Do endothelial cells dream of eclectic shape?

Developmental Cell

Volumn 29, Issue 2, 2014, Pages 146-158

  Bentley, Katie ^a   Philippides, Andrew ^b   Ravasz Regan, Erzsébet ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE BEHAVIOR; CELL FUNCTION; CELL INTERACTION; CELL SHAPE; CELL STIMULATION; CELL STRUCTURE; ENDOTHELIUM CELL; FEEDBACK SYSTEM; HUMAN; MORPHOGENESIS; MUTATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSORY FEEDBACK;

ANIMALS; CELL SHAPE; ENDOTHELIAL CELLS; HUMANS; MORPHOGENESIS; SIGNAL TRANSDUCTION;

EID: 84899645615     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.03.019     Document Type: Review

References (123)

1. Aird W.C. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ. Res. 2007, 100:174-190.
2. Arima S., Nishiyama K., Ko T., Arima Y., Hakozaki Y., Sugihara K., Koseki H., Uchijima Y., Kurihara Y., Kurihara H. Angiogenic morphogenesis driven by dynamic and heterogeneous collective endothelial cell movement. Development 2011, 138:4763-4776.
3. Bartha K., Rieger H. Vascular network remodeling via vessel cooption, regression and growth in tumors. J. Theor. Biol. 2006, 241:903-918.
4. Bentley K., Gerhardt H., Bates P.A. Agent-based simulation of notch-mediated tip cell selection in angiogenic sprout initialisation. J. Theor. Biol. 2008, 250:25-36.
5. Bentley K., Mariggi G., Gerhardt H., Bates P.A. Tipping the balance: robustness of tip cell selection, migration and fusion in angiogenesis. PLoS Comput. Biol. 2009, 5:e1000549.
6. Bentley K., Jones M., Cruys B. Predicting the future: towards symbiotic computational and experimental angiogenesis research. Exp. Cell Res. 2013, 319:1240-1246.
7. Bentley K., Franco C.A., Philippides A., Blanco R., Dierkes M., Gebala V., Stanchi F., Jones M., Aspalter I.M., Cagna G., et al. The role of differential VE-cadherin dynamics in cell rearrangement during angiogenesis. Nat. Cell Biol. 2014, 16:309-321.
8. Blum Y., Belting H.G., Ellertsdottir E., Herwig L., Lüders F., Affolter M. Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 2008, 316:312-322.
9. Boas S.E., Merks R.M. Synergy of cell-cell repulsion and vacuolation in a computational model of lumen formation. J. R. Soc. Interface 2014, 11:20131049.
10. Bonabeau E., Dorigo M., Theraulaz G. Swarm intelligence 1999, Oxford University Press, New York.
11. Braitenberg V. Vehicles: Experiments in synthetic psychology 1986, MIT Press, Cambridge, MA.
12. Brandman O., Meyer T. Feedback loops shape cellular signals in space and time. Science 2008, 322:390-395.
13. Brody S., McMahon J., Yao L., O'Brien M., Dockery P., Pandit A. The effect of cholecyst-derived extracellular matrix on the phenotypic behaviour of valvular endothelial and valvular interstitial cells. Biomaterials 2007, 28:1461-1469.
14. Brooks R. A robust layered control system for a mobile robot. IEEE J. Robot. Autom. 1986, 2:14-23.
15. Brooks R.A. Elephants don't play chess. Robot. Auton. Syst. 1990, 6:3-15.
16. Brooks R.A. Intelligence without reason. Proceedings of the 12th international joint conference on artificial intelligence 1991, 1:569-595.
17. Burri P.H., Djonov V. Intussusceptive angiogenesis-the alternative to capillary sprouting. Mol. Aspects Med. 2002, 23(6S):S1-S27.
18. Camazine S. Self-organization in biological systems 2003, Princeton University Press, Princeton, NJ.
19. Carlier A., Geris L., Bentley K., Carmeliet G., Carmeliet P., Van Oosterwyck H. MOSAIC: a multiscale model of osteogenesis and sprouting angiogenesis with lateral inhibition of endothelial cells. PLoS Comput. Biol. 2012, 8:e1002724.
20. Carman C.V., Jun C.D., Salas A., Springer T.A. Endothelial cells proactively form microvilli-like membrane projections upon intercellular adhesion molecule 1 engagement of leukocyte LFA-1. J. Immunol. 2003, 171:6135-6144.
21. Chappell J.C., Taylor S.M., Ferrara N., Bautch V.L. Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev. Cell 2009, 17:377-386.
22. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Geometric control of cell life and death. Science 1997, 276:1425-1428.
23. Chen M.B., Whisler J.A., Jeon J.S., Kamm R.D. Mechanisms of tumor cell extravasation in an in vitro microvascular network platform. Integr Biol (Camb) 2013, 5:1262-1271.
24. Czirok A. Endothelial cell motility, coordination and pattern formation during vasculogenesis. Wiley Interdiscip Rev Syst Biol Med 2013, 5:587-602.
25. Czirok A., Zamir E.A., Szabo A., Little C.D. Multicellular sprouting during vasculogenesis. Curr. Top. Dev. Biol. 2008, 81:269-289.
26. De Bock K., Cauwenberghs S., Carmeliet P. Vessel abnormalization: another hallmark of cancer? Molecular mechanisms and therapeutic implications. Curr. Opin. Genet. Dev. 2011, 21:73-79.
27. Dewey J. The Reflex Arc Concept in Psychology. Psychological Review 1896, 3:357-370.
28. Di Ventura B., Lemerle C., Michalodimitrakis K., Serrano L. From in vivo to in silico biology and back. Nature 2006, 443:527-533.
29. Dill M.T., Rothweiler S., Djonov V., Hlushchuk R., Tornillo L., Terracciano L., Meili-Butz S., Radtke F., Heim M.H., Semela D. Disruption of Notch1 induces vascular remodeling, intussusceptive angiogenesis, and angiosarcomas in livers of mice. Gastroenterology 2012, 142:967-977. e2.
30. Dorigo M., Floreano D., Gambardella L.M., Mondada F., Nolfi S., Baaboura T., Birattari M., Bonani M., Brambilla M., Brutschy A. Swarmanoid: a novel concept for the study of heterogeneous robotic swarms. IEEE Robot. Autom. Mag. 2012, 20:60-71.
31. Fan Y., Arif A., Gong Y., Jia J., Eswarappa S.M., Willard B., Horowitz A., Graham L.M., Penn M.S., Fox P.L. Stimulus-dependent phosphorylation of profilin-1 in angiogenesis. Nat. Cell Biol. 2012, 14:1046-1056.
32. Fraccaroli A., Franco C.A., Rognoni E., Neto F., Rehberg M., Aszodi A., Wedlich-Söldner R., Pohl U., Gerhardt H., Montanez E. Visualization of endothelial actin cytoskeleton in the mouse retina. PLoS ONE 2012, 7:e47488.
33. Franco C.A., Blanc J., Parlakian A., Blanco R., Aspalter I.M., Kazakova N., Diguet N., Mylonas E., Gao-Li J., Vaahtokari A., et al. SRF selectively controls tip cell invasive behavior in angiogenesis. Development 2013, 140:2321-2333.
34. Friedl P., Wolf K. Plasticity of cell migration: a multiscale tuning model. J. Cell. Biol. 2010, 188:11-19.
35. Galbraith C.G., Skalak R., Chien S. Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. Cell Motil. Cytoskeleton 1998, 40:317-330.
36. 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. 2003, 161:1163-1177.
37. Geudens I., Gerhardt H. Coordinating cell behaviour during blood vessel formation. Development 2011, 138:4569-4583.
38. Giannotta M., Trani M., Dejana E. VE-cadherin and endothelial adherens junctions: active guardians of vascular integrity. Dev. Cell 2013, 26:441-454.
39. Grimm V., Railsback S.F. Individual-based modeling and ecology 2013, Princeton University Press, Princeton, NJ.
40. Guarani V., Deflorian G., Franco C.A., Krüger M., Phng L.K., Bentley K., Toussaint L., Dequiedt F., Mostoslavsky R., Schmidt M.H., et al. Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase. Nature 2011, 473:234-238.
41. Håkansson J., Ståhlberg A., Wolfhagen Sand F., Gerhardt H., Semb H. N-CAM exhibits a regulatory function in pathological angiogenesis in oxygen induced retinopathy. PLoS ONE 2011, 6:e26026.
42. Harris A., Guidoboni G., Arciero J.C., Amireskandari A., Tobe L.A., Siesky B.A. Ocular hemodynamics and glaucoma: the role of mathematical modeling. Eur. J. Ophthalmol. 2013, 23:139-146.
43. Hashambhoy Y.L., Chappell J.C., Peirce S.M., Bautch V.L., Mac Gabhann F. Computational modeling of interacting VEGF and soluble VEGF receptor concentration gradients. Front Physiol 2011, 2:62.
44. Hashizume H., Baluk P., Morikawa S., McLean J.W., Thurston G., Roberge S., Jain R.K., McDonald D.M. Openings between defective endothelial cells explain tumor vessel leakiness. Am. J. Pathol. 2000, 156:1363-1380.
45. Hellström M., Phng L.K., Gerhardt H. VEGF and Notch signaling: the yin and yang of angiogenic sprouting. Cell Adhes. Migr. 2007, 1:133-136.
46. Huang S. Non-genetic heterogeneity of cells in development: more than just noise. Development 2009, 136:3853-3862.
47. Huang Y.J., Samorajski J., Kreimer R., Searson P.C. The influence of electric field and confinement on cell motility. PLoS ONE 2013, 8:e59447.
48. Huh D., Kim H.J., Fraser J.P., Shea D.E., Khan M., Bahinski A., Hamilton G.A., Ingber D.E. Microfabrication of human organs-on-chips. Nat. Protoc. 2013, 8:2135-2157.
49. Humphrey J.D. Vascular adaptation and mechanical homeostasis at tissue, cellular, and sub-cellular levels. Cell Biochem. Biophys. 2008, 50:53-78.
50. Husbands P., Philippides A., Vargas P., Buckley C.L., Fine P., Di Paolo E., O'Shea M. Spatial, temporal, and modulatory factors affecting gasnet evolvability in a visually guided robotics task. Complexity 2010, 16:35-44.
51. Imoukhuede P.I., Popel A.S. Quantification and cell-to-cell variation of vascular endothelial growth factor receptors. Exp. Cell Res. 2011, 317:955-965.
52. Imoukhuede P.I., Dokun A.O., Annex B.H., Popel A.S. Endothelial cell-by-cell profiling reveals the temporal dynamics of VEGFR1 and VEGFR2 membrane localization after murine hindlimb ischemia. Am. J. Physiol. Heart Circ. Physiol. 2013, 304:H1085-H1093.
53. Ingber D.E., Prusty D., Sun Z., Betensky H., Wang N. Cell shape, cytoskeletal mechanics, and cell cycle control in angiogenesis. J. Biomech. 1995, 28:1471-1484.
54. Jakobsson L., Franco C.A., Bentley K., Collins R.T., Ponsioen B., Aspalter I.M., 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.
55. Kamba T., Tam B.Y., Hashizume H., Haskell A., Sennino B., Mancuso M.R., Norberg S.M., O'Brien S.M., Davis R.B., Gowen L.C., et al. VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H560-H576.
56. Kitano H. Systems biology: a brief overview. Science 2002, 295:1662-1664.
57. Kouklis P., Konstantoulaki M., Malik A.B. VE-cadherin-induced Cdc42 signaling regulates formation of membrane protrusions in endothelial cells. J. Biol. Chem. 2003, 278:16230-16236.
58. Kullander K., Croll S.D., Zimmer M., Pan L., McClain J., Hughes V., Zabski S., DeChiara T.M., Klein R., Yancopoulos G.D., Gale N.W. Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes Dev. 2001, 15:877-888.
59. Lampugnani M.G., Orsenigo F., Rudini N., Maddaluno L., Boulday G., Chapon F., Dejana E. CCM1 regulates vascular-lumen organization by inducing endothelial polarity. J. Cell Sci. 2010, 123:1073-1080.
60. Lenard A., Ellertsdottir E., Herwig L., Krudewig A., Sauteur L., Belting H.G., Affolter M. In vivo analysis reveals a highly stereotypic morphogenetic pathway of vascular anastomosis. Dev. Cell 2013, 25:492-506.
61. Lewis J. From signals to patterns: space, time, and mathematics in developmental biology. Science 2008, 322:399-403.
62. Lizama C.O., Zovein A.C. Polarizing pathways: balancing endothelial polarity, permeability, and lumen formation. Exp. Cell Res. 2013, 319:1247-1254.
63. Long B.L., Rekhi R., Abrego A., Jung J., Qutub A.A. Cells as state machines: cell behavior patterns arise during capillary formation as a function of BDNF and VEGF. J. Theor. Biol. 2013, 326:43-57.
64. Mac Gabhann F., Popel A.S. Model of competitive binding of vascular endothelial growth factor and placental growth factor to VEGF receptors on endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 2004, 286:H153-H164.
65. Mac Gabhann F., Popel A.S. Interactions of VEGF isoforms with VEGFR-1, VEGFR-2, and neuropilin in vivo: a computational model of human skeletal muscle. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H459-H474.
66. Maes P. Modeling adaptive autonomous agents. Artif. Life 1993, 1:135-162.
67. Mammoto A., Ingber D.E. Cytoskeletal control of growth and cell fate switching. Curr. Opin. Cell Biol. 2009, 21:864-870.
68. Mao Y., Tournier A.L., Bates P.A., Gale J.E., Tapon N., Thompson B.J. Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. Genes Dev. 2011, 25:131-136.
69. Marchuk D.A., Srinivasan S., Squire T.L., Zawistowski J.S. Vascular morphogenesis: tales of two syndromes. Hum. Mol. Genet. 2003, 12(Spec No 1):R97-R112.
70. Marcon L., Sharpe J. Turing patterns in development: what about the horse part?. Curr. Opin. Genet. Dev. 2012, 22:578-584.
71. Martinelli R., Kamei M., Sage P.T., Massol R., Varghese L., Sciuto T., Toporsian M., Dvorak A.M., Kirchhausen T., Springer T.A., Carman C.V. Release of cellular tension signals self-restorative ventral lamellipodia to heal barrier micro-wounds. J. Cell Biol. 2013, 201:449-465. 10.1083/jcb.201209077.
72. McKenzie J.A., Fruttiger M., Abraham S., Lange C.A., Stone J., Gandhi P., Wang X., Bainbridge J., Moss S.E., Greenwood J. Apelin is required for non-neovascular remodeling in the retina. Am. J. Pathol. 2012, 180:399-409.
73. 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. 2006, 289:44-54.
74. Morelli L.G., Uriu K., Ares S., Oates A.C. Computational approaches to developmental patterning. Science 2012, 336:187-191.
75. Morgan J.P., Delnero P.F., Zheng Y., Verbridge S.S., Chen J., Craven M., Choi N.W., Diaz-Santana A., Kermani P., Hempstead B., et al. Formation of microvascular networks in vitro. Nat. Protoc. 2013, 8:1820-1836.
76. Murphy P.A., Kim T.N., Lu G., Bollen A.W., Schaffer C.B., Wang R.A. Notch4 normalization reduces blood vessel size in arteriovenous malformations. Sci. Transl. Med. 2012, 4:ra8.
77. Nagy J.A., Chang S.H., Shih S.C., Dvorak A.M., Dvorak H.F. Heterogeneity of the tumor vasculature. Semin. Thromb. Hemost. 2010, 36:321-331.
78. O'Grady R., Christensen A.L., Pinciroli C., Dorigo M. Robots autonomously self-assemble into dedicated morphologies to solve different tasks. Proceedings of the Ninth International Conference on Autonomous Agents and Multiagent Systems 2010, 1:1517-1518.
79. Parsa H., Upadhyay R., Sia S.K. Uncovering the behaviors of individual cells within a multicellular microvascular community. Proc. Natl. Acad. Sci. USA 2011, 108:5133-5138.
80. Perryn E.D., Czirók A., Little C.D. Vascular sprout formation entails tissue deformations and VE-cadherin-dependent cell-autonomous motility. Dev. Biol. 2008, 313:545-555.
81. Pfeifer R. Building fungus eaters: Design principles of autonomous agents. Proceedings of the Fourth International Conference on Simulation of Adaptive Behavior SAB96 (From Animals to Animats) 1996, 4:3-12.
82. Pfeifer R. Sensory-Motor Coordination: The Metaphor and Beyond. Robotics and Autonomous Systems 1997, 20:157-178.
83. Pfeifer R., Lungarella M., Iida F. Self-organization, embodiment, and biologically inspired robotics. Science 2007, 318:1088-1093.
84. Phng L.K., Stanchi F., Gerhardt H. Filopodia are dispensable for endothelial tip cell guidance. Development 2013, 140:4031-4040.
85. Piaget J., Inhelder B. The Child's Conception of Space 1967, W.W. Norton & Company, New York.
86. Pries A.R., Cornelissen A.J., Sloot A.A., Hinkeldey M., Dreher M.R., Höpfner M., Dewhirst M.W., Secomb T.W. Structural adaptation and heterogeneity of normal and tumor microvascular networks. PLoS Comput. Biol. 2009, 5:e1000394.
87. Qutub A.A., Mac Gabhann F., Karagiannis E.D., Vempati P., Popel A.S. Multiscale models of angiogenesis. IEEE Eng. Med. Biol. Mag. 2009, 28:14-31.
88. Regan E.R., Aird W.C. Dynamical systems approach to endothelial heterogeneity. Circ. Res. 2012, 111:110-130.
89. Ribeiro C., Neumann M., Affolter M. Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr. Biol. 2004, 14:2197-2207.
90. Rice W.L., Van Hoek A.N., Pǎunescu T.G., Huynh C., Goetze B., Singh B., Scipioni L., Stern L.A., Brown D. High resolution helium ion scanning microscopy of the rat kidney. PLoS ONE 2013, 8:e57051.
91. Ross T.D., Coon B.G., Yun S., Baeyens N., Tanaka K., Ouyang M., Schwartz M.A. Integrins in mechanotransduction. Curr. Opin. Cell Biol. 2013, 25:613-618.
92. Rubenstein M., Shen W.-M. Automatic scalable size selection for the shape of a distributed robotic collective. 2010 IEEE/RSJ International Conference on Intelligent Robots and Systems 2010, 508-513. 10.1109/IROS.2010.5650906.
93. Rubenstein M., Sai Y., Chuong C.M., Shen W.M. Regenerative patterning in Swarm Robots: mutual benefits of research in robotics and stem cell biology. Int. J. Dev. Biol. 2009, 53:869-881.
94. Rubenstein M., Ahler C., Nagpal R. Kilobot: A low cost scalable robot system for collective behaviors. 2012 IEEE International Conference on Robotics and Automation 2012, 3293-3298. 10.1109/ICRA.2012.6224638.
95. Rubin R., Strayer D.S., Rubin E., McDonald J.M. Rubin's pathology: clinicopathologic foundations of medicine 2008, Lippincott Williams & Wilkins, Baltimore, MD.
96. Secomb T.W., Alberding J.P., Hsu R., Dewhirst M.W., Pries A.R. Angiogenesis: an adaptive dynamic biological patterning problem. PLoS Comput. Biol. 2013, 9:e1002983.
97. Shasby D.M., Shasby S.S., Sullivan J.M., Peach M.J. Role of endothelial cell cytoskeleton in control of endothelial permeability. Circ. Res. 1982, 51:657-661.
98. Simon H.A. The sciences of the artificial 1996, MIT Press, Cambridge, MA.
99. Simons M. Integrative signaling in angiogenesis. Mol. Cell. Biochem. 2004, 264:99-102.
100. Stefanini M.O., Wu F.T., Mac Gabhann F., Popel A.S. The presence of VEGF receptors on the luminal surface of endothelial cells affects VEGF distribution and VEGF signaling. PLoS Comput. Biol. 2009, 5:e1000622.
101. Stefanini M.O., Wu F.T., Mac Gabhann F., Popel A.S. Increase of plasma VEGF after intravenous administration of bevacizumab is predicted by a pharmacokinetic model. Cancer Res. 2010, 70:9886-9894.
102. Szabo A., Perryn E.D., Czirok A. Network formation of tissue cells via preferential attraction to elongated structures. Phys. Rev. Lett. 2007, 98:038102.
103. Szczerba D., Kurz H., Szekely G. A computational model of intussusceptive microvascular growth and remodeling. J. Theor. Biol. 2009, 261:570-583.
104. Tambe D.T., Hardin C.C., Angelini T.E., Rajendran K., Park C.Y., Serra-Picamal X., Zhou E.H., Zaman M.H., Butler J.P., Weitz D.A., et al. Collective cell guidance by cooperative intercellular forces. Nat. Mater. 2011, 10:469-475.
105. Thorne B.C., Hayenga H.N., Humphrey J.D., Peirce S.M. Toward a multi-scale computational model of arterial adaptation in hypertension: verification of a multi-cell agent based model. Front Physiol 2011, 2:20.
106. Tomlin C.J., Axelrod J.D. Biology by numbers: mathematical modelling in developmental biology. Nat. Rev. Genet. 2007, 8:331-340.
107. Tozluoǧlu M., Tournier A.L., Jenkins R.P., Hooper S., Bates P.A., Sahai E. Matrix geometry determines optimal cancer cell migration strategy and modulates response to interventions. Nat. Cell Biol. 2013, 15:751-762.
108. Tsai Y.C., Hsieh H.J., Liao F., Ni C.W., Chao Y.J., Hsieh C.Y., Wang D.L. Laminar flow attenuates interferon-induced inflammatory responses in endothelial cells. Cardiovasc. Res. 2007, 74:497-505.
109. Tyson J.J., Chen K.C., Novak B. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr. Opin. Cell Biol. 2003, 15:221-231.
110. Villefranc J.A., Nicoli S., Bentley K., Jeltsch M., Zarkada G., Moore J.C., Gerhardt H., Alitalo K., Lawson N.D. A truncation allele in vascular endothelial growth factor c reveals distinct modes of signaling during lymphatic and vascular development. Development 2013, 140:1497-1506.
111. Vitorino P., Meyer T. Modular control of endothelial sheet migration. Genes Dev. 2008, 22:3268-3281.
112. Vitorino P., Hammer M., Kim J., Meyer T. A steering model of endothelial sheet migration recapitulates monolayer integrity and directed collective migration. Mol. Cell. Biol. 2011, 31:342-350.
113. Von Uexküll J. Theoretische Biologie 1920, 260. Verlag von Gebrüder Paetel, Berlin.
114. Wallace D.K., Kylstra J.A., Greenman D.B., Freedman S.F. Significance of isolated neovascular tufts ("popcorn") in retinopathy of prematurity. J. AAPOS 1998, 2:52-56.
115. Walpole J., Papin J.A., Peirce S.M. Multiscale computational models of complex biological systems. Annu. Rev. Biomed. Eng. 2013, 15:137-154.
116. Watson M.G., McDougall S.R., Chaplain M.A., Devlin A.H., Mitchell C.A. Dynamics of angiogenesis during murine retinal development: a coupled in vivo and in silico study. J. R. Soc. Interface 2012, 9:2351-2364.
117. Webb B. What does robotics offer animal behaviour?. Anim. Behav. 2000, 60:545-558.
118. Webb B. Can robots make good models of biological behaviour?. Behav. Brain Sci. 2001, 24:1033-1050. discussion 1050-1094.
119. Webb B. Animals versus animats: Or why not model the real iguana?. Adapt. Behav. 2009, 17:269-286.
120. Werfel J., Krause S., Bischof A.G., Mannix R.J., Tobin H., Bar-Yam Y., Bellin R.M., Ingber D.E. How changes in extracellular matrix mechanics and gene expression variability might combine to drive cancer progression. PLoS ONE 2013, 8:e76122.
121. Yao L.C., Baluk P., Srinivasan R.S., Oliver G., McDonald D.M. Plasticity of button-like junctions in the endothelium of airway lymphatics in development and inflammation. Am. J. Pathol. 2012, 180:2561-2575.
122. Zakrzewicz A., Secomb T.W., Pries A.R. Angioadaptation: keeping the vascular system in shape. News Physiol. Sci. 2002, 17:197-201.
123. Zovein A.C., Luque A., Turlo K.A., Hofmann J.J., Yee K.M., Becker M.S., Fassler R., Mellman I., Lane T.F., Iruela-Arispe M.L. Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev. Cell 2010, 18:39-51.