Interactions between VEGFR and Notch signaling pathways in endothelial and neural cells

Cellular and Molecular Life Sciences

Volumn 70, Issue 10, 2013, Pages 1779-1792

  Thomas, Jean Leon ^a,b,c   Baker, Kasey ^a   Han, Jinah ^a   Calvo, Charles ^b,c   Nurmi, Harri ^d   Eichmann, Anne C ^a,e   Alitalo, Kari ^d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SORBONNE UNIVERSITÉ   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d UNIVERSITY OF HELSINKI   (Finland)

^e PSL RESEARCH UNIVERSITY   (France)

Author keywords

Angiogenesis; Neurogenesis; Neurovascular interactions; Notch; VEGFRs; VEGFs

Indexed keywords

NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH4 RECEPTOR; TRANSCRIPTION FACTOR HES 1; VASCULOTROPIN A; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; BRAIN DEVELOPMENT; CELL INTERACTION; CELL PROLIFERATION; DENTATE GYRUS; ENDOTHELIUM CELL; GLIA CELL; HUMAN; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; NOTCH SIGNALING PATHWAY; REVIEW; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; WNT SIGNALING PATHWAY;

METAZOA; VERTEBRATA;

EID: 84876891617     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1312-6     Document Type: Review

References (131)

1. Bautch VL, James JM (2009) Neurovascular development: the beginning of a beautiful friendship. Cell Adhesion Migr 3(2):199-204
2. Ruhrberg C, Bautch VL (2013) Neurovascular development and links to disease. Cell Mol Life Sci (CMLS this issue)
3. Greenberg DA, Jin K (2013) Vascular endothelial growth factors (VEGFs) and stroke. Cell Mol Life Sci (CMLS this issue)
4. Carmeliet P, Ruiz de Almodovar C (2013) VEGF ligands and receptors: implications in neurodevelopment and neurodegeneration. Cell Mol Life Sci (CMLS this issue)
5. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284(5415):770-776
6. Louvi A, Artavanis-Tsakonas S (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7(2):93-102
7. Yoon K, Gaiano N (2005) Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 8(6):709-715
8. Artavanis-Tsakonas S, Muskavitch MA (2010) Notch: the past, the present, and the future. Curr Top Dev Biol 92:1-29
9. D'Souza B, Meloty-Kapella L, Weinmaster G (2010) Canonical and non-canonical Notch ligands. Curr Top Dev Biol 92:73-129
10. 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
11. Phng LK, Potente M, Leslie JD, Babbage J, Nyqvist D, Lobov I, Ondr JK, Rao S, Lang RA, Thurston G, Gerhardt H (2009) Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev Cell 16(1):70-82
12. del Toro R, Prahst C, Mathivet T, Siegfried G, Kaminker JS, Larrivee B, Breant C, Duarte A, Takakura N, Fukamizu A, Penninger J, Eichmann A (2010) Identification and functional analysis of endothelial tip cell-enriched genes. Blood 116(19):4025-4033
13. Hellstrom M, Phng LK, Gerhardt H (2007) VEGF and Notch signaling: the yin and yang of angiogenic sprouting. Cell Adhesion Migr 1(3):133-136
14. Leslie JD, Ariza-McNaughton L, Bermange AL, McAdow R, Johnson SL, Lewis J (2007) Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134(5):839-844
15. Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, Yancopoulos GD, Wiegand SJ (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
16. Siekmann AF, Lawson ND (2007) Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445(7129):781-784
17. Suchting S, Freitas C, le Noble F, Benedito R, Breant 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
18. Scehnet JS, Jiang W, Kumar SR, Krasnoperov V, Trindade A, Benedito R, Djokovic D, Borges C, Ley EJ, Duarte A, Gill PS (2007) Inhibition of Dll4-mediated signaling induces proliferation of immature vessels and results in poor tissue perfusion. Blood 109(11):4753-4760
19. Benedito R, Rocha SF, Woeste M, Zamykal M, Radtke F, Casanovas O, Duarte A, Pytowski B, Adams RH (2012) Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 484(7392):110-114
20. Hogan BM, Herpers R, Witte M, Helotera H, Alitalo K, Duckers HJ, Schulte-Merker S (2009) Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development 136(23):4001-4009
21. Tammela T, Zarkada G, Nurmi H, Jakobsson L, Heinolainen K, Tvorogov D, Zheng W, Franco CA, Murtomaki A, Aranda E, Miura N, Yla-Herttuala S, Fruttiger M, Makinen T, Eichmann A, Pollard JW, Gerhardt H, Alitalo K (2011) VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat Cell Biol 13(10):1202-1213
22. Tammela T, Zarkada G, Wallgard E, Murtomäki A, Suchting S, Wirzenius M, Waltari M, Hellström M, Schomber T, Peltonen R, Freitas C, Duarte A, Isoniemi H, Laakkonen P, Christofori G, Ylä-Herttuala S, Shibuya M, Pytowski B, Eichmann A, Betsholtz C, Alitalo K (2008) Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454(7204):656-660. doi: 10.1038/nature07083
23. Andersson ER, Sandberg R, Lendahl U (2011) Notch signaling: simplicity in design, versatility in function. Development 138(17):3593-3612
24. Bray S, Bernard F (2010) Notch targets and their regulation. Curr Top Dev Biol 92:253-275
25. Wu L, Aster JC, Blacklow SC, Lake R, Artavanis-Tsakonas S, Griffin JD (2000) MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat Genet 26(4):484-489
26. Fryer CJ, White JB, Jones KA (2004) Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol Cell 16(4):509-520
27. Iso T, Kedes L, Hamamori Y (2003) HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194(3):237-255
28. Kageyama R, Ohtsuka T (1999) The Notch-Hes pathway in mammalian neural development. Cell Res 9(3):179-188
29. Mazzone M (2010) Novel alternatives for anti-angiogenetic therapy and therapeutic angiogenesis. Verhandelingen Koninklijke Academie voor Geneeskunde van Belgie 72(3-4):165-175
30. Hurlbut GD, Kankel MW, Lake RJ, Artavanis-Tsakonas S (2007) Crossing paths with Notch in the hyper-network. Curr Opin Cell Biol 19(2):166-175
31. Kankel MW, Hurlbut GD, Upadhyay G, Yajnik V, Yedvobnick B, Artavanis-Tsakonas S (2007) Investigating the genetic circuitry of mastermind in Drosophila, a notch signal effector. Genetics 177(4):2493-2505
32. Louvi A, Artavanis-Tsakonas S (2012) Notch and disease: a growing field. Semin Cell Dev Biol 23(4):473-480
33. Peter IS, Davidson EH (2011) A gene regulatory network controlling the embryonic specification of endoderm. Nature 474(7353):635-639
34. Saj A, Arziman Z, Stempfle D, van Belle W, Sauder U, Horn T, Durrenberger M, Paro R, Boutros M, Merdes G (2010) A combined ex vivo and in vivo RNAi screen for notch regulators in Drosophila reveals an extensive notch interaction network. Dev Cell 18(5):862-876
35. Heitzler P (2010) Biodiversity and noncanonical Notch signaling. Curr Top Dev Biol 92:457-481
36. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380(6573):439-442
37. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380(6573):435-439
38. Gille H, Kowalski J, Li B, LeCouter J, Moffat B, Zioncheck TF, Pelletier N, Ferrara N (2001) Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J Biol Chem 276(5):3222-3230
39. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376(6535):62-66
40. Shinkai A, Ito M, Anazawa H, Yamaguchi S, Shitara K, Shibuya M (1998) Mapping of the sites involved in ligand association and dissociation at the extracellular domain of the kinase insert domain-containing receptor for vascular endothelial growth factor. J Biol Chem 273(47):31283-31288
41. Koch S, Claesson-Welsh L (2012) Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harbor Perspect Med 2(7):a006502
42. Kappas NC, Zeng G, Chappell JC, Kearney JB, Hazarika S, Kallianos KG, Patterson C, Annex BH, Bautch VL (2008) The VEGF receptor Flt-1 spatially modulates Flk-1 signaling and blood vessel branching. J Cell Biol 181(5):847-858
43. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9(6):669-676
44. Kukk E, Lymboussaki A, Taira S, Kaipainen A, Jeltsch M, Joukov V, Alitalo K (1996) VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 122(12):3829-3837
45. Tammela T, Alitalo K (2010) Lymphangiogenesis: molecular mechanisms and future promise. Cell 140(4):460-476
46. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K (1996) A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15(7):1751
47. Dumont DJ, Jussila L, Taipale J, Lymboussaki A, Mustonen T, Pajusola K, Breitman M, Alitalo K (1998) Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282(5390):946-949
48. Covassin L, Amigo JD, Suzuki K, Teplyuk V, Straubhaar J, Lawson ND (2006) Global analysis of hematopoietic and vascular endothelial gene expression by tissue specific microarray profiling in zebrafish. Dev Biol 299(2):551-562
49. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, Betsholtz C, Alitalo K (2004) Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 5(1):74-80
50. Wang JF, Zhang XF, Groopman JE (2001) Stimulation of beta 1 integrin induces tyrosine phosphorylation of vascular endothelial growth factor receptor-3 and modulates cell migration. J Biol Chem 276(45):41950-41957
51. Galvagni F, Pennacchini S, Salameh A, Rocchigiani M, Neri F, Orlandini M, Petraglia F, Gotta S, Sardone GL, Matteucci G, Terstappen GC, Oliviero S (2010) Endothelial cell adhesion to the extracellular matrix induces c-Src-dependent VEGFR-3 phosphorylation without the activation of the receptor intrinsic kinase activity. Circ Res 106(12):1839-1848
52. Benedito R, Hellstrom M (2013) Notch as a hub for signaling in angiogenesis. Exp Cell Res
53. Kume T (2009) Novel insights into the differential functions of Notch ligands in vascular formation. J Angiogenes Res 1:8
54. Gale NW, Dominguez MG, Noguera I, Pan L, Hughes V, Valenzuela DM, Murphy AJ, Adams NC, Lin HC, Holash J, Thurston G, Yancopoulos GD (2004) Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci USA 101(45):15949-15954
55. Limbourg FP, Takeshita K, Radtke F, Bronson RT, Chin MT, Liao JK (2005) Essential role of endothelial Notch1 in angiogenesis. Circulation 111(14):1826-1832
56. Hellstrom M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, Alva J, Nilsson AK, Karlsson L, Gaiano N, Yoon K, Rossant J, Iruela-Arispe ML, Kalen M, Gerhardt H, Betsholtz C (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445(7129):776-780
57. Thurston G, Noguera-Troise I, Yancopoulos GD (2007) The Delta paradox: DLL4 blockade leads to more tumour vessels but less tumour growth. Nat Rev Cancer 7(5):327-331
58. Jakobsson L, Franco CA, Bentley K, Collins RT, Ponsioen B, Aspalter IM, Rosewell I, Busse M, Thurston G, Medvinsky A, Schulte-Merker S, Gerhardt H (2010) Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 12(10):943-953. doi: 10.1038/ncb2103
59. Sainson RC, Aoto J, Nakatsu MN, Holderfield M, Conn E, Koller E, Hughes CC (2005) Cell-autonomous notch signaling regulates endothelial cell branching and proliferation during vascular tubulogenesis. FASEB J 19(8):1027-1029
60. Eilken HM, Adams RH (2010) Turning on the angiogenic microswitch. Nat Med 16(8):853-854
61. Benedito R, Roca C, Sorensen I, Adams S, Gossler A, Fruttiger M, Adams RH (2009) The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137(6):1124-1135
62. Li Q, Michaud M, Canosa S, Kuo A, Madri JA (2011) GSK-3beta: a signaling pathway node modulating neural stem cell and endothelial cell interactions. Angiogenesis 14(2):173-185
63. Hayashi H, Kume T (2009) Foxc2 transcription factor as a regulator of angiogenesis via induction of integrin beta3 expression. Cell Adhesion Migr 3(1):24-26
64. Jensen LD, Cao Y (2013) Clock controls angiogenesis. Cell Cycle 12(3):405-408
65. Jensen LD, Cao Z, Nakamura M, Yang Y, Brautigam L, Andersson P, Zhang Y, Wahlberg E, Lanne T, Hosaka K, Cao Y (2012) Opposing effects of circadian clock genes bmal1 and period2 in regulation of VEGF-dependent angiogenesis in developing zebrafish. Cell Rep 2(2):231-241
66. Koyanagi S, Kuramoto Y, Nakagawa H, Aramaki H, Ohdo S, Soeda S, Shimeno H (2003) A molecular mechanism regulating circadian expression of vascular endothelial growth factor in tumor cells. Cancer Res 63(21):7277-7283
67. Kageyama R, Niwa Y, Shimojo H (2009) Rhythmic gene expression in somite formation and neural development. Mol Cells 27(5):497-502
68. Oates AC, Morelli LG, Ares S (2012) Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock. Development 139(4):625-639
69. Poulson DF (1937) Chromosomal deficiencies and the embryonic development of Drosophila Melanogaster. Proc Natl Acad Sci USA 23(3):133-137
70. de la Pompa JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, Nakano T, Honjo T, Mak TW, Rossant J, Conlon RA (1997) Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124(6):1139-1148
71. Lutolf S, Radtke F, Aguet M, Suter U, Taylor V (2002) Notch1 is required for neuronal and glial differentiation in the cerebellum. Development 129(2):373-385
72. Yoon K, Nery S, Rutlin ML, Radtke F, Fishell G, Gaiano N (2004) Fibroblast growth factor receptor signaling promotes radial glial identity and interacts with Notch1 signaling in telencephalic progenitors. J Neurosci Off J Soci Neurosci 24(43):9497-9506
73. Yang X, Klein R, Tian X, Cheng HT, Kopan R, Shen J (2004) Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway. Dev Biol 269(1):81-94
74. Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, Nye JS, Conlon RA, Mak TW, Bernstein A, van der Kooy D (2002) Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16(7):846-858
75. Breunig JJ, Silbereis J, Vaccarino FM, Sestan N, Rakic P (2007) Notch regulates cell fate and dendrite morphology of newborn neurons in the postnatal dentate gyrus. Proc Natl Acad Sci USA 104(51):20558-20563
76. Givogri MI, de Planell M, Galbiati F, Superchi D, Gritti A, Vescovi A, de Vellis J, Bongarzone ER (2006) Notch signaling in astrocytes and neuroblasts of the adult subventricular zone in health and after cortical injury. Dev Neurosci 28(1-2):81-91
77. Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R (2010) Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci Off J Soc Neurosci 30(9):3489-3498
78. Irvin DK, Nakano I, Paucar A, Kornblum HI (2004) Patterns of Jagged1, Jagged2, Delta-like 1 and Delta-like 3 expression during late embryonic and postnatal brain development suggest multiple functional roles in progenitors and differentiated cells. J Neurosci Res 75(3):330-343
79. Stump G, Durrer A, Klein AL, Lutolf S, Suter U, Taylor V (2002) Notch1 and its ligands Delta-like and Jagged are expressed and active in distinct cell populations in the postnatal mouse brain. Mech Dev 114(1-2):153-159
80. Ables JL, Decarolis NA, Johnson MA, Rivera PD, Gao Z, Cooper DC, Radtke F, Hsieh J, Eisch AJ (2010) Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci Off J Soci Neurosci 30(31):10484-10492
81. Ehm O, Goritz C, Covic M, Schaffner I, Schwarz TJ, Karaca E, Kempkes B, Kremmer E, Pfrieger FW, Espinosa L, Bigas A, Giachino C, Taylor V, Frisen J, Lie DC (2010) RBPJkappa-dependent signaling is essential for long-term maintenance of neural stem cells in the adult hippocampus. J Neurosci Off J Soc Neurosci 30(41):13794-13807
82. Borghese L, Dolezalova D, Opitz T, Haupt S, Leinhaas A, Steinfarz B, Koch P, Edenhofer F, Hampl A, Brustle O (2010) Inhibition of notch signaling in human embryonic stem cell-derived neural stem cells delays G1/S phase transition and accelerates neuronal differentiation in vitro and in vivo. Stem Cells 28(5):955-964
83. Basak O, Giachino C, Fiorini E, Macdonald HR, Taylor V (2012) Neurogenic subventricular zone stem/progenitor cells are Notch1-dependent in their active but not quiescent state. J Neurosci Off J Soc Neurosci 32(16):5654-5666
84. Shimojo H, Ohtsuka T, Kageyama R (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58(1):52-64
85. Shimojo H, Ohtsuka T, Kageyama R (2011) Dynamic expression of notch signaling genes in neural stem/progenitor cells. Front Neurosci 5:78
86. Nomura T, Goritz C, Catchpole T, Henkemeyer M, Frisen J (2010) EphB signaling controls lineage plasticity of adult neural stem cell niche cells. Cell Stem Cell 7(6):730-743
87. Aguirre A, Rubio ME, Gallo V (2010) Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467(7313):323-327
88. Rash BG, Lim HD, Breunig JJ, Vaccarino FM (2011) FGF signaling expands embryonic cortical surface area by regulating Notch-dependent neurogenesis. J Neurosci Off J Soc Neurosci 31(43):15604-15617
89. Agathocleous M, Iordanova I, Willardsen MI, Xue XY, Vetter ML, Harris WA, Moore KB (2009) A directional Wnt/beta-catenin-Sox2-proneural pathway regulates the transition from proliferation to differentiation in the Xenopus retina. Development 136(19):3289-3299
90. Amoyel M, Cheng YC, Jiang YJ, Wilkinson DG (2005) Wnt1 regulates neurogenesis and mediates lateral inhibition of boundary cell specification in the zebrafish hindbrain. Development 132(4):775-785
91. Hirsch C, Campano LM, Wohrle S, Hecht A (2007) Canonical Wnt signaling transiently stimulates proliferation and enhances neurogenesis in neonatal neural progenitor cultures. Exp Cell Res 313(3):572-587
92. Esteve P, Sandonis A, Cardozo M, Malapeira J, Ibanez C, Crespo I, Marcos S, Gonzalez-Garcia S, Toribio ML, Arribas J, Shimono A, Guerrero I, Bovolenta P (2011) SFRPs act as negative modulators of ADAM10 to regulate retinal neurogenesis. Nat Neurosci 14(5):562-569
93. Hashimoto M, Ishii K, Nakamura Y, Watabe K, Kohsaka S, Akazawa C (2008) Neuroprotective effect of sonic hedgehog up-regulated in Schwann cells following sciatic nerve injury. J Neurochem 107(4):918-927
94. Dave RK, Ellis T, Toumpas MC, Robson JP, Julian E, Adolphe C, Bartlett PF, Cooper HM, Reynolds BA, Wainwright BJ (2011) Sonic hedgehog and notch signaling can cooperate to regulate neurogenic divisions of neocortical progenitors. PLoS ONE 6(2):e14680
95. Borrell V, Cardenas A, Ciceri G, Galceran J, Flames N, Pla R, Nobrega-Pereira S, Garcia-Frigola C, Peregrin S, Zhao Z, Ma L, Tessier-Lavigne M, Marin O (2012) Slit/Robo signaling modulates the proliferation of central nervous system progenitors. Neuron 76(2):338-352
96. Ma S, Kwon HJ, 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
97. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S (2008) Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3(3):289-300
98. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3(3):279-288
99. High FA, Lu MM, Pear WS, Loomes KM, Kaestner KH, Epstein JA (2008) Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development. Proc Natl Acad Sci USA 105(6):1955-1959
100. Popovici C, Isnardon D, Birnbaum D, Roubin R (2002) Caenorhabditis elegans receptors related to mammalian vascular endothelial growth factor receptors are expressed in neural cells. Neurosci Lett 329(1):116-120
101. Procko C, Lu Y, Shaham S (2011) Glia delimit shape changes of sensory neuron receptive endings in C. elegans. Development 138(7):1371-1381
102. Eichmann A, Thomas JL (2013) Molecular parallels between neural and vascular development. Cold Spring Harbor Perspect Med 3(1)
103. Eichmann A, Simons M (2012) VEGF signaling inside vascular endothelial cells and beyond. Curr Opin Cell Biol 24(2):188-193
104. Licht T, Goshen I, Avital A, Kreisel T, Zubedat S, Eavri R, Segal M, Yirmiya R, Keshet E (2011) Reversible modulations of neuronal plasticity by VEGF. Proc Natl Acad Sci USA 108(12):5081-5086
105. Raab S, Plate KH (2007) Different networks, common growth factors: shared growth factors and receptors of the vascular and the nervous system. Acta Neuropathol 113(6):607-626
106. Quaegebeur A, Lange C, Carmeliet P (2011) The neurovascular link in health and disease: molecular mechanisms and therapeutic implications. Neuron 71(3):406-424
107. 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
108. Hogan KA, Bautch VL (2004) Blood vessel patterning at the embryonic midline. Curr Top Dev Biol 62:55-85
109. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 99(18):11946-11950
110. Zhang H, Vutskits L, Pepper MS, Kiss JZ (2003) VEGF is a chemoattractant for FGF-2-stimulated neural progenitors. J Cell Biol 163(6):1375-1384
111. Sun J, Zhou W, Ma D, Yang Y (2010) Endothelial cells promote neural stem cell proliferation and differentiation associated with VEGF activated Notch and Pten signaling. Dev Dyn 239(9):2345-2353
112. Bellon A, Luchino J, Haigh K, Rougon G, Haigh J, Chauvet S, Mann F (2010) VEGFR2 (KDR/Flk1) signaling mediates axon growth in response to semaphorin 3E in the developing brain. Neuron 66(2):205-219
113. Ruiz de Almodovar C, Lambrechts D, Mazzone M, Carmeliet P (2009) Role and therapeutic potential of VEGF in the nervous system. Physiol Rev 89(2):607-648
114. Pajusola K, Aprelikova O, Korhonen J, Kaipainen A, Pertovaara L, Alitalo R, Alitalo K (1992) FLT4 receptor tyrosine kinase contains seven immunoglobulin-like loops and is expressed in multiple human tissues and cell lines. Cancer Res 52(20):5738-5743
115. Wittko-Schneider IM, Schneider FT, Plate KH (2013) Brain homeostasis: VEGF receptor 1 and 2 - two unequal brothers in mind. Cell Mol Life Sci (CMLS this issue)
116. Licht T, Keishet E (2013) Delineating multiple functions of VEGF-A in the adult brain. Cell Mol Life Sci (CMLS this issue)
117. Le Bras B, Barallobre MJ, Homman-Ludiye J, Ny A, Wyns S, Tammela T, Haiko P, Karkkainen MJ, Yuan L, Muriel MP, Chatzopoulou E, Breant C, Zalc B, Carmeliet P, Alitalo K, Eichmann A, Thomas JL (2006) VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nat Neurosci 9(3):340-348
118. Choi JS, Shin YJ, Lee JY, Yun H, Cha JH, Choi JY, Chun MH, Lee MY (2010) Expression of vascular endothelial growth factor receptor-3 mRNA in the rat developing forebrain and retina. J Comp Neurol 518(7):1064-1081
119. Hou Y, Choi JS, Shin YJ, Cha JH, Choi JY, Chun MH, Lee MY (2011) Expression of vascular endothelial growth factor receptor-3 mRNA in the developing rat cerebellum. Cell Mol Neurobiol 31(1):7-16
120. Hou Y, Shin YJ, Han EJ, Choi JS, Park JM, Cha JH, Choi JY, Lee MY (2011) Distribution of vascular endothelial growth factor receptor-3/Flt4 mRNA in adult rat central nervous system. J Chem Neuroanat 42(1):56-64
121. Shin YJ, Choi JS, Lee JY, Choi JY, Cha JH, Chun MH, Lee MY (2008) Differential regulation of vascular endothelial growth factor-C and its receptor in the rat hippocampus following transient forebrain ischemia. Acta Neuropathol 116(5):517-527
122. Calvo CF, Fontaine RH, Soueid J, Tammela T, Makinen T, Alfaro-Cervello C, Bonnaud F, Miguez A, Benhaim L, Xu Y, Barallobre MJ, Moutkine I, Lyytikka J, Tatlisumak T, Pytowski B, Zalc B, Richardson W, Kessaris N, Garcia-Verdugo JM, Alitalo K, Eichmann A, Thomas JL (2011) Vascular endothelial growth factor receptor 3 directly regulates murine neurogenesis. Genes Dev 25(8):831-844
123. Haiko P, Makinen T, Keskitalo S, Taipale J, Karkkainen MJ, Baldwin ME, Stacker SA, Achen MG, Alitalo K (2008) Deletion of vascular endothelial growth factor C (VEGF-C) and VEGF-D is not equivalent to VEGF receptor 3 deletion in mouse embryos. Mol Cell Biol 28(15):4843-4850
124. Samuels BA, Hen R (2011) Neurogenesis and affective disorders. Eur J Neurosci 33(6):1152-1159
125. Schmidt HD, Duman RS (2007) The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav Pharmacol 18(5-6):391-418
126. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132(4):645-660
127. Mauceri D, Freitag HE, Oliveira AM, Bengtson CP, Bading H (2011) Nuclear calcium-VEGFD signaling controls maintenance of dendrite arborization necessary for memory formation. Neuron 71(1):117-130
128. Shen Q, Goderie SK, 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
129. Hashimoto T, Zhang XM, Chen BY, Yang XJ (2006) VEGF activates divergent intracellular signaling components to regulate retinal progenitor cell proliferation and neuronal differentiation. Development 133(11):2201-2210
130. De Schaepdrijver L, Simoens P, Lauwers H, De Geest JP (1989) Retinal vascular patterns in domestic animals. Res Vet Sci 47(1):34-42
131. Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N (2005) Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19(9):1028-1033