Vascular endothelial growth factor (VEGF) and its role in the central nervous system: A new element in the neurotrophic hypothesis of antidepressant drug action

Neuropeptides

Volumn 46, Issue 1, 2012, Pages 1-10

  Nowacka, Marta Maria ^a   Obuchowicz, Ewa ^a  

^a MEDICAL UNIVERSITY OF SILESIA   (Poland)

Author keywords

Antidepressant drugs; Depression; Neurogenesis; Neuroprotection; Signal transduction; Synaptic plasticity; Vascular endothelial growth factor (VEGF)

Indexed keywords

AMITRIPTYLINE; ANTIDEPRESSANT AGENT; DESIPRAMINE; FLUOXETINE; SEMAXANIB; SERTRALINE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3; VENLAFAXINE;

ANGIOGENESIS; ASTROCYTE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; DRUG MECHANISM; ELECTROCONVULSIVE THERAPY; GENE EXPRESSION; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MAJOR DEPRESSION; MICROGLIA; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTIDEPRESSIVE AGENTS; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; ENDOTHELIAL CELLS; HUMANS; MICE; NERVE GROWTH FACTORS; NEURONAL PLASTICITY; NEURONS; NEUROPROTECTIVE AGENTS; RATS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

ANIMALIA;

EID: 84855951147     PISSN: 01434179     EISSN: 15322785     Source Type: Journal    
DOI: 10.1016/j.npep.2011.05.005     Document Type: Review

References (69)

1. Autiero M., De Smet F., Claes F., Carmeliet P. Role of neural guidance signals in blood vessel navigation. Cardiovasc. Res. 2005, 65:629-638.
2. Azam F., Mehta S., Harris A.L. Mechanism of resistance to antiangiogenesis therapy. Eur. J. Cancer 2010, 46:1323-1332.
3. Bergström A., Jayatissa M.N., MØrk A., Wiborg O. Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study. Brain Res. 2008, 1196:41-52.
4. Blumberg H.P., Wang F., Chepenik L.G., Kalmar J.H., Edmiston E., Duman R.S., Gelernter J. Influence of vascular endothelial growth factor variation on human hippocampus morphology. Biol. Psychiatry 2008, 64:901-903.
5. Brochington A., Lewist C., Wharton S., Shaw P.J. Vascular endothelial growth factor and the nervous sysyem. Neuropathol. Appl. Neurobiol. 2004, 30:427-446.
6. Carmeliet P., Strokebaum E. Vascular and neuronal effect of VEGF in the nervous system: implications for neurological disorders. Cell Dev. Biol. 2002, 13:39-53.
7. Cross M.J., Claesson-Welsh L. FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol. Sci. 2001, 22:201-207.
8. Cross M.J., Dixelius J., Matsumoto T., Claesson-Welsh L. VEGF-receptor signal transduction. Trends Biochem. Sci. 2003, 28:488-494.
9. Cursiefen C., Chen L., Leonardo P.B., Jackson D., Cao J. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J. Clin. Invest. 2004, 7:1040-1050.
10. Eichmann A., Le Noble F., Auterio M., Carmeliet P. Guidance of vascular and neural network formation. Curr. Opin. Neurobiol. 2005, 15:108-115.
11. Elfving B., Plougmann P.H., Wegener G. Differential brain, but not serum VEGF levels in a genetic model of depression. Neurosci. Lett. 2010, 474:13-16.
12. Fabel K., Fabel K., Tam B., Kaufer D., Baiker A., Simmons N., Kuo C.J., Palmer T.D. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci. 2003, 18:2803-2812.
13. Ferrara N. Vascular endothelial growth factor. Arterioscler. Thromb. Vasc. Biol. 2009, 29:789-791.
14. Ferrara N., Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr. Rev. 1997, 1:4-25.
15. Folkman J., D'Amore P.A. Blood vessel formation: what is its molecular basis?. Cell 1996, 87:1153-1155.
16. Greene J., Banasr M., Lee B., Warner-Schmidt J., Duman R.S. Vascular endothelial growth factor signaling is required for the behavioral actions of antidepressant treatment: pharmacological and cellular characterization. Neuropsychopharmacology 2009, 1-10.
17. Harms K.M., Li L., Cunningham L.A. Murine neural stem/progenitor cells protect neurons against ischemia by HIF-1-regulated VEGF signaling. PloS ONE 2010, 5(3):e9767. 10.1371/journal.pone.0009767.
18. Holmes K., Roberts O.L., Thomas A.M., Cross M.J. Vascular endothelial growth factor receptor-2: structure, function, intracellular signaling and therapeutic inhibition. Cell. Signal. 2007, 19:2003-2012.
19. Iga J.-ichi., Ueno S.-ichi., Yamauchi K., Numata S., Tayoshi-Shibuya S., Kinouchi S., Nakataki M., Song H., Hokoishi K., Tanabe H., Sano A., Ohmori T. Gene expression and association analysis of vascular endothelial growth factor in major depressive disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31:658-663.
20. Jin K., Zhu Y., Sun Y., Mao X.O., Xie L., Greenberg D.A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. PNAS 2002, 18:11946-11950.
21. Joo J.-Y., Kim B.-W., Lee J.-S., Park J.-Y., Kim S., Yun Y.-J., Lee S.-H., Lee S.-H., Rhim H., Son H. Activation of NMDA receptors increases proliferation and differentiation of hippocampal neural progenitor cells. J. Cell Sci. 2007, 120:1358-1370.
22. Kahl K.G., Bens S., Ziegler K., Rudolf S., Kordon A., Dibbelt L., Schweiger U. Angiogenic factors in patients with current major depressive disorder comorbid with borderline personality disorder. Psychneuroendocrinology 2009, 34:353-357.
23. Khaibullina A.A., Rosenstein J.M., Krum J.M. Vascular endothelial growth factor promotes neurite maturation in primary CNS neuronal cultures. Brain Res. Dev. Brain Res. 2004, 148:59-68.
24. Kim W.B., Choi M., Kim Y.-S., Park H., Lee H.-R., Yun C.-O., Kim E.J., Choi J.-S., Kim S., Rhim H., Kaang B.-K., Son H. Vascular endothelial growth factor (VEGF) signaling regulates hippocampal neurons by elevation of intracellular calcium and activation of calcium/calmodulin protein kinase II and mammalian target of rapamycin. Cell. Signal. 2008, 20:714-725.
25. Kułak W., Sobaniec W. Mechanisms of damage and plasticity of brain. Terapia 2006, 10:56-59.
26. Lee H.-T., Chang Y.-C., Tu Y.-F., Huang C.-C. VEGF-A/VEGFR2 signaling leading to cAMP response element-binding protein phosphorylation is a shared pathway underlying the protective effect of preconditioning on neurons and endothelial cells. J. Neurosci. 2009, 29:4356-4368.
27. Lee E., Son H. Adult hippocampal neurogenesis and related neurotrophic factors. BMB reports 2009, 239-244.
28. Li B., Xu W., Luo C., Gozal D., Liu R. VEGF-induced activation of the PI3-K/Akt pathway reduces mutant SOD1-mediated motor neuron cell death. Mol. Brain Res. 2003, 111:155-164.
29. Lucas G., Rymar V.V., Du J., Mnie-Filali O., Bisgaard C., Manta S. Serotonin (4) (5-HT(4)) receptor agonists are putative antidepressants with rapid onset of action. Neuron 2007, 55:712-725.
30. Madsen T.M., Treschow A., Bengzon J., Bolwig T.G., Lindvall O., Tingström A. Increased neurogenesis in a model of electroconvulsive therapy. Biol. Psychiatry 2000, 47:1043-1049.
31. Mani N., Khaibullina A., Krum J.M., Rosenstein J.M. Astrocyte growth effects of vascular endothelial growth factor (VEGF) application to perinatal neocortical explants: receptor mediation and signal transduction pathways. Exp. Neurol. 2005, 192:394-406.
32. Mani N., Khaibullina A., Krum J.M., Rosenstein J.M. Vascular endothelial growth factor enhances migration of astroglial cells in subventricular zone neurosphere cultures. J. Neurosci. Res. 2010, 88:248-257.
33. Manoonkitiwongsa P.S., Schultz R.L., McCreery D.B., Whitter E.F. Neuroprotection of ischemic brain by vascular endothelial growth factor is critically dependent on proper dosage and may be compromised by angiogenesis. J. Cerebr. Blood Flow Metab. 2004, 24:693-702.
34. Maurer M.H., Tripps W.K.C., Feldman R.E., Kuschinsky W. Expression of vascular endothelial growth factor and its receptors in rat neural stem cells. Neurosci. Lett. 2003, 344:165-168.
35. McCloskey D.P., Croll S.D., Scharfman H.E. Depression of synaptic transmission by vascular endothelial growth factor in adult rat hippocampus and evidence for increased efficacy after chronic seizures. J. Neurosci. 2005, 25:8889-8897.
36. McCloskey D.P., Hintz T.M., Scharfman H.E. Modulation of vascular endothelial growth factor (VEGF) expression in motor neurons and its electrophysiological effects. Brain Res. Bull. 2008, 76:36-44.
37. Mukouyama Y.S., Shin D., Britsch S., Taniguchi M., Anderson D.J. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 2002, 109:693-705.
38. Nakamura, K., Tan, F., Li, Z., Thiele, C.J., 2010. NGF activation of TrkA inducesvascular endothelial growth factor expression via induction of hypoxia inducible-factor 1- Mol. Cell. Neurosci. doi:10.1016/j.mcn.2010.12.002.
39. Namiecińska M., Marciniak K., Nowak J.Z. VEGF as an angiogenic, neurotrophic, and neuroprotective factor. Poste{ogonek}py Hig. Med. Dosw. 2005, 59:573-583.
40. Neufeld G., Cohen T., Gengrinovitch S., Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB 1999, 13:9-22.
41. Ogunshola O.O., Antic A., Donoghue M.J., Fan S.-Y., Kim H., Stewart W.B., Madri J.A., Ment L.R. Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J. Biol. Chem. 2002, 277:11410-11415.
42. Olsson A.K., Dimberg A., Kreuger J., Claesson-Welsh L. VEGF receptor signaling-in control of vascular function. Nat. Rev. Mol. Cell Biol. 2006, 7:359-371.
43. Proia P., Schiera G., Mineo M., Ingrassia A.M.R., Santoro G., Savettieri G., Di Liegro I. Astrocytes shed extracellular vesicles that contain fibroblast growth factor-2 and vascular endothelial growth factor. Int. J. Mol. Med. 2008, 21:63-67.
44. Quinn T.P., Peters K.G., De Vries C., Ferrara N., Williams L.T. Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Cell Biol. 1993, 90:7533-7537.
45. Robinson C.J., Stringer S.E. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J. Cell Sci. 2001, 114:853-865.
46. Rosenstein J.M., Krum J.M. New roles for VEGF in nervous tissue-beyond blood vessels. Exp. Neurol. 2004, 187:246-253.
47. Rosenstein J.M., Mani N., Khaibullina A., Krum J.M. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J. Neurosci. 2003, 23:11036-11044.
48. Ruiz De Almodovar C., Lambrechts D., Mazzone M., Carmeliet P. Role and therapeutic potential of VEGF in the nervous system. Physiol. Rev. 2009, 89:607-648.
49. Schratzberger P., Schratzberger G., Silver M., Curry C., Kearney M., Magner M., Alroy J., Adelman L.S., Weinberg D.H., Ropper A.H., Isner J.M. Favorable effect of VEGF gene transfer on ischemic peripheral neuropathy. Nature 2000, 6:405-413.
50. Segi-Nishida E., Warner-Schmidt J.L., Duman R.S. Electroconvulsive seizure and VEGF increase the proliferation of neural stem-like cells in rat hippocampus. PNAS 2008, 32:11352-11357.
51. Senger D.R., Galli S.J., Dvorak A.M., Peruzzi C.A., Havrey V.S., Dvorak M.F. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983, 219:983-985.
52. Strokebaum E., Lambrechts D., Carmeliet P. VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. BioEssays 2004, 26:943-954.
53. Sun Y., Jin K., Xie L., Childs J., Mao X.O., Logvinova A., Greenberg D.A. VEGF-induced neuroprotection, neurogenesis and angiogenesis after focal cerebral ischemia. J. Clin. Invest. 2003, 111:1843-1851.
54. Sun F.-Y., Guo X. Molecular and cellular mechanisms of neuroprotection by vascular endothelial growth factor. J Neurosci. Res. 1999, 79:180-184.
55. 4 receptor partial agonist, SL65.0155: behavioral and neurochemical studies in rats. Prog. Neuropsychopharmacol Biol Psychiatry 2009, 33:1205-1210.
56. Tassona, E., Maran, C., Masola, V., Bradaschia, A., Garbisa, S., Onisto, M., 2010. Antidepressant hyperforin up-regulates VEGF in CNS tumor cells. Pharmacol. Res. doi:10.1016/j.phrs.2010.09.005.
57. Terman B.I., Stoletov K.V. VEGF and tumor angiogenesis. Einstein Q. J. Biol. Med. 2001, 18:59-66.
58. Tsai S.-J., Hong C.-J., Liou Y.-J., Chen T.-J., Chen M.-L., Hou S.-J., Yen F.-C., Younger Yu W.-Y. Haplotype analysis of single nucleotide polymorphisms in the vascular endothelial growth factor (VEGFA) gene and antidepressant treatment response in major depressive disorder. Psychiatry Res. 2009, 169:113-117.
59. Ventriglia M., Zanardini R., Pedrini L., Placentino A., Nielsen M.G., Gennarelli M., Bocchio-Chiavetto L. VEGF serum levels in depressed patients during SSRI antidepressant treatment. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:146-149.
60. Vicale M., Leggio G.M., Mazzola C., Drago F. Cognitive effects of SL65.0155, a serotonin 5-HT4 receptor partial agonist, in animal model of amnesia. Brain Res. 2006, 1121:207-215.
61. Viikki M., Anttila S., Kampman O., Illi A., Huuhka M., Setälä-Soikkeli E., Mononen N., Lehtimäki T., Leinonen E. Vascular endothelial growth factor (VEGF) polymorphism is associated with treatment resistant depression. Neurosci. Lett. 2010, 477:105-108.
62. Wada T., Haigh J.J., Ema M., Hitoshi S., Chaddah R., Rossant J., Nagy A., van der Kooy D. Vascular endothelial growth factor directly inhibits primitive neural stem cell survival but promotes definitive neural stem cell survival. J. Neurosci. 2006, 26:6803-6812.
63. Warner-Schmidt J.L., Duman R.S. VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. PNAS 2007, 11:4647-4652.
64. Warner-Schmidt J.L., Duman R.S. VEGF as a potential target for therapeutic intervention in depression. Curr. Opin. Pharmacol. 2008, 8:14-19.
65. Wick A., Wick W., Weltenberger J., Weller M., Dichgans J., Schulz J.B. Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J. Neurosci. 2002, 22:6401-6407.
66. Yang S.-Z., Zhang L.-M., Huang Y.-L., Sun F.-Y. Distribution of Flk-1 and Flt-1 receptors in neonatal and adult rat brains. Anat. Rec. 2003, 274A:851-856.
67. Zachary I. Integration of mitogenic and migratory signals from G-Protein-coupled receptor and tyrosine kinases. Biochem. Soc. Trans. 2003, 31:1171-1177.
68. Zhang Z.G., Zhang L., Jiang Q., Zhang R. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest. 2000, 106:829-838.
69. Zhu Y., Jin K., Mao X.O., Greenberg D.A. Vascular endothelial growth factor promotes proliferation of cortical neuron precursors by regulating E2F expression. FASEB 2003, 17:186-193.