Morphogenesis on the Multicellular Level: Patterns of Mechanical Stresses and Main Modes of Collective Cell Behavior

  • Lev V. BeloussovEmail author


Regular patterns of mechanical stresses are perfectly expressed on the macromorphological level in the embryos of all taxonomic groups studied in this respect. Stress patterns are characterized by the topological invariability retained during prolonged time periods and drastically changing in between. After explanting small pieces of embryonic tissues, they are restored within several dozens minutes. Disturbance of stress patterns in developing embryos irreversibly breaks the long-range order of subsequent development. Morphogenetically important stress patterns are established by three geometrically different modes of cell alignment: parallel, perpendicular, and oblique. The first of them creates prolonged files of actively elongated cells. The second is responsible for segregation of an epithelial layer to the domains of columnar and flattened cells. The model of this process, demonstrating its scaling capacities, is described. The third mode which follows the previous one is responsible for making the curvatures. It is associated with formation of “cell fans,” the universal devices for shapes formation due to slow relaxation of the stored elastic energy.


Blastula Stage Cell Alignment Amphibian Embryo Retraction Phase Tangential Tension 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aegerter-Wilmsen T, Smith AC, Christen AJ, Aegerter CM, Hafen E, Basler K (2010) Exploring the effects of mechanical feedback on epithelial topology. Development 137:499–506PubMedCrossRefGoogle Scholar
  2. Belintzev BN, Beloussov LV, Zaraiskii AG (1987) Model of pattern formation in epithelial morphogenesis. J Theor Biol 129:369–394CrossRefGoogle Scholar
  3. Belintzev BN (1988) Physical foundations of biological morphogenesis. Nauka, Moskva (in Russian)Google Scholar
  4. Beloussov LV (1988) Contact polarization of Xenopus laevis cells during gastrulation. Ontogenez (Sov J Devel Biol) 19:405–413Google Scholar
  5. Beloussov LV (1998) The dynamic architecture of a developing organism. Kluwer Academic Publishers, Dordrecht/Boston/LondonGoogle Scholar
  6. Beloussov LV (2013) Morphogenesis can be driven by properly parametrised mechanical feedback. Eur Phys J E 36:132–147PubMedCrossRefGoogle Scholar
  7. Beloussov LV, Badenko LA, Katchurin AL, Kurilo LF (1972) Cell movements in morphogenesis of hydroid polyps. J Embr Exp Morphol 27:317–337Google Scholar
  8. Beloussov LV, Bogdanovsky SB (1980) Cellular mechanisms of embryonic regulations in sea urchin embryos. Ontogenez (Sov J Devel Biol) 11:467–475Google Scholar
  9. Beloussov LV, Dorfman JG, Cherdantzev VG (1975) Mechanical stresses and morphological patterns in amphibian embryos. J Embr Exp Morphol 34:559–574Google Scholar
  10. Beloussov LV, Grabovsky VI (2005) A common biomechanical model for the formation of stationary cell domains and propagating waves in the developing organisms. Comput Methods Biomech Biomed Eng 8:381–391CrossRefGoogle Scholar
  11. Beloussov LV, Labas JA, Kazakova NI, Zaraisky AG (1989) Cytophysiology of growth pulsations in hydroid polyps. J Exp Zool 249:258–270CrossRefGoogle Scholar
  12. Beloussov LV, Lakirev AV (1988) Self-organization of biological morphogenesis: general approaches and topo-geometrical models. In: Thermodynamics and pattern formation in biology (I. Lamprecht, A.I. Zotineds). Walter de Gruyter, Berlin, pp 321–336Google Scholar
  13. Beloussov LV, Lakirev AV, Naumidi II, Novoselov VV (1990) Effects of relaxation of mechanical tensions upon the early morphogenesis of Xenopuslaevis embryos. Int J Dev Biol 34:409–419PubMedGoogle Scholar
  14. Beloussov LV, Luchinskaia NN (1983) A study of relay cell interactions in the explants of amphibian embryonic tissues. Tsitologia 25:939–944 (in Russian)Google Scholar
  15. Beloussov LV, Luchinskaia NN, Ermakov AS, Glagoleva NS (2006) Gastrulation in amphibian embryos, regarded as a succession of biomechanical feedback events. Int J Dev Biol 50:113–122PubMedCrossRefGoogle Scholar
  16. Beloussov LV, Luchinskaia NN, Stein AA (2000) Tension-dependent collective cell movements in the early gastrula ectoderm of Xenopus laevis embryos. Dev Genes Evol 210:92–104PubMedCrossRefGoogle Scholar
  17. Beloussov LV, Saveliev SV, Naumidi II, Novoselov VV (1994) Mechanical stresses in embryonic tissues: patterns, morphogenetic role and involvement in regulatory feedback. Int Rev Cytol 150:1–34PubMedCrossRefGoogle Scholar
  18. Brevier J, Montero D, Svitkina T, Riveline D (2008) The asymmetric self-assembly mechanism of adherent junctions: a cellular push-pull unit. Phys Biol 5(1):016005PubMedCrossRefGoogle Scholar
  19. Cherdantzev VG (2003) Morphogenesis and evolution. KMK, Moskva (in Russian)Google Scholar
  20. Cherdantzev VG (2006) The dynamic geometry of mass cell movements in animal morphogenesis. Int J Dev Biol 50:169–182CrossRefGoogle Scholar
  21. Cherdantzeva EM, Cherdantzev VG (2006) Geometry and mechanics of teleost gastrulation and the formation of primary embryonic axes. Int J Dev Biol 50:157–168CrossRefGoogle Scholar
  22. Chisholm AD, Hardin J (2005) Epidermal morphogenesis. WormBook 1–22Google Scholar
  23. Darken RS, Scola AM, Rakeman AS, Das G, Mlodzik M, Wilson PA (2002) The planar polarity gene strabismus regulates convergent extension movements in Xenopus. EMBO J 21(5):976–985PubMedCentralPubMedCrossRefGoogle Scholar
  24. Davidson LA, Marsden M, Keller R, Desimone DW (2006) Integrin alpha5beta1 and fibronectin regulate polarized cell protrusions required for Xenopus convergence and extension. Curr Biol 16(9):833–844PubMedCrossRefGoogle Scholar
  25. Elsdale T (1972) Pattern formation in fibroblast cultures: an inherently precise morphogenetic process. In: Waddington CH (ed) Towards a theoretical biology 4: essays. Edinburgh Univ Press, Edinburgh, pp 95–108Google Scholar
  26. Evstifeeva AJ, Kremnyov SV, Beloussov LV (2010) Topological and geometrical changes in Xenopus laevis embryonic epithelia under relaxation of mechanical tensions. Ontogenez (Russ J Dev Biol) 41:190–198Google Scholar
  27. Farge E (2003) Mechanical induction of twist in the drosophila foregut/stomodeal primordium. Curr Biol 13:1365–1377PubMedCrossRefGoogle Scholar
  28. Farhadifar R, Röper J-C, Algouy B, Eaton S, Jülicher F (2007) The influence of cell mechanics, cell-cell interactions and proliferation on epithelial packing. Curr Biol 17:2095–2104PubMedCrossRefGoogle Scholar
  29. Goto T, Keller R (2002) The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. Dev Biol 247(1):165–181PubMedCrossRefGoogle Scholar
  30. Gurwitsch AG (1914) Der Vererbungsmechanismus der form. Arch Entw-Mech 39:516–577Google Scholar
  31. Gustafson T, Wolpert L (1967) Cellular movements and contacts in sea urchin morphogenesis. Biol Rev 42:442–498PubMedCrossRefGoogle Scholar
  32. Hardin JD, Cheng LY (1986) The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation. Dev Biol 115:490–501CrossRefGoogle Scholar
  33. Harris AK, Stopak D, Warner P (1984) Generation of spatially periodic patterns by a mechanical instability: a mechanical alternative to the Turing model. J Embryol Exp Morphol 80:1–20PubMedGoogle Scholar
  34. Harris AK, Wild P, Stopak D (1980) Silicone rubber substrate: a new wrinkle in the study of cell locomotion. Science 208:177–179PubMedCrossRefGoogle Scholar
  35. Hofmann DK, Gottlieb M (1991) Bud formation in the scyphozoan Cassiopea andromeda: epithelial dynamics and fate map. Hydrobiologia 216(217):53–59CrossRefGoogle Scholar
  36. Hutson MS (2003) Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300:145–149PubMedCrossRefGoogle Scholar
  37. Isaeva VV, Kasyanov NV, Presnov EV (2012) Topological singularities and symmetry breaking in development. BioSystems 109:280–298PubMedCrossRefGoogle Scholar
  38. Johnson MH (1981) Membrane events associated with the generation of a blastocyst. Int Rev Cytol Suppl 12:1–37PubMedGoogle Scholar
  39. Kazakova NI, Zierold K, Plickert G, Labas JA, Beloussov LV (1994) X-ray microanalysis of ion contents in vacuoles and cytoplasm of the growing tips of a hydroid polyp as related to osmotic changes and growth pulsations. Tissue Cell 26:687–697PubMedCrossRefGoogle Scholar
  40. Keller R, Tibbetts P (1989) Mediolateral cell intercalation in the dorsal, axial mesoderm of Xenopus laevis. Dev Biol 131(2):539–549PubMedCrossRefGoogle Scholar
  41. Kinoshita N, Iioka H, Miyakoshi A, Ueno N (2003) PKC delta is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. Genes Dev 17(13):1663–1676PubMedCentralPubMedCrossRefGoogle Scholar
  42. Kornikova ES, Korvin-Pavlovskaya EG, Beloussov LV (2009) Relocations of cell convergence sites and formation of pharyngula-like shapes in mechanically relaxed Xenopus embryos. Dev Genes Evol 219:1–10PubMedCrossRefGoogle Scholar
  43. Kucera P, Monnet-Tschudi F (1987) Early functional differentiation in the chick embryonic disc: interactions between mechanical activity and extracellular matrix. J Cell Sci Suppl 8:415–432PubMedCrossRefGoogle Scholar
  44. Labas YA, Beloussov LV, Kazakova NI (1992) Kinematics, biological role and cytophysiology of growth pulsations in hydroid polyps. Tsitologia 34:5–23Google Scholar
  45. Liem T (2006) Morphodynamik in der Osteopathie. Hippokrates Verlag, StuttgartGoogle Scholar
  46. Marsden M, DeSimone DW (2003) Integrin-ECM interactions regulate cadherin-dependent cell adhesion and are required for convergent extension in Xenopus. Curr Biol 13(14):1182–1191PubMedCrossRefGoogle Scholar
  47. Martin AC, Kashube M, Wieshaus EF (2009) Pulsed contractions of an actomyosin network drive apical constriction. Nature 457:495–499PubMedCentralPubMedCrossRefGoogle Scholar
  48. Moore AR (1941) On the mechanisms of gastrulation in Dendraster excentricus. J Exp Zool 87:101–111CrossRefGoogle Scholar
  49. Naumidi II, Beloussov LV (1977) Contractility and epithelization of the axial mesoderm in the chick embryo. Ontogenez (Sov J Dev Biol) 8:517–520 (in Russian)Google Scholar
  50. Osterfeld M, Du XX, Schüpbach T, Wieschaus E, Shwartsman SY (2013) Three-dimensional epithelial morphogenesis in the developing Drosophila egg. Dev Cell 24:400–410CrossRefGoogle Scholar
  51. Otto JJ, Campbell RD (1977) Budding in hydra attenuate: bud stages and fate map. J Exp Zool 200:417–428PubMedCrossRefGoogle Scholar
  52. Peralta XG, Noyama Y, Hutson MS, Montague R, Vernakides S, Kiehart DP, Edwards GS (2007) Upregulation of forces and morphogenic asymmetries in dorsal closure during Drosophila development. Biophys J 92:2583–2596PubMedCentralPubMedCrossRefGoogle Scholar
  53. Petrov KV, Beloussov LV (1984) The kinetics of contact polarization of the cells in the induced tissues of amphibian embryos. Ontogenez (Sov J Dev Biol) 15:643–648Google Scholar
  54. Plickert G (1980) Mechanically induced stolon branching in Eirene viridula (Thecata, Campanulinidae). In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. Elsevier, North Holland, pp 185–193Google Scholar
  55. Rauzi M, Lenne P-F (2011) Cortical forces in cell shape changes and tissue morphogenesis. Curr Top Dev Biol 95:93–121PubMedCrossRefGoogle Scholar
  56. Saveliev SV (1988) Experimental studies of mechanical tensions in neuroepithelial brain layers. Ontogenez (Sov J Dev Biol) 19:165–174Google Scholar
  57. Saveliev SV, Besova NV (1990) Polarization of neuroepithelial cells after introduction of a portion of the neural tube into the neural cavity in amphibian embryos. Ontogenez (Sov J Dev Biol) 21:298–302Google Scholar
  58. Shih J, Keller R (1992) Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 116(4):901–914PubMedGoogle Scholar
  59. Steding G (1967) Ursachen der embryonalen Epithelverdickungen. Acta Anat 68:37–67PubMedCrossRefGoogle Scholar
  60. Sugimura K, Ishihara Shuji (2013) The mechanical anisotropy in a tissue promotes ordering in hexagonal cell packing. Development 140:4091–4101PubMedCrossRefGoogle Scholar
  61. Sumina EL, Sumin DL (2013) Morphogenesis in the aggregates of filamentous Cyanobacteria. Ontogenez (Russ J Dev Biol 44:203–220Google Scholar
  62. Tambe DT et al (2011) Collective cell guidance by cooperative intercellular forces. Nat Mater 10(6):469–475PubMedCentralPubMedCrossRefGoogle Scholar
  63. Thompson DA (1942, 2000) On growth and form. Cambridge University Press, CambridgeGoogle Scholar
  64. Trinkaus JP (1969) Cells into organs. The forces that shape the embryo. Prentice Hall, New JerseyGoogle Scholar
  65. Troshina TG, Glagoleva NS, Beloussov LV (2011) Statistical study of rapid mechanodependent cell movements in deformed explants in Xenopus laevis embryonic tissues. Ontogenez (Russ J Dev Biol) 42:301–310Google Scholar
  66. Vedula RK, Leong BC, Lai TL, Hersen P, Kabla AJ, Lim CT, Ladoux B (2012) Emerging modes of collective cell migration induced by geometrical constraints. PNAS 109:12974–12979PubMedCentralPubMedCrossRefGoogle Scholar
  67. Wallingford JB, Fraser SE, Harland RM (2002) Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev Cell 2(6):695–706PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of EmbryologyMoscow State UniversityMoscowRussia

Personalised recommendations