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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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“Besides this, VEGFR-2 expression has been found in cultured superior cervical ganglia and DRGs of adult mice [13].”
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Increased vascularisation enhances axonal regeneration within an acellular nerve conduit.
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“…to exert trophic functions on neuronal cells, as shown by induction of neurite outgrowth and by demonstration of proliferative and antiapoptotic effects of VEGF on neuronal cells of the dorsal root ganglia and superior cervical ganglia through the action of VEGF receptor-2 (Sondell et al., 1999).”
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“While each family’s predominant isoform, VEGF-A165a and VEGF-A165b respectively, is neuroprotective for sensory neurons [13, 14], VEGF-A165a is also pro-nociceptive [15].”
Thyroid Hormones Crosstalk with Growth Factors: Old Facts and New Hypotheses
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Comparison of Acellular Nerve Allograft Modification with Schwann Cells or VEGF
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“In a similar fashion, this neuroprotective effect of VEGF against hypoxic neuronal injury is also observed in in vitro models (Silverman et al. 1999; Sondell et al. 1999; Jin et al. 2000a,b).”
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VEGF Protein Associates to Neurons in Remote Regions following Cortical Infarct
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Glial type specific regulation of CNS angiogenesis by HIFα-activated different signaling pathways
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“In the same assay system, the MAP kinase kinase (MEK) inhibitor PD 098059 at a concentration that effectively blocks Ras–MAP kinase signaling (50 mM) did not prevent BDNF-induced ES (Dudley et al., 1995; Roberson et al., 1999; Sondell et al., 1999).”
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“Beyond protection, VEGF-A has also been shown to promote neuronal growth with cultures of adult mouse dorsal root ganglion and superior cervical ganglion explants (6,8).”
BackgroundIntermittent Hypoxia Conditioning: A Potential Multi-Organ Protective Therapeutic Strategy
Zhang, Q., Zhao, W., Li, S., Ding, Y., Wang, Y., & Ji, X. (2023) · International Journal of Medical Sciences · doi:10.7150/ijms.86622 · Cited by 59
“[99] VEGF also plays a role in angiogenesis and neurotrophic processes by increasing vascular density and blood flow.[3, 100] As such, cerebral ischemia injury could be significantly reduced following hypoxic conditioning due to the increased expression of HIF-1 and its target genes.”
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“The pathogenesis of DPN is not yet fully understood; however, ischemia and oxidative stress are thought to be involved [4,16,17].”
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“Moreover, nerve grafts pretreated with VEGF display an increased outgrowth of Schwann cells in vivo (Sondell et al. 1999a,b).”
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“As well as being an epidermal growth factor and a vascular endothelial growth factor (Rahmatullah et al., 1998; Sondell et al., 1999), bFGF is an exogenous growth factor that promotes the proliferation of Schwann cells, but the use of exogenous bFGF for in vivo regeneration of the peripheral nerves…”
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“VEGF, several studies have also reported its mitogenic effects on certain nonendothelial cells, such as retinal pigment epithelial cells [23], pancreatic duct cells [24], and Schwann cells [25]; as well as on cancer cells, including breast cancer [26–28], prostate cancer [29,30], and gastric adenocarcinoma [31].”
BackgroundNerve and ganglion blood flow in diabetes: An appraisal
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Oxidative Stress Increases Neurogenesis and Oligodendrogenesis in Adult Neural Progenitor Cells
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“Vegf-a and Vegf -r1 expression was increased in differentiated NPC cultures that had been previously exposed to H 2 O 2 .”
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“Although we have not found expression of VEGFR2 on neurons after TBI, earlier reports show expression of VEGFR2 in peripheral nerve cells (Sondell et al., 1999), spinal cord motoneurons (Oosthuyse et al., 2001), immature neurons in vivo and in vitro (Jin et al., 2002) and cortical neurons in vitro…”
BackgroundCell‐Laden Scaffolds for Vascular‐Innervated Bone Regeneration
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“Although this polymorphism may play an important functional role in VEGF gene expression, the association of this and other VEGF polymorphisms with the development of DN remains elusive.(107,108)”
BackgroundSRPK1 inhibition in vivo: modulation of VEGF splicing and potential treatment for multiple diseases
Oltean, S., Gammons, M. V. R., Hulse, R. P., Hamdollah‐Zadeh, M., Mavrou, A., Donaldson, L. F., Salmon, A. H. J., Harper, S. J., Ladomery, M., & Bates, D. O. (2012) · Biochemical Society Transactions · doi:10.1042/bst20120051 · Cited by 55
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“Endothelial cells secrete vascular endothelial growth factor (VEGF), which promotes cell survival and axonal outgrowth (Sondell et al., 1999).”
BackgroundNeonatal hypoxic preconditioning involves vascular endothelial growth factor
Laudenbach, V., Fontaine, R. H., Medja, F., Carmeliet, P., Hicklin, D. J., Gallego, J., Leroux, P., Marret, S., & Gressèns, P. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.12.020 · Cited by 54
Peripheral Nerve Defect Repair With Epineural Tubes Supported With Bone Marrow Stromal Cells
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Enhancing and Regulating Neurite Outgrowth
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“Thus, Sondell et al. (1999) assessed whether VEGF could affect neuronal cell survival, axonal outgrowth, and proliferation of Schwann cells.”
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Anti-VEGF Agents for Ocular Angiogenesis and Vascular Permeability
Kimoto, K., & Kubota, T. (2011) · Journal of Ophthalmology · doi:10.1155/2012/852183 · Cited by 54
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VEGF - A Stimulus for Neuronal Development and Regeneration in the CNS and PNS
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The role of angiogenic and wound-healing factors after spinal cord injury in mammals
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The dose-effectiveness of intranasal VEGF in treatment of experimental stroke
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Local Tolerance and Systemic Safety of Pegaptanib Sodium in the Dog and Rabbit
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“20 Evidence indicates that VEGF 164/165 is the isoform primarily responsible for pathologic ocular neovascularization.”
Dessem, D., Ambalavanar, R., Evancho, M., Moutanni, A., Yallampalli, C., & Bai, G. (2010) · Pain · doi:10.1016/j.pain.2010.02.022 · Cited by 52
“VEGF is also a neurotrophic factor selectively expressed in small-diameter neurons [91].”
BackgroundPark, J., Kim, J., Jeon, W. J., Kim, D. H., Rhyu, I. J., Kim, Y., & Youn, I. (2014) · Neural Regeneration Research · doi:10.4103/1673-5374.137587 · Cited by 52
“…that vascular endothelial growth factor and endothelial cell growth factor, which are major growth factors in PRP, promote neoangiogenesis in regenerating nerves and may contribute to early axonal sprouting and myelination (Sondell et al., 1999; Hobson et al., 2000; Pereira Lopes et al., 2011).”
Roles of Vascular Endothelial Growth Factor in Amyotrophic Lateral Sclerosis
Pronto‐Laborinho, A. C., Pinto, S., & de Carvalho, M. A. (2014) · BioMed Research International · doi:10.1155/2014/947513 · Cited by 55
“In nervous system, VEGFR-2 stimulates migration, proliferation, and survival of different neural cell types [90, 102, 103].”
BackgroundDiCicco-Bloom, E. M., Lelièvre, V., Zhou, X., Rodriguez, W. I., Nguyen‐Van‐Tam, J. S., & Waschek, J. A. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.03.028 · Cited by 52
“Previously defined Schwann cell mitogens include PDGF, FGF, VEGF, and neuregulins (Eccleston et al., 1990; Sondell et al., 1999; Tabernero et al., 1998; Verdi et al., 1996), which generally employ tyrosine kinase cascades to enhance proliferation.”
BackgroundSuzuki, T., Sekido, H., Kato, N., Nakayama, Y., & Yabe‐Nishimura, C. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02824.x · Cited by 51
“1999), and vascular endothelial growth factor (Sondell et al. 1999).”
Li, Y., Luo, J.-M., Lau, B. W.-M., Zheng, G., Fu, S., Wang, T., Zeng, H., So, K., Chung, S. K., Tong, Y., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022901 · Cited by 52
“Flk1, a VEGF receptor, mediates the activation of p44/42MAPK and subsequently promotes neurite extension in peripheral or central neurons [29,30].”
BackgroundFacilitate Angiogenesis and Neurogenesis by Growth Factors Integrated Decellularized Matrix Hydrogel
Li, R., Xu, J., Rao, Z., Deng, R., Xu, Y., Qiu, S., Long, H., Zhu, Q., Liu, X., Bai, Y., et al. (2020) · Tissue Engineering Part A · doi:10.1089/ten.tea.2020.0227 · Cited by 51
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Kusaka, N., Sugiu, K., Tokunaga, K., Katsumata, A., Nishida, A., Namba, K., Hamada, H., Nakashima, H., & Date, I. (2005) · Journal of neurosurgery · doi:10.3171/jns.2005.103.5.0882 · Cited by 51
VEGF is increased in serum but not in spinal cord from patients with amyotrophic lateral sclerosis
Nygren, I., Larsson, A. O., Johansson, A., & Askmark, H. (2002) · Neuroreport · doi:10.1097/00001756-200212030-00007 · Cited by 51
Effect of vegf gene therapy and hyaluronic acid film sheath on peripheral nerve regeneration
Zor, F., Deveci, M., Kilic, A., Ozdag, M. F., Kurt, B., Sengezer, M., & SÖnmez, T. T. (2014) · Microsurgery · doi:10.1002/micr.22196 · Cited by 50
“Studies have shown that VEGF not only stimulates angiogenesis but also has neurotrophic effects.(11,12) Various agents are used to alter the microenvironment at the coaptation line.”
BackgroundResultKano, F., Matsubara, K., Ueda, M., Hibi, H., & Yamamoto, A. (2016) · Stem Cells · doi:10.1002/stem.2534 · Cited by 50
Masłowska, K., Halik, P. K., Tymecka, D., Misicka, A., & Gniazdowska, E. (2021) · Cancers · doi:10.3390/cancers13051072 · Cited by 53
“Activation of VEGFR-2 leads to stimulation of the cell cycle, proliferation, migration, cell differentiation, angiogenesis, increased permeability of blood vessels but also inhibition of the apoptotic death and up-regulation of VEGF-A synthesis in endothelial cells [58,101].”
BackgroundDose-Response Features of Neuroprotective Agents: An Integrative Summary
Calabrese, E. J. (2008) · Critical Reviews in Toxicology · doi:10.1080/10408440801981965 · Cited by 50
“…hormetic dose responses for neurite outgrowth include a variety of endogenous agonists such as melanocortins (Joosten et al., 1995), VEGF (Sondell et al., 1999), EPO (Bocker-Meffert et al., 2002), FGF (Williams et al., 1994a, 1994c), NGF (Rosoff et al., 2004), and arachidonic acid…”
BackgroundInfluentialLee, E. J., Xu, L., Kim, G.-H., Kang, S. K., Lee, S.-W., Park, S., Kim, S., Choi, T. H., & Kim, H.-S. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.06.047 · Cited by 49
Peripheral nerve morphogenesis induced by scaffold micropatterning
Cerri, F., Salvatore, L., Memon, D., Boneschi, F. M., Madaghiele, M., Brambilla, P., Carro, U. D., Taveggia, C., Riva, N., Trimarco, A., et al. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.01.069 · Cited by 49
“The expression of vascular endothelial growth factors (Vegf), a crucial molecule for angiogenesis and nerve regeneration [27], was also up-regulated in both groups (Fig.”
Salehi, M., Naseri‐Nosar, M., Ebrahimi‐Barough, S., Nourani, M., Khojasteh, A., Farzamfar, S., Mansouri, K., & Ai, J. (2017) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-017-0535-8 · Cited by 49
“…vascular endothelial growth factor (VEGF), fibroblast growth factor II (FGF-II), and transforming growth factor-b (TGF-b), which their proliferative effects on SCs have been demonstrated by several studies (Davis and Stroobant 1990; Sondell et al. 1999; Danielsen et al. 1988; Ridley et al. 1989).”
BackgroundHausott, B., & Klimaschewski, L. P. (2019) · The Anatomical Record · doi:10.1002/ar.24126 · Cited by 49
“Similarly, ERK blockade did not interfere with spontaneous axon outgrowth of adult DRG explants, while growth factor-induced outgrowth was significantly impaired (Sjogreen et al., 2000; Sondell et al., 1999).”
BackgroundZhang, J., Liu, X., Ma, K., Chen, M., Xu, H., Niu, X., Gu, H., Wang, R., Chen, X., & Sun, H. (2020) · Biomaterials Science · doi:10.1039/c9bm01446b · Cited by 49
Vascular endothelial growth factor (VEGF) expression in noise-induced hearing loss
Picciotti, P. M., Fetoni, A. R., Paludetti, G., Wolf, F. I., Torsello, A., Troiani, D., Ferraresi, A., Pola, R., & Sergi, B. (2006) · Hearing Research · doi:10.1016/j.heares.2006.02.004 · Cited by 48
Hypoxic-preconditioning induces neuroprotection against hypoxia–ischemia in newborn piglet brain
Ara, J. E., Fekete, S. M. W., Frank, M., Golden, J. A., Pleasure, D., & Valencia, I. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.04.021 · Cited by 47
“In cultured superior cervical and dorsal route ganglion neurons, VEGF promotes both axonal outgrowth and cell survival (Sondell et al., 1999), and improves neuronal survival in organotypic midbrain explant cultures (Silverman et al., 1999).”
BackgroundZhang, Y., Li, Y., Wang, S., Han, Z., Huang, X., Li, S., Chen, F., Niu, R., Dong, J.-F., Jiang, R., et al. (2013) · Journal of Surgical Research · doi:10.1016/j.jss.2013.05.073 · Cited by 48
“Once homed, these cells differentiate and secrete VEGF,which promotes the survival and proliferation of newly homed EPCs [35,36] as well as stimulates the axonal outgrowth of neurons [37,38].”
BackgroundVascular growth factors in neuropsychiatry
Newton, S. S., Fournier, N. M., & Duman, R. S. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1281-9 · Cited by 48
“Activation of the MAPK and Akt pathways is well known to mediate important trophic effects related to synaptic plasticity, neuronal survival/protection and neurogenesis [20, 21, 37, 121, 142, 143].”
BackgroundInvolvement of RB gene family in tumor angiogenesis
Gabellini, C., Del Bufalo, D., & Zupi, G. (2006) · Oncogene · doi:10.1038/sj.onc.1209631 · Cited by 47
“In fact, in addition to the well-established proangiogenic role of VEGF, this molecule appears to have direct neurotrophic and neuroprotective functions (Sondell et al., 1999; Jin et al., 2000; Sondell et al., 2000) and more recently to act as a neurogenesis factor (Jin et al., 2002).”
BackgroundWhat can we learn about stroke from retinal ischemia models?
D’Onofrio, P. M., & Koeberle, P. D. (2012) · Acta Pharmacologica Sinica · doi:10.1038/aps.2012.165 · Cited by 46
Feng, Y., Rhodes, P. G., & Bhatt, A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.01.050 · Cited by 47
“In vitro studies have demonstrated that VEGF is a otent neurotrophic factor which also confers protection to njured neurons (Sondell et al., 1999; Jin et al., 2000; Kilic t al., 2006).”
Laporte, L. D., Rieux, A. D., Tuinstra, H. M., Zelivyanskaya, M. L., Clerck, N. M. D., Postnov, A., Véronique Préat, A., & Shea, L. D. (2011) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.33112 · Cited by 47
“Several axon guidance cues are involved in blood vessel guidance,(19,20) while VEGF and FGF-2 have been suggested to play a role in nerve regeneration.(2,4,21) VEGF can pattern small arteries along peripheral nerves,(22) stimulate neurogenesis of neural stem cells in the adult central nervous system,(23) have a mitoge…”
BackgroundEffect of eye NGF administration on two animal models of retinal ganglion cells degeneration.
Colafrancesco, V., Coassin, M., Rossi, S., & Aloe, L. (2011) · PubMed · doi:10.4415/ann_11_03_08 · Cited by 47
“In fact, a key mechanism leading to optic nerve injury and RGC loss is the elevated intraocular pressure [8], while in DR the degenerative event of these cells is associated to proliferation of new blood vessels, increased vascular permeability and vascular occlusion [9] and altered levels of vascular endothelial grow…”
BackgroundMuratori, L., Gnavi, S., Fregnan, F., Mancardi, A., Raimondo, S., Perroteau, I., & Geuna, S. (2018) · The Anatomical Record · doi:10.1002/ar.23842 · Cited by 49
“…administration enhances axonal outgrowth from dorsal root ganglia adult mice explants promoting the survival of neurons and satellite glial cells (Sondell, Lundborg et al. 1999; Sondell, Lundborg et al. 1999; Hobson, Green et al. 2000; Brockington, Lewis et al. 2004; Pereira Lopes, Lisboa et al.…”
Cheng, L., Jia, H., Löhr, M., Bagherzadeh, A., Holmes, D. I. R., Selwood, D. L., & Zachary, I. C. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402488200 · Cited by 46
Wuestefeld, R., Chen, J., Meller, K., Brand‐Saberi, B., & Theiß, C. (2012) · Glia · doi:10.1002/glia.22325 · Cited by 46
“In the recent years, it was shown that VEGF also has a trophic activity on neurons (Sondell et al., 1999; Zachary, 2005).”
BackgroundKolar, M. K., Kingham, P. J., Novikova, L. N., Wiberg, M., & Novikov, L. N. (2014) · Stem Cells and Development · doi:10.1089/scd.2013.0416 · Cited by 46
“As well as the angiogenic effects of VEGF-A, it has also been shown to exert neuroprotective effects when injected into the injured tissue, by reducing retrograde degeneration, apoptosis and spinal cord tissue loss [56,57].”
Influence of Experimental Diabetes on the Microcirculation of Injured Peripheral Nerve
Kennedy, J. M., & Zochodne, D. W. (2002) · Diabetes · doi:10.2337/diabetes.51.7.2233 · Cited by 46
PEDF and VEGF-A Output from Human Retinal Pigment Epithelial Cells Grown on Novel Microcarriers
Falk, T., Congrove, N. R., Zhang, S., McCourt, A. D., Sherman, S. J., & McKay, B. S. (2012) · BioMed Research International · doi:10.1155/2012/278932 · Cited by 45
“VEGF-A has been shown to cause axonal outgrowth on cultured ganglia in a dose-responsive manner [31].”
BackgroundSemaphorin and neuropilin expression in motoneurons after intraspinal motoneuron axotomy
Lindholm, T., Sköld, M. K., Suneson, A., Carlstedt, T. P., Cullheim, S., & Risling, M. (2004) · Neuroreport · doi:10.1097/00001756-200403220-00015 · Cited by 45
“Induction of VEGF and NP1 can be found in the VFL scar [16].”
BackgroundInfluentialBogaert, E., Damme, P. V., Bosch, L. V. D., & Robberecht, W. (2006) · Muscle & Nerve · doi:10.1002/mus.20609 · Cited by 45
VEGF: necessary to prevent motoneuron degeneration, sufficient to treat ALS?
Lambrechts, D., Storkebaum, E., & Carmeliet, P. (2004) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2004.04.004 · Cited by 46
Rezza, A. S., Külahçı, Y., Gorantla, V. S., Zor, F., & Drzeniek, N. M. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.863969 · Cited by 49
“Beside its proangiogenic activity, VEGF can stimulate axonal outgrowth and promote Schwann cell proliferation and migration, suggesting an entire palette of additional mechanisms through which VEGF could enhance nerve regeneration (Sondell et al., 1999; Muratori et al., 2018).”
BackgroundmiR-376b-5p regulates angiogenesis in cerebral ischemia
Li, L., Huang, Q. B., Zhang, N., WANG, G.-B., & LIU, Y.-H. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.2172 · Cited by 44
“VEGFA also demonstrated a neuroprotective effect by improving local microcirculation, promoting the injured nerve generation and neural proliferation (27-31).”
Najafi, B., Crews, R. T., & Wrobel, J. S. (2013) · Gerontology · doi:10.1159/000352072 · Cited by 45
Liu, Q., Huang, J., Shao, H., Song, L., & Zhang, Y. (2016) · RSC Advances · doi:10.1039/c5ra22054h · Cited by 44
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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