 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, May 15, 2001, 21(10):3332-3341
Semaphorin 3A-Vascular Endothelial Growth Factor-165 Balance Mediates Migration and Apoptosis of Neural Progenitor Cells by the Recruitment of Shared Receptor
Dominique Bagnard1, Catherine Vaillant1, Seng-Thuon Khuth1, Nathalie Dufay1, Marion Lohrum2, Andreas W. Püschel2, Marie-Françoise Belin1, Jürgen Bolz3, and Nicole Thomasset1 1 Institut National de la Santé et de la Recherche Médicale U433, Neurobiologie Experimentale et Physiopathologie, Faculté de Médecine Laënnec, 69372 Lyon cedex 08, France, 2 Max-Planck-Institut für Hirnforschung, Abt. Neurochemie, Molecular Neurogenetics Laboratory, 60528 Frankfurt, Germany, and 3 Universität Jena, Institut für Allgemeine Zoologie, 07743 Jena, Germany
The dynamic and coordinated interaction between cells and their microenvironment controls cell migration, proliferation, and apoptosis, mediated by different cell surface molecules. We have studied the response of a neuroectodermal progenitor cell line, Dev, to a guidance molecule, semaphorin 3A (Sema3A), described previously as a repellent-collapsing signal for axons, and we have shown that Sema3A acts as a repellent guidance cue for migrating progenitor cells and, on prolonged application, induces apoptosis. Both repulsion and induction of cell death are mediated by neuropilin-1, the ligand-binding component of the Sema3A receptor. The vascular endothelial growth factor, VEGF165, antagonizes Sema3A-induced apoptosis and promotes cell survival, migration, and proliferation. Surprisingly, repulsion by Sema3A also depends on expression of VEGFR1, a VEGF165 receptor, expressed in Dev cells. Moreover, we found that these repulsive effects of Sema3A require tyrosine kinase activity, which can be attributed to VEGFR1. These results indicate that the balance between guidance molecules and angiogenic factors can modulate the migration, apoptosis (or survival), and proliferation of neural progenitor cells through shared receptors.
Key words: apoptosis; semaphorin; VEGF; migration; neuropilin; VEGFR1
Copyright © 2001 Society for Neuroscience 0270-6474/01/21103332-10$05.00/0
This article has been cited by other articles:
K. J. Reidy, G. Villegas, J. Teichman, D. Veron, W. Shen, J. Jimenez, D. Thomas, and A. Tufro
Semaphorin3a regulates endothelial cell number and podocyte differentiation during glomerular development
Development, December 1, 2009; 136(23): 3979 - 3989.
[Abstract] [Full Text] [PDF]
A. Le, R. Zielinski, C. He, M. T. Crow, S. Biswal, R. M. Tuder, and P. M. Becker
Pulmonary Epithelial Neuropilin-1 Deletion Enhances Development of Cigarette Smoke-induced Emphysema
Am. J. Respir. Crit. Care Med., September 1, 2009; 180(5): 396 - 406.
[Abstract] [Full Text] [PDF]
C. Ruiz de Almodovar, D. Lambrechts, M. Mazzone, and P. Carmeliet
Role and Therapeutic Potential of VEGF in the Nervous System
Physiol Rev, April 1, 2009; 89(2): 607 - 648.
[Abstract] [Full Text] [PDF]
S. Moretti, A. Procopio, R. Lazzarini, M. R. Rippo, R. Testa, M. Marra, L. Tamagnone, and A. Catalano
Semaphorin3A signaling controls Fas (CD95)-mediated apoptosis by promoting Fas translocation into lipid rafts
Blood, February 15, 2008; 111(4): 2290 - 2299.
[Abstract] [Full Text] [PDF]
L. Roth, C. Nasarre, S. Dirrig-Grosch, D. Aunis, G. Cremel, P. Hubert, and D. Bagnard
Transmembrane Domain Interactions Control Biological Functions of Neuropilin-1
Mol. Biol. Cell, February 1, 2008; 19(2): 646 - 654.
[Abstract] [Full Text] [PDF]
M. L. Slongo, B. Molena, A. M. Brunati, M. Frasson, M. Gardiman, M. Carli, G. Perilongo, A. Rosolen, and M. Onisto
Functional VEGF and VEGF receptors are expressed in human medulloblastomas
Neuro-oncol, October 1, 2007; 9(4): 384 - 392.
[Abstract] [Full Text] [PDF]
J. M. Vieira, Q. Schwarz, and C. Ruhrberg
Selective requirements for NRP1 ligands during neurovascular patterning
Development, May 15, 2007; 134(10): 1833 - 1843.
[Abstract] [Full Text] [PDF]
A. Cariboni, J. Hickok, S. Rakic, W. Andrews, R. Maggi, S. Tischkau, and J. G. Parnavelas
Neuropilins and Their Ligands Are Important in the Migration of Gonadotropin-Releasing Hormone Neurons
J. Neurosci., February 28, 2007; 27(9): 2387 - 2395.
[Abstract] [Full Text] [PDF]
J. D. Berndt and M. C. Halloran
Semaphorin 3d promotes cell proliferation and neural crest cell development downstream of TCF in the zebrafish hindbrain
Development, October 15, 2006; 133(20): 3983 - 3992.
[Abstract] [Full Text] [PDF]
N. Banu, J. Teichman, M. Dunlap-Brown, G. Villegas, and A. Tufro
Semaphorin 3C regulates endothelial cell function by increasing integrin activity
FASEB J, October 1, 2006; 20(12): 2150 - 2152.
[Abstract] [Full Text] [PDF]
D. H. Damon
Vascular endothelial-derived semaphorin 3 inhibits sympathetic axon growth
Am J Physiol Heart Circ Physiol, March 1, 2006; 290(3): H1220 - H1225.
[Abstract] [Full Text] [PDF]
H. H. Majed, S. Chandran, S. P. Niclou, R. S. Nicholas, A. Wilkins, M. G. Wing, K. E. Rhodes, M. G. Spillantini, and A. Compston
A Novel Role for Sema3A in Neuroprotection from Injury Mediated by Activated Microglia
J. Neurosci., February 8, 2006; 26(6): 1730 - 1738.
[Abstract] [Full Text] [PDF]
I. Chabbert-de Ponnat, A. Marie-Cardine, R. J. Pasterkamp, V. Schiavon, L. Tamagnone, N. Thomasset, A. Bensussan, and L. Boumsell
Soluble CD100 functions on human monocytes and immature dendritic cells require plexin C1 and plexin B1, respectively
Int. Immunol., April 1, 2005; 17(4): 439 - 447.
[Abstract] [Full Text] [PDF]
Q. Schwarz, C. Gu, H. Fujisawa, K. Sabelko, M. Gertsenstein, A. Nagy, M. Taniguchi, A. L. Kolodkin, D. D. Ginty, D. T. Shima, et al.
Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve
Genes & Dev., November 15, 2004; 18(22): 2822 - 2834.
[Abstract] [Full Text] [PDF]
E. Castro-Rivera, S. Ran, P. Thorpe, and J. D. Minna
Semaphorin 3B (SEMA3B) induces apoptosis in lung and breast cancer, whereas VEGF165 antagonizes this effect
PNAS, August 3, 2004; 101(31): 11432 - 11437.
[Abstract] [Full Text] [PDF]
J. C. Schwamborn, R. Fiore, D. Bagnard, J. Kappler, C. Kaltschmidt, and A. W. Puschel
Semaphorin 3A Stimulates Neurite Extension and Regulates Gene Expression in PC12 Cells
J. Biol. Chem., July 23, 2004; 279(30): 30923 - 30926.
[Abstract] [Full Text] [PDF]
D. J. Finley, N. Arora, B. Zhu, L. Gallagher, and T. J. Fahey III
Molecular Profiling Distinguishes Papillary Carcinoma from Benign Thyroid Nodules
J. Clin. Endocrinol. Metab., July 1, 2004; 89(7): 3214 - 3223.
[Abstract] [Full Text] [PDF]
P. Giraudon, P. Vincent, C. Vuaillat, O. Verlaeten, L. Cartier, A. Marie-Cardine, M. Mutin, A. Bensussan, M.-F. Belin, and L. Boumsell
Semaphorin CD100 from Activated T Lymphocytes Induces Process Extension Collapse in Oligodendrocytes and Death of Immature Neural Cells
J. Immunol., January 15, 2004; 172(2): 1246 - 1255.
[Abstract] [Full Text] [PDF]
H. Zhang, L. Vutskits, M. S. Pepper, and J. Z. Kiss
VEGF is a chemoattractant for FGF-2-stimulated neural progenitors
J. Cell Biol., December 22, 2003; 163(6): 1375 - 1384.
[Abstract] [Full Text] [PDF]
R. E. Bachelder, E. A. Lipscomb, X. Lin, M. A. Wendt, N. H. Chadborn, B. J. Eickholt, and A. M. Mercurio
Competing Autocrine Pathways Involving Alternative Neuropilin-1 Ligands Regulate Chemotaxis of Carcinoma Cells
Cancer Res., September 1, 2003; 63(17): 5230 - 5233.
[Abstract] [Full Text] [PDF]
W. Shoji, S. Isogai, M. Sato-Maeda, M. Obinata, and J. Y. Kuwada
Semaphorin3a1 regulates angioblast migration and vascular development in zebrafish embryos
Development, July 15, 2003; 130(14): 3227 - 3236.
[Abstract] [Full Text] [PDF]
K. D. Miller, C. J. Sweeney, and G. W. Sledge
The Snark is a Boojum: the continuing problem of drug resistance in the antiangiogenic era
Ann. Onc., January 1, 2003; 14(1): 20 - 28.
[Abstract] [Full Text] [PDF]
A. Shirvan, M. Kimron, V. Holdengreber, I. Ziv, Y. Ben-Shaul, S. Melamed, E. Melamed, A. Barzilai, and A. S. Solomon
Anti-semaphorin 3A Antibodies Rescue Retinal Ganglion Cells from Cell Death following Optic Nerve Axotomy
J. Biol. Chem., December 13, 2002; 277(51): 49799 - 49807.
[Abstract] [Full Text] [PDF]
N. Spassky, F. de Castro, B. Le Bras, K. Heydon, F. Queraud-LeSaux, E. Bloch-Gallego, A. Chedotal, B. Zalc, and J.-L. Thomas
Directional Guidance of Oligodendroglial Migration by Class 3 Semaphorins and Netrin-1
J. Neurosci., July 15, 2002; 22(14): 5992 - 6004.
[Abstract] [Full Text] [PDF]
C. Gu, B. J. Limberg, G. B. Whitaker, B. Perman, D. J. Leahy, J. S. Rosenbaum, D. D. Ginty, and A. L. Kolodkin
Characterization of Neuropilin-1 Structural Features That Confer Binding to Semaphorin 3A and Vascular Endothelial Growth Factor 165
J. Biol. Chem., May 10, 2002; 277(20): 18069 - 18076.
[Abstract] [Full Text] [PDF]
D. Pleasure, P. Bannerman, J. Ara, M. Scarlato, and T. Itoh
Prospects for Vascular Endothelial Growth Factor Neurotherapeutics
Arch Neurol, May 1, 2002; 59(5): 692 - 694.
[Full Text] [PDF]
B. J. Eickholt, F. S. Walsh, and P. Doherty
An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling
J. Cell Biol., April 15, 2002; 157(2): 211 - 217.
[Abstract] [Full Text] [PDF]
P. S. Steeg
Collapsin Response Mediator Protein-1: a Lung Cancer Invasion Suppressor Gene With Nerve
J Natl Cancer Inst, September 19, 2001; 93(18): 1364 - 1365.
[Full Text] [PDF]
D. Ricard, V. Rogemond, E. Charrier, M. Aguera, D. Bagnard, M.-F. Belin, N. Thomasset, and J. Honnorat
Isolation and Expression Pattern of Human Unc-33-Like Phosphoprotein 6/Collapsin Response Mediator Protein 5 (Ulip6/CRMP5): Coexistence with Ulip2/CRMP2 in Sema3A- Sensitive Oligodendrocytes
J. Neurosci., September 15, 2001; 21(18): 7203 - 7214.
[Abstract] [Full Text] [PDF]
B. J. Eickholt, F. S. Walsh, and P. Doherty
An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling
J. Cell Biol., April 15, 2002; 157(2): 211 - 217.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|