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Nrarp Coordinates Endothelial Notch and Wnt Signaling to Control Vessel Density in Angiogenesis
Open accessAbstract
SUMMARY When and where to make or break new blood vessel connections is the key to understanding guided vascular patterning. VEGF-A stimulation and Dll4/Notch signaling cooperatively control the number of new connections by regulating endothelial tip cell formation. Here, we show that the Notch-regulated ankyrin repeat protein (Nrarp) acts as a molecular link between Notch- and Lef1-dependent Wnt signaling in endothelial cells to control stability of new vessel connections in mouse and zebrafish. Dll4/Notch-induced expression of Nrarp limits Notch signaling and promotes Wnt/Ctnnb1 signaling in endothelial stalk cells through interactions with Lef1. BATgal-reporter expression confirms Wnt signaling activity in endothelial stalk cells. Ex vivo, combined Wnt3a and Dll4 stimulation of endothelial cells enhances Wnt-reporter activity, which is abrogated by loss of Nrarp. In vivo, loss of Nrarp, Lef1, or endothelial Ctnnb1 causes vessel regression. We suggest that the balance between Notch and Wnt signaling determines whether to make or break new vessel connections.
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Cites
Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus
Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M., & Costantini, F. (2001) · BMC Developmental Biology · doi:10.1186/1471-213x-1-4 · Cited by 3,121
VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia
Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302047 · Cited by 2,894
Self-citationThe cyclin D1 gene is a target of the β-catenin/LEF-1 pathway
Shtutman, M., Zhurinsky, J., Simcha, I., Albanese, C., D’Amico, M., Pestell, R., & Ben-Ze’ev, A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.10.5522 · Cited by 2,230
In Vivo Imaging of Embryonic Vascular Development Using Transgenic Zebrafish
Lawson, N. D., & Weinstein, B. M. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0711 · Cited by 2,151
Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis
Hellström, 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) · Nature · doi:10.1038/nature05571 · Cited by 1,775
Self-citationIntestinal polyposis in mice with a dominant stable mutation of the beta -catenin gene
Harada, N. (1999) · The EMBO Journal · doi:10.1093/emboj/18.21.5931 · Cited by 1,212
Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O., & Kemler, R. (2001) · Development · doi:10.1242/dev.128.8.1253 · Cited by 1,088
LDL receptor-related proteins 5 and 6 in Wnt/β-catenin signaling:Arrows point the way
He, X., Semenov, M., Tamai, K., & Zeng, X. (2004) · Development · doi:10.1242/dev.01117 · Cited by 1,044
Zebrafish Prickle, a Modulator of Noncanonical Wnt/Fz Signaling, Regulates Gastrulation Movements
Veeman, M. T., Slusarski, D. C., Kaykas, A., Louie, S. H., & Moon, R. T. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00240-9 · Cited by 945
Vascular Development in the Retina and Inner Ear
Xu, Q., Wang, Y., Dabdoub, A., Smallwood, P. M., Williams, J., Woods, C., Kelley, M. W., Jiang, L., Tasman, W., Zhang, K., et al. (2004) · Cell · doi:10.1016/s0092-8674(04)00216-8 · Cited by 875
Morita, K., Sasaki, H., Furuse, M., & Tsukita, S. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.147.1.185 · Cited by 869
Suchting, S., Freitas, C., le Noble, F., Benedito, R., Bréant, C., Duarte, A., & Eichmann, A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611177104 · Cited by 811
Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting
Lobov, I. B., Renard, R. A., Papadopoulos, N., Gale, N. W., Thurston, G., Yancopoulos, G. D., & Wiegand, S. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611206104 · Cited by 774
Self-citationMapping Wnt/β-catenin signaling during mouse development and in colorectal tumors
Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M., & Piccolo, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0434590100 · Cited by 761
Inai, T., Mancuso, M., Hashizume, H., Baffert, F., Haskell, A., Baluk, P., Hu-Lowe, D. D., Shalinsky, D. R., Thurston, G., Yancopoulos, G. D., et al. (2004) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63273-7 · Cited by 757
Self-citationNotch signalling limits angiogenic cell behaviour in developing zebrafish arteries
Siekmann, A. F., & Lawson, N. D. (2007) · Nature · doi:10.1038/nature05577 · Cited by 687
Vascular endothelial–cadherin is an important determinant of microvascular integrity invivo
Corada, M., Mariotti, M., Thurston, G., Smith, K., Kunkel, R., Brockhaus, M., Lampugnani, M. G., Martin-Padura, I., Stoppacciaro, A., Ruco, L., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9815 · Cited by 676
Self-citationPericytes and the Pathogenesis of Diabetic Retinopathy
Hammes, H.-P., Lin, J., Renner, O., Shani, M., Lundqvist, A., Betsholtz, C., Brownlee, M., & Deutsch, U. (2002) · Diabetes · doi:10.2337/diabetes.51.10.3107 · Cited by 665
Lubarsky, B., & Krasnow, M. A. (2003) · Cell · doi:10.1016/s0092-8674(02)01283-7 · Cited by 660
SIRT1 Controls Endothelial Angiogenic Functions During Vascular Growth
Potente, M., Ghaeni, L., Baldessari, D., Mostoslavsky, R., Rossig, L., Dequiedt, F., Haendeler, J., Mione, M., Dejana, E., Alt, F. W., et al. (2007) · Genes & Development · doi:10.1101/gad.435107 · Cited by 608
Self-citationHigh-throughput engineering of the mouse genome coupled with high-resolution expression analysis
Valenzuela, D. M., Murphy, A. J., Frendewey, D., Gale, N. W., Economides, A. N., Auerbach, W., Poueymirou, W. T., Adams, N. C., Rojas, J., Yasenchak, J., et al. (2003) · Nature Biotechnology · doi:10.1038/nbt822 · Cited by 584
Regulation of LEF-1/TCF transcription factors by Wnt and other signals
Eastman, Q., & Grosschedl, R. (1999) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)80031-3 · Cited by 540
Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization
Potente, M., Urbich, C., Sasaki, K.-I., Hofmann, W. K., Heeschen, C., Aicher, A., Kollipara, R., DePinho, R. A., Zeiher, A. M., & Dimmeler, S. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23126 · Cited by 531
Self-citationLiu, Z.-J., Shirakawa, T., Li, Y., Soma, A., Oka, M., Dotto, G. P., Fairman, R. M., Velazquez, O. C., & Herlyn, M. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.1.14-25.2003 · Cited by 500
WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature
Lobov, I. B., Rao, S., Carroll, T. J., Vallance, J. E., Ito, M., Ondr, J. K., Kurup, S., Glass, D. A., Patel, M. S., Shu, W., et al. (2005) · Nature · doi:10.1038/nature03928 · Cited by 430
Self-citationNotch signaling in vascular development and physiology
Gridley, T. (2007) · Development · doi:10.1242/dev.004184 · Cited by 429
Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis
Leslie, J. D., Ariza-McNaughton, L., Bermange, A. L., McAdow, R., Johnson, S. L., & Lewis, J. (2007) · Development · doi:10.1242/dev.003244 · Cited by 415
Self-citationBaffert, F., Le, T., Sennino, B., Thurston, G., Kuo, C. J., Hu-Lowe, D., & McDonald, D. M. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00616.2005 · Cited by 374
Self-citationHsu, S.-C., Galceran, J., & Grosschedl, R. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.8.4807 · Cited by 363
Efficient, inducible Cre‐recombinase activation in vascular endothelium
Claxton, S., Kostourou, V., Jadeja, S., Chambon, P., Hodivala‐Dilke, K., & Fruttiger, M. (2008) · genesis · doi:10.1002/dvg.20367 · Cited by 327
Cattelino, A., Liebner, S., Gallini, R., Zanetti, A., Balconi, G., Corsi, A., Bianco, P., Wolburg, H., Moore, R., Oreda, B., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200212157 · Cited by 323
Blum, Y., Belting, H.-G., Ellertsdottir, E., Herwig, L., Lüders, F., & Affolter, M. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.01.038 · Cited by 315
Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis.
Fruttiger, M. (2002) · PubMed · Cited by 278
Wnt/β-Catenin Signaling Induces Proliferation, Survival and Interleukin-8 in Human Endothelial Cells
Masckauchán, T. N. H., Shawber, C. J., Funahashi, Y., Li, C.-M., & Kitajewski, J. (2005) · Angiogenesis · doi:10.1007/s10456-005-5612-9 · Cited by 249
Masckauchán, T. N. H., Agalliu, D., Vorontchikhina, M., Ahn, A., Parmalee, N. L., Li, C.-M., Khoo, A., Tycko, B., Brown, A. M. C., & Kitajewski, J. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-04-0320 · Cited by 223
Noseda, M., Chang, L., McLean, G., Grim, J. E., Clurman, B. E., Smith, L. L., & Karsan, A. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.20.8813-8822.2004 · Cited by 218
Harrington, L. S., Sainson, R. C. A., Williams, C. K., Taylor, J. M., Shi, W., Li, J.-L., & Harris, A. L. (2008) · Microvascular Research · doi:10.1016/j.mvr.2007.06.006 · Cited by 215
Nrarp is a novel intracellular component of the Notch signaling pathway
Lamar, E., Deblandre, G., Wettstein, D., Gawantka, V., Pollet, N., Niehrs, C., & Kintner, C. (2001) · Genes & Development · doi:10.1101/gad.908101 · Cited by 188
VEGF and Notch Signaling: The Yin and Yang of Angiogenic Sprouting
Hellström, M., Phng, L.-K., & Gerhardt, H. (2007) · Cell Adhesion & Migration · doi:10.4161/cam.1.3.4978 · Cited by 167
Self-citationKrebs, L. T., Deftos, M. L., Bevan, M. J., & Gridley, T. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0408 · Cited by 133
RBP-L, a Transcription Factor Related to RBP-Jκ
Minoguchi, S., Taniguchi, Y., Kato, H., Okazaki, T., Strobl, L. J., Zimber‐Strobl, U., Bornkamm, G. W., & Honjo, T. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.5.2679 · Cited by 131
The Notch Intracellular Domain Can Function as a Coactivator for LEF-1
Ross, D. A., & Kadesch, T. R. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.22.7537-7544.2001 · Cited by 122
Yun, T. J., & Bevan, M. J. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.12.5834 · Cited by 119
Obligatory participation of macrophages in an angiopoietin 2-mediated cell death switch
Rao, S., Lobov, I. B., Vallance, J. E., Tsujikawa, K., Shiojima, I., Akunuru, S., Walsh, K. X., Benjamin, L. E., & Lang, R. A. (2007) · Development · doi:10.1242/dev.012187 · Cited by 116
Self-citationA model for familial exudative vitreoretinopathy caused by LPR5 mutations
Xia, C., Liu, H., Cheung, D., Wang, M., Cheng, C., Du, X., Chang, B., Beutler, B., & Gong, X. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn047 · Cited by 108
Nrarp functions to modulate neural-crest-cell differentiation by regulating LEF1 protein stability
Ishitani, T., Matsumoto, K., Chitnis, A. B., & Itoh, M. (2005) · Nature Cell Biology · doi:10.1038/ncb1311 · Cited by 90
Martin, M., Potente, M., Janssens, V., Vertommen, D., Twizere, J., Rider, M. H., Goris, J., Dimmeler, S., Kettmann, R., & Dequiedt, F. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708455105 · Cited by 80
Self-citationBader, H. L., Keene, D. R., Charvet, B., Veit, G., Driever, W., Koch, M., & Ruggiero, F. (2008) · Matrix Biology · doi:10.1016/j.matbio.2008.09.580 · Cited by 79
Direct regulation of the Nrarp gene promoter by the Notch signaling pathway
Pirot, P., van Grunsven, L. A., Marine, J., Huylebroeck, D., & Bellefroid, E. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.07.157 · Cited by 56
Oxygen modifies artery differentiation and network morphogenesis in the retinal vasculature
Claxton, S., & Fruttiger, M. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20407 · Cited by 50
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Potente, M., Gerhardt, H., & Carmeliet, P. (2011) · Cell · doi:10.1016/j.cell.2011.08.039 · Cited by 2,771
Self-citationNotch signaling: simplicity in design, versatility in function
Andersson, E. R., Sandberg, R., & Lendahl, U. (2011) · Development · doi:10.1242/dev.063610 · Cited by 950
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Metadata
- Authors
- Phng, L.-K., Potente, M., Leslie, J. D., Babbage, J., Nyqvist, D., Lobov, I., Ondr, J. K., Rao, S., Lang, R. A., Thurston, G., & Gerhardt, H.
- Venue
- Developmental Cell
- Publisher
- Elsevier BV
- Published
- 2009-01
- Volume
- 16
- Issue
- 1
- Pages
- 70-82
- ISSN
- 1534-5807 (ISSN-L)
- OpenAlex
- W2028561648
- Cited by
- 349
- References
- 50
- FWCI
- 10.32
- Type
- journal article
- Language
- en
- Open access
- bronze
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