Maturation but not survival of dopaminergic nigrostriatal neurons is affected in developing and aging BDNF-deficient mice

Brain Research

Volumn 1039, Issue 1-2, 2005, Pages 177-188

  Baker, Sarah A ^a,b   Stanford, Lianne E ^c   Brown, Richard E ^c   Hagg, Theo ^a,b,d  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b University of Louisville School of Medicine   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

^d NONE   (United States)

Author keywords

Brain derived neurotrophic factor; Knockout mice; Parkinson's disease; Substantia nigra; Tyrosine hydroxylase

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; TYROSINE 3 MONOOXYGENASE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; DENDRITE; DOPAMINERGIC NERVE CELL; FEMALE; MALE; MORPHOLOGY; MOTOR COORDINATION; MOUSE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PERIKARYON; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; QUANTITATIVE ANALYSIS; SUBSTANTIA NIGRA; WILD TYPE;

EID: 15244354999     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2005.01.052     Document Type: Article

References (78)

1. M. Abercrombie Estimation of nuclear population from microtome sections Anat. Rec. 94 1946 239 247
2. M.A. Alonso-Vanegas, J.P. Fawcett, C.G. Causing, F.D. Miller, and A.F. Sadikot Characterization of dopaminergic midbrain neurons in a DBH:BDNF transgenic mouse J. Comp. Neurol. 413 1999 449 462
3. C.A. Altar, C.B. Boylan, M. Fritsche, B.E. Jones, C. Jackson, S.J. Wiegand, R.M. Lindsay, and C. Hyman Efficacy of brain-derived neurotrophic factor and neurotrophin-3 on neurochemical and behavioral deficits associated with partial nigrostriatal dopamine lesions J. Neurochem. 63 1994 1021 1032
4. C.A. Altar, N. Cai, T. Bliven, M. Jahasz, J.M. Conner, A.L. Acheson, R.M. Lindsay, and S.J. Wiegand Anterograde transport of brain-derived neurotrophic factor and its role in the brain Nature 389 1997 856 860
5. R.F. Alderson, A.L. Alterman, Y.A. Barde, and R.M. Lindsay Brain-derived neurotrophic factor increases survival and differentiation functions of rat septal cholinergic neurons in culture Neuron 5 1990 297 306
6. B.B. Anderson, H.J. Gundersen, and B. Pakkenberg Aging of the human cerebellum: a stereological study J. Comp. Neurol. 466 2003 356 365
7. H. Bernheimer, W. Birkmayer, O. Hornykiewicz, K. Jellinger, and F. Seitelberger Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations J. Neurol. Sci. 20 1973 415 455
8. E.P. Brandon, S.F. Logue, M.R. Adams, M. Qi, S.P. Sullivan, A.M. Matsumoto, D.M. Dorsa, J.M. Wehner, G.S. McKnight, and R.L. Idzerda Defective motor behavior and neural gene expression in RIIbeta-protein kinase A mutant mice J. Neurosci. 18 1998 3639 3649
9. G. Bustos, J. Abarca, J. Campusano, V. Bustos, V. Noriega, and E. Aliaga Functional interactions between somatodendritic dopamine release, glutamate receptors and brain-derived neurotrophic factor expression in mesencephalic structures of the brain Brain Res Rev. 47 2004 126 144
10. C.R. Cabello, J.J. Thune, H. Pakkenberg, and B. Pakkenberg Ageing of substantia nigra in humans: cell loss may be compensated by hypertrophy Neuropathol. Appl. Neurobiol. 28 2002 283 291
11. M. Carli, J.L. Evenden, and T.W. Robbins Depletion of unilateral striatal dopamine impairs initiation of contralateral actions and not sensory attention Nature 313 1985 679 682
12. J.C. Conover, J.T. Erickson, D.M. Katz, L.M. Bianchi, W.T. Poueymirou, J. McClain, L. Pan, M. Helgren, N.Y. Ip, P. Boland, B. Friedman, S. Wiegand, R. Vejsada, A.C. Kato, T.M. DeChiara, and G.D. Yancopoulos Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4 Nature 375 1995 235 238
13. J.T. Coyle Biochemical aspects of neurotransmission in the developing brain Int. Rev. Neurobiol. 20 1977 65 103
14. D.A. Di Monte, M. Lavasani, and A.B. Manning-Bog Environmental factors in Parkinson's disease Neurotoxicology 23 2002 487 502
15. D.E. Dluzen, G. Xuemei, G.M. Story, L.I. Anderson, J. Kucera, and J.M. Walro Evaluation of nigrostriatal dopaminergic function in adult +/+ and +/- BDNF mutant mice Exp. Neurol. 170 2001 121 128
16. D.E. Dluzen, L.I. Anderson, J.L. McDermoot, J. Kucera, and J.M. Walro Striatal dopamine output is compromised within +/- BDNF mice Synapse 43 2002 112 117
17. D.F. Emerich, P. McDermott, P. Krueger, M. Banks, J. Zhao, J. Marszalkowski, B. Frydel, S.R. Winn, and P.R. Sanberg Locomotion of aged rats: relationship to neurochemical not morphological changes in nigrostriatal dopaminergic neurons Brain Res. Bull. 32 1993 477 486
18. D.F. Emerich, M. Plone, J. Francis, B.R. Frydel, S.R. Winn, and M.D. Lindner Alleviation of behavioral deficits in aged rodents following implantation of encapsulated GDNF-producing fibroblasts Brain Res. 736 1996 99 110
19. P. Ernfors, K.F. Lee, and R. Jaenisch Mice lacking brain-derived neurotrophic factor develop with sensory deficits Nature 368 1994 147 150
20. S.C. Fowler, T.J. Zarcone, E. Vorontsova, and R. Chen Motor and associative deficits in D2 dopamine receptor knockout mice Int. J. Dev. Neurosci. 20 2002 309 321
21. K.B.J. Franklin, and G. Paxinos The mouse brain in stereotaxic coordinates 1997 Academic Press San Diego
22. D.M. Frim, T.A. Uhler, W.R. Galpern, M.F. Beal, X.O. Breakefield, and O. Isacson Implanted fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevent 1-methyl-4-phenylpyridinium toxicity to dopaminergic neurons in the rat Proc. Natl. Acad. Sci. 91 1994 5104 5108
23. L. Geffen, T. Jesell, A. Cuello, and L. Iversen Release of dopamine dendrites in rat substantia nigra Nature 260 1976 258 260
24. A. Ghohs, J. Carnahan, and M.E. Greenberg Requirement for BDNF in activity-dependent survival of cortical neurons Science 263 1994 1618 1623
25. T. Hagg Neurotrophins prevent death and differentially affect tyrosine hydroxylase of adult rat nigrostriatal neurons in vivo Exp. Neurol. 149 1998 183 192
26. E.C. Hirsch Biochemistry of Parkinson's disease with special reference to the dopaminergic systems Mol. Neurobiol. 9 1994 135 142
27. B.A. Horger, C.A. Iyasere, M.T. Berhow, C.J. Messer, E.J. Nestler, and J.R. Taylor Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor J. Neurosci. 19 1999 4110 4122
28. D.W. Howells, M.J. Porritt, J.Y.F. Wong, P.E. Batchelor, R. Kalnins, A.J. Hughes, and G.A. Donnan Reduced BDNF mRNA expression in the Parkinson's disease substantia nigra Exp. Neurol. 166 2000 127 135
29. H.C. Hung, and E.H. Lee The mesolimbic dopaminergic pathway is more resistant than the nigrostriatal dopaminergic pathway to MPTP and MPP+toxicity: BDNF gene expression Brain Res. Mol. Brain Res. 41 1996 14 26
30. C. Hyman, M. Hofer, Y.A. Barde, M. Juhasz, G. Yancopoulos, S.P. Squinto, and R.M. Lindsay BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra Nature 350 1991 230 232
31. C. Hyman, M. Jahasz, C. Jackson, P. Wright, N.Y. Ip, and R.M. Lindsay Overlapping and distinct actions of the neurotrophins BDNF, NT-3, and NT-4/5 on cultured dopaminergic and GABAergic neurons of the ventral mesencephalon J. Neurosci. 14 1994 335 347
32. M.A. Hynes, K. Poulsen, M. Armanini, L. Berkemeier, H. Phillips, and A. Rosenthal Neurotrophin-4/5 is a survival factor for embryonic midbrain dopaminergic neurons in enriched cultures J. Neurosci. Res. 37 1994 144 154
33. K.R. Jones, I. Farinas, C. Backus, and L.F. Reichardt Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development Cell 76 1994 989 999
34. S.J. Kish, K. Shannak, and O. Hornykiewicz Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications N. Engl. J. Med. 318 1988 876 880
35. R.L. Klein, M.H. Lewis, N. Muzyczka, and E.M. Meyer Prevention of 6-hydroxydopamine-induced rotational behavior by BDNF somatic gene transfer Brain Res. 847 1999 314 320
36. B. Knusel, J.W. Winslow, A. Rosenthal, L.E. Burton, D.P. Seid, K. Nikolics, and F. Hefti Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin 3 Proc. Natl. Acad. Sci. U. S. A. 88 1991 961 965
37. J. Kohn, R.S. Aloyz, J.G. Toma, M. Haak-Frendscho, and F.D. Miller Functionally antagonistic interactions between the TrkA and p75 neurotrophin receptors regulate sympathetic neuron growth and target innervation J. Neurosci. 19 1999 5393 5408
38. R. Kolbeck, I. Bartke, W. Eberle, and Y.A. Barde Brain-derived neurotrophic factor levels in the nervous system of wild-type and neurotrophin gene mutant mice J. Neurochem. 72 1999 1930 1938
39. P.A. Lapchak, K.D. Beck, D.M. Araujo, I. Irwin, J.W. Langston, and F. Hefti Chronic intranigral administration of brain-derived neurotrophic factor produces striatal dopaminergic hypofunction in unlesioned adult rats and fails to attenuate the decline of striatal dopaminergic function following medial forebrain bundle transaction Neuroscience 53 1993 639 650
40. Y.S. Lau, R. Hao, Y.K. Fung, L.S. Fu, J.F. Bishop, R.F. Pfeiffer, and M.M. Mouradian Modulation of nigrostriatal dopaminergic transmission by antisense oligodeoxynucleotide against brain-derived neurotrophic factor Neurochem. Res. 23 1998 525 532
41. M. Levivier, S. Przedborski, C. Bencsics, and U.J. Kang Intrastriatal implantation of fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevents degeneration of dopaminergic neurons in a rat model of Parkinson's disease J. Neurosci. 15 1995 7810 7820
42. R.M. Liao, S.C. Fowler, and M.J. Kallman Quantifying operant behavior deficits in rats with bilateral 6-hydroxydopamine lesions of the ventrolateral striatum Chin. J. Physiol. 40 1997 71 78
43. P. Lingor, K. Unsicker, and K. Krieglstein GDNF and NT-4 protect midbrain dopaminergic neurons from toxic damage by iron and nitric oxide Exp. Neurol. 163 2000 55 62
44. R.G. Lister The use of a plus-maze to measure anxiety in the mouse Psychopharmacology 92 1987 180 185
45. B. Lom, J. Cogen, A. Lontok Sanchez, T. Vu, and S. Cohen-Cory Local and target-derived brain-derived neurotrophic factor exert opposing effects on the dendritic arborization of retinal ganglion cells in vivo J. Neurosci. 22 2002 7639 7649
46. L.A. Mamounas, M.E. Blue, J.A. Siuciak, and A. Altar Brain-derived neurotrophic factor promotes the survival and sprouting of serotonergic axons in rat brain J. Neurosci. 15 1995 7929 7939
47. S. Marty, B. Berninger, P. Carroll, and H. Thoenen GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor Neuron 16 1996 565 570
48. T. Masaki, S. Matsushita, H. Arai, A. Takeda, Y. Itoyama, H. Mochizuki, K. Kamakura, S. Ohara, and S. Higuchi Association between a polymorphism of brain-derived neurotrophic factor gene and sporadic Parkinson's disease Ann. Neurol. 54 2003 276 277
49. A.K. McAllister, L.C. Katz, and D.C. Lo Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth Neuron 18 1997 767 778
50. D.A. McRitchie, H.R. Cartwright, and G.M. Halliday Specific A10 dopaminergic nuclei in the midbrain degenerate in Parkinson's disease Exp. Neurol. 114 1997 202 213
51. M. Mogi, A. Togari, T. Kondo, Y. Mizuno, O. Komure, S. Kuno, H. Ichinose, and T. Nagatsu Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease Neurosci. Lett. 270 1999 45 48
52. Y. Momose, M. Murata, K. Kobayashi, M. Tachikawa, Y. Nakabayashi, I. Kanazawa, and T. Toda Association studies of multiple candidate genes for Parkinson's disease using single nucleotide polymorphisms Ann. Neurol. 51 2002 133 136
53. A. Nieoullon, A. Cheramy, and J. Glowinski Release of dopamine in vivo from rat substantia nigra Nature 266 1977 375 377
54. S. Numan, and K.B. Seroogy Expression of trkB and trkC mRNAs by adult midbrain dopamine neurons: a double-label in situ hybridization study J. Comp. Neurol. 403 1999 295 308
55. B. Pakkenberg, and H.J.G. Gundersen Neocortical neuron number in humans: effect of sex and age J. Comp. Neurol. 384 1997 312 320
56. K. Parain, M.G. Murer, Q. Yan, B. Faucheux, Y. Agid, E. Hirsch, and R. Raisman-Vozari Reduced expression of brain-derived neurotrophic factor protein in Parkinson's disease substantia nigra NeuroReport 10 1999 557 561
57. S. Pellow, and S.E. File Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus maze: a novel test of anxiety in the rat Pharmacol. Biochem. Behav. 24 1986 525 529
58. G. Rozas, and J.L. Labandeira Garcia Drug-free evaluation of rat models of parkinsonism and nigra grafts using a new automated rotarod test Brain Res. 749 1997 188 199
59. G. Rozas, E. Lopez-Martin, M.J. Guerra, and J.L. Labandeira-Garcia The overall rod performance test in the MPTP-treated-mouse model of Parkinsonism J. Neurosci. Methods 83 1998 165 175
60. H.M. Schellinck, L. Stanford, and M. Darrah Repetitive pain in infancy increases anxiety but does not alter spatial learning ability in juvenile mice Behav. Brain Res. 142 2003 157 165
61. R. Schuligoi, J. Fernandez, R.P. Heavens, and D.J. Sirinathsinghji Decreased tyrosine-hydroxylase mRNA but not cholecystokinin mRNA in the pars compacta of the substantia nigra and ventral tegmental area of aged rats Brain Res. Mol. Brain Res. 19 1993 333 338
62. P.M. Schwartz, P.R. Borghesani, R.L. Levy, S.L. Pomeroy, and R.A. Segal Abnormal cerebellar development and foliation in BDNF-/- mice reveals a role for neurotrophins in CNS patterning Neuron 19 1997 269 281
63. K.B. Seroogy, K.H. Lundgren, T.M. Tran, K.M. Guthrie, P.J. Isackson, and C.M. Gall Dopaminergic neurons in rat ventral midbrain express brain-derived neurotrophic factor and neurotrophin-3 mRNAs J. Comp. Neurol. 342 1994 321 334
64. J.K. Shepherd, S.S. Grewal, A. Fletcher, D.J. Bill, and C.T. Dourish Behavioural and pharmacological characterisation of the elevated zero-maze as an animal model of anxiety Psychopharmacology 116 1994 56 64
65. C.W. Shults, T. Kimber, and C.A. Altar BDNF attenuates the effects of intrastriatal injection of 6-hydroxydopamine NeuroReport 6 1995 1109 1112
66. D.E. Smith, J. Roberts, F.H. Gage, and M.H. Tuszynski Age-associated neuronal atrophy occurs in the primate brain and is reversible by growth factor gene therapy Proc. Natl. Acad. Sci. U. S. A. 96 1999 10893 10898
67. J.H. Son, H.S. Chun, T.H. Joh, S. Cho, B. Conti, and J.W. Lee Neuroprotection and neuronal differentiation studies using substantia nigra dopaminergic cells derived from transgenic mouse embryos J. Neurosci. 19 1999 10 20
68. E.L. Spangler, K.S. Waggie, J. Hengemihle, D. Roberts, B. Hess, and D.K. Ingram Behavioral assessment of aging in male Fischer 344 and brown Norway rat strains and their F1 hybrids Neurobiol. Aging 15 1994 319 328
69. C. Spenger, C. Hyman, L. Studer, M. Egli, L. Evtouchenko, C. Jackson, A. Dahl-Jorgensen, R.M. Lindsay, and R.W. Seiler Effects of BDNF on dopaminergic, serotonergic, and GABAergic neurons in cultures of human fetal ventral mesencephalon Exp. Neurol. 133 1995 50 63
70. M.B. Spina, S.P. Squinto, J. Miller, R.M. Lindsay, and C. Hyman Brain-derived neurotrophic factor protects dopamine neurons against 6-hydroxydopamine and N-methyl-4-phenylpyridinium ion toxicity: involvement of the glutathione system J. Neurochem. 59 1992 99 106
71. W.W. Spirduso, P.E. Gilliam, T. Schallert, M. Upchurch, D.M. Vaughn, and R.E. Wilcox Reactive capacity: a sensitive behavioral marker of movement initiation and nigrostriatal dopamine function Brain. Res. 335 1985 45 54
72. G.R. Uhl, J.C. Hedreen, and D.L. Price Parkinson's disease: loss of neurons from the ventral tegmental area contralateral to therapeutic surgical lesions Neurology 35 1985 1215 1218
73. P. Voorn, A. Kalsbeek, B. Jorritsma-Byham, and H.J. Groenewegen The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat Neuroscience 25 1988 857 887
74. S.L. Walsh, and G.C. Wagner Motor impairments after methamphetamine- induced neurotoxicity in the rat J. Pharmacol. Exp. Ther. 263 1992 617 626
75. N.L. Ward, and T. Hagg BDNF is needed for postnatal maturation of basal forebrain and neostriatum cholinergic neurons in vivo Exp. Neurol. 162 2000 297 310
76. I.Q. Whishaw, K. Li, P.A. Whishaw, B. Gorny, and G.A. Metz Distinct forelimb and hindlimb stepping impairments in unilateral dopamine-depleted rats: use of the Rotarod as a method for the qualitative analysis of skilled walking J. Neurosci. Methods 126 2003 13 23
77. Q. Yan, C. Matheson, O.T. Lopez, and J.A. Miller The biological responses of axotomized adult motoneurons to brain-derived neurotrophic factor J. Neurosci. 4 1994 5281 5291
78. J. Zhou, H.F. Bradford, and G.M. Stern The response of human and fetal ventral mesencephalon in culture to the brain-derived neurotrophic factor treatment Brain Res. 656 1994 147 156