Guidance from above: common cues direct distinct signaling outcomes in vascular and neural patterning

Trends in Cell Biology

Volumn 19, Issue 3, 2009, Pages 99-110

  Gelfand, Maria V ^a   Hong, Shangyu ^a   Gu, Chenghua ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN; SEMAPHORIN; VASCULOTROPIN;

ASSOCIATION; BRAIN NERVE CELL; CARDIOVASCULAR SYSTEM; COMPREHENSION; CYTOSKELETON; ENDOTHELIUM CELL; HUMAN; NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

ANIMALS; BLOOD VESSELS; CUES; ENDOTHELIUM, VASCULAR; HUMANS; NEURONS; SIGNAL TRANSDUCTION;

EID: 61449237318     PISSN: 09628924     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tcb.2009.01.001     Document Type: Review

References (92)

1. Carmeliet P., and Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature 436 (2005) 193-200
2. Gerhardt H., et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161 (2003) 1163-1177
3. Freitas C., et al. Netrins and UNC5 receptors in angiogenesis. Angiogenesis 11 (2008) 23-29
4. Legg J.A., et al. Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 11 (2008) 13-21
5. Jones C.A., and Li D.Y. Common cues regulate neural and vascular patterning. Curr. Opin. Genet. Dev. 17 (2007) 332-336
6. Suchting S., et al. Neuronal clues to vascular guidance. Exp. Cell Res. 312 (2006) 668-675
7. Tran T.S., et al. Semaphorin regulation of cellular morphology. Annu. Rev. Cell Dev. Biol. 23 (2007) 263-292
8. Oinuma I., et al. The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 305 (2004) 862-865
9. Oinuma I., et al. Molecular dissection of the semaphorin 4D receptor plexin-B1-stimulated R-Ras GTPase-activating protein activity and neurite remodeling in hippocampal neurons. J. Neurosci. 24 (2004) 11473-11480
10. Ito Y., et al. Sema4D/plexin-B1 activates GSK-3β through R-Ras GAP activity, inducing growth cone collapse. EMBO Rep. 7 (2006) 704-709
11. Fazzari P., et al. Plexin-B1 plays a redundant role during mouse development and in tumour angiogenesis. BMC Dev. Biol. 7 (2007) 55
12. Basile J.R., et al. Class IV semaphorins promote angiogenesis by stimulating Rho-initiated pathways through plexin-B. Cancer Res. 64 (2004) 5212-5224
13. Basile J.R., et al. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 9017-9022
14. Sierra J.R., et al. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumor-associated macrophages. J. Exp. Med. 205 (2008) 1673-1685
15. Vikis H.G., et al. The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 12457-12462
16. Vikis H.G., et al. The plexin-B1/Rac interaction inhibits PAK activation and enhances Sema4D ligand binding. Genes Dev. 16 (2002) 836-845
17. Swiercz J.M., et al. Plexin-B1/RhoGEF-mediated RhoA activation involves the receptor tyrosine kinase ErbB-2. J. Cell Biol. 165 (2004) 869-880
18. Basile J.R., et al. Plexin-B1 utilizes RhoA and Rho kinase to promote the integrin-dependent activation of Akt and ERK and endothelial cell motility. J. Biol. Chem. 282 (2007) 34888-34895
19. Fukata Y., et al. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4 (2002) 583-591
20. Toyofuku T., et al. FARP2 triggers signals for Sema3A-mediated axonal repulsion. Nat. Neurosci. 8 (2005) 1712-1719
21. Eickholt B.J., et al. An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J. Cell Biol. 157 (2002) 211-217
22. Gallo G. Semaphorin 3A inhibits ERM protein phosphorylation in growth cone filopodia through inactivation of PI3K. Dev. Neurobiol. 68 (2008) 926-933
23. Orlova I., et al. Regulation of actomyosin contractility by PI3K in sensory axons. Dev. Neurobiol. 67 (2007) 1843-1851
24. Chadborn N.H., et al. PTEN couples Sema3A signalling to growth cone collapse. J. Cell Sci. 119 (2006) 951-957
25. Sasaki Y., et al. Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35 (2002) 907-920
26. Uchida Y., et al. Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10 (2005) 165-179
27. Mitsui N., et al. Involvement of Fes/Fps tyrosine kinase in semaphorin3A signaling. EMBO J. 21 (2002) 3274-3285
28. Shapovalova Z., et al. The Fer tyrosine kinase regulates an axon retraction response to Semaphorin 3A in dorsal root ganglion neurons. BMC Dev. Biol. 7 (2007) 133
29. Acevedo L.M., et al. Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 111 (2008) 2674-2680
30. Miao H.Q., et al. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J. Cell Biol. 146 (1999) 233-242
31. Serini G., et al. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424 (2003) 391-397
32. Shoji W., et al. Semaphorin3a1 regulates angioblast migration and vascular development in zebrafish embryos. Development 130 (2003) 3227-3236
33. Torres-Vazquez J., et al. Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev. Cell 7 (2004) 117-123
34. Herzog Y., et al. Segregation of arterial and venous markers in subpopulations of blood islands before vessel formation. Dev. Dyn. 232 (2005) 1047-1055
35. Soker S., et al. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92 (1998) 735-745
36. Gu C., et al. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell 5 (2003) 45-57
37. Vieira J.M., et al. Selective requirements for NRP1 ligands during neurovascular patterning. Development 134 (2007) 1833-1843
38. Appleton B.A., et al. Structural studies of neuropilin/antibody complexes provide insights into semaphorin and VEGF binding. EMBO J. 26 (2007) 4902-4912
39. Pan Q., et al. Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J. Biol. Chem. 282 (2007) 24049-24056
40. Gu C., et al. Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 307 (2005) 265-268
41. Chauvet S., et al. Gating of Sema3E/PlexinD1 signaling by neuropilin-1 switches axonal repulsion to attraction during brain development. Neuron 56 (2007) 807-822
42. Bielenberg D.R., and Klagsbrun M. Targeting endothelial and tumor cells with semaphorins. Cancer Metastasis Rev. 26 (2007) 421-431
43. Neufeld G., and Kessler O. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat. Rev. Cancer 8 (2008) 632-645
44. Himanen J.P., et al. Cell-cell signaling via Eph receptors and ephrins. Curr. Opin. Cell Biol. 19 (2007) 534-542
45. Rashid T., et al. Opposing gradients of ephrin-As and EphA7 in the superior colliculus are essential for topographic mapping in the mammalian visual system. Neuron 47 (2005) 57-69
46. Ogawa K., et al. The ephrin-A1 ligand and its receptor, EphA2, are expressed during tumor neovascularization. Oncogene 19 (2000) 6043-6052
47. Yamashita T., et al. Hypoxia-inducible transcription factor-2α in endothelial cells regulates tumor neovascularization through activation of ephrin A1. J. Biol. Chem. 283 (2008) 18926-18936
48. Richter M., et al. The EphA4 receptor regulates neuronal morphology through SPAR-mediated inactivation of Rap GTPases. J. Neurosci. 27 (2007) 14205-14215
49. Beg A.A., et al. alpha2-Chimaerin is an essential EphA4 effector in the assembly of neuronal locomotor circuits. Neuron 55 (2007) 768-778
50. Wegmeyer H., et al. EphA4-dependent axon guidance is mediated by the RacGAP α2-chimaerin. Neuron 55 (2007) 756-767
51. Iwasato T., et al. Rac-GAP α-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 130 (2007) 742-753
52. Cowan C.W., et al. Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron 46 (2005) 205-217
53. Shamah S.M., et al. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105 (2001) 233-244
54. Fu W.Y., et al. Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 10 (2007) 67-76
55. Zhou L., et al. EphA4 signaling regulates phospholipase Cγ1 activation, cofilin membrane association, and dendritic spine morphology. J. Neurosci. 27 (2007) 5127-5138
56. Lim Y.S., et al. p75(NTR) mediates ephrin-A reverse signaling required for axon repulsion and mapping. Neuron 59 (2008) 746-758
57. Schubert V., and Dotti C.G. Transmitting on actin: synaptic control of dendritic architecture. J. Cell Sci. 120 (2007) 205-212
58. Takasu M.A., et al. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295 (2002) 491-495
59. Hoogenraad C.C., et al. GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat. Neurosci. 8 (2005) 906-915
60. Reber M., et al. Eph receptors and ephrin ligands in axon guidance. Adv. Exp. Med. Biol. 621 (2007) 32-49
61. Lamont R.E., and Childs S. MAPping out arteries and veins. Sci. STKE 2006 (2006) pe39
62. Tolias K.F., et al. The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 7265-7270
63. Penzes P., et al. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37 (2003) 263-274
64. Moeller M.L., et al. EphB receptors regulate dendritic spine morphogenesis through the recruitment/phosphorylation of focal adhesion kinase and RhoA activation. J. Biol. Chem. 281 (2006) 1587-1598
65. Groeger G., and Nobes C.D. Co-operative Cdc42 and Rho signalling mediates ephrinB-triggered endothelial cell retraction. Biochem. J. 404 (2007) 23-29
66. Aoto J., et al. Postsynaptic ephrinB3 promotes shaft glutamatergic synapse formation. J. Neurosci. 27 (2007) 7508-7519
67. Segura I., et al. Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat. Neurosci. 10 (2007) 301-310
68. Cowan C.A., and Henkemeyer M. The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413 (2001) 174-179
69. Georgakopoulos A., et al. Metalloproteinase/Presenilin1 processing of ephrinB regulates EphB-induced Src phosphorylation and signaling. EMBO J. 25 (2006) 1242-1252
70. Cowan C.A., and Henkemeyer M. Ephrins in reverse, park and drive. Trends Cell Biol. 12 (2002) 339-346
71. Salvucci O., et al. EphB2 and EphB4 receptors forward signaling promotes SDF-1-induced endothelial cell chemotaxis and branching remodeling. Blood 108 (2006) 2914-2922
72. Lee S., et al. Autocrine VEGF signaling is required for vascular homeostasis. Cell 130 (2007) 691-703
73. Rosenstein J.M. VEGF in the nervous system. In: Ruhrberg C. (Ed). VEGF in Development (2008), Landes Bioscience 118
74. Sakurai Y., et al. Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 1076-1081
75. Kitamura T., et al. Regulation of VEGF-mediated angiogenesis by the Akt/PKB substrate Girdin. Nat. Cell Biol. 10 (2008) 329-337
76. Taylor C.J., et al. Protein kinase C and downstream signaling pathways in a three-dimensional model of phorbol ester-induced angiogenesis. Angiogenesis 9 (2006) 39-51
77. Olsson A.K., et al. VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7 (2006) 359-371
78. Storkebaum E., et al. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat. Neurosci. 8 (2005) 85-92
79. Tolosa L., et al. Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase. J. Neurochem. 105 (2008) 1080-1090
80. Kilic U., et al. Human vascular endothelial growth factor protects axotomized retinal ganglion cells in vivo by activating ERK-1/2 and Akt pathways. J. Neurosci. 26 (2006) 12439-12446
81. Zhu Y., et al. Vascular endothelial growth factor promotes proliferation of cortical neuron precursors by regulating E2F expression. FASEB J. 17 (2003) 186-193
82. Salikhova A., et al. Vascular endothelial growth factor and semaphorin induce neuropilin-1 endocytosis via separate pathways. Circ. Res. 103 (2008) e71-e79
83. Wang L., et al. Neuropilin-1 modulates p53/caspases axis to promote endothelial cell survival. PLoS One 2 (2007) e1161
84. Pan Q., et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 11 (2007) 53-67
85. Kawamura H., et al. Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood 112 (2008) 3638-3649
86. Wang L., et al. Neuropilin-1-mediated vascular permeability factor/vascular endothelial growth factor-dependent endothelial cell migration. J. Biol. Chem. 278 (2003) 48848-48860
87. Toyofuku T., et al. 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. 18 (2004) 435-447
88. Gallo G., and Letourneau P.C. Regulation of growth cone actin filaments by guidance cues. J. Neurobiol. 58 (2004) 92-102
89. Lu X., et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432 (2004) 179-186
90. Lamalice L., et al. Endothelial cell migration during angiogenesis. Circ. Res. 100 (2007) 782-794
91. Pasquale E.B. Eph-ephrin bidirectional signaling in physiology and disease. Cell 133 (2008) 38-52
92. Siekmann A.F., et al. Modulation of VEGF signalling output by the Notch pathway. Bioessays 30 (2008) 303-313