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Vascular Endothelial Growth Factor Has Neurotrophic Activity and Stimulates Axonal Outgrowth, Enhancing Cell Survival and Schwann Cell Proliferation in the Peripheral Nervous System
Open accessAbstract
Vascular endothelial growth factor (VEGF) is a mitogen for endothelial cells, and it promotes angiogenesis in vivo. Here we report that VEGF 165 has neurotrophic actions on cultured adult mouse superior cervical ganglia (SCG) and dorsal root ganglia (DRG), measured as axonal outgrowth. Maximal effect was observed at 10–50 ng/ml for SCG and 100 ng/ml for DRG. VEGF-induced axonal outgrowth was inhibited by the mitogen-activated protein kinase kinase inhibitor PD 98059 but not by the protein kinase inhibitor K252a. VEGF also increased survival of both neurons and satellite cells and the number of proliferating Schwann cells. Immunocytochemistry and immunoblotting revealed that VEGF was expressed in virtually all nerve cells in the SCG but only in a population of small-diameter (<35 μm) neurons representing ∼30% of the neurons in DRG. Immunostaining showed that the VEGF receptor fetal liver kinase receptor (flk-1) was found on nerve cell bodies in DRG and to a lesser extent on neurons in SCG. Growth cones of regenerating axons from both types of ganglia exhibited flk-1 immunoreactivity, as did Schwann cells. We conclude that VEGF has both neurotrophic and mitogenic activity on cells in the peripheral nervous system.
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“Vascular endothelial growth factor (VEGF) is known to promote revascularization, axonal outgrowth, and Schwann cell proliferation.58”
From Regenerative Electrode Interfaces for Neural Prostheses. (2016) · cites this paper as [58]
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Citations
Cites
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
LAEMMLI, U. K. (1970) · Nature · doi:10.1038/227680a0 · Cited by 249,961 · cited 2×
“The samples were electrophoresed according to Laemmli (1970).”
MethodRaza, H., John, A., & Nemmar, A. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350087 · Cited by 47,311
The Biology of Vascular Endothelial Growth Factor
Ferrara, N., & Davis-Smyth, T. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.1.0287 · Cited by 4,585
Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice
Shalaby, F., Rossant, J., Yamaguchi, T. P., Gertsenstein, M., Wu, X.-F., Breitman, M. L., & Schuh, A. C. (1995) · Nature · doi:10.1038/376062a0 · Cited by 3,931 · cited 2×
“Both receptor types are essential for development and organization of endothelial cells and the disruption of the genes encoding flk-1 and flt-1 results in defects of blood vessel formation and an early death of homozygous mice embryo (Fong et al., 1995; Shalaby et al., 1995 ).”
BackgroundRole of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium
Fong, G.-H., Rossant, J., Gertsenstein, M., & Breitman, M. L. (1995) · Nature · doi:10.1038/376066a0 · Cited by 2,606 · cited 1×
“Both receptor types are essential for development and organization of endothelial cells and the disruption of the genes encoding flk-1 and flt-1 results in defects of blood vessel formation and an early death of homozygous mice embryo (Fong et al., 1995; Shalaby et al., 1995).”
BackgroundSöker, S., Takashima, S., Miao, H. Q., Neufeld, G., & Klagsbrun, M. (1998) · Cell · doi:10.1016/s0092-8674(00)81402-6 · Cited by 2,493 · cited 2×
“It has also been reported that VEGF165 binds to neurophilin-1 ( Soker et al., 1998 ), a neuronal cell surface molecule that is important for chemorepulsive signaling during peripheral axonal outgrowth in the developing mice (Kitsukawa et al., 1997).”
BackgroundVascular Permeability Factor, an Endothelial Cell Mitogen Related to PDGF
Keck, P. J., Hauser, S. D., Krivi, G. G., Sanzo, K., Warren, T. G., Feder, J., & Connolly, D. T. (1989) · Science · doi:10.1126/science.2479987 · Cited by 2,058 · cited 2×
“However, other angiogenic factors, including basic fibroblast growth factor (bFGF) and platelet-derived growth factor (PDGF), have been shown to be neurotrophic or exert growthpromoting activity (Rydel and Greene, 1987; Davis and Stroobant, 1990; Smits et al., 1991; Fujimoto et al., 1997).”
BackgroundThe fms -Like Tyrosine Kinase, a Receptor for Vascular Endothelial Growth Factor
de Vries, C. J. M., Escobedo, J. A., Ueno, H., Houck, K. A., Ferrara, N., & Williams, L. T. (1992) · Science · doi:10.1126/science.1312256 · Cited by 2,019 · cited 2×
“VEGF exerts its action via high-affinity binding to two types of phosphotyrosine kinase receptors: fms-like tyrosine kinase (flt-1) and fetal liver kinase receptor (flk-1) (De Vries et al., 1992; Quinn et al., 1993).”
BackgroundWaltenberger, J. L., Claesson, L., Siegbahn, A., Shibuya, M., & Heldin, C. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47116-5 · Cited by 1,661 · cited 2×
“The human counterpart to the flk-1 receptor, which activates the mitogen-activated protein kinase (MAPK) pathway, is also known to induce reorganization of actin filaments, chemotaxis, and give rise to a mitogen response in endothelial cells (Waltenberger et al., 1994; Kroll and Waltenberger, 1997).”
BackgroundMolecular and Biological Properties of the Vascular Endothelial Growth Factor Family of Proteins
Ferrara, N., Houck, K. A., Jakeman, L. B., & LEUNG, D. W. (1992) · Endocrine Reviews · doi:10.1210/edrv-13-1-18 · Cited by 1,655 · cited 1×
“In the nervous system, VEGF mRNA has been found in neurons in the capillary-rich areas of the brain, for instance in the pars distalis cells of the pituitary gland but also in glial cells in the retina after hypoxia (Ferrara et al., 1992; Stone et al., 1995).”
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Zhang, Z. G., Zhang, L., Jiang, Q., Zhang, R., Davies, K., Powers, C., Bruggen, N. V., & Chopp, M. (2000) · Journal of Clinical Investigation · doi:10.1172/jci9369 · Cited by 1,296
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“For example, VEGF stimulates axonal outgrowth and improves the survival of cultured superior cervical and dorsal-route ganglion neurons (15, 16) and enhances the survival of mesencephalic neurons in organotypic explant cultures (17).”
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Ferrara, N. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.280.6.c1358 · Cited by 1,094
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BackgroundThe splice variants of vascular endothelial growth factor (VEGF) and their receptors
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“However, VEGF might also affect neural cells directl”
BackgroundRegulation of angiogenesis via vascular endothelial growth factor receptors.
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“(Oosthuyse et al., 2001; Sondell et al., 1999, 2000).”
Nishijima, K., Ng, Y., Zhong, L., Bradley, J. M. B., Schubert, W., Jo, N., Akita, J., Samuelsson, S. J., Robinson, G. S., Adamis, A. P., et al. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.061237 · Cited by 712
Vascular endothelial growth factor: Direct neuroprotective effect in in vitro ischemia
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Zachary, I. C. (2001) · Cardiovascular Research · doi:10.1016/s0008-6363(00)00268-6 · Cited by 672
Lundborg, G. (2000) · The Journal Of Hand Surgery · doi:10.1053/jhsu.2000.4165 · Cited by 654
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Gardner, T. W., Antonetti, D. A., Barber, A. J., LaNoue, K. F., & Levison, S. W. (2002) · Survey of Ophthalmology · doi:10.1016/s0039-6257(02)00387-9 · Cited by 535
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VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection
Storkebaum, E., Lambrechts, D., & Carmeliet, P. (2004) · BioEssays · doi:10.1002/bies.20092 · Cited by 505
“axonal outgrowth and promotes the survival of neurons and satellite cells,((14)) whereas inhibition of VEGFR-2 signaling blocks axonal outgrowth in response to VEGF.”
BackgroundThe Role of Vascular Endothelial Growth Factor in Angiogenesis
Ferrara, N., & Gerber, H. (2001) · Acta Haematologica · doi:10.1159/000046610 · Cited by 452
“However, recent studies have reported mitogenic effects of VEGF also on a few nonendothelial cell types [ , ,”
BackgroundAtorvastatin Induction of VEGF and BDNF Promotes Brain Plasticity after Stroke in Mice
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“In addition to its role in inducing angiogenesis, VEGF also stimulates neurogenesis and axonal outgrowth, and improves the survival of mouse superior cervical, dorsal root ganglion neurons, and mesencephalic neurons (Hess et al, 2002; Sondell et al, 1999).”
BackgroundRole and Therapeutic Potential of VEGF in the Nervous System
de Almodóvar, C. R., Lambrechts, D., Mazzone, M., & Carmeliet, P. (2009) · Physiological Reviews · doi:10.1152/physrev.00031.2008 · Cited by 461
VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants
Warner-Schmidt, J. L., & Duman, R. S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610282104 · Cited by 438
Altmann, C., & Schmidt, M. H. H. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19010110 · Cited by 413
“VEGF is neuroprotective in peripheral and central neurons [206,207] and is induced by hypoxia through the transcription factor HIF-1 [208].”
BackgroundBio-printing of collagen and VEGF-releasing fibrin gel scaffolds for neural stem cell culture
Lee, Y., Polio, S. R., Lee, W., Dai, G., Menon, L. G., Carroll, R. S., & Yoo, S. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.02.014 · Cited by 389
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VEGF 164 Is Proinflammatory in the Diabetic Retina
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“Schwann cells (45, 46), and bone marrow stromal”
BackgroundReversal of experimental diabetic neuropathy by VEGF gene transfer
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“The results of these experiments do not exclude the possible contribution of direct effects of VEGF on nerve integrity (35, 47, 48).”
Neurotrophic factors and neuroplasticity pathways in the pathophysiology and treatment of depression
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Schwann cell interactions with axons and microvessels in diabetic neuropathy
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“…during development (Levi-Montalcini and Booker 1960; Li and Bernd, 1999; Levi- Montalcini and Angeletti, 1966; Chun and Patterson, 1977; Johnson et al., 1983; Lindsay, 1988; Martin et al., 1988; Ruit et al., 1990; Snider, 1994; Belliveau et al., 1997; Bamji et al., 1998; Sondell et al., 1999).”
VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy
HOBSON, M. I., Green, C. J., & Terenghi, G. (2000) · Journal of Anatomy · doi:10.1046/j.1469-7580.2000.19740591.x · Cited by 298
Chen, X., Katakowski, M., Li, Y., Lu, D., Wang, L., Zhang, L., Chen, J., Xu, Y., Gautam, S. C., Mahmood, A., et al. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10334 · Cited by 293
“VEGF, a strong promoter of angiogenesis, also stimulates axonal outgrowth, nerve cell survival, and Schwann cell proliferation (Sondell et al., 1999).”
BackgroundDiverse roles for VEGF-A in the nervous system
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“…it has been reported that VEGF-A promotes neurite outgrowth from perinatal dorsal root ganglion explants containing VEGFR2-positive sensory neurons (Sondell et al., 1999a), a subsequent study showed that VEGFR2 expression in these ganglia is restricted to endothelial cells, and that VEGF-A…”
BackgroundInfluentialWick, A., Wick, W., Waltenberger, J. L., Weller, M., DICHGANS, J., & Schulz, J. B. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06401.2002 · Cited by 284
“, 1989), recent studies have shown neurotrophic and neuroprotective functions of VEGF, as well as induction of VEGF in pathological states of the CNS (Sondell et al., 1999; Jin et al., 2000; Matsuzaki et al., 2001; Oosthuyse et al., 2001).”
BackgroundNew roles for VEGF in nervous tissue?beyond blood vessels
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Petrova, T. V., Mäkinen, T., & Alitalo, K. K. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4707 · Cited by 275
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“These findings are consistent with two recent report”
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Rosenstein, J. M., Mani, N., Khaibullina, A., & Krum, J. M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11036.2003 · Cited by 220
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Mu, D., Jiang, X., Sheldon, R. A., Fox, C. K., Hamrick, S. E. G., Vexler, Z. S., & Ferriero, D. M. (2003) · Neurobiology of Disease · doi:10.1016/j.nbd.2003.08.020 · Cited by 178
VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain
Bras, B. L., Barallobre, M. J., Homman‐Ludiye, J., Ny, A., Wyns, S., Tammela, T., Haiko, P., Karkkainen, M. J., Yuan, L., Muriel, M., et al. (2006) · Nature Neuroscience · doi:10.1038/nn1646 · Cited by 180
Jones, D. M., Tucker, B. A., Rahimtula, M., & Mearow, K. M. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01925.x · Cited by 176
“…are increasingly being shown to influence axonal growth from adult sensory neurons, either acting alone or modulating the responses of the neurons to trophins like NGF (e.g., Fernyhough et al. 1993; Gavazzi et al. 1999; Sondell et al. 1999; Cafferty et al. 2001; Kimpinski and Mearow 2001).”
BackgroundThe Complex Molecular Biology of Amyotrophic Lateral Sclerosis (ALS)
Redler, R. L., & Dokholyan, N. V. (2012) · Progress in Molecular Biology and Translational Science · doi:10.1016/b978-0-12-385883-2.00002-3 · Cited by 172
“VEGF and ANG, which are involved in maintenance of both neural networks and vasculature, have also been implicated in ALS.(202,203) VEGF, in particular, has received significant attention as a disease-modifying factor since the discovery that diminished VEGF expression in transgenic mice is sufficient to cause late-on…”
VEGF ligands and receptors: implications in neurodevelopment and neurodegeneration
Carmeliet, P., & de Almodovar, C. R. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1283-7 · Cited by 173
“In vitro experiments using adult DRG in culture have shown that VEGF promotes neurite outgrowth, enhances cell survival and promotes Schwann cell proliferation [56].”
BackgroundKrarup, C., Archibald, S. J., & Madison, R. D. (2001) · Annals of Neurology · doi:10.1002/ana.10054 · Cited by 172
Crawford, S. E., Stellmach, V. M., Ranalli, M. A., Huang, X., Huang, L., Volpert, O. V., Vries, G. H. D., Abramson, L. P., & Bouck, N. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.24.4421 · Cited by 171
The role of growth factors in diabetic peripheral neuropathy
Leinninger, G. M., Vincent, A. M., & Feldman, E. L. (2004) · Journal of the Peripheral Nervous System · doi:10.1111/j.1085-9489.2004.09105.x · Cited by 170
“These responses are blocked by inhibition of VEGFR-2, which is expressed in DRG and Schwann cells (Sondell et al., 1999).”
BackgroundYang, S., Bae, D., Kang, H. J., Gwag, B. J., Gho, Y. S., & Chae, C. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00111-8 · Cited by 178
Bates, D., Taylor, G. I., Minichiello, J., Farlie, P. G., Cichowitz, A., Watson, N., Klagsbrun, M., Mamluk, R., & Newgreen, D. F. (2003) · Developmental Biology · doi:10.1016/s0012-1606(02)00045-3 · Cited by 159
“However, the possibility that VEGF165 was acting directly on forelimb nerves (Jin et al., 2000; Sondell et al., 1999a, 1999b, 2000) remained to be excluded (see below).”
InfluentialKaya, D., Özdemir, Y., Yemişçi, M., Tuncer, N., Aktan, S., & Dalkara, T. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600109 · Cited by 160
“For example, VEGF exerts neurotrophic effects on cultured adult mouse superior cervical and dorsal root ganglion neurons (Sondell et al, 1999).”
BackgroundRoss, M. A., Sander, C. M., Kleeb, T. B., Watkins, S. C., & Stolz, D. B. (2001) · Hepatology · doi:10.1053/jhep.2001.29624 · Cited by 156
Role of vascular endothelial growth factor in ovarian physiology - an overview.
Kaczmarek, M. M., Schams, D., & Ziȩcik, A. J. (2005) · PubMed · Cited by 155
Caspase-3 and the regulation of hypoxic neuronal death by vascular endothelial growth factor
Jin, K., Mao, X., Parmentier‐Batteur, S., McEachron, E., Leahy, A. A., & Greenberg, D. A. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00154-3 · Cited by 155
Duffy, A. M., Bouchier‐Hayes, D. J., & Harmey, J. H. (2004) · Springer eBooks · doi:10.1007/978-1-4419-9148-5_13 · Cited by 154
Jin, K., Mao, X. O., Nagayama, T., Goldsmith, P. C., & Greenberg, D. A. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00207-4 · Cited by 153
Molecular Diversity of VEGF-A as a Regulator of Its Biological Activity
Woolard, J., Bevan, H. S., Harper, S. J., & Bates, D. O. (2009) · Microcirculation · doi:10.1080/10739680902997333 · Cited by 163
“Although VEGF165 primarily targets endothelial cells, several studies have reported its role in the function and maintenance of nonendothelial cells, such as lymphocytes [120], retinal pigmental cells [58], and Schwann cells [149].”
BackgroundJin, K., Mao, X. O., & Greenberg, D. A. (2005) · Journal of Neurobiology · doi:10.1002/neu.20215 · Cited by 149
Nikkheslat, N., Zunszain, P. A., Horowitz, M. A., Barbosa, I. G., Parker, J. A., Myint, A.-M., Schwarz, M. J., Tylee, A. T., Carvalho, L. A., & Pariante, C. M. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.02.002 · Cited by 147
“The direct neurotrophic activity of VEGF in the brain has shown to be exerted through stimulating axonal outgrowth and enhancing cell survival (Sondell et al., 1999), protecting hippocampal neurons against glutamate mediated toxicity (Matsuzaki et al., 2001), and influencing synaptic plasticity…”
Kirwan, R. P., Fenerty, C., Crean, J. K. G., Wordinger, R. J., Clark, A. F., & O'Brien, C. J. (2005) · PubMed · Cited by 147
IL-17 and VEGF Are Necessary for Efficient Corneal Nerve Regeneration
Li, Z., Burns, A. R., Han, L., Rumbaut, R. E., & Smith, C. W. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2010.12.001 · Cited by 147
Mechanisms of endothelial cell guidance and vascular patterning in the developing mouse retina
Dorrell, M. I., & Friedlander, M. (2006) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2006.01.001 · Cited by 150
Shyu, W., Lin, S. Z., Chiang, M., Chen, D.-C., Su, C.-Y., Wang, H.-J., Liu, R. S., Tsai, C. H., & Li, H. (2008) · Journal of Clinical Investigation · doi:10.1172/jci32723 · Cited by 145
Li, B., Xu, W., Luo, C., Gozal, D., & Liu, R. (2003) · Molecular Brain Research · doi:10.1016/s0169-328x(03)00025-1 · Cited by 141
Erba, P., Mantovani, C., Kalbermatten, D. F., Pierer, G., Terenghi, G., & Kingham, P. J. (2010) · Journal of Plastic Reconstructive & Aesthetic Surgery · doi:10.1016/j.bjps.2010.08.013 · Cited by 142
VEGF and VEGF Receptor Expression after Experimental Brain Contusion in Rat
Sköld, M. K., von Gertten, C., Sandberg-Nordqvist, A.-C., Mathiesen, T. I., & Holmin, S. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.353 · Cited by 142
“Also, possible neurotrophic/neuroprotective effects of VEGF, either directly or due to VEGF-stimulated vessel sprouting, has been discussed (Hayashi et al., 1998; Jin et al., 2000; Ogunshola et al., 2002; Sondell et al., 1999, 2000; Sun et al., 2003; Zhang et al., 2000).”
VEGF Mediates Commissural Axon Chemoattraction through Its Receptor Flk1
de Almodóvar, C. R., Fabre, P. J., Knevels, E., Coulon, C., Segura, I., Haddick, P. C. G., Aerts, L., Delattin, N., Strasser, G. A., Oh, W., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.014 · Cited by 151
“The lack of a growth-promoting effect of VEGF on precrossing commissural axonsdiffers from its ability to promote axonal outgrowth of superior cervical and dorsal root ganglia, cortical neurons and retinal ganglion cells (Böcker-Meffert et al., 2002; Jin et al., 2002; Rosenstein et al., 2003; Sondell and Kanje, 2001;…”
Molecular and cellular mechanisms of neuroprotection by vascular endothelial growth factor
Sun, F., & Guo, X. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20321 · Cited by 137
“Application of VEGF enhances axonal outgrowth (Sondell et al., 1999) and protects neurons against ischemic injury (Silverman et al.”
BackgroundMolecular Parallels between Neural and Vascular Development
Eichmann, A., & Thomas, J.-L. (2013) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006551 · Cited by 133
“VEGF promotes the extension of axons of various types of neurons in vitro (Silverman et al. 1999; Sondell et al. 1999, 2000).”
Manoonkitiwongsa, P. S., Schultz, R. L., McCreery, D. B., Whitter, E. F., & Lyden, P. D. (2004) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000126236.54306.21 · Cited by 131
“…affirm that VEGF also has a significant neuroprotective effect on neurons and glial cells and stimulates their growth and survival (Carmeliet and Storkebaum, 2002; Hayashi et al., 1998; Jin et al., 2000, 2002; Krum and Khaibullina, 2003; Krum et al., 2002; Sondell et al., 1999; Sun et al., 2003).”
BackgroundNicoletti, J. N., Shah, S. K., McCloskey, D. P., Goodman, J. H., Elkady, A., Atassi, H., Hylton, D., Rudge, J. S., Scharfman, H. E., & Croll, S. D. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.09.083 · Cited by 131
“During development, VEGF stimulates axonal outgrowth and increases the survival of dorsal root ganglion neurons and developing retinal cells (Sondell et al., 1999; Yourey et al., 2000).”
Background
Metadata
- Authors
- Sondell, M., Lundborg, G., & Kanje, M.
- Affiliations
- Lund University (SE)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1999-07-15
- Volume
- 19
- Issue
- 14
- Pages
- 5731-5740
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6783109
- OpenAlex
- W1962154683
- Cited by
- 750
- References
- 44
- Citations by year
- 2026: 8 · 2025: 14 · 2024: 8 · 2023: 11 · 2022: 16 · 2021: 19 · 2020: 26 · 2019: 25 · 2018: 26 · 2017: 28 · 2016: 33 · 2015: 22 · 2014: 44 · 2013: 42 · 2012: 37
- FWCI
- 8.92
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, public-domain)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Keywords
- vascular endothelial growth factor, VEGF165, neurotrophic activity, axon growth, Schwann cell proliferation, satellite cells, superior cervical ganglion, dorsal root ganglia, MEK, PD98059, K252a, axon regeneration, peripheral nervous system, small-diameter neurons, cell survival
- MeSH terms
- Animals, Axons, Carbazoles, Cell Survival, Cells, Cultured, Enzyme Inhibitors, Flavonoids, Ganglia, Spinal, Humans, Lymphokines, Male, Mice, Inbred Strains, Nerve Growth Factors, Recombinant Proteins, Schwann Cells, Time Factors, Endothelial Growth Factors, Superior Cervical Ganglion, Indole Alkaloids, Vascular Endothelial Growth Factors, Vascular Endothelial Growth Factor A, Protein Kinase Inhibitors, Mice
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