Early Striatal Dendrite Deficits followed by Neuron Loss with Advanced Age in the Absence of Anterograde Cortical Brain-Derived Neurotrophic Factor

Journal of Neuroscience

Volumn 24, Issue 17, 2004, Pages 4250-4258

  Baquet, Zachary C ^a   Gorski, Jessica A ^a   Jones, Kevin R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

BDNF; Cre lox; Dendrite; Huntington's disease; Mouse; Mutant; Neurotrophin; Striatum

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIN;

AGED; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BDNF GENE; BRAIN CORTEX; CONTROLLED STUDY; DEGENERATIVE DISEASE; DENDRITE; EMX BDNF KO GENE; EMX1 1RESCRE GENE; GENE; GENE EXPRESSION; GENE MUTATION; HUNTINGTIN GENE; HUNTINGTON CHOREA; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRIATE CORTEX; SURVIVAL;

AGE FACTORS; AGING; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL COUNT; CEREBRAL CORTEX; DENDRITES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GAIT DISORDERS, NEUROLOGIC; GENE TARGETING; HUNTINGTON DISEASE; MICE; MICE, NEUROLOGIC MUTANTS; NEOSTRIATUM; NEURONS; PHENOTYPE;

EID: 2442506955     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3920-03.2004     Document Type: Article

References (60)

1. Alberch J, Perez-Navarro E, Canals JM (2002) Neuroprotection by neurotrophins and GDNF family members in the excitotoxic model of Huntington's disease. Brain Res Bull 57:817-822.
2. Alcantara S, Frisen J, del Rio JA, Soriano E, Barbacid M, Silos-Santiago I (1997) TrkB signaling is required for postnatal survival of CNS neurons and protects hippocampal and motor neurons from axotomy-induced cell death. J Neurosci 17:3623-3633.
3. Altar CA, DiStefano PS (1998) Neurotrophin trafficking by anterograde transport. Trends Neurosci 21:433-437.
4. Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, Acheson AL, Lindsay RM, Wiegand SJ (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856-860.
5. Andrew SE, Goldberg YP, Kremer B, Telenius H, Theilmann J, Adam S, Starr E, Squitieri F, Lin B, Kalchman MA, et al. (1993) The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nat Genet 4:398-403.
6. Aoki C, Wu K, Elste A, Len G, Lin S, McAuliffe G, Black IB (2000) Localization of brain-derived neurotrophic factor and TrkB receptors to postsynaptic densities of adult rat cerebral cortex. J Neurosci Res 59:454-463.
7. Auerbach W, Hurlbert MS, Hilditch-Maguire P, Wadghiri YZ, Wheeler VC, Cohen SI, Joyner AL, MacDonald ME, Turnbull DH (2001) The HD mutation causes progressive lethal neurological disease in mice expressing reduced levels of huntingtin. Hum Mol Genet 10:2515-2523.
8. Benitez J, Fernandez E, Garcia Ruiz P, Robledo M, Ramos C, Yebenes J (1994) Trinucleotide (CAG) repeat expansion in chromosomes of Spanish patients with Huntington's disease. Hum Genet 94:563-564.
9. Bennett JL, Zeiler SR, Jones KR (1999) Patterned expression of BDNF and NT-3 in the retina and anterior segment of the developing mammalian eye. Invest Ophthalmol Vis Sci 40:2996-3005.
10. Bibel M, Barde YA (2000) Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 14:2919-2937.
11. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, Dunnett SB, Morton AJ (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 19:3248-3257.
12. Cattaneo E, Rigamonti D, Goffredo D, Zuccato C, Squitieri F, Sipione S (2001) Loss of normal huntingtin function: new developments in Huntington's disease research. Trends Neurosci 24:182-188.
13. Costantini LC, Feinstein SC, Radeke MJ, Snyder-Keller A (1999) Compartmental expression of trkB receptor protein in the developing striatum. Neuroscience 89:505-513.
14. Duan W, Guo Z, Jiang H, Ware M, Li XJ, Mattson MP (2003) Dietary restriction normalizes glucose metabolism and BDNF levels, slows disease progression, and increases survival in huntingtin mutant mice. Proc Natl Acad Sci USA 100:2911-2916.
15. Dube L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267:455-471.
16. Ferrer I, Goutan E, Marin C, Rey MJ, Ribalta T (2000) Brain-derived neurotrophic factor in Huntington disease. Brain Res 866:257-261.
17. Friedman WJ, Ernfors P, Persson H (1991) Transient and persistent expression of NT-3/HDNF mRNA in the rat brain during postnatal development. J Neurosci 11:1577-1584.
18. Friedman WJ, Ibanez CF, Hallbook F, Persson H, Cain LD, Dreyfus CF, Black IB (1993) Differential actions of neurotrophins in the locus coeruleus and basal forebrain. Exp Neurol 119:72-78.
19. Fusco FR, Zuccato C, Tartari M, Martorana A, De March Z, Giampa C, Cattaneo E, Bernardi G (2003) Co-localization of brain-derived neurotrophic factor (BDNF) and wild-type huntingtin in normal and quinolinic acid-lesioned rat brain. Eur J Neurosci 18:1093-1102.
20. Galvin KA, Oorschot DE (2003) Continuous low-dose treatment with brain-derived neurotrophic factor or neurotrophin-3 protects striatal medium spiny neurons from mild neonatal hypoxia/ischemia: a stereological study. Neuroscience 118:1023-1032.
21. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR (2002) Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22:6309-6314.
22. Gorski JA, Zeiler SR, Tamowski S, Jones KR (2003a) Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J Neurosci 23:6856-6865.
23. Gorski JA, Balogh SA, Wehner JM, Jones KR (2003b) Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice. Neuroscience 121:341-354.
24. Guidetti P, Charles V, Chen EY, Reddy PH, Kordower JH, Whetsell Jr WO, Schwarcz R, Tagle DA (2001) Early degenerative changes in transgenic mice expressing mutant huntingtin involve dendritic abnormalities but no impairment of mitochondrial energy production. Exp Neurol 169:340-350.
25. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis 96:379-394.
26. Hamilton BA, Frankel WN, Kerrebrock AW, Hawkins TL, FitzHugh W, Kusumi K, Russell LB, Mueller KL, van Berkel V, Birren BW, Kruglyak L, Lander ES (1996) Disruption of the nuclear hormone receptor RORalpha in staggerer mice. Nature 379:736-739.
27. Hofer M, Pagliusi SR, Hohn A, Leibrock J, Barde YA (1990) Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J 9:2459-2464.
28. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24:677-736.
29. Ivkovic S, Ehrlich ME (1999) Expression of the striatal DARPP-32/ARPP-21 phenotype in GABAergic neurons requires neurotrophins in vivo and in vitro. J Neurosci 19:5409-5419.
30. Ivkovic S, Polonskaia O, Farinas I, Ehrlich ME (1997) Brain-derived neurotrophic factor regulates maturation of the DARPP-32 phenotype in striatal medium spiny neurons: studies in vivo and in vitro. Neuroscience 79:509-516.
31. Johnston JG, Gerfen CR, Haber SN, van der Kooy D (1990) Mechanisms of striatal pattern formation: conservation of mammalian compartmentalization. Brain Res Dev Brain Res 57:93-102.
32. Jones KR, Farinas I, Backus C, Reichardt LF (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-999.
33. Kemp JM, Powell TP (1971a) The synaptic organization of the caudate nucleus. Philos Trans R Soc Lond B Biol Sci 262:403-412.
34. Kemp JM, Powell TP (1971b) The termination of fibres from the cerebral cortex and thalamus upon dendritic spines in the caudate nucleus: a study with the Golgi method. Philos Trans R Soc Lond B Biol Sci 262:429-439.
35. Kohara K, Kitamura A, Adachi N, Nishida M, Itami C, Nakamura S, Tsumoto T (2003) Inhibitory but not excitatory cortical neurons require presynaptic brain-derived neurotrophic factor for dendritic development, as revealed by chimera cell culture. J Neurosci 23:6123-6131.
36. Lalonde R (1987) Motor abnormalities in staggerer mutant mice. Exp Brain Res 68:417-420.
37. Martinez-Serrano A, Bjorklund A (1996) Protection of the neostriatum against excitotoxic damage by neurotrophin-producing, genetically modified neural stem cells. J Neurosci 16:4604-4616.
38. Merlio JP, Ernfors P, Jaber M, Persson H (1992) Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience 51:513-532.
39. Mizuno K, Carnahan J, Nawa H (1994) Brain-derived neurotrophic factor promotes differentiation of striatal GABAergic neurons. Dev Biol 165:243-256.
40. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
41. Nakao N, Brundin P, Funa K, Lindvall O, Odin P (1995) Trophic and protective actions of brain-derived neurotrophic factor on striatal DARPP-32-containing neurons in vitro. Brain Res Dev Brain Res 90:92-101.
42. Nimchinsky EA, Sabatini BL, Svoboda K (2002) Structure and function of dendritic spines. Annu Rev Physiol 64:313-353.
43. Nisenbaum LK, Webster SM, Chang SL, McQueeney KD, LoTurco JJ (1998) Early patterning of prelimbic cortical axons to the striatal patch compartment in the neonatal mouse. Dev Neurosci 20:113-124.
44. Perez-Navarro E, Canudas AM, Akerund P, Alberch J, Arenas E (2000) Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4/5 prevent the death of striatal projection neurons in a rodent model of Huntington's disease. J Neurochem 75:2190-2199.
45. Regeur L, Pakkenberg B (1989) Optimizing sampling designs for volume measurements of components of human brain using a stereological method. J Microsc 155:113-121.
46. Reiner A, Albin RL, Anderson KD, D'Amato CJ, Penney JB, Young AB (1988) Differential loss of striatal projection neurons in Huntington disease. Proc Natl Acad Sci USA 85:5733-5737.
47. Schmidtke K, Manner H, Kaufmann R, Schmolck H (2002) Cognitive procedural learning in patients with fronto-striatal lesions. Learn Mem 9:419-429.
48. Segal M, Andersen P (2000) Dendritic spines shaped by synaptic activity. Curr Opin Neurobiol 10:582-586.
49. Seroogy KB, Lundgren KH, Tran TM, Guthrie KM, Isackson PJ, Gall CM (1994) Dopaminergic neurons in rat ventral midbrain express brain-derived neurotrophic factor and neurotrophin-3 mRNAs. J Comp Neurol 342:321-334.
50. Sheth AN, McKee ML, Bhide PG (1998) The sequence of formation and development of corticostriate connections in mice. Dev Neurosci 20:98-112.
51. Tyler WJ, Pozzo-Miller L (2003) Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones. J Physiol (Lond) 553:497-509.
52. van Dellen A, Deacon R, York D, Blakemore C, Hannan AJ (2001) Anterior cingulate cortical transplantation in transgenic Huntington's disease mice. Brain Res Bull 56:313-318.
53. van den Akker E, Reijnen M, Korving J, Brouwer A, Meijlink F, Deschamps J (1999) Targeted inactivation of Hoxb8 affects survival of a spinal ganglion and causes aberrant limb reflexes. Mech Dev 89:103-114.
54. Ventimiglia R, Mather PE, Jones BE, Lindsay RM (1995) The neurotrophins BDNF, NT-3 and NT-4/5 promote survival and morphological and biochemical differentiation of striatal neurons in vitro. Eur J Neurosci 7:213-222.
55. Vigers AJ, Baquet ZC, Jones KR (2000) Expression of neurotrophin-3 in the mouse forebrain: insights from a targeted LacZ reporter. J Comp Neurol 416:398-415.
56. von Bartheld CS, Byers MR, Williams R, Bothwell M (1996) Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system. Nature 379:830-833.
57. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
58. Widmer HR, Hefti F (1994) Neurotrophin-4/5 promotes survival and differentiation of rat striatal neurons developing in culture. Eur J Neurosci 6:1669-1679.
59. Wu K, Xu JL, Suen PC, Levine E, Huang YY, Mount HT, Lin SY, Black IB (1996) Functional trkB neurotrophin receptors are intrinsic components of the adult brain postsynaptic density. Brain Res Mol Brain Res 43:286-290.
60. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, Conti L, MacDonald ME, Friedlander RM, Silani V, Hayden MR, Timmusk T, Sipione S, Cattaneo E (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293:493-498.