Multiple neurotrophic effects of VEGF on cultured neurons

Neuropeptides

Volumn 44, Issue 4, 2010, Pages 323-331

  Sanchez, Alma ^a   Wadhwani, Suchin ^a   Grammas, Paula ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

Amyloid beta; Apoptosis; Bcl 2; Caspase 3; P38 MAP kinase; PEDF; Survival

Indexed keywords

AMYLOID BETA PROTEIN; CASPASE 3; DICOUMAROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PIGMENT EPITHELIUM DERIVED FACTOR; PROTEIN BCL 3; STRESS ACTIVATED PROTEIN KINASE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL LEVEL; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RAT;

AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA; DICUMAROL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDE FRAGMENTS; RATS; RECOMBINANT PROTEINS; UNCOUPLING AGENTS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 77953545998     PISSN: 01434179     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.npep.2010.04.002     Document Type: Article

References (67)

1. Alard, A., Fabre, B., Anesia, R., Marboeuf, C., Pierre, P., Susini, C., Bousquet, C., Pyronnet, S., 2009. NAD(P)H quinone-oxydoreductase 1 (NQO1) protects eIF4GI from degradation by the proteosome. Mol. Cell Biol., December 22 [Epub ahead of print].
2. Antonsson B., Martinou J.C. The Bcl-2 protein family. Exp. Cell. Res. 2000, 407:802-809.
3. Barnstable C., Tombran-Tink J. Neuroprotective and antiangiogenic actions of PEDF in the eye: molecular targets and therapeutic potential. Prog. Retin. Eye Res. 2004, 23:561-577.
4. Bhisitkul R.B., Rutar T. Expanding treatment options in age-related macular degeneration. Int. Ophthalmol. Clin. 2006, 46:123-129.
5. Böcker-Meffert S., Rosenstiel P., Röhl C., Warneke N., Held-Feindt J., Sievers J., Lucius R. Erythropoietin and VEGF promote neural outgrowth from retinal explants in postnatal rats. Invest. Ophthalmol. Vis. Sci. 2002, 43:2021-2026.
6. Bürger S., Noack M., Kirazov L.P., Kirazov E.P., Naydenov C.L., Kouznetsova E., Yafai Y., Schliebs R. Vascular endothelial growth factor (VEGF) affects processing of amyloid precursor protein and beta-amyloidosis in brain slice cultures derived from transgenic Tg2576 mouse brain. Int. J. Dev. Neurosci. 2009, 27:517-523.
7. Cao L., Jiao X., Zuzga D.S., Liu Y., Fong D.M., Young D., During M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 2004, 36:827-835.
8. Choi W.S., Eom D.S., Han B.S., Kim W.K., Han B.H., Choi E.J., Oh T.H., Markelonis G.J., Cho J.W., Oh Y.J. Phosphorylation of p38 MAPK induced by oxidative stress is linked to activation of both caspase-8- and -9-mediated apoptotic pathways in dopaminergic neurons. J. Biol. Chem. 2004, 279:20451-20460.
9. Cross J.V., Deak J.C., Rich E.A., Qian Y., Lewis M., Parrot L.A., Mochida K., Gustafson D., Vande Pol S., Templeton D.J. Quinone reductase inhibitors block SAPK/JNK and NFκB pathways and potentiate apoptosis. J. Biol. Chem. 1999, 274:31150-31154.
10. Detmar M., Brown L.F., Schon M.P., Elicker B.M., Velasco P., Richard L., Fukumura D., Monsky W., Claffey K.P., Jain R.K. Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J. Invest. Dermatol. 1998, 111:1-6.
11. Dvorak H.F., Brown L.F., Detmar M., Dvorak A.M. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 1995, 146:1029-1039.
12. Ferrara N., Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr. Rev. 1997, 18:4-25.
13. Grammas P., Moore P., Weigel P.H. Microvessels from Alzheimer's disease brains kill neurons in vitro. Am. J. Pathol. 1999, 154:337-342.
14. Grazul-Bilska A.T., Johnson M.L., Bilski J.J., Redmer D.A., Reynolds L.P., Abdullah A., Abdullah K.M. Wound healing: the role of growth factors. Drugs Today (Barc.) 2003, 39:787-800.
15. Hernandez A., Lopez-Lluch G., Bernal J.A., Navas P., Pintor-Toro J.A. Dicoumarol down regulates human PTTG1/Securin mRNA expression through inhibition of Hsp90. Mol. Cancer Ther. 2008, 7:474-482.
16. Hou S.T., Xie X., Baggley A., Park D.S., Chen G., Walker T. Activation of the Rb/E2F1 pathway by the nonproliferative p38 MAPK during Fas (APO1/CD95)-mediated neuronal apoptosis. J. Biol. Chem. 2002, 277:48764-48770.
17. Issa R., Krupinski J., Bujny T., Kumar S., Kaluza J., Kumar P. Vascular endothelial growth factor and its receptor, KDR, in human brain tissue after ischemic stroke. Lab. Invest. 1999, 79:417-425.
18. Jeohn G.H., Cooper C.L., Wilson B., Chang R.C., Jang K.J., Kim H.C., Liu B., Hong J.S. P38 MAP kinase is involved in lipopolysaccharide-induced dopaminergic neuronal cell death in rat mesencephalic neuron-glia cultures. Ann. N. Y. Acad. Sci. 2002, 962:332-346.
19. Jin K.L., Mao X.O., Greenberg D.A. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc. Natl. Acad. Sci. USA 2000, 97:10242-10247.
20. Jin K.L., Mao X.O., Nagayama T., Goldsmith P.C., Greenberg D.A. Induction of vascular endothelial growth factor receptors and phosphatidylinositol 3'-kinase/Akt signaling by global cerebral ischemia in the rat. Neuroscience 2000, 100:713-717.
21. Jin K., Mao X.O., Batteur S.P., McEachron E., Leahy A., Greenberg D.A. Caspase-3 and the regulation of hypoxic neuronal death by vascular endothelial growth factor. Neuroscience 2001, 108:351-359.
22. Junn E., Mouradian M.M. Apoptotic signaling in dopamine-induced cell death: the role of oxidative stress, p38 mitogen-activated protein kinase, cytochrome c and caspases. J. Neurochem. 2001, 78:374-383.
23. Kalaria R.N., Cohen D.L., Premkumar D.R., Nag S., LaManna J.C., Lust W.D. Vascular endothelial growth factor in Alzheimer's disease and experimental cerebral ischemia. Brain Res. Mol. Brain Res. 1998, 62:101-105.
24. 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.
25. Kilic E., Kilic U., Wang Y., Bassetti C.L., Marti H.H., Hermann D.M. The phosphatidylinositol-3 kinase/Akt pathway mediates VEGF's neuroprotective activity and induces blood brain barrier permeability after focal cerebral ischemia. FASEB J. 2006, 20:1185-1187.
26. Kilic U., Kilic E., Jarve A., Guo Z., Spudich A., Bieber K., Barzena U., Bassetti C.L., Marti H.H., Hermann D.M. Human vascular endothelial growth factor protects axotomized retinal ganglion cells in vivo by activating ERK-1/2 and Akt pathways. J. Neurosci. 2006, 26:12439-12446.
27. Kim K.J., Li B., Winer J., Armanini M., Gillett N., Phillips H.S., Ferrara N. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 1993, 362:841-844.
28. Kumar P., Miller A.I., Polverini P.J. P38 MAPK mediates gamma-irradiation-induced endothelial cell apoptosis, and vascular endothelial growth factor protects endothelial cells through the phosphoinositide 3-kinase-Akt-Bcl-2 pathway. J. Biol. Chem. 2004, 279:43352-43360.
29. Lee J.D., Huh J.E., Jeon G., Yang H.R., Woo H.S., Choi D.Y., Park D.S. Flavonol-rich RVHxR from Rhus verniciflua stokes and its major compound fisetin inhibits inflammation-related cytokines and angiogenic factor in rheumatoid arthritic fibroblast-like synovial cells and in vivo models. Int. Immunopharmacol. 2009, 9:268-276.
30. Leung D.W., Cachianes G., Kuang W.J., Goeddel D.V., Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989, 246:1306-1309.
31. Matsuzaki H., Tamatani M., Yamaguchi A., Namikawa K., Kiyama H., Vitek M.P., Mitsuda N., Tohyama M. Vascular endothelial growth factor rescues hippocampal neurons from glutamate-induced toxicity: signal transduction cascades. FASEB J. 2001, 15:1218-1220.
32. Merrill M.J., Oldfield E.H. A reassessment of vascular endothelial growth factor in central nervous system pathology. J. Neurosurg. 2005, 103:853-868.
33. Ng Y.S., Krilleke D., Shima D.T. VEGF function in vascular pathogenesis. Exp. Cell Res. 2006, 312:527-537.
34. Nieves B.J., D'Amore P.A., Bryan B.A. The function of vascular endothelial growth factor. Biofactors 2009, 35:332-337.
35. Oosthuyse B., Moons L., Storkebaum E., Beck H., Nuyens D., Brusselmans K., Van Dorpe J., Hellings P., Gorselink M., Heymans S., Theilmeier G., Dewerchin M., Laudenbach V., Vermylen P., Raat H., Acker T., Vleminckx V., Van Den Bosch L., Cashman N., Fujisawa H., Drost M.R., Sciot R., Bruyninckx F., Hicklin D.J., Ince C., Gressens P., Lupu F., Plate K.H., Robberecht W., Herbert J., Collen D., Carmeliet P. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat. Genet. 2001, 28:131-138.
36. Reimann-Philipp U., Ovase R., Weigel P.H., Grammas P. Mechanisms of cell death in primary cortical neurons and PC12 cells. J. Neurosci. Res. 2001, 64:654-660.
37. Rosenstein J.M., Krum J.M. New roles for VEGF in nervous tissue-beyond blood vessels. Exp. Neurol. 2004, 187:246-253.
38. 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.
39. Ryu J.K., Cho T., Choi H.B., Wang Y.T., McLarnon J.G. Microglial VEGF receptor response is an integral chemotactic component in Alzheimer's disease pathology. J. Neurosci. 2009, 29:3-13.
40. Sadowski-Debbing K., Coy J.F., Mier W., Hug H., Los M. Caspases-their role in apoptosis and other physiological processes as revealed by knock-out studies. Arch. Immunol. Ther. Exp. (Warsz) 2002, 50:19-34.
41. Salikhova A., Wang L., Lanahan A.A., Liu M., Simons M., Leenders W.P., Mukhopadhyay D., Horowitz A. Vascular endothelial growth factor and semaphoring induce neuropilin-1 endocytosis via separate pathways. Circ. Res. 2008, 103:e71-e79.
42. Schneider A., Rajendran L., Honsho M., Gralle M., Donnert G., Wouters F., Hell S.W., Simons M. Flotillin-dependent clustering of the amyloid precursor protein regulates its endocytosis and amyloidogenic processing in neurons. J. Neurosci. 2008, 28:2874-2882.
43. Schwarz Q., Gu C., Fujisawa H., Sabelko K., Gertsenstein M., Nagy A., Taniguchi M., Kolodkin A.L., Ginty D.D., Shima D.T., Ruhrberg C. Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve. Genes Dev. 2004, 18:2822-2834.
44. Seanor K.L., Cross J.V., Nguyen S.M., Yan M., Templeton D.J. Reative quinones differentially regulate SAPK/JNK and p38/mHOG stress kinases. Antioxid. Redox Signal. 2003, 5:103-113.
45. Shen F., Su H., Fan Y., Chen Y., Zhu Y., Liu W., Young W.L., Yang G.Y. Adeno-associated viral-vector-mediated hypoxia-inducible vascular endothelial growth factor gene expression attenuates ischemic brain injury after focal cerebral ischemia in mice. Stroke 2006, 37:2601-2606.
46. Shore P.M., Jackson E.K., Wisniewski S.R., Clark R.S.B., Adelson P.D., Kochanek P.M. Vascular endothelial growth factor is increased in cerebrospinal fluid after traumatic brain injury in infants and children. Neurosurgery 2004, 54:605-612.
47. Skirgaudas M., Awad I.A., Kim J., Rothbart D., Criscuolo G. Expression of angiogenesis factors and selected vascular wall matrix proteins in intracranial saccular aneurysms. Neurosurgery 1996, 39:537-547.
48. Sköld M.K., Kanje M. Vascular endothelial growth factor in central nervous system injuries - a vascular growth factor getting nervous?. Curr. Neurovasc. Res. 2008, 5:246-259.
49. Sondell M., Sundler F., Kanje M. Vascular endothelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur. J. Neurosci. 2000, 12:4243-4254.
50. Storkebaum E., Lambrechts D., Carmeliet P. VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays 2004, 26:943-954.
51. Swift M.E., Kleinman H.K., DiPietro L.A. Impaired wound repair and delayed angiogenesis in aged mice. Lab. Invest. 1999, 79:1479-1487.
52. Thornton T.M., Rincon M. Non-classical p38 map kinase functions: cell cycle checkpoints and survival. Int. J. Biol. Sci. 2009, 5:44-52.
53. Tolosa L., Mir M., Asensio V.J., Olmos G., Lladó J. Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase. J. Neurochem. 2008, 105:1080-1090.
54. Tolosa L., Mir M., Olmos G., Lladó J. Vascular endothelial growth factor protects motoneurons from serum deprivation-induced cell death through phosphatidylinositol 3-kinase-mediated p38 mitogen-activated protein kinase inhibition. Neuroscience 2009, 158:1348-1355.
55. Tripathy D., Grammas P. Acetaminophen inhibits neuronal inflammation and protects neurons from oxidative stress. J. Neuroinflamm. 2009, 6:10-18.
56. Wang Y., Mao X.O., Xie L., Banwait S., Marti H.H., Greenberg D.A., Jin K. Vascular endothelial growth factor overexpression delays neurodegeneration and prolongs survival in amyotrophic lateral sclerosis mice. J. Neurosci. 2007, 27:304-307.
57. Wick A., Wick W., Waltenberger 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.
58. Widenfalk J., Lipson A., Jubran M., Hofstetter C., Ebendal T., Cao Y., Olson L. Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury. Neuroscience 2003, 120:951-960.
59. Yamagishi S., Abe R., Jinnouchi Y., Matsui T., Imaizumi T., Inoue H. Pigment-epithelium-derived factor inhibits vascular endothelial growth factor-induced vascular hyperpermeability both in vitro and in vivo. J. Int. Med. Res. 2007, 35:896-900.
60. Yancopoulos G.D., Davis S., Gale N.W., Rudge J.S., Wiegand S.J., Holash J. Vascular-specific growth factors and blood vessel formation. Nature 2000, 407:242-248.
61. Yang S.P., Bae D.G., Kang H.J., Gwag B.J., Gho Y.S., Chae C.B. Co-accumulation of vascular endothelial growth factor with beta-amyloid in the brain of patients with Alzheimer's disease. Neurobiol. Aging 2004, 25:283-290.
62. Yang S.P., Kwon B.O., Gho Y.S., Chae C.B. Specific interaction of VEGF165 with beta-amyloid, and its protective effect on beta-amyloid-induced neurotoxicity. J. Neurochem. 2005, 93:118-127.
63. Yasuda T., Fukuda-Tani M., Nihira T., Wada K., Hattori N., Mizuno Y., Mochizuki H. Correlation between levels of pigment epithelium-derived factor and vascular endothelial growth factor in the striatum of patients with Parkinson's disease. Exp. Neurol. 2007, 206:308-317.
64. Yoshino Y., Aoyagi M., Tamaki M., Duan L., Morimoto T., Ohno K. Activation of p38 MAPK and/or JNK contributes to increased levels of VEGF secretion in human malignant glioma cells. Int. J. Oncol. 2006, 29:981-987.
65. Youn J.Y., Wang T., Cai H. An ezrin/calpain/PI3K/AMPK/eNOSs1179 signaling cascade mediating VEGF-dependent endothelial nitric oxide production. Circ. Res. 2009, 104:50-59.
66. Yuan J., Yankner B.A. Apoptosis in the nervous system. Nature 2000, 407:802-809.
67. Zhu X., Mei M., Lee H.G., Wang Y., Han J., Perry G., Smith M.A. P38 activation mediates amyloid-beta cytotoxicity. Neurochem. Res. 2005, 30:791-796.