VEGF Signaling through Neuropilin 1 Guides Commissural Axon Crossing at the Optic Chiasm

Neuron

Volumn 70, Issue 5, 2011, Pages 951-965

  Erskine, Lynda ^a   Reijntjes, Susan ^a   Pratt, Thomas ^b   Denti, Laura ^c   Schwarz, Quenten ^c,d   Vieira, Joaquim M ^c,e   Alakakone, Bennett ^c   Shewan, Derryck ^a   Ruhrberg, Christiana ^c  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d CENTRE FOR CANCER BIOLOGY   (Australia)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPILIN 1; SEMAPHORIN 3A; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN 164; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GROWTH CONE; MOUSE; NERVE FIBER; NONHUMAN; OPTIC CHIASM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; RETINA GANGLION CELL; SIGNAL TRANSDUCTION;

AGE FACTORS; AMINO ACIDS; ANIMALS; AXONS; EMBRYO, MAMMALIAN; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH CONES; INDOLES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPILIN-1; NEUROPILIN-2; OPTIC CHIASM; ORGAN CULTURE TECHNIQUES; RETINA; RETINAL GANGLION CELLS; SEMAPHORIN-3A; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 79958044393     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.02.052     Document Type: Article

References (61)

1. Adams R.H., Eichmann A. Axon guidance molecules in vascular patterning. Cold Spring Harb. Perspect. Biol. 2010, 2:a001875.
2. Böcker-Meffert S., Rosenstiel P., Röhl C., Warneke N., Held-Feindt J., Sievers J., Lucius R. Erythropoietin and VEGF promote neural outgrowth from retinal explants in postnatal rats. Invest. Ophthalmol. Vis. Sci. 2002, 43:2021-2026.
3. Carmeliet P. Blood vessels and nerves: common signals, pathways and diseases. Nat. Rev. Genet. 2003, 4:710-720.
4. Charron F., Stein E., Jeong J., McMahon A.P., Tessier-Lavigne M. The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 2003, 113:11-23.
5. Claudepierre T., Koncina E., Pfrieger F.W., Bagnard D., Aunis D., Reber M. Implication of neuropilin 2/semaphorin 3F in retinocollicular map formation. Dev. Dyn. 2008, 237:3394-3403.
6. Deiner M.S., Sretavan D.W. Altered midline axon pathways and ectopic neurons in the developing hypothalamus of netrin-1- and DCC-deficient mice. J. Neurosci. 1999, 19:9900-9912.
7. Erskine L., Herrera E. The retinal ganglion cell axon's journey: insights into molecular mechanisms of axon guidance. Dev. Biol. 2007, 308:1-14.
8. Erskine L., Williams S.E., Brose K., Kidd T., Rachel R.A., Goodman C.S., Tessier-Lavigne M., Mason C.A. Retinal ganglion cell axon guidance in the mouse optic chiasm: expression and function of robos and slits. J. Neurosci. 2000, 20:4975-4982.
9. Falk J., Bechara A., Fiore R., Nawabi H., Zhou H., Hoyo-Becerra C., Bozon M., Rougon G., Grumet M., Püschel A.W., et al. Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 2005, 48:63-75.
10. Fantin A., Vieira J.M., Gestri G., Denti L., Schwarz Q., Prykhozhij S., Peri F., Wilson S.W., Ruhrberg C. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010, 116:829-840.
11. Gariano R.F., Hu D., Helms J. Expression of angiogenesis-related genes during retinal development. Gene Expr. Patterns 2006, 6:187-192.
12. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., Jeltsch M., Mitchell C., Alitalo K., Shima D., Betsholt C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 2003, 161:1163-1177.
13. 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.
14. Gitay-Goren H., Cohen T., Tessler S., Soker S., Gengrinovitch S., Rockwell P., Klagsbrun M., Levi B.Z., Neufeld G. Selective binding of VEGF121 to one of the three vascular endothelial growth factor receptors of vascular endothelial cells. J. Biol. Chem. 1996, 271:5519-5523.
15. Godement P., Vanselow J., Thanos S., Bonhoeffer F. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 1987, 101:697-713.
16. Godement P., Wang L.C., Mason C.A. Retinal axon divergence in the optic chiasm: dynamics of growth cone behavior at the midline. J. Neurosci. 1994, 14:7024-7039.
17. Gu C., Rodriguez E.R., Reimert D.V., Shu T., Fritzsch B., Richards L.J., Kolodkin A.L., Ginty D.D. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell 2003, 5:45-57.
18. Hashimoto T., Zhang X.M., Chen B.Y., Yang X.J. VEGF activates divergent intracellular signaling components to regulate retinal progenitor cell proliferation and neuronal differentiation. Development 2006, 133:2201-2210.
19. Herrera E., Brown L., Aruga J., Rachel R.A., Dolen G., Mikoshiba K., Brown S., Mason C.A. Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 2003, 114:545-557.
20. Kawakami A., Kitsukawa T., Takagi S., Fujisawa H. Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J. Neurobiol. 1996, 29:1-17.
21. Kawasaki T., Kitsukawa T., Bekku Y., Matsuda Y., Sanbo M., Yagi T., Fujisawa H. A requirement for neuropilin-1 in embryonic vessel formation. Development 1999, 126:4895-4902.
22. Lohof A.M., Quillan M., Dan Y., Poo M.M. Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. J. Neurosci. 1992, 12:1253-1261.
23. Manuel M., Pratt T., Liu M., Jeffery G., Price D.J. Overexpression of Pax6 results in microphthalmia, retinal dysplasia and defective retinal ganglion cell axon guidance. BMC Dev. Biol. 2008, 8:59.
24. Marcus R.C., Blazeski R., Godement P., Mason C.A. Retinal axon divergence in the optic chiasm: uncrossed axons diverge from crossed axons within a midline glial specialization. J. Neurosci. 1995, 15:3716-3729.
25. Marcus R.C., Shimamura K., Sretavan D., Lai E., Rubenstein J.L., Mason C.A. Domains of regulatory gene expression and the developing optic chiasm: correspondence with retinal axon paths and candidate signaling cells. J. Comp. Neurol. 1999, 403:346-358.
26. Marneros A.G., Fan J., Yokoyama Y., Gerber H.P., Ferrara N., Crouch R.K., Olsen B.R. Vascular endothelial growth factor expression in the retinal pigment epithelium is essential for choriocapillaris development and visual function. Am. J. Pathol. 2005, 167:1451-1459.
27. Mason C.A., Wang L.C. Growth cone form is behavior-specific and, consequently, position-specific along the retinal axon pathway. J. Neurosci. 1997, 17:1086-1100.
28. Murray A.J., Shewan D.A. Epac mediates cyclic AMP-dependent axon growth, guidance and regeneration. Mol. Cell. Neurosci. 2008, 38:578-588.
29. Nakagawa S., Brennan C., Johnson K.G., Shewan D., Harris W.A., Holt C.E. Ephrin-B regulates the Ipsilateral routing of retinal axons at the optic chiasm. Neuron 2000, 25:599-610.
30. Nawabi H., Briançon-Marjollet A., Clark C., Sanyas I., Takamatsu H., Okuno T., Kumanogoh A., Bozon M., Takeshima K., Yoshida Y., et al. A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev. 2010, 24:396-410.
31. Petros T.J., Rebsam A., Mason C.A. Retinal axon growth at the optic chiasm: to cross or not to cross. Annu. Rev. Neurosci. 2008, 31:295-315.
32. Pinter R., Hindges R. Perturbations of microRNA function in mouse dicer mutants produce retinal defects and lead to aberrant axon pathfinding at the optic chiasm. PLoS ONE 2010, 5:e10021.
33. Plump A.S., Erskine L., Sabatier C., Brose K., Epstein C.J., Goodman C.S., Mason C.A., Tessier-Lavigne M. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 2002, 33:219-232.
34. Robinson G.S., Ju M., Shih S.C., Xu X., McMahon G., Caldwell R.B., Smith L.E. Nonvascular role for VEGF: VEGFR-1, 2 activity is critical for neural retinal development. FASEB J. 2001, 15:1215-1217.
35. 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.
36. Ruiz de Almodovar C., Lambrechts D., Mazzone M., Carmeliet P. Role and therapeutic potential of VEGF in the nervous system. Physiol. Rev. 2009, 89:607-648.
37. Sabatier C., Plump A.S., Ma Le, Brose K., Tamada A., Murakami F., Lee E.Y., Tessier-Lavigne M. The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 2004, 117:157-169.
38. Saint-Geniez M., Maldonado A.E., D'Amore P.A. VEGF expression and receptor activation in the choroid during development and in the adult. Invest. Ophthalmol. Vis. Sci. 2006, 47:3135-3142.
39. Sakai J.A., Halloran M.C. Semaphorin 3d guides laterality of retinal ganglion cell projections in zebrafish. Development 2006, 133:1035-1044.
40. Sánchez-Camacho C., Bovolenta P. Autonomous and non-autonomous Shh signalling mediate the in vivo growth and guidance of mouse retinal ganglion cell axons. Development 2008, 135:3531-3541.
41. Schwarz Q., Ruhrberg C. Neuropilin, you gotta let me know: should I stay or should I go?. Cell Adh. Migr. 2010, 4:61-66.
42. Schwarz Q., Gu C., Fujisawa H., Sabelko K., Gertsenstein M., Nagy A., Taniguchi M., Kolodkin A.L., Ginty D.D., Shima D.T., Ruhrberg C. Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve. Genes Dev. 2004, 18:2822-2834.
43. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., Tessier-Lavigne M. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 1996, 87:1001-1014.
44. Seth A., Culverwell J., Walkowicz M., Toro S., Rick J.M., Neuhauss S.C., Varga Z.M., Karlstrom R.O. belladonna/(lhx2) is required for neural patterning and midline axon guidance in the zebrafish forebrain. Development 2006, 133:725-735.
45. Shirasaki R., Katsumata R., Murakami F. Change in chemoattractant responsiveness of developing axons at an intermediate target. Science 1998, 279:105-107.
46. Soker S., Fidder H., Neufeld G., Klagsbrun M. Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain. J. Biol. Chem. 1996, 271:5761-5767.
47. 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.
48. Sretavan D.W., Puré E., Siegel M.W., Reichardt L.F. Disruption of retinal axon ingrowth by ablation of embryonic mouse optic chiasm neurons. Science 1995, 269:98-101.
49. Taniguchi M., Yuasa S., Fujisawa H., Naruse I., Saga S., Mishina M., Yagi T. Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 1997, 19:519-530.
50. Tessier-Lavigne M., Placzek M., Lumsden A.G., Dodd J., Jessell T.M. Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 1988, 336:775-778.
51. Thompson H., Barker D., Camand O., Erskine L. Slits contribute to the guidance of retinal ganglion cell axons in the mammalian optic tract. Dev. Biol. 2006, 296:476-484.
52. Thompson H., Camand O., Barker D., Erskine L. Slit proteins regulate distinct aspects of retinal ganglion cell axon guidance within dorsal and ventral retina. J. Neurosci. 2006, 26:8082-8091.
53. Tian N.M., Pratt T., Price D.J. Foxg1 regulates retinal axon pathfinding by repressing an ipsilateral program in nasal retina and by causing optic chiasm cells to exert a net axonal growth-promoting activity. Development 2008, 135:4081-4089.
54. Traver D., Zon L.I. Walking the walk: migration and other common themes in blood and vascular development. Cell 2002, 108:731-734.
55. Trousse F., Martí E., Gruss P., Torres M., Bovolenta P. Control of retinal ganglion cell axon growth: a new role for Sonic hedgehog. Development 2001, 128:3927-3936.
56. Wang L.C., Dani J., Godement P., Marcus R.C., Mason C.A. Crossed and uncrossed retinal axons respond differently to cells of the optic chiasm midline in vitro. Neuron 1995, 15:1349-1364.
57. Wang L.C., Rachel R.A., Marcus R.C., Mason C.A. Chemosuppression of retinal axon growth by the mouse optic chiasm. Neuron 1996, 17:849-862.
58. Williams S.E., Mann F., Erskine L., Sakurai T., Wei S., Rossi D.J., Gale N.W., Holt C.E., Mason C.A., Henkemeyer M. Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 2003, 39:919-935.
59. Williams S.E., Grumet M., Colman D.R., Henkemeyer M., Mason C.A., Sakurai T. A role for Nr-CAM in the patterning of binocular visual pathways. Neuron 2006, 50:535-547.
60. Xiang M., Zhou L., Macke J.P., Yoshioka T., Hendry S.H.C., Eddy R.L., Shows T.B., Nathans J. The Brn-3 family of POU-domain factors: primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. J. Neurosci. 1995, 15:4762-4785.
61. Zhou X., Jeker L.T., Fife B.T., Zhu S., Anderson M.S., McManus M.T., Bluestone J.A. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 2008, 205:1983-1991.