The role of differential VE-cadherin dynamics in cell rearrangement during angiogenesis

Nature Cell Biology

Volumn 16, Issue 4, 2014, Pages 309-321

  Bentley, Katie ^a,f   Franco, Claudio Areias ^a   Philippides, Andrew ^b   Blanco, Raquel ^a   Dierkes, Martina ^c   Gebala, Véronique ^a   Stanchi, Fabio ^d   Jones, Martin ^a   Aspalter, Irene M ^a   Cagna, Guiseppe ^c   Weström, Simone ^e   Claesson Welsh, Lena ^e   Vestweber, Dietmar ^c   Gerhardt, Holger ^a,d  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e UPPSALA UNIVERSITY   (Sweden)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRANCHING MORPHOGENESIS; CELL ADHESION, CELL AGGLUTINATION AND CELL AGGREGATION; CELL INTERACTION; CELL JUNCTION; CELL MOTION; CELL REARRANGEMENT; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; MALE; MATHEMATICAL MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD; CADHERINS; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; COMPUTER SIMULATION; DIABETIC RETINOPATHY; ENDOTHELIAL CELLS; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INTERCELLULAR JUNCTIONS; MALE; MICE; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84897536435     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2926     Document Type: Article

References (60)

1. Potente, M., Gerhardt, H. & Carmeliet, P. Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887 (2011).
2. Jakobsson, L. et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat. Cell Biol. 12, 943-953 (2010).
3. Arima, S. et al. Angiogenic morphogenesis driven by dynamic and heterogeneous collective endothelial cell movement. Development 138, 4763-4776 (2011).
4. Suchting, S. et al. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc. Natl Acad. Sci. USA 104, 3225-3230 (2007).
5. Siekmann, A. F. & Lawson, N. D. Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784 (2007).
6. Lobov, I. B. et al. Delta-like ligand 4 (Dll4 is induced by VEGF as a negative regulator of angiogenic sprouting. Proc. Natl Acad. Sci. USA 104, 3219-3224 (2007).
7. Hellstrom, M. et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780 (2007).
8. Gerhardt, H. et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177 (2003).
9. 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. 5, e1000549 (2009).
10. Pilot, F. & Lecuit, T. Compartmentalized morphogenesis in epithelia: From cell to tissue shape. Dev. Dyn. 232, 685-694 (2005).
11. Zallen, J. A. & Blankenship, J. T. Multicellular dynamics during epithelial elongation. Semin. Cell Dev. Biol. 19, 263-270 (2008).
12. Keller, R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950-1954 (2002).
13. Jung, A. C., Denholm, B., Skaer, H. & Affolter, M. Renal tubule development in Drosophila: A closer look at the cellular level. J. Am. Soc. Nephrol. 16, 322-328 (2005).
14. Neumann, M. & Affolter, M. Remodelling epithelial tubes through cell rearrangements: From cells to molecules. EMBO Rep. 7, 36-40 (2006).
15. Blum, Y. et al. Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316, 312-322 (2008).
16. Lenard, A. et al. In vivo analysis reveals a highly stereotypic morphogenetic pathway of vascular anastomosis. Dev. Cell 25, 492-506 (2013).
17. Perryn, E. D., Czirok, A. & Little, C. D. Vascular sprout formation entails tissue deformations and VE-cadherin-dependent cell-Autonomous motility. Dev. Biol. 313, 545-555 (2008).
18. Vitorino, P. & Meyer, T. Modular control of endothelial sheet migration. Genes Dev. 3268-3281 (2008).
19. Steinberg, M. S. Differential adhesion in morphogenesis: A modern view. Curr. Opin. Genet. Dev. 17, 281-286 (2007).
20. Foty, R. A. & Steinberg, M. S. The differential adhesion hypothesis: A direct evaluation. Dev. Biol. 278, 255-263 (2005).
21. Gavard, J. & Gutkind, J. S. VEGF controls endothelial-cell permeability by promoting the beta-Arrestin-dependent endocytosis of VE-cadherin. Nat. Cell Biol. 8, 1223-1234 (2006).
22. Bertet, C., Sulak, L. & Lecuit, T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671 (2004).
23. Bentley, K., Gerhardt, H. & Bates, P. A. Agent-based simulation of notchmediated tip cell selection in angiogenic sprout initialisation. J. Theor. Biol. 250, 25-36 (2008).
24. Graner, F. & Glazier, J. A. Simulation of biological cell sorting using a two-dimensional extended Potts model. Phys. Rev. Lett. 69, 2013-2016 (1992).
25. Merks, R. M. & Glazier, J. A. A cell-centered approach to developmental biology. Physics A 352, 113-130 (2005).
26. Kametani, Y. & Takeichi, M. Basal-To-Apical cadherin flow at cell junctions. Nat. Cell Biol. 9, 92-98 (2007).
27. Huveneers, S. et al. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J. Cell Biol. 196, 641-652 (2012).
28. Ngok, S. P. et al. VEGF and Angiopoietin-1 exert opposing effects on cell junctions by regulating the Rho GEF Syx. J. Cell Biol. 199, 1103-1115 (2012).
29. Saharinen, P. & Alitalo, K. The yin, the yang, and the angiopoietin-1. J. Clin. Invest. 121, 2157-2159 (2011).
30. Orsenigo, F. et al. Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nature Commun. 3, 1208 (2012).
31. Matsumoto, T. et al. VEGF receptor-2 Y951 signaling and a role for the adapter molecule TSAd in tumor angiogenesis. EMBO J. 24, 2342-2353 (2005).
32. Sun, Z. et al. VEGFR2 induces c-Src signaling and vascular permeability in vivo via the adaptor protein TSAd. J. Exp. Med. 209, 1363-1377 (2012).
33. Smith, L. E. et al. Oxygen-induced retinopathy in the mouse. Invest. Ophthal. Visual Sci. 35, 101-111 (1994).
34. Goddard, L. M. & Iruela-Arispe, M. L. Cellular and molecular regulation of vascular permeability. Thrombos. Haemo. 109, 407-415 (2013).
35. Amack, J. D. & Manning, M. L. Knowing the boundaries: Extending the differential adhesion hypothesis in embryonic cell sorting. Science 338, 212-215 (2012).
36. Levayer, R., Pelissier-Monier, A. & Lecuit, T. Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat. Cell Biol. 13, 529-540 (2011).
37. Nelson, C. M., Pirone, D. M., Tan, J. L. & Chen, C. S. Vascular endothelial-cadherin regulates cytoskeletal tension, cell spreading, and focal adhesions by stimulating RhoA. Mol. Biol. Cell 15, 2943-2953 (2004).
38. Kouklis, P., Konstantoulaki, M. & Malik, A. B. VE-cadherin-induced Cdc42 signaling regulates formation of membrane protrusions in endothelial cells. J. Biol. Chem. 278, 16230-16236 (2003).
39. Podgorski, G. J., Bansal, M. & Flann, N. S. Regular mosaic pattern development: A study of the interplay between lateral inhibition, apoptosis and differential adhesion. Theor. Biol. Med. Model. 4, 43 (2007).
40. Goodwin, B. C., Kauffman, S. & Murray, J. D. Is morphogenesis an intrinsically robust process?. J. Theor. Biol. 163, 135-144 (1993).
41. Bauer, A. L., Jackson, T. L., Jiang, Y. & Rohlf, T. Receptor cross-Talk in angiogenesis: Mapping environmental cues to cell phenotype using a stochastic, Boolean signaling network model. J. Theor. Biol. 264, 838-846 (2010).
42. Sandersius, S. A. & Newman, T. J. Modeling cell rheology with the Subcellular Element Model. Phys. Biol. 5, 015002 (2008).
43. Van Oss, C., Panfilov, A. V., Hogeweg, P., Siegert, F. & Weijer, C. J. Spatial pattern formation during aggregation of the slime mould Dictyostelium discoideum. J. Theor. Biol. 181, 203-213 (1996).
44. Mao, Y. et al. Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. Genes Dev. 25, 131-136 (2011).
45. Meineke, F. A., Potten, C. S. & Loeffler, M. Cell migration and organization in the intestinal crypt using a lattice-free model. Cell Prolif. 34, 253-266 (2001).
46. Tozluoglu, M. et al. Matrix geometry determines optimal cancer cell migration strategy and modulates response to interventions. Nat. Cell Biol. 15, 751-762 (2013).
47. 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. American J. Phys. Heart Circul. Phys. 286, H153-H164 (2004).
48. Bartha, K. & Rieger, H. Vascular network remodeling via vessel cooption, regression and growth in tumors. J. Theor. Biol. 241, 903-918 (2006).
49. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. & Melton, D. A. Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl Acad. Sci. USA 100, 14920-14925 (2003).
50. Claxton, S. et al. Efficient, inducible Cre-recombinase activation in vascular endothelium. Genesis 46, 74-80 (2008).
51. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global doublefluorescent Cre reporter mouse. Genesis 45, 593-605 (2007).
52. Rajagopal, K. et al. RIBP, a novel Rlk/Txk-And itk-binding adaptor protein that regulates T cell activation. J. Exp. Med. 190, 1657-1668 (1999).
53. Franco, C. A. et al. SRF selectively controls tip cell invasive behavior in angiogenesis. Development 140, 2321-2333 (2013).
54. Broermann, A. et al. Dissociation of VE-PTP from VE-cadherin is required for leukocyte extravasation and for VEGF-induced vascular permeability in vivo. J. Exp. Med. 208, 2393-2401 (2011).
55. Shaw, S. K., Bamba, P. S., Perkins, B. N. & Luscinskas, F. W. Real-Time imaging of vascular endothelial-cadherin during leukocyte transmigration across endothelium. J. Immunol. 167, 2323-2330 (2001).
56. Winderlich, M. et al. VE-PTP controls blood vessel development by balancing Tie-2 activity. J. Cell Biol. 185, 657-671 (2009).
57. Hayashi, M. et al. VE-PTP regulates VEGFR2 activity in stalk cells to establish endothelial cell polarity and lumen formation. Nat. Commun. 4, 1672 (2013).
58. Seyfried, T. N., el-Abbadi, M. & Roy, M. L. Ganglioside distribution in murine neural tumors. Mol. Chem. Neuropathol. 17, 147-167 (1992).
59. Subach, O. M. et al. Conversion of red fluorescent protein into a bright blue probe. Chem. Biol. 15, 1116-1124 (2008).
60. Holtmaat, A. et al. Long-Term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4, 1128-1144 (2009).