Wiring the Vascular Network with Neural Cues: A CNS Perspective

Neuron

Volumn 87, Issue 2, 2015, Pages 271-296

  Wälchli, Thomas ^a,b,c   Wacker, Andrin ^a   Frei, Karl ^b   Regli, Luca ^b   Schwab, Martin E ^c   Hoerstrup, Simon P ^b   Gerhardt, Holger ^d,e,f   Engelhardt, Britta ^g  

^a Neuroscience Center Zurich and Division of Neurosurgery   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^f MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^g UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH RECEPTOR; DEATH RECEPTOR 6; DELTA LIKE LIGAND 4; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 124; JAGGED1; MEMBRANE PROTEIN; NETRIN; NOTCH RECEPTOR; PLEXIN; PROTEIN NGBR; PROTEIN NOGO; RECEPTOR PROTEIN; SEMAPHORIN; TUMOR NECROSIS FACTOR RECEPTOR SUPERFAMILY MEMBER 19; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; WNT PROTEIN; VASCULOTROPIN A;

ANGIOGENESIS; BINDING AFFINITY; BLOOD BRAIN BARRIER; CELL INTERACTION; CENTRAL NERVOUS SYSTEM; HUMAN; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; ASSOCIATION; METABOLISM; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; CENTRAL NERVOUS SYSTEM; CUES; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84937427835     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.06.038     Document Type: Review

References (169)

1. Abbott N.J., Rönnbäck L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53.
2. Acevedo L., Yu J., Erdjument-Bromage H., Miao R.Q., Kim J.E., Fulton D., Tempst P., Strittmatter S.M., Sessa W.C. A new role for Nogo as a regulator of vascular remodeling. Nat. Med. 2004, 10:382-388.
3. Acevedo L.M., Barillas S., Weis S.M., Göthert J.R., Cheresh D.A. Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 2008, 111:2674-2680.
4. Adams R.H., Wilkinson G.A., Weiss C., Diella F., Gale N.W., Deutsch U., Risau W., Klein R. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 1999, 13:295-306.
5. Alvarez J.I., Dodelet-Devillers A., Kebir H., Ifergan I., Fabre P.J., Terouz S., Sabbagh M., Wosik K., Bourbonnière L., Bernard M., et al. The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science 2011, 334:1727-1731.
6. Anderson K.D., Pan L., Yang X.M., Hughes V.C., Walls J.R., Dominguez M.G., Simmons M.V., Burfeind P., Xue Y., Wei Y., et al. Angiogenic sprouting into neural tissue requires Gpr124, an orphan G protein-coupled receptor. Proc. Natl. Acad. Sci. USA 2011, 108:2807-2812.
7. Bareyre F.M., Haudenschild B., Schwab M.E. Long-lasting sprouting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord. J.Neurosci. 2002, 22:7097-7110.
8. Barros C.S., Franco S.J., Müller U. Extracellular matrix: functions in the nervous system. Cold Spring Harb. Perspect. Biol. 2011, 3:a005108.
9. Bates D., Taylor G.I., Minichiello J., Farlie P., Cichowitz A., Watson N., Klagsbrun M., Mamluk R., Newgreen D.F. Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1. Dev. Biol. 2003, 255:77-98.
10. Bautch V.L. VEGF-directed blood vessel patterning: from cells to organism. Cold Spring Harb. Perspect. Med. 2012, 2:a006452.
11. Bautch V.L., James J.M. Neurovascular development: The beginning of a beautiful friendship. Cell Adhes. Migr. 2009, 3:199-204.
12. Bedell V.M., Yeo S.Y., Park K.W., Chung J., Seth P., Shivalingappa V., Zhao J., Obara T., Sukhatme V.P., Drummond I.A., et al. roundabout4 is essential for angiogenesis invivo. Proc. Natl. Acad. Sci. USA 2005, 102:6373-6378.
13. Blanco R., Gerhardt H. VEGF and Notch in tip and stalk cell selection. Cold Spring Harb. Perspect. Med. 2013, 3:a006569.
14. Bouvrée K., Larrivée B., Lv X., Yuan L., DeLafarge B., Freitas C., Mathivet T., Bréant C., Tessier-Lavigne M., Bikfalvi A., et al. Netrin-1 inhibits sprouting angiogenesis in developing avian embryos. Dev. Biol. 2008, 318:172-183.
15. Bussmann J., Wolfe S.A., Siekmann A.F. Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signaling. Development 2011, 138:1717-1726.
16. Butler J.M., Kobayashi H., Rafii S. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat. Rev. Cancer 2010, 10:138-146.
17. Capparuccia L., Tamagnone L. Semaphorin signaling in cancer cells and in cells of the tumor microenvironment-two sides of a coin. J.Cell Sci. 2009, 122:1723-1736.
18. Carmeliet P., Jain R.K. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011, 473:298-307.
19. Carmeliet P., Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature 2005, 436:193-200.
20. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., Fahrig M., Vandenhoeck A., Harpal K., Eberhardt C., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439.
21. Castets M., Mehlen P. Netrin-1 role in angiogenesis: to be or not to be a pro-angiogenic factor?. Cell Cycle 2010, 9:1466-1471.
22. Cerani A., Tetreault N., Menard C., Lapalme E., Patel C., Sitaras N., Beaudoin F., Leboeuf D., De Guire V., Binet F., et al. Neuron-derived semaphorin 3A is an early inducer of vascular permeability in diabetic retinopathy via neuropilin-1. Cell Metab. 2013, 18:505-518.
23. Charron F., Tessier-Lavigne M. The Hedgehog, TGF-beta/BMP and Wnt families of morphogens in axon guidance. Adv. Exp. Med. Biol. 2007, 621:116-133.
24. Chen G., Sima J., Jin M., Wang K.Y., Xue X.J., Zheng W., Ding Y.Q., Yuan X.B. Semaphorin-3A guides radial migration of cortical neurons during development. Nat. Neurosci. 2008, 11:36-44.
25. Cheng L., Huang Z., Zhou W., Wu Q., Donnola S., Liu J.K., Fang X., Sloan A.E., Mao Y., Lathia J.D., et al. Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 2013, 153:139-152.
26. Coma S., Shimizu A., Klagsbrun M. Hypoxia induces tumor and endothelial cell migration in a semaphorin 3F- and VEGF-dependent manner via transcriptional repression of their common receptor neuropilin 2. Cell Adhes. Migr. 2011, 5:266-275.
27. Corada M., Nyqvist D., Orsenigo F., Caprini A., Giampietro C., Taketo M.M., Iruela-Arispe M.L., Adams R.H., Dejana E. The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling. Dev. Cell 2010, 18:938-949.
28. Cullen M., Elzarrad M.K., Seaman S., Zudaire E., Stevens J., Yang M.Y., Li X., Chaudhary A., Xu L., Hilton M.B., et al. GPR124, an orphan G protein-coupled receptor, is required for CNS-specific vascularization and establishment of the blood-brain barrier. Proc. Natl. Acad. Sci. USA 2011, 108:5759-5764.
29. Daneman R., Agalliu D., Zhou L., Kuhnert F., Kuo C.J., Barres B.A. Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proc. Natl. Acad. Sci. USA 2009, 106:641-646.
30. Daneman R., Zhou L., Kebede A.A., Barres B.A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010, 468:562-566.
31. De Bock K., Mazzone M., Carmeliet P. Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not?. Nat. Rev. Clin. Oncol. 2011, 8:393-404.
32. de Castro F., López-Mascaraque L., De Carlos J.A. Cajal: lessons on brain development. Brain Res. Brain Res. Rev. 2007, 55:481-489.
33. De Smet F., Segura I., De Bock K., Hohensinner P.J., Carmeliet P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler. Thromb. Vasc. Biol. 2009, 29:639-649.
34. deCharms R.C. Applications of real-time fMRI. Nat. Rev. Neurosci. 2008, 9:720-729.
35. Dickson B.J. Molecular mechanisms of axon guidance. Science 2002, 298:1959-1964.
36. Eby M.T., Jasmin A., Kumar A., Sharma K., Chaudhary P.M. TAJ, a novel member of the tumor necrosis factor receptor family, activates the c-Jun N-terminal kinase pathway and mediates caspase-independent cell death. J.Biol. Chem. 2000, 275:15336-15342.
37. Eichmann A., Thomas J.L. Molecular parallels between neural and vascular development. Cold Spring Harb. Perspec.t Med. 2013, 3:a006551.
38. Ellertsdóttir E., Lenard A., Blum Y., Krudewig A., Herwig L., Affolter M., Belting H.G. Vascular morphogenesis in the zebrafish embryo. Dev. Biol. 2010, 341:56-65.
39. Engelhardt B. Development of the blood-brain barrier. Cell Tissue Res. 2003, 314:119-129.
40. Estrach S., Cailleteau L., Franco C.A., Gerhardt H., Stefani C., Lemichez E., Gagnoux-Palacios L., Meneguzzi G., Mettouchi A. Laminin-binding integrins induce Dll4 expression and Notch signaling in endothelial cells. Circ. Res. 2011, 109:172-182.
41. Fantin A., Vieira J.M., Plein A., Denti L., Fruttiger M., Pollard J.W., Ruhrberg C. NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis. Blood 2013, 121:2352-2362.
42. Fantin A., Vieira J.M., Plein A., Maden C.H., Ruhrberg C. The embryonic mouse hindbrain as a qualitative and quantitative model for studying the molecular and cellular mechanisms of angiogenesis. Nat. Protoc. 2013, 8:418-429.
43. Ferent J., Traiffort E. Hedgehog: multiple paths for multiple roles in shaping the brain and spinal cord. Neuroscientist 2014, Published online May 8, 2014. 10.1177/1073858414531457.
44. Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K.S., Powell-Braxton L., Hillan K.J., Moore M.W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996, 380:439-442.
45. Fiore R., Rahim B., Christoffels V.M., Moorman A.F., Püschel A.W. Inactivation of the Sema5a gene results in embryonic lethality and defective remodeling of the cranial vascular system. Mol. Cell. Biol. 2005, 25:2310-2319.
46. Fischer R.S., Gardel M., Ma X., Adelstein R.S., Waterman C.M. Local cortical tension by myosin II guides 3D endothelial cell branching. Curr. Biol. 2009, 19:260-265.
47. 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.
48. Fukushima Y., Okada M., Kataoka H., Hirashima M., Yoshida Y., Mann F., Gomi F., Nishida K., Nishikawa S., Uemura A. Sema3E-PlexinD1 signaling selectively suppresses disoriented angiogenesis in ischemic retinopathy in mice. J.Clin. Invest. 2011, 121:1974-1985.
49. 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.
50. Gerhardt H., Ruhrberg C., Abramsson A., Fujisawa H., Shima D., Betsholtz C. Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev. Dyn. 2004, 231:503-509.
51. Germain S., Monnot C., Muller L., Eichmann A. Hypoxia-driven angiogenesis: role of tip cells and extracellular matrix scaffolding. Curr. Opin. Hematol. 2010, 17:245-251.
52. Geudens I., Gerhardt H. Coordinating cell behaviour during blood vessel formation. Development 2011, 138:4569-4583.
53. Ghajar C.M., Peinado H., Mori H., Matei I.R., Evason K.J., Brazier H., Almeida D., Koller A., Hajjar K.A., Stainier D.Y., et al. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 2013, 15:807-817.
54. Gu C., Yoshida Y., Livet J., Reimert D.V., Mann F., Merte J., Henderson C.E., Jessell T.M., Kolodkin A.L., Ginty D.D. Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 2005, 307:265-268.
55. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
56. Harb R., Whiteus C., Freitas C., Grutzendler J. Invivo imaging of cerebral microvascular plasticity from birth to death. J.Cereb. Blood Flow Metab. 2013, 33:146-156.
57. Herbert S.P., Stainier D.Y. Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat. Rev. Mol. Cell Biol. 2011, 12:551-564.
58. Hjelmeland A.B., Lathia J.D., Sathornsumetee S., Rich J.N. Twisted tango: brain tumor neurovascular interactions. Nat. Neurosci. 2011, 14:1375-1381.
59. Hoang S., Liauw J., Choi M., Choi M., Guzman R.G., Steinberg G.K. Netrin-4 enhances angiogenesis and neurologic outcome after cerebral ischemia. J.Cereb. Blood Flow Metab. 2009, 29:385-397.
60. Hogan K.A., Ambler C.A., Chapman D.L., Bautch V.L. The neural tube patterns vessels developmentally using the VEGF signaling pathway. Development 2004, 131:1503-1513.
61. Honma Y., Araki T., Gianino S., Bruce A., Heuckeroth R., Johnson E., Milbrandt J. Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 2002, 35:267-282.
62. Jain R.K., Carmeliet P. SnapShot: Tumor angiogenesis. Cell 2012, 149:1408-1408.e1.
63. 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.
64. James J.M., Gewolb C., Bautch V.L. Neurovascular development uses VEGF-A signaling to regulate blood vessel ingression into the neural tube. Development 2009, 136:833-841.
65. Jeansson M., Gawlik A., Anderson G., Li C., Kerjaschki D., Henkelman M., Quaggin S.E. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J.Clin. Invest. 2011, 121:2278-2289.
66. Jeong J.Y., Kwon H.B., Ahn J.C., Kang D., Kwon S.H., Park J.A., Kim K.W. Functional and developmental analysis of the blood-brain barrier in zebrafish. Brain Res. Bull. 2008, 75:619-628.
67. Jones C.A., London N.R., Chen H., Park K.W., Sauvaget D., Stockton R.A., Wythe J.D., Suh W., Larrieu-Lahargue F., Mukouyama Y.S., et al. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 2008, 14:448-453.
68. Jones C.A., Nishiya N., London N.R., Zhu W., Sorensen L.K., Chan A.C., Lim C.J., Chen H., Zhang Q., Schultz P.G., et al. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 2009, 11:1325-1331.
69. Joset P., Wacker A., Babey R., Ingold E.A., Andermatt I., Stoeckli E.T., Gesemann M. Rostral growth of commissural axons requires the cell adhesion molecule MDGA2. Neural Dev. 2011, 6:22.
70. Kempf A., Montani L., Petrinovic M.M., Schroeter A., Weinmann O., Patrignani A., Schwab M.E. Upregulation of axon guidance molecules in the adult central nervous system of Nogo-A knockout mice restricts neuronal growth and regeneration. Eur. J. Neurosci. 2013, 38:3567-3579.
71. Kempf A., Tews B., Arzt M.E., Weinmann O., Obermair F.J., Pernet V., Zagrebelsky M., Delekate A., Iobbi C., Zemmar A., et al. The sphingolipid receptor S1PR2 is a receptor for Nogo-a repressing synaptic plasticity. PLoS Biol. 2014, 12:e1001763.
72. Kim J., Oh W.J., Gaiano N., Yoshida Y., Gu C. Semaphorin 3E-Plexin-D1 signaling regulates VEGF function in developmental angiogenesis via a feedback mechanism. Genes Dev. 2011, 25:1399-1411.
73. Koch A.W., Mathivet T., Larrivée B., Tong R.K., Kowalski J., Pibouin-Fragner L., Bouvrée K., Stawicki S., Nicholes K., Rathore N., et al. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev. Cell 2011, 20:33-46.
74. Kritz A.B., Yu J., Wright P.L., Wan S., George S.J., Halliday C., Kang N., Sessa W.C., Baker A.H. Invivo modulation of Nogo-B attenuates neointima formation. Mol. Ther. 2008, 16:1798-1804.
75. Kuhnert F., Mancuso M.R., Shamloo A., Wang H.T., Choksi V., Florek M., Su H., Fruttiger M., Young W.L., Heilshorn S.C., Kuo C.J. Essential regulation of CNS angiogenesis by the orphan G protein-coupled receptor GPR124. Science 2010, 330:985-989.
76. Lambert E., Coissieux M.M., Laudet V., Mehlen P. Netrin-4 acts as a pro-angiogenic factor during zebrafish development. J.Biol. Chem. 2012, 287:3987-3999.
77. Lamont R.E., Lamont E.J., Childs S.J. Antagonistic interactions among Plexins regulate the timing of intersegmental vessel formation. Dev. Biol. 2009, 331:199-209.
78. Larrieu-Lahargue F., Welm A.L., Thomas K.R., Li D.Y. Netrin-4 induces lymphangiogenesis invivo. Blood 2010, 115:5418-5426.
79. Larrieu-Lahargue F., Welm A.L., Thomas K.R., Li D.Y. Netrin-4 activates endothelial integrin alpha6beta1. Circ. Res. 2011, 109:770-774.
80. Larrieu-Lahargue F., Thomas K.R., Li D.Y. Netrin ligands and receptors: lessons from neurons to the endothelium. Trends Cardiovasc. Med. 2012, 22:44-47.
81. Larrivée B., Freitas C., Trombe M., Lv X., Delafarge B., Yuan L., Bouvrée K., Bréant C., Del Toro R., Bréchot N., et al. Activation of the UNC5B receptor by Netrin-1 inhibits sprouting angiogenesis. Genes Dev. 2007, 21:2433-2447.
82. Larrivée B., Prahst C., Gordon E., del Toro R., Mathivet T., Duarte A., Simons M., Eichmann A. ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev. Cell 2012, 22:489-500.
83. Lejmi E., Leconte L., Pédron-Mazoyer S., Ropert S., Raoul W., Lavalette S., Bouras I., Feron J.G., Maitre-Boube M., Assayag F., et al. Netrin-4 inhibits angiogenesis via binding to neogenin and recruitment of Unc5B. Proc. Natl. Acad. Sci. USA 2008, 105:12491-12496.
84. Lenard A., Ellertsdottir E., Herwig L., Krudewig A., Sauteur L., Belting H.G., Affolter M. Invivo analysis reveals a highly stereotypic morphogenetic pathway of vascular anastomosis. Dev. Cell 2013, 25:492-506.
85. Li W., Kohara H., Uchida Y., James J.M., Soneji K., Cronshaw D.G., Zou Y.R., Nagasawa T., Mukouyama Y.S. Peripheral nerve-derived CXCL12 and VEGF-A regulate the patterning of arterial vessel branching in developing limb skin. Dev. Cell 2013, 24:359-371.
86. Liebner S., Corada M., Bangsow T., Babbage J., Taddei A., Czupalla C.J., Reis M., Felici A., Wolburg H., Fruttiger M., et al. Wnt/beta-catenin signaling controls development of the blood-brain barrier. J.Cell Biol. 2008, 183:409-417.
87. Lim A.H., Suli A., Yaniv K., Weinstein B., Li D.Y., Chien C.B. Motoneurons are essential for vascular pathfinding. Development 2011, 138:3847-3857.
88. Liu G., Beggs H., Jürgensen C., Park H.T., Tang H., Gorski J., Jones K.R., Reichardt L.F., Wu J., Rao Y. Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat. Neurosci. 2004, 7:1222-1232.
89. Lowery L.A., Van Vactor D. The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 2009, 10:332-343.
90. Lu X., Le Noble F., Yuan L., Jiang Q., De Lafarge B., Sugiyama D., Bréant C., Claes F., De Smet F., Thomas J.L., et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 2004, 432:179-186.
91. Luhmann U.F., Meunier D., Shi W., Lüttges A., Pfarrer C., Fundele R., Berger W. Fetal loss in homozygous mutant Norrie disease mice: a new role of Norrin in reproduction. Genesis 2005, 42:253-262.
92. Mackenzie F., Ruhrberg C. Diverse roles for VEGF-A in the nervous system. Development 2012, 139:1371-1380.
93. Makita T., Sucov H.M., Gariepy C.E., Yanagisawa M., Ginty D.D. Endothelins are vascular-derived axonal guidance cues for developing sympathetic neurons. Nature 2008, 452:759-763.
94. Mammoto A., Connor K.M., Mammoto T., Yung C.W., Huh D., Aderman C.M., Mostoslavsky G., Smith L.E., Ingber D.E. A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 2009, 457:1103-1108.
95. Mancuso M.R., Kuhnert F., Kuo C.J. Developmental angiogenesis of the central nervous system. Lymphat. Res. Biol. 2008, 6:173-180.
96. Marin-Padilla M. Early vascularization of the embryonic cerebral cortex: Golgi and electron microscopic studies. J.Comp. Neurol. 1985, 241:237-249.
97. Miao R.Q., Gao Y., Harrison K.D., Prendergast J., Acevedo L.M., Yu J., Hu F., Strittmatter S.M., Sessa W.C. Identification of a receptor necessary for Nogo-B stimulated chemotaxis and morphogenesis of endothelial cells. Proc. Natl. Acad. Sci. USA 2006, 103:10997-11002.
98. Miao R.Q., Fontana J., Fulton D., Lin M.I., Harrison K.D., Sessa W.C. Dominant-negative Hsp90 reduces VEGF-stimulated nitric oxide release and migration in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2008, 28:105-111.
99. Moore S.W., Biais N., Sheetz M.P. Traction on immobilized netrin-1 is sufficient to reorient axons. Science 2009, 325:166.
100. Morote-Garcia J.C., Napiwotzky D., Köhler D., Rosenberger P. Endothelial Semaphorin 7A promotes neutrophil migration during hypoxia. Proc. Natl. Acad. Sci. USA 2012, 109:14146-14151.
101. Moya I.M., Umans L., Maas E., Pereira P.N., Beets K., Francis A., Sents W., Robertson E.J., Mummery C.L., Huylebroeck D., Zwijsen A. Stalk cell phenotype depends on integration of Notch and Smad1/5 signaling cascades. Dev. Cell 2012, 22:501-514.
102. Nacht M., St Martin T.B., Byrne A., Klinger K.W., Teicher B.A., Madden S.L., Jiang Y. Netrin-4 regulates angiogenic responses and tumor cell growth. Exp. Cell Res. 2009, 315:784-794.
103. Nagase T., Nagase M., Machida M., Fujita T. Hedgehog signalling in vascular development. Angiogenesis 2008, 11:71-77.
104. Navankasattusas S., Whitehead K.J., Suli A., Sorensen L.K., Lim A.H., Zhao J., Park K.W., Wythe J.D., Thomas K.R., Chien C.B., Li D.Y. The netrin receptor UNC5B promotes angiogenesis in specific vascular beds. Development 2008, 135:659-667.
105. Nikolaev A., McLaughlin T., O'Leary D.D., Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009, 457:981-989.
106. Niswander L. Pattern formation: old models out on a limb. Nat. Rev. Genet. 2003, 4:133-143.
107. Nolan D.J., Ginsberg M., Israely E., Palikuqi B., Poulos M.G., James D., Ding B.S., Schachterle W., Liu Y., Rosenwaks Z., et al. Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev. Cell 2013, 26:204-219.
108. Nourshargh S., Hordijk P.L., Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat. Rev. Mol. Cell Biol. 2010, 11:366-378.
109. Oertle T., van der Haar M.E., Bandtlow C.E., Robeva A., Burfeind P., Buss A., Huber A.B., Simonen M., Schnell L., Brösamle C., et al. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J.Neurosci. 2003, 23:5393-5406.
110. Ogunshola O.O., Stewart W.B., Mihalcik V., Solli T., Madri J.A., Ment L.R. Neuronal VEGF expression correlates with angiogenesis in postnatal developing rat brain. Brain Res. Dev. Brain Res. 2000, 119:139-153.
111. Pan Q., Chanthery Y., Liang W.C., Stawicki S., Mak J., Rathore N., Tong R.K., Kowalski J., Yee S.F., Pacheco G., et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 2007, 11:53-67.
112. Park K.W., Crouse D., Lee M., Karnik S.K., Sorensen L.K., Murphy K.J., Kuo C.J., Li D.Y. The axonal attractant Netrin-1 is an angiogenic factor. Proc. Natl. Acad. Sci. USA 2004, 101:16210-16215.
113. 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. Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev. Cell 2009, 16:70-82.
114. Phng L.K., Stanchi F., Gerhardt H. Filopodia are dispensable for endothelial tip cell guidance. Development 2013, 140:4031-4040.
115. Pitulescu M.E., Schmidt I., Benedito R., Adams R.H. Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat. Protoc. 2010, 5:1518-1534.
116. Pola R., Ling L.E., Silver M., Corbley M.J., Kearney M., Blake Pepinsky R., Shapiro R., Taylor F.R., Baker D.P., Asahara T., Isner J.M. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat. Med. 2001, 7:706-711.
117. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
118. Powell A.W., Sassa T., Wu Y., Tessier-Lavigne M., Polleux F. Topography of thalamic projections requires attractive and repulsive functions of Netrin-1 in the ventral telencephalon. PLoS Biol. 2008, 6:e116.
119. Quaegebeur A., Lange C., Carmeliet P. The neurovascular link in health and disease: molecular mechanisms and therapeutic implications. Neuron 2011, 71:406-424.
120. Rehm H.L., Zhang D.S., Brown M.C., Burgess B., Halpin C., Berger W., Morton C.C., Corey D.P., Chen Z.Y. Vascular defects and sensorineural deafness in a mouse model of Norrie disease. J.Neurosci. 2002, 22:4286-4292.
121. Ricci-Vitiani L., Pallini R., Biffoni M., Todaro M., Invernici G., Cenci T., Maira G., Parati E.A., Stassi G., Larocca L.M., De Maria R. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010, 468:824-828.
122. Rocha S.F., Adams R.H. Molecular differentiation and specialization of vascular beds. Angiogenesis 2009, 12:139-147.
123. Ruhrberg C., Gerhardt H., Golding M., Watson R., Ioannidou S., Fujisawa H., Betsholtz C., Shima D.T. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 2002, 16:2684-2698.
124. Runkle E.A., Antonetti D.A. The blood-retinal barrier: structure and functional significance. Methods Mol. Biol. 2011, 686:133-148.
125. Sawamiphak S., Ritter M., Acker-Palmer A. Preparation of retinal explant cultures to study exvivo tip endothelial cell responses. Nat. Protoc. 2010, 5:1659-1665.
126. Sawamiphak S., Seidel S., Essmann C.L., Wilkinson G.A., Pitulescu M.E., Acker T., Acker-Palmer A. Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Nature 2010, 465:487-491.
127. Schwab M.E. Functions of Nogo proteins and their receptors in the nervous system. Nat. Rev. Neurosci. 2010, 11:799-811.
128. Segura I., De Smet F., Hohensinner P.J., Ruiz de Almodovar C., Carmeliet P. The neurovascular link in health and disease: an update. Trends Mol. Med. 2009, 15:439-451.
129. Serini G., Valdembri D., Zanivan S., Morterra G., Burkhardt C., Caccavari F., Zammataro L., Primo L., Tamagnone L., Logan M., et al. Class3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 2003, 424:391-397.
130. Soker S., Takashima S., Miao H.Q., Neufeld G., Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998, 92:735-745.
131. Stenman J.M., Rajagopal J., Carroll T.J., Ishibashi M., McMahon J., McMahon A.P. Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science 2008, 322:1247-1250.
132. Stenzel D., Franco C.A., Estrach S., Mettouchi A., Sauvaget D., Rosewell I., Schertel A., Armer H., Domogatskaya A., Rodin S., et al. Endothelial basement membrane limits tip cell formation by inducing Dll4/Notch signalling invivo. EMBO Rep. 2011, 12:1135-1143.
133. Stewart P.A., Wiley M.J. Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev. Biol. 1981, 84:183-192.
134. Stone J., Itin A., Alon T., Pe'er J., Gnessin H., Chan-Ling T., Keshet E. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J. Neurosci. 1995, 15:4738-4747.
135. Storkebaum E., Quaegebeur A., Vikkula M., Carmeliet P. Cerebrovascular disorders: molecular insights and therapeutic opportunities. Nat. Neurosci. 2011, 14:1390-1397.
136. Sultana H., Neelakanta G., Foellmer H.G., Montgomery R.R., Anderson J.F., Koski R.A., Medzhitov R.M., Fikrig E. Semaphorin 7A contributes to West Nile virus pathogenesis through TGF-β1/Smad6 signaling. J.Immunol. 2012, 189:3150-3158.
137. Tam S.J., Watts R.J. Connecting vascular and nervous system development: angiogenesis and the blood-brain barrier. Annu. Rev. Neurosci. 2010, 33:379-408.
138. Tam S.J., Richmond D.L., Kaminker J.S., Modrusan Z., Martin-McNulty B., Cao T.C., Weimer R.M., Carano R.A., van Bruggen N., Watts R.J. Death receptors DR6 and TROY regulate brain vascular development. Dev. Cell 2012, 22:403-417.
139. Tavazoie M., Van der Veken L., Silva-Vargas V., Louissaint M., Colonna L., Zaidi B., Garcia-Verdugo J.M., Doetsch F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3:279-288.
140. Torres-Vázquez J., Gitler A.D., Fraser S.D., Berk J.D., Fishman M.C., Childs S., Epstein J.A., Weinstein B.M., Van N Pham. Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev. Cell 2004, 7:117-123.
141. Toyofuku T., Zhang H., Kumanogoh A., Takegahara N., Suto F., Kamei J., Aoki K., Yabuki M., Hori M., Fujisawa H., Kikutani H. Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, Plexin-A1, with off-track and vascular endothelial growth factor receptor type 2. Genes Dev. 2004, 18:435-447.
142. Toyofuku T., Yabuki M., Kamei J., Kamei M., Makino N., Kumanogoh A., Hori M. Semaphorin-4A, an activator for T-cell-mediated immunity, suppresses angiogenesis via Plexin-D1. EMBO J. 2007, 26:1373-1384.
143. Uchida C., Gee E., Ispanovic E., Haas T.L. JNK as a positive regulator of angiogenic potential in endothelial cells. Cell Biol. Int. 2008, 32:769-776.
144. Vasudevan A., Long J.E., Crandall J.E., Rubenstein J.L., Bhide P.G. Compartment-specific transcription factors orchestrate angiogenesis gradients in the embryonic brain. Nat. Neurosci. 2008, 11:429-439.
145. Vieira J.M., Schwarz Q., Ruhrberg C. Selective requirements for NRP1 ligands during neurovascular patterning. Development 2007, 134:1833-1843.
146. Wacker A., Gerhardt H. Endothelial development taking shape. Curr. Opin. Cell Biol. 2011, 23:676-685.
147. Wälchli T., Pernet V., Weinmann O., Shiu J.Y., Guzik-Kornacka A., Decrey G., Yüksel D., Schneider H., Vogel J., Ingber D.E., et al. Nogo-A is a negative regulator of CNS angiogenesis. Proc. Natl. Acad. Sci. USA 2013, 110:E1943-E1952.
148. Wälchli T., Mateos J.M., Weinman O., Babic D., Regli L., Hoerstrup S.P., Gerhardt H., Schwab M.E., Vogel J. Quantitative assessment of angiogenesis, perfused blood vessels and endothelial tip cells in the postnatal mouse brain. Nat. Protoc. 2015, 10:53-74.
149. Wang H.U., Chen Z.F., Anderson D.J. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998, 93:741-753.
150. Wang B., Xiao Y., Ding B.B., Zhang N., Yuan Xb., Gui L., Qian K.X., Duan S., Chen Z., Rao Y., Geng J.G. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell 2003, 4:19-29.
151. Wang R., Chadalavada K., Wilshire J., Kowalik U., Hovinga K.E., Geber A., Fligelman B., Leversha M., Brennan C., Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010, 468:829-833.
152. Wang Y., Nakayama M., Pitulescu M.E., Schmidt T.S., Bochenek M.L., Sakakibara A., Adams S., Davy A., Deutsch U., Lüthi U., et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 2010, 465:483-486.
153. Wang Y., Rattner A., Zhou Y., Williams J., Smallwood P.M., Nathans J. Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity. Cell 2012, 151:1332-1344.
154. Weerasuriya A., Mizisin A.P. The blood-nerve barrier: structure and functional significance. Methods Mol. Biol. 2011, 686:149-173.
155. Wei Y.T., He Y., Xu C.L., Wang Y., Liu B.F., Wang X.M., Sun X.D., Cui F.Z., Xu Q.Y. Hyaluronic acid hydrogel modified with nogo-66 receptor antibody and poly-L-lysine to promote axon regrowth after spinal cord injury. J.Biomed. Mater. Res. B Appl. Biomater. 2010, 95:110-117.
156. Weis S.M., Cheresh D.A. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat. Med. 2011, 17:1359-1370.
157. Whiteus C., Freitas C., Grutzendler J. Perturbed neural activity disrupts cerebral angiogenesis during a postnatal critical period. Nature 2014, 505:407-411.
158. Wilson B.D., Ii M., Park K.W., Suli A., Sorensen L.K., Larrieu-Lahargue F., Urness L.D., Suh W., Asai J., Kock G.A., et al. Netrins promote developmental and therapeutic angiogenesis. Science 2006, 313:640-644.
159. Wong H.K., Shimizu A., Kirkpatrick N.D., Garkavtsev I., Chan A.W., di Tomaso E., Klagsbrun M., Jain R.K. Merlin/NF2 regulates angiogenesis in schwannomas through a Rac1/semaphorin 3F-dependent mechanism. Neoplasia 2012, 14:84-94.
160. Xu Q., Wang Y., Dabdoub A., Smallwood P.M., Williams J., Woods C., Kelley M.W., Jiang L., Tasman W., Zhang K., Nathans J. Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell 2004, 116:883-895.
161. Ye X., Wang Y., Cahill H., Yu M., Badea T.C., Smallwood P.M., Peachey N.S., Nathans J. Norrin, frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization. Cell 2009, 139:285-298.
162. Ye X., Wang Y., Nathans J. The Norrin/Frizzled4 signaling pathway in retinal vascular development and disease. Trends Mol. Med. 2010, 16:417-425.
163. Yin Y., Sanes J.R., Miner J.H. Identification and expression of mouse netrin-4. Mech. Dev. 2000, 96:115-119.
164. Yu J., Fernández-Hernando C., Suarez Y., Schleicher M., Hao Z., Wright P.L., DiLorenzo A., Kyriakides T.R., Sessa W.C. Reticulon 4B (Nogo-B) is necessary for macrophage infiltration and tissue repair. Proc. Natl. Acad. Sci. USA 2009, 106:17511-17516.
165. Zacchigna S., Lambrechts D., Carmeliet P. Neurovascular signalling defects in neurodegeneration. Nat. Rev. Neurosci. 2008, 9:169-181.
166. Zhao B., Chun C., Liu Z., Horswill M.A., Pramanik K., Wilkinson G.A., Ramchandran R., Miao R.Q. Nogo-B receptor is essential for angiogenesis in zebrafish via Akt pathway. Blood 2010, 116:5423-5433.
167. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.
168. Zlokovic B.V. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 2011, 12:723-738.
169. 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. Semaphorin-PlexinD1 signaling limits angiogenic potential via the VEGF decoy receptor sFlt1. Dev. Cell 2011, 21:301-314.