Abstract
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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Notes
- 1.
The eccentricity, denoted e or \( \varepsilon \), is a measure of how much any conic section deviates from being circular. For our purposes, it is enough to know that the eccentricity of a circle is zero and the eccentricity of an ellipse which is not a circle is greater than zero but less than 1.
References
Aegerter-Wilmsen T, Smith AC, Christen AJ, Aegerter CM, Hafen E, Basler K (2010) Exploring the effects of mechanical feedback on epithelial topology. Development 137:499–506
Belintzev BN, Beloussov LV, Zaraiskii AG (1987) Model of pattern formation in epithelial morphogenesis. J Theor Biol 129:369–394
Belintzev BN (1988) Physical foundations of biological morphogenesis. Nauka, Moskva (in Russian)
Beloussov LV (1988) Contact polarization of Xenopus laevis cells during gastrulation. Ontogenez (Sov J Devel Biol) 19:405–413
Beloussov LV (1998) The dynamic architecture of a developing organism. Kluwer Academic Publishers, Dordrecht/Boston/London
Beloussov LV (2013) Morphogenesis can be driven by properly parametrised mechanical feedback. Eur Phys J E 36:132–147
Beloussov LV, Badenko LA, Katchurin AL, Kurilo LF (1972) Cell movements in morphogenesis of hydroid polyps. J Embr Exp Morphol 27:317–337
Beloussov LV, Bogdanovsky SB (1980) Cellular mechanisms of embryonic regulations in sea urchin embryos. Ontogenez (Sov J Devel Biol) 11:467–475
Beloussov LV, Dorfman JG, Cherdantzev VG (1975) Mechanical stresses and morphological patterns in amphibian embryos. J Embr Exp Morphol 34:559–574
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 8:381–391
Beloussov LV, Labas JA, Kazakova NI, Zaraisky AG (1989) Cytophysiology of growth pulsations in hydroid polyps. J Exp Zool 249:258–270
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 321–336
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 34:409–419
Beloussov LV, Luchinskaia NN (1983) A study of relay cell interactions in the explants of amphibian embryonic tissues. Tsitologia 25:939–944 (in Russian)
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 50:113–122
Beloussov LV, Luchinskaia NN, Stein AA (2000) Tension-dependent collective cell movements in the early gastrula ectoderm of Xenopus laevis embryos. Dev Genes Evol 210:92–104
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 150:1–34
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):016005
Cherdantzev VG (2003) Morphogenesis and evolution. KMK, Moskva (in Russian)
Cherdantzev VG (2006) The dynamic geometry of mass cell movements in animal morphogenesis. Int J Dev Biol 50:169–182
Cherdantzeva EM, Cherdantzev VG (2006) Geometry and mechanics of teleost gastrulation and the formation of primary embryonic axes. Int J Dev Biol 50:157–168
Chisholm AD, Hardin J (2005) Epidermal morphogenesis. WormBook 1–22
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):976–985
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):833–844
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 95–108
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) 41:190–198
Farge E (2003) Mechanical induction of twist in the drosophila foregut/stomodeal primordium. Curr Biol 13:1365–1377
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 17:2095–2104
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):165–181
Gurwitsch AG (1914) Der Vererbungsmechanismus der form. Arch Entw-Mech 39:516–577
Gustafson T, Wolpert L (1967) Cellular movements and contacts in sea urchin morphogenesis. Biol Rev 42:442–498
Hardin JD, Cheng LY (1986) The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation. Dev Biol 115:490–501
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 80:1–20
Harris AK, Wild P, Stopak D (1980) Silicone rubber substrate: a new wrinkle in the study of cell locomotion. Science 208:177–179
Hofmann DK, Gottlieb M (1991) Bud formation in the scyphozoan Cassiopea andromeda: epithelial dynamics and fate map. Hydrobiologia 216(217):53–59
Hutson MS (2003) Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300:145–149
Isaeva VV, Kasyanov NV, Presnov EV (2012) Topological singularities and symmetry breaking in development. BioSystems 109:280–298
Johnson MH (1981) Membrane events associated with the generation of a blastocyst. Int Rev Cytol Suppl 12:1–37
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 26:687–697
Keller R, Tibbetts P (1989) Mediolateral cell intercalation in the dorsal, axial mesoderm of Xenopus laevis. Dev Biol 131(2):539–549
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):1663–1676
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 219:1–10
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 8:415–432
Labas YA, Beloussov LV, Kazakova NI (1992) Kinematics, biological role and cytophysiology of growth pulsations in hydroid polyps. Tsitologia 34:5–23
Liem T (2006) Morphodynamik in der Osteopathie. Hippokrates Verlag, Stuttgart
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):1182–1191
Martin AC, Kashube M, Wieshaus EF (2009) Pulsed contractions of an actomyosin network drive apical constriction. Nature 457:495–499
Moore AR (1941) On the mechanisms of gastrulation in Dendraster excentricus. J Exp Zool 87:101–111
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)
Osterfeld M, Du XX, Schüpbach T, Wieschaus E, Shwartsman SY (2013) Three-dimensional epithelial morphogenesis in the developing Drosophila egg. Dev Cell 24:400–410
Otto JJ, Campbell RD (1977) Budding in hydra attenuate: bud stages and fate map. J Exp Zool 200:417–428
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 92:2583–2596
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) 15:643–648
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 185–193
Rauzi M, Lenne P-F (2011) Cortical forces in cell shape changes and tissue morphogenesis. Curr Top Dev Biol 95:93–121
Saveliev SV (1988) Experimental studies of mechanical tensions in neuroepithelial brain layers. Ontogenez (Sov J Dev Biol) 19:165–174
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) 21:298–302
Shih J, Keller R (1992) Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 116(4):901–914
Steding G (1967) Ursachen der embryonalen Epithelverdickungen. Acta Anat 68:37–67
Sugimura K, Ishihara Shuji (2013) The mechanical anisotropy in a tissue promotes ordering in hexagonal cell packing. Development 140:4091–4101
Sumina EL, Sumin DL (2013) Morphogenesis in the aggregates of filamentous Cyanobacteria. Ontogenez (Russ J Dev Biol 44:203–220
Tambe DT et al (2011) Collective cell guidance by cooperative intercellular forces. Nat Mater 10(6):469–475
Thompson DA (1942, 2000) On growth and form. Cambridge University Press, Cambridge
Trinkaus JP (1969) Cells into organs. The forces that shape the embryo. Prentice Hall, New Jersey
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) 42:301–310
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 109:12974–12979
Wallingford JB, Fraser SE, Harland RM (2002) Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev Cell 2(6):695–706
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Beloussov, L.V. (2015). Morphogenesis on the Multicellular Level: Patterns of Mechanical Stresses and Main Modes of Collective Cell Behavior. In: Morphomechanics of Development. Springer, Cham. https://doi.org/10.1007/978-3-319-13990-6_3
Download citation
DOI: https://doi.org/10.1007/978-3-319-13990-6_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-13989-0
Online ISBN: 978-3-319-13990-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)