Vascular endothelial growth factor controls neuronal migration and cooperates with SemaSA to pattern distinct compartments of the facial nerve

Genes and Development

Volumn 18, Issue 22, 2004, Pages 2822-2834

  Schwarz, Quenten ^a   Gu, Chenghua ^b   Fujisawa, Hajime ^c   Sabelko, Kimberly ^d   Gertsenstein, Marina ^e   Nagy, Andras ^e   Taniguchi, Masahiko ^f   Kolodkin, Alex L ^b   Ginty, David D ^b   Shima, David T ^g   Ruhrberg, Christiana ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NAGOYA UNIVERSITY   (Japan)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e MOUNT SINAI HOSPITAL   (Canada)

^f UNIVERSITY OF TOKYO   (Japan)

^g Eyetech Pharmaceuticals Inc   (United States)

Author keywords

Axon guidance; Neuronal migration; Neuropilin; Semaphorins; VEGF

Indexed keywords

LIGAND; MEMBRANE RECEPTOR; NEUROPILIN 1; SEMAPHORIN 3A; VASCULOTROPIN;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; FACIAL NERVE; MOTONEURON; MOUSE; MUTANT; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANIMALS; AXONS; BODY PATTERNING; CELL COMPARTMENTATION; CELL MOVEMENT; FACIAL NERVE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIGANDS; MALE; MICE; MICE, KNOCKOUT; NEURONS; NEUROPILIN-1; PROTEIN ISOFORMS; RHOMBENCEPHALON; SEMAPHORIN-3A; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA; STAPHYLOCOCCUS PHAGE 3A;

EID: 8644219642     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.322904     Document Type: Article

References (58)

1. Altman, J. and Bayer, S.A. 1982. Development of the cranial nerve ganglia and related nuclei in the rat. Adv. Anat. Embryol. Cell Biol. 74: 1-90.
2. Auclair, F., Valdes, N., and Marchand, R. 1996. Rhombomere-specific origin of branchial and visceral motoneurons of the facial nerve in the rat embryo. J. Comp. Neurol. 369: 451-461.
3. Bagnard, D., Vaillant, C., Khuth, S.T., Dufay, N., Lohrum, M., Puschel, A.W., Belin, M.F., BoIz, J., and Thomasset, N. 2001. Semaphorin 3A-vascular endothelial growth factor-165 balance mediates migration and apoptosis of neural progenitor cells by the recruitment of shared receptor. J. Neurosci. 21:3332-3341.
4. Bingham, S., Higashijima, S., Okamoto, H., and Chandrasekhar, A. 2002. The zebrafish trilobite gene is essential for tangential migration of branchiomotor neurons. Dev. Biol. 242: 149-160.
5. Bloch-Gallego, E., Ezan, F., Tessier-Lavigne, M., and Sotelo, C. 1999. Floor plate and netrin-1 are involved in the migration and survival of inferior olivary neurons. J. Neurosci. 19: 4407-4420.
6. Breier, G., Albrecht, U., Sterrer, S., and Risau, W. 1992. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114: 521-532.
7. Carmeliet, P. 2003. Blood vessels and nerves: Common signals, pathways and diseases. Nat. Rev. Genet. 4: 710-720.
8. Carmeliet, P., Ng, Y.S., Nuyens, D., Theilmeier, G., Brusselmans, K., Cornelissen, I., Ehler, E., Kakkar, V.V., Stalmans, I., Mattot, V., et al. 1999. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nat. Med. 5: 495-502.
9. Castellani, V. and Rougon, G. 2002. Control of semaphorin signaling. Curr. Opin. Neurobiol 12: 532-541.
10. Cordes, S. P. 2001. Molecular genetics of cranial nerve development in mouse. Nat. Rev. Neurosci. 2: 611-623.
11. Davenne, M., Maconochie, M.K., Neun, R., Pattyn, A., Chambon, P., Krumlauf, R., and Rijli, P.M. 1999. Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22: 677-691.
12. Dickson, B.J. 2002. Molecular mechanisms of axon guidance. Science 298: 1959-1964.
13. Ericson, J., Thor, S., Edlund, T., Jessell, T.M., and Yamada, T. 1992. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256: 1555-1560.
14. Feiner, L., Webber, A.L., Brown, C.B., Lu, M.M., Jia, L., Feinstein, P., Mombaerts, P., Epstein, J.A., and Raper, J.A. 2001. Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development 128: 3061-3070.
15. Feng, Y. and Walsh, C.A. 2001. Protein-protein interactions, cytoskeletal regulation and neuronal migration. Nat. Rev. Neurosci. 2: 408-416.
16. Gavalas, A., Ruhrberg, C., Livet, J., Henderson, C.E., and Krumlauf, R. 2003. Neuronal defects in the hindbrain of Hoxal, Hoxb1 and Hoxb2 mutants reflect regulatory interactions among these Hox genes. Development 130: 5663-5679.
17. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D., et al. 2003. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161: 1163-1177.
18. Gluzman-Poltorak, Z., Cohen, T., Herzog, Y., and Neufeld, G. 2000. Neuropilin-2 is a receptor for the vascular endothelial growth factor (VEGF) forms VEGF-145 and VEGF-165. J. Biol. Chem. 275: 18040-18045.
19. Gu, C., Limberg, B.J., Whitaker, G.B., Perman, B., Leahy, D.J., Rosenbaum, J.S., Ginty, D.D., and Kolodkin, A.L. 2002. Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165. J. Biol Chem. 277: 18069-18076.
20. Gu, C., Rodriguez, E.R., Reimert, D.V., Shu, T., Fritzsch, B., Richards, L.J., Kolodkin, A.L., and Ginty, D.D. 2003. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell 5: 45-57.
21. Hafezparast, M., Klocke, R., Ruhrberg, C., Marquardt, A., Ahmad-Annuar, A., Bowen, S., Lalli, G., Witherden, A.S., Hummerich, H., Nicholson, S., et al. 2003. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300: 808-812.
22. Haigh, J.J., Morelli, P.I., Gerhardt, H., Haigh, K., Tsien, J., Damert, A., Miquerol, L., Muhlner, U., Klein, R., Ferrara, N., et al. 2003. Cortical and retinal defects caused by dosage-dependent reductions in VEGF-A paracrine signaling. Dev. Biol 262: 225-241.
23. Harris, W.A., Holt, C.E., and Bonhoeffer, F. 1987. Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: A time-lapse video study of single fibres in vivo. Development 101: 123-133.
24. He, Z. and Tessier-Lavigne, M. 1997. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90: 739-751.
25. Kawakami, A., Kitsukawa, T., Takagi, S., and Fujisawa, H. 1996. Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J. Neurobiol. 29: 1-17.
26. Kawasaki, T., Kitsukawa, T., Bekku, Y., Matsuda, Y., Sanbo, M., Yagi, T., and Fujisawa, H. 1999. A requirement for neuropi0in-1 in embryonic vessel formation. Development 126: 4895-4902.
27. Kitsukawa, T., Shimizu, M., Sanbo, M., Hirata, T., Taniguchi, M., Bekku, Y., Yagi, T., and Fujisawa, H. 1997. Neuropilinsemaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19: 995-1005.
28. Kolodkin, A.L., Levcngood, D.V., Rowe, E.G., Tai, Y.T., Giger, R.J., and Ginty, D.D. 1997. Neuropilin is a semaphorin III receptor. Cell 90: 753-762.
29. Lambrechts, D., Storkebaum, E., Morimoto, M., Del-Favero, J., Desmet, F., Marklund, S.L., Wyns, S., Thijs, V., Andersson, J., van Marion, L, et al. 2003. VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat. Genet. 34: 383-394.
30. Levy, A.P., Levy, M.S., Wegner, S., and Goldberg, M.A. 1995. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J. Biol. Chem. 270: 13333-13340.
31. Maina, F., Hilton, M.C., Ponzetto, C., Davies, A.M., and Klein, R. 1997. Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. Genes & Dev. 11: 3341-3350.
32. Mamluk, R., Gechtman, Z., Kutcher, M.E., Gasiunas, N., Gallagher, J., and Klagsbrun, M. 2002. Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain. J. Biol. Chem. 277: 24818-24825.
33. Marin, O. and Rubenstein, J.L. 2003. Cell migration in the forebrain. Annu. Rev. Neurosci. 26: 441-83.
34. Marin, O., Yaron, A , Bagri, A., Tessier-Lavigne, M., and Ruben-stein, J.L. 2001. Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science 293: 872-875.
35. Miao, H.Q., Soker, S., Feiner, L., Alonso, J.L., Raper, J.A., and Klagsbrun, M. 1999. 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: 233-242.
36. Miquerol, L., Gertsenstein, M., Harpal, K., Rossant, J., and Nagy, A. 1999. Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev. Biol. 212: 307-322.
37. Ohshima, T. and Mikoshiba, K. 2002. Reelin signaling and Cdk5 in the control of neuronal positioning. Mol. Neurobiol. 26: 153-166.
38. Ohshima, T., Ogawa, M., Takeuchi, K., Takahashi, S., Kulkarni, A.B., and Mikoshiba, K. 2002. Cyclin-dependent kinase 5/p35 contributes synergistically with Reelin/Dab1 to the positioning of facial branchiomotor and inferior olive neurons in the developing mouse hindbrain. J. Neurosci. 22: 4036-4044.
39. Oosthuyse, B., Moons, L., Storkebaum, E., Beck, H., Nuyens, D., Brusselmans, K., Van Dorpe, J., Hellings, P., Gorselink, M., Heymans, S., et al. 2001. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat. Genet. 28: 131-138.
40. Pattyn, A., Hirsch, M., Goridis, C, and Brunei, J.F. 2000. Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 127: 1349-1358.
41. Raper, J.A. 2000. Semaphorins and their receptors in vertebrates and invertebrates. Curr. Opin. Neurobiol. 10: 88-94.
42. Rice, D.S. and Curran, T. 2001. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24: 1005-1039.
43. Riddle, R.D., Johnson, R.L., Laufer, E., and Tabin, C. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401-1416.
44. Ruhrberg, C. 2003. Growing and shaping the vascular tree: Multiple roles for VEGF. Bioessays 25: 1052-1060.
45. Ruhrberg, C., Gerhardt, H., Golding, M., Watson, R., Ioannidou, S., Fujisawa, H., Betsholtz, C., and Shima, D.T. 2002. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes & Dev. 16: 2684-2698.
46. Sasaki, Y., Cheng, C., Uchida, Y., Nakajima, O., Ohshima, T., Yagi, T., Taniguchi, M., Nakayama, T., Kishida, R., Kudo, Y., et al. 2002. Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35: 907-920.
47. Soker, S., Takashima, S., Miao, H.Q., Neufeld, G., and Klagsbrun, M. 1998. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92: 735-745.
48. Stalmans, I., Ng, Y.S., Rohan, R., Fruttiger, M., Bouche, A., Yuce, A., Fujisawa, H., Hermans, B., Shani, M., Jansen, S., et al. 2002. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109:327-336.
49. Studer, M., Lumsden, A., Ariza-McNaughton, L., Bradley, A., and Krumlauf, R. 1996. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384: 630-634.
50. Takashima, S., Kitakaze, M., Asakura, M., Asanuma, H., Sanada, S., Tashiro, F., Niwa, H., Miyazaki Ji, J., Hirota, S., Kitamura, Y., et al. 2002. Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc. Natl. Acad. Sci. 99: 3657-3662.
51. Tamamaki, N., Fujimori, K., Nojyo, Y., Kaneko, T., and Takauji, R. 2003. Evidence that Sema3A and Sema3F regulate the migration of GABAergic neurons in the developing neocortex. J. Comp. Neurol. 455: 238-248.
52. Taniguchi, M., Yuasa, S., Fujisawa, H., Naruse, I., Saga, S., Mishina, M., and Yagi, T. 1997. Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 19: 519-530.
53. Tessier-Lavigne, M. and Goodman, C.S. 1996. The molecular biology of axon guidance. Science 274: 1123-1133.
54. Tiret, L., Le Mouellic, H., Maury, M., and Brulet, P. 1998. Increased apoptosis of motoneurons and altered somatotopic maps in the brachial spinal cord of Hoxc-8-deficient mice. Development 125: 279-291.
55. Varela-Echavarria, A., Tucker, A., Puschel, A.W., and Guthrie, S. 1997. Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin D. Neuron 18: 193-207.
56. Verzijl, H.T., van den Helm, B., Veldman, B., Hamel, B.C., Kuyt, L.P., Padberg, G.W., and Kremer, H. 1999. A second gene for autosomal dominant Mobius syndrome is localized to chromosome 10q, in a Dutch family. Am. J. Hum. Genet. 65: 752-756.
57. Yee, K.T., Simon, H.H., Tessier-Lavigne, M., and O'Leary, D.M. 1999. Extension of long leading processes and neuronal migration in the mammalian brain directed by the chemoattractant netrin-1. Neuron 24: 607-622.
58. Zhang, H., Vutskits, L., Pepper, M.S., and Kiss, J.Z. 2003. VEGF is a chemoattractant for FGF-2-stimulated neural progenitors. J. Cell Biol. 163: 1375-1384.