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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Vascular endothelial growth factor is known to promote revascularization, axonal outgrowth, and Schwann cell proliferation.
“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]
The Abstract (page not provided) reports VEGF-induced axonal outgrowth and increased Schwann cell proliferation in cultured adult mouse ganglia. It also says VEGF promotes angiogenesis in vivo, but does not specifically establish revascularization—the restoration of a blood supply—so that part of the claim is more specific than the source supports. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
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 · see citing works
Raza, H., John, A., & Nemmar, A. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350087 · Cited by 47,311 · see citing works
The Biology of Vascular Endothelial Growth Factor
Ferrara, N., & Davis-Smyth, T. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.1.0287 · Cited by 4,540 · see citing works
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 · see citing works
Soker, S., Takashima, S., Miao, H., Neufeld, G., & Klagsbrun, M. (1998) · Cell · doi:10.1016/s0092-8674(00)81402-6 · Cited by 2,634 · see citing works
Role 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 · see citing works
Vascular 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 · see citing works
The 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 · see citing works
Waltenberger, 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 1,656 · see citing works
Molecular 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 · see citing works
Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor
Terman, B. I., Dougher-Vermazen, M., Carrion, M. E., Dimitrov, D. S., Armellino, D. C., Gospodarowicz, D., & Böhlen, P. (1992) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(92)90483-2 · Cited by 1,519 · see citing works
The Biology of Vascular Endothelial Growth Factor
Ferrara, N. (1997) · Endocrine Reviews · doi:10.1210/er.18.1.4 · Cited by 1,225 · see citing works
Breier, G., Albrecht, U., Sterrer, S., & Risau, W. (1992) · Development · doi:10.1242/dev.114.2.521 · Cited by 1,087 · see citing works
Stone, J., Itin, A., Alon, T., Pe'er, J., Gnessin, H., Chan‐Ling, T., & Keshet, E. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-04738.1995 · Cited by 1,004 · see citing works
Berse, B., Brown, L. F., Water, L. V. D., Dvorak, H. F., & Senger, D. R. (1992) · Molecular Biology of the Cell · doi:10.1091/mbc.3.2.211 · Cited by 897 · see citing works
A BDNF autocrine loop in adult sensory neurons prevents cell death
Acheson, A., Conover, J. C., Fandl, J. P., DeChiara, T. M., Russell, M., Thadani, A., Squinto, S. P., Yancopoulos, G. D., & Lindsay, R. M. (1995) · Nature · doi:10.1038/374450a0 · Cited by 765 · see citing works
Quinn, T. P., Peters, K. G., de Vries, C. J. M., Ferrara, N., & Williams, L. T. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.16.7533 · Cited by 754 · see citing works
Kitsukawa, T., Shimizu, M., Sanbo, M., Hirata, T., Taniguchi, M., Bekku, Y., Yagi, T., & Fujisawa, H. (1997) · Neuron · doi:10.1016/s0896-6273(00)80392-x · Cited by 709 · see citing works
Averill, S., McMahon, S. B., Clary, D. O., Reichardt, L. F., & Priestley, J. V. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01143.x · Cited by 629 · see citing works
VEGF145, a Secreted Vascular Endothelial Growth Factor Isoform That Binds to Extracellular Matrix
Gluzman‐Poltorak, Z., Cohen, T., Sivan, R., Kandelis, Y., Spira, G., Vlodavsky, I., Keshet, E., & Neufeld, G. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.11.7151 · Cited by 519 · see citing works
Peters, K. G., de Vries, C., & Williams, L. T. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.19.8915 · Cited by 462 · see citing works
Levi‐Montalcini, R., Meyer, H., & Hamburger, V. (1997) · World Scientific series in 20th century biology · doi:10.1142/9789812830319_0007 · Cited by 446 · see citing works
Krøll, J., & Waltenberger, J. L. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.51.32521 · Cited by 430 · see citing works
Rydel, R. E., & Greene, L. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-11-03639.1987 · Cited by 356 · see citing works
A Vital Stain for the Golgi Apparatus
Lipsky, N. G., & Pagano, R. E. (1985) · Science · doi:10.1126/science.2581316 · Cited by 352 · see citing works
Platelet-derived growth factors and fibroblast growth factors are mitogens for rat Schwann cells.
Davis, J. L., & Stroobant, P. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.110.4.1353 · Cited by 313 · see citing works
A glial protein specific for the nervous system.
Hydén, H., & McEwen, B. (1966) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.55.2.354 · Cited by 233 · see citing works
Smits, A., Kato, M., Westermark, B., Nistér, M., Heldin, C. H., & Funa, K. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.18.8159 · Cited by 219 · see citing works
TrkA, But Not TrkC, Receptors Are Essential for Survival of Sympathetic NeuronsIn Vivo
Fagan, A. M., Zhang, H., Landis, S. C., Smeyne, R. J., Silos‐Santiago, I., & Barbacid, M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06208.1996 · Cited by 205 · see citing works
Tissue culture assay of Nerve Growth Factor and of the specific antiserum
Fenton, E. L. (1970) · Experimental Cell Research · doi:10.1016/0014-4827(70)90645-2 · Cited by 173 · see citing works
Bacic, M., Edwards, N. A., & Merrill, M. J. (1995) · Growth Factors · doi:10.3109/08977199509003209 · Cited by 139 · see citing works
Verdi, J. M., Groves, A. K., Fariñas, I., Jones, K. R., Marchionni, M. A., Reichardt, L. F., & Anderson, D. J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80071-9 · Cited by 135 · see citing works
Moran, R., Darżynkiewicz, Z., Staiano‐Coico, L., & Melamed, M. R. (1985) · Journal of Histochemistry & Cytochemistry · doi:10.1177/33.8.3860561 · Cited by 134 · see citing works
Ohmichi, M., Decker, S. J., Pang, L., & Saltiel, A. R. (1992) · Biochemistry · doi:10.1021/bi00131a019 · Cited by 130 · see citing works
Effects of fasciculation on the outgrowth of neurites from spinal ganglia in culture.
Rutishauser, U. S., & Edelman, G. M. (1980) · The Journal of Cell Biology · doi:10.1083/jcb.87.2.370 · Cited by 116 · see citing works
Bartholdi, D., Rubin, B. P., & Schwab, M. E. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01684.x · Cited by 115 · see citing works
Fujimoto, E., Mizoguchi, A., Hanada, K., Yahima, M., & Idé, C. (1997) · Journal of Neurocytology · doi:10.1023/a:1015410023132 · Cited by 113 · see citing works
Schluesener, H. J., Seid, K., Zhao, Y., & Meyermann, R. (1997) · Glia · doi:10.1002/(sici)1098-1136(199708)20:4 · Cited by 79 · see citing works
Inhibition of axonal growth from sensory neurons by excess nerve growth factor
Conti, A. M. F., Fischer, S. J., & Windebank, A. J. (1997) · Annals of Neurology · doi:10.1002/ana.410420604 · Cited by 70 · see citing works
Ekström, P. A. R. (1995) · Neuroreport · doi:10.1097/00001756-199505090-00020 · Cited by 64 · see citing works
Edström, A., Ekström, P. A. R., & Tonge, D. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00324-7 · Cited by 63 · see citing works
A Novel Alternatively Spliced Form of Murine Vascular Endothelial Growth Factor, VEGF 115
Sugihara, T., Wadhwa, R., Kaul, S. C., & Mitsui, Y. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.5.3033 · Cited by 45 · see citing works
Tonge, D., Edstrøm, A. C., & Ekström, P. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00072-5 · Cited by 42 · see citing works
The insulin-like growth factors I and II stimulate proliferation of different types of Schwann cells
Sondell, M., Svenningsen, Å. F., & Kanje, M. (1997) · Neuroreport · doi:10.1097/00001756-199709080-00014 · Cited by 28 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Molecular Mechanisms of Depression: Perspectives on New Treatment Strategies
Lang, U. E., & Borgwardt, S. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350094 · Cited by 8,501 · see citing works
Vascular Endothelial Growth Factor: Basic Science and Clinical Progress
Ferrara, N. (2004) · Endocrine Reviews · doi:10.1210/er.2003-0027 · Cited by 3,707 · see citing works
Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones
Xiao, M., & Hendrickson, A. E. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001002)425:4 · Cited by 165 · see citing works
Vascular endothelial growth factor (VEGF) stimulates neurogenesis <i>in vitro</i> and <i>in vivo</i>
Jin, K., Zhu, Y., Sun, Y., Mao, X. O., Xie, L., & Greenberg, D. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182296499 · Cited by 1,507 · see citing works
VEGF enhances angiogenesis and promotes blood–brain barrier leakage in the ischemic brain
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 · see citing works
VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia
Sun, Y., Jin, K., Xie, L., Childs, J., Mao, X. O., Logvinova, A., & Greenberg, D. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200317977 · Cited by 1,189 · see citing works
VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia
Sun, Y., Jin, K., Xie, L., Childs, J., Mao, X. O., Logvinova, A. V., & Greenberg, D. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17977 · Cited by 1,181 · see citing works
Role of vascular endothelial growth factor in regulation of physiological angiogenesis
Ferrara, N. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.280.6.c1358 · Cited by 1,084 · see citing works
The splice variants of vascular endothelial growth factor (VEGF) and their receptors
Robinson, C. J., & Stringer, S. E. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.5.853 · Cited by 944 · see citing works
Oosthuyse, B., Moons, L., Storkebaum, E., Beck, H., Nuyens, D., Brusselmans, K., Dorpe, J. V., Hellings, P., Gorselink, M., Heymans, S., et al. (2001) · Nature Genetics · doi:10.1038/88842 · Cited by 1,007 · see citing works
Regulation of angiogenesis via vascular endothelial growth factor receptors.
Veikkola, T., Karkkainen, M. J., Claesson, L., & Alitalo, K. K. (2000) · PubMed · Cited by 739 · see citing works
Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development.
Gu, C.-H., Rodríguez, E., Reimert, D. V., Shu, T., Fritzsch, B., Richards, L. J., Kolodkin, A., & Ginty, D. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00169-2 · Cited by 756 · see citing works
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 705 · see citing works
Vascular endothelial growth factor: Direct neuroprotective effect in <i>in vitro</i> ischemia
Jin, K. L., Mao, X. O., & Greenberg, D. A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.18.10242 · Cited by 684 · see citing works
Zachary, I. C. (2001) · Cardiovascular Research · doi:10.1016/s0008-6363(00)00268-6 · Cited by 659 · see citing works
Lundborg, G. (2000) · The Journal Of Hand Surgery · doi:10.1053/jhsu.2000.4165 · Cited by 654 · see citing works
Self-citationNeural tissue engineering options for peripheral nerve regeneration
Gu, X., Ding, F., & Williams, D. F. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.04.064 · Cited by 630 · see citing works
A new view of diabetic retinopathy: a neurodegenerative disease of the eye
Barber, A. J. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(03)00023-x · Cited by 623 · see citing works
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 · see citing works
From angiogenesis to neuropathology
Greenberg, D. A., & Jin, K. (2005) · Nature · doi:10.1038/nature04481 · Cited by 532 · see citing works
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 · see citing works
The Role of Vascular Endothelial Growth Factor in Angiogenesis
Ferrara, N., & Gerber, H. (2001) · Acta Haematologica · doi:10.1159/000046610 · Cited by 452 · see citing works
Atorvastatin Induction of VEGF and BDNF Promotes Brain Plasticity after Stroke in Mice
Chen, J., Zhang, C., Jiang, H., Li, Y., Zhang, L., Robin, A. M., Katakowski, M., Lü, M., & Chopp, M. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600034 · Cited by 451 · see citing works
Role 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 443 · see citing works
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 · see citing works
Altmann, C., & Schmidt, M. H. H. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19010110 · Cited by 410 · see citing works
Bio-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 · see citing works
VEGF 164 Is Proinflammatory in the Diabetic Retina
Ishida, S., Usui, T., Yamashiro, K., Kaji, Y., Ahmed, E., Carrasquillo, K. G., Amano, S., Hida, T., Oguchi, Y., & Adamis, A. P. (2003) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.02-0807 · Cited by 383 · see citing works
Ischemic rat brain extracts induce human marrow stromal cell growth factor production
Chen, X., Li, Y., Wang, L., Katakowski, M., Zhang, L., Chen, J., Xu, Y., Gautam, S. C., & Chopp, M. (2002) · Neuropathology · doi:10.1046/j.1440-1789.2002.00450.x · Cited by 382 · see citing works
VEGF: an update on biological and therapeutic aspects
Ferrara, N. (2000) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(00)00153-1 · Cited by 373 · see citing works
Sondell, M., Sundler, F., & Kanje, M. (2000) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2000.01326.x · Cited by 369 · see citing works
Self-citationNf1-Dependent Tumors Require a Microenvironment Containing Nf1+/−- and c-kit-Dependent Bone Marrow
Yang, F., Ingram, D. A., Shi, C., Zhu, Y., Yuan, J., Li, X., Yang, X., Knowles, S. M., Horn, W., Li, Y., et al. (2008) · Cell · doi:10.1016/j.cell.2008.08.041 · Cited by 363 · see citing works
VEGF Scaffolds Enhance Angiogenesis and Bone Regeneration in Irradiated Osseous Defects
Kaigler, D., Wang, Z., Horger, K. S., Mooney, D. J., & Krebsbach, P. H. (2006) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.060120 · Cited by 340 · see citing works
Rosenstein, J. M., Krum, J. M., & Ruhrberg, C. (2010) · Organogenesis · doi:10.4161/org.6.2.11687 · Cited by 315 · see citing works
Neuropilin‐1 expression by tumor cells promotes tumor angiogenesis and progression
Miao, H., Lee, P. P., Lin, H., Söker, S., & Klagsbrun, M. (2000) · The FASEB Journal · doi:10.1096/fj.00-0250com · Cited by 311 · see citing works
Reversal of experimental diabetic neuropathy by VEGF gene transfer
Schratzberger, P., Walter, D. H., Rittig, K., Bahlmann, F. H., Pola, R., Curry, C., Silver, M., Krainin, J. G., Weinberg, D. H., Ropper, A. H., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci12188 · Cited by 310 · see citing works
Neurotrophic factors and neuroplasticity pathways in the pathophysiology and treatment of depression
Levy, M. J. F., Boulle, F., Steinbusch, H. W., van den Hove, D. L. A., Kenis, G., & Lanfumey, L. (2018) · Psychopharmacology · doi:10.1007/s00213-018-4950-4 · Cited by 308 · see citing works
Schwann cell interactions with axons and microvessels in diabetic neuropathy
Gonçalves, N. P., Vægter, C. B., Andersen, H., Østergaard, L., Calcutt, N. A., & Jensen, T. S. (2017) · Nature Reviews Neurology · doi:10.1038/nrneurol.2016.201 · Cited by 311 · see citing works
Mechanisms underlying hypoxia-induced neuronal apoptosis
Banasiak, K. J., Xia, Y., & Haddad, G. G. (2000) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00011-3 · Cited by 302 · see citing works
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 · see citing works
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 · see citing works
Diverse roles for VEGF-A in the nervous system
Mackenzie, F., & Ruhrberg, C. (2012) · Development · doi:10.1242/dev.072348 · Cited by 266 · see citing works
Wick, 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 283 · see citing works
New roles for VEGF in nervous tissue?beyond blood vessels
Rosenstein, J. M. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.01.022 · Cited by 281 · see citing works
Signaling via Vascular Endothelial Growth Factor Receptors
Petrova, T. V., Mäkinen, T., & Alitalo, K. K. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4707 · Cited by 275 · see citing works
Ayata, C., & Ropper, A. H. (2002) · Journal of Clinical Neuroscience · doi:10.1054/jocn.2001.1031 · Cited by 276 · see citing works
Targeting angiogenesis, the underlying disorder in neovascular age-related macular degeneration
Ng, E. W. M., & Adamis, A. P. (2005) · Canadian Journal of Ophthalmology · doi:10.1016/s0008-4182(05)80078-x · Cited by 274 · see citing works
Vascular endothelial growth factors (VEGFs) and stroke
Greenberg, D. A., & Jin, K. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1282-8 · Cited by 269 · see citing works
Ogunshola, O. O., Antic, A., Donoghue, M. J., Fan, S.-Y., Kim, H., Stewart, W. B., Jr., Madri, J. A., & Ment, L. R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111085200 · Cited by 268 · see citing works
Zachary, I. C. (2005) · Neurosignals · doi:10.1159/000088637 · Cited by 267 · see citing works
Jang, Y., Kim, M., & Hwang, S. W. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1703-1 · Cited by 269 · see citing works
Vascular and neuronal effects of VEGF in the nervous system: implications for neurological disorders
Carmeliet, P., & Storkebaum, E. (2002) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2001.0290 · Cited by 249 · see citing works
VEGF: a critical player in neurodegeneration
Storkebaum, E., & Carmeliet, P. (2004) · Journal of Clinical Investigation · doi:10.1172/jci20682 · Cited by 258 · see citing works
Favorable effect of VEGF gene transfer on ischemic peripheral neuropathy
Schratzberger, P., Schratzberger, G., Silver, M., Curry, C., Kearney, M., Magner, M., Alroy, J., Adelman, L. S., Weinberg, D. H., Ropper, A. H., et al. (2000) · Nature Medicine · doi:10.1038/74664 · Cited by 247 · see citing works
Neural guidance molecules regulate vascular remodeling and vessel navigationPreprint
Eichmann, A., Mäkinen, T., & Alitalo, K. K. (2005) · Genes & Development · doi:10.1101/gad.1305405 · Cited by 246 · see citing works
Polyneuropathy in POEMS syndrome: role of angiogenic factors in the pathogenesis
Scarlato, M., Previtali, S. C., Carpo, M., Pareyson, D., Briani, C., Bo, R. D., Nobile‐Orazio, E., Quattrini, A., & Comi, G. P. (2005) · Brain · doi:10.1093/brain/awh519 · Cited by 241 · see citing works
Vascular Endothelial Growth Factor Modulates Skeletal Myoblast Function
Germani, A., Carlo, A. D., Mangoni, A., Straino, S., Giacinti, C., Turrini, P., Biglioli, P., & Capogrossi, M. C. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63499-2 · Cited by 238 · see citing works
Widenfalk, J., Lipson, A. C., Jubran, M., Hofstetter, C. P., Ebendal, T., Cao, Y., & Olson, L. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00399-3 · Cited by 234 · see citing works
Heine, V. M., Zareno, J., Maslam, S., Joëls, M., & Lucassen, P. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03951.x · Cited by 225 · see citing works
Wang, Y. (2004) · Brain · doi:10.1093/brain/awh325 · Cited by 221 · see citing works
Neurofibromin-deficient Schwann cells secrete a potent migratory stimulus for Nf1+/– mast cells
Yang, F., Ingram, D. A., Shi, C., Hingtgen, C. M., Ratner, N., Monk, K. R., Clegg, T., White, H. A., Mead, L. E., Wenning, M. J., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci19195 · Cited by 221 · see citing works
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 · see citing works
Nerve growth factor control of neuronal expression of angiogenetic and vasoactive factors
Calzà, L., Giardino, L., Giuliani, A., Aloe, L., & Levi‐Montalcini, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051626998 · Cited by 214 · see citing works
VEGF is a chemoattractant for FGF-2–stimulated neural progenitors
Zhang, H., Vutskits, L., Pepper, M. S., & Kiss, J. Z. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200308040 · Cited by 200 · see citing works
Sondell, M., Lundborg, G., & Kanje, M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02056-9 · Cited by 192 · see citing works
Self-citationVEGF-A Is Necessary and Sufficient for Retinal Neuroprotection in Models of Experimental Glaucoma
Foxton, R. H., Finkelstein, A., Vijay, S., Dahlmann-Noor, A. H., Khaw, P. T., Morgan, J. E., Shima, D. T., & Ng, Y. (2013) · American Journal Of Pathology · doi:10.1016/j.ajpath.2012.12.032 · Cited by 189 · see citing works
Neurovascular coupling in bone regeneration
Qin, Q., Lee, S., Patel, N., Walden, K., Gomez-Salazar, M. A., Lévi, B., & James, A. W. (2022) · Experimental & Molecular Medicine · doi:10.1038/s12276-022-00899-6 · Cited by 199 · see citing works
Krum, J. M., Mani, N., & Rosenstein, J. M. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00615-7 · Cited by 185 · see citing works
Zhu, Y., Jin, K., Mao, X. O., & Greenberg, D. A. (2003) · The FASEB Journal · doi:10.1096/fj.02-0515com · Cited by 177 · see citing works
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 · see citing works
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 177 · see citing works
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 · see citing works
The 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 · see citing works
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 · see citing works
Krarup, C., Archibald, S. J., & Madison, R. D. (2001) · Annals of Neurology · doi:10.1002/ana.10054 · Cited by 172 · see citing works
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 · see citing works
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 · see citing works
Yang, 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 170 · see citing works
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 · see citing works
Kaya, 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 · see citing works
Ross, 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 · see citing works
Role of vascular endothelial growth factor in ovarian physiology - an overview.
Kaczmarek, M. M., Schams, D., & Ziȩcik, A. J. (2005) · PubMed · Cited by 155 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 151 · see citing works
Jin, K., Mao, X. O., & Greenberg, D. A. (2005) · Journal of Neurobiology · doi:10.1002/neu.20215 · Cited by 148 · see citing works
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 · see citing works
Kirwan, R. P., Fenerty, C., Crean, J. K. G., Wordinger, R. J., Clark, A. F., & O'Brien, C. J. (2005) · PubMed · Cited by 147 · see citing works
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 144 · see citing works
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 145 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 138 · see citing works
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 139 · see citing works
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 · see citing works
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 · see citing works
Nicoletti, 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 · see citing works
Emerging roles for semaphorins in neural regeneration
Pasterkamp, R. J. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(00)00050-3 · Cited by 130 · see citing works
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
