Novel ethological endophenotypes in a transgenic mouse model of Huntington's disease

Behavioural Brain Research

Volumn 276, Issue , 2015, Pages 17-27

  Mo, Christina ^a   Renoir, Thibault ^a   Hannan, Anthony J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Ethological; Huntington's disease; Nest building; Olfactory; Sexual; Vocalization

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOPHENOTYPE; FEMALE; GENE MUTATION; GENOTYPE; HUNTINGTON CHOREA; MALE; MOUSE; NESTING; NONHUMAN; OLFACTORY DISCRIMINATION; SEXUAL BEHAVIOR; VOCALIZATION; ANIMAL; DISEASE MODEL; ESTRUS; ETHOLOGY; GENETICS; HUMAN; MUTATION; PHYSIOLOGY; PROCEDURES; SMELLING; TRANSGENIC MOUSE; URINE;

HTT PROTEIN, HUMAN; NERVE PROTEIN;

ANIMALS; DISEASE MODELS, ANIMAL; ENDOPHENOTYPES; ESTRUS; ETHOLOGY; FEMALE; HUMANS; HUNTINGTON DISEASE; MALE; MICE; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; NESTING BEHAVIOR; OLFACTORY PERCEPTION; URINE; VOCALIZATION, ANIMAL;

EID: 84910062160     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.04.003     Document Type: Article

References (89)

1. Aziz N.A., Swaab D.F., Pijl H., Roos R.A. Hypothalamic dysfunction and neuroendocrine and metabolic alterations in Huntington's disease: clinical consequences and therapeutic implications. Rev Neurosci 2007, 18:223-251.
2. Bacon Moore A., Paulsen J.S., Murphy C. A test of odor fluency in patients with Alzheimer's and Huntington's disease. J Clin Exp Neuropsychol 1999, 21:341-351.
3. Ballard T.M., Pauly-Evers M., Higgins G.A., Ouagazzal A.-M., Mutel V., et al. Severe impairment of NMDA receptor function in mice carrying targeted point mutations in the glycine binding site results in drug-resistant nonhabituating hyperactivity. J Neurosci 2002, 22:6713-6723.
4. Barnett S.A., Hocking W.E. Are nests built for fun? Effects of alternative activities on nest-building by wild house mice. Behav Neural Biol 1981, 31:73-81.
5. Bean N.J., Nunez A.A., Conner R. Effects of medial preoptic lesions on male mouse ultrasonic vocalizations and copulatory behavior. Brain Res Bull 1981, 6:109-112.
6. Beglinger L.J., O'Rourke J.J.F., Wang C., Langbehn D.R., Duff K., Paulsen J.S. Earliest functional declines in Huntington disease. Psychiatry Res 2010, 178:414-418.
7. Bennur S., Tsunada J., Cohen Y.E., Liu R.C. Understanding the neurophysiological basis of auditory abilities for social communication: a perspective on the value of ethological paradigms. Hearing Res 2013, 305:3-9.
8. Brooks S.P., Janghra N., Workman V.L., Bayram-Weston Z., Jones L., Dunnett S.B. Longitudinal analysis of the behavioural phenotype in R6/1 (C57BL/6J) Huntington's disease transgenic mice. Brain Res Bull 2012, 88:94-103.
9. Byatt S., Nyby J. Hormonal regulation of chemosignals of female mice that elicit ultrasonic vocalizations from males. Horm Behav 1986, 20:60-72.
10. Bylsma F., Moberg P., Doty R., Brandt J. Odor identification in Huntington's disease patients and asymptomatic gene carriers. J Neuropsychiatry Clin Neurosci 1997, 9:598-600.
11. Clifford J.J., Drago J., Natoli A.L., Wong J.Y.F., Kinsella A., et al. Essential fatty acids given from conception prevent topographies of motor deficit in a transgenic model of Huntington's disease. Neuroscience 2002, 109:81-88.
12. Costantini F., D'Amato F. Ultrasonic vocalizations in mice and rats: social contexts and functions. Acta Zool Sin 2006, 52:619-633.
13. Crawley J.N. Behavioral phenotyping strategies for mutant mice. Neuron 2008, 57:809-818.
14. Cunningham C., Deacon R., Wells H., Boche D., Waters S., et al. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur J Neurosci 2003, 17:2147-2155.
15. D'Amato F.R. Courtship ultrasonic vocalizations and social status in mice. Anim Behav 1991, 41:875-885.
16. Deacon R.M.J., Croucher A., Rawlins J.N.P. Hippocampal cytotoxic lesion effects on species-typical behaviours in mice. Behav Brain Res 2002, 132:203-213.
17. Delmaire C., Dumas E.M., Sharman M.A., van den Bogaard S.J.A., Valabregue R., et al. The structural correlates of functional deficits in early Huntington's disease. Hum Brain Mapp 2013, 34:2141-2153.
18. Dewhurst K., Oliver J.E., McKnight A.L. Socio-psychiatric consequences of Huntington's disease. Br J Psychiatry 1970, 116:255-258.
19. Dizinno G., Whitney G., Nyby J. Ultrasonic vocalizations by male mice (Mus musculus) to female sex pheromone: experiential determinants. Behav Biol 1978, 22:104-113.
20. Doty R. Odor-guided behavior in mammals. Experientia 1986, 42:257-271.
21. Du X., Leang L., Mustafa T., Renoir T., Pang T.Y., Hannan A.J. Environmental enrichment rescues female-specific hyperactivity of the hypothalamic-pituitary-adrenal axis in a model of Huntington's disease. Transl Psychiatry 2012, 2:e133.
22. Everitt B.J. Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci Biobehav Rev 1990, 14:217-232.
23. Ferrante R.J. Mouse models of Huntington's disease and methodological considerations for therapeutic trials. Biochim Biophys Acta (BBA)-Mol Basis Dis 2009, 1792:506-520.
24. Filali M., Lalonde R., Rivest S. Cognitive and non-cognitive behaviors in an APPswe/PS1 bigenic model of Alzheimer's disease. Genes, Brain Behav 2009, 8:143-148.
25. Fleming S.M., Salcedo J., Fernagut P.-O., Rockenstein E., Masliah E., et al. Early and progressive sensorimotor anomalies in mice overexpressing wild-type human α-synuclein. J Neurosci 2004, 24:9434-9440.
26. Gaskill B.N., Gordon C.J., Pajor E.A., Lucas J.R., Davis J.K., Garner J.P. Impact of nesting material on mouse body temperature and physiology. Physiol Behav 2013, 110-111:87-95.
27. Gaskill B.N., Karas A.Z., Garner J.P., Pritchett-Corning K.R. Nest building as an indicator of health and welfare in laboratory mice. J Vis Exp 2013, e51012.
28. Gerlai R., Clayton N.S. Analysing hippocampal function in transgenic mice: an ethological perspective. Trends Neurosci 1999, 22:47-51.
29. Gheusi G., Cremer H., McLean H., Chazal G., Vincent J.D., Lledo P.M. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Nat Acad Sci USA 2000, 97:1823-1828.
30. Gross A.N.-M., Engel A.K.J., Würbel H. Simply a nest? Effects of different enrichments on stereotypic and anxiety-related behaviour in mice. Appl Anim Behav Sci 2011, 134:239-245.
31. Grote H.E., Bull N.D., Howard M.L., Van Dellen A., Blakemore C., et al. Cognitive disorders and neurogenesis deficits in Huntington's disease mice are rescued by fluoxetine. Eur J Neurosci 2005, 22:2081-2088.
32. Hamilton J., Murphy C., Paulsen J. Odor detection, learning, and memory in Huntington's disease. J Int Neuropsychol Soc 1999, 5:609-615.
33. Hamilton J.M., Salmon D.P., Corey-Bloom J., Gamst A., Paulsen J.S., et al. Behavioural abnormalities contribute to functional decline in Huntington's disease. J Neurol, Neurosurg Psychiatry 2003, 74:120-122.
34. Hannan A.J., Ransome M.I. Deficits in spermatogenesis but not neurogenesis are alleviated by chronic testosterone therapy in R6/1 Huntington's disease mice. J Neuroendocrinol 2012, 24:341-356.
35. Hess S., Rohr S., Dufour B., Gaskill B., Pajor E., Garner J. Home improvement: C57BL/6J mice given more naturalistic nesting materials build better nests. J Am Assoc Lab Anim Sci 2008, 47:25-31.
36. Hockly E., Cordery P.M., Woodman B., Mahal A., van Dellen A., et al. Environmental enrichment slows disease progression in R6/2 Huntington's disease mice. Ann Neurol 2002, 51:235-242.
37. Hölter S.M., Stromberg M., Kovalenko M., Garrett L., Glasl L., et al. A broad phenotypic screen identifies novel phenotypes driven by a single mutant allele in Huntington's disease CAG knock-in mice. PLoS One 2013, 8:e80923.
38. Hull E.M., Dominguez J.M. Getting his act together: roles of glutamate, nitric oxide, and dopamine in the medial preoptic area. Brain Res 2006, 1126:66-75.
39. 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.
40. Jhanjee A., Anand K., Bajaj B. Hypersexual features in Huntington's disease. Singapore Med J 2011, 25:e131-e133.
41. Kalueff A.V., Ren-Patterson R.F., LaPorte J.L., Murphy D.L. Domain interplay concept in animal models of neuropsychiatric disorders: a new strategy for high-throughput neurophenotyping research. Behav Brain Res 2008, 188:243-249.
42. Kalueff A.V., Stewart A.M. Modeling neuropsychiatric spectra to empower translational biological psychiatry. Behav Brain Res 2014.
43. Katz S. Assessing self-maintenance: activities of daily living, mobility, and instrumental activities of daily living. J Am Geriatr Soc 1983, 31:721-727.
44. Kohl Z., Regensburger M., Aigner R., Kandasamy M., Winner B., et al. Impaired adult olfactory bulb neurogenesis in the R6/2 mouse model of Huntington's disease. BMC Neurosci 2010, 11:114.
45. Koyama S., Soini H.A., Foley J., Novotny M.V., Lai C. Stimulation of cell proliferation in the subventricular zone by synthetic murine pheromones. Front Behav Neurosci 2013, 7:101.
46. Larsson M., Lundin A., Robins Wahlin T. Olfactory functions in asymptomatic carriers of the Huntington disease mutation. J Clin Exp Neuropsychol 2006, 28:1373-1380.
47. Latham N., Mason G. From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl Anim Behav Sci 2004, 86:261-289.
48. Lazic S.E., Goodman A.O.G., Grote H.E., Blakemore C., Morton A.J., et al. Olfactory abnormalities in Huntington's disease: decreased plasticity in the primary olfactory cortex of R6/1 transgenic mice and reduced olfactory discrimination in patients. Brain Res 2007, 1151:219-226.
49. Li X., Morrow D., Witkin J.M. Decreases in nestlet shredding of mice by serotonin uptake inhibitors: comparison with marble burying. Sciences 2006, 78:1933-1939.
50. Malkesman O., Scattoni M.L., Paredes D., Tragon T., Pearson B., et al. The female urine sniffing test: a novel approach for assessing reward-seeking behavior in rodents. Biol Psychiatry 2010, 67:864-871.
51. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., et al. Exon I 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.
52. Mazarakis N.K., Cybulska-Klosowicz A., Grote H., Pang T., Van Dellen A., et al. Deficits in experience-dependent cortical plasticity and sensory-discrimination learning in presymptomatic Huntington's disease mice. J Neurosci 2005, 25:3059-3066.
53. Mo C., Renoir T., Pang T.Y.C., Hannan A.J. Short-term memory acquisition in female Huntington's disease mice is vulnerable to acute stress. Behav Brain Res 2013, 253:318-322.
54. Moberg P., Doty R. Olfactory function in Huntington's disease patients and at-risk offspring. Int J Neurosci 1997, 89:133-139.
55. Moretti P., Bouwknecht J.A., Teague R., Paylor R., Zoghbi H.Y. Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Hum Mol Genet 2005, 14:205-220.
56. Nelson J.F., Felicio L.S., Randall P.K., Sims C., Finch C.E. A longitudinal study of estrous cyclicity in aging C57BL/6J mice: I. Cycle frequency, length and vaginal cytology. Biol Reprod 1982, 27:327-339.
57. Nithianantharajah J., Barkus C., Murphy M., Hannan A.J. Gene-environment interactions modulating cognitive function and molecular correlates of synaptic plasticity in Huntington's disease transgenic mice. Neurobiol Dis 2008, 29:490-504.
58. Nordin S., Paulsen J.S., Murphy C. Sensory- and memory-mediated olfactory dysfunction in Huntington's disease. J Int Neuropsychol Soc 1995, 1:281-290.
59. Nunez A.A., Tan D.T. Courtship ultrasonic vocalizations in male Swiss-Webster mice: effects of hormones and sexual experience. Physiol Behav 1984, 32:717-721.
60. Nyby J. Ultrasonic vocalizations during sex behavior of male house mice (Mus musculus): a description. Behav Neural Biol 1983, 39:128-134.
61. Pang T.Y.C., 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.
62. Pang T.Y.C., Stam N.C., Nithianantharajah J., Howard M.L., Hannan A.J. Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in huntington's disease transgenic mice. Neuroscience 2006, 141:569-584.
63. Papalexi E., Persson A., Björkqvist M., Petersén Å., Woodman B., et al. Reduction of GnRH and infertility in the R6/2 mouse model of Huntington's disease. Eur J Neurosci 2005, 22:1541-1546.
64. Petersén Å., Gil J., Maat-Schieman M.L.C., Björkqvist M., Tanila H., et al. Orexin loss in Huntington's disease. Hum Mol Genet 2005, 14:39-47.
65. Petersén Å., Puschban Z., Lotharius J., NicNiocaill B., Wiekop P., et al. Evidence for dysfunction of the nigrostriatal pathway in the R6/1 line of transgenic Huntington's disease mice. Neurobiol Dis 2002, 11:134-146.
66. Pietropaolo S., Delage P., Cayzac S., Crusio W.E., Cho Y.H. Sex-dependent changes in social behaviors in motor pre-symptomatic R6/1 mice. PLoS One 2011, 6:e19965.
67. Pouladi M.A., Morton A.J., Hayden M.R. Choosing an animal model for the study of Huntington's disease. Nat Rev Neurosci 2013, 14:708-721.
68. Rattray I., Smith E.J., Crum W.R., Walker T.A., Gale R., et al. Correlations of behavioral deficits with brain pathology assessed through longitudinal mri and histopathology in the R6/1 mouse model of Huntington's disease. PLoS One 2013, 8:e84726.
69. Renoir T., Pang T.Y.C., Mo C., Chan G., Chevarin C., et al. Differential effects of early environmental enrichment on emotionality related behaviours in Huntington's disease transgenic mice. J Physiol 2013, 591:41-55.
70. Renoir T., Zajac M.S., Du X., Pang T.Y., Leang L., et al. Sexually dimorphic serotonergic dysfunction in a mouse model of Huntington's disease and depression. PLoS One 2011, 6:e22133.
71. Roullet F.I., Wöhr M., Crawley J.N. Female urine-induced male mice ultrasonic vocalizations, but not scent-marking, is modulated by social experience. Behav Brain Res 2011, 216:19-28.
72. Sager T.N., Kirchhoff J., MÃrk A., Van Beek J., Thirstrup K., et al. Nest building performance following MPTP toxicity in mice. Behav Brain Res 2010, 208:444-449.
73. Sassone J., Colciago C., Cislaghi G., Silani V., Ciammola A. Huntington's disease: the current state of research with peripheral tissues. Exp Neurol 2009, 219:385-397.
74. Schmidt E.Z., Bonelli R.M. Sexuality in Huntington's disease. WMW: Wien Med Wochenschr 2008, 158:78-83.
75. Sipos M.L., Kerchner M., Nyby J.G. An ephemeral sex pheromone in the urine of female house mice (Mus domesticus). Behav Neural Biol 1992, 58:138-143.
76. Sipos M.L., Wysocki C.J., Nyby J.G., Wysocki L., Nemura T.A. An ephemeral pheromone of female house mice: perception via the main and accessory olfactory systems. Physiol Behav 1995, 58:529-534.
77. Spires T.L., Grote H.E., Varshney N.K., Cordery P.M., van Dellen A., et al. Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease indicating a possible disease mechanism. J Neurosci 2004, 24:2270-2276.
78. Sugimoto H., Okabe S., Kato M., Koshida N., Shiroishi T., et al. A role for strain differences in waveforms of ultrasonic vocalizations during male-female interaction. PLoS One 2011, 6:e22093.
79. Van de Weerd H., Van Loo P., Van Zutphen L., Koolhaas J., Baumans V. Preferences for nesting material as environmental enrichment for laboratory mice. Lab Anim 1997, 31:133-143.
80. van Dellen A., Blakemore C., Deacon R., York D., Hannan A.J. Delaying the onset of Huntington's in mice. Nature 2000, 404:721-722.
81. van der Borght K., Brundin P. Reduced expression of PSA-NCAM in the hippocampus and piriform cortex of the R6/1 and R6/2 mouse models of Huntington's disease. Exp Neurol 2007, 204:473-478.
82. Voci V.E., Carlson N.R. Enhancement of maternal behavior and nest building following systemic and diencephalic administration of prolactin and progesterone in the mouse. J Comp Physiol Psychol 1973, 83:388-393.
83. Weydt P., Pineda V.V., Torrence A.E., Libby R.T., Satterfield T.F., et al. Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1α in Huntington's disease neurodegeneration. Cell Metab 2006, 4:349-362.
84. Whitney G., Alpern M., Dizinno G., Horowitz G. Female odors evoke ultrasounds from male mice. Anim Learn Behav 1974, 2:13-18.
85. Willke R.J., Burke L.B., Erickson P. Measuring treatment impact: a review of patient-reported outcomes and other efficacy endpoints in approved product labels. Controlled Clin Trials 2004, 25:535-552.
86. Witt R.M., Galligan M.M., Despinoy J.R., Segal R. Olfactory behavioral testing in the adult mouse. J Vis Exp 2009, e949.
87. Wolfe J.L., Barnett S.A. Effects of cold on nest-building by wild and domestic mice Mus musculus L. Biol J Linnean Soc 1977, 9:73-85.
88. Würbel H. Ideal homes? Housing effects on rodent brain and behaviour. Trends Neurosci 2001, 24:207-211.
89. Zarrow M.X., Gandelman R., Denenberg V.H. Lack of nest building and maternal behavior in the mouse following olfactory bulb removal. Horm Behav 1971, 2:227-238.