Normal protein composition of synapses in Ts65Dn mice: A mouse model of Down syndrome

Journal of Neurochemistry

Volumn 110, Issue 1, 2009, Pages 157-169

  Fernandez, Fabian ^a   Trinidad, Jonathan C ^b   Blank, Martina ^a   Feng, Dong Dong ^a   Burlingame, Alma L ^b   Garner, Craig C ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Down syndrome; Mass spectrometry; Plasticity; Post synaptic density; Synapse; Ts65Dn

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DOWN SYNDROME; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEOMICS; SYNAPSE;

ANIMALS; BIOLOGICAL MARKERS; CEREBRAL CORTEX; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; FEMALE; HOMEOSTASIS; MALE; MEMBRANE PROTEINS; MICE; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PHOSPHORYLATION; PROTEOMICS; SYNAPSES; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION;

MUS;

EID: 67449168368     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06110.x     Document Type: Article

References (72)

1. Akeson E. C., Lambert J. P., Narayanswami S., Gardiner K., Bechtel L. J. Davisson M. T. (2001) Ts65Dn - localization of the translocation breakpoint and trisomic gene content in a mouse model for Down syndrome. Cytogenet. Cell Genet. 93, 270 276. (Pubitemid 32799817)
2. Aldridge G. M., Podrebarac D. M., Greenough W. T. Weiler I. J. (2008) The use of total protein stains as loading controls: an alternative to high-abundance single-protein controls in semi-quantitative immunoblotting. J. Neurosci. Methods 172, 250 254.
3. Baxter L. L., Moran T. H., Richtmeier J. T., Troncoso J. Reeves R. H. (2000) Discovery and genetic localization of Down syndrome cerebellar phenotypes using the Ts65Dn mouse. Hum. Mol. Genet. 9, 195 202. (Pubitemid 30052743)
4. Becker L. E., Armstrong D. L. Chan F. (1986) Dendritic atrophy in children with Down's syndrome. Ann. Neurol. 20, 520 526. (Pubitemid 16005672)
5. Belichenko P. V., Masliah E., Kleschevnikov A. M., Villar A. J., Epstein C. J., Salehi A. Mobley W. C. (2004) Synaptic structural abnormalities in the Ts65Dn mouse model of Down syndrome. J. Comp. Neurol. 480, 281 298. (Pubitemid 39578025)
6. Belichenko P. V., Kleschevnikov A. M., Masliah E., Wu C., Takimoto-Kimura R., Salehi A. Mobley W. C. (2009) Excitatory-inhibitory relationship in the fascia dentata in the Ts65Dn mouse model of down syndrome. J. Comp. Neurol. 512, 453 466.
7. Bimonte-Nelson H. A., Hunter C. L., Nelson M. E. Granholm A.-C. E. (2003) Frontal cortex BDNF levels correlate with working memory in an animal model of Down syndrome. Behav. Brain Res. 139, 47 57. (Pubitemid 36300789)
8. Brugge K. L., Nichols S. L., Salmon D. P., Hill L. R., Delis D. C., Aaron L. Trauner D. A. (1994) Cognitive impairment in adults with Down's syndrome: similarities to early cognitive changes in Alzheimer's disease. Neurology 44, 232 238. (Pubitemid 24070957)
9. Busciglio J., Pelsman A., Wong C., Pigino G., Yuan M., Mori H. Yankner B. A. (2002) Altered metabolism of the amyloid beta precursor protein is associated with mitochondrial dysfunction in Down's syndrome. Neuron 33, 677 688. (Pubitemid 34219240)
10. Chechlacz M. Gleeson J. G. (2003) Is mental retardation a defect of synapse structure and function? Pediatr. Neurol. 29, 11 17. (Pubitemid 37117171)
11. Chi P., Greengard P. Ryan T. A. (2001) Synapsin dispersion and reclustering during synaptic activity. Nat. Neurosci. 4, 1187 1193. (Pubitemid 33135623)
12. Costa A. C. S. Grybko M. J. (2005) Deficits in hippocampal CA1 LTP induced by TBS but not HFS in the Ts65Dn mouse: a model of Down syndrome. Neurosci. Lett. 382, 317 322. (Pubitemid 40733644)
13. Dai Y., Taru H., Deken S. L., Grill B., Ackley B., Nonet M. L. Jin Y. (2006) SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 9, 1479 1487. (Pubitemid 44862655)
14. Davidoff L. M. (1928) The brain in Mongolian idiocy. Arch. Neurol. Psychiatr. 20, 1229 1257.
15. Davisson M. T., Schmidt C. 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.
16. Deguchi-Tawarada M., Inoue E., Takao-Rikitsu E., Inoue M., Ohtsuka T. Takai Y. (2004) CAST2: identification and characterization of a protein structurally related to the presynaptic cytomatrix protein CAST 2. Genes Cells 9, 15 23. (Pubitemid 38180878)
17. Demas G. E., Nelson R. J., Krueger B. K. Yarowsky P. J. (1996) Spatial memory deficits in segmental trisomic Ts65Dn mice. Behav. Brain Res. 82, 85 92. (Pubitemid 27033629)
18. Demas G. E., Nelson R. J., Krueger B. K. Yarowsky P. J. (1998) Impaired spatial working and reference memory in segmental Trisomy (Ts65Dn) mice. Behav. Brain Res. 90, 199 201. (Pubitemid 28080561)
19. Dresbach T., Qualmann B., Kessels M. M., Garner C. C. Gundelfinger E. D. (2001) The presynaptic cytomatrix of brain synapses. Cell. Mol. Life Sci. 58, 94 116. (Pubitemid 32146160)
20. Ehlers M. D. (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6, 231 242. (Pubitemid 36278281)
21. Elias G. M. Nicoll R. A. (2007) Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol. 17, 343 352.
22. Elias G. M., Funke L., Stein V., Grant S. G., Bredt D. S. Nicoll R. A. (2006) Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 52, 307 320. (Pubitemid 44548345)
23. Escorihuela R. M., Fernandez-Teruel A., Vallina I. F., Baamonde C., Lumbreras M. A., Dierssen M., Tobena A. Florez J. (1995) A behavioral assessment of Ts65Dn mice: a putative Down syndrome model. Neurosci. Lett. 199, 142 146.
24. Escorihuela R. M., Vallina I. F., Martinez-Cue C., Baamonde C., Dierssen M., Tobena A., Florez J. Fernandez-Teruel A. (1998) Impaired short- and long-term memory in Ts65Dn mice, a model for Down syndrome. Neurosci. Lett. 247, 171 174. (Pubitemid 28240124)
25. Fellin T., Pascual O. Haydon P. G. (2006) Astrocytes coordinate synaptic networks: balanced excitation and inhibition. Physiology 21, 208 215. (Pubitemid 43801250)
26. Fernandez F. Garner C. C. (2007) Over-inhibition: a model for developmental intellectual disability. TINS 30, 497 503. (Pubitemid 47513234)
27. Fernandez F., Morishita W., Zuniga E., Nguyen J., Blank M., Malenka R. C. Garner C. C. (2007) Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat. Neurosci. 10, 411 413. (Pubitemid 46494581)
28. Ferrer I. Gullota F. (1990) Down's syndrome and Alzheimer's disease: dendritic spine counts in the hippocampus. Acta Neuropathol. 79, 680 685. (Pubitemid 20170346)
29. Galvez R. Greenough W. T. (2005) Sequence of abnormal dendritic spine development in primary somatosensory cortex of a mouse model of the fragile X mental retardation syndrome. Am J Med Genet A 135, 155 160. (Pubitemid 40769965)
30. 2+ sensor for transmitter release at a central synapse. Cell 79, 717 727.
31. Greengard P., Valtorta F., Czernik A. J. Benfenati F. (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259, 780 785.
32. Hanson J. E., Blank M., Valenzuela R. A., Garner C. C. Madison D. V. (2007) The functional nature of synaptic circuitry is altered in area CA3 of the hippocampus in a mouse model of Down syndrome. J. Physiol. 579, 53 67. (Pubitemid 46243396)
33. Holtzman D. M., Santucci D., Kilbridges J. et al. (1996) Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc. Natl Acad. Sci. USA. 93, 13333 13338.
34. Hunter C. L., Bimonte H. A. Granholm A.-C. E. (2003) Behavioral comparison of 4 and 6 month-old Ts65Dn mice: age-related impairments in working and reference memory. Behav. Brain Res. 138, 121 131. (Pubitemid 36071351)
35. Hyde L. A. Crnic L. S. (2001) Age-related deficits in context discrimination learning in Ts65Dn mice that model Down's syndrome and Alzheimer's disease. Behav. Neurosci. 115, 1239 1246. (Pubitemid 33139131)
36. Kleschevnikov A. M., Belichenko P. V., Villar A. J., Epstein C. J., Malenka R. C. 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. (Pubitemid 39280835)
37. Kurt M. A., Davies D. C., Kidd M., Dierssen M. Florez J. (2000) Synaptic deficit in the temporal cortex of partial trisomy 16 Ts65Dn mice. Brain Res. 858, 191 197. (Pubitemid 30105799)
38. Lejeune J., Turpin R. Gautier M. (1959) Le mongolisme, premier exemple d'aberration autosomique humain. Ann. Genet. 1, 92 101.
39. Malenka R. C. Bear M. F. (2004) LTP and LTD: an embarrassment of riches. Neuron 44, 5 21. (Pubitemid 39348827)
40. Malinow R. Malenka R. C. (2002) AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103 126. (Pubitemid 34748013)
41. Marin-Padilla M. (1972) Structural abnormalities of the cerebral cortex in human chromosomal aberrations: a Golgi study. Brain Res. 44, 625 629.
42. Marin-Padilla M. (1976) Pyramidal cell abnormalities in the motor cortex of a child with Down's syndrome. A Golgi study. J. Comp. Neurol. 167, 63 81.
43. Nadel L. (2003) Down's syndrome: a genetic disorder in biobehavioral perspective. Genes Brain Behav. 2, 156 166. (Pubitemid 36898802)
44. Olson L. E., Roper R. J., Baxter L. L., Carlson E. J., Epstein C. J. Reeves R. H. (2004) Down syndrome mouse models Ts65Dn, Ts1Cje, and Ms1Cje/Ts65Dn exhibit variable severity of cerebellar phenotypes. Dev. Dyn. 230, 581 589. (Pubitemid 38802484)
45. Patel M. R., Lehrman E. K., Poon V. Y., Crump J. G., Zhen M., Bargmann C. I. Shen K. (2006) Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat. Neurosci. 9, 1488 1498. (Pubitemid 44862656)
46. Pollonini G., Gao V., Rabe A., Palminiello S., Albertini G. Alberini C. M. (2008) Abnormal expression of synaptic proteins and neurotrophin-3 in the Down syndrome mouse model Ts65Dn. Neuroscience 156, 99 106.
47. Reeves R. H., Irving N. G., Moran T. H. et al. (1995) A mouse model for down syndrome exhibits learning and behavior deficits. Nat. Genet. 11, 177 184.
48. Richtsmeier J. T., Baxter L. L. Reeves R. H. (2000) Parallels of craniofacial maldevelopment in Down syndrome and Ts65Dn mice. Dev. Dyn. 217, 137 145. (Pubitemid 30080493)
49. Richtsmeier J. T., Zumwalt A., Carlson E. J., Epstein C. J. Reeves R. H. (2002) Craniofacial phenotypes in segmentally trisomic mouse models for Down syndrome. Am. J. Med. Genet. 107, 317 324. (Pubitemid 34062085)
50. Schmidt-Sidor B., Wisniewski K., Shepard T. Sersen E. (1990) Brain growth in Down syndrome subjects 15-22 weeks of gestational age at birth to 60 months. Clin. Neuropathol. 9, 181 190. (Pubitemid 20287898)
51. Schoch S. Gundelfinger E. D. (2006) Molecular organization of the presynaptic active zone. Cell Tissue Res. 326, 379 391. (Pubitemid 44435815)
52. Shen K., Teruel M. N., Connor J. H., Shenolikar S. Meyer T. (2000) Molecular memory by reversible translocation of calcium/calmodulin-dependent protein kinase II. Nat. Neurosci. 3, 881 886. (Pubitemid 30677174)
53. Sheng M. Hoogenraad C. C. (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 76, 823 847.
54. Siarey R. J., Stoll J., Rapoport S. I. Galdzicki Z. (1997) Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down syndrome. Neuropharmacology 36, 1549 1554. (Pubitemid 28085914)
55. Siarey R. J., Carlson E. J., Epstein C. J., Balbo A., Rapoport S. I. Galdzicki Z. (1999) Increased synaptic depression in the Ts65Dn mouse, a model for mental retardation in Down syndrome. Neuropharmacology 38, 1917 1920. (Pubitemid 29509730)
56. Siarey R. J., Kline-Burgess A., Cho M., Balbo A., Best T. K., Harashima C., Klann E. Galdzicki Z. (2006) Altered signaling pathways underlying abnormal hippocampal synaptic plasticity in the Ts65Dn mouse model of Down syndrome. J. Neurochem. 98, 1266 1277. (Pubitemid 44127800)
57. Siddiqui A., Lacroix T., Stasko M. R., Scott-McKean J. J., Costa A. C. S. Gardiner K. J. (2008) Molecular responses of the Ts65Dn and Ts1Cje mouse models of Down syndrome to MK-801. Genes Brain Behav. 7, 810 820.
58. Sudhof T. C. (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903 911.
59. Sudhof T. C., Lottspeich F., Greengard P., Mehl E. Jahn R. (1987) A synaptic vesicle protein with a novel cytoplasmic domain and four transmembrane regions. Science 238, 1142 1144.
60. Suetsugu M. Mehraein P. (1980) Spine distribution along the apical dendrites of the pyramidal neurons in Down's syndrome. A quantitative Golgi study. Acta Neuropathol. 50, 207 210. (Pubitemid 10030034)
61. Takashima S., Becker L. E., Armstrong D. L. Chan F.-W. (1981) Abnormal neuronal development in the visual cortex of the human fetus and infant with Down's syndrome. A quantitative and qualitative Golgi study. Brain Res. 225, 1 21. (Pubitemid 11026571)
62. Trinidad J. C., Specht C. G., Thalhammer A., Schoepfer R. Burlingame A. L. (2006) Comprehensive identification of phosphorylation sites in postsynaptic density preparations. Mol. Cell Proteomics 5, 914 922. (Pubitemid 43792800)
63. Trinidad J. C., Thalhammer A., Specht C. G., Lynn A. J., Baker P. R., Schoepfer R. Burlingame A. L. (2008) Quantitative analysis of synaptic phosphorylation and protein expression. Mol. Cell Proteomics 7, 684 696. (Pubitemid 351597480)
64. Turrigiano G. G. Nelson S. B. (2000) Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 10, 358 364. (Pubitemid 30389303)
65. Turrigiano G. G., Leslie K. R., Desai N. S., Rutherford L. C. Nelson S. B. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892 896. (Pubitemid 28157666)
66. Wagh D. A., Rasse T. M., Asan E. et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49, 833 844. (Pubitemid 43376081)
67. Waites C. L., Craig A. M. Garner C. C. (2005) Mechanisms of vertebrate synaptogenesis. Annu. Rev. Neurosci. 28, 251 274. (Pubitemid 41098906)
68. Walikonis R. S., Jensen O. N., Mann M., Provance D. W., Mercer J. A. Kennedy M. B. (2000) Identification of proteins in the postsynaptic density fraction by mass spectrometry. J. Neurosci. 20, 4069 4080. (Pubitemid 30365677)
69. Wenger G. R., Schmidt C. Davisson M. T. (2004) Operant conditioning in the Ts65Dn mouse: learning. Behav. Genet. 34, 105 119. (Pubitemid 38141757)
70. Willemsen R., Oostra B. A., Bassell G. J. Dictenberg J. (2004) The fragile X syndrome: from molecular genetics to neurobiology. Ment. Retard. Dev. Disabil. Res. Rev. 10, 60 67. (Pubitemid 38375355)
71. Ziv N. E. Garner C. C. (2004) Cellular and molecular mechanisms of presynaptic assembly. Nat. Rev. Neurosci. 5, 385 399. (Pubitemid 38568499)
72. Zoghbi H. Y. (2003) Postnatal neurodevelopmental disorders: meeting at the synapse? Science 302, 826 830. (Pubitemid 37339616)