Early behavioral deficits in R6/2 mice suitable for use in preclinical drug testing

Neurobiology of Disease

Volumn 20, Issue 1, 2005, Pages 1-11

  Hickey, M A ^a   Gallant, K ^b   Gross, G G ^b   Levine, M S ^b   Chesselet, Marie Françoise ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Behavior; Climbing activity; Degenerative disease; High throughput screening; Huntington's disease; Mice; Motor activity; Mutant; Running wheels; Spontaneous activity

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOANALYSIS; BEHAVIOR DISORDER; CLIMBING; CONTROLLED STUDY; CORPUS STRIATUM; COST EFFECTIVENESS ANALYSIS; EXPERIMENTAL MODEL; FEMALE; GRIP STRENGTH; HIGH THROUGHPUT SCREENING; HUNTINGTON CHOREA; MALE; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; TRANSGENIC MOUSE; TREADMILL EXERCISE;

AGE FACTORS; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BODY WEIGHT; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; EXPLORATORY BEHAVIOR; FEMALE; HUNTINGTON DISEASE; MALE; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PHENOTYPE;

EID: 24044442568     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2005.01.024     Document Type: Article

References (61)

1. S.L. Andersen, P.J. Lyss, N.L. Dumont, and M.H. Teicher Enduring neurochemical effects of early maternal separation on limbic structures Ann. N. Y. Acad. Sci. 877 1999 756 759
2. G.P. Bates, and E. Hockly Experimental therapeutics in Huntington's disease: are models useful for therapeutic trials? Curr. Opin. Neurol. 16 2003 465 470
3. M.L. Beane, M.A. Cole, R.L. Spencer, and J.W. Rudy Neonatal handling enhances contextual fear conditioning and alters corticosterone stress responses in young rats Horm. Behav. 41 2002 33 40
4. J.A. Bibb, Z. Yan, P. Svenningsson, G.L. Snyder, V.A. Pieribone, A. Horiuchi, A.C. Nairn, A. Messer, and P. Greengard Severe deficiencies in dopamine signaling in presymptomatic Huntington's disease mice Proc. Natl. Acad. Sci. U. S. A. 97 2000 6809 6814
5. B.F. Boeve, M.H. Silber, T.J. Ferman, J.A. Lucas, and J.E. Parisi Association of REM sleep behavior disorder and neurodegenerative disease may reflect an underlying synucleinopathy Mov. Disord. 16 2001 622 630
6. V.J. Bolivar, K. Manley, and A. Messer Exploratory activity and fear conditioning abnormalities develop early in R6/2 Huntington's disease transgenic mice Behav. Neurosci. 117 2003 1233 1242
7. D. Brunner, E. Nestler, and E. Leahy In need of high-throughput behavioral systems Drug Discovery Today 7 2002 S107 S112
8. R.J. Carter, L.A. Lione, T. Humby, L. Mangiarini, A. Mahal, G.P. Bates, S.B. Dunnett, and A.J. Morton Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation J. Neurosci. 19 1999 3248 3257
9. C. Cepeda, M.A. Ariano, C.R. Calvert, J. Flores-Hernandez, S.H. Chandler, B.R. Leavitt, M.R. Hayden, and M.S. Levine NMDA receptor function in mouse models of Huntington disease J. Neurosci. Res. 66 2001 525 539
10. C. Cepeda, R.S. Hurst, C.R. Calvert, E. Hernandez-Echeagaray, O.K. Nguyen, E. Jocoy, L.J. Christian, M.A. Ariano, and M.S. Levine Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease J. Neurosci. 23 2003 961 969
11. J.H. Cha, C.M. Kosinski, J.A. Kerner, S.A. Alsdorf, L. Mangiarini, S.W. Davies, J.B. Penney, G.P. Bates, and A.B. Young Altered brain neurotransmitter receptors in transgenic mice expressing a portion of an abnormal human Huntington disease gene Proc. Natl. Acad. Sci. U. S. A. 95 1998 6480 6485
12. P. Chapillon, V. Patin, V. Roy, A. Vincent, and J. Caston Effects of pre- and postnatal stimulation on developmental, emotional, and cognitive aspects in rodents: a review Dev. Psychobiol. 41 2002 373 387
13. C.J. Cook Patterns of weaning and adult response to stress Physiol. Behav. 67 1999 803 808
14. D. Craufurd, J.C. Thompson, and J.S. Snowden Behavioral changes in Huntington disease Neuropsychiatry Neuropsychol. Behav. Neurol. 14 2001 219 226
15. S.W. Davies, M. Turmaine, B.A. Cozens, M. DiFiglia, A.H. Sharp, C.A. Ross, E. Scherzinger, E.E. Wanker, L. Mangiarini, and G.P. Bates Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation Cell 90 1997 537 548
16. A.W. Deckel, R. Elder, and G. Fuhrer Biphasic developmental changes in Ca2+/calmodulin-dependent proteins in R6/2 Huntington's disease mice NeuroReport 13 2002 707 711
17. M. de Tommaso, V. Sciruicchio, A. Spinelli, N. Specchio, O. Difruscolo, F. Puca, and L.M. Specchio Features of the blink reflex in individuals at risk for Huntington's disease Muscle Nerve 24 2001 1520 1525
18. A.W. Dunah, H. Jeong, A. Griffin, Y.M. Kim, D.G. Standaert, S.M. Hersch, M.M. Mouradian, A.B. Young, N. Tanese, and D. Krainc Sp1 and TAFII130 transcriptional activity disrupted in early Huntington's disease Science 296 2002 2238 2243
19. S.B. Dunnett, R.J. Carter, C. Watts, E.M. Torres, A. Mahal, L. Mangiarini, G. Bates, and A.J. Morton Striatal transplantation in a transgenic mouse model of Huntington's disease Exp. Neurol. 154 1998 31 40
20. J.N. Fain, N.A. Del Mar, C.A. Meade, A. Reiner, and D. Goldowitz Abnormalities in the functioning of adipocytes from R6/2 mice that are transgenic for the Huntington's disease mutation Hum. Mol. Genet. 10 2001 145 152
21. A. Feigin, K.L. Leenders, J.R. Moeller, J. Missimer, G. Kuenig, P. Spetsieris, A. Antonini, and D. Eidelberg Metabolic network abnormalities in early Huntington's disease: an [(18)F]FDG PET study J. Nucl. Med. 42 2001 1591 1595
22. S.E. File, A. Mahal, L. Mangiarini, and G.P. Bates Striking changes in anxiety in Huntington's disease transgenic mice Brain Res. 805 1998 234 240
23. E. Gómez-Tortosa, M.E. MacDonald, J.C. Friend, S.A. Taylor, L.J. Weiler, L.A. Cupples, J. Srinidhi, J.F. Gusella, E.D. Bird, J.P. Vonsattel, and R.H. Myers Quantitative neuropathological changes in presymptomatic Huntington's disease Ann. Neurol. 49 2001 29 34
24. G.T. Grossberg Diagnosis and treatment of Alzheimer's disease J. Clin. Psychiatry 64 Suppl. 9 2003 3 6
25. M. Hascoët, M. Bourin, and B.A. Dhonnchadha The mouse light-dark paradigm: a review Prog. Neuro-Psychopharmacol. Biol. Psychiatry 25 2001 141 166
26. M.A. Hickey, and M.F. Chesselet The use of transgenic and knock-in mice to study Huntington's disease Cytogenet. Genome Res. 100 2003 276 286
27. M.A. Hickey, S.E. Thomasian, E. Gruen, S. Zeitlin, X.J. Li, K.F. Faull, M.S. Levine, and M.F. Chesselet Antioxidant treatment and behavioural characterisation of a knock-in mouse model of Huntington's disease, Program No. 208.9. Abstract Viewer/Itinerary Planner 2003 Soc. Neurosci. 33rd Annual Meeting Washington, DC (online)
28. E. Hockly, P.M. Cordery, B. Woodman, A. Mahal, A. van Dellen, C. Blakemore, C.M. Lewis, A.J. Hannan, and G.P. Bates Environmental enrichment slows disease progression in R6/2 Huntington's disease mice Ann. Neurol. 51 2002 235 242
29. J.G. Hodgson, N. Agopyan, C.A. Gutekunst, B.R. Leavitt, F. LePiane, R. Singaraja, D.J. Smith, N. Bissada, K. McCutcheon, J. Nasir, L. Jamot, X.J. Li, M.E. Stevens, E. Rosemond, J.C. Roder, A.G. Phillips, E.M. Rubin, S.M. Hersch, and M.R. Hayden A YAC mouse model for Huntington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration Neuron 23 1999 181 192
30. F.C. Hsu, G.J. Zhang, Y.S. Raol, R.J. Valentino, D.A. Coulter, and A.R. Brooks-Kayal Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses Proc. Natl. Acad. Sci. U. S. A. 100 2003 12213 12218
31. M.S. Hurlbert, W. Zhou, C. Wasmeier, F.G. Kaddis, J.C. Hutton, and C.R. Freed Mice transgenic for an expanded CAG repeat in the Huntington's disease gene develop diabetes Diabetes 48 1999 649 651
32. Huntington's Disease Collaborative Research Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group Cell 72 1993 971 983
33. M. Kalinichev, K.W. Easterling, and S.G. Holtzman Early neonatal experience of Long-Evans rats results in long-lasting changes in reactivity to a novel environment and morphine-induced sensitization and tolerance Neuropsychopharmacology 27 2002 518 533
34. S.C. Kirkwood, E. Siemers, M.E. Hodes, P.M. Conneally, J.C. Christian, and T. Foroud Subtle changes among presymptomatic carriers of the Huntington's disease gene J. Neurol., Neurosurg. Psychiatry 69 2000 773 779
35. S.C. Kirkwood, E. Siemers, C. Bond, P.M. Conneally, J.C. Christian, and T. Foroud Confirmation of subtle motor changes among presymptomatic carriers of the Huntington disease gene Arch. Neurol. 57 2000 1040 1044
36. H. Kita, J. Carmichael, J. Swartz, S. Muro, A. Wyttenbach, K. Matsubara, D.C. Rubinsztein, and K. Kato Modulation of polyglutamine-induced cell death by genes identified by expression profiling Hum. Mol. Genet. 11 2002 2279 2287
37. G.J. Klapstein, R.S. Fisher, H. Zanjani, C. Cepeda, E.S. Jokel, M.F. Chesselet, and M.S. Levine Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice J. Neurophysiol. 86 2001 2667 2677
38. G.A. Laforet, E. Sapp, K. Chase, C. McIntyre, F.M. Boyce, M. Campbell, B.A. Cadigan, L. Warzecki, D.A. Tagle, P.H. Reddy, C. Cepeda, C.R. Calvert, E.S. Jokel, G.J. Klapstein, M.A. Ariano, M.S. Levine, M. DiFiglia, and N. Aronin Changes in cortical and striatal neurons predict behavioral and electrophysiological abnormalities in a transgenic murine model of Huntington's disease J. Neurosci. 21 2001 9112 9123
39. Y.Y. Lai, and J.M. Siegel Physiological and anatomical link between Parkinson-like disease and REM sleep behavior disorder Mol. Neurobiol. 27 2003 137 152
40. M.S. Levine, G.J. Klapstein, A. Koppel, E. Gruen, C. Cepeda, M.E. Vargas, E.S. Jokel, E.M. Carpenter, H. Zanjani, R.S. Hurst, A. Efstratiadis, S. Zeitlin, and M.F. Chesselet Enhanced sensitivity to N-methyl-d-aspartate receptor activation in transgenic and knockin mouse models of Huntington's disease J. Neurosci. Res. 58 1999 515 532
41. L.A. Lione, R.J. Carter, M.J. Hunt, G.P. Bates, A.J. Morton, and S.B. Dunnett Selective discrimination learning impairments in mice expressing the human Huntington's disease mutation J. Neurosci. 19 1999 10428 10437
42. H.G. Lüesse, J. Schiefer, A. Spruenken, C. Puls, F. Block, and C.M. Kosinski Evaluation of R6/2 HD transgenic mice for therapeutic studies in Huntington's disease: behavioral testing and impact of diabetes mellitus Behav. Brain Res. 126 2001 185 195
43. R. Luthi-Carter, S.A. Hanson, A.D. Strand, D.A. Bergstrom, W. Chun, N.L. Peters, A.M. Woods, E.Y. Chan, C. Kooperberg, D. Krainc, A.B. Young, S.J. Tapscott, and J.M. Olson Dysregulation of gene expression in the R6/2 model of polyglutamine disease: parallel changes in muscle and brain Hum. Mol. Genet. 11 2002 1911 1926
44. L. Mangiarini, K. Sathasivam, M. Seller, B. Cozens, A. Harper, C. Hetherington, M. Lawton, Y. Trottier, H. Lehrach, S.W. Davies, and G.P. Bates Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice Cell 87 1996 493 506
45. P. Meerlo, K.M. Horvath, G.M. Nagy, B. Bohus, and J.M. Koolhaas The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity J. Neuroendocrinol. 11 1999 925 933
46. L.B. Menalled, J.D. Sison, Y. Wu, M. Olivieri, X.J. Li, H. Li, S. Zeitlin, and M.F. Chesselet Early motor dysfunction and striosomal distribution of huntingtin microaggregates in Huntington's disease knock-in mice J. Neurosci. 22 2002 8266 8276
47. L.B. Menalled, J.D. Sison, S. Zeitlin, and M.F. Chesselet Time course of early motor and neuropathological anomalies in a knock-in mouse model of Huntington's disease with 140 CAG repeats J. Comp. Neurol. 465 2003 11 26
48. T.J. Morgan, T. Garland, and P.A. Jr. Carter Ontogenies in mice selected for high voluntary wheel-running activity: I. Mean ontogenies Evol. Int. J. Org. Evol. 57 2003 646 657
49. J.F. Morley, H.R. Brignull, J.J. Weyers, and R.I. Morimoto The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans Proc. Natl. Acad. Sci. U. S. A. 99 2002 10417 10422
50. A.J. Morton, M.A. Lagan, J.N. Skepper, and S.B. Dunnett Progressive formation of inclusions in the striatum and hippocampus of mice transgenic for the human Huntington's disease mutation J. Neurocytol. 29 2000 679 702
51. M.A. Nance, and R.H. Myers Juvenile onset Huntington's disease-clinical and research perspectives Ment. Retard. Dev. Disabil. Res. Rev. 7 2001 153 157
52. I.A.S. Olsson, and K. Dahlborn Improving housing conditions for laboratory mice: a review of 'environmental enrichment' Lab. Anim. 36 2002 243 270
53. L. Quinn, R. Reilmann, K. Marder, and A.M. Gordon Altered movement trajectories and force control during object transport in Huntington's disease Mov. Disord. 16 2001 469 480
54. R. Reilmann, F. Kirsten, L. Quinn, H. Henningsen, K. Marder, and A.M. Gordon Objective assessment of progression in Huntington's disease: a 3-year follow-up study Neurology 57 2001 920 924
55. G.E. Rockman, A. Hall, L. Markert, and G.B. Glavin Early weaning effects on voluntary ethanol consumption and stress responsivity in rats Physiol. Behav. 40 1987 673 676
56. M.A. Smith, J. Brandt, and R. Shadmehr Motor disorder in Huntington's disease begins as a dysfunction in error feedback control Nature 403 2000 544 549
57. A.J. Starling, S.H. Chandler, C. Cepeda, and M.S. Levine Alterations in NMDA and magnesium sensitivity occur early in development in the R6/2 mouse model of Huntington's disease, Program No. 206.3. Abstract Viewer/Itinerary Planner 2003 Soc. Neurosci. 33rd Annual Meeting Washington, DC (online)
58. G. Szebenyi, G.A. Morfini, A. Babcock, M. Gould, K. Selkoe, D.L. Stenoien, M. Young, P.W. Faber, M.E. MacDonald, M.J. McPhaul, and S.T. Brady Neuropathogenic forms of huntingtin and androgen receptor inhibit fast axonal transport Neuron 40 2003 41 52
59. J.P. van Vugt, S. Siesling, K.K. Piet, A.H. Zwinderman, H.A. Middelkoop, J.J. van Hilten, and R.A. Roos Quantitative assessment of daytime motor activity provides a responsive measure of functional decline in patients with Huntington's disease Mov. Disord. 16 2001 481 488
60. S. von Horsten, M.S. Exton, J. Voge, M. Schult, E. Nagel, R.E. Schmidt, J. Westermann, and M. Schedlowski Cyclosporine A affects open field behavior in DA rats Pharmacol. Biochem. Behav. 60 1998 71 76
61. M.M. Zeron, O. Hansson, N. Chen, C.L. Wellington, B.R. Leavitt, P. Brundin, M.R. Hayden, and L.A. Raymond Increased sensitivity to N-methyl-d-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease Neuron 33 2002 849 860