Endothelial cell motility, coordination and pattern formation during vasculogenesis

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 5, Issue 5, 2013, Pages 587-602

  Czirok, Andras ^a,b  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; FIBRONECTIN; MORPHOGEN; NOTCH RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR;

ACTIN POLYMERIZATION; ANGIOGENESIS; ARTICLE; AUTOCRINE EFFECT; CELL ADHESION; CELL CONTACT; CELL DENSITY; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CELL POLARITY; CELL STRESS; CELL SURFACE; CHEMOTAXIS; COMPUTER SIMULATION; DEVELOPMENTAL BIOLOGY; DISEASE COURSE; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; INTRACELLULAR SIGNALING; MECHANICAL STRESS; MEMORY CELL; MOLECULAR BIOLOGY; MONOLAYER CULTURE; NONHUMAN; PARACRINE SIGNALING; POSITIVE FEEDBACK; SIGNAL TRANSDUCTION; SPROUTING;

CELL MOVEMENT; CHEMOTAXIS; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION;

EID: 84881639246     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.1233     Document Type: Article

References (119)

1. Ziyad S, Iruela-Arispe ML. Molecular mechanisms of tumor angiogenesis. Genes Cancer 2011, 2:1085-1096.
2. Chekhonin VP, Shein SA, Korchagina AA, Gurina OI. Vegf in tumor progression and targeted therapy. Curr Cancer Drug Targets 2012, 13:423-443.
3. Carmeliet P, Jain RK. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov 2011, 10:417-427.
4. Serini G, Bussolino F, Maione F, Giraudo E. Class 3 semaphorins: physiological vascular normalizing agents for anti-cancer therapy. J Intern Med 2013, 273:138-155.
5. Wu X, Rabkin-Aikawa E, Guleserian KJ, Perry TE, Masuda Y, Sutherland FWH, Schoen FJ, Mayer JEJ, Bischoff J. Tissue-engineered microvessels on three-dimensional biodegradable scaffolds using human endothelial progenitor cells. Am J Physiol Heart Circ Physiol 2004, 287:H480-H487.
6. Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen DHT, Cohen DM, Toro E, Chen AA, Galie PA, Yu X, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 2012, 11:768-774.
7. Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 1995, 11:73-91.
8. Pardanaud L, Altmann C, Kitos P, Dieterlen-Lievre F, Buck C. Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 1987, 100:339-349.
9. Hamburger V, Hamilton H. A series of normal stages in the development of the chick embryo. J Morphol 1951, 88:49-92.
10. Drake CJ, Brandt SJ, Trusk TC, Little CD. Tal1/scl is expressed in endothelial progenitor cells/angioblasts and defines a dorsal-to-ventral gradient of vasculogenesis. Dev Biol 1997, 192:17-30.
11. Rupp PA, Czirok A, Little CD. αvβ3 integrin-dependent endothelial cell dynamics in vivo. Development 2004, 131:2887-2897.
12. Sato Y, Poynter G, Huss D, Filla MB, Czirok A, Rongish BJ, Little CD, Fraser SE, Lansford R. Dynamic analysis of vascular morphogenesis using transgenic quail embryos. PLoS One 2010, 5:e12674.
13. Hendrix MJC, Seftor EA, Hess AR, Seftor REB. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat Rev Cancer 2003, 3:411-421.
14. Szabo A, Perryn ED, Czirok A. Network formation of tissue cells via preferential attraction to elongated structures. Phys Rev Lett 2007, 98:038102.
15. Szabo A, Mehes E, Kosa E, Czirok A. Multicellular sprouting in vitro. Biophys J 2008, 95:2702-2710.
16. Liu G, Qutub AA, Vempati P, Gabhann FM, Popel AS. Module-based multiscale simulation of angiogenesis in skeletal muscle. Theor Biol Med Model 2011, 8:6.
17. Foty RA, Pfleger CM, Forgacs G, Steinberg MS. Surface tensions of embryonic tissues predict their mutual envelopment behavior. Development 1996, 122:1611-1620.
18. Forgacs G, Foty RA, Shafrir Y, Steinberg MS. Viscoelastic properties of living embryonic tissues: a quantitative study. Biophys J 1998, 74:2227-2234.
19. Beysens DA, Forgacs G, Glazier JA. Cell sorting is analogous to phase ordering in fluids. Proc Natl Acad Sci USA 2000, 97:9467-9471.
20. Foty RA, Steinberg MS. The differential adhesion hypothesis: a direct evaluation. Dev Biol 2005, 278:255-263.
21. Hegedüs B, Marga F, Jakab K, Sharpe-Timms KL, Forgacs G. The interplay of cell-cell and cell-matrix interactions in the invasive properties of brain tumors. Biophys J 2006, 91:2708-2716.
22. Maître JL, Berthoumieux H, Krens SFG, Salbreux G, Jülicher F, Paluch E, Heisenberg CP. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 2012, 338:253-256.
23. Glazier JA, Graner F. Simulation of the differential adhesion driven rearrangement of biological cells. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 1993, 47:2128-2154.
24. Izaguirre JA, Chaturvedi R, Huang C, Cickovski T, Coffland J, Thomas G, Forgacs G, Alber M, Hentschel G, Newman SA, et al. COMPUCELL, a multi-model framework for simulation of morphogenesis. Bioinformatics 2004, 20:1129-1137.
25. Newman T. Modeling multicellular systems using subcellular elements. Math Biosci Eng 2005, 2:611-622.
26. Szabó A, Varga K, Garay T, Hegedus B, Czirók A. Invasion from a cell aggregate-the roles of active cell motion and mechanical equilibrium. Phys Biol 2012, 9:016010.
27. Stokes CL, Lauffenburger DA, Williams SK. Migration of individual microvessel endothelial cells: stochastic model and parameter measurement. J Cell Sci 1991, 99:419-430.
28. Kouvroukoglou S, Dee KC, Bizios R, McIntire LV, Zygourakis K. Endothelial cell migration on surfaces modified with immobilized adhesive peptides. Biomaterials 2000, 21:1725-1733.
29. Szabó A, Ünnep R, Méhes E, Twal WO, Argraves WS, Cao Y, Czirók A. Collective cell motion in endothelial monolayers. Phys Biol 2010, 7:046007.
30. Aleksandrova A, Czirók A, Szabó A, Filla MB, Hossain MJ, Whelan PF, Lansford R, Rongish BJ. Convective tissue movements play a major role in avian endocardial morphogenesis. Dev Biol 2012, 363:348-361.
31. Vitorino P, Meyer T. Modular control of endothelial sheet migration. Genes Dev 2008, 22:3268-3281.
32. Srinivasan S, Wang F, Glavas S, Ott A, Hofmann F, Aktories K, Kalman D, Bourne HR. Rac and cdc42 play distinct roles in regulating pi(3, 4, 5)p3 and polarity during neutrophil chemotaxis. J Cell Biol 2003, 160:375-385.
33. Dawes AT, 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 2007, 92:744-768.
34. Yoshida A, Anand-Apte B, Zetter BR. Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors 1996, 13:57-64.
35. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature 2000, 407:242-248.
36. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH. Different signal transduction properties of kdr and flt1, two receptors for vascular endothelial growth factor. J Biol Chem 1994, 269:26988-26995.
37. Cao Y, Linden P, Shima D, Browne F, Folkman J. In vivo angiogenic activity and hypoxia induction of heterodimers of placenta growth factor/vascular endothelial growth factor. J Clin Invest 1996, 98:2507-2511.
38. Alt W. Biased random walk models for chemotaxis and related diffusion approximations. J Math Biol 1980, 9:147-177.
39. Chen RR, Silva EA, Yuen WW, Brock AA, Fischbach C, Lin AS, Guldberg RE, Mooney DJ. Integrated approach to designing growth factor delivery systems. FASEB J 2007, 21:3896-3903.
40. Shamloo A, Ma N, Poo MM, Sohn LL, Heilshorn SC. Endothelial cell polarization and chemotaxis in a microfluidic device. Lab Chip 2008, 8:1292-1299.
41. Fontana L, Chen Y, Prijatelj P, Sakai T, Fässler R, Sakai LY, Rifkin DB. Fibronectin is required for integrin αvβ6-mediated activation of latent TGF-β complexes containing LTBP-1. FASEB J 2005, 19:1798-1808.
42. Leiss M, Beckmann K, Girós A, Costell M, Fässler R. The role of integrin binding sites in fibronectin matrix assembly in vivo. Curr Opin Cell Biol 2008, 20:502-507.
43. Wijelath ES, Murray J, Rahman S, Patel Y, Ishida A, Strand K, Aziz S, Cardona C, Hammond WP, Savidge GF, et al. Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circ Res 2002, 91:25-31.
44. Stenzel D, Lundkvist A, Sauvaget D, Busse M, Graupera M, van der Flier A, Wijelath ES, Murray J, Sobel M, Costell M, et al. Integrin-dependent and -independent functions of astrocytic fibronectin in retinal angiogenesis. Development 2011, 138:4451-4463.
45. Gabhann FM, Popel AS. Systems biology of vascular endothelial growth factors. Microcirculation 2008, 15:715-738.
46. Autiero M, Waltenberger J, Communi D, Kranz A, Moons L, Lambrechts D, Kroll J, Plaisance S, Mol MD, Bono F, et al. Role of plgf in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat Med 2003, 9:936-943.
47. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995, 376:66-70.
48. Hiratsuka S, Kataoka Y, Nakao K, Nakamura K, Morikawa S, Tanaka S, Katsuki M, Maru Y, Shibuya M. Vascular endothelial growth factor a (VEGF-A) is involved in guidance of VEGF receptor-positive cells to the anterior portion of early embryos. Mol Cell Biol 2005, 25:355-363.
49. Kappas NC, Zeng G, Chappell JC, Kearney JB, Hazarika S, Kallianos KG, Patterson C, Annex BH, Bautch VL. The VEGF receptor flt-1 spatially modulates Flk-1 signaling and blood vessel branching. J Cell Biol 2008, 181:847-858.
50. Chappell JC, Taylor SM, Ferrara N, Bautch VL. Local guidance of emerging vessel sprouts requires soluble flt-1. Dev Cell 2009, 17:377-386.
51. Ingber DE, Folkman J. How does extracellular matrix control capillary morphogenesis? Cell 1989, 58:803-805.
52. Korff T, Augustin HG. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci 1999, 112(Pt 19):3249-3258.
53. Davis GE, Bayless KJ, Mavila A. Molecular basis of endothelial cell morphogenesis in three-dimensional extracellular matrices. Anat Rec 2002, 268:252-275.
54. Stupack DG, Cheresh DA. Get a ligand, get a life: integrins, signaling and cell survival. J Cell Sci 2002, 115:3729-3738.
55. Critser PJ, Kreger ST, Voytik-Harbin SL, Yoder MC. Collagen matrix physical properties modulate endothelial colony forming cell-derived vessels in vivo. Microvasc Res 2010, 80:23-30.
56. Shamloo A, Heilshorn SC. Matrix density mediates polarization and lumen formation of endothelial sprouts in VEGF gradients. Lab Chip 2010, 10:3061-3068.
57. Reinhart-King CA, Dembo M, Hammer DA. Cell-cell mechanical communication through compliant substrates. Biophys J 2008, 95:6044-6051.
58. Bayless KJ, Davis GE. Microtubule depolymerization rapidly collapses capillary tube networks in vitro and angiogenic vessels in vivo through the small gtpase rho. J Biol Chem 2004, 279:11686-11695.
59. Stratman AN, Saunders WB, Sacharidou A, Koh W, Fisher KE, Zawieja DC, Davis MJ, Davis GE. Endothelial cell lumen and vascular guidance tunnel formation requires mt1-mmp-dependent proteolysis in 3-dimensional collagen matrices. Blood 2009, 114:237-247.
60. Jakobsson L, Franco CA, Bentley K, Collins RT, Ponsioen B, Aspalter IM, Rosewell I, Busse M, Thurston G, Medvinsky A, et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 2010, 12:943-953.
61. Bentley K, Mariggi G, Gerhardt H, Bates PA. Tipping the balance: robustness of tip cell selection, migration and fusion in angiogenesis. PLoS Comput Biol 2009, 5:e1000549.
62. Liu ZJ, Shirakawa T, Li Y, Soma A, Oka M, Dotto GP, Fairman RM, Velazquez OC, Herlyn M. Regulation of notch1 and dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Mol Cell Biol 2003, 23:14-25.
63. Williams CK, Li JL, Murga M, Harris AL, Tosato G. Up-regulation of the notch ligand delta-like 4 inhibits VEGF-induced endothelial cell function. Blood 2006, 107:931-939.
64. Sainson RCA, Aoto J, Nakatsu MN, Holderfield M, Conn E, Koller E, Hughes CCW. Cell-autonomous notch signaling regulates endothelial cell branching and proliferation during vascular tubulogenesis. FASEB J 2005, 19:1027-1029.
65. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, et al. Vegf guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 2003, 161:1163-1177.
66. Stokes CL, Lauffenburger DA. Analysis of the roles of microvessel endothelial cell random motility and chemotaxis in angiogenesis. J Theor Biol 1991, 152:377-403.
67. Anderson A, Chaplain M. Continuous and discrete mathematical-models of tumor-induced angiogenesis. Bull Math Biol 1998, 60:857-899.
68. Ambler CA, Nowicki JL, Burke AC, Bautch VL. Assembly of trunk and limb blood vessels involves extensive migration and vasculogenesis of somite-derived angioblasts. Dev Biol 2001, 234:352-364.
69. Cleaver O, Krieg PA. Vegf mediates angioblast migration during development of the dorsal aorta in xenopus. Development 1998, 125:3905-3914.
70. Poole T, Coffin J. Vasculogenesis and angiogenesis: two distinct morphogenetic mechanisms establish embryonic vascular pattern. J Exp Zool 1989, 251:224-231.
71. Uemura A, Kusuhara S, Wiegand SJ, Yu RT, Nishikawa S. Tlx acts as a proangiogenic switch by regulating extracellular assembly of fibronectin matrices in retinal astrocytes. J Clin Invest 2006, 116:369-377.
72. Weinstein B. What guides early embryonic blood vessel formation? Dev Dyn 1999, 215:2-11.
73. Czirok A, Rongish BJ, Little CD. Vascular network formation in expanding versus static tissues: embryos and tumors. Genes Cancer 2011, 2:1072-1080.
74. Crosby CV, Fleming PA, Argraves WS, Corada M, Zanetta L, Dejana E, Drake CJ. Ve-cadherin is not required for the formation of nascent blood vessels but acts to prevent their disassembly. Blood 2005, 105:2771-2776.
75. Perryn ED, Czirok A, Little CD. Vascular sprout formation entails tissue deformations and ve-cadherin-dependent cell-autonomous motility. Dev Biol 2008, 313:545-555.
76. Montesano R, Orci L. Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell 1985, 42:469-477.
77. Davis GE, Black SM, Bayless KJ. Capillary morphogenesis during human endothelial cell invasion of three-dimensional collagen matrices. In Vitro Cell Dev Biol Anim 2000, 36:513-519.
78. Stoplak D, Harris A. Connective tissue morphogenesis by fibroblast traction. Dev Biol 1982, 90:383-398.
79. Guido S, Tranquillo RT. A methodology for the systematic and quantitative study of cell contact guidance in oriented collagen gels. Correlation of fibroblast orientation and gel birefringence. J Cell Sci 1993, 105(Pt 2):317-331.
80. Vernon R, Lara S, Drake C, Iruela-Arispe M, Angello J, Little C, Wight T, Sage E. Organized type I collagen influences endothelial patterns during "spontaneous angiogenesis in vitro": planar cultures as models of vascular development. In Vitro Cell Dev Biol Anim 1995, 31:120-131.
81. Manoussaki D, Lubkin SR, Vernon RB, Murray JD. A mechanical model for the formation of vascular networks in vitro. Acta Biotheor 1996, 44:271-282.
82. Namy P, Ohayon J, Tracqui P. Critical conditions for pattern formation and in vitro tubulogenesis driven by cellular traction fields. J Theor Biol 2004, 227:103-120.
83. Fung YC. Biomechanics: mechanical properties of living tissues. New York: Springer-Verlag; 1993.
84. Taber LA. Towards a unified theory for morphomechanics. Philos Transact A Math Phys Eng Sci 2009, 367:3555-3583.
85. Murray J, Oster G, Harris A. A mechanical model for mesenchymal morphogenesis. J Math Biol 1983, 17:125-129.
86. Barocas VH, Tranquillo RT. An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance. J Biomech Eng 1997, 119:137-145.
87. Califano JP, Reinhart-King CA. The effects of substrate elasticity on endothelial cell network formation and traction force generation. Conf Proc IEEE Eng Med Biol Soc 2009, 2009:3343-3345.
88. Vernon RB, Angello JC, Iruela-Arispe ML, Lane TF, Sage EH. Reorganization of basement membrane matrices by cellular traction promotes the formation of cellular networks in vitro. Lab Invest 1992, 66:536-547.
89. Painter KJ. Modelling cell migration strategies in the extracellular matrix. J Math Biol 2009, 58:511-543.
90. Mente C, Prade I, Brusch L, Breier G, Deutsch A. Parameter estimation with a novel gradient-based optimization method for biological lattice-gas cellular automaton models. J Math Biol 2011, 63:173-200.
91. Vittori K, Talbot G, Gautrais J, Fourcassié V, Araújo AFR, Theraulaz G. Path efficiency of ant foraging trails in an artificial network. J Theor Biol 2006, 239:507-515.
92. John K, Bärr M, Thiele U. Self-propelled running droplets on solid substrates driven by chemical reactions. Eur Phys J E 2005, 18:183-199.
93. Rupp PA, Visconti RP, Czirok A, Cheresh DA, Little CD. Matrix metalloproteinase 2-integrin α(v)β3 binding is required for mesenchymal cell invasive activity but not epithelial locomotion: a computational time-lapse study. Mol Biol Cell 2008, 19:5529-5540.
94. Friedl P, Wolf K. Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res 2008, 68:7247-7249.
95. Fisher KE, Sacharidou A, Stratman AN, Mayo AM, Fisher SB, Mahan RD, Davis MJ, Davis GE. Mt1-mmp- and cdc42-dependent signaling co-regulate cell invasion and tunnel formation in 3d collagen matrices. J Cell Sci 2009, 122:4558-4569.
96. Ilina O, Bakker GJ, Vasaturo A, Hofmann RM, Friedl P. Two-photon laser-generated microtracks in 3d collagen lattices: principles of mmp-dependent and -independent collective cancer cell invasion. Phys Biol 2011, 8:015010.
97. 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 2003, 90:118101.
98. Serini G, Ambrosi D, Giraudo E, Gamba A, Preziosi L, Bussolino F. Modeling the early stages of vascular network assembly. EMBO J 2003, 22:1771-1779.
99. Ambrosi D, Bussolino F, Preziosi L. A review of vasculogenesis models. J Theor Med 2005, 6:1-19.
100. Gamba A, de Candia A, Talia SD, Coniglio A, Bussolino F, Serini G. Diffusion-limited phase separation in eukaryotic chemotaxis. Proc Natl Acad Sci USA 2005, 102:16927-16932.
101. Keller EF, Segel LA. Initiation of slime mold aggregation viewed as an instability. J Theor Biol 1970, 26:399-415.
102. Merks RMH, Perryn ED, Shirinifard A, Glazier JA. Contact-inhibited chemotaxis in de novo and sprouting blood-vessel growth. PLoS Comput Biol 2008, 4:e1000163.
103. Merks RM, Brodsky SV, Goligorksy MS, Newman SA, Glazier JA. Cell elongation is key to in silico replication of in vitro vasculogenesis and subsequent remodeling. Dev Biol 2006, 289:44-54.
104. Flamme I, Breier G, Risau W. Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (Flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev Biol 1995, 169:699-712.
105. Poole TJ, Finkelstein EB, Cox CM. The role of fgf and VEGF in angioblast induction and migration during vascular development. Dev Dyn 2001, 220:1-17.
106. Vernon RB, Sage EH. A novel, quantitative model for study of endothelial cell migration and sprout formation within three-dimensional collagen matrices. Microvasc Res 1999, 57:118-133.
107. Koh W, Stratman AN, Sacharidou A, Davis GE. In vitro three dimensional collagen matrix models of endothelial lumen formation during vasculogenesis and angiogenesis. Methods Enzymol 2008, 443:83-101.
108. Köhn-Luque A, de Back W, Starruss J, Mattiotti A, Deutsch A, Pérez-Pomares JM, Herrero MA. Early embryonic vascular patterning by matrix-mediated paracrine signalling: a mathematical model study. PLoS One 2011, 6:e24175.
109. Hashambhoy YL, Chappell JC, Peirce SM, Bautch VL, Gabhann FM. Computational modeling of interacting VEGF and soluble VEGF receptor concentration gradients. Front Physiol 2011, 2:62.
110. Vicsek T. Fractal growth phenomena. 2nd ed. Singapore: World Scientific Publishing Co.; 1992.
111. Mller J, Saarloos WV. Morphological instability and dynamics of fronts in bacterial growth models with nonlinear diffusion. Phys Rev E Stat Nonlin Soft Matter Phys 2002, 65:061111.
112. Szabo A, Czirok A. The role of cell-cell adhesion in the formation of multicellular sprouts. Math Model Nat Phenom 2010, 5:106.
113. du Roure O, Saez A, Buguin A, Austin RH, Chavrier P, Silberzan P, Siberzan P, Ladoux B. Force mapping in epithelial cell migration. Proc Natl Acad Sci USA 2005, 102:2390-2395.
114. Dipasquale A. Locomotion of epithelial cells. factors involved in extension of the leading edge. Exp Cell Res 1975, 95:425-439.
115. Friedl P. Dynamic imaging of cellular interactions with extracellular matrix. Histochem Cell Biol 2004, 122:183-190.
116. de Gennes P, Brochard-Wyart F, Quere D. Capillarity and wetting phenomena. New York: Springer; 2003.
117. Hutson MS, Brodland GW, Yang J, Viens D. Cell sorting in three dimensions: topology, fluctuations, and fluidlike instabilities. Phys Rev Lett 2008, 101:148105.
118. Bauer AL, Jackson TL, Jiang Y. Topography of extracellular matrix mediates vascular morphogenesis and migration speeds in angiogenesis. PLoS Comput Biol 2009, 5:e1000445.
119. 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 2007, 81:803-810.