Reck enables cerebrovascular development by promoting canonical Wnt signaling

Development (Cambridge)

Volumn 143, Issue 1, 2016, Pages 147-159

  Ulrich, Florian ^a   Carretero Ortega, Jorge ^a   Menéndez, Javier ^a   Narvaez, Carlos ^a   Sun, Belinda ^a   Lancaster, Eva ^a   Pershad, Valerie ^a   Trzaska, Sean ^a   Véliz, Evelyn ^a   Kamei, Makoto ^b   Prendergast, Andrew ^c   Kidd, Kameha R ^b   Shaw, Kenna M ^b   Castranova, Daniel A ^b   Pham, Van N ^b   Lo, Brigid D ^b   Martin, Benjamin L ^d   Raible, David W ^c   Weinstein, Brant M ^b   Torres Vázquez, Jesús ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

Angiogenesis; Blood brain barrier; Brain vasculature; Reck; VEGF; Wnt

Indexed keywords

BETA CATENIN; GLUCOSE TRANSPORTER 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; SUPPRESSOR OF TUMORIGENICITY 15; TRANSCRIPTION FACTOR 7 LIKE 1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; WNT PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; RECK PROTEIN, ZEBRAFISH; VASCULOTROPIN A; VEGF PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CANONICAL ANALYSIS; CELL ACTIVITY; CELL DIFFERENTIATION; CELL HYPERPLASIA; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; FISH GENETICS; GENE EXPRESSION; GENETIC SCREENING; HOMOZYGOTE; HUMAN; HUMAN CELL; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; OPEN READING FRAME; PERIPHERAL CIRCULATION; PRIORITY JOURNAL; PROTEIN FUNCTION; THORACIC DUCT; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM; WNT SIGNALING PATHWAY; ZEBRA FISH; ANGIOGENESIS; ANIMAL; BRAIN; BRAIN CIRCULATION; CELL LINE; CYTOLOGY; EMBRYOLOGY; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; TRANSGENIC ANIMAL; VASCULARIZATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE; CEREBROVASCULAR CIRCULATION; ENDOTHELIAL CELLS; GPI-LINKED PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WNT SIGNALING PATHWAY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84953399568     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.123059     Document Type: Article

References (136)

1. Amoyel, M., Cheng, Y.-C., Jiang, Y.-J. and Wilkinson, D. G. (2005). Wnt1 regulates neurogenesis and mediates lateral inhibition of boundary cell specification in the zebrafish hindbrain. Development 132, 775-785.
2. Anderson, M. J., Pham, V. N., Vogel, A. M., Weinstein, B. M. and Roman, B. L. (2008). Loss of unc45a precipitates arteriovenous shunting in the aortic arches. Dev. Biol. 318, 258-267.
3. Arnold, T. D., Niaudet, C., Pang, M.-F., Siegenthaler, J., Gaengel, K., Jung, B., Ferrero, G. M., Mukouyama, Y.-S., Fuxe, J., Akhurst, R. et al. (2014). Excessive vascular sprouting underlies cerebral hemorrhage in mice lacking alphaVbeta8- TGFbeta signaling in the brain. Development 141, 4489-4499.
4. Bai, S., Thummel, R., Godwin, A. R., Nagase, H., Itoh, Y., Li, L., Evans, R., McDermott, J., Seiki, M. and Sarras, M. P.Jr. (2005). Matrix metalloproteinase expression and function during fin regeneration in zebrafish: analysis of MT1- MMP, MMP2 and TIMP2. Matrix Biol. 24, 247-260.
5. Blum, Y., Belting, H.-G., Ellertsdottir, E., Herwig, L., Lüders, F. and Affolter, M. (2008). Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316, 312-322.
6. Bodin, L., Di Pasquale, E., Fabre, S., Bontoux, M., Monget, P., Persani, L. and Mulsant, P. (2007). A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. Endocrinology 148, 393-400.
7. Boute, N., Zilberfarb, V., Camoin, L., Bonnafous, S., Le Marchand-Brustel, Y. and Issad, T. (2004). The formation of an intrachain disulfide bond in the leptin protein is necessary for efficient leptin secretion. Biochimie 86, 351-356.
8. Brogna, S. and Wen, J. (2009). Nonsense-mediated mRNA decay (NMD) mechanisms. Nat. Struct. Mol. Biol. 16, 107-113.
9. Brown, L. A., Rodaway, A. R. F., Schilling, T. F., Jowett, T., Ingham, P. W., Patient, R. K. and Sharrocks, A. D. (2000). Insights into early vasculogenesis revealed by expression of the ETS-domain transcription factor Fli-1 in wild-type and mutant zebrafish embryos. Mech. Dev. 90, 237-252.
10. Bussmann, J., Lawson, N., Zon, L., Schulte-Merker, S. and Zebrafish Nomenclature Committee. (2008). Zebrafish VEGF receptors: a guideline to nomenclature. PLoS Genet. 4, e1000064.
11. Bussmann, J., Bos, F. L., Urasaki, A., Kawakami, K., Duckers, H. J. and Schulte-Merker, S. (2010). Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 137, 2653-2657.
12. Bussmann, J., Wolfe, S. A. and Siekmann, A. F. (2011). Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signaling. Development 138, 1717-1726.
13. Carmany-Rampey, A. and Moens, C. B. (2006). Modern mosaic analysis in the zebrafish. Methods 39, 228-238.
14. Carmeliet, P. (2005). VEGF as a key mediator of angiogenesis in cancer. Oncology 69 Suppl. 3, 4-10.
15. Carson, M. J., Doose, J. M., Melchior, B., Schmid, C. D. and Ploix, C. C. (2006). CNS immune privilege: hiding in plain sight. Immunol. Rev. 213, 48-65.
16. Chandana, E. P. S., Maeda, Y., Ueda, A., Kiyonari, H., Oshima, N., Yamamoto, M., Kondo, S., Oh, J., Takahashi, R., Yoshida, Y. et al. (2010). Involvement of the Reck tumor suppressor protein in maternal and embryonic vascular remodeling in mice. BMC Dev. Biol. 10, 84.
17. Chang, C.-K., Hung, W.-C. and Chang, H.-C. (2008). The Kazal motifs of RECK protein inhibit MMP-9 secretion and activity and reduce metastasis of lung cancer cells in vitro and in vivo. J. Cell. Mol. Med. 12, 2781-2789.
18. Chen, Q., Jiang, L., Li, C., Hu, D., Bu, J.-W., Cai, D. and Du, J.-L. (2012). Haemodynamics-driven developmental pruning of brain vasculature in zebrafish. PLoS Biol. 10, e1001374.
19. Chi, N. C., Shaw, R. M., De Val, S., Kang, G., Jan, L. Y., Black, B. L. and Stainier, D. Y. R. (2008). Foxn4 directly regulates tbx2b expression and atrioventricular canal formation. Genes Dev. 22, 734-739.
20. Choi, J., Dong, L., Ahn, J., Dao, D., Hammerschmidt, M. and Chen, J.-N. (2007). FoxH1 negatively modulates flk1 gene expression and vascular formation in zebrafish. Dev. Biol. 304, 735-744.
21. Choi, H. M. T., Beck, V. A. and Pierce, N. A. (2014). Next-generation in situ hybridization chain reaction: higher gain, lower cost, greater durability. ACS Nano 8, 4284-4294.
22. Claffey, K. P., Senger, D. R. and Spiegelman, B. M. (1995). Structural requirements for dimerization, glycosylation, secretion, and biological function of VPF/VEGF. Biochim. Biophys. Acta 1246, 1-9.
23. Clark, J. C. M., Akiyama, T., Thomas, D. M., Labrinidis, A., Evdokiou, A., Galloway, S. J., Kim, H.-S., Dass, C. R. and Choong, P. F. M. (2011). RECK in osteosarcoma: a novel role in tumour vasculature and inhibition of tumorigenesis in an orthotopic model. Cancer 117, 3517-3528.
24. Corti, P., Young, S., Chen, C.-Y., Patrick, M. J., Rochon, E. R., Pekkan, K. and Roman, B. L. (2011). Interaction between alk1 and blood flow in the development of arteriovenous malformations. Development 138, 1573-1582.
25. Covassin, L. D., Villefranc, J. A., Kacergis, M. C.,Weinstein, B. M. and Lawson, N. D. (2006). Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish. Proc. Natl. Acad. Sci. USA 103, 6554-6559.
26. Covassin, L. D., Siekmann, A. F., Kacergis, M. C., Laver, E., Moore, J. C., Villefranc, J. A., Weinstein, B. M. and Lawson, N. D. (2009). A genetic screen for vascular mutants in zebrafish reveals dynamic roles for Vegf/Plcg1 signaling during artery development. Dev. Biol. 329, 212-226.
27. Daneman, R., Agalliu, D., Zhou, L., Kuhnert, F., Kuo, C. J. and Barres, B. A. (2009). Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proc. Natl. Acad. Sci. USA 106, 641-646.
28. Dejana, E. (2010). The role of wnt signaling in physiological and pathological angiogenesis. Circ. Res. 107, 943-952.
29. Fish, J. E., Santoro, M. M., Morton, S. U., Yu, S., Yeh, R.-F., Wythe, J. D., Ivey, K. N., Bruneau, B. G., Stainier, D. Y. R. and Srivastava, D. (2008). miR-126 regulates angiogenic signaling and vascular integrity. Dev. Cell 15, 272-284.
30. Fujita, M., Cha, Y. R., Pham, V. N., Sakurai, A., Roman, B. L., Gutkind, J. S. and Weinstein, B. M. (2011). Assembly and patterning of the vascular network of the vertebrate hindbrain. Development 138, 1705-1715.
31. Fukuhara, S., Zhang, J., Yuge, S., Ando, K.,Wakayama, Y., Sakaue-Sawano, A., Miyawaki, A. and Mochizuki, N. (2014). Visualizing the cell-cycle progression of endothelial cells in zebrafish. Dev. Biol. 393, 10-23.
32. Goel, H. L. and Mercurio, A. M. (2013). VEGF targets the tumour cell. Nat. Rev. Cancer 13, 871-882.
33. Gridley, T. (2010). Notch signaling in the vasculature. Curr. Top. Dev. Biol. 92, 277-309.
34. Habeck, H., Odenthal, J., Walderich, B., Maischein, H.-M., Schulte-Merker, S. and Tubingen 2000 Screen Consortium. (2002). Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis. Curr. Biol. 12, 1405-1412.
35. Hagan, N. and Ben-Zvi, A. (2014). The molecular, cellular, and morphological components of blood-brain barrier development during embryogenesis. Semin. Cell Dev. Biol.
36. Halliday, D., Hutchinson, S., Kettle, S., Firth, H.,Wordsworth, P. and Handford, P. A. (1999). Molecular analysis of eight mutations in FBN1. Hum. Genet. 105, 587-597.
37. Hallmann, R., Mayer, D. N., Berg, E. L., Broermann, R. and Butcher, E. C. (1995). Novel mouse endothelial cell surface marker is suppressed during differentiation of the blood brain barrier. Dev. Dyn. 202, 325-332.
38. Hawkins, B. T. and Davis, T. P. (2005). The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 57, 173-185.
39. Helisch, A. and Schaper, W. (2003). Arteriogenesis: the development and growth of collateral arteries. Microcirculation 10, 83-97.
40. Hogan, B. M., Bos, F. L., Bussmann, J., Witte, M., Chi, N. C., Duckers, H. J. and Schulte-Merker, S. (2009). Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 41, 396-398.
41. Hong, K.-J., Hsu, M.-C., Hou, M.-F. and Hung,W.-C. (2011). The tumor suppressor RECK interferes with HER-2/Neu dimerization and attenuates its oncogenic signaling. FEBS Lett. 585, 591-595.
42. Hong, K.-J., Wu, D.-C., Cheng, K.-H., Chen, L.-T. and Hung, W.-C. (2014). RECK inhibits stemness gene expression and tumorigenicity of gastric cancer cells by suppressing ADAM-mediated Notch1 activation. J. Cell. Physiol. 229, 191-201.
43. Hu, J., Dong, A., Fernandez-Ruiz, V., Shan, J., Kawa, M., Martinez-Anso, E., Prieto, J. and Qian, C. (2009). Blockade of Wnt signaling inhibits angiogenesis and tumor growth in hepatocellular carcinoma. Cancer Res. 69, 6951-6959.
44. Imhof, I., Gasper, W. J. and Derynck, R. (2008). Association of tetraspanin CD9 with transmembrane TGF{alpha} confers alterations in cell-surface presentation of TGF{alpha} and cytoskeletal organization. J. Cell Sci. 121, 2265-2274.
45. Isogai, S., Horiguchi, M. andWeinstein, B. M. (2001). The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 230, 278-301.
46. Janssens, E., Gaublomme, D., De Groef, L., Darras, V. M., Arckens, L., Delorme, N., Claes, F., Van Hove, I. and Moons, L. (2013). Matrix metalloproteinase 14 in the zebrafish: an eye on retinal and retinotectal development. PLoS ONE 8, e52915.
47. Kagermeier-Schenk, B., Wehner, D., Ozhan-Kizil, G., Yamamoto, H., Li, J., Kirchner, K., Hoffmann, C., Stern, P., Kikuchi, A., Schambony, A. et al. (2011). Waif1/5T4 inhibits Wnt/beta-catenin signaling and activates noncanonical Wnt pathways by modifying LRP6 subcellular localization. Dev. Cell 21, 1129-1143.
48. Kaufmann, A., Mickoleit, M., Weber, M. and Huisken, J. (2012). Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope. Development 139, 3242-3247.
49. Klaus, A. and Birchmeier,W. (2008). Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 8, 387-398.
50. Klein, P. S. and Melton, D. A. (1996). A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA 93, 8455-8459.
51. Koch, S., Tugues, S., Li, X., Gualandi, L. and Claesson-Welsh, L. (2011). Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 437, 169-183.
52. Kochhan, E., Lenard, A., Ellertsdottir, E., Herwig, L., Affolter, M., Belting, H.-G. and Siekmann, A. F. (2013). Blood flow changes coincide with cellular rearrangements during blood vessel pruning in zebrafish embryos. PLoS ONE 8, e75060.
53. Kok, F. O., Shin, M., Ni, C.-W., Gupta, A., Grosse, A. S., van Impel, A., Kirchmaier, B. C., Peterson-Maduro, J., Kourkoulis, G., Male, I. et al. (2015). Reverse genetic screening reveals poor correlation between Morpholino-induced and mutant phenotypes in zebrafish. Dev. Cell 32, 97-108.
54. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C.-B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
55. Lanahan, A., Zhang, X., Fantin, A., Zhuang, Z., Rivera-Molina, F., Speichinger, K., Prahst, C., Zhang, J., Wang, Y., Davis, G. et al. (2013). The neuropilin 1 cytoplasmic domain is required for VEGF-A-dependent arteriogenesis. Dev. Cell 25, 156-168.
56. Larrivee, B., Prahst, C., Gordon, E., del Toro, R., Mathivet, T., Duarte, A., Simons, M. and Eichmann, A. (2012). ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev. Cell 22, 489-500.
57. Larson, J. D.,Wadman, S. A., Chen, E., Kerley, L., Clark, K. J., Eide, M., Lippert, S., Nasevicius, A., Ekker, S. C., Hackett, P. B. et al. (2004). Expression of VEcadherin in zebrafish embryos: a new tool to evaluate vascular development. Dev. Dyn. 231, 204-213.
58. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
59. Lawson, N. D., Vogel, A. M. and Weinstein, B. M. (2002). sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell 3, 127-136.
60. Lawson, N. D., Mugford, J. W., Diamond, B. A. and Weinstein, B. M. (2003). phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 17, 1346-1351.
61. Liang, D., Chang, J. R., Chin, A. J., Smith, A., Kelly, C.,Weinberg, E. S. and Ge, R. (2001). The role of vascular endothelial growth factor (VEGF) in vasculogenesis, angiogenesis, and hematopoiesis in zebrafish development. Mech. Dev. 108, 29-43.
62. Liebner, S., Corada, M., Bangsow, T., Babbage, J., Taddei, A., Czupalla, C. J., Reis, M., Felici, A., Wolburg, H., Fruttiger, M. et al. (2008). Wnt/beta-catenin signaling controls development of the blood-brain barrier. J. Cell Biol. 183, 409-417.
63. Lyons, M. S., Bell, B., Stainier, D. and Peters, K. G. (1998). Isolation of the zebrafish homologues for the tie-1 and tie-2 endothelium-specific receptor tyrosine kinases. Dev. Dyn. 212, 133-140.
64. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
65. Mackenzie, F. and Ruhrberg, C. (2012). Diverse roles for VEGF-A in the nervous system. Development 139, 1371-1380.
66. Mantuano, E., Inoue, G., Li, X., Takahashi, K., Gaultier, A., Gonias, S. L. and Campana, W. M. (2008). The hemopexin domain of matrix metalloproteinase-9 activates cell signaling and promotes migration of schwann cells by binding to lowdensity lipoprotein receptor-related protein. J. Neurosci. 28, 11571-11582.
67. Martin, B. L. and Kimelman, D. (2012). Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Dev. Cell 22, 223-232.
68. Masckauchan, T. N. H. and Kitajewski, J. (2006). Wnt/Frizzled signaling in the vasculature: new angiogenic factors in sight. Physiology 21, 181-188.
69. Mason, A. J. (1994). Functional analysis of the cysteine residues of activin A. Mol. Endocrinol. 8, 325-332.
70. McGraw, H. F., Nechiporuk, A. and Raible, D. W. (2008). Zebrafish dorsal root ganglia neural precursor cells adopt a glial fate in the absence of neurogenin1. J. Neurosci. 28, 12558-12569.
71. Meng, X., Noyes, M. B., Zhu, L. J., Lawson, N. D. and Wolfe, S. A. (2008). Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat. Biotechnol. 26, 695-701.
72. Mergenthaler, P., Lindauer, U., Dienel, G. A. and Meisel, A. (2013). Sugar for the brain: the role of glucose in physiological and pathological brain function. Trends Neurosci. 36, 587-597.
73. Miki, T., Shamma, A., Kitajima, S., Takegami, Y., Noda, M., Nakashima, Y., Watanabe, K. I. and Takahashi, C. (2010). The β1-integrin-dependent function of RECK in physiologic and tumor angiogenesis. Mol. Cancer Res. 8, 665-676.
74. Mori, H., Lo, A. T., Inman, J. L., Alcaraz, J., Ghajar, C. M., Mott, J. D., Nelson, C. M., Chen, C. S., Zhang, H., Bascom, J. L. et al. (2013). Transmembrane/ cytoplasmic, rather than catalytic, domains of Mmp14 signal to MAPK activation and mammary branching morphogenesis via binding to integrin beta1. Development 140, 343-352.
75. Moro, E., Vettori, A., Porazzi, P., Schiavone, M., Rampazzo, E., Casari, A., Ek, O., Facchinello, N., Astone, M., Zancan, I. et al. (2013). Generation and application of signaling pathway reporter lines in zebrafish. Mol. Genet. Genom. 288, 231-242.
76. Muraguchi, T., Takegami, Y., Ohtsuka, T., Kitajima, S., Chandana, E. P. S., Omura, A., Miki, T., Takahashi, R., Matsumoto, N., Ludwig, A. et al. (2007). RECK modulates Notch signaling during cortical neurogenesis by regulating ADAM10 activity. Nat. Neurosci. 10, 838-845.
77. Nagini, S. (2012). RECKing MMP: relevance of reversion-inducing cysteine-rich protein with kazal motifs as a prognostic marker and therapeutic target for cancer (a review). Anti-cancer Agents Med. Chem. 12, 718-725.
78. Nicoli, S., Standley, C., Walker, P., Hurlstone, A., Fogarty, K. E. and Lawson, N. D. (2010). MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature 464, 1196-1200.
79. Noda, M. and Takahashi, C. (2007). Recklessness as a hallmark of aggressive cancer. Cancer Sci. 98, 1659-1665.
80. Obermeier, B., Daneman, R. and Ransohoff, R. M. (2013). Development, maintenance and disruption of the blood-brain barrier. Nat. Med. 19, 1584-1596.
81. Oh, J., Takahashi, R., Kondo, S., Mizoguchi, A., Adachi, E., Sasahara, R. M., Nishimura, S., Imamura, Y., Kitayama, H., Alexander, D. B. et al. (2001). The membrane-anchoredMMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107, 789-800.
82. Olszewska-Pazdrak, B., Hein, T. W., Olszewska, P. and Carney, D. H. (2009). Chronic hypoxia attenuates VEGF signaling and angiogenic responses by downregulation of KDR in human endothelial cells. Am. J. Physiol. Cell Physiol. 296, C1162-C1170.
83. Omura, A., Matsuzaki, T., Mio, K., Ogura, T., Yamamoto, M., Fujita, A., Okawa, K., Kitayama, H., Takahashi, C., Sato, C. et al. (2009). RECK forms cowbellshaped dimers and inhibits matrix metalloproteinase-catalyzed cleavage of fibronectin. J. Biol. Chem. 284, 3461-3469.
84. Ousman, S. S. and Kubes, P. (2012). Immune surveillance in the central nervous system. Nat. Neurosci. 15, 1096-1101.
85. Page-McCaw, A., Ewald, A. J. andWerb, Z. (2007). Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233.
86. Park, S., Lee, C., Sabharwal, P., Zhang, M., Meyers, C. L. F. and Sockanathan, S. (2013). GDE2 promotes neurogenesis by glycosylphosphatidylinositol-anchor cleavage of RECK. Science 339, 324-328.
87. Posokhova, E., Shukla, A., Seaman, S., Volate, S., Hilton, M. B., Wu, B., Morris, H., Swing, D. A., Zhou, M., Zudaire, E. et al. (2015). GPR124 functions as a WNT7-specific coactivator of canonical beta-catenin signaling. Cell Rep. 10, 123-130.
88. Prendergast, A., Linbo, T. H., Swarts, T., Ungos, J. M., McGraw, H. F., Krispin, S., Weinstein, B. M. and Raible, D. W. (2012). The metalloproteinase inhibitor Reck is essential for zebrafish DRG development. Development 139, 1141-1152.
89. Prieve, M. G. and Waterman, M. L. (1999). Nuclear localization and formation of beta-catenin-lymphoid enhancer factor 1 complexes are not sufficient for activation of gene expression. Mol. Cell. Biol. 19, 4503-4515.
90. Qian, F., Zhen, F., Ong, C., Jin, S.-W., Meng Soo, H., Stainier, D. Y. R., Lin, S., Peng, J. and Wen, Z. (2005). Microarray analysis of zebrafish cloche mutant using amplified cDNA and identification of potential downstream target genes. Dev. Dyn. 233, 1163-1172.
91. Rahmah, N. N., Sakai, K., Sano, K. and Hongo, K. (2012). Expression of RECK in endothelial cells of glioma: comparison with CD34 and VEGF expressions. J. Neuro-Oncol. 107, 559-564.
92. Reis, M. and Liebner, S. (2013). Wnt signaling in the vasculature. Exp. Cell Res. 319, 1317-1323.
93. Rims, C. R. and McGuire, J. K. (2014). Matrilysin (MMP-7) catalytic activity regulates beta-catenin localization and signaling activation in lung epithelial cells. Exp. Lung Res. 40, 126-136.
94. Ring, D. B., Johnson, K.W., Henriksen, E. J., Nuss, J. M., Goff, D., Kinnick, T. R., Ma, S. T., Reeder, J.W., Samuels, I., Slabiak, T. et al. (2003). Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52, 588-595.
95. Rolfe, D. F. and Brown, G. C. (1997). Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731-758.
96. Ruhrberg, C. and Bautch, V. L. (2013). Neurovascular development and links to disease. Cell. Mol. Life Sci. 70, 1675-1684.
97. Sakao, S. and Tatsumi, K. (2011). The effects of antiangiogenic compound SU5416 in a rat model of pulmonary arterial hypertension. Respiration 81, 253-261.
98. Schrijver, I., Liu, W., Brenn, T., Furthmayr, H. and Francke, U. (1999). Cysteine substitutions in epidermal growth factor-like domains of fibrillin-1: distinct effects on biochemical and clinical phenotypes. Am. J. Hum. Genet. 65, 1007-1020.
99. Schulte-Merker, S. and Stainier, D. Y. R. (2014). Out with the old, in with the new: reassessing morpholino knockdowns in light of genome editing technology. Development 141, 3103-3104.
100. Seals, D. F. and Courtneidge, S. A. (2003). The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17, 7-30.
101. Sehnert, A. J., Huq, A., Weinstein, B. M., Walker, C., Fishman, M. and Stainier, D. Y. R. (2002). Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 31, 106-110.
102. Shaw, K. M., Castranova, D. A., Pham, V. N., Kamei, M., Kidd, K. R., Lo, B. D., Torres-Vasquez, J., Ruby, A. and Weinstein, B. M. (2006). fused-somites-like mutants exhibit defects in trunk vessel patterning. Dev. Dyn. 235, 1753-1760.
103. Siegenthaler, J. A., Sohet, F. and Daneman, R. (2013). 'Sealing off the CNS': cellular and molecular regulation of blood-brain barriergenesis. Curr. Opin. Neurobiol. 23, 1057-1064.
104. Silveira Correa, T. C., Massaro, R. R., Brohem, C. A., Taboga, S. R., Lamers, M. L., Santos, M. F. and Maria-Engler, S. S. (2010). RECK-mediated inhibition of glioma migration and invasion. J. Cell. Biochem. 110, 52-61.
105. Simizu, S., Takagi, S., Tamura, Y. and Osada, H. (2005). RECK-mediated suppression of tumor cell invasion is regulated by glycosylation in human tumor cell lines. Cancer Res. 65, 7455-7461.
106. Sivaraj, K. K., Takefuji, M., Schmidt, I., Adams, R. H., Offermanns, S. and Wettschureck, N. (2013). G13 controls angiogenesis through regulation of VEGFR-2 expression. Dev. Cell 25, 427-434.
107. Snow, C. J., Peterson, M. T., Khalil, A. and Henry, C. A. (2008). Muscle development is disrupted in zebrafish embryos deficient for fibronectin. Dev. Dyn. 237, 2542-2553.
108. Sohet, F. and Daneman, R. (2013). Genetic mouse models to study blood-brain barrier development and function. Fluids Barriers CNS 10, 3.
109. Srivastava, A., Pastor-Pareja, J. C., Igaki, T., Pagliarini, R. and Xu, T. (2007). Basement membrane remodeling is essential for Drosophila disc eversion and tumor invasion. Proc. Natl. Acad. Sci. USA 104, 2721-2726.
110. Stainier, D. Y. R., Kontarakis, Z. and Rossi, A. (2015). Making sense of anti-sense data. Dev. Cell 32, 7-8.
111. Stamos, J. L. and Weis, W. I. (2013). The beta-catenin destruction complex. Cold Spring Harb. Perspect. Biol. 5, a007898.
112. Stenman, J. M., Rajagopal, J., Carroll, T. J., Ishibashi, M., McMahon, J. and McMahon, A. P. (2008). Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science 322, 1247-1250.
113. Taelman, V. F., Dobrowolski, R., Plouhinec, J.-L., Fuentealba, L. C., Vorwald, P. P., Gumper, I., Sabatini, D. D. and De Robertis, E. M. (2010). Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143, 1136-1148.
114. Takahashi, C., Sheng, Z., Horan, T. P., Kitayama, H., Maki, M., Hitomi, K., Kitaura, Y., Takai, S., Sasahara, R. M., Horimoto, A. et al. (1998). Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membraneanchored glycoprotein RECK. Proc. Natl. Acad. Sci. USA 95, 13221-13226.
115. Tam, S. J., Richmond, D. L., Kaminker, J. S., Modrusan, Z., Martin-McNulty, B., Cao, T. C., Weimer, R. M., Carano, R. A. D., van Bruggen, N. and Watts, R. J. (2012). Death receptors DR6 and TROY regulate brain vascular development. Dev. Cell 22, 403-417.
116. Traver, D., Paw, B. H., Poss, K. D., Penberthy,W. T., Lin, S. and Zon, L. I. (2003). Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat. Immunol. 4, 1238-1246.
117. Ulrich, F., Ma, L.-H., Baker, R. G. and Torres-Vazquez, J. (2011). Neurovascular development in the embryonic zebrafish hindbrain. Dev. Biol. 357, 134-151.
118. Umans, R. A. and Taylor, M. R. (2012). Zebrafish as a model to study drug transporters at the blood-brain barrier. Clin. Pharmacol. Ther. 92, 567-570.
119. Vallon, M., Chang, J., Zhang, H. and Kuo, C. J. (2014). Developmental and pathological angiogenesis in the central nervous system. Cell. Mol. Life Sci. 71, 3489-3506.
120. Vanhollebeke, B., Stone, O. A., Bostaille, N., Cho, C., Zhou, Y., Maquet, E., Gauquier, A., Cabochette, P., Fukuhara, S., Mochizuki, N. et al. (2015). Tip cell-specific requirement for an atypical Gpr124- and Reck-dependent Wnt/betacatenin pathway during brain angiogenesis. Elife 4, e06489.
121. Veldman, M. B., Zhao, C., Gomez, G. A., Lindgren, A. G., Huang, H., Yang, H., Yao, S., Martin, B. L., Kimelman, D. and Lin, S. (2013). Transdifferentiation of fast skeletal muscle into functional endothelium in vivo by transcription factor Etv2. PLoS Biol. 11, e1001590.
122. Venkiteswaran, G., Lewellis, S. W., Wang, J., Reynolds, E., Nicholson, C. and Knaut, H. (2013). Generation and dynamics of an endogenous, self-generated signaling gradient across a migrating tissue. Cell 155, 674-687.
123. Villefranc, J. A., Amigo, J. and Lawson, N. D. (2007). Gateway compatible vectors for analysis of gene function in the zebrafish. Dev. Dyn. 236, 3077-3087.
124. Wada, H., Ghysen, A., Asakawa, K., Abe, G., Ishitani, T. and Kawakami, K. (2013). Wnt/Dkk negative feedback regulates sensory organ size in zebrafish. Curr. Biol. 23, 1559-1565.
125. Wang, Y. and Nakayama, N. (2009). WNT and BMP signaling are both required for hematopoietic cell development from human ES cells. Stem Cell Res. 3, 113-125.
126. Wang, Y., Cho, S.-G., Wu, X., Siwko, S. and Liu, M. (2014). G-protein coupled receptor 124 (GPR124) in endothelial cells regulates vascular endothelial growth factor (VEGF)-induced tumor angiogenesis. Curr. Mol. Med. 14, 543-554.
127. Watson, O., Novodvorsky, P., Gray, C., Rothman, A. M. K., Lawrie, A., Crossman, D. C., Haase, A., McMahon, K., Gering, M., Van Eeden, F. J. M. et al. (2013). Blood flow suppresses vascular Notch signalling via dll4 and is required for angiogenesis in response to hypoxic signalling. Cardiovasc. Res. 100, 252-261.
128. Wittko-Schneider, I. M., Schneider, F. T. and Plate, K. H. (2013). Brain homeostasis: VEGF receptor 1 and 2-two unequal brothers in mind. Cell. Mol. Life Sci. 70, 1705-1725.
129. Wu, S.-Y., Shin, J., Sepich, D. S. and Solnica-Krezel, L. (2012). Chemokine GPCR signaling inhibits beta-catenin during zebrafish axis formation. PLoS Biol. 10, e1001403.
130. Wythe, J. D., Dang, L. T. H., Devine, W. P., Boudreau, E., Artap, S. T., He, D., Schachterle, W., Stainier, D. Y. R., Oettgen, P., Black, B. L. et al. (2013). ETS factors regulate VEGF-dependent arterial specification. Dev. Cell 26, 45-58.
131. Yamamoto, M., Matsuzaki, T., Takahashi, R., Adachi, E., Maeda, Y., Yamaguchi, S., Kitayama, H., Echizenya, M., Morioka, Y., Alexander, D. B. et al. (2012). The transformation suppressor gene Reck is required for postaxial patterning in mouse forelimbs. Biol. Open 1, 458-466.
132. Yost, C., Torres, M., Miller, J. R., Huang, E., Kimelman, D. and Moon, R. T. (1996). The axis-inducing activity, stability, and subcellular distribution of betacatenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10, 1443-1454.
133. Zachary, I. (2003). VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem. Soc. Trans. 31, 1171-1177.
134. Zhou, Y. and Nathans, J. (2014). Gpr124 controls CNS angiogenesis and bloodbrain barrier integrity by promoting ligand-specific canonical wnt signaling. Dev. Cell 31, 248-256.
135. Zhou, Y., Wang, Y., Tischfield, M., Williams, J., Smallwood, P. M., Rattner, A., Taketo, M. M. and Nathans, J. (2014). Canonical WNT signaling components in vascular development and barrier formation. J. Clin. Invest. 124, 3825-3846.
136. Zygmunt, T., Gay, C. M., Blondelle, J., Singh, M. K., Flaherty, K. M., Means, P. C., Herwig, L., Krudewig, A., Belting, H.-G., Affolter, M. et al. (2011). Semaphorin- PlexinD1 signaling limits angiogenic potential via the VEGF decoy receptor sFlt1. Dev. Cell 21, 301-314.