. 43.
    Wei SY, Escudero LM, Yu F, Chang LH, Chen LY, Ho YH, Lin CM, Chou CS, Chia W, Modolell J et al (2005) Echinoid is a component of adherens junctions that cooperates with DE-Cadherin to mediate cell adhesion. Dev Cell 8:493–504PubMedCrossRefGoogle Scholar
  44. 44.
    Bejarano F, Luque CM, Herranz H, Sorrosal G, Rafel N, Pham TT, Milan M (2008) A gain-of-function suppressor screen for genes involved in dorsal-ventral boundary formation in the Drosophila wing. Genetics 178:307–323PubMedCrossRefGoogle Scholar
  45. 45.
    Vegh M, Basler K (2003) A genetic screen for Hedgehog targets involved in the maintenance of the Drosophila anteroposterior compartment boundary. Genetics 163:1427–1438PubMedGoogle Scholar
  46. 46.
    Major RJ, Irvine KD (2005) Influence of Notch on dorsoventral compartmentalization and actin organization in the Drosophila wing. Development 132:3823–3833PubMedCrossRefGoogle Scholar
  47. 47.
    O’Brochta DA, Bryant PJ (1985) A zone of non-proliferating cells at a lineage restriction boundary in Drosophila. Nature 313:138–141PubMedCrossRefGoogle Scholar
  48. 48.
    Major RJ, Irvine KD (2006) Localization and requirement for Myosin II at the dorsal-ventral compartment boundary of the Drosophila wing. Dev Dyn 235:3051–3058PubMedCrossRefGoogle Scholar
  49. 49.
    Landsberg KP, Farhadifar R, Ranft J, Umetsu D, Widmann TJ, Bittig T, Said A, Julicher F, Dahmann C (2009) Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr Biol 19:1950–1955PubMedCrossRefGoogle Scholar
  50. 50.
    Monier B, Pelissier-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; suppl pp 61–69Google Scholar
  51. 51.
    Cohen SM (1993) Imaginal disc development. In: Bate MAE (ed) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 747–841Google Scholar
  52. 52.
    Martinez-Arias A, Lawrence PA (1985) Parasegments and compartments in the Drosophila embryo. Nature 313:639–642PubMedCrossRefGoogle Scholar
  53. 53.
    Larsen CW, Hirst E, Alexandre C, Vincent JP (2003) Segment boundary formation in Drosophila embryos. Development 130:5625–5635PubMedCrossRefGoogle Scholar
  54. 54.
    Herranz H, Perez L, Martin FA, Milan M (2008) A Wingless and Notch double-repression mechanism regulates G1-S transition in the Drosophila wing. EMBO J 27:1633–1645PubMedCrossRefGoogle Scholar
  55. 55.
    Johnston LA, Edgar BA (1998) Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature 394:82–84PubMedCrossRefGoogle Scholar
  56. 56.
    Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster, 2nd edn. Spinger, Berlin, pp 287–308Google Scholar
  57. 57.
    Martinez-Arias A (1993) Development and patterning of the larval epidermis of Drosophila. In: Bate MAE (ed) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 517–608Google Scholar
  58. 58.
  59. 59.
    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. Nat Cell Biol 11:859–864PubMedCrossRefGoogle Scholar
  60. 60.
    Zallen JA, Wieschaus E (2004) Patterned gene expression directs bipolar planar polarity in Drosophila. Dev Cell 6:343–355PubMedCrossRefGoogle Scholar
  61. 61.
    Blankenship JT, Backovic ST, Sanny JS, Weitz O, Zallen JA (2006) Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev Cell 11:459–470PubMedCrossRefGoogle Scholar
  62. 62.
    Edwards KA, Chang XJ, Kiehart DP (1995) Essential light chain of Drosophila nonmuscle myosin II. J Muscle Res Cell Motil 16:491–498PubMedCrossRefGoogle Scholar
  63. 63.
    Karess RE, Chang XJ, Edwards KA, Kulkarni S, Aguilera I, Kiehart DP (1991) The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65:1177–1189PubMedCrossRefGoogle Scholar
  64. 64.
    Young PE, Richman AM, Ketchum AS, Kiehart DP (1993) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7:29–41PubMedCrossRefGoogle Scholar
  65. 65.
    Jacobson K, Rajfur Z, Vitriol E, Hahn K (2008) Chromophore-assisted laser inactivation in cell biology. Trends Cell Biol 18:443–450PubMedCrossRefGoogle Scholar
  66. 66.
    Jay DG (1988) Selective destruction of protein function by chromophore-assisted laser inactivation. Proc Natl Acad Sci USA 85:5454–5458PubMedCrossRefGoogle Scholar
  67. 67.
    Horstkotte E, Schroder T, Niewohner J, Jay DG, Henning SW (2005) Toward understanding the mechanism of chromophore-assisted laser inactivation—evidence for the primary photochemical steps. Photochem Photobiol 81:358–366PubMedCrossRefGoogle Scholar
  68. 68.
    Liao JC, Roider J, Jay DG (1994) Chromophore-assisted laser inactivation of proteins is mediated by the photogeneration of free-radicals. Proc Natl Acad Sci USA 91:2659–2663PubMedCrossRefGoogle Scholar
  69. 69.
    Yan P, Xiong Y, Chen B, Negash S, Squier T, Mayer MU (2006) Fluorophore-assisted light inactivation of Calmodulin involves singlet-oxygen mediated cross-linking and methionine oxidation. Biochemistry 45:4736–4748PubMedCrossRefGoogle Scholar
  70. 70.
    Martin AC (2010) Pulsation and stabilization: contractile forces that underlie morphogenesis. Dev Biol 341:114–125PubMedCrossRefGoogle Scholar
  71. 71.
    Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10:778–790PubMedCrossRefGoogle Scholar
  72. 72.
    Escudero LM, Bischoff M, Freeman M (2007) Myosin II regulates complex cellular arrangement and epithelial architecture in Drosophila. Dev Cell 13:717–729PubMedCrossRefGoogle Scholar
  73. 73.
    Brower D, Smith R, Wilcox M (1982) Cell shapes on the surface of the Drosophila wing imaginal disc. J Embryol Exp Morphol 67:137–151Google Scholar
  74. 74.
    Larsen C, Bardet PL, Vincent JP, Alexandre C (2008) Specification and positioning of parasegment grooves in Drosophila. Dev Biol 321:310–318PubMedCrossRefGoogle Scholar
  75. 75.
    Shen J, Dorner C, Bahlo A, Pflugfelder GO (2008) Optomotor-blind suppresses instability at the A/P compartment boundary of the Drosophila wing. Mech Dev 125:233–246PubMedCrossRefGoogle Scholar
  76. 76.
    Umemori M, Takemura M, Maeda K, Ohba K, Adachi-Yamada T (2007) Drosophila T-box transcription factor Optomotor-blind prevents pathological folding and local overgrowth in wing epithelium through confining Hh signal. Dev Biol 308:68–81PubMedCrossRefGoogle Scholar
  77. 77.
    Kunda P, Pelling AE, Liu T, Baum B (2008) Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr Biol 18:91–101PubMedCrossRefGoogle Scholar
  78. 78.
    Masucci JD, Miltenberger RJ, Hoffmann FM (1990) Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal disks is regulated by 3′ cis-regulatory elements. Genes Dev 4:2011–2023PubMedCrossRefGoogle Scholar
  79. 79.
    Padgett RW, St Johnston RD, Gelbart WM (1987) A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-beta family. Nature 325:81–84PubMedCrossRefGoogle Scholar
  80. 80.
    Corrigall D, Walther RF, Rodriguez L, Fichelson P, Pichaud F (2007) Hedgehog signaling is a principal inducer of Myosin-II-driven cell ingression in Drosophila epithelia. Dev Cell 13:730–742PubMedCrossRefGoogle Scholar
  81. 81.
    Laplante C, Nilson LA (2006) Differential expression of the adhesion molecule echinoid drives epithelial morphogenesis in Drosophila. Development 133:3255–3264PubMedCrossRefGoogle Scholar
  82. 82.
    Krieg M, Arboleda-Estudillo Y, Puech PH, Kafer J, Graner F, Muller DJ, Heisenberg CP (2008) Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 10:429–436PubMedCrossRefGoogle Scholar
  83. 83.
    Fernandez-Gonzalez R, Simoes Sde M, Roper JC, Eaton S, Zallen JA (2009) Myosin II dynamics are regulated by tension in intercalating cells. Dev Cell 17:736–743PubMedCrossRefGoogle Scholar
  84. 84.
  85. 85.
    Manning ML, Foty RA, Steinberg MS, Schoetz EM (2010) Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. Proc Natl Acad Sci USA 107:12517–12522PubMedCrossRefGoogle Scholar
  86. 86.
    Simoes Sde M, Blankenship JT, Weitz O, Farrell DL, Tamada M, Fernandez-Gonzalez R, Zallen JA (2010) Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation. Dev Cell 19:377–388PubMedCrossRefGoogle Scholar
  87. 87.
    Huber AB, Kolodkin AL, Ginty DD, Cloutier J-Fo (2003) Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26:509–563PubMedCrossRefGoogle Scholar
  88. 88.
    Ogita H, Kunimoto S, Kamioka Y, Sawa H, Masuda M, Mochizuki N (2003) EphA4-mediated rho activation via Vsm-RhoGEF expressed specifically in vascular smooth muscle cells. Circ Res 93:23–31PubMedCrossRefGoogle Scholar
  89. 89.
    Townes PL, Holtfreter J (1955) Directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool 128:53–120CrossRefGoogle Scholar
  90. 90.
    Harris AK (1976) Is cell sorting caused by differences in the work of intercellular adhesion? A critique of the Steinberg hypothesis. J Theor Biol 61:267–285PubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  1. 1.Department of Physiology, Development and NeuroscienceCambridgeUK
  2. 2.Wellcome Trust, Cancer Research UK Gurdon InstituteUniversity of CambridgeCambridgeUK
  3. 3.Institut de Biologie du Développement de Marseille-LuminyUMR6216, Campus de LuminyMarseille cedex 9France

Personalised recommendations