NGF rescues hippocampal cholinergic neuronal markers, restores neurogenesis, and improves the spatial working memory in a mouse model of huntington’s disease

Journal of Huntington's Disease

Volumn 2, Issue 1, 2013, Pages 69-82

  Zhang, Hongyu ^a,c,d   Petit, Géraldine H ^a   Gaughwin, Philip M ^a   Hansen, Christian ^a   Ranganathan, Srikanth ^a   Zuo, Xiaoyi ^a,e   Smith, Ruben ^a   Roybon, Laurent ^a   Brundin, Patrik ^a,f   Mobley, William C ^b   Li, Jia Yi ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d University of Bordeaux   (France)

^e SICHUAN UNIVERSITY   (China)

^f VAN ANDEL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL; ARTICLE; CHOLINERGIC FUNCTION; CHOLINERGIC NERVE CELL; DISEASE MODEL; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; MOUSE; NERVOUS SYSTEM DEVELOPMENT; R6/1 MICE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHORT TERM MEMORY; TRANSGENIC MOUSE; WESTERN BLOTTING;

CHOLINERGIC FUNCTION; HUNTINGTON'S DISEASE; NERVE GROWTH FACTOR; NEUROGENESIS; R6/1 MICE;

ANIMALS; BLOTTING, WESTERN; CHOLINERGIC NEURONS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; INFUSIONS, INTRAVENTRICULAR; MEMORY, SHORT-TERM; MICE; MICE, TRANSGENIC; NERVE GROWTH FACTOR; NEUROGENESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84906932529     PISSN: 18796397     EISSN: 18796400     Source Type: Journal    
DOI: 10.3233/JHD-120026     Document Type: Article

References (63)

1. Byers RK, Gilles FH, Fung C. Huntington’s disease in children. Neuropathologic study of four cases. Neurology. 1973;23:561-9.
2. Lange H, Thorner G, Hopf A, Schroder KF. Morphometric studies of the neuropathological changes in choreatic diseases. J Neurol Sci. 1976;28:401-25.
3. Spargo E, Everall IP, Lantos PL. Neuronal loss in the hippocampus in Huntington’s disease: A comparison with HIV infection. J Neurol Neurosurg Psychiatry. 1993;56:487-91.
4. Lazic SE, Grote H, Armstrong RJ, Blakemore C, Hannan AJ, van Dellen A, Barker RA. Decreased hippocampal cell proliferation in R6/1 Huntington’s mice. Neuroreport. 2004;15:811-3.
5. Gil JM, Mohapel P, Araujo IM, Popovic N, Li JY, Brundin P, Petersen A. Reduced hippocampal neurogenesis in R6/2 transgenic Huntington’s disease mice. Neurobiol Dis. 2005;20:744-51.
6. Phillips W, Morton AJ, Barker RA. Abnormalities of neurogenesis in the R6/2 mouse model of Huntington’s disease are attributable to the in vivo microenvironment. J Neurosci. 2005;25:11564-76.
7. Lazic SE, Grote HE, Blakemore C, Hannan AJ, van Dellen A, Phillips W, Barker RA. Neurogenesis in the R6/1 transgenic mouse model of Huntington’s disease: Effects of environmental enrichment. Eur J Neurosci. 2006;23:1829-38.
8. Fedele V, Roybon L, Nordstrom U, Li JY, Brundin P. Neurogenesis in the R6/2 mouse model of Huntington’s disease is impaired at the level of NeuroD1. Neuroscience. 2011;173:76-81.
9. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP, Jr. Neuropathological classification of Huntington’s disease. J Neuropathol Exp Neurol. 1985;44:559-77.
10. Lawrence AD, Hodges JR, Rosser AE, Kershaw A, ffrench-Constant C, Rubinsztein DC, Robbins TW, Sahakian BJ. Evidence for specific cognitive deficits in preclinical Huntington’s disease. Brain. 1998;121(Pt 7):1329-41.
11. Lione LA, Carter RJ, Hunt MJ, Bates GP, Morton AJ, Dunnett SB. Selective discrimination learning impairments in mice expressing the human Huntington’s disease mutation. J Neurosci. 1999;19:10428-37.
12. Ho AK, Sahakian BJ, Brown RG, Barker RA, Hodges JR, Ane MN, Snowden J, Thompson J, Esmonde T, Gentry R, Moore JW, Bodner T. Profile of cognitive progression in early Huntington’s disease. Neurology. 2003;61:1702-6.
13. Lemiere J, Decruyenaere M, Evers-Kiebooms G, Vandenbussche E, Dom R. Cognitive changes in patients with Huntington’s disease (HD) and asymptomatic carriers of the HD mutation-a longitudinal follow-up study. J Neurol. 2004;251:935-42.
14. Mazarakis NK, Cybulska-Klosowicz A, Grote H, Pang T, Van Dellen A, Kossut M, Blakemore C, Hannan AJ. Deficits in experience-dependent cortical plasticity and sensorydiscrimination learning in presymptomatic Huntington’s disease mice. J Neurosci. 2005;25:3059-66.
15. Van Raamsdonk JM, Pearson J, Slow EJ, Hossain SM, Leavitt BR, Hayden MR. Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington’s disease. J Neurosci. 2005; 25:4169-80.
16. Solomon AC, Stout JC, Johnson SA, Langbehn DR, Aylward EH, Brandt J, Ross CA, Beglinger L, Hayden MR, Kieburtz K, Kayson E, Julian-Baros E, Duff K, Guttman M, Nance M, Oakes D, Shoulson I, Penziner E, Paulsen JS. Verbal episodic memory declines prior to diagnosis in Huntington’s disease. Neuropsychologia. 2007;45:1767-76.
17. Duff K, Beglinger LJ, Theriault D, Allison J, Paulsen JS. Cognitive deficits in Huntington’s disease on the Repeatable Battery for the Assessment of Neuropsychological Status. J Clin Exp Neuropsychol. 2010;32:231-8.
18. Aquilonius SM, Eckernas SA, Sundwall A. Regional distribution of choline acetyltransferase in the human brain:Changes in Huntington’s chorea. J Neurol Neurosurg Psychiatry. 1975;38:669-77.
19. Ferrante RJ, Beal MF, Kowall NW, Richardson EP, Jr., Martin JB. Sparing of acetylcholinesterase-containing striatal neurons in Huntington’s disease. Brain Res. 1987;411:162-6.
20. Suzuki M, Desmond TJ, Albin RL, Frey KA. Vesicular neurotransmitter transporters in Huntington’s disease: Initial observations and comparison with traditional synaptic markers. Synapse. 2001;41:329-36.
21. Vetter JM, Jehle T, Heinemeyer J, Franz P, Behrens PF, Jackisch R, Landwehrmeyer GB, Feuerstein TJ. Mice transgenic for exon 1 of Huntington’s disease: Properties of cholinergic and dopaminergic pre-synaptic function in the striatum. J Neurochem. 2003;85:1054-1063.
22. Smith R, Chung H, Rundquist S, Maat-Schieman ML, Colgan L, Englund E, Liu YJ, Roos RA, Faull RL, Brundin P, Li JY. Cholinergic neuronal defect without cell loss in Huntington’s disease. Hum Mol Genet. 2006;15:3119-31.
23. Pang TY, Stam NC, Nithianantharajah J, Howard ML, Hannan AJ. Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington’s disease transgenic mice. Neuroscience. 2006;141:569-84.
24. Nithianantharajah J, Barkus C, MurphyM, Hannan AJ. Geneenvironment interactions modulating cognitive function and molecular correlates of synaptic plasticity in Huntington’s disease transgenic mice. Neurobiol Dis. 2008;29:490-504.
25. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 1999;2:266-70.
26. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature. 2002;415:1030-4.
27. Bruel-Jungerman E, Laroche S, Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci. 2005;21:513-21.
28. Fischer W, Bjorklund A, Chen K, Gage FH. NGF improves spatial memory in aged rodents as a function of age. J Neurosci. 1991;11:1889-906.
29. Moises HC, Womble MD, Washburn MS, Williams LR. Nerve growth factor facilitates cholinergic neurotransmission between nucleus basalis and the amygdala in rat: An electrophysiological analysis. J Neurosci. 1995;15:8131-42.
30. Cooper JD, Salehi A, Delcroix JD, Howe CL, Belichenko PV, Chua-Couzens J, Kilbridge JF, Carlson EJ, Epstein CJ, MobleyWC. Failed retrograde transport of NGF in a mouse model of Down’s syndrome: Reversal of cholinergic neurodegenerative phenotypes following NGF infusion. Proc Natl Acad Sci U S A. 2001;98:10439-44.
31. Kordower JH, Winn SR, Liu YT, Mufson EJ, Sladek JR, Jr., Hammang JP, Baetge EE, Emerich DF. The aged monkey basal forebrain: Rescue and sprouting of axotomized basal forebrain neurons after grafts of encapsulated cells secreting human nerve growth factor. Proc Natl Acad Sci U S A. 1994;91:10898-902.
32. Perez-Navarro E, Alberch J, Arenas E, Calvo N, Marsal J. Nerve growth factor and basic fibroblast growth factor protect cholinergic neurons against quinolinic acid excitotoxicity in rat neostriatum. Eur J Neurosci. 1994;6:706-11.
33. Jiang Y, Lv H, Huang S, Tan H, Zhang Y, Li H. Bone marrow mesenchymal stem cells can improve the motor function of a Huntington’s disease rat model. Neurol Res. 2011;33:331-7.
34. Im W, Lee ST, Park JE, Oh HJ, Shim J, Lim J, Chu K, Kim M. Transplantation of patient-derived adipose stem cells in YAC128 Huntington’s disease transgenic mice. PLoS Curr. 2010;2.
35. Dey ND, Bombard MC, Roland BP, Davidson S, Lu M, Rossignol J, Sandstrom MI, Skeel RL, Lescaudron L, Dunbar GL. Genetically engineered mesenchymal stem cells reduce behavioral deficits in the YAC 128 mouse model of Huntington’s disease. Behav Brain Res. 2010;214:193-200.
36. Frielingsdorf H, Simpson DR, Thal LJ, Pizzo DP. Nerve growth factor promotes survival of new neurons in the adult hippocampus. Neurobiol Dis. 2007;26:47-55.
37. Pardon MC. Role of neurotrophic factors in behavioral processes:Implications for the treatment of psychiatric and neurodegenerative disorders. Vitam Horm. 2010;82:185-200.
38. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell. 1996;87:493-506.
39. Rogers DC, Peters J, Martin JE, Ball S, Nicholson SJ, Witherden AS, Hafezparast M, Latcham J, Robinson TL, Quilter CA, Fisher EM. SHIRPA, a protocol for behavioral assessment:Validation for longitudinal study of neurological dysfunction in mice. Neurosci Lett. 2001;306:89-92.
40. Schwegler H, Crusio WE, Brust I. Hippocampal mossy fibers and radial-maze learning in the mouse: A correlation with spatial working memory but not with non-spatial reference memory. Neuroscience. 1990;34:293-8.
41. Fouquet C, Petit GH, Auffret A, Gaillard E, Rovira C, Mariani J, Rondi-Reig L. Early detection of age-related memory deficits in individual mice. Neurobiol Aging. 2011;32:1881-95.
42. Petit GH, Tobin C, Krishnan K, MoricardY, CoveyDF, Rondi-Reig L, Akwa Y. Pregnenolone sulfate and its enantiomer:Differential modulation of memory in a spatial discrimination task using forebrain NMDA receptor deficient mice. Eur Neuropsychopharmacol. 2011;21:211-5.
43. Roybon L, Deierborg T, Brundin P, Li JY. Involvement of Ngn2, Tbr and NeuroD proteins during postnatal olfactory bulb neurogenesis. Eur J Neurosci. 2009;29:232-43.
44. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A. et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis. 1988;96:379-94.
45. Haque NS, Isacson O. Neurotrophic factors NGF and FGF-2 alter levels of huntingtin (IT15) in striatal neuronal cell cultures. Cell Transplant. 2000;9:623-7.
46. Kee NJ, Preston E, Wojtowicz JM. Enhanced neurogenesis after transient global ischemia in the dentate gyrus of the rat. Exp Brain Res. 2001;136:313-20.
47. Schmidt-Hieber C, Jonas P, Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature. 2004;429:184-7.
48. Hodges A, Hughes G, Brooks S, Elliston L, Holmans P, Dunnett SB, Jones L. Brain gene expression correlates with changes in behavior in the R6/1 mouse model of Huntington’s disease. Genes Brain Behav. 2008;7:288-99.
49. Giralt A, Rodrigo T, Martin ED, Gonzalez JR, Mila M, Cena V, Dierssen M, Canals JM, Alberch J. Brain-derived neurotrophic factor modulates the severity of cognitive alterations induced by mutant huntingtin: Involvement of phospholipaseCgamma activity and glutamate receptor expression. Neuroscience. 2009;158:1234-50.
50. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature. 2001;410:372-6.
51. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci U S A. 2003;100:14385-90.
52. Spires TL, Grote HE, Varshney NK, Cordery PM, van Dellen A, Blakemore C, Hannan AJ. Environmental enrichment rescues protein deficits in a mouse model of Huntington’s disease, indicating a possible disease mechanism. J Neurosci. 2004;24:2270-6.
53. Zweifel LS, Kuruvilla R, Ginty DD. Functions and mechanisms of retrograde neurotrophin signalling. Nat Rev Neurosci. 2005;6:615-25.
54. Conner JM, Franks KM, Titterness AK, Russell K, Merrill DA, Christie BR, Sejnowski TJ, Tuszynski MH. NGF is essential for hippocampal plasticity and learning. J Neurosci. 2009;29:10883-9.
55. Cooper-Kuhn CM, Winkler J, Kuhn HG. Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J Neurosci Res. 2004;77:155-65.
56. Mohapel P, Leanza G, Kokaia M, Lindvall O. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging. 2005;26:939-46.
57. Carlen M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Frisen J. Functional integration of adult-born neurons. Curr Biol. 2002;12:606-8.
58. Abrous DN, Koehl M, Le Moal M. Adult neurogenesis:From precursors to network and physiology. Physiol Rev. 2005;85:523-69.
59. Lledo PM, Alonso M, Grubb MS. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci. 2006;7:179-93.
60. Dougherty KD, Milner TA. p75NTR immunoreactivity in the rat dentate gyrus is mostly within presynaptic profiles but is also found in some astrocytic and postsynaptic profiles. J Comp Neurol. 1999;407:77-91.
61. Kiss J, McGovern J, Patel AJ. Immunohistochemical localization of cells containing nerve growth factor receptors in the different regions of the adult rat forebrain. Neuroscience. 1988;27:731-48.
62. Gage FH, Batchelor P, Chen KS, Chin D, Higgins GA, Koh S, Deputy S, Rosenberg MB, Fischer W, Bjorklund A. NGF receptor reexpression and NGF-mediated cholinergic neuronal hypertrophy in the damaged adult neostriatum. Neuron. 1989;2:1177-84.
63. Fouquet C, Tobin C, Rondi-Reig L. A new approach for medeling episodic memory from rodents to humans: The temporal order memory. Behav Brain Res. 2010;215:172-9.