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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
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Background
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Items 401–500 of 750
Chen, C., Huang, S., Chen, N.-F., Feng, C., Hung, H.-C., Sung, C.-S., Jean, Y., Wen, Z., & Chen, W.-F. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.02.017 · Cited by 24
“Many studies have indicated that both VEGFR-1 and VEGFR-2 activation could produce neuroprotection (Silverman et al., 1999; Sondell et al., 1999; Jin et al., 2000; Oosthuyse et al., 2001; Sun et al., 2004, 2006).”
Fast rearrangement of the neuronal growth cone’s actin cytoskeleton following VEGF stimulation
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“This accumulating effect could be due to an expression of TrkA receptors alongside with VEGF receptors (Sondell et al. 1999).”
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Sornelli, F., Lambìase, A., Mantelli, F., & Aloe, L. (2010) · PubMed Central · Cited by 26
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Vascular endothelial-derived semaphorin 3 inhibits sympathetic axon growth
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“(21) reported that VEGF promotes the growth of sympathetic axons.”
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“It has been shown that VEGF do have a direct neurotropic/neuroprotective function (45, 46).”
BackgroundThe role of vascular endothelial growth factor and vascular stability in diseases of the ear
London, N. R., & Gurgel, R. K. (2013) · The Laryngoscope · doi:10.1002/lary.24564 · Cited by 25
“VEGF directly promotes axonal outgrowth and enhances neuron survival.(66,67) In a study investigating noise-induced sensorineural damage in guinea pigs, VEGF was up-regulated in the cochlea on both days 1 and 7 after noise exposure.”
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“VEGF has been demonstrated to act as an autocrine growth factor for many cell types that secrete VEGF and express VEGF receptors (VEGFRs), including cancer cells [8], podocytes [9,10], hematopoietic stem cells [11], osteoblasts [12], osteoclasts [12], chondrocytes, monocytes [13] and neurons [14,15].”
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“It stimulates axonal outgrowth and promotes the survival of mouse superior cervical neurons, dorsal root ganglion neurons, and rat mesencephalic neurons in culture [8].”
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“Cultured neurons from the peripheral nervous system treated with VEGF displayed increased axonal outgrowth and survival, while proliferation of Schwann cells was also observed (Sondell et al., 1999).”
BackgroundSchwann cells promote endothelial cell migration
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“On the other hand, VEGF prolongs the survival and stimulates the proliferation of SCs in explant cultures of superior cervical and dorsal root ganglia.(17) Gerber et al.”
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VEGF-Induced Growth Cone Enhancement Is Diminished by Inhibiting Tyrosine-Residue 1214 of VEGFR-2
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“In conclusion, the presented results show that the growth cone size of DRG neurons was significantly enhanced following exposure to VEGF at a concentration of 0.1 g/ml, which is in accordance with previous reports [Sondell et al., 1999].”
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“Some experiments have demonstrated that increased levels of VEGF in a damaged nerve, by direct or plasmid delivery, support and enhance the growth of regenerating nerve fibers, probably by stimulation of Schwann cells [17] or by a combination of angiogenic, neurotrophic and neuroprotective effects [18,19].”
BackgroundResultA nerve conduit filled with Wnt5a‐loaded fibrin hydrogels promotes peripheral nerve regeneration
Liu, Y., Chen, X., Zhou, L., Rao, F., Zhang, D., & Wang, Y. Y. (2021) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13752 · Cited by 25
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VEGF Receptor-2 (Flk-1) Overexpression in Mice Counteracts Focal Epileptic Seizures
Nikitidou, L., Kanter‐Schlifke, I., Dhondt, J., Carmeliet, P., Lambrechts, D., & Kokaia, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040535 · Cited by 23
“are predominantly mediated by VEGF receptor-2, also called fetal liver kinase receptor 1 (Flk-1) [13,23,24], or kinase insert-domain containing receptor (KDR) in humans [25].”
Current and investigational pharmacotherapeutic approaches for modulating retinal angiogenesis
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“(2,5,6) describe a postnatal decrease in the percentage of VEGFR-2-IR neurons in the DRG, with less than 10% of sensory neurons expressing VEGFR-2 in adult mouse DRG.”
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Shen, H., Chen, X., Li, X., Jia, K., Xiao, Z., & Dai, J. (2019) · Science China Life Sciences · doi:10.1007/s11427-019-9490-8 · Cited by 23
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“It has been stated that VEGF has a neurotrophic and mitogenic activity on cells in the peripheral nervous system, and in an avascular nerve graft model local application of VEGF promoted invasion of the graft with Schwann cells and neovascularization [ 7 , 8 ].”
BackgroundThe effects of bevacizumab treatment in a rat model of retinal ischemia and perfusion injury.
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Anti-VEGF treatment improves neurological function in tumors of the nervous system
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“…and in the adult (Calvo et al., 2011; Falk et al., 2011; Jin et al., 2002; Le Bras et al., 2006; Licht et al., 2010; Licht et al., 2011; Louissaint et al., 2002; Palmer et al., 2000; Ruiz de Almodovar et al., 2010; Schanzer et al., 2004; Sondell et al., 1999; Sun et al., 2006; Wittko et al., 2009).”
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“Therefore, when the endometriosis lesions are subjected to the estrus cycle, the expression of Vegf will generate neuro-angiogenic cues [31], supporting our goal to establish an endometriosis model for ongoing pain.”
BackgroundVEGFR-3/Flt-4 mediates proliferation and chemotaxis in glial precursor cells
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“, 2015), but also contribute to the survival and proliferation of a variety of glial cells (Sondell et al., 1999; Mani et al., 2005).”
BackgroundButler, S. M., Abrassart, J., Hubbell, M. C., Adeoye, O. O., Semotiuk, A., Williams, J. M., Mata‐Greenwood, E., Khorram, O., & Pearce, W. J. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00413.2010 · Cited by 21
“VEGF also appears to have important trophic and protective effects on cellular elements of the peripheral nervous system, including both Schwann cells (55) and perivascular sympathetic neurons (39).”
BackgroundVEGF Triggers the Activation of Cofilin and the Arp2/3 Complex within the Growth Cone
Schlau, M., Terheyden-Keighley, D., Theis, V., Mannherz, H. G., & Theiß, C. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020384 · Cited by 21
“It supports neuroprotection, as well as neurodevelopment and neuroregeneration [22,23].”
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“Vascular endothelial growth factor (VEGF) has potent neurotrophic and mitogenic activity, and increases axonal outgrowth and survival of neurons (Annex et al., 1998; Sondell et al., 1999).”
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“VEGF has neurotrophic activity and stimulates axonal outgrowth, thereby enhancing cell survival and cell proliferation.([10]) Therefore, long-term anti-VEGF therapy may accelerate apoptosis in the inner retinal layers, including the retinal nerve fiber layer (RNFL) and retinal ganglion cell (RGC) layer.”
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Geometrical versus Random β-TCP Scaffolds: Exploring the Effects on Schwann Cell Growth and Behavior
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“Vascular endothelial growth factor (VEGF) is a crucial mediator of vasculogenesis and angiogenesis, and has been also demonstrated to have neurotrophic and neuroprotective effects (Sondell et al., 1999; Cheng et al., 2004).”
BackgroundLong, C., Lankford, L., Kumar, P., Grahn, R. A., Borjesson, D. L., Farmer, D. L., & Wang, A. (2017) · Cytometry Part A · doi:10.1002/cyto.a.23171 · Cited by 22
Growth Factors as Axon Guidance Molecules: Lessons From in vitro Studies
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“Pioneering work showed that VEGF had dose-dependent neurotrophic effects on mouse superior cervical ganglion and DRG neurons (Sondell et al., 1999).”
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“VEGF-A is a potent angiogenic factor that stimulates both the proliferation and migration of endothelial cells in vitro, and the in vivo formation of new blood vessels, and also enhances vascular permeability [15, 21, 16–18, 22, 23].”
BackgroundProtective effects of VEGF treatment on focal cerebral ischemia in rats
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“Recent evidence suggests that both vascular endothelial growth factor and fibroblast growth factor stimulate neurogenesis [29].”
BackgroundMichel, O., Heß, A., Bloch, W., Schmidt, A., Stennert, E., & Addicks, K. (2001) · Hearing Research · doi:10.1016/s0378-5955(01)00262-3 · Cited by 20
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“reported that VEGF and its receptor are expressed in neurons, in growth cones, and in Schwann cells.(31) Activation of the VEGF receptors resulted in proliferation of Schwann cells, axonal outgrowth, and increased survival of both neurons and satellite cells.”
BackgroundGimeno-Hernández, R., Cantó, A., Fernández-Carbonell, Á., Olivar, T., Hernández‐Rabaza, V., Almansa, I., & Miranda, M. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.590572 · Cited by 19
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“Te third isoform is the neuronal isoform (nNOS) located in specifc neuronal populations [6, 94, 134, 135].”
van Neerven, S., Joosten, E. A. J., Brook, G. A., Lambert, C. A., Mey, J., Weis, J., Marcus, M. A. E., Steinbusch, H. W. M., van Kleef, M., Patijn, J., et al. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2010.1484 · Cited by 19
“Vascular endothelial growth factor (VEGF) is a key factor in the process of angiogenesis, but has also been associated with neuroprotection and neurite outgrowth (Rosenstein and Krum 2004; Sondell et al., 1999).”
D’Onofrio, P. M., Thayapararajah, M., Lysko, M. D., Magharious, M. M., Spratt, S. K., Lee, G., Ando, D. G., Surosky, R. T., Fehlings, M. G., & Koeberle, P. D. (2011) · Journal of Neurotrauma · doi:10.1089/neu.2011.1896 · Cited by 19
“Previous studies have shown both neuroprotective and neuroproliferative properties for VEGF-A (Greenberg and Jin, 2005; Jin et al., 2000; Sondell et al., 1999).”
VEGF polymorphisms and serum VEGF levels in Parkinson's disease
Mihçi, E., Özkaynak, S., Sallakçı, N., Kızılay, F., & Yavuzer, U. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.02.027 · Cited by 19
Tse, K., Kingham, P. J., Novikov, L. N., & Wiberg, M. (2011) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.452 · Cited by 19
“VEGF was shown to promote neuroprotection and accelerate axonal regeneration, both in vitro and in vivo (Hobson et al., 2000; Jin et al., 2000; Sondell et al., 1999).”
BackgroundMukhamedshina, Y. O., Gilazieva, Z., Arkhipova, S. S., Galieva, L. R., Garanina, E. E., Shulman, A., Гульусовна, Я. Г., Chelyshev, Y. A., Вагизовна, Ш. Н., & Rizvanov, A. A. (2017) · Neural Plasticity · doi:10.1155/2017/9857918 · Cited by 19
Zhang, H., Wang, Y., & He, Z. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00644 · Cited by 19
“Additional studies have demonstrated that VEGFA promotes neuronal survival and neurite outgrowth in primary cortical neurons and dorsal root ganglia (Sondell et al., 1999; Rosenstein et al., 2003).”
BackgroundGlaesel, K., May, C., Marcus, K., Matschke, V., Theiß, C., & Theis, V. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113839 · Cited by 19
“Since the initial description of VEGFR-2 as a key player in angiogenesis and motility of endothelial cells and cancer development [30], the understanding of the neuronal functions has expanded rapidly in recent years [5,31].”
BackgroundInfluentialАршалуйсович, М. В., Safiullov, Z. Z., Izmailov, A., Fadeev, F., Sokolov, M. E., Kuznetsov, M., Trofimov, D. A., Kim, E., Kundakchyan, G., Gibadullin, A., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186858 · Cited by 19
“It supports survival of sensitive [41] and motor neurons [42] and stimulates proliferation of astrocytes [43], neural stem cells [44], and Schwann’s cells [41].”
BackgroundWang, L., Swaminathan, S. S., Yang, J. Y., Barikian, A., Shi, Y., Shen, M., Jiang, X., Feuer, W. J., Gregori, G., & Rosenfeld, P. J. (2020) · Ophthalmology Retina · doi:10.1016/j.oret.2020.10.004 · Cited by 19
Endothelial cell influence on dorsal root ganglion cell formation
Mompeó, B., Engele, J., & Spanel‐Borowski, K. (2003) · Journal of Neurocytology · doi:10.1023/b:neur.0000005597.28053.2a · Cited by 19
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Castillo, X., Melo, Z., Varela‐Echavarría, A., Tamaríz, E., Aroña, R. M., Arnold, E., Clapp, C., & de la Escalera, G. M. (2017) · Neuroendocrinology · doi:10.1159/000477768 · Cited by 18
Abdolrahimzadeh, S., Gharbiya, M., Formisano, M., Bertini, F., Cerini, A., & Pacella, E. (2019) · Current Eye Research · doi:10.1080/02713683.2019.1610179 · Cited by 18
Salehi, M., Ehtrami, A., Bastami, F., Farzamfar, S., Hosseinpour, S., Vahedi, H., Vaez, A., Rahvar, M., & Goodarzi, A. (2019) · Fibers and Polymers · doi:10.1007/s12221-019-8939-3 · Cited by 18
George, L., Dunkel, H., Hunnicutt, B. J., Filla, M. B., Little, C. D., Lansford, R. D., & Lefcort, F. B. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.02.028 · Cited by 17
Shen, J., Xiao, R., Bair, J. A., Wang, F., Vandenberghe, L. H., Dartt, D. A., Baranov, P. Y., & Ng, Y. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-1049-0 · Cited by 18
In vitro activation of extracellular signal-regulated kinase1/2 in the inner ear of guinea pigs
Heß, A., Labbé, D., Michel, O., Teranishi, M., Orzechowska, O., Schmidt, A., Addicks, K., & Bloch, W. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03545-x · Cited by 18
Sköld, M. K., Marti, H. H., Lindholm, T., Lindå, H., Hammarberg, H., Risling, M., & Cullheim, S. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.03.024 · Cited by 18
Sun, J., Zhou, W., Bin, S., & Yang, Y. (2009) · Brain and Development · doi:10.1016/j.braindev.2009.01.004 · Cited by 17
“VEGF, discovered as an angiogenic and vascular permeability factor, is now recognized as a neurotrophic factor [19].”
Triple-Gene Therapy for Stroke: A Proof-of-Concept in Vivo Study in Rats
Sokolov, M. E., Bashirov, F. V., Аршалуйсович, М. В., Povysheva, T. V., Fadeev, F., Izmailov, A., Kuztetsov, M. S., Safiullov, Z. Z., Шмаров, М. М., Naroditskyi, B. S., et al. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00111 · Cited by 17
“The mortality rate of the experimental animals during the surgery and in first post-operative week was 20% which corresponds to the severity of the surgery (Ström et al., 2013).”
BackgroundChoi, S.-H., Kim, H., Cho, H., Park, S.-D., Lee, N.-E., Hwang, S., Rhim, H., Kim, H., Cho, I., & Nah, S.-Y. (2018) · Journal of Ginseng Research · doi:10.1016/j.jgr.2018.05.006 · Cited by 17
“VEGF thus exhibits both angiogenesis-dependent and angiogenesis-independent functions that maintain homeostasis in the brain and its blood vessels [16,17,29].”
BackgroundYip, H.-K., Chen, K., Dubey, N. K., Sun, C., Deng, Y.-H., Su, C.-W., Lo, W., Cheng, H.-C., & Deng, W. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119227 · Cited by 17
Sadri, M., Hirosawa, N., Le, J., Romero, H. K., Martellucci, S., Kwon, H. J., Pizzo, D. P., Ohtori, S., Gonias, S. L., & Campana, W. M. (2021) · Glia · doi:10.1002/glia.24098 · Cited by 19
“…by SC EVs including MIP1α, GM-CSF, Cinc-1, fracktalkine, IL-6, VEGF, IP-10, and MIP3α, which are previously reported to be regulated in PNS injury (Be' eri et al., 1998; Bhangoo et al., 2007; Elliott et al., 2009; Perrin et al., 2005; Rotshenker, 2011; Sondell et al., 1999; Zhang et al., 2013).”
BackgroundSuzuki, M., Watanabe, T., Mikami, H., Nomura, M., Yamazaki, T., Irie, T., Yasui, H. I. K., & Ono, S. (2009) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2009.06.021 · Cited by 17
Sun, G., & Ma, Y. (2013) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b12-00841 · Cited by 17
Entezari, M., Ramezani, A., & Yaseri, M. (2014) · Journal of Ophthalmic and Vision Research · doi:10.4103/2008-322x.150815 · Cited by 17
Zhang, Q.-L., Liu, J., Lin, P., & Webster, H. D. (2002) · Journal of the Peripheral Nervous System · doi:10.1046/j.1529-8027.2002.02018.x · Cited by 17
“Tissue culture studies have shown that VEGF enhances axonal outgrowth from explants of sympathetic and dorsal root ganglia and increases the survival of cultured neurons and satellite cells (Sondell et al., 1999).”
BackgroundNeurotrophins and Peripheral Neuropathies
Sahenk, Z. (2006) · Brain Pathology · doi:10.1111/j.1750-3639.2006.00038.x · Cited by 17
“A role for VEGF in regeneration was suggested, with studies illustrating that VEGF stimulates SC invasion and neovascularization of acellular grafts, used to bridge a gap in the sciatic nerve (78, 79).”
BackgroundIslet-Neogenesis-Associated Protein Enhances Neurite Outgrowth from DRG Neurons
Tam, J., Rosenberg, L. C., & Maysinger, D. (2002) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2002.6497 · Cited by 17
Ramesh, S., Qin, Q., Li, Z., Cherief, M., Zhong, L., Archer, M., Xing, X., Thottappillil, N., Balaji, D., Bae, S. S., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2500161122 · Cited by 18
“These aggregate findings suggest a likelihood that NGF secreting endothelial cells may secondarily contribute to the changes in tumor vasculature as both VEGFA and NGF sensitize peripheral sensory nerve fibers to several sensory stimuli ( 70 , 71 ).”
dos Santos, T. C., de Oliveira, M. F., Papa, P. D. C., Dantzer, V., & Miglino, M. A. (2014) · Theriogenology · doi:10.1016/j.theriogenology.2014.06.016 · Cited by 16
Fast rearrangement of the neuronal growth cone�s actincytoskeleton following VEGF stimulation
Bali, P. (2013) · Annals of Neurosciences · doi:10.5214/ans.0972.7531.200307 · Cited by 16
Ward, N. L., Hatala, D. A., Wolfram, J. A., Knutsen, D. A., & Loyd, C. M. (2010) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2010.11.004 · Cited by 16
“KC-specific overexpression of Ang1, VEGF and Ang1-VEGF all resulted in increases in angiogenesis, with the combined Ang1-VEGF further amplifying this response compared to Ang1 alone, confirming prior reports [15, 16, 27, 38], Moreover, all three lines of mice also had increases in cutaneous innervation, thus providing…”
Result
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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