Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T11:59:18.577Z Has data issue: false hasContentIssue false
  • English
  • Français

The Role of Cell-Cell Adhesion in the Formation of Multicellular Sprouts

Published online by Cambridge University Press:  03 February 2010

A. Szabó  and
A. Czirók
A. Szabó
Affiliation:
Department of Biological Physics, Eötvos University, Budapest, Hungary
A. Czirók*
Affiliation:
Department of Biological Physics, Eötvos University, Budapest, Hungary Department of Anatomy & Cell Biology, University of Kansas Medical Center Kansas City, KS, USA
*
*Corresponding author: aczirok@kumc.edu
Get access

Abstract

Collective cell motility and its guidance via cell-cell contacts is instrumental in several morphogenetic and pathological processes such as vasculogenesis or tumor growth. Multicellular sprout elongation, one of the simplest cases of collective motility, depends on a continuous supply of cells streaming along the sprout towards its tip. The phenomenon is often explained as leader cells pulling the rest of the sprout forward via cell-cell adhesion. Building on an empirically demonstrated analogy between surface tension and cell-cell adhesion, we demonstrate that such a mechanism is unable to recruit cells to the sprout. Moreover, the expansion of such hypothetical sprouts is limited by a form of the Plateau-Taylor instability. In contrast, actively moving cells – guided by cell-cell contacts – can readily populate and expand linear sprouts. We argue that preferential attraction to the surfaces of elongated cells can provide a generic mechanism, shared by several cell types, for multicellular sprout formation.

Keywords

sproutingleader cellPotts model
Type
Research Article
Information
Mathematical Modelling of Natural Phenomena , Volume 5 , Issue 1: Cell migration , 2010 , pp. 106 - 122
Copyright
© EDP Sciences, 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alber, M., Chen, N., Glimm, T., Lushnikov, P. M.. Multiscale dynamics of biological cells with chemotactic interactions: from a discrete stochastic model to a continuous description . Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 73 (2006), No. 5/1, 051901. CrossRefGoogle ScholarPubMed
Bauer, A. L., Jackson, T. L. Jiang, Y.. A cell-based model exhibiting branching and anastomosis during tumor-induced angiogenesis . Biophys. J., 92 (2007), No. 9, 3105–3121 CrossRefGoogle ScholarPubMed
A. L. Bauer, T. L. Jackson, Y. Jiang. Topography of extracellular matrix mediates vascular morphogenesis and migration speeds in angiogenesis. PLOS Comp. Biol., (in press), 2009.
Belmonte, J. M., Thomas, G. L., Brunnet, L. G., de Almeida, R. M. C., Chaté, H.. Self-propelled particle model for cell-sorting phenomena . Phys. Rev. Lett., 100 (2008), No. 24, 248702. CrossRefGoogle ScholarPubMed
Beysens, D. A., Forgacs, G. Glazier, J. A.. Cell sorting is analogous to phase ordering in fluids . PNAS, 97 (2000), 9467–71 CrossRefGoogle ScholarPubMed
Czirók, A., Zamir, E. A., Szabó, A. Little, C. D.. Multicellular sprouting during vasculogenesis . Curr. Top. Dev. Biol., 81 (2008), 269–289 CrossRefGoogle ScholarPubMed
Dawes, A. T. Edelstein-Keshet, L.. Phosphoinositides and rho proteins spatially regulate actin polymerization to initiate and maintain directed movement in a one-dimensional model of a motile cell . Biophys. J., 92 (2007), No. 3, 744–768 CrossRefGoogle Scholar
P. G. de Gennes, F. Brochard-Wyart, D. Quere. Capillarity and wetting phenomena. Springer, New York, 2003.
Dipasquale, A.. Locomotion of epithelial cells. Factors involved in extension of the leading edge . Exp. Cell Res., 95 (1975), No. 2, 425–439 CrossRefGoogle ScholarPubMed
Roure, O. du, Saez, A., Buguin, A., Austin, R. H., Chavrier, P., Silberzan, P. Ladoux, B.. Force mapping in epithelial cell migration . Proc. Natl. Acad. Sci. U S A, 102 (2005), No. 7, 2390–2395 CrossRefGoogle ScholarPubMed
Forgacs, G., Foty, R. A., Shafrir, Y. Steinberg, M. S.. Viscoelastic properties of living embryonic tissues: a quantitative study . Biophys. J., 74 (1998), No. 5, 2227–2234 CrossRefGoogle ScholarPubMed
Foty, R. A., Pfleger, C. M., Forgacs, G. Steinberg, M. S.. Surface tensions of embryonic tissues predict their mutual envelopment behavior . Development, 122 (1996), No. 5, 1611–1620 Google ScholarPubMed
Foty, R. A. Steinberg, M. S.. The differential adhesion hypothesis: a direct evaluation . Dev. Biol., 278 (2005), No. 1 , 255–263 CrossRefGoogle Scholar
Friedl, P.. Dynamic imaging of cellular interactions with extracellular matrix . Histochem. Cell Biol., 122 (2004), 183–90 CrossRefGoogle ScholarPubMed
Friedl, P. Wolf, K.. Tube travel: the role of proteases in individual and collective cancer cell invasion . Cancer Res., 68 (2008), No. 18, 7247–7249 CrossRefGoogle ScholarPubMed
Gamba, A., Ambrosi, D., Coniglio, A., de Candia, A., Di Talia, S., Giraudo, E., Serini, G., Preziosi, L., Bussolino, F.. Percolation, morphogenesis, and burgers dynamics in blood vessels formation . Phys. Rev. Lett., 90 (2003), No. 11, 118101. CrossRefGoogle ScholarPubMed
Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. Betsholtz, C.. Vegf guides angiogenic sprouting utilizing endothelial tip cell filopodia . J. Cell Biol., 161 (2003), No. 6, 1163–1177 CrossRefGoogle ScholarPubMed
Glazier, J. A. Graner, F.. Simulation of the differential adhesion driven rearrangement of biological cells . Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics, 47 (1993), No. 3, 2128–2154 Google Scholar
Graner, F. Glazier, J. A.. Simulation of biological cell sorting using a two-dimensional extended potts model . Phys. Rev. Lett., 69 (1992), No. 13, 2013–2016 CrossRefGoogle Scholar
Gray, D. S., Tien, J. Chen, C. S.. Repositioning of cells by mechanotaxis on surfaces with micropatterned young’s modulus . J. Biomed. Mater. Res. A., 66 (2003), 605–14 CrossRefGoogle ScholarPubMed
Hegedüs, B., Marga, F., Jakab, K., Sharpe-Timms, K. L. Forgacs, G.. The interplay of cell-cell and cell-matrix interactions in the invasive properties of brain tumors . Biophysical J., 91 (2006), No. 7, 2708–16 CrossRefGoogle ScholarPubMed
Hogan, K. A. Bautch, V. L.. Blood vessel patterning at the embryonic midline . Curr. Top. Dev. Biol., 62 (2004), 55–85 CrossRefGoogle ScholarPubMed
Hutson, M. S., Brodland, G. W., Yang, J., Viens, D.. Cell sorting in three dimensions: topology, fluctuations, and fluidlike instabilities . Phys. Rev. Lett., 101 (2008), No. 14, 148105. CrossRefGoogle ScholarPubMed
Izaguirre, J. A., Chaturvedi, R., Huang, C., Cickovski, T., Coffland, J., Thomas, G., Forgacs, G., Alber, M., Hentschel, G., Newman, S. A., Glazier, J. A.. Compucell, a multi-model framework for simulation of morphogenesis . Bioinformatics, 20 (2004), No. 7, 1129–1137. CrossRefGoogle Scholar
Jiang, G., Huang, A. H., Cai, Y., Tanase, M. Sheetz, M. P.. Rigidity sensing at the leading edge through alphavbeta3 integrins and rptpalpha . Biophys J., 90 (2006), 1804–9 CrossRefGoogle ScholarPubMed
Kidoaki, S. Matsuda, T.. Shape-engineered fibroblasts: cell elasticity and actin cytoskeletal features characterized by fluorescence and atomic force microscopy . J. Biomed. Mater. Res. A., 81 (2007), No. 4, 803–810 CrossRefGoogle ScholarPubMed
Libotte, T., Kaiser, H. W., Alt, W., Bretschneider, T.. Polarity, protrusion-retraction dynamics and their interplay during keratinocyte cell migration . Exp. Cell Res., 270 (2001), No 2, 129–137. CrossRefGoogle ScholarPubMed
Lo, C. M., Wang, H. B., Dembo, M. Wang, Y. L.. Cell movement is guided by the rigidity of the substrate . Biophys J., 79 (2000), No. 1 , 144–152 CrossRefGoogle Scholar
Manoussaki, D., Lubkin, S. R., Vernon, R. B. Murray, J. D.. A mechanical model for the formation of vascular networks in vitro . Acta Biotheor, 44 (1996), No. 3-4, 271–282 CrossRefGoogle ScholarPubMed
Merks, R. M., Brodsky, S. V., Goligorksy, M. S., Newman, S. A. Glazier, J. A.. Cell elongation is key to in silico replication of in vitro vasculogenesis and subsequent remodeling . Dev. Biol., 289 (2006), 44–54 CrossRefGoogle ScholarPubMed
Merks, R. M. H., Perryn, E. D., Shirinifard, A., Glazier, J. A.. Contact-inhibited chemotaxis in de novo and sprouting blood-vessel growth . PLoS Comput. Biol., 4 (2008), No. 9, e1000163. CrossRefGoogle ScholarPubMed
Montell, D. J.. Morphogenetic cell movements: diversity from modular mechanical properties . Science, 322 (2008), No. 5907, 1502–1505 CrossRefGoogle ScholarPubMed
J. D. Murray. Mathematical Biology. Springer Verlag, Berlin, 2nd edition, 2003.
J. D. Murray, D. Manoussaki, S. R. Lubkin, R. Vernon. A mechanical theory of in vitro vascular network formation. In C. D. Little, V Mironov, and E. H. Sage, editors, Vascular morphogenesis: In vivo, in vitro, in mente., pages 223–239. Birkhauser, Boston, 1998.
Newman, T. J.. Modeling multicellular systems using subcellular elements . Math. Biosci. Eng., 2 (2005), 611–622 CrossRefGoogle ScholarPubMed
Perryn, E. D., Czirók, A. Little, C. D.. Vascular sprout formation entails tissue deformations and ve-cadherin-dependent cell-autonomous motility . Dev. Biol., 313 (2008), 545–55 CrossRefGoogle ScholarPubMed
Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. Horwitz, A. R.. Cell migration: integrating signals from front to back . Science, 302 (2003), No. 5651, 1704–1709 CrossRefGoogle ScholarPubMed
Rieu, J. P., Upadhyaya, A., Glazier, J. A., Ouchi, N. B. Sawada, Y.. Diffusion and deformations of single hydra cells in cellular aggregates . Biophys J., 79 (2000), 1903–14 CrossRefGoogle ScholarPubMed
Rupp, P. A., Czirók, A. Little, C. D.. alphavbeta3 integrin-dependent endothelial cell dynamics in vivo . Development, 131 (2004), No. 12, 2887–97 CrossRefGoogle ScholarPubMed
Sawhney, R. K. Howard, J.. Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels . J. Cell Biol., 157 (2002), No. 6, 1083–1091 CrossRefGoogle Scholar
Selmeczi, D., Mosler, S., Hagedorn, P. H., Larsen, N. B. Flyvbjerg, H.. Cell motility as persistent random motion: theories from experiments . Biophys J., 89 (2005), 912–31 CrossRefGoogle ScholarPubMed
Serini, G., Ambrosi, D., Giraudo, E., Gamba, A., Preziosi, L. Bussolino, F.. Modeling the early stages of vascular network assembly . EMBO J., 22 (2003), 1771–9 CrossRefGoogle ScholarPubMed
Stokes, C. L., Lauffenburger, D. A. Williams, S. K.. Migration of individual microvessel endothelial cells: stochastic model and parameter measurement . J. Cell Sci., 99 (1991), 419–30 Google Scholar
A. Szabó, R. Ünnep, E. Méhes, W. Twal, S. Argraves, Y. Cho, A. Czirók. Collective cell motion in endothelial monolayers. (preprint)
Szabó, A., Méhes, E., Kósa, E. Czirók, A.. Multicellular sprouting in vitro . Biophys J., 95 (2008), No. 6, 2702–2710 CrossRefGoogle ScholarPubMed
Szabó, A., Perryn, E. D., Czirók, A.. Network formation of tissue cells via preferential attraction to elongated structures . Phys. Rev. Lett., 98 (2007), No. 3, 038102. CrossRefGoogle ScholarPubMed
Teddy, J. M. Kulesa, P. M.. In vivo evidence for short- and long-range cell communication in cranial neural crest cells . Development, 131 (2004), No. 24, 6141–6151 CrossRefGoogle Scholar
Tzima, E., Irani-Tehrani, M., Kiosses, W. B., Dejana, E., Schultz, D. A., Engelhardt, B., Cao, G., DeLisser, H. Schwartz, M. A.. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress . Nature, 437 (2005), No. 7057, 426–431 CrossRefGoogle ScholarPubMed
Upadhyaya, A., Rieu, J.-P., Glazier, J. A. Sawada, Y.. Anomalous diffusion and non-gaussian velocity distribution of hydra cells in cellular aggregates . Physica A, 293 (2001), 549–558 CrossRefGoogle Scholar
Verkhovsky, A. B., Svitkina, T. M. Borisy, G. G.. Self-polarization and directional motility of cytoplasm . Curr. Biol., 9 (1999), No. 1 , 11–20 CrossRefGoogle ScholarPubMed