Mouse models of cognitive disorders in trisomy 21: A review

Behavior Genetics

Volumn 36, Issue 3, 2006, Pages 387-404

  Sérégaza, Zohra ^a   Roubertoux, Pierre L ^a,c   Jamon, Marc ^a   Soumireu Mourat, Bernard ^b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c CNRS   (France)

Author keywords

Cognition; Down's syndrome; Learning disorders; Memory; Mental retardation; Transgenic mice; Trisomy 21

Indexed keywords

BRAIN DISEASE; BRAIN FUNCTION; CHROMOSOME 21; COGNITION; COGNITIVE DEFECT; DISEASE MODEL; EXPLORATORY BEHAVIOR; GENE; GENE EXPRESSION; GENETIC MODEL; GENETIC TRANSFECTION; HUMAN CHROMOSOME; HUMAN CHROMOSOME 21 GENE; LEARNING; MEMORY; MENTAL DEFICIENCY; NONHUMAN; PHENOTYPE; REVIEW; SKILL; TRISOMY 21;

ANIMALS; COGNITION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; GENE EXPRESSION REGULATION; GENOME; HUMANS; LEARNING; MICE;

EID: 33745032837     PISSN: 00018244     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10519-006-9056-9     Document Type: Review

References (80)

1. Altafaj, X., Dierssen, M., Baamonde, C., Marti, E., Visa, J., Guimera, J., Oset, M., Gonzalez, J. R., Florez, J., and Fillat, C. et al., (2001). Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum. Mol. Genet. 10:1915-1923.
2. Antonarakis, S. E., Lyle, R., Dermitzakis, E. T., Reymond, A., and Deutsch, S. (2004). Chromosome 21 and down syndrome: from genomics to pathophysiology. Nat. Rev. Genet. 5:725-738.
3. Baxter, L. L., Moran, T. H., Richtsmeier, J. T., Troncoso, J., and Reeves, R. H. (2000). Discovery and genetic localization of Down syndrome cerebellar phenotypes using the Ts65Dn mouse. Hum. Mol. Genet. 9:195-202.
4. Belichenko, P. V., Masliah, E., Kleschevnikov, A. M., Villar, A. J., Epstein, C. J., Salehi, A., and Mobley, W. C. (2004). Synaptic structural abnormalities in the Ts65Dn mouse model of Down Syndrome. J. Comp. Neurol. 480:281-298.
5. Bell, K., Shokrian, D., Potenzieri, C., and Whitaker-Azmitia, P. M. (2003). Harm avoidance, anxiety, and response to novelty in the adolescent S-100beta transgenic mouse: role of serotonin and relevance to Down syndrome. Neuropsychopharmacology 28:1810-1816.
6. Bimonte-Nelson, H. A., Hunter, C. L., Nelson, M. E., and Granholm, A. C. (2003). Frontal cortex BDNF levels correlate with working memory in an animal model of Down syndrome. Behav. Brain Res. 139:47-57.
7. Branchi, I., Bichler, Z., Minghetti, L., Delabar, J. M., Malchiodi-Albedi, F., Gonzalez, M. C., Chettouh, Z., Nicolini, A., Chabert, C., and Smith, D. J. et al., (2004). Transgenic mouse in vivo library of human Down syndrome critical region 1: association between DYRK1A overexpression, brain development abnormalities, and cell cycle protein alteration. J. Neuropathol. Exp. Neurol. 63:429-440.
8. Brown, J. H., Johnson, M. H., Paterson, S. J., Gilmore, R., Longhi, E., and Karmiloff-Smith, A. (2003). Spatial representation and attention in toddlers with Williams syndrome and Down syndrome. Neuropsychology 41:1037-1046.
9. Caycho, L., Gunn, P., and Siegal, M. (1991). Counting by children with Down syndrome. Am. J. Ment. Retard. 95:575-583.
10. Chabert, C., Jamon, M., Cherfouh, A., Duquenne, V., Smith, D. J., Rubin, E. M., and Roubertoux, P. L. (2004). Functional analysis of genes implicated in Down Syndrome: 1. Cognitive abilities in Mice Transpolygenic for Down Syndrome Chromosomal Region-1 (DCR-1). Behav. Genet. 34:559-569.
11. Chapman, R. S., and Hesketh, L. J. (2000). Behavioral phenotype of individuals with Down syndrome. Ment. Retard Dev. Disabil. Res. Rev. 6:84-95.
12. Chrast, R., Scott, H. S., Madani, R., Huber, L., Wolfer, D. P., Prinz, M., Aguzzi, A., Lipp, H. P., and Antonarakis, S. E. (2000). Mice trisomie for a bacterial artificial chromosome with the single-minded 2 gene (Sim2) show phenotypes similar to some of those present in the partial trisomy 16 mouse models of Down syndrome. Hum. Mol. Genet. 9:1853-1864.
13. Clark, D., and Wilson, G. N. (2003). Behavioral assessment of children with Down syndrome using the Reiss psychopathology scale. Am. J. Med. Genet. A 118:210-216.
14. Coussons-Read, M. E., and Crnic, L. S. (1996). Behavioral assessment of the Ts65Dn mouse, a model for Down syndrome: altered behavior in the elevated plus maze and open field. Behav. Genet. 26:7-13.
15. Crnic, L. S., and Pennington, B. F. (2000). Down syndrome: Neuropsychology and animal models. Progr. Infanc. Res. 1:69-111.
16. Davisson, M. T., Schmidt, C., and Akeson, E. C. (1990). Segmental trisomy of murine chromosome 16: a new model system for studying Down syndrome. Prog. Clin. Biol. Res. 360:263-280.
17. Davisson, M. T., Schmidt, C., Reeves, R. H., Irving, N. G., Akeson, E. C., Harris, B. S., and Bronson, R. T. (1993). Segmental trisomy as a mouse model for Down syndrome. Prog. Clin. Biol. Res. 384:117-133.
18. Delabar, J. M., Theophile, D., Rahmani, Z., Chettouh, Z., Blouin, J. L., Prieur, M., Noel, B., and Sinet, P. M. (1993). Molecular mapping of twenty-four features of Down syndrome on chromosome 21. Eur. J. Hum. Genet. 1:114-124.
19. Demas, G. E., Nelson, R. J., Krueger, B. K., and Yarowsky, P. J. (1996). Spatial memory deficits in segmental trisomie Ts65Dn mice. Behav. Brain Res. 82:85-92.
20. Demas, G. E., Nelson, R. J., Krueger, B. K., and Yarowsky, P. J. (1998). Impaired spatial working and reference memory in segmental trisomy (Ts65Dn) mice. Behav. Brain Res. 90:199-201.
21. Dierssen, M., Fillat, C., Crnic, L., Arbones, M., Florez, J., and Estivill, X. (2001a). Murine models for Down syndrome. Physiol. Behav. 73:859-871.
22. Dierssen, M., Marti, E., Pucharcos, C., Fotaki, V., Altafaj, X., Casas, K., Solans, A., Arbones, M.L., Fillat, C., and Estivill, X. (2001b). Functional genomics of Down syndrome: a multidisciplinary approach. J. Neural. Transm. Suppl.: 131-148
23. Ema, M., Ikegami, S., Hosoya, T., Mimura. J., Ohtani, H., Nakao, K., Inokuchi, K., Katsuki, M., and Fujii-Kuriyama, Y. (1999). Mild impairment of learning and memory in mice overexpressing the mSim2 gene located on chromosome 16: an animal model of Down's syndrome. Hum. Mol. Genet. 8:1409-1415.
24. Escorihuela, R. M., Vallina, I. F., Martinez-Cue, C., Baamonde, C., Dierssen, M., Tobena, A., Florez, J., and Fernandez-Teruel, A. (1998). Impaired short- and long-term memory in Ts65Dn mice, a model for Down syndrome. Neurosci. Lett. 247:171-174.
25. Fotaki, V., Dierssen, M., Alcantara, S., Martinez, S., Marti, E., Casas, C., Visa, J., Soriano, E., Estivill, X., and Arbones, M. L. (2002). Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice. Mol. Cell. Biol. 22:6636-6647.
26. Fotaki, V., Martinez De Lagran, M., Estivill, X., Arbones, M., and Dierssen, M. (2004). Haploinsufficiency of Dyrk1A in mice leads to specific alterations in the development and regulation of motor activity. Behav. Neurosci. 118:815-821.
27. Gahtan, E., Auerbach, J. M., Groner, Y., and Segal, M. (1998). Reversible impairment of long-term potentiation in transgenic Cu/Zn-SOD mice. Eur. J. Neurosci. 10:538-544.
28. Gerlai, R., and Roder, J. (1993). Female specific hyperactivity in S100 beta transgenic mice does not habituate in open-field. Behav. Brain Res. 59:119-124.
29. Gerlai, R., and Roder, J. (1995). Abnormal exploratory behavior in transgenic mice carrying multiple copies of the human gene for S100 beta. J. Psych. Neurosci. 20:105-112.
30. Gerlai, R., and Roder, J. (1996). Spatial and nonspatial learning in mice: effects of S100 beta overexpression and age. Neurobiol. Learn. Mem. 66:143-154.
31. Gitton, Y., Dahmane, N., Baik, S., Ruizi Altaba, A., Neidhardt, L., Scholze, M., Herrmann, B. G., Kahlem, P., Benkahla, A., and Schrinner, S. et al., (2002). A gene expression map of human chromosome 21 orthologues in the mouse. Nature 420:586-590.
32. Granholm, A. C., Sanders, L. A., and Crnic, L. S. (2000). Loss of cholinergic phenotype in basal forebrain coincides with cognitive decline in a mouse model of Down's syndrome. Exp. Neurol. 161:647-663.
33. Gropp, A., Kolbus, U., and Giers, D. (1975). Systematic approach to the study of trisomy in the mouse. II. Cytogenet. Cell. Genet. 14:42-62.
34. Harris-Cerruti, C., Kamsler, A., Kaplan, B., Lamb, B., Segal, M., and Groner, Y. (2004). Functional and morphological alterations in compound transgenic mice overexpressing Cu/Zn superoxide dismutase and amyloid precursor protein [correction]. Eur. J. Neurosci. 19:1174-1190.
35. Hattori, M., Fujiyama, A., Taylor, T. D., Watanabe, H., Yada, T., Park, H. S., Toyoda, A., Ishii, K., Totoki, Y., and Choi, D. K. et al., (2000). The DNA sequence of human chromosome 21. Nature 405:311-319.
36. Hodapp, R. M., Ewans, D. E., and Gray, F. L. (1999). Intellectuel development in children with Down syndrome. In J.-A. Rondal, J. Perera and L. Nadel (eds.), Down Syndrome: A Review of Current Knowledge. London, U.K.: Whurr Publisher, pp. 124-132.
37. Holtzman, D. M., Santucci, D., Kilbridge, J., Chua-Couzens, J., Fontana, D. J., Daniels, S. E., Johnson, R. M., Chen, K., Sun, Y., and Carlson, E. et al., (1996). Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc. Natl. Acad. Sci. U.S.A 93:13333-13338.
38. Hunter, C. L., Bimonte-Nelson, H. A., Nelson, M., Eckman, C. B., and Granholm, A. C. (2004). Behavioral and neurobiological markers of Alzheimer's disease in Ts65Dn mice: effects of estrogen. Neurobiol. Aging 25:873-884.
39. Hyde, L. A., and Crnic, L. S. (2002). Reactivity to object and spatial novelty is normal in older Ts65Dn mice that model Down syndrome and Alzheimer's disease. Brain Res. 945:26-30.
40. Hyde, L. A., Frisone, D. F., and Crnic, L. S. (2001). Ts65Dn mice, a model for Down syndrome, have deficits in context discrimination learning suggesting impaired hippocampal function. Behav. Brain Res. 118:53-60.
41. Jackson, J. F., North, E. R. III, and Thomas, J. G. (1976). Clinical diagnosis of Down's syndrome. Clin. Genet. 9:483-487.
42. Janus, C., Janus, M., and Roder, J. (1995). Spatial exploration in transgenic mice expressing human beta-S100. Neurobiol. Learn. Mem. 64:58-67.
43. Kahlem, P., Sultan, M., Herwig, R., Steinfath, M., Balzereit, D., Eppens, B., Saran, N. G., Pletcher, M. T., South, S. T., and Stetten, G. et al., (2004). Transcript level alterations reflect gene dosage effects across multiple tissues in a mouse model of down syndrome. Genome Res. 14:1258-1267.
44. Klein, R. C., Siarey, R. J., Caruso, A., Rapoport, S. I., Castellino, F. J., and Galdzicki, Z. (2001). Increased expression of NR2A subunit does not alter NMDA-evoked responses in cultured fetal trisomy 16 mouse hippocampal neurons. J. Neurochem. 76:1663-1669.
45. Kleschevnikov, A. M., Belichenko, P. V., Villar, A. J., Epstein, C. J., Malenka, R. C., and Mobley, W. C. (2004). Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J. Neurosci. 24:8153-8160.
46. Korenberg, J. R., Chen, X. N., Schipper, R., Sun, Z., Gonsky, R., Gerwehr, S., Carpenter, N., Daumer, C., Dignan, P., and Disteche, C. et al., (1994). Down syndrome phenotypes: the consequences of chromosomal imbalance. Proc. Natl. Acad. Sci. U.S.A 91:4997-5001.
47. Krinsky-McHale, S. J., Devenny, D. A., and Silverman, W. P. (2002). Changes in explicit memory associated with early dementia in adults with Down's syndrome. J. Intellect. Disabil. Res. 46:198-208.
48. Laws, G. (2002). Working memory in children and adolescents with Down syndrome: evidence from a colour memory experiment. J. Child Psychol. Psych. 43:353-364.
49. Lejeune, J. (1990). Pathogenesis of mental deficiency in trisomy 21. Am. J. Med. Genet. Suppl. 7:20-30.
50. Lejeune, J., Gautier, M., and Turpin, R. (1959). [Study of somatic chromosomes from 9 mongoloid children.]. C. R. Hebd Seances Acad. Sci. 248:1721-1722.
51. Lyle, R., Gehrig, C., Neergaard-Henrichsen, C., Deutsch, S., and Antonarakis, S. E. (2004). Gene expression from the aneuploid chromosome in a trisomy mouse model of down syndrome. Genome Res. 14:1268-1274.
52. Marti, E., Altafaj, X., Dierssen, M., de la Luna, S., Fotaki, V., Alvarez, M., Perez-Riba, M., Ferrer, I., and Estivill, X. (2003). Dyrk1A expression pattern supports specific roles of this kinase in the adult central nervous system. Brain Res. 964:250-263.
53. Martinez-Cue, C., Baamonde, C., Lumbreras, M., Paz, J., Davisson, M. T., Schmidt, C., Dierssen, M., and Florez, J. (2002). Differential effects of environmental enrichment on behavior and learning of male and female Ts65Dn mice, a model for Down syndrome. Behav. Brain Res. 134:185-200.
54. Milner, B., Squire, L. R., and Kandel, E. R. (1998). Cognitive neuroscience and the study of memory. Neuron 20:445-468.
55. Moore, C. S., Lee, J. S., Birren, B., Stetten, G., Baxter, L. L., and Reeves, R. H. (1999). Integration of cytogenetic with recombinational and physical maps of mouse chromosome 16. Genomics 59:1-5.
56. Muller, W., Heinemann, U., and Schuchmann, S. (1997). Impaired Ca-signaling in astrocytes from the Ts16 mouse model of Down syndrome. Neurosci. Lett. 223:81-84.
57. Patterson, D., and Costa, A. C. (2005). Down syndrome and genetics - a case of linked histories. Nat. Rev. Genet. 6:137-147.
58. Peled-Kamar, M., Degani, H., Bendel, P., Margalit, R., and Groner, Y. (1998). Altered brain glucose metabolism in transgenic-PFKL mice with elevated L-phosphofructokinase: in vivo NMR studies. Brain Res. 810:138-145.
59. Pennington, B. F., Moon, J., Edgin, J., Stedron, J., and Nadel, L. (2003). The neuropsychology of Down syndrome: evidence for hippocampal dysfunction. Child Dev. 74:75-93.
60. Poissonnier, M., Saint-Paul, B., Dutrillaux, B., Chassaigne, M., Gruyer, P., and de Blignieres-Strouk, G. (1976). [Partial trisomy 21 (21q21 - 21q22.2)]. Ann. Genet. 19:69-73.
61. Raz, N., Torres, I. J., Briggs, S. D., Spencer, W. D., Thornton, A. E., Loken, W. J., Gunning, F. M., McQuain, J. D., Driesen, N. R., and Acker, J. D. (1995). Selective neuroanatomic abnormalities in Down's syndrome and their cognitive correlates: evidence from MRI morphometry. Neurology 45:356-366.
62. Reeves, R. H., Irving, N. G., Moran, T. H., Wohn, A., Kitt, C., Sisodia, S. S., Schmidt, C., Bronson, R. T., and Davisson, M. T. (1995). A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat. Genet. 11:177-184.
63. Roder, J. K., Roder, J. C., and Gerlai, R. (1996). Memory and the effect of cold shock in the water maze in S100 beta transgenic mice. Physiol. Behav. 60:611-615.
64. Roizen, N. J., and Patterson, D. (2003). Down's syndrome. Lancet 361:1281-1289.
65. Roubertoux, P., Sérégaza, Z., Jamon, M., Bichler, Z., Pinoteau, W., Smith, D. J., Rubin, E. M., and Carlier, M. (2005). Functional analysis of genes implicated in Down Syndrome: 2. laterality in mice transpolygenic for Down Syndrome Chromosomal Region-1 (DCR-1). Behav. Genet. 35:333-341.
66. Sago, H., Carlson, E. J., Smith, D. J., Kilbridge, J., Rubin, E. M., Mobley, W. C., Epstein, C. J., and Huang, T. T. (1998). Ts1Cje, a partial trisomy 16 mouse model for Down syndrome, exhibits learning and behavioral abnormalities. Proc. Natl. Acad. Sci. U.S.A 95:6256-6261.
67. Sago, H., Carlson, E. J., Smith, D. J., Rubin, E. M., Crnic, L. S., Huang, T. T., and Epstein, C. J. (2000). Genetic dissection of region associated with behavioral abnormalities in mouse models for Down syndrome. Pediatr. Res. 48:606-613.
68. 2+ signaling and mitochondrial deficiencies in hippocampal neurons of trisomy 16 mice: a model of Down's syndrome. J. Neurosci. 18:7216-7231.
69. Shapiro, L. A., Marks, A., and Whitaker-Azmitia, P. M. (2004). Increased clusterin expression in old but not young adult S100B transgenic mice: evidence of neuropathological aging in a model of Down Syndrome. Brain Res. 1010:17-21.
70. Shinohara, T., Tomizuka, K., Miyabara, S., Takehara, S., Kazuki, Y., Inoue, J., Katoh, M., Nakane, H., Iino, A., and Ohguma, A. et al., (2001). Mice containing a human chromosome 21 model behavioral impairment and cardiac anomalies of Down's syndrome. Hum. Mol. Genet. 10:1163-1175.
71. Siarey, R. J., Carlson, E. J., Epstein, C. J., Balbo, A., Rapoport, S. I., and Galdzicki, Z. (1999). Increased synaptic depression in the Ts65Dn mouse, a model for mental retardation in Down syndrome. Neuropharmacology 38:1917-1920.
72. Siarey, R. J., Stoll, J., Rapoport, S. I., and Galdzicki, Z. (1997). Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down Syndrome. Neuropharmacology 36:1549-1554.
73. Smith, D. J., and Rubin, E. M. (1997). Functional screening and complex traits: human 21q22.2 sequences affecting learning in mice. Hum. Mol. Genet. 6:1729-1733.
74. Smith, D. J., Zhu, Y.. Zhang, J., Cheng, J. F., and Rubin, E. M. (1995). Construction of a panel of transgenic mice containing a contiguous 2-Mb set of YAC/P1 clones from human chromosome 21q22.2. Genomics 27:425-434.
75. Stasko, M. R., and Costa, A. C. (2004). Experimental parameters affecting the Morris water maze performance of a mouse model of Down syndrome. Behav. Brain Res. 154:1-17.
76. Turner, C. A., Presti, M. F., Newman, H. A., Bugenhagen, P., Crnic, L., and Lewis, M. H. (2001). Spontaneous stereotypy in an animal model of Down syndrome: Ts65Dn mice. Behav. Genet. 31:393-400.
77. Wenger, G. R., Schmidt, C., and Davisson, M. T. (2004). Operant conditioning in the Ts65Dn mouse: learning. Behav. Genet. 34:105-119.
78. Whitaker-Azmitia, P. M., Wingate, M., Borella, A., Gerlai, R., Roder, J., and Azmitia, E. C. (1997). Transgenic mice overexpressing the neurotrophic factor S-100 beta show neuronal cytoskeletal and behavioral signs of altered aging processes: implications for Alzheimer's disease and Down's syndrome. Brain Res. 776:51-60.
79. Winocur, G., Roder, J., and Lobaugh, N. (2001). Learning and memory in S100-beta transgenic mice: an analysis of impaired and preserved function. Neurobiol. Learn. Mem. 75:230-243.
80. Zang da, W., Yang, Q., Wang, H. X., Egan, G., Lopes, E. C., and Cheema, S. S. (2004). Magnetic resonance imaging reveals neuronal degeneration in the brainstem of the superoxide dismutase 1 transgenic mouse model of amyotrophic lateral sclerosis. Eur. J. Neurosci. 20:1745-1751.