Targeted quantitative analysis of synaptic proteins in Alzheimer's disease brain

Neurochemistry International

Volumn 75, Issue , 2014, Pages 66-75

  Chang, Rachel Yoon Kyung ^a   Etheridge, Naomi ^a   Dodd, Peter R ^a   Nouwens, Amanda S ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Creatine kinase; Cytoskeleton; Degeneration; Multiple reaction monitoring; Oxidative stress; Peroxiredoxin

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN; CREATINE KINASE; CREATINE KINASE B; FRUCTOSE BISPHOSPHATE ALDOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE C; NERVE PROTEIN; PEROXIREDOXIN 1; SYNAPTOTAGMIN; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; ION TRAP MASS SPECTROMETRY; MOTOR CORTEX; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; BRAIN; METABOLISM; SYNAPSE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BRAIN; FEMALE; HUMANS; NERVE TISSUE PROTEINS; SYNAPSES;

EID: 84903158688     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2014.05.011     Document Type: Article

References (61)

1. T.A. Addona, S.E. Abbatiello, B. Schilling, S.J. Skates, D.R. Mani, D.M. Bunk, C.H. Spiegelman, L.J. Zimmerman, A.J. Ham, H. Keshishian, S.C. Hall, S. Allen, R.K. Blackman, C.H. Borchers, C. Buck, H.L. Cardasis, M.P. Cusack, N.G. Dodder, B.W. Gibson, J.M. Held, T. Hiltke, A. Jackson, E.B. Johansen, C.R. Kinsinger, J. Li, M. Mesri, T.A. Neubert, R.K. Niles, T.C. Pulsipher, D. Ransohoff, H. Rodriguez, P.A. Rudnick, D. Smith, D.L. Tabb, T.J. Tegeler, A.M. Variyath, L.J. Vega-Montoto, A. Wahlander, S. Waldemarson, M. Wang, J.R. Whiteaker, L. Zhao, N.L. Anderson, S.J. Fisher, D.C. Liebler, A.G. Paulovich, F.E. Regnier, P. Tempst, and S.A. Carr Multi-site assessment of the precision and reproducibility of multiple reaction monitoring-based measurements of proteins in plasma Nat. Biotechnol. 27 2009 633 641
2. M.Y. Aksenov, M.V. Aksenova, R.M. Payne, C.D. Smith, W.R. Markesbery, and J.M. Carney The expression of creatine kinase isoenzymes in neocortex of patients with neurodegenerative disorders: Alzheimer's and Pick's disease Exp. Neurol. 146 1997 458 465 (Pubitemid 27381852)
3. M.V. Aksenova, M.Y. Aksenov, R.M. Payne, J.Q. Trojanowski, M.L. Schmidt, J.M. Carney, D.A. Butterfield, and W.R. Markesbery Oxidation of cytosolic proteins and expression of creatine kinase BB in frontal lobe in different neurodegenerative disorders Dement. Geriatr. Cogn. Disord. 10 1999 158 165 (Pubitemid 29099701)
4. A. Ames 3rd CNS energy metabolism as related to function Brain Res. Brain Res. Rev. 34 2000 42 68
5. L. Anderson, and C.L. Hunter Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins Mol. Cell. Proteomics 5 2006 573 588
6. V.P. Andreev, V.A. Petyuk, H.M. Brewer, Y.V. Karpievitch, F. Xie, J. Clarke, D. Camp, R.D. Smith, A.P. Lieberman, R.L. Albin, Z. Nawaz, J. El Hokayem, and A.J. Myers Label-free quantitative LC-MS proteomics of Alzheimer's disease and normally aged human brains J. Proteome Res. 11 2012 3053 3067
7. M. Arundine, and M. Tymianski Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity Cell Calcium 34 2003 325 337 (Pubitemid 37021228)
8. J.P. Brion, and J. Flament-Durand Distribution and expression of the α-tubulin mRNA in the hippocampus and the temporal cortex in Alzheimer's disease Pathol. Res. Pract. 191 1995 490 498
9. D.A. Butterfield, D. Boyd-Kimball, and A. Castegna Proteomics in Alzheimer's disease: insights into potential mechanisms of neurodegeneration J. Neurochem. 86 2003 1313 1327 (Pubitemid 37174249)
10. A. Castegna, M. Aksenov, M. Aksenova, V. Thongboonkerd, J.B. Klein, W.M. Pierce, R. Booze, W.R. Markesbery, and D.A. Butterfield Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1 Free Radical Biol. Med. 33 2002 562 571 (Pubitemid 34874977)
11. A. Castegna, M. Aksenov, V. Thongboonkerd, J.B. Klein, W.M. Pierce, R. Booze, W.R. Markesbery, and D.A. Butterfield Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, α-enolase and heat shock cognate 71 J. Neurochem. 82 2002 1524 1532
12. A.M. Cataldo, J.L. Barnett, S.A. Berman, J. Li, S. Quarless, S. Bursztajn, C. Lippa, and R.A. Nixon Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: evidence for early up-regulation of the endosomal-lysosomal system Neuron 14 1995 671 680
13. R.Y.K. Chang, N. Etheridge, P.R. Dodd, and A. Nouwens Quantitative multiple reaction monitoring analysis of synaptic proteins from human brain J. Neurosci. Methods 227 2014 189 210
14. R.Y.K. Chang, A.S. Nouwens, P.R. Dodd, and N. Etheridge The synaptic proteome in Alzheimer's disease Alzheimers Dement. 9 2013 499 511
15. S.H. Chang, I.S. Jung, G.Y. Han, N.H. Kim, H.J. Kim, and C.W. Kim Proteomic profiling of brain cortex tissues in a tau transgenic mouse model of Alzheimer's disease Biochem. Biophys. Res. Commun. 430 2013 670 675
16. T.C. Chang, W.Y. Chou, and G.G. Chang Protein oxidation and turnover J. Biomed. Sci. 7 2000 357 363
17. E. Charrier, S. Reibel, V. Rogemond, M. Aguera, N. Thomasset, and J. Honnorat Collapsin response mediator proteins (CRMPs): involvement in nervous system development and adult neurodegenerative disorders Mol. Neurobiol. 28 2003 51 64
18. J. Chen, M. Wang, and I.V. Turko Mass spectrometry quantification of clusterin in the human brain Mol. Neurodegener. 7 2012 41
19. J.T. Coyle, and P. Puttfarcken Oxidative stress, glutamate, and neurodegenerative disorders Science 262 1993 689 695 (Pubitemid 23350687)
20. J.A. Daniel, C.S. Malladi, E. Kettle, A. McCluskey, and P.J. Robinson Analysis of synaptic vesicle endocytosis in synaptosomes by high-content screening Nat. Protoc. 7 2012 1439 1455
21. S.T. DeKosky, and S.W. Scheff Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity Ann. Neurol. 27 1990 457 464 (Pubitemid 20149963)
22. P.R. Dodd, J.A. Hardy, E.B. Baiq, A.M. Kidd, E.D. Bird, W.E. Watson, and G.A. Johnson Optimization of freezing, storage, and thawing conditions for the preparation of metabolically active synaptosomes from frozen rat and human brain Neurochem. Pathol. 4 1986 177 198
23. P.R. Dodd, W.E. Watson, M.M. Morrison, G.A. Johnston, E.D. Bird, R.F. Cowburn, and J.A. Hardy Uptake of γ-aminobutyric acid and l-glutamic acid by synaptosomes from postmortem human cerebral cortex: multiple sites, sodium dependence and effect of tissue preparation Brain Res. 490 1989 320 331 (Pubitemid 19158564)
24. N. Etheridge, J.M. Lewohl, R.D. Mayfield, and R.A. Harris Synaptic proteome changes in the superior frontal gyrus and occipital cortex of the alcoholic brain Proteomics Clin. Appl. 3 2009 730 742
25. C.G. Hahn, A. Banerjee, M.L. Macdonald, D.S. Cho, J. Kamins, Z. Nie, K.E. Borgmann-Winter, T. Grosser, A. Pizarro, E. Ciccimaro, S.E. Arnold, H.Y. Wang, and I.A. Blair The post-synaptic density of human postmortem brain tissues: an experimental study paradigm for neuropsychiatric illnesses PLoS One 4 2009 e5251
26. G. Halliday, T. Ng, M. Rodriguez, A. Harding, P. Blumbergs, W. Evans, V. Fabian, J. Fryer, M. Gonzales, C. Harper, R. Kalnins, C.L. Masters, C. McLean, D.G. Milder, R. Pamphlett, G. Scott, A. Tannenberg, and J. Kril Consensus neuropathological diagnosis of common dementia syndromes: testing and standardising the use of multiple diagnostic criteria Acta Neuropathol. 104 2002 72 78 (Pubitemid 36075361)
27. J.A. Hardy, D.E. Bateman, A.M. Kidd, J.A. Edwardson, G.B. Singh, and P.R. Dodd Amino acid transport by synaptosomes isolated from post mortem human brain J. Neural Transm. 60 1984 57 62 (Pubitemid 14065254)
28. J.A. Hardy, and P.R. Dodd Metabolic and functional studies on post-mortem human brain Neurochem. Int. 5 1983 253 266 (Pubitemid 13034848)
29. B. Hempen, and J.P. Brion Reduction of acetylated α-tubulin immunoreactivity in neurofibrillary tangle-bearing neurons in Alzheimer's disease J. Neuropathol. Exp. Neurol. 55 1996 964 972 (Pubitemid 126449410)
30. K. Hensley, N. Hall, R. Subramaniam, P. Cole, M. Harris, M. Aksenov, M. Aksenova, S.P. Gabbita, J.F. Wu, and J.M. Carney et al. Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation J. Neurochem. 65 1995 2146 2156
31. M.R. Hynd, J.M. Lewohl, H.L. Scott, and P.R. Dodd Biochemical and molecular studies using human autopsy brain tissue J. Neurochem. 85 2003 543 562 (Pubitemid 36531920)
32. L. Ijsselstijn, L.J. Dekker, P.J. Koudstaal, A. Hofman, P.A. Sillevis Smitt, M.M. Breteler, and T.M. Luider Serum clusterin levels are not increased in presymptomatic Alzheimer's disease J. Proteome Res. 10 2011 2006 2010
33. P. Iwangoff, R. Armbruster, A. Enz, and W. Meier-Ruge Glycolytic enzymes from human autoptic brain cortex: normal aged and demented cases Mech. Ageing Dev. 14 1980 203 209 (Pubitemid 11175996)
34. S.H. Kim, M. Fountoulakis, N. Cairns, and G. Lubec Protein levels of human peroxiredoxin subtypes in brains of patients with Alzheimer's disease and Down syndrome J. Neural Transm. Suppl. 2001 223 235 (Pubitemid 38085085)
35. R.E. Kohnken, U.S. Ladror, G.T. Wang, T.F. Holzman, B.E. Miller, and G.A. Krafft Cathepsin D from Alzheimer's-diseased and normal brains Exp. Neurol. 133 1995 105 112
36. M.A. Korolainen, G. Goldsteins, T.A. Nyman, I. Alafuzoff, J. Koistinaho, and T. Pirttila Oxidative modification of proteins in the frontal cortex of Alzheimer's disease brain Neurobiol. Aging 27 2006 42 53 (Pubitemid 41627949)
37. S.W. Kuo, and P.R. Dodd Electrically evoked synaptosomal amino acid transmitter release in human brain in alcohol misuse Neuro-Signals 19 2011 117 127
38. V. Lange, J.A. Malmstrom, J. Didion, N.L. King, B.P. Johansson, J. Schafer, J. Rameseder, C.H. Wong, E.W. Deutsch, M.Y. Brusniak, P. Buhlmann, L. Bjorck, B. Domon, and R. Aebersold Targeted quantitative analysis of Streptococcus pyogenes virulence factors by multiple reaction monitoring Mol. Cell. Proteomics 7 2008 1489 1500
39. Y.J. Lee, J.S. Goo, J.E. Kim, S.H. Nam, I.S. Hwang, S.I. Choi, H.R. Lee, E.P. Lee, H.W. Choi, H.S. Kim, J.H. Lee, Y.J. Jung, H.J. Kim, and D.Y. Hwang Peroxiredoxin I regulates the component expression of γ-secretase complex causing the Alzheimer's disease Lab. Anim. Res. 27 2011 293 299
40. G. Li, H. Jiang, M. Chang, H. Xie, and L. Hu HDAC6 α-tubulin deacetylase: a potential therapeutic target in neurodegenerative diseases J. Neurol. Sci. 304 2011 1 8
41. B. MacLean, D.M. Tomazela, N. Shulman, M. Chambers, G.L. Finney, B. Frewen, R. Kern, D.L. Tabb, D.C. Liebler, and M.J. MacCoss Skyline: an open source document editor for creating and analyzing targeted proteomics experiments Bioinformatics 26 2010 966 968
42. P. Mallick, M. Schirle, S.S. Chen, M.R. Flory, H. Lee, D. Martin, J. Ranish, B. Raught, R. Schmitt, T. Werner, B. Kuster, and R. Aebersold Computational prediction of proteotypic peptides for quantitative proteomics Nat. Biotechnol. 25 2007 125 131 (Pubitemid 46098780)
43. E. Masliah, M. Mallory, M. Alford, R. DeTeresa, L.A. Hansen, D.W. McKeel Jr., and J.C. Morris Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease Neurology 56 2001 127 129 (Pubitemid 32059669)
44. I. Nikonenko, B. Boda, S. Steen, G. Knott, E. Welker, and D. Muller PSD-95 promotes synaptogenesis and multiinnervated spine formation through nitric oxide signaling J. Cell Biol. 183 2008 1115 1127
45. S. Oddo, A. Caccamo, J.D. Shepherd, M.P. Murphy, T.E. Golde, R. Kayed, R. Metherate, M.P. Mattson, Y. Akbari, and F.M. LaFerla Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Aβ and synaptic dysfunction Neuron 39 2003 409 421 (Pubitemid 36937044)
46. P. Picotti, B. Bodenmiller, L.N. Müller, B. Domon, and R. Aebersold Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics Cell 138 2009 795 806
47. T.T. Reed, W.M. Pierce, W.R. Markesbery, and D.A. Butterfield Proteomic identification of HNE-bound proteins in early Alzheimer disease: Insights into the role of lipid peroxidation in the progression of AD Brain Res. 1274 2009 66 76
48. S.W. Scheff, S.T. DeKosky, and D.A. Price Quantitative assessment of cortical synaptic density in Alzheimer's disease Neurobiol. Aging 11 1990 29 37 (Pubitemid 20097857)
49. A. Shiozaki, T. Tsuji, R. Kohno, J. Kawamata, K. Uemura, H. Teraoka, and S. Shimohama Proteome analysis of brain proteins in Alzheimer's disease: subproteomics following sequentially extracted protein preparation J. Alzheimers Dis. 6 2004 257 268 (Pubitemid 38823260)
50. E.R. Stadtman, and R.L. Levine Free radical-mediated oxidation of free amino acids and amino acid residues in proteins Amino Acids 25 2003 207 218 (Pubitemid 38043943)
51. R. Sultana, D. Boyd-Kimball, J. Cai, W.M. Pierce, J.B. Klein, M. Merchant, and D.A. Butterfield Proteomics analysis of the Alzheimer's disease hippocampal proteome J. Alzheimers Dis. 11 2007 153 164 (Pubitemid 47010980)
52. R. Sultana, M. Perluigi, S.F. Newman, W.M. Pierce, C. Cini, R. Coccia, and D.A. Butterfield Redox proteomic analysis of carbonylated brain proteins in mild cognitive impairment and early Alzheimer's disease Antioxid. Redox Signal. 12 2010 327 336
53. R. Sultana, T. Reed, M. Perluigi, R. Coccia, W.M. Pierce, and D.A. Butterfield Proteomic identification of nitrated brain proteins in amnestic mild cognitive impairment: a regional study J. Cell. Mol. Med. 11 2007 839 851 (Pubitemid 47313301)
54. H.Y. Tang, L.A. Beer, K.T. Barnhart, and D.W. Speicher Rapid verification of candidate serological biomarkers using gel-based, label-free multiple reaction monitoring J. Proteome Res. 10 2011 4005 4017
55. R.D. Terry, E. Masliah, D.P. Salmon, N. Butters, R. Deteresa, R. Hill, L.A. Hansen, and R. Katzman Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment Ann. Neurol. 30 1991 572 580
56. UniProtConsortium, 2014. Dihydropyrimidinase-related protein 1, UniProtKB Protein Knowledgebase.
57. L. Urbanelli, C. Emiliani, C. Massini, E. Persichetti, A. Orlacchio, G. Pelicci, S. Sorbi, A. Hasilik, G. Bernardi, and A. Orlacchio Cathepsin D expression is decreased in Alzheimer's disease fibroblasts Neurobiol. Aging 29 2008 12 22 (Pubitemid 350102710)
58. M. Wang, and I.V. Turko Mass spectrometry quantification revealed accumulation of C-terminal fragment of apolipoprotein E in the Alzheimer's frontal cortex PLoS One 8 2013 e61498
59. Wimo, A., Prince, M., 2011. World Alzheimer Report 2010: The Global Economic Impact of Dementia, In: International, A.s.D. (Ed.), London, UK.
60. P.J. Yao, I. Bushlin, and K. Furukawa Preserved synaptic vesicle recycling in hippocampal neurons in a mouse Alzheimer's disease model Biochem. Biophys. Res. Commun. 330 2005 34 38 (Pubitemid 40394932)
61. J. Zhou, D.R. Jones, D.M. Duong, A.I. Levey, J.J. Lah, and J. Peng Proteomic analysis of postsynaptic density in Alzheimer's Disease Clin. Chim. Acta 420 2013 62 68