Altered adult hippocampal neurogenesis in the YAC128 transgenic mouse model of Huntington disease

Neurobiology of Disease

Volumn 41, Issue 2, 2011, Pages 249-260

  Simpson, Jessica M ^a   Gil Mohapel, Joana ^a   Pouladi, Mahmoud A ^b   Ghilan, Mohamed ^a   Xie, Yuanyun ^b   Hayden, Michael R ^b   Christie, Brian R ^a,b,c  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adult neurogenesis; Cell proliferation; Dentate gyrus; Hippocampus; Huntington disease; Subventricular zone; YAC128 transgenic mice

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; DISEASE COURSE; DNA REPAIR; FEMALE; HIPPOCAMPUS; HUNTINGTON CHOREA; KINETICS; LEARNING; MALE; MORPHOLOGY; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SPATIAL MEMORY; SUBVENTRICULAR ZONE; TRANSGENE; YEAST ARTIFICIAL CHROMOSOME;

ANIMALS; COGNITION DISORDERS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HUMANS; HUNTINGTON DISEASE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONAL PLASTICITY; NUCLEAR PROTEINS;

EID: 78650588883     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.09.012     Document Type: Article

References (92)

1. Ahlenius H., Visan V., Kokaia M., Lindvall O., Kokaia Z. Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J. Neurosci. 2009, 29:4408-4419.
2. Andrade M.A., Bork P. HEAT repeats in the Huntington's disease protein. Nat. Genet. 1995, 11:115-116.
3. Attardo A., Fabel K., Krebs J., Haubensak W., Huttner W.B., Kempermann G. Tis21 expression marks not only populations of neurogenic precursor cells but also new postmitotic neurons in adult hippocampal neurogenesis. Cereb. Cortex 2010, 20:304-314.
4. Ben Abdallah N.M., Slomianka L., Vyssotski A.L., Lipp H.P. Early age-related changes in adult hippocampal neurogenesis in C57 mice. Neurobiol. Aging 2010, 31:151-161.
5. Bizon J.L., Lee H.J., Gallagher M. Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 2004, 3:227-234.
6. Borgs L., Beukelaers P., Vandenbosch R., Nguyen L., Moonen G., Maquet P., Albrecht U., Belachew S., Malgrange B. Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci. 2009, 10:30.
7. Breunig J.J., Silbereis J., Vaccarino F.M., Sestan N., Rakic P. Notch regulates cell fate and dendrite morphology of newborn neurons in the postnatal dentate gyrus. Proc. Natl Acad. Sci. USA 2007, 104:20558-20563.
8. Brown J.P., Couillard-Després S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 2003, 467:1-10.
9. Calingasan N.Y., Ho D.J., Wille E.J., Campagna M.V., Ruan J., Dumont M., Yang L., Shi Q., Gibson G.E., Beal M.F. Influence of mitochondrial enzyme deficiency on adult neurogenesis in mouse models of neurodegenerative diseases. Neuroscience 2008, 153:986-996.
10. Cameron H.A., McKay R. Stem cells and neurogenesis in the adult brain. Curr. Opin. Neurobiol. 1998, 8:677-680.
11. Canals J.M., Pineda J.R., Torres-Peraza J.F., Bosch M., Martín-Ibañez R., Muñoz M.T., Mengod G., Ernfors P., Alberch J. Brain-derived neurotrophic factor regulates the onset and severity of motor dysfunction associated with enkephalinergic neuronal degeneration in Huntington's disease. J. Neurosci. 2004, 24:7727-7739.
12. Christie B.R., Cameron H.A. Neurogenesis in the adult hippocampus. Hippocampus 2006, 16:199-207.
13. Cooper-Kuhn C.M., Kuhn H.G. Is it all DNA repair? Methodological considerations for detecting neurogenesis in the adult brain. Brain Res. Dev. Brain Res. 2002, 134:13-21.
14. Crews L., Mizuno H., Desplats P., Rockenstein E., Adame A., Patrick C., Winner B., Winkler J., Masliah E. Alpha-synuclein alters Notch-1 expression and neurogenesis in mouse embryonic stem cells and in the hippocampus of transgenic mice. J. Neurosci. 2008, 28:4250-4260.
15. Curtis M.A., Penney E.B., Pearson A.G., van Roon-Mom W.M., Butterworth N.J., Dragunow M., Connor B., Faull R.L. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc. Natl Acad. Sci. USA 2003, 100:9023-9027.
16. Dayer A.G., Ford A.A., Cleaver K.M., Yassaee M., Cameron H.A. Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol. 2003, 460:563-572.
17. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.P., Vonsattel J.P., Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997, 277:1990-1993.
18. Drapeau E., Montaron M.F., Aguerre S., Abrous D.N. Learning-induced survival of new neurons depends on the cognitive status of aged rats. J. Neurosci. 2007, 27:6037-6044.
19. Duan W., Peng Q., Masuda N., Ford E., Tryggestad E., Ladenheim B., Zhao M., Cadet J.L., Wong J., Ross C.A. Sertraline slows disease progression and increases neurogenesis in N171-82Q mouse model of Huntington's disease. Neurobiol. Dis. 2008, 30:312-322.
20. Duff K., McGuigan A., Huxley C., Schulz F., Hardy J. Insertion of a pathogenic mutation into a yeast artificial chromosome containing the human amyloid precursor protein gene. Gene Ther. 1994, 1:70-75.
21. Ehrnhoefer D.E., Butland S.L., Pouladi M.A., Hayden M.R. Mouse models of Huntington disease: variations on a theme. Dis Model Mech 2009, 2:123-129.
22. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 1998, 4:1313-1317.
23. Fedele V., Roybon L., Nordström U., Li J.Y., Brundin P. Neurogenesis in R6/2 mouse model of Huntington's disease is impaired at the level of NeuroD1. Neuroscience 2010, [Electronic publication ahead of print].
24. Fournier J.M., DeRubeis R.J., Hollon S.D., Dimidjian S., Amsterdam J.D., Shelton R.C., Fawcett J. Antidepressant drug effects and depression severity: a patient-level meta-analysis. JAMA 2010, 303:47-53.
25. Gil J.M., Leist M., Popovic N., Brundin P., Petersén A. Asialoerythropoietin is not effective in the R6/2 line of Huntington's disease mice. BMC Neurosci. 2004, 5:17.
26. Gil J.M., Mohapel P., Araújo I.M., Popovic N., Li J.Y., Brundin P., Petersén A. Reduced hippocampal neurogenesis in R6/2 transgenic Huntington's disease mice. Neurobiol. Dis. 2005, 20:744-751.
27. Gil J.M., Rego A.C. Mechanisms of neurodegeneration in Huntington's disease. Eur. J. Neurosci. 2008, 27:2803-2820.
28. Gil J.M., Rego A.C. The R6 lines of transgenic mice: a model for screening new therapies for Huntington's disease. Brain Res. Rev. 2009, 59:410-431.
29. Gil-Mohapel J., Simpson J., Christie B.R. Modulation of adult neurogenesis by physical exercise and environmental enrichment: insights for the treatment of neurological disorders. Adult Neurogenesis and Central Nervous System Diseases 2010, 125-150. Transworld Research Network, Kerala, India. J. Kunlin (Ed.).
30. Godin J.D., Colombo K., Molina-Calavita M., Keryer G., Zala D., Charrin B.C., Dietrich P., Volvert M.L., Guillemot F., Dragatsis I., Bellaiche Y., Saudou F., Nguyen L., Humbert S. Huntingtin is required for mitotic spindle orientation and mammalian neurogenesis. Neuron 2010, 67:392-406.
31. Gould E., Beylin A., Tanapat P., Reeves A., Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 1999, 2:260-265.
32. Graham R.K., Deng Y., Slow E.J., Haigh B., Bissada N., Lu G., Pearson J., Shehadeh J., Bertram L., Murphy Z., Warby S.C., Doty C.N., Roy S., Wellington C.L., Leavitt B.R., Raymond L.A., Nicholson D.W., Hayden M.R. Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 2006, 125:1179-1191.
33. Grote H.E., Bull N.D., Howard M.L., van Dellen A., Blakemore C., Bartlett P.F., Hannan A.J. Cognitive disorders and neurogenesis deficits in Huntington's disease mice are rescued by fluoxetine. Eur. J. Neurosci. 2005, 22:2081-2088.
34. Gutekunst C.A., Levey A.I., Heilman C.J., Whaley W.L., Yi H., Nash N.R., Rees H.D., Madden J.J., Hersch S.M. Identification and localization of huntingtin in brain and human lymphoblastoid cell lines with anti-fusion protein antibodies. Proc. Natl Acad. Sci. USA 1995, 92:8710-8714.
35. Heng M.Y., Detloff P.J., Albin R.L. Rodent genetic models of Huntington disease. Neurobiol. Dis. 2008, 32:1-9.
36. Hodgson J.G., Agopyan N., Gutekunst C.A., Leavitt B.R., LePiane F., Singaraja R., Smith D.J., Bissada N., McCutcheon K., Nasir J., Jamot L., Li X.J., Stevens M.E., Rosemond E., Roder J.C., Phillips A.G., Rubin E.M., Hersch S.M., Hayden M.R. A YAC mouse model for Huntington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron 1999, 23:181-192.
37. Hoffner G., Kahlem P., Djian P. Perinuclear localization of huntingtin as a consequence of its binding to microtubules through an interaction with beta-tubulin: relevance to Huntington's disease. J. Cell Sci. 2002, 115:941-948.
38. Höglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I., Hirsch E.C. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 2004, 7:726-735.
39. Hsieh J., Nakashima K., Kuwabara T., Mejia E., Gage F.H. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc. Natl Acad. Sci. USA 2004, 101:16659-16664.
40. Iannicola C., Moreno S., Oliverio S., Nardacci R., Ciofi-Luzzatto A., Piacentini M. Early alterations in gene expression and cell morphology in a mouse model of Huntington's disease. J. Neurochem. 2000, 75:830-839.
41. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl Acad. Sci. USA 2004, 101:343-347.
42. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis.
43. Kempermann G. The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for?. Trends Neurosci. 2008, 31:163-169.
44. Kempermann G., Kuhn H.G., Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 1998, 18:3206-3212.
45. Kempermann G., Wiskott L., Gage F.H. Functional significance of adult neurogenesis. Curr. Opin. Neurobiol. 2004, 14:186-191.
46. Klivenyi P., Starkov A.A., Caligasan N.Y., Gardian G., Browne S.E., Yang L., Bubber P., Gibson G.E., Patel M.S., Beal M.F. Mice deficient in dihydrolipoamide dehydrogenase show increased vulnerability to MPTP, malonate and 3-nitropropionic acid neurotoxicity. J. Neurochem. 2004, 88:1352-1360.
47. Laforet G.A., Sapp E., Chase K., McIntyre C., Boyce F.M., Campbell M., Cadigan B.A., Warzecki L., Tagle D.A., Reddy P.H., Cepeda C., Calvert C.R., Jokel E.S., Klapstein G.J., Ariano M.A., Levine M.S., DiFiglia M., Aronin N. Changes in cortical and striatal neurons predict behavioral and electrophysiological abnormalities in a transgenic murine model of Huntington's disease. J. Neurosci. 2001, 21:9112-9123.
48. Lazic S.E., Grote H., Armstrong R.J., Blakemore C., Hannan A.J., van Dellen A., Barker R.A. Decreased hippocampal cell proliferation in R6/1 Huntington's mice. NeuroReport 2004, 15:811-813.
49. Lazic S.E., Grote H.E., Blakemore C., Hannan A.J., van Dellen A., Phillips W., Barker R.A. Neurogenesis in the R6/1 transgenic mouse model of Huntington's disease: effects of environmental enrichment. Eur. J. Neurosci. 2006, 23:1829-1838.
50. Li S.H., Li X.J. Huntingtin-protein interactions and the pathogenesis of Huntington's disease. Trends Genet. 2004, 20:146-154.
51. Li B., Yamamori H., Tatebayashi Y., Shafit-Zagardo B., Tanimukai H., Chen S., Iqbal K., Grundke-Iqbal I. Failure of neuronal maturation in Alzheimer disease dentate gyrus. J. Neuropathol. Exp. Neurol. 2008, 67:78-84.
52. Lie D.C., Song H., Colamarino S.A., Ming G.L., Gage F.H. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol. 2004, 44:399-421.
53. Liu M., Pleasure S.J., Collins A.E., Noebels J.L., Naya F.J., Tsai M.J., Lowenstein D.H. Loss of BETA2/NeuroD leads to malformation of the dentate gyrus and epilepsy. Proc. Natl Acad. Sci. USA 2000, 97:865-870.
54. Luthi-Carter R., Hanson S.A., Strand A.D., Bergstrom D.A., Chun W., Peters N.L., Woods A.M., Chan E.Y., Kooperberg C., Krainc D., Young A.B., Tapscott S.J., Olson J.M. Dysregulation of gene expression in the R6/2 model of polyglutamine disease: parallel changes in muscle and brain. Hum. Mol. Genet. 2002, 11:1911-1926.
55. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 2000, 20:9104-9110.
56. Manev H., Uz T., Smalheiser N.R., Manev R. Antidepressants alter cell proliferation in the adult brain in vivo and in neural cultures in vitro. Eur. J. Pharmacol. 2001, 411:67-70.
57. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP (1996). Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice.
58. Marcora E., Gowan K., Lee J.E. Stimulation of NeuroD activity by huntingtin and huntingtin-associated proteins HAP1 and MLK2. Proc. Natl Acad. Sci. USA 2003, 100:9578-9583.
59. Meade C.A., Deng Y.P., Fusco F.R., Del Mar N., Hersch S., Goldowitz D., Reiner A. Cellular localization and development of neuronal intranuclear inclusions in striatal and cortical neurons of R6/2 transgenic mice. J. Comp. Neurol. 2002, 449:241-269.
60. Miller B.H., Schultz L.E., Gulati A., Cameron M.D., Pletcher M.T. Genetic regulation of behavioral and neuronal responses to fluoxetine. Neuropsychopharmacology 2008, 33:1312-1322.
61. Mirescu C., Gould E. Stress and adult neurogenesis. Hippocampus 2006, 16:233-238.
62. Miyata T., Maeda T., Lee J.E. NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev. 1999, 13:1647-1652.
63. Mohapel P., Brundin P. Harnessing endogenous stem cells to treat neurodegenerative disorders of the basal ganglia. Parkinsonism Relat. Disord. 2004, 10:259-264.
64. Murphy K.P., Carter R.J., Lione L.A., Mangiarini L., Mahal A., Bates G.P., Dunnett S.B., Morton A.J. Abnormal synaptic plasticity and impaired spatial cognition in mice transgenic for exon 1 of the human Huntington's disease mutation. J. Neurosci. 2000, 20:5115-5123.
65. Neuwald A.F., Hirano T. HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions. Genome Res. 2000, 10:1445-1452.
66. Nibuya M., Morinobu S., Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci. 1995, 15:7539-7547.
67. Pang T.Y., Du X., Zajac M.S., Howard M.L., Hannan A.J. Altered serotonin receptor expression is associated with depression-related behavior in the R6/1 transgenic mouse model of Huntington's disease. Hum. Mol. Genet. 2009, 18:753-766.
68. Paxinos G., Franklin K. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press Inc., Elsevier, San Diego, CA, USA. 2nd ed.
69. Peng Q., Masuda N., Jiang M., Li Q., Zhao M., Ross C.A., Duan W. The antidepressant sertraline improves the phenotype, promotes neurogenesis and increases BDNF levels in the R6/2 Huntington's disease mouse model. Exp. Neurol. 2008, 210:154-163.
70. Petersen Å., Gil J., Maat-Schieman M.L.C., Björkqvist M., Tanila H., Araújo I.M., Smith R., Popovic N., Wierup N., Norlén P., Li J.Y., Roos R.A.C., Sundler F., Mulder H., Brundin P. Orexin loss in Huntington's disease. Hum. Mol. Genet. 2005, 14:39-47.
71. Phillips W., Morton A.J., Barker R.A. Abnormalities of neurogenesis in the R6/2 mouse model of Huntington's disease are attributable to the in vivo microenvironment. J. Neurosci. 2005, 25:11564-11576.
72. Pleasure S.J., Collins A.E., Lowenstein D.H. Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J. Neurosci. 2000, 20:6095-6105.
73. Pouladi M.A., Graham R.K., Karasinska J.M., Xie Y., Santos R.D., Petersén A., Hayden M.R. Prevention of depressive behaviour in the YAC128 mouse model of Huntington disease by mutation at residue 586 of huntingtin. Brain 2009, 132:919-932.
74. Reynolds G.P., Dalton C.F., Tillery C.L., Mangiarini L., Davies S.W., Bates G.P. Brain neurotransmitter deficits in mice transgenic for the Huntington's disease mutation. J. Neurochem. 1999, 72:1773-1776.
75. Rosas H.D., Koroshetz W.J., Chen Y.I., Skeuse C., Vangel M., Cudkowicz M.E., Caplan K., Marek K., Seidman L.J., Makris N., Jenkins B.G., Goldstein J.M. Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology 2003, 60:1615-1620.
76. Slow E.J., van Raamsdonk J., Rogers D., Coleman S.H., Graham R.K., Deng Y., Oh R., Bissada N., Hossain S.M., Yang Y.Z., Li X.J., Simpson E.M., Gutekunst C.A., Leavitt B.R., Hayden M.R. Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum. Mol. Genet. 2003, 12:1555-1567.
77. Spargo E., Everall I.P., Lantos P.L. Neuronal loss in the hippocampus in Huntington's disease: a comparison with HIV infection. J. Neurol. Neurosurg. Psychiatry 1993, 56:487-491.
78. Spires T.L., Grote H.E., Garry S., Cordery P.M., Van Dellen A., Blakemore C., Hannan A.J. Dendritic spine pathology and deficits in experience-dependent dendritic plasticity in R6/1 Huntington's disease transgenic mice. Eur. J. Neurosci. 2004, 19:2799-2807.
79. Stack E.C., Kubilus J.K., Smith K., Cormier K., Del Signore S.J., Guelin E., Ryu H., Hersch S.M., Ferrante R.J. Chronology of behavioral symptoms and neuropathological sequela in R6/2 Huntington's disease transgenic mice. J. Comp. Neurol. 2005, 490:354-370.
80. Steiner B., Klempin F., Wang L., Kott M., Kettenmann H., Kempermann G. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 2006, 54:805-814.
81. Steward L.J., Bufton K.E., Hopkins P.C., Davies W.E., Barnes N.M. Reduced levels of 5-HT3 receptor recognition sites in the putamen of patients with Huntington's disease. Eur. J. Pharmacol. 1993, 242:137-143.
82. The Huntington's Disease Collaborative Research Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 1993, 72:971-983.
83. Tomasevic G., Kamme F., Wieloch T. Changes in proliferating cell nuclear antigen, a protein involved in DNA repair, in vulnerable hippocampal neurons following global cerebral ischemia. Brain Res. Mol. Brain Res. 1998, 60:168-176.
84. Turmaine M., Raza A., Mahal A., Mangiarini L., Bates G.P., Davies S.W. Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc. Natl Acad. Sci. USA 2000, 97:8093-8097.
85. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 2005, 25:8680-8685.
86. Van Raamsdonk J.M., Pearson J., Slow E.J., Hossain S.M., Leavitt B.R., Hayden M.R. Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington's disease. J. Neurosci. 2005, 25:4169-4180.
87. Vonsattel J.P., DiFiglia M. Huntington disease. J. Neuropathol. Exp. Neurol. 1998, 57:369-384.
88. Yu Z.X., Li S.H., Evans J., Pillarisetti A., Li H., Li X.J. Mutant huntingtin causes context-dependent neurodegeneration in mice with Huntington's disease. J. Neurosci. 2003, 23:2193-2202.
89. Zhao B., Zhong M., Jin K. Neurogenesis and neurodegenerative diseases in human. Panminerva Med. 2008, 50:55-64.
90. Zigova T., Pencea V., Wiegand S.J., Luskin M.B. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol. Cell. Neurosci. 1998, 11:234-245.
91. Zuccato C., Cattaneo E. Role of brain-derived neurotrophic factor in Huntington's disease. Prog. Neurobiol. 2007, 81:294-330.
92. Zuccato C., Ciammola A., Rigamonti D., Leavitt B.R., Goffredo D., Conti L., MacDonald M.E., Friedlander R.M., Silani V., Hayden M.R., Timmusk T., Sipione S., Cattaneo E. Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 2001, 293:493-498.