VEGF signalling controls GnRH neuron survival via NRP1 independently of KDR and blood vessels

Development

Volumn 138, Issue 17, 2011, Pages 3723-3733

  Cariboni, Anna ^a,b   Davidson, Kathryn ^c   Dozio, Elena ^b   Memi, Fani ^a   Schwarz, Quenten ^c,d   Stossi, Fabio ^d   Parnavelas, John G ^a   Ruhrberg, Christiana ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

FLK1; Gnrh neuron; KDR; Mouse; Neuronal survival; Neuropilin; VEGF; VEGFR2

Indexed keywords

GONADORELIN; MITOGEN ACTIVATED PROTEIN KINASE; NEUROPILIN 1; NEUROPILIN 2; PROTEIN KINASE B; SEMAPHORIN 3A; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN 164; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL; BRAIN; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVATION; IN VITRO STUDY; MIGRATION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; BLOOD VESSELS; CELL PROLIFERATION; CELL SURVIVAL; GONADOTROPIN-RELEASING HORMONE; MICE; NEURONS; NEUROPILIN-1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VASCULAR ENDOTHELIAL GROWTH FACTORS;

MUS;

EID: 80051490622     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.063362     Document Type: Article

References (58)

1. Cariboni, A., Pimpinelli, F., Colamarino, S., Zaninetti, R., Piccolella, M., Rumio, C., Piva, F., Rugarli, E. and Maggi, R. (2004). The product of X-linked Kallmann's syndrome gene (KAL1) affects the migratory activity of gonadotropin-releasing hormone (GnRH)-producing neurons. Hum. Mol. Genet. 13, 2781-2791
2. Cariboni, A., Rakic, S., Liapi, A., Maggi, R., Goffinet, A. and Parnavelas, J. (2005). Reelin provides an inhibitory signal in the migration of gonadotropinreleasing hormone neurons. Development 132, 4709-4718
3. Cariboni, A., Hickok, J., Rakic, S., Andrews, W., Maggi, R., Tischkau, S. and Parnavelas, J. (2007a). Neuropilins and their ligands are important in the migration of gonadotropin-releasing hormone neurons. J. Neurosci. 27, 2387-2395
4. Cariboni, A., Maggi, R. and Parnavelas, J. (2007b). From nose to fertility: the long migratory journey of gonadotropin-releasing hormone neurons. Trends Neurosci. 30, 638-644
5. Cariboni, A., Davidson, K., Rakic, S., Maggi, R., Parnavelas, J. G. and Ruhrberg, C. (2011). Defective gonadotropin-releasing hormone neuron migration in mice lacking SEMA3A signalling through NRP1 and NRP2: implications for the aetiology of hypogonadotropic hypogonadism. Hum. Mol. Genet. 20, 336-344
6. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C. et al. (1996). Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439
7. 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
8. Erskine, L., Reijntjes, S., Pratt, T, Denti, L, Schwarz, Q, Vieira, J. M. V., Alakakone, B, Shewan, D. and Ruhrberg, C. (2011). VEGF signalling through neuropilin 1 guides commissural axon crossing at the optic chiasm. Neuron 70, 951-965
9. Fantin, A., Maden, C. H. and Ruhrberg, C. (2009). Neuropilin ligands in vascular and neuronal patterning. Biochem. Soc. Trans. 37, 1228-1232
10. Fantin, A., Vieira, J. M., Gestri, G., Denti, L., Schwarz, Q., Prykhozhij, S., Peri, F., Wilson, S. W. and Ruhrberg, C. (2010). Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116, 829-840
11. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K. S., Powell-Braxton, L., Hillan, K. J. and Moore, M. W. (1996). Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442
12. Gerber, H. P., McMurtrey, A., Kowalski, J., Yan, M., Keyt, B. A., Dixit, V. and Ferrara, N. (1998). Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J. Biol. Chem. 273, 30336-30343
13. 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
14. Gerhardt, H., Ruhrberg, C., Abramsson, A., Fujisawa, H., Shima, D. and Betsholtz, C. (2004). Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev. Dyn. 231, 503-509
15. Giacobini, P., Messina, A., Wray, S., Giampietro, C., Crepaldi, T., Carmeliet, P. and Fasolo, A. (2007). Hepatocyte growth factor acts as a motogen and guidance signal for gonadotropin hormone-releasing hormone-1 neuronal migration. J. Neurosci. 27, 431-445
16. Giacobini, P., Messina, A., Morello, F., Ferraris, N., Corso, S., Penachioni, J., Giordano, S., Tamagnone, L. and Fasolo, A. (2008). Semaphorin 4D regulates gonadotropin hormone-releasing hormone-1 neuronal migration through PlexinB1-Met complex. J. Cell Biol. 183, 555-566
17. Gitay-Goren, H., Cohen, T., Tessler, S., Soker, S., Gengrinovitch, S., Rockwell, P., Klagsbrun, M., Levi, B. Z. and Neufeld, G. (1996). Selective binding of VEGF121 to one of the three vascular endothelial growth factor receptors of vascular endothelial cells. J. Biol. Chem. 271, 5519-5523
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 [correction]. J. Biol. Chem. 275, 29922.
19. 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
20. 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
21. Hardelin, J. P. (2001). Kallmann syndrome: towards molecular pathogenesis. Mol. Cell. Endocrinol. 179, 75-81
22. Hardelin, J. P. and Dode, C. (2008). The complex genetics of Kallmann syndrome: KAL1, FGFR1, FGF8, PROKR2, PROK2 et al. Sex. Dev. 2, 181-193
23. Jin, K. L., Mao, X. O. and Greenberg, D. A. (2000). Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc. Natl. Acad. Sci. USA 97, 10242-10247
24. Jin, K., Mao, X. O., Batteur, S. P., McEachron, E., Leahy, A. and Greenberg, D. A. (2001). Caspase-3 and the regulation of hypoxic neuronal death by vascular endothelial growth factor. Neuroscience 108, 351-358
25. Jones, E. A., Yuan, L., Breant, C., Watts, R. J. and Eichmann, A. (2008). Separating genetic and hemodynamic defects in neuropilin 1 knockout embryos. Development 135, 2479-2488
26. Kawasaki, T., Kitsukawa, T., Bekku, Y., Matsuda, Y., Sanbo, M., Yagi, T. and Fujisawa, H. (1999). A requirement for neuropilin-1 in embryonic vessel formation. Development 126, 4895-4902
27. Kisanuki, Y. Y., Hammer, R. E., Miyazaki, J., Williams, S. C., Richardson, J. A. and Yanagisawa, M. (2001). Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230-242
28. Kitsukawa, T., Shimizu, M., Sanbo, M., Hirata, T., Taniguchi, M., Bekku, Y., Yagi, T. and Fujisawa, H. (1997). Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995-1005
29. Kramer, P. and Wray, S. (2000). Midline nasal tissue influences nestin expression in nasal-placode-derived luteinizing hormone-releasing hormone neurons during development. Dev. Biol. 227, 343-357
30. Maggi, R., Pimpinelli, F., Molteni, L., Milani, M., Martini, L. and Piva, F. (2000). Immortalized luteinizing hormone-releasing hormone neurons show a different migratory activity in vitro. Endocrinology 141, 2105-2112
31. Matsuzaki, H., Tamatani, M., Yamaguchi, A., Namikawa, K., Kiyama, H., Vitek, M. P., Mitsuda, N. and Tohyama, M. (2001). Vascular endothelial growth factor rescues hippocampal neurons from glutamate-induced toxicity: signal transduction cascades. FASEB J. 15, 1218-1220
32. Merchenthaler, I., Gorcs, T., Setalo, G., Petrusz, P. and Flerko, B. (1984). Gonadotropin-releasing hormone (GnRH) neurons and pathways in the rat brain. Cell Tissue Res. 237, 15-29
33. 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
34. Ogunshola, O. O., Antic, A., Donoghue, M. J., Fan, S. Y., Kim, H., Stewart, W. B., Madri, J. A. and Ment, L. R. (2002). Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J. Biol. Chem. 277, 11410-11415
35. 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
36. Pan, Q., Chathery, Y., Wu, Y., Rathore, N., Tong, R. K., Peale, F., Bagri, A., Tessier-Lavigne, M., Koch, A. W. and Watts, R. J. (2007). Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J. Biol. Chem. 282, 24049-24056
37. Petersen, P. H., Zou, K., Hwang, J. K., Jan, Y. N. and Zhong, W. (2002). Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 419, 929-934
38. Pierce, A., Bliesner, B., Xu, M., Nielsen-Preiss, S., Lemke, G., Tobet, S. and Wierman, M. (2008). Axl and Tyro3 modulate female reproduction by influencing gonadotropin-releasing hormone neuron survival and migration. Mol. Endocrinol. 22, 2481-2495
39. Radovick, S., Wray, S., Lee, E., Nicols, D., Nakayama, Y., Weintraub, B., Westphal, H., Cutler, G. J. and Wondisford, F. (1991). Migratory arrest of gonadotropin-releasing hormone neurons in transgenic mice. Proc. Natl. Acad. Sci. USA 88, 3402-3406
40. Rosenstein, J. M., Krum, J. M. and Ruhrberg, C. (2010). VEGF in the nervous system. Organogenesis 6, 107-114
41. Ruhrberg, C. (2003). Growing and shaping the vascular tree: multiple roles for VEGF. BioEssays 25, 1052-1060
42. 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
43. Ruiz de Almodovar, C., Lambrechts, D., Mazzone, M. and Carmeliet, P. (2009). Role and therapeutic potential of VEGF in the nervous system. Physiol. Rev. 89, 607-648
44. Ruiz de Almodovar, C., Coulon, C., Salin, P. A., Knevels, E., Chounlamountri, N., Poesen, K., Hermans, K., Lambrechts, D., Van Geyte, K., Dhondt, J. et al. (2010). Matrix-binding vascular endothelial growth factor (VEGF) isoforms guide granule cell migration in the cerebellum via VEGF receptor Flk1. J. Neurosci. 30, 15052-15066
45. Ruiz de Almodovar, C., Fabre, P. J., Knevels, E., Coulon, C., Segura, I., Haddick, P. C. G., Aerts, L., Delattin, N., Strasser, G., Oh, W. et al. (2011). VEGF mediates commissural axon chemoattraction through its receptor Flk1. Neuron 70, 966-978
46. Schwanzel-Fukuda, M., Bick, D. and Pfaff, D. W. (1989). Luteinizing hormonereleasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome. Brain Res. Mol. Brain Res. 6, 311-326
47. Schwarz, Q., Gu, C., Fujisawa, H., Sabelko, K., Gertsenstein, M., Nagy, A., Taniguchi, M., Kolodkin, A. L., Ginty, D. D., Shima, D. T. et al. (2004). Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve. Genes Dev. 18, 2822-2834
48. Shalaby, F., Rossant, J., Yamaguchi, T. P., Gertsenstein, M., Wu, X. F., Breitman, M. L. and Schuh, A. C. (1995). Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62-66
49. Soker, S., Fidder, H., Neufeld, G. and Klagsbrun, M. (1996). Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain. J. Biol. Chem. 271, 5761-5767
50. 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
51. Soker, S., Miao, H. Q., Nomi, M., Takashima, S. and Klagsbrun, M. (2002). VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding. J. Cell. Biochem. 85, 357-368
52. Sondell, M., Lundborg, G. and Kanje, M. (1999). Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J. Neurosci. 19, 5731-5740
53. 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
54. Tissir, F., Ravni, A., Achouri, Y., Riethmacher, D., Meyer, G. and Goffinet, A. M. (2009). DeltaNp73 regulates neuronal survival in vivo. Proc. Natl. Acad. Sci. USA 106, 16871-16876
55. Tobet, S. A., Crandall, J. E. and Schwarting, G. A. (1993). Relationship of migrating luteinizing hormone-releasing hormone neurons to unique olfactory system glycoconjugates in embryonic rats. Dev. Biol. 155, 471-482
56. Wang, L., Dutta, S. K., Kojima, T., Xu, X., Khosravi-Far, R., Ekker, S. C. and Mukhopadhyay, D. (2007). Neuropilin-1 modulates p53/caspases axis to promote endothelial cell survival. PLoS ONE 2, e1161.
57. Whitaker, G. B., Limberg, B. J. and Rosenbaum, J. S. (2001). Vascular endothelial growth factor receptor-2 and neuropilin-1 form a receptor complex that is responsible for the differential signaling potency of VEGF(165) and VEGF(121). J. Biol. Chem. 276, 25520-25531
58. Wray, S., Grant, P. and Gainer, H. (1989). Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc. Natl. Acad. Sci. USA 86, 8132-8136.