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

A. Szabó¹ ; A. Czirók^2, 1

¹ Department of Biological Physics, Eötvos University, Budapest, Hungary
² Department of Anatomy & Cell Biology, University of Kansas Medical Center Kansas City, KS, USA

Mathematical modelling of natural phenomena, Tome 5 (2010) no. 1, pp. 106-122.

Résumé

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.

Détail

DOI : 10.1051/mmnp/20105105

Bibliographie

[1] M. Alber, N. Chen, T. Glimm, P. M. Lushnikov 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. 2006

[2] A. L. Bauer, T. L. Jackson, Y. Jiang A cell-based model exhibiting branching and anastomosis during tumor-induced angiogenesis Biophys. J. 2007 3105 3121

[3] 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.

[4] J. M. Belmonte, G. L. Thomas, L. G. Brunnet, R. M. C. De Almeida, H. Chaté Self-propelled particle model for cell-sorting phenomena Phys. Rev. Lett. 2008

[5] D. A. Beysens, G. Forgacs, J. A. Glazier Cell sorting is analogous to phase ordering in fluids PNAS 2000 9467 71

[6] A. Czirók, E. A. Zamir, A. Szabó, C. D. Little Multicellular sprouting during vasculogenesis Curr. Top. Dev. Biol. 2008 269 289

[7] A. T. Dawes, L. Edelstein-Keshet 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. 2007 744 768

[8] P. G. de Gennes, F. Brochard-Wyart, D. Quere. Capillarity and wetting phenomena. Springer, New York, 2003.

[9] A. Dipasquale Locomotion of epithelial cells. Factors involved in extension of the leading edge Exp. Cell Res. 1975 425 439

[10] O. Du Roure, A. Saez, A. Buguin, R. H. Austin, P. Chavrier, P. Silberzan, B. Ladoux Force mapping in epithelial cell migration Proc. Natl. Acad. Sci. U S A 2005 2390 2395

[11] G. Forgacs, R. A. Foty, Y. Shafrir, M. S. Steinberg Viscoelastic properties of living embryonic tissues: a quantitative study Biophys. J. 1998 2227 2234

[12] R. A. Foty, C. M. Pfleger, G. Forgacs, M. S. Steinberg Surface tensions of embryonic tissues predict their mutual envelopment behavior Development 1996 1611 1620

[13] R. A. Foty, M. S. Steinberg The differential adhesion hypothesis: a direct evaluation Dev. Biol. 2005 255 263

[14] P. Friedl Dynamic imaging of cellular interactions with extracellular matrix Histochem. Cell Biol. 2004 183 90

[15] P. Friedl, K. Wolf Tube travel: the role of proteases in individual and collective cancer cell invasion Cancer Res. 2008 7247 7249

[16] A. Gamba, D. Ambrosi, A. Coniglio, A. De Candia, S. Di Talia, E. Giraudo, G. Serini, L. Preziosi, F. Bussolino Percolation, morphogenesis, and burgers dynamics in blood vessels formation Phys. Rev. Lett. 2003

[17] H. Gerhardt, M. Golding, M. Fruttiger, C. Ruhrberg, A. Lundkvist, A. Abramsson, M. Jeltsch, C. Mitchell, K. Alitalo, D. Shima, C. Betsholtz Vegf guides angiogenic sprouting utilizing endothelial tip cell filopodia J. Cell Biol. 2003 1163 1177

[18] J. A. Glazier, F. Graner Simulation of the differential adhesion driven rearrangement of biological cells Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 1993 2128 2154

[19] F. Graner, J. A. Glazier Simulation of biological cell sorting using a two-dimensional extended potts model Phys. Rev. Lett. 1992 2013 2016

[20] D. S. Gray, J. Tien, C. S. Chen Repositioning of cells by mechanotaxis on surfaces with micropatterned young’s modulus J. Biomed. Mater. Res. A. 2003 605 14

[21] B. Hegedüs, F. Marga, K. Jakab, K. L. Sharpe-Timms, G. Forgacs The interplay of cell-cell and cell-matrix interactions in the invasive properties of brain tumors Biophysical J. 2006 2708 16

[22] K. A. Hogan, V. L. Bautch Blood vessel patterning at the embryonic midline Curr. Top. Dev. Biol. 2004 55 85

[23] M. S. Hutson, G. W. Brodland, J. Yang, D. Viens Cell sorting in three dimensions: topology, fluctuations, and fluidlike instabilities Phys. Rev. Lett. 2008

[24] J. A. Izaguirre, R. Chaturvedi, C. Huang, T. Cickovski, J. Coffland, G. Thomas, G. Forgacs, M. Alber, G. Hentschel, S. A. Newman, J. A. Glazier Compucell, a multi-model framework for simulation of morphogenesis Bioinformatics 2004 1129 1137

[25] G. Jiang, A. H. Huang, Y. Cai, M. Tanase, M. P. Sheetz Rigidity sensing at the leading edge through alphavbeta3 integrins and rptpalpha Biophys J. 2006 1804 9

[26] S. Kidoaki, T. Matsuda Shape-engineered fibroblasts: cell elasticity and actin cytoskeletal features characterized by fluorescence and atomic force microscopy J. Biomed. Mater. Res. A. 2007 803 810

[27] T. Libotte, H. W. Kaiser, W. Alt, T. Bretschneider Polarity, protrusion-retraction dynamics and their interplay during keratinocyte cell migration Exp. Cell Res. 2001 129 137

[28] C. M. Lo, H. B. Wang, M. Dembo, Y. L. Wang Cell movement is guided by the rigidity of the substrate Biophys J. 2000 144 152

[29] D. Manoussaki, S. R. Lubkin, R. B. Vernon, J. D. Murray A mechanical model for the formation of vascular networks in vitro Acta Biotheor 1996 271 282

[30] R. M. Merks, S. V. Brodsky, M. S. Goligorksy, S. A. Newman, J. A. Glazier Cell elongation is key to in silico replication of in vitro vasculogenesis and subsequent remodeling Dev. Biol. 2006 44 54

[31] R. M. H. Merks, E. D. Perryn, A. Shirinifard, J. A. Glazier Contact-inhibited chemotaxis in de novo and sprouting blood-vessel growth PLoS Comput. Biol. 2008

[32] D. J. Montell Morphogenetic cell movements: diversity from modular mechanical properties Science 2008 1502 1505

[33] J. D. Murray. Mathematical Biology. Springer Verlag, Berlin, 2nd edition, 2003.

[34] 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.

[35] T. J. Newman Modeling multicellular systems using subcellular elements Math. Biosci. Eng. 2005 611 622

[36] E. D. Perryn, A. Czirók, C. D. Little Vascular sprout formation entails tissue deformations and ve-cadherin-dependent cell-autonomous motility Dev. Biol. 2008 545 55

[37] A. J. Ridley, M. A. Schwartz, K. Burridge, R. A. Firtel, M. H. Ginsberg, G. Borisy, J. T. Parsons, A. R. Horwitz Cell migration: integrating signals from front to back Science 2003 1704 1709

[38] J. P. Rieu, A. Upadhyaya, J. A. Glazier, N. B. Ouchi, Y. Sawada Diffusion and deformations of single hydra cells in cellular aggregates Biophys J. 2000 1903 14

[39] P. A. Rupp, A. Czirók, C. D. Little alphavbeta3 integrin-dependent endothelial cell dynamics in vivo Development 2004 2887 97

[40] R. K. Sawhney, J. Howard Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels J. Cell Biol. 2002 1083 1091

[41] D. Selmeczi, S. Mosler, P. H. Hagedorn, N. B. Larsen, H. Flyvbjerg Cell motility as persistent random motion: theories from experiments Biophys J. 2005 912 31

[42] G. Serini, D. Ambrosi, E. Giraudo, A. Gamba, L. Preziosi, F. Bussolino Modeling the early stages of vascular network assembly EMBO J. 2003 1771 9

[43] C. L. Stokes, D. A. Lauffenburger, S. K. Williams Migration of individual microvessel endothelial cells: stochastic model and parameter measurement J. Cell Sci. 1991 419 30

[44] A. Szabó, R. Ünnep, E. Méhes, W. Twal, S. Argraves, Y. Cho, A. Czirók. Collective cell motion in endothelial monolayers. (preprint)

[45] A. Szabó, E. Méhes, E. Kósa, A. Czirók Multicellular sprouting in vitro Biophys J. 2008 2702 2710

[46] A. Szabó, E. D. Perryn, A. Czirók Network formation of tissue cells via preferential attraction to elongated structures Phys. Rev. Lett. 2007

[47] J. M. Teddy, P. M. Kulesa In vivo evidence for short- and long-range cell communication in cranial neural crest cells Development 2004 6141 6151

[48] E. Tzima, M. Irani-Tehrani, W. B. Kiosses, E. Dejana, D. A. Schultz, B. Engelhardt, G. Cao, H. Delisser, M. A. Schwartz A mechanosensory complex that mediates the endothelial cell response to fluid shear stress Nature 2005 426 431

[49] A. Upadhyaya, J.-P. Rieu, J. A. Glazier, Y. Sawada Anomalous diffusion and non-gaussian velocity distribution of hydra cells in cellular aggregates Physica A 2001 549 558

[50] A. B. Verkhovsky, T. M. Svitkina, G. G. Borisy Self-polarization and directional motility of cytoplasm Curr. Biol. 1999 11 20