Loss of correlations among proteins in brains of the Ts65Dn mouse model of down syndrome

Journal of Proteome Research

Volumn 11, Issue 2, 2012, Pages 1251-1263

  Ahmed, Md Mahiuddin ^a   Sturgeon, Xiaolu ^a   Ellison, Misoo ^b   Davisson, Muriel T ^d   Gardiner, Katheleen J ^a,c  

^a Children's Hospital Colorado   (United States)

^b Global Health and Health Disparities   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d JACKSON LABORATORY   (United States)

Author keywords

MAP kinase; NMDA receptor; protein profiles; reverse phase protein array; Trisomy 21

Indexed keywords

BRAIN PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CEREBELLUM; CHROMOSOME 21; CONTROLLED STUDY; DOWN SYNDROME; FEMALE; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; TRISOMY;

ANIMALS; BLOTTING, WESTERN; BRAIN; BRAIN CHEMISTRY; DISEASE MODELS, ANIMAL; DOWN SYNDROME; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PROTEIN ARRAY ANALYSIS; PROTEIN INTERACTION MAPS; PROTEOME; RECEPTORS, N-METHYL-D-ASPARTATE; REPRODUCIBILITY OF RESULTS;

MUS;

EID: 84856688136     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2011582     Document Type: Article

References (59)

1. CDC, Centers for Disease Control and Prevention Improved National Prevalence for 18 Major Birth Defects Morbidity Mortal. Wkly. Rep. 2006, 54, 6-12
2. Chapman, R. S.; Hesketh, L. J. Behavioral phenotype of individuals with Down syndrome Ment. Retard. Dev. Disabil. Res. Rev. 2000, 6, 84-95
3. Silverman, W. Down syndrome: cognitive phenotype Ment. Retard. Dev. Disabil. Res. Rev. 2007, 13, 228-36
4. Vilardell, M.; Rasche, A.; Thormann, A.; Maschke-Dutz, E.; Pérez-Jurado, L. A.; Lehrach, H.; Herwig, R. Meta-analysis of heterogeneous Down Syndrome data reveals consistent genome-wide dosage effects related to neurological processes BMC Genomics 2011, 12, 229
5. Maier, T.; Güell, M.; Serrano, L. Correlation of mRNA and protein in complex biological samples FEBS Lett. 2009, 583, 3966-73
6. Schwanhäusser, B.; Busse, D.; Li, N.; Dittmar, G.; Schuchhardt, J.; Wolf, J.; Chen, W.; Selbach, M. Global quantification of mammalian gene expression control Nature 2011, 473, 337-42
7. Yang, S. H.; Jaffray, E.; Hay, R. T.; Sharrocks, A. D. Dynamic interplay of the SUMO and ERK pathways in regulating Elk-1 transcriptional activity Mol. Cell 2003, 12, 63-74
8. Salinas, S.; Briançon-Marjollet, A.; Bossis, G.; Lopez, M. A.; Piechaczyk, M.; Jariel-Encontre, I.; Debant, A.; Hipskind, R. A. SUMOylation regulates nucleo-cytoplasmic shuttling of Elk-1 J. Cell Biol. 2004, 165, 767-73
9. Sananbenesi, F.; Fischer, A.; Schrick, C.; Spiess, J.; Radulovic, J. Phosphorylation of hippocampal Erk-1/2, Elk-1, and p90-Rsk-1 during contextual fear conditioning: interactions between Erk-1/2 and Elk-1 Mol. Cell. Neurosci. 2002, 21 (3) 463-76
10. Braudeau, J.; Delatour, B.; Duchon, A.; Lopes-Pereira, P.; Dauphinot, L.; de Chaumont, F.; Olivo- Marin, J. C.; Dodd, R. H.; Hérault, Y.; Potier, M. C. Specific targeting of the GABA-A receptor {alpha}5 subtype by a selective inverse agonist restores cognitive deficits in Down syndrome mice J. Psychopharmacol. 2011, 25 (8) 1030-1042
11. Faizi, M.; Bader, P. L.; Tun, C.; Encarnacion, A.; Kleschevnikov, A.; Belichenko, P.; Saw, N.; Priestley, M.; Tsien, R. W.; Mobley, W. C.; Shamloo, M. Comprehensive behavioral phenotyping of Ts65Dn mouse model of Down Syndrome: Activation of β(1)-adrenergic receptor by xamoterol as a potential cognitive enhancer Neurobiol. Dis. 2011, 43, 397-413
12. Gardiner, K. J. Molecular basis of pharmacotherapies for cognition in Down syndrome Trends Pharmacol. Sci. 2010, 31, 66-73
13. Fernandez, F.; Trinidad, J. C.; Blank, M.; Feng, D. D.; Burlingame, A. L.; Garner, C. C. Normal protein composition of synapses in Ts65Dn mice: a mouse model of Down syndrome J. Neurochem. 2009, 110, 157-69
14. Wang, Y.; Mulligan, C.; Denyer, G.; Delom, F.; Dagna-Bricarelli, F.; Tybulewicz, V. L.; Fisher, E. M.; Griffiths, W. J.; Nizetic, D.; Groet, J. Quantitative proteomics characterization of a mouse embryonic stem cell model of Down syndrome Mol. Cell. Proteomics 2009, 8 (4) 585-95
15. Sun, Y.; Dierssen, M.; Toran, N.; Pollak, D. D.; Chen, W. Q.; Lubec, G. A gel-based proteomic method reveals several protein pathway abnormalities in fetal Down syndrome brain J. Proteomics 2011, 74, 547-57
16. Siddiqui, A.; Lacroix, T.; Stasko, M. R.; Scott-McKean, J. J.; Costa, A. C.; Gardiner, K. J. Molecular responses of the Ts65Dn and Ts1Cje mouse models of Down syndrome to MK-801 Genes Brain Behav. 2008, 7, 810-80
17. Siarey, R. J.; Kline-Burgess, A.; Cho, M.; Balbo, A.; Best, T. K.; Harashima, C.; Klann, E.; Galdzicki, Z. Altered signaling pathways underlying abnormal hippocampal synaptic plasticity in the Ts65Dn mouse model of Down syndrome J. Neurochem. 2006, 98, 1266-77
18. Gardiner, K.; Davisson, M. T.; Crnic, L. S. Building protein interaction maps for Down syndrome Briefings Funct. Genomics Proteomics 2004, 3, 142-56
19. Sturgeon, X.; Gardiner, K. J. Transcript catalogs of human chromosome 21 and orthologous chimpanzee and mouse regions Mamm. Genome 2011, 22, 261-71
20. Espina, V.; Mehta, A. I.; Winters, M. E.; Calvert, V.; Wulfkuhle, J.; Petricoin, E. F., 3rd; Liotta, L. Protein microarrays: molecular profiling technologies for clinical specimens Proteomics 2003, 3 (11) 2091-100
21. Nishizuka, S.; Charboneau, L.; Young, L.; Major, S.; Reinhold, W. C.; Waltham, M.; Kouros-Mehr, H.; Bussey, K. J.; Lee, J. K.; Espina, V.; Munson, P. J.; Petricoin, E. F., 3rd.; Liotta, L. A.; Weinstein, J. N. Proteomic profiling of the NCI-60 cancer cell lines using new high-density reverse-phase lysate microarrays Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (24) 14229-34
22. Wulfkuhle, J. D.; Edmiston, K. H.; Liotta, L. A.; Petricoin, E. F., 3rd. Technology insight: pharmacoproteomics for cancer - promises of patient-tailored medicine using protein microarrays Nat. Clin. Pract. Oncol. 2006, 3 (5) 256-68
23. Espina, V.; Wulfkuhle, J.; Calvert, V. S.; Liotta, L. A.; Petricoin, E. F., 3rd. Reverse phase protein microarrays for theranostics and patient-tailored therapy Methods Mol. Biol. 2008, 441, 113-28
24. Voshol, H.; Ehrat, M.; Traenkle, J.; Bertrand, E.; van Oostrum, J. Antibody-based proteomics: analysis of signaling networks using reverse protein arrays FEBS J. 2009, 276 (23) 6871-9
25. Davisson, M. T.; Schmidt, C.; Reeves, R. H.; Irving, N. G.; Akeson, E. C.; Harris, B. S.; Bronson, R. T. Segmental trisomy as a mouse model for Down syndrome Prog. Clin. Biol. Res. 1993, 384, 117-33
26. Liu, D. P.; Schmidt, C.; Billings, T.; Davisson, M. T. Quantitative PCR genotyping assay for the Ts65Dn mouse model of Down syndrome Biotechniques 2003, 35, 1170-4, 1176, 1178
27. Svensson, M.; Boren, M.; Sköld, K.; Fälth, M.; Sjögren, B.; Andersson, M.; Svenningsson, P.; Andren, P. E. Heat stabilization of the tissue proteome: a new technology for improved proteomics J. Proteome Res. 2009, 8, 974-81
28. Ahmed, M. M.; Gardiner, K. J. Preserving protein profiles in tissue samples: differing outcomes with and without heat stabilization J. Neurosci. Methods 2011, 196 (1) 99-106
29. Qi, H.; Juo, P.; Masuda-Robens, J.; Caloca, M. J.; Zhou, H.; Stone, N.; Kazanietz, M. G.; Chou, M. M. Caspase-mediated cleavage of the TIAM1 guanine nucleotide exchange factor during apoptosis Cell Growth Differ. 2001, 12, 603-11
30. Cousins, S. L.; Hoey, S. E.; Anne Stephenson, F.; Perkinton, M. S. Amyloid precursor protein 695 associates with assembled NR2A- and NR2B-containing NMDA receptors to result in the enhancement of their cell surface delivery J. Neurochem. 2009, 111, 1501-13
31. Hoe, H. S.; Fu, Z.; Makarova, A.; Lee, J. Y.; Lu, C.; Feng, L.; Pajoohesh-Ganji, A.; Matsuoka, Y.; Hyman, B. T.; Ehlers, M. D.; Vicini, S.; Pak, D. T.; Rebeck, G. W. The effects of amyloid precursor protein on postsynaptic composition and activity J. Biol. Chem. 2009, 284, 8495-506
32. Tolias, K. F.; Bikoff, J. B.; Burette, A.; Paradis, S.; Harrar, D.; Tavazoie, S.; Weinberg, R. J.; Greenberg, M. E. The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines Neuron 2005, 45, 525-38
33. Tolias, K. F.; Bikoff, J. B.; Kane, C. G.; Tolias, C. S.; Hu, L.; Greenberg, M. E. The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 7265-70
34. Nishimura, T.; Yamaguchi, T.; Tokunaga, A.; Hara, A.; Hamaguchi, T.; Kato, K.; Iwamatsu, A.; Okano, H.; Kaibuchi, K. Role of numb in dendritic spine development with a Cdc42 GEF intersectin and EphB2 Mol. Biol. Cell 2006, 17, 1273-85
35. Johnson, J. E. Numb and Numblike control cell number during vertebrate neurogenesis Trends Neurosci. 2003, 26 (8) 395-6
36. Kyriazis, G. A.; Wei, Z.; Vandermey, M.; Jo, D. G.; Xin, O.; Mattson, M. P.; Chan, S. L. Numb endocytic adapter proteins regulate the transport and processing of the amyloid precursor protein in an isoform-dependent manner: implications for Alzheimer disease pathogenesis J. Biol. Chem. 2008, 283, 25492-502
37. Roncarati, R.; Sestan, N.; Scheinfeld, M. H.; Berechid, B. E.; Lopez, P. A.; Meucci, O.; McGlade, J. C.; Rakic, P.; D'Adamio, L. The gamma-secretase- generated intracellular domain of beta-amyloid precursor protein binds Numb and inhibits Notch signaling Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 7102-7
38. Nguyen, C. D.; Costa, A. C.; Cios, K. J.; Gardiner, K. J. Machine learning methods predict locomotor response to MK-801 in mouse models of down syndrome J. Neurogenet. 2011, 25, 40-51
39. Gardiner, K.; Costa, A. C. The proteins of human chromosome 21 Am. J. Med. Genet., Part C 2006, 142C, 196-205
40. Sturgeon, X.; Ahmed, M. M.; Li, T.; Gardiner, K. J. Pathways to cognitive deficits in Down syndrome. Prog. Brain Res. 2012, in press.
41. Trazzi, S.; Mitrugno, V. M.; Valli, E.; Fuchs, C.; Rizzi, S.; Guidi, S.; Perini, G.; Bartesaghi, R.; Ciani, E. APP-dependent up-regulation of Ptch1 underlies proliferation impairment of neural precursors in Down syndrome Hum. Mol. Genet. 2011, 20, 1560-73
42. Nixon, R. A. Endosome function and dysfunction in Alzheimer's disease and other neurodegenerative diseases Neurobiol. Aging 2005, 26, 373-82
43. Lott, I. T.; Head, E.; Doran, E.; Busciglio, J. Beta-amyloid, oxidative stress and down syndrome Curr. Alzheimer Res. 2006, 3, 521-8
44. Tejedor, F. J.; Hämmerle, B. MNB/DYRK1A as a multiple regulator of neuronal development FEBS J. 2011, 278, 223-35
45. Yabut, O.; Domogauer, J.; D'Arcangelo, G. Dyrk1A overexpression inhibits proliferation and induces premature neuronal differentiation of neural progenitor cells J. Neurosci. 2010, 30 (11) 4004-14
46. Keating, D. J.; Chen, C.; Pritchard, M. A. Alzheimer's disease and endocytic dysfunction: clues from the Down syndrome-related proteins, DSCR1 and ITSN1 Ageing Res. Rev. 2006, 5, 388-401
47. Harris-Cerruti, C.; Kamsler, A.; Kaplan, B.; Lamb, B.; Segal, M.; Groner, Y. Functional and morphological alterations in compound transgenic mice overexpressing Cu/Zn superoxide dismutase and amyloid precursor protein [correction] Eur. J. Neurosci. 2004, 19, 1174-90
48. Zhang, H.; Macara, I. G. The polarity protein PAR-3 and TIAM1 cooperate in dendritic spine morphogenesis Nat. Cell Biol. 2006, 8, 227-37
49. Shirazi Fard, S.; Kele, J.; Vilar, M.; Paratcha, G.; Ledda, F. (2010). Tiam1 as a signaling mediator of nerve growth factor-dependent neurite outgrowth. PLoS One 2010, 5, e9647.
50. Sanij, E.; Hatzistavrou, T.; Hertzog, P.; Kola, I.; Wolvetang, E. J. Ets-2 is induced by oxidative stress and sensitizes cells to H(2)O(2)-induced apoptosis: implications for Down's syndrome Biochem. Biophys. Res. Commun. 2001, 287, 1003-8
51. Wolvetang, E. J.; Bradfield, O. M.; Hatzistavrou, T.; Crack, P. J.; Busciglio, J.; Kola, I.; Hertzog, P. J. Overexpression of the chromosome 21 transcription factor Ets2 induces neuronal apoptosis Neurobiol. Dis. 2003, 14, 349-56
52. Choi, J. H.; Berger, J. D.; Mazzella, M. J.; Morales-Corraliza, J.; Cataldo, A. M.; Nixon, R. A.; Ginsberg, S. D.; Levy, E.; Mathews, P. M. Age-dependent dysregulation of brain amyloid precursor protein in the Ts65Dn Down syndrome mouse model J. Neurochem. 2009, 110, 1818-27
53. Gioeli, D.; Wunderlich, W.; Sebolt-Leopold, J.; Bekiranov, S.; Wulfkuhle, J. D.; Petricoin, E. F.; Conaway, M.; Weber, M. J. Compensatory pathways induced by MEK inhibition are effective drug targets for combination therapy against castration-resistant prostate cancer Mol. Cancer Ther. 2011, 10, 1581-90
54. Wang, X.; Nadarajah, B.; Robinson, A. C.; McColl, B. W.; Jin, J. W.; Dajas-Bailador, F.; Boot-Handford, R. P.; Tournier, C. Targeted deletion of the mitogen-activated protein kinase kinase 4 gene in the nervous system causes severe brain developmental defects and premature death Mol. Cell. Biol. 2007, 27 (22) 7935-46
55. Costa, A. C.; Scott-Mckean, J. J.; Stasko, M. R. Acute injections of the NMDA receptor antagonist memantine rescue performance deficits of the Ts65Dn mouse model of Down syndrome on a Fear conditioning Test Neuropsychopharmacology 2008, 33 (7) 1624-32
56. Britschgi, M.; Rufibach, K.; Bauer-Huang, S. L.; Clark, C. M.; Kaye, J. A.; Li, G.; Peskind, E. R.; Quinn, J. F.; Galasko, D. R.; Wyss-Coray, T. Modeling of pathological traits in Alzheimer's disease based on systemic extracellular signaling proteome Mol. Cell. Proteomics 2011, 10, M111.008862
57. Sultan, M; Piccini, I; Balzereit, D; Herwig, R; Saran, N. G; Lehrach, H; Reeves, R. H; Yaspo, M. L. Gene expression variation in Down's syndrome mice allows prioritization of candidate genes Genome Biol. 2007, 8 (5) R91
58. Rueda, N.; Flórez, J.; Martínez-Cué, C. The Ts65Dn mouse model of Down syndrome shows reduced expression of the Bcl-X(L) antiapoptotic protein in the hippocampus not accompanied by changes in molecular or cellular markers of cell death Int. J. Dev. Neurosci 2011, 29, 711-6
59. Espina, V.; Mueller, C.; Edmiston, K.; Sciro, M.; Petricoin, E. F.; Liotta, L. A. Tissue is alive: New technologies are needed to address the problems of protein biomarker pre-analytical variability Proteomics Clin. Appl. 2009, 3, 874-82