AAV-mediated delivery of BDNF augments neurogenesis in the normal and quinolinic acid-lesioned adult rat brain

European Journal of Neuroscience

Volumn 25, Issue 12, 2007, Pages 3513-3525

  Henry, Rebecca A ^a   Hughes, Stephanie M ^a   Connor, Bronwen ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Adeno associated viral vector; Adult neural progenitor cell; Gene transfer; Neurogenesis; Subventricular zone

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BROXURIDINE; PARVOVIRUS VECTOR; QUINOLINIC ACID;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; BRAIN INJURY; BRAIN REGION; CELL COUNT; CELL LABELING; CELL LOSS; CELL MIGRATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE TRANSFER; IMMUNOREACTIVITY; MALE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RAT; STRIATE CORTEX; SUBVENTRICULAR ZONE; VIRAL GENE DELIVERY SYSTEM;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN INJURIES; BRAIN-DERIVED NEUROTROPHIC FACTOR; BROMODEOXYURIDINE; CELL COUNT; CELL DIFFERENTIATION; CEREBRAL VENTRICLES; DEPENDOVIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MALE; NERVE TISSUE PROTEINS; NEURONS; QUINOLINIC ACID; RATS; RATS, WISTAR; STEM CELLS;

EID: 34347385652     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05625.x     Document Type: Article

References (47)

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. Ahmed, S., Reynolds, B.A. Weiss, S. (1995) BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J. Neurosci., 15, 5765 5778.
3. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. Lindvall, O. (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med., 8, 963 970.
4. Beal, M.F., Ferrante, R.J., Swartz, K.J. Kowall, N.W. (1991) Chronic quinolinic acid lesions in rats closely resemble Huntington's disease. J. Neurosci., 11, 1649 1659.
5. Bedard, A., Cossette, M., Levesque, M. Parent, A. (2002) Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci. Lett., 328, 213 216.
6. Bedard, A., Gravel, C. Parent, A. (2006) Chemical characterization of newly generated neurons in the striatum of adult primates. Exp. Brain Res., 170, 501 512.
7. Benraiss, A., Chmielnicki, E., Lerner, K., Roh, D. Goldman, S.A. (2001) Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J. Neurosci., 21, 6718 6731.
8. Bjorklund, H., Olson, L., Dahl, D. Schwarcz, R. (1986) Short- and long-term consequences of intracranial injections of the excitotoxin, quinolinic acid, as evidenced by GFA immunohistochemistry of astrocytes. Brain Res., 371, 267 277.
9. Bull., N.D. Bartlett, P.F. (2005) The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J. Neurosci., 25, 10815 10821.
10. Chmielnicki, E., Benraiss, A., Economides, A.N. Goldman, S.A. (2004) Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J. Neurosci., 24, 2133 2142.
11. Craig, C.G., Tropepe, V., Morshead, C.M., Reynolds, B.A., Weiss, S. van der Kooy, D. (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci., 16, 2649 2658.
12. Curtis, M.A., Penney, E.B., Pearson, A.G., van Roon-Mom, W.M., Butterworth, N.J., Dragunow, M., Connor, B. Faull, R.L. (2003) Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc. Natl Acad. Sci. USA, 100, 9023 9027.
13. During, M.J., Young, D., Baer, K., Lawlor, P. Klugmann, M. (2003) Development and optimization of adeno-associated virus vector transfer into the central nervous system. In Machida, C.A. (Ed.), Methods in Molecular Medicine: Viral Vectors for Gene Therapy: Methods and Protocols. Human Press, Totowa, NJ, USA, pp. 221 236.
14. Eriksson, P.S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A. Gage, F.H. (1998) Neurogenesis in the adult human hippocampus. Nat. Med., 4, 1313 1317.
15. Gould, E., Reeves, A.J., Graziano, M.S. Gross, C.G. (1999) Neurogenesis in the neocortex of adult primates. Science, 286, 548 552.
16. Gustafsson, E., Andsberg, G., Darsalia, V., Mohapel, P., Mandel, R.J., Kirik, D., Lindvall, O. Kokaia, Z. (2003) Anterograde delivery of brain-derived neurotrophic factor to striatum via nigral transductions of recombinant adeno-associated virus increase neuronal death but promotes neurogenic response following stroke. Eur. J. Neurosci., 17, 2667 2678.
17. Hodge, R.D., D'Ercole, A.J. O'Kusky, J.R. (2004) Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J. Neurosci., 24, 10201 10210.
18. Huttner, W.B. Kosodo, Y. (2005) Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr. Opin. Cell Biol., 17, 648 657.
19. Kells, A.P., Fong, D.M., Dragunow, M., During, M.J., Young, D. Connor, B. (2004) AAV-mediated gene delivery of BDNF or GDNF is neuroprotective in a model of Huntington disease. Mol. Ther., 9, 682 688.
20. Kells, A.P., Henry, R.A., Hughes, S.M. Connor, B. (2007) Verification of functional AAV-mediated neurotrophic and anti-apoptotic factor expression. J. Neurosci. Meth., 161, 291 300.
21. Kirschenbaum, B. Goldman, S.A. (1995) Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc. Natl Acad. Sci. USA, 92, 210 214.
22. Kokaia, Z. Lindvall, O. (2003) Neurogenesis after ischaemic brain insults. Curr. Opin. Neurobiol., 13, 127 132.
23. Kornack, D.R. Rakic, P. (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl Acad. Sci. USA, 96, 5768 5773.
24. Kuhn, H.G., Winkler, J., Kempermann, G., Thal, L.J. Gage, F.H. (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci., 17, 5820 5829.
25. Larsson, E., Mandel, R.J., Klein, R.L., Muzyczka, N., Lindvall, O. Kokaia, Z. (2002) Suppression of insult-induced neurogenesis in adult rat brain by brain-derived neurotrophic factor. Exp. Neurol., 177, 1 8.
26. 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.
27. Lindholm, D., Carroll, P., Tzimagiogis, G. Thoenen, H. (1996) Autocrine-paracrine regulation of hippocampal neuron survival by IGF-1 and the neurotrophins BDNF, NT-3 and NT-4. Eur. J. Neurosci., 8, 1452 1460.
28. Lois, C. Alvarez-Buylla, A. (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA, 90, 2074 2077.
29. Lois, C. Alvarez-Buylla, A. (1994) Long-distance neuronal migration in the adult mammalian brain. Science, 264, 1145 1148.
30. 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.
31. Mohapel, P., Frielingsdorf, H., Haggblad, J., Zachrisson, O. Brundin, P. (2005) Platelet-derived growth factor (PDGF-BB) and brain-derived neurotrophic factor (BDNF) induce striatal neurogenesis in adult rats with 6-hydroxydopamine lesions. Neuroscience, 132, 767 776.
32. 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.
33. Palmer, T.D., Ray, J. Gage, F.H. (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell. Neurosci., 6, 474 486.
34. Parent, J.M., Valentin, V.V. Lowenstein, D.H. (2002a) Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J. Neurosci., 22, 3174 3188.
35. Parent, J.M., Vexler, Z.S., Gong, C., Derugin, N. Ferriero, D.M. (2002b) Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol., 52, 802 813.
36. Paxinos, G. Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
37. Pencea, V., Bingaman, K.D., Wiegand, S.J. Luskin, M.B. (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J. Neurosci., 21, 6706 6717.
38. Pincus, D.W., Keyoung, H.M., Harrison-Restelli, C., Goodman, R.R., Fraser, R.A., Edgar, M., Sakakibara, S., Okano, H., Nedergaard, M. Goldman, S.A. (1998) Fibroblast growth factor-2/brain-derived neurotrophic factor-associated maturation of new neurons generated from adult human subependymal cells. Ann. Neurol., 43, 576 585.
39. Reynolds, B.A. Weiss, S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255, 1707 1710.
40. Richards, L.J., Kilpatrick, T.J. Bartlett, P.F. (1992) De novo generation of neuronal cells from the adult mouse brain. Proc. Natl Acad. Sci. USA, 89, 8591 8595.
41. Suzuki, S.O. Goldman, J.E. (2003) Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways: a dynamic study of glial and neuronal progenitor migration. J. Neurosci., 23, 4240 4250.
42. Tattersfield, A.S., Croon, R.J., Liu, Y.W., Kells, A.P., Faull, R.L. Connor, B. (2004) Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington's disease. Neuroscience, 127, 319 332.
43. Vescovi, A.L., Reynolds, B.A., Fraser, D.D. Weiss, S. (1993) bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron, 11, 951 966.
44. Winner, B., Cooper-Kuhn, C.M., Aigner, R., Winkler, J. Kuhn, H.G. (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur. J. Neurosci., 16, 1681 1689.
45. Yoshimura, S., Takagi, Y., Harada, J., Teramoto, T., Thomas, S.S., Waeber, C., Bakowska, J.C., Breakefield, X.O. Moskowitz, M.A. (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc. Natl Acad. Sci. USA, 98, 5874 5879.
46. Zhang, R., Zhang, Z., Zhang, C., Zhang, L., Robin, A., Wang, Y., Lu, M. Chopp, M. (2004) Stroke transiently increases subventricular zone cell division from asymmetric to symmetric and increases neuronal differentiation in the adult rat. J. Neurosci., 24, 5810 5815.
47. Zigova, T., Pencea, V., Wiegand, S.J. Luskin, M.B. (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol. Cell. Neurosci., 11, 234 245.