VEGF is necessary for exercise-induced adult hippocampal neurogenesis

European Journal of Neuroscience

Volumn 18, Issue 10, 2003, Pages 2803-2812

  Fabel, Klaus ^a   Fabel, Konstanze ^a   Tam, Betty ^a   Kaufer, Daniela ^a   Baiker, Armin ^a   Simmons, Natalie ^a   Kuo, Calvin J ^a   Palmer, Theo D ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Mouse; Neural stem cells; Running; Vascular endothelial growth factor

Indexed keywords

ANTIDEPRESSANT AGENT; GLUTAMIC ACID; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; DOWN REGULATION; EXERCISE; HIPPOCAMPUS; HORMONAL REGULATION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEARNING; MALE; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; RUNNING; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION; STRESS;

ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, NORTHERN; BROMODEOXYURIDINE; CELL COUNT; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX PROTEINS; GENISTEIN; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MITOTIC INDEX; NEURONS; NEUROPILINS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, INBRED F344; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RUNNING; STEM CELLS; TUBULIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 0346751060     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2003.03041.x     Document Type: Article

References (43)

1. Aberg, M.A., Aberg, N.D., Hedbacker, H., Oscarsson, J. & Eriksson, P.S. (2000) Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci., 20, 2896-2903.
2. Asano, M., Kaneoka, K., Nomura, T., Asano, K., Sone, H., Tsurumaru, K., Yamashita, K., Matsuo, K., Suzuki, H. & Okuda, Y. (1998) Increase in serum vascular endothelial growth factor levels during altitude training. Acta Physiol. Scand., 162, 455-459.
3. Becker, C.M., Farnebo, F.A., Iordanescu, I., Behonick, D.J., Shin, M.C., Dunning, P., Christofferson, R., Mulligan, R.C., Taylor, G.A., Kuo, C.J. & Zetter, B.R. (2002) Gene therapy of prostate cancer with the soluble vascular endothelial growth factor receptor flk1. Cancer Biol. Ther., 1, 548-553.
4. Brown, J., Cooper-Kuhn, C.M., Kempermann, G., van Praag, H., Winkler, J., Gage, F.H. & Kuhn, H.G. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci., 17, 2042-2046.
5. Cameron, H.A. & McKay, R. (1998) Stem cells and neurogenesis in the adult brain. Curr. Opin. Neurobiol., 8, 677-680.
6. Cameron, H.A., Tanapat, P. & Gould, E. (1998) Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience, 82, 349-354.
7. Campuzano, R., Barrios, V., Cuevas, B., Asin-Cardiel, E., Muela, A., Castro, J.M., Fernandez-Ayerdi, A. & Cuevas, P (2002) Serum basic fibroblast growth factor levels in exercise-induced myocardial ischemia more likely a marker of endothelial dysfunction than a marker of ischemia? Eur. J. Med. Res., 7, 93-97.
8. Duman, R.S., Malberg, J. & Thome. J. (1999) Neural plasticity to stress and antidepressant treatment. Biol. Psychiatry, 46, 1181-1191.
9. Gomez-Pinilla, F., Dao, L. & So, V. (1997) Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res., 764, 1-8.
10. Gomez-Pinilla, F., Ying, Z., Roy, R.R., Molteni, R. & Edgerton, V.R. (2002) Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J. Neurophysiol., 88, 2187-2195.
11. Holash, J., Davis, S., Papadopoulos, N., Croll, S.D., Ho, L., Russell, M., Boland, P., Leidich, R., Hylton, D., Burova, E., Ioffe, E., Huang, T., Radziejewski, C., Bailey, K., Fandl, J.P., Daly, T., Wiegand, S.J., Yancopoulos, G.D. & Rudge, J.S. (2002) VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc. Natl Acad. Sci. USA, 99, 11393-11398.
12. Huang, J., Frischer, J.S., Serur, A., Kadenhe, A., Yokoi, A., McCrudden, K.W., New, T., O'Toole. K., Zabski, S., Rudge, J.S., Holash, J., Yancopoulos, G.D., Yamashiro, D.J. & Kandel, J.J. (2003) Regression of established tumors and metastases by potent vascular endothelial growth factor blockade. Proc. Natl Acad. Sci. USA, 100, 7785-7790.
13. Jin, K., Minami, M., Lan, J.Q., Mao, X.O., Batteur, S., Simon, R.P. & Greenberg, D.A. (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl Acad. Sci. USA, 98, 4710-4715.
14. Jin, K., Zhu, Y., Sun, Y., Mao, X.O., Xie, L. & Greenberg, D.A. (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl Acad. Sci. USA, 99, 11946-11950.
15. Kempermann, G. (2002) Regulation of adult hippocampal neurogenesis - implications for novel theories of major depression. Bipolar. Disord., 4, 17-33.
16. Kim, E.S., Serur, A., Huang, J., Manley, C.A., McCrudden, K.W., Frischer, J.S., Soffer, S.Z., Ring, L., New, T., Zabski, S., Rudge, J.S., Holash, J., Yancopoulos, G.D., Kandel, J.J. & Yamashiro, D.J. (2002) Potent VEGF blockade causes regression of coopted vessels in a model of neuroblastoma. Proc. Natl Acad. Sci. USA, 99, 11399-11404.
17. Kuo, C.J., Farnebo, F., Yu, E.Y., Christofferson, R., Swearingen, R.A., Carter, R., von Recum, H.A., Yuan, J., Kamihara, J., Flynn, E., D'Amato, R., Folkman, J. & Mulligan, R.C. (2001) Comparative evaluation of the antitumor activity of antiangiogenic proteins delivered by gene transfer. Proc. Natl Acad. Sci. USA, 98, 4605-4610.
18. Leventhal, C., Rafii, S., Rafii, D., Shahar, A. & Goldman, S.A. (1999) Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol. Cell Neurosci., 13, 450-464.
19. Louissaint, A. Jr, Rao, S., Leventhal, C. & Goldman, S.A. (2002) Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron, 34, 945-960.
20. Makatsori, A., Duncko, R., Schwendt, M., Moncek, F., Johansson, B.B. & Jezova, D. (2003) Voluntary wheel running modulates glutamate receptor subunit gene expression and stress hormone release in Lewis rats. Psychoneuroendocrinology, 28, 702-714.
21. Maurer, M.H., Tripps, W.K., Feldmann, R.E. Jr & Kuschinsky, W. (2003) Expression of vascular endothelial growth factor and its receptors in rat neural stem cells. Neurosci. Lett., 344, 165-168.
22. Mizumatsu, S., Monje, M.L., Morhardt, D.R., Rola, R., Palmer, T.D. & Fike, J.R. (2003) Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res., 63, 4021-4027.
23. Monje, M.L., Mizumatsu, S., Fike, J.R. & Palmer, T.D. (2002) Irradiation induces neural precursor-cell dysfunction. Nature Med., 8, 955-962.
24. Monje, M.L. & Palmer, T. (2003) Radiation injury and neurogenesis. Curr. Opin. Neurol., 16, 129-134.
25. Neeper, S.A., Gomez-Pinilla, F., Choi, J. & Cotman, C.W. (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res., 726, 49-56.
26. Oliff, H.S., Berchtold, N.C., Isackson, P & Cotman, C.W. (1998) Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcripts in the rat hippocampus. Brain Res. Mol. Brain Res., 61, 147-153.
27. Palmer, T.D., Markakis, E.A., Willhoite, A.R., Safar, F & Gage, F.H. (1999) Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci., 19, 8487-8497.
28. Palmer, T.D., Takahashi, J. & Gage, F.H. (1997) The adult rat hippocampus contains primordial neural stem cells. Mol. Cell Neurosci., 8, 389-404.
29. Palmer, T.D., Willhoite, A.R. & Gage, F.H. (2000) Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol., 425, 479-494.
30. van Praag, H., Christie, B.R., Sejnowski, T.J. & Gage, F.H. (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl Acad. Sci. USA, 96, 13427-13431.
31. Radley, J.J. & Jacobs, B.L. (2002) 5-HT1A receptor antagonist administration decreases cell proliferation in the dentate gyrus. Brain Res., 955, 264-267.
32. Schobersberger, W., Hobisch-Hagen, P., Fries, D., Wiedermann, F., Rieder-Scharinger, J., Villiger, B., Frey, W., Herold, M., Fuchs, D. & Jelkmann, W. (2000) Increase in immune activation, vascular endothelial growth factor and erythropoietin after an ultramarathon run at moderate altitude. Immunobiology, 201, 611-620.
33. Schoch, H.J., Fischer, S. & Marti, H.H. (2002) Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain, 125, 2549-2557.
34. Schwarz, A.J., Brasel, J.A., Hintz, R.L., Mohan, S. & Cooper, D.M. (1996) Acute effect of brief low-and high-intensity exercise on circulating insulin-like growth factor (IGF) I, II, and IGF-binding protein-3 and its proteolysis in young healthy men. J. Clin. Endocrinol. Metab., 81, 3492-3497.
35. Semenza, G.L. (2001) Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol. Med., 7, 345-350.
36. Shors, T.J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. & Gould, E. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410, 372-376.
37. Song, H., Stevens, C.F. & Gage, F.H. (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature, 417, 39-44.
38. Tanapat, P., Galea, L.A. & Gould, E. (1998) Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int. J. Dev. Neurosci., 16, 235-239.
39. Trejo, J.L., Carro, E. & Torres-Aleman, I. (2001) Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci., 21, 1628-1634.
40. Tseng, J.F., Farnebo, F.A., Kisker, O., Becker, C.M., Kuo, C.J., Folkman, J. & Mulligan, R.C. (2002) Adenovirus-mediated delivery of a soluble form of the VEGF receptor Flk1 delays the growth of murine and human pancreatic adenocarcinoma in mice. Surgery, 132, 857-865.
41. Wagner, J.P., Black, I.B. & DiCicco-Bloom, E. (1999) Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J. Neurosci., 19, 6006-6016.
42. Zhang, Z.G., Zhang, L., Tsang, W., Soltanian-Zadeh, H., Morris, D., Zhang, R., Goussev, A., Powers, C., Yeich, T. & Chopp, M. (2002) Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J. Cereb. Blood Flow Metab., 22, 379-392.
43. Zhu, Y., Jin, K., Mao, X.O. & Greenberg, D.A. (2003) Vascular endothelial growth factor promotes proliferation of cortical neuron precursors by regulating E2F expression. FASEB J., 17, 186-193.