Angiogenic morphogenesis driven by dynamic and heterogeneous collective endothelial cell movement

Development

Volumn 138, Issue 21, 2011, Pages 4763-4776

  Arima, Satoshi ^a   Nishiyama, Koichi ^a   Ko, Toshiyuki ^a   Arima, Yuichiro ^a   Hakozaki, Yuji ^a   Sugihara, Kei ^a   Koseki, Hiroaki ^a   Uchijima, Yasunobu ^a   Kurihara, Yukiko ^a   Kurihara, Hiroki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Angiogenesis; Collective cell movement; Mouse; Time lapse imaging

Indexed keywords

GAMMA SECRETASE; NOTCH RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MIGRATION; CELL MOTION; CELL STRUCTURE; COMPUTER ANALYSIS; DELTA LIKE 4 GENE; ENDOTHELIUM CELL; GENE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; RETINA BLOOD VESSEL;

ANIMALS; AORTA; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; IMAGE PROCESSING, COMPUTER-ASSISTED; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MORPHOGENESIS; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, NOTCH; RETINAL VESSELS; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING;

MURINAE;

EID: 80053980982     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.068023     Document Type: Article

References (45)

1. Armulik, A., Abramsson, A. and Betsholtz, C. (2005). Endothelial/pericyte interactions. Circ. Res. 97, 512-523.
2. Asai, R., Kurihara, Y., Fujisawa, K., Sato, T., Kawamura, Y., Kokubo, H., Tonami, K., Nishiyama, K., Uchijima, Y., Miyagawa-Tomita, S. et al. (2010). Endothelin receptor type A expression defines a distinct cardiac subdomain within the heart field and is later implicated in chamber myocardium formation. Development 137, 3823-3833.
3. Bauer, H. C., Steiner, M. and Bauer, H. (1992). Embryonic development of the CNS microvasculature in the mouse: new insights into the structural mechanisms of early angiogenesis. EXS 61, 64-68.
4. Blacher, S., Devy, L., Burbridge, M. F., Roland, G., Tucker, G., Noel, A. and Foidart, J. M. (2001). Improved quantification of angiogenesis in the rat aortic ring assay. Angiogenesis 4, 133-142.
5. Boulton, M. E., Cai, J. and Grant, M. B. (2008). Gamma-Secretase: a multifaceted regulator of angiogenesis. J. Cell. Mol. Med. 12, 781-795.
6. Claxton, S. and Fruttiger, M. (2004). Periodic Delta-like 4 expression in developing retinal arteries. Gene Expr. Patterns 5, 123-127.
7. Dai, J., Sultan, S., Taylor, S. S. and Higgins, J. M. (2005). The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev. 19, 472-488.
8. De Smet, F., Segura, I., De Bock, K., Hohensinner, P. J. and Carmeliet, P. (2009). Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler. Thromb. Vasc. Biol. 29, 639-649.
9. del Toro, R., Prahst, C., Mathivet, T., Siegfried, G., Kaminker, J. S., Larrivee, B., Breant, C., Duarte, A., Takakura, N., Fukamizu, A. et al. (2010). Identification and functional analysis of endothelial tip cell-enriched genes. Blood 116, 4025-4033.
10. Domenga, V., Fardoux, P., Lacombe, P., Monet, M., Maciazek, J., Krebs, L. T., Klonjkowski, B., Berrou, E., Mericskay, M., Li, Z. et al. (2004). Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 18, 2730-2735.
11. Friedl, P. and Gilmour, D. (2009). Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10, 445-457.
12. Gaengel, K., Genove, G., Armulik, A. and Betsholtz, C. (2009). Endothelialmural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 29, 630-638.
13. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177.
14. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
15. Hellstrom, M., Gerhardt, H., Kalen, M., Li, X., Eriksson, U., Wolburg, H. and Betsholtz, C. (2001). Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J. Cell Biol. 153, 543-553.
16. Hellstrom, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P., Alva, J., Nilsson, A. K., Karlsson, L., Gaiano, N. et al. (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780.
17. Hendzel, M. J., Wei, Y., Mancini, M. A., Van Hooser, A., Ranalli, T., Brinkley, B. R., Bazett-Jones, D. P. and Allis, C. D. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360.
18. Hofmann, J. J. and Luisa Iruela-Arispe, M. (2007). Notch expression patterns in the retina: an eye on receptor-ligand distribution during angiogenesis. Gene Expr. Patterns 7, 461-470.
19. Holderfield, M. T. and Hughes, C. C. (2008). Crosstalk between vascular endothelial growth factor, notch, and transforming growth factor-beta in vascular morphogenesis. Circ. Res. 102, 637-652.
20. Itoh, F., Itoh, S., Goumans, M.-J., Valdimarsdottir, G., Iso, T., Dotto, G. P., Hamamori, Y., Kedes, L., Kato, M. and ten Dijke, P. (2004). Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. EMBO J. 23, 541-551.
21. 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. (2010). Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat. Cell Biol. 12, 943-953.
22. Jin, S., Hansson, E. M., Tikka, S., Lanner, F., Sahlgren, C., Farnebo, F., Baumann, M., Kalimo, H. and Lendahl, U. (2008). Notch signaling regulates platelet-derived growth factor receptor-beta expression in vascular smooth muscle cells. Circ. Res. 102, 1483-1491.
23. Lafleur, M. A., Forsyth, P. A., Atkinson, S. J., Murphy, G. and Edwards, D. R. (2001). Perivascular cells regulate endothelial membrane type-1 matrix metalloproteinase activity. Biochem. Biophys. Res. Commun. 282, 463-473.
24. Liu, H., Kennard, S. and Lilly, B. (2009). NOTCH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1. Circ. Res. 104, 466-475.
25. Montell, D. J. (2008). Morphogenetic cell movements: diversity from modular mechanical properties. Science 322, 1502-1505.
26. Murakami, T., Suzuma, K., Takagi, H., Kita, M., Ohashi, H., Watanabe, D., Ojima, T., Kurimoto, M., Kimura, T., Sakamoto, A. et al. (2006). Time-lapse imaging of vitreoretinal angiogenesis originating from both quiescent and mature vessels in a novel ex vivo system. Invest. Ophthalmol. Vis. Sci. 47, 5529-5536.
27. Nishiyama, K., Takaji, K., Kataoka, K., Kurihara, Y., Yoshimura, M., Kato, A., Ogawa, H. and Kurihara, H. (2005). Id1 gene transfer confers angiogenic property on fully differentiated endothelial cells and contributes to therapeutic angiogenesis. Circulation 112, 2840-2850.
28. Noguera-Troise, I., Daly, C., Papadopoulos, N. J., Coetzee, S., Boland, P., Gale, N. W., Lin, H. C., Yancopoulos, G. D. and Thurston, G. (2006). Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444, 1032-1037.
29. Ozerdem, U. and Stallcup, W. B. (2003). Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 6, 241-249.
30. Ozerdem, U., Grako, K. A., Dahlin-Huppe, K., Monosov, E. and Stallcup, W. B. (2001). NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev. Dyn. 222, 218-227.
31. Perryn, E. D., Czirok, A. and Little, C. D. (2008). Vascular sprout formation entails tissue deformations and VE-cadherin-dependent cell-autonomous motility. Dev. Biol. 313, 545-555.
32. Phng, L. K. and Gerhardt, H. (2009). Angiogenesis: a team effort coordinated by notch. Dev. Cell 16, 196-208.
33. Provis, J. M., Leech, J., Diaz, C. M., Penfold, P. L., Stone, J. and Keshet, E. (1997). Development of the human retinal vasculature: cellular relations and VEGF expression. Exp. Eye Res. 65, 555-568.
34. Ridgway, J., Zhang, G., Wu, Y., Stawicki, S., Liang, W. C., Chanthery, Y., Kowalski, J., Watts, R. J., Callahan, C., Kasman, I. et al. (2006). Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444, 1083-1087.
35. Schmidt, M., Paes, K., De Maziere, A., Smyczek, T., Yang, S., Gray, A., French, D., Kasman, I., Klumperman, J., Rice, D. S. et al. (2007). EGFL7 regulates the collective migration of endothelial cells by restricting their spatial distribution. Development 134, 2913-2923.
36. Siekmann, A. F. and Lawson, N. D. (2007). Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784.
37. Stone, J., Itin, A., Alon, T., Pe'er, J., Gnessin, H., Chan-Ling, T. and Keshet, E. (1995). Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J. Neurosci. 15, 4738-4747.
38. Suchting, S., Freitas, C., le Noble, F., Benedito, R., Breant, C., Duarte, A. and Eichmann, A. (2007). The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc. Natl. Acad. Sci. USA 104, 3225-3230.
39. Theveneau, E., Marchant, L., Kuriyama, S., Gull, M., Moepps, B., Parsons, M. and Mayor, R. (2010). Collective chemotaxis requires contact-dependent cell polarity. Dev. Cell 19, 39-53.
40. Uemura, A., Ogawa, M., Hirashima, M., Fujiwara, T., Koyama, S., Takagi, H., Honda, Y., Wiegand, S. J., Yancopoulos, G. D. and Nishikawa, S. (2002). Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J. Clin. Invest. 110, 1619-1628.
41. van Hinsbergh, V. W. and Koolwijk, P. (2008). Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovasc. Res. 78, 203-212.
42. Vitorino, P. and Meyer, T. (2008). Modular control of endothelial sheet migration. Genes Dev. 22, 3268-3281.
43. Williams, C. K., Li, J. L., Murga, M., Harris, A. L. and Tosato, G. (2006). Upregulation of the Notch ligand Delta-like 4 inhibits VEGF-induced endothelial cell function. Blood 107, 931-939.
44. Yamanda, S., Ebihara, S., Asada, M., Okazaki, T., Niu, K., Ebihara, T., Koyanagi, A., Yamaguchi, N., Yagita, H. and Arai, H. (2009). Role of ephrinB2 in nonproductive angiogenesis induced by Delta-like 4 blockade. Blood 113, 3631-3639.
45. Yamashita, J., Itoh, H., Hirashima, M., Ogawa, M., Nishikawa, S., Yurugi, T., Naito, M. and Nakao, K. (2000). Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408, 92-96.