Neural regulation of CNS angiogenesis during development

Shang MA, Zhen HUANG

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Front. Biol. ›› 2015, Vol. 10 ›› Issue (1) : 61-73. DOI: 10.1007/s11515-014-1331-y
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Neural regulation of CNS angiogenesis during development

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Abstract

Vertebrates have evolved a powerful vascular system that involves close interactions between blood vessels and target tissues. Vascular biology had been mostly focused on the study of blood vessels for decades, which has generated large bodies of knowledge on vascular cell development, function and pathology. We argue that the prime time has arrived for vascular research on vessel-tissue interactions, especially target tissue regulation of vessel development. The central nervous system (CNS) requires a highly efficient vascular system for oxygen and nutrient transport as well as waste disposal. Therefore, neurovascular interaction is an excellent entry point to understanding target tissue regulation of blood vessel development. In this review, we summarize signaling pathways that transmit information from neural cells to blood vessels during development and the mechanisms by which they regulate each step of CNS angiogenesis. We also review important mechanisms of neural regulation of blood-brain barrier establishment and maturation, highlighting different functions of neural progenitor cells and pericytes. Finally, we evaluate potential contribution of malfunctioning neurovascular signaling to the development of brain vascular diseases and discuss how neurovascular interactions could be involved in brain tumor angiogenesis.

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Shang MA, Zhen HUANG. Neural regulation of CNS angiogenesis during development. Front. Biol., 2015, 10(1): 61‒73 https://doi.org/10.1007/s11515-014-1331-y

References

[1]
Abbott N J, Rönnbäck L, Hansson E (2006). Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci, 7(1): 41-53
CrossRef Pubmed Google scholar
[2]
Alon T, Hemo I, Itin A, Pe’er J, Stone J, Keshet E (1995). Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med, 1(10): 1024-1028
CrossRef Pubmed Google scholar
[3]
Alvarez J I, Dodelet-Devillers A, Kebir H, Ifergan I, Fabre P J, Terouz S, Sabbagh M, Wosik K, Bourbonnière L, Bernard M, van Horssen J, de Vries H E, Charron F, Prat A (2011). The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science, 334(6063): 1727-1731
CrossRef Pubmed Google scholar
[4]
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, Macdonald L E, Thurston G, Daly C, Lin H C, Economides A N, Valenzuela D M, Murphy A J, Yancopoulos G D, Gale N W (2011). Angiogenic sprouting into neural tissue requires Gpr124, an orphan G protein-coupled receptor. Proc Natl Acad Sci USA, 108(7): 2807-2812
CrossRef Pubmed Google scholar
[5]
Armulik A, Abramsson A, Betsholtz C (2005). Endothelial/pericyte interactions. Circ Res, 97(6): 512-523
CrossRef Pubmed Google scholar
[6]
Arnold T D, Ferrero G M, Qiu H, Phan I T, Akhurst R J, Huang E J, Reichardt L F (2012). Defective retinal vascular endothelial cell development as a consequence of impaired integrin αVβ8-mediated activation of transforming growth factor-β. J Neurosci, 32(4): 1197-1206
CrossRef Pubmed Google scholar
[7]
Ballabh P (2010). Intraventricular hemorrhage in premature infants: mechanism of disease. Pediatr Res, 67(1): 1-8
CrossRef Pubmed Google scholar
[8]
Ballabh P, Xu H, Hu F, Braun A, Smith K, Rivera A, Lou N, Ungvari Z, Goldman S A, Csiszar A, Nedergaard M (2007). Angiogenic inhibition reduces germinal matrix hemorrhage. Nat Med, 13(4): 477-485
CrossRef Pubmed Google scholar
[9]
Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland A B, Shi Q, McLendon R E, Bigner D D, Rich J N (2006). Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res, 66(16): 7843-7848
CrossRef Pubmed Google scholar
[10]
Bell R D, Winkler E A, Sagare A P, Singh I, LaRue B, Deane R, Zlokovic B V (2010). Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron, 68(3): 409-427
CrossRef Pubmed Google scholar
[11]
Ben-Zvi A, Lacoste B, Kur E, Andreone B J, Mayshar Y, Yan H, Gu C (2014). Mfsd2a is critical for the formation and function of the blood-brain barrier. Nature, 509(7501): 507-511
CrossRef Pubmed Google scholar
[12]
Benedito R, Roca C, Sörensen I, Adams S, Gossler A, Fruttiger M, Adams R H (2009). The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell, 137(6): 1124-1135
CrossRef Pubmed Google scholar
[13]
Berg J N, Gallione C J, Stenzel T T, Johnson D W, Allen W P, Schwartz C E, Jackson C E, Porteous M E, Marchuk D A (1997). The activin receptor-like kinase 1 gene: genomic structure and mutations in hereditary hemorrhagic telangiectasia type 2. Am J Hum Genet, 61(1): 60-67
CrossRef Pubmed Google scholar
[14]
Bergametti F, Denier C, Labauge P, Arnoult M, Boetto S, Clanet M, Coubes P, Echenne B, Ibrahim R, Irthum B, Jacquet G, Lonjon M, Moreau J J, Neau J P, Parker F, Tremoulet M, Tournier-Lasserve E, the Société Française de Neurochirurgie (2005). Mutations within the programmed cell death 10 gene cause cerebral cavernous malformations. Am J Hum Genet, 76(1): 42-51
CrossRef Pubmed Google scholar
[15]
Boulday G, Rudini N, Maddaluno L, Blécon A, Arnould M, Gaudric A, Chapon F, Adams R H, Dejana E, Tournier-Lasserve E (2011). Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice. J Exp Med, 208(9): 1835-1847
CrossRef Pubmed Google scholar
[16]
Braun A, Xu H, Hu F, Kocherlakota P, Siegel D, Chander P, Ungvari Z, Csiszar A, Nedergaard M, Ballabh P (2007). Paucity of pericytes in germinal matrix vasculature of premature infants. J Neurosci, 27(44): 12012-12024
CrossRef Pubmed Google scholar
[17]
Breier G, Albrecht U, Sterrer S, Risau W (1992). Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development, 114(2): 521-532
Pubmed
[18]
Breier G, Clauss M, Risau W (1995). Coordinate expression of vascular endothelial growth factor receptor-1 (flt-1) and its ligand suggests a paracrine regulation of murine vascular development. Dev Dyn, 204(3): 228-239
CrossRef Pubmed Google scholar
[19]
Calabrese C, Poppleton H, Kocak M, Hogg T L, Fuller C, Hamner B, Oh E Y, Gaber M W, Finklestein D, Allen M, Frank A, Bayazitov I T, Zakharenko S S, Gajjar A, Davidoff A, Gilbertson R J (2007). A perivascular niche for brain tumor stem cells. Cancer Cell, 11(1): 69-82
CrossRef Pubmed Google scholar
[20]
Cambier S, Gline S, Mu D, Collins R, Araya J, Dolganov G, Einheber S, Boudreau N, Nishimura S L (2005). Integrin α(v8-mediated activation of transforming growth factor-β by perivascular astrocytes: an angiogenic control switch. Am J Pathol, 166(6): 1883-1894
CrossRef Pubmed Google scholar
[21]
Clarke M F, Fuller M (2006). Stem cells and cancer: two faces of eve. Cell, 124(6): 1111-1115
CrossRef Pubmed Google scholar
[22]
Cullen M, Elzarrad M K, Seaman S, Zudaire E, Stevens J, Yang M Y, Li X, Chaudhary A, Xu L, Hilton M B, Logsdon D, Hsiao E, Stein E V, Cuttitta F, Haines D C, Nagashima K, Tessarollo L, St Croix B (2011). 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, 108(14): 5759-5764
CrossRef Pubmed Google scholar
[23]
Daneman R, Agalliu D, Zhou L, Kuhnert F, Kuo C J, Barres B A (2009). Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proc Natl Acad Sci USA, 106(2): 641-646
CrossRef Pubmed Google scholar
[24]
Daneman R, Zhou L, Kebede A A, Barres B A (2010). Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature, 468(7323): 562-566
CrossRef Pubmed Google scholar
[25]
Doherty P, Williams G, Williams E J (2000). CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol Cell Neurosci, 16(4): 283-295
CrossRef Pubmed Google scholar
[26]
Dorrell M I, Aguilar E, Friedlander M (2002). Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci, 43(11): 3500-3510
Pubmed
[27]
Gallione C J, Repetto G M, Legius E, Rustgi A K, Schelley S L, Tejpar S, Mitchell G, Drouin E, Westermann C J, Marchuk D A (2004). A combined syndrome of juvenile polyposis and hereditary haemorrhagic telangiectasia associated with mutations in MADH4 (SMAD4). Lancet, 363(9412): 852-859
CrossRef Pubmed Google scholar
[28]
Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol, 161(6): 1163-1177
CrossRef Pubmed Google scholar
[29]
Gerhardt H, Ruhrberg C, Abramsson A, Fujisawa H, Shima D, Betsholtz C (2004). Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev Dyn, 231(3): 503-509
CrossRef Pubmed Google scholar
[30]
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 (2005). Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science, 307(5707): 265-268
CrossRef Pubmed Google scholar
[31]
Hayashi Y, Nomura M, Yamagishi S, Harada S, Yamashita J, Yamamoto H (1997). Induction of various blood-brain barrier properties in non-neural endothelial cells by close apposition to co-cultured astrocytes. Glia, 19(1): 13-26
CrossRef Pubmed Google scholar
[32]
Hellström M, Kalén M, Lindahl P, Abramsson A, Betsholtz C (1999). Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development, 126(14): 3047-3055
Pubmed
[33]
Hellström M, Phng L K, Hofmann J J, Wallgard E, Coultas L, Lindblom P, Alva J, Nilsson A K, Karlsson L, Gaiano N, Yoon K, Rossant J, Iruela-Arispe M L, Kalén M, Gerhardt H, Betsholtz C (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature, 445(7129): 776-780
CrossRef Pubmed Google scholar
[34]
Heuchan A M, Evans N, Henderson Smart D J, Simpson J M (2002). Perinatal risk factors for major intraventricular haemorrhage in the Australian and New Zealand Neonatal Network, 1995-97. Arch Dis Child Fetal Neonatal Ed, 86(2): F86-F90
CrossRef Pubmed Google scholar
[35]
Hirota S, Liu Q, Lee H S, Hossain M G, Lacy-Hulbert A, McCarty J H (2011). The astrocyte-expressed integrin αvβ8 governs blood vessel sprouting in the developing retina. Development, 138(23): 5157-5166
CrossRef Pubmed Google scholar
[36]
Johnson D W, Berg J N, Baldwin M A, Gallione C J, Marondel I, Yoon S J, Stenzel T T, Speer M, Pericak-Vance M A, Diamond A, Guttmacher A E, Jackson C E, Attisano L, Kucherlapati R, Porteous M E M, Marchuk D A (1996). Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat Genet, 13(2): 189-195
CrossRef Pubmed Google scholar
[37]
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 (2010). Essential regulation of CNS angiogenesis by the orphan G protein-coupled receptor GPR124. Science, 330(6006): 985-989
CrossRef Pubmed Google scholar
[38]
Lang R A, Bishop J M (1993). Macrophages are required for cell death and tissue remodeling in the developing mouse eye. Cell, 74(3): 453-462
CrossRef Pubmed Google scholar
[39]
Lee S W, Kim W J, Choi Y K, Song H S, Son M J, Gelman I H, Kim Y J, Kim K W (2003). SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat Med, 9(7): 900-906
CrossRef Pubmed Google scholar
[40]
Li F, Lan Y, Wang Y, Wang J, Yang G, Meng F, Han H, Meng A, Wang Y, Yang X (2011). Endothelial Smad4 maintains cerebrovascular integrity by activating N-cadherin through cooperation with Notch. Dev Cell, 20(3): 291-302
CrossRef Pubmed Google scholar
[41]
Liebner S, Corada M, Bangsow T, Babbage J, Taddei A, Czupalla C J, Reis M, Felici A, Wolburg H, Fruttiger M, Taketo M M, von Melchner H, Plate K H, Gerhardt H, Dejana E (2008). Wnt/beta-catenin signaling controls development of the blood-brain barrier. J Cell Biol, 183(3): 409-417
CrossRef Pubmed Google scholar
[42]
Lindahl P, Johansson B R, Levéen P, Betsholtz C (1997). Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science, 277(5323): 242-245
CrossRef Pubmed Google scholar
[43]
Lobov I B, Brooks P C, Lang R A (2002). Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci USA, 99(17): 11205-11210
CrossRef Pubmed Google scholar
[44]
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, Morrisey E E, McMahon A P, Karsenty G, Lang R A (2005). WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature, 437(7057): 417-421
CrossRef Pubmed Google scholar
[45]
Lobov I B, Renard R A, Papadopoulos N, Gale N W, Thurston G, Yancopoulos G D, Wiegand S J (2007). Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci USA, 104(9): 3219-3224
CrossRef Pubmed Google scholar
[46]
Louvi A, Chen L, Two A M, Zhang H, Min W, Günel M (2011). Loss of cerebral cavernous malformation 3 (Ccm3) in neuroglia leads to CCM and vascular pathology. Proc Natl Acad Sci USA, 108(9): 3737-3742
CrossRef Pubmed Google scholar
[47]
Lu X, Le Noble F, Yuan L, Jiang Q, De Lafarge B, Sugiyama D, Bréant C, Claes F, De Smet F, Thomas J L, Autiero M, Carmeliet P, Tessier-Lavigne M, Eichmann A (2004). The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature, 432(7014): 179-186
CrossRef Pubmed Google scholar
[48]
Ma S, Kwon H J, Johng H, Zang K, Huang Z (2013). Radial glial neural progenitors regulate nascent brain vascular network stabilization via inhibition of Wnt signaling. PLoS Biol, 11(1): e1001469
CrossRef Pubmed Google scholar
[49]
Maddaluno L, Rudini N, Cuttano R, Bravi L, Giampietro C, Corada M, Ferrarini L, Orsenigo F, Papa E, Boulday G, Tournier-Lasserve E, Chapon F, Richichi C, Retta S F, Lampugnani M G, Dejana E (2013). EndMT contributes to the onset and progression of cerebral cavernous malformations. Nature, 498(7455): 492-496
CrossRef Pubmed Google scholar
[50]
McAllister K A, Grogg K M, Johnson D W, Gallione C J, Baldwin M A, Jackson C E, Helmbold E A, Markel D S, McKinnon W C, Murrell J, McCormick M K, Pericak-Vance M A, Heutink P, Oostra B A, Haitjema T, Westerman C J J, Porteous M E, Guttmacher A E, Letarte M, Marchuk D A (1994). Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet, 8(4): 345-351
CrossRef Pubmed Google scholar
[51]
McCarty J H, Monahan-Earley R A, Brown L F, Keller M, Gerhardt H, Rubin K, Shani M, Dvorak H F, Wolburg H, Bader B L, Dvorak A M, Hynes R O (2002). Defective associations between blood vessels and brain parenchyma lead to cerebral hemorrhage in mice lacking alphav integrins. Mol Cell Biol, 22(21): 7667-7677
CrossRef Pubmed Google scholar
[52]
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 (2012). Stalk cell phenotype depends on integration of Notch and Smad1/5 signaling cascades. Dev Cell, 22(3): 501-514
CrossRef Pubmed Google scholar
[53]
Mu D, Cambier S, Fjellbirkeland L, Baron J L, Munger J S, Kawakatsu H, Sheppard D, Broaddus V C, Nishimura S L (2002). The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J Cell Biol, 157(3): 493-507
CrossRef Pubmed Google scholar
[54]
Mu D, Jiang X, Sheldon R A, Fox C K, Hamrick S E, Vexler Z S, Ferriero D M (2003). Regulation of hypoxia-inducible factor 1alpha and induction of vascular endothelial growth factor in a rat neonatal stroke model. Neurobiol Dis, 14(3): 524-534
CrossRef Pubmed Google scholar
[55]
Ng Y S, Rohan R, Sunday M E, Demello D E, D’Amore P A (2001). Differential expression of VEGF isoforms in mouse during development and in the adult. Dev Dyn, 220(2): 112-121
CrossRef Pubmed Google scholar
[56]
Palmer T D, Willhoite A R, Gage F H (2000). Vascular niche for adult hippocampal neurogenesis. J Comp Neurol, 425(4): 479-494
CrossRef Pubmed Google scholar
[57]
Pen A, Moreno M J, Durocher Y, Deb-Rinker P, Stanimirovic D B (2008). Glioblastoma-secreted factors induce IGFBP7 and angiogenesis by modulating Smad-2-dependent TGF-beta signaling. Oncogene, 27(54): 6834-6844
CrossRef Pubmed Google scholar
[58]
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 (2009). Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev Cell, 16(1): 70-82
CrossRef Pubmed Google scholar
[59]
Proctor J M, Zang K, Wang D, Wang R, Reichardt L F (2005). Vascular development of the brain requires beta8 integrin expression in the neuroepithelium. J Neurosci, 25(43): 9940-9948
CrossRef Pubmed Google scholar
[60]
Qiu B, Zhang D, Wang C, Tao J, Tie X, Qiao Y, Xu K, Wang Y, Wu A (2011). IL-10 and TGF-β2 are overexpressed in tumor spheres cultured from human gliomas. Mol Biol Rep, 38(5): 3585-3591
CrossRef Pubmed Google scholar
[61]
Raab S, Beck H, Gaumann A, Yüce A, Gerber H P, Plate K, Hammes H P, Ferrara N, Breier G (2004). Impaired brain angiogenesis and neuronal apoptosis induced by conditional homozygous inactivation of vascular endothelial growth factor. Thromb Haemost, 91(3): 595-605
Pubmed
[62]
Risau W (1993). Development of the vascular system of organs and tissues. In: Schaper W, Schaper J, ed. Collateral Circulation. Kluwer Academic Publishers, 17-28
[63]
Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, Fujisawa H, Betsholtz C, Shima D T (2002). Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev, 16(20): 2684-2698
CrossRef Pubmed Google scholar
[64]
Sato T N, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gendron-Maguire M, Gridley T, Wolburg H, Risau W, Qin Y (1995). Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature, 376(6535): 70-74
CrossRef Pubmed Google scholar
[65]
Saunders W B, Bohnsack B L, Faske J B, Anthis N J, Bayless K J, Hirschi K K, Davis G E (2006). Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J Cell Biol, 175(1): 179-191
CrossRef Pubmed Google scholar
[66]
Scott A, Powner M B, Gandhi P, Clarkin C, Gutmann D H, Johnson R S, Ferrara N, Fruttiger M (2010). Astrocyte-derived vascular endothelial growth factor stabilizes vessels in the developing retinal vasculature. PLoS ONE, 5(7): e11863
CrossRef Pubmed Google scholar
[67]
Shen Q, Goderie S K, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science, 304(5675): 1338-1340
CrossRef Pubmed Google scholar
[68]
Stenman J M, Rajagopal J, Carroll T J, Ishibashi M, McMahon J, McMahon A P (2008). Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science, 322(5905): 1247-1250
CrossRef Pubmed Google scholar
[69]
Stewart P A, Wiley M J (1981). Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev Biol, 84(1): 183-192
CrossRef Pubmed Google scholar
[70]
Stone J, Itin A, Alon T, Pe’er J, Gnessin H, Chan-Ling T, Keshet E (1995). Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci, 15(7 Pt 1): 4738-4747
Pubmed
[71]
Stubbs D, DeProto J, Nie K, Englund C, Mahmud I, Hevner R, Molnár Z (2009). Neurovascular congruence during cerebral cortical development. Cereb Cortex, 19(Suppl 1): i32-i41
CrossRef Pubmed Google scholar
[72]
Suchting S, Freitas C, le Noble F, Benedito R, Bréant C, Duarte A, Eichmann A (2007). The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci USA, 104(9): 3225-3230
CrossRef Pubmed Google scholar
[73]
Suri C, McClain J, Thurston G, McDonald D M, Zhou H, Oldmixon E H, Sato T N, Yancopoulos G D (1998). Increased vascularization in mice overexpressing angiopoietin-1. Science, 282(5388): 468-471
CrossRef Pubmed Google scholar
[74]
Tam S J, Watts R J (2010). Connecting vascular and nervous system development: angiogenesis and the blood-brain barrier. Annu Rev Neurosci, 33(1): 379-408
CrossRef Pubmed Google scholar
[75]
Tchaicha J H, Reyes S B, Shin J, Hossain M G, Lang F F, McCarty J H (2011). Glioblastoma angiogenesis and tumor cell invasiveness are differentially regulated by β8 integrin. Cancer Res, 71(20): 6371-6381
CrossRef Pubmed Google scholar
[76]
Thurston G, Suri C, Smith K, McClain J, Sato T N, Yancopoulos G D, McDonald D M (1999). Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science, 286(5449): 2511-2514
CrossRef Pubmed Google scholar
[77]
Tomita S, Ueno M, Sakamoto M, Kitahama Y, Ueki M, Maekawa N, Sakamoto H, Gassmann M, Kageyama R, Ueda N, Gonzalez F J, Takahama Y (2003). Defective brain development in mice lacking the Hif-1alpha gene in neural cells. Mol Cell Biol, 23(19): 6739-6749
CrossRef Pubmed Google scholar
[78]
Vasudevan A, Long J E, Crandall J E, Rubenstein J L, Bhide P G (2008). Compartment-specific transcription factors orchestrate angiogenesis gradients in the embryonic brain. Nat Neurosci, 11(4): 429-439
CrossRef Pubmed Google scholar
[79]
Volpe J J (2005). Encephalopathy of prematurity includes neuronal abnormalities. Pediatrics, 116(1): 221-225
CrossRef Pubmed Google scholar
[80]
Weidenfeller C, Svendsen C N, Shusta E V (2007). Differentiating embryonic neural progenitor cells induce blood-brain barrier properties. J Neurochem, 101(2): 555-565
CrossRef Pubmed Google scholar
[81]
Wu B, Crampton S P, Hughes C C (2007). Wnt signaling induces matrix metalloproteinase expression and regulates T cell transmigration. Immunity, 26(2): 227-239
CrossRef Pubmed Google scholar
[82]
Yang S X, Chen J H, Jiang X F, Wang Q L, Chen Z Q, Zhao W, Feng Y H, Xin R, Shi J Q, Bian X W (2005). Activation of chemokine receptor CXCR4 in malignant glioma cells promotes the production of vascular endothelial growth factor. Biochem Biophys Res Commun, 335(2): 523-528
CrossRef Pubmed Google scholar
[83]
Yang Z, Mu Z, Dabovic B, Jurukovski V, Yu D, Sung J, Xiong X, Munger J S (2007). Absence of integrin-mediated TGFbeta1 activation in vivo recapitulates the phenotype of TGFbeta1-null mice. J Cell Biol, 176(6): 787-793
CrossRef Pubmed Google scholar
[84]
Yao Y, Chen Z L, Norris E H, Strickland S (2014). Astrocytic laminin regulates pericyte differentiation and maintains blood brain barrier integrity. Nat Commun, 5: 3413
CrossRef Pubmed Google scholar
[85]
Zhu J, Motejlek K, Wang D, Zang K, Schmidt A, Reichardt L F (2002). β8 integrins are required for vascular morphogenesis in mouse embryos. Development, 129(12): 2891-2903
Pubmed
[86]
Zlokovic B V (2008). The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron, 57(2): 178-201
CrossRef Pubmed Google scholar

Acknowledgements

This work was supported by an NIH grant NS076729 to Z. H and an AHA pre-doctoral fellowship award 14PRE19080006 to S.M.

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2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
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