Explorative and targeted neuroproteomics in Alzheimer's disease

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1854, Issue 7, 2015, Pages 769-778

  Brinkmalm, Ann ^a   Portelius, Erik ^a   Öhrfelt, Annika ^a   Brinkmalm, Gunnar ^a   Andreasson, Ulf ^a   Gobom, Johan ^a   Blennow, Kaj ^a   Zetterberg, Henrik ^a,b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Alzheimer's disease; Neuroproteomic

Indexed keywords

BIOLOGICAL MARKER; NERVE PROTEIN;

ALZHEIMER DISEASE; BIOSYNTHESIS; BRAIN; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; PROTEOMICS;

ALZHEIMER DISEASE; BIOLOGICAL MARKERS; BIOMARKERS; BRAIN; GENE EXPRESSION REGULATION; HUMANS; NERVE TISSUE PROTEINS; PROTEOMICS;

EID: 84939992465     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2015.01.009     Document Type: Review

References (143)

1. K. Blennow, M.J. de Leon, and H. Zetterberg Alzheimer's disease Lancet 368 2006 387 403
2. C.L. Masters, G. Simms, N.A. Weinman, G. Multhaup, B.L. McDonald, and K. Beyreuther Amyloid plaque core protein in Alzheimer disease and Down syndrome Proc. Natl. Acad. Sci. U. S. A. 82 1985 4245 4249
3. A. Goate, M.C. Chartier-Harlin, M. Mullan, J. Brown, F. Crawford, L. Fidani, L. Giuffra, A. Haynes, N. Irving, and L. James Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease Nature 349 1991 704 706
4. E. Levy-Lahad, W. Wasco, P. Poorkaj, D.M. Romano, J. Oshima, W.H. Pettingell, C.E. Yu, P.D. Jondro, S.D. Schmidt, and K. Wang Candidate gene for the chromosome 1 familial Alzheimer's disease locus Science 269 1995 973 977
5. R. Sherrington, E.I. Rogaev, Y. Liang, E.A. Rogaeva, G. Levesque, M. Ikeda, H. Chi, C. Lin, G. Li, K. Holman, T. Tsuda, L. Mar, J.F. Foncin, A.C. Bruni, M.P. Montesi, S. Sorbi, I. Rainero, L. Pinessi, L. Nee, I. Chumakov, D. Pollen, A. Brookes, P. Sanseau, R.J. Polinsky, W. Wasco, H.A. Da Silva, J.L. Haines, M.A. Perkicak-Vance, R.E. Tanzi, A.D. Roses, P.E. Fraser, J.M. Rommens, and P.H. St George-Hyslop Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease Nature 375 1995 754 760
6. I. Grundke-Iqbal, K. Iqbal, Y.C. Tung, M. Quinlan, H.M. Wisniewski, and L.I. Binder Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology Proc. Natl. Acad. Sci. U. S. A. 83 1986 4913 4917
7. N. Nukina, and Y. Ihara One of the antigenic determinants of paired helical filaments is related to tau protein J. Biochem. 99 1986 1541 1544
8. C. Rosen, O. Hansson, K. Blennow, and H. Zetterberg Fluid biomarkers in Alzheimer's disease - current concepts Mol. Neurodegener. 8 2013 20
9. C.R. Jack Jr., D.S. Knopman, W.J. Jagust, L.M. Shaw, P.S. Aisen, M.W. Weiner, R.C. Petersen, and J.Q. Trojanowski Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade Lancet Neurol. 9 2010 119 128
10. J. Hardy Alzheimer's disease: the amyloid cascade hypothesis: an update and reappraisal J. Alzheimers Dis. 9 2006 151 153
11. E. Karran, and J. Hardy Antiamyloid therapy for Alzheimer's disease - are we on the right road? N. Engl. J. Med. 370 2014 377 378
12. M. Mann, N.A. Kulak, N. Nagaraj, and J. Cox The coming age of complete, accurate, and ubiquitous proteomes Mol. Cell 49 2013 583 590
13. J. Zhang, D.R. Goodlett, and T.J. Montine Proteomic biomarker discovery in cerebrospinal fluid for neurodegenerative diseases J. Alzheimers Dis. 8 2005 377 386
14. T. Hokfelt, C. Broberger, Z.Q. Xu, V. Sergeyev, R. Ubink, and M. Diez Neuropeptides - an overview Neuropharmacology 39 2000 1337 1356
15. C.E. Johanson, J.A. Duncan III, P.M. Klinge, T. Brinker, E.G. Stopa, and G.D. Silverberg Multiplicity of cerebrospinal fluid functions: new challenges in health and disease Cerebrospinal Fluid Res. 5 2008 10
16. M.A. Korolainen, T.A. Nyman, T. Aittokallio, and T. Pirttila An update on clinical proteomics in Alzheimer's research J. Neurochem. 112 2010 1386 1414
17. F. Abdi, J.F. Quinn, J. Jankovic, M. McIntosh, J.B. Leverenz, E. Peskind, R. Nixon, J. Nutt, K. Chung, C. Zabetian, A. Samii, M. Lin, S. Hattan, C. Pan, Y. Wang, J. Jin, D. Zhu, G.J. Li, Y. Liu, D. Waichunas, T.J. Montine, and J. Zhang Detection of biomarkers with a multiplex quantitative proteomic platform in cerebrospinal fluid of patients with neurodegenerative disorders J. Alzheimers Dis. 9 2006 293 348
18. D. Chiasserini, J.R. van Weering, S.R. Piersma, T.V. Pham, A. Malekzadeh, C.E. Teunissen, H. de Wit, and C.R. Jimenez Proteomic analysis of cerebrospinal fluid extracellular vesicles: a comprehensive dataset J. Proteomics 106 2014 191 204
19. J.M. Ringman, H. Schulman, C. Becker, T. Jones, Y. Bai, F. Immermann, G. Cole, S. Sokolow, K. Gylys, D.H. Geschwind, J.L. Cummings, and H.I. Wan Proteomic changes in cerebrospinal fluid of presymptomatic and affected persons carrying familial Alzheimer disease mutations Arch. Neurol. 69 2012 96 104
20. J. Zhang, D.R. Goodlett, E.R. Peskind, J.F. Quinn, Y. Zhou, Q. Wang, C. Pan, E. Yi, J. Eng, R.H. Aebersold, and T.J. Montine Quantitative proteomic analysis of age-related changes in human cerebrospinal fluid Neurobiol. Aging 26 2005 207 227
21. M. Holtta, H. Zetterberg, E. Mirgorodskaya, N. Mattsson, K. Blennow, and J. Gobom Peptidome analysis of cerebrospinal fluid by LC-MALDI MS PLoS One 7 2012 e42555
22. P. Schulz-Knappe, H.D. Zucht, G. Heine, M. Jurgens, R. Hess, and M. Schrader Peptidomics: the comprehensive analysis of peptides in complex biological mixtures Comb. Chem. High Throughput Screen. 4 2001 207 217
23. X. Yuan, and D.M. Desiderio Human cerebrospinal fluid peptidomics J. Mass Spectrom. 40 2005 176 181
24. A. Zougman, B. Pilch, A. Podtelejnikov, M. Kiehntopf, C. Schnabel, C. Kumar, and M. Mann Integrated analysis of the cerebrospinal fluid peptidome and proteome J. Proteome Res. 7 2008 386 399
25. H. Jahn, S. Wittke, P. Zurbig, T.J. Raedler, S. Arlt, M. Kellmann, W. Mullen, M. Eichenlaub, H. Mischak, and K. Wiedemann Peptide fingerprinting of Alzheimer's disease in cerebrospinal fluid: identification and prospective evaluation of new synaptic biomarkers PLoS One 6 2011 e26540
26. D. Wijte, L.A. McDonnell, C.I. Balog, K. Bossers, A.M. Deelder, D.F. Swaab, J. Verhaagen, and O.A. Mayboroda A novel peptidomics approach to detect markers of Alzheimer's disease in cerebrospinal fluid Methods 56 2012 500 507
27. L. Dayon, A. Hainard, V. Licker, N. Turck, K. Kuhn, D.F. Hochstrasser, P.R. Burkhard, and J.C. Sanchez Relative quantification of proteins in human cerebrospinal fluids by MS/MS using 6-plex isobaric tags Anal. Chem. 80 2008 2921 2931
28. A.J. Percy, J. Yang, A.G. Chambers, R. Simon, D.B. Hardie, and C.H. Borchers Multiplexed MRM with internal standards for cerebrospinal fluid candidate protein biomarker quantitation J. Proteome Res. 2014 (Electronic publication ahead of print)
29. 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
30. H. Braak, and E. Braak Neuropathological stageing of Alzheimer-related changes Acta Neuropathol. 82 1991 239 259
31. W.R. Markesbery, F.A. Schmitt, R.J. Kryscio, D.G. Davis, C.D. Smith, and D.R. Wekstein Neuropathologic substrate of mild cognitive impairment Arch. Neurol. 63 2006 38 46
32. M. Bigl, M.K. Bruckner, T. Arendt, V. Bigl, and K. Eschrich Activities of key glycolytic enzymes in the brains of patients with Alzheimer's disease J. Neural Transm. 106 1999 499 511
33. S. Seipp, and W. Buselmaier Isolation of glyceraldehyde 3-phosphate dehydrogenase (Gapdh) cDNA from the distal half of mouse chromosome 16: further indication of a link between Alzheimer's disease and glycolysis Neurosci. Lett. 182 1994 91 94
34. R. Fukuyama, T. Izumoto, and S. Fushiki The cerebrospinal fluid level of glial fibrillary acidic protein is increased in cerebrospinal fluid from Alzheimer's disease patients and correlates with severity of dementia Eur. Neurol. 46 2001 35 38
35. C. Hjalmarsson, M. Bjerke, B. Andersson, K. Blennow, H. Zetterberg, N.D. Aberg, B. Olsson, C. Eckerstrom, L. Bokemark, and A. Wallin Neuronal and glia-related biomarkers in cerebrospinal fluid of patients with acute ischemic stroke J. Cent. Nerv. Syst. Dis. 6 2014 51 58
36. S. Jesse, P. Steinacker, L. Cepek, C.A. von Arnim, H. Tumani, S. Lehnert, H.A. Kretzschmar, M. Baier, and M. Otto Glial fibrillary acidic protein and protein S-100B: different concentration pattern of glial proteins in cerebrospinal fluid of patients with Alzheimer's disease and Creutzfeldt-Jakob disease J. Alzheimers Dis. 17 2009 541 551
37. M. Bjerke, H. Zetterberg, A. Edman, K. Blennow, A. Wallin, and U. Andreasson Cerebrospinal fluid matrix metalloproteinases and tissue inhibitor of metalloproteinases in combination with subcortical and cortical biomarkers in vascular dementia and Alzheimer's disease J. Alzheimers Dis. 27 2011 665 676
38. A. Ohrfelt, U. Andreasson, A. Simon, H. Zetterberg, A. Edman, W. Potter, D. Holder, V. Devanarayan, J. Seeburger, A.D. Smith, K. Blennow, and A. Wallin Screening for new biomarkers for subcortical vascular dementia and Alzheimer's disease Dement. Geriatr. Cogn. Disord. Extra 1 2011 31 42
39. P. Steinacker, B. Mollenhauer, M. Bibl, L. Cepek, H. Esselmann, P. Brechlin, P. Lewczuk, S. Poser, H.A. Kretzschmar, J. Wiltfang, C. Trenkwalder, and M. Otto Heart fatty acid binding protein as a potential diagnostic marker for neurodegenerative diseases Neurosci. Lett. 370 2004 36 39
40. G.E. Craft, A. Chen, and A.C. Nairn Recent advances in quantitative neuroproteomics Methods 61 2013 186 218
41. 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
42. L.E. Donovan, L. Higginbotham, E.B. Dammer, M. Gearing, H.D. Rees, Q. Xia, D.M. Duong, N.T. Seyfried, J.J. Lah, and A.I. Levey Analysis of a membrane-enriched proteome from postmortem human brain tissue in Alzheimer's disease Proteomics Clin. Appl. 6 2012 201 211
43. J. Choi, A.I. Levey, S.T. Weintraub, H.D. Rees, M. Gearing, L.S. Chin, and L. Li Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases J. Biol. Chem. 279 2004 13256 13264
44. T. Muller, K. Jung, A. Ullrich, A. Schrotter, H.E. Meyer, C. Stephan, R. Egensperger, and K. Marcus Disease state, age, sex, and post-mortem time-dependent expression of proteins in AD vs. control frontal cortex brain samples Curr. Alzheimer Res. 5 2008 562 571
45. Y.M. Gozal, D.M. Duong, M. Gearing, D. Cheng, J.J. Hanfelt, C. Funderburk, J. Peng, J.J. Lah, and A.I. Levey Proteomics analysis reveals novel components in the detergent-insoluble subproteome in Alzheimer's disease J. Proteome Res. 8 2009 5069 5079
46. P.D. Piehowski, V.A. Petyuk, D.J. Orton, F. Xie, R.J. Moore, M. Ramirez-Restrepo, A. Engel, A.P. Lieberman, R.L. Albin, D.G. Camp, R.D. Smith, and A.J. Myers Sources of technical variability in quantitative LC-MS proteomics: human brain tissue sample analysis J. Proteome Res. 12 2013 2128 2137
47. W.J. Qian, J.M. Jacobs, T. Liu, D.G. Camp II, and R.D. Smith Advances and challenges in liquid chromatography-mass spectrometry-based proteomics profiling for clinical applications Mol. Cell. Proteomics 5 2006 1727 1744
48. A. Manavalan, M. Mishra, L. Feng, S.K. Sze, H. Akatsu, and K. Heese Brain site-specific proteome changes in aging-related dementia Exp. Mol. Med. 45 2013 e39
49. I. Begcevic, H. Kosanam, E. Martinez-Morillo, A. Dimitromanolakis, P. Diamandis, U. Kuzmanov, L.N. Hazrati, and E.P. Diamandis Semiquantitative proteomic analysis of human hippocampal tissues from Alzheimer's disease and age-matched control brains Clin. Proteomics 10 2013 5
50. E.M. Castano, C.L. Maarouf, T. Wu, M.C. Leal, C.M. Whiteside, L.F. Lue, T.A. Kokjohn, M.N. Sabbagh, T.G. Beach, and A.E. Roher Alzheimer disease periventricular white matter lesions exhibit specific proteomic profile alterations Neurochem. Int. 62 2013 145 156
51. R.Y. Chang, A.S. Nouwens, P.R. Dodd, and N. Etheridge The synaptic proteome in Alzheimer's disease Alzheimers Dement. 9 2013 499 511
52. F. Di Domenico, R. Sultana, E. Barone, M. Perluigi, C. Cini, C. Mancuso, J. Cai, W.M. Pierce, and D.A. Butterfield Quantitative proteomics analysis of phosphorylated proteins in the hippocampus of Alzheimer's disease subjects J. Proteomics 74 2011 1091 1103
53. S. Greber, G. Lubec, N. Cairns, and M. Fountoulakis Decreased levels of synaptosomal associated protein 25 in the brain of patients with Down syndrome and Alzheimer's disease Electrophoresis 20 1999 928 934
54. M.A. Korolainen, S. Auriola, T.A. Nyman, I. Alafuzoff, and T. Pirttila Proteomic analysis of glial fibrillary acidic protein in Alzheimer's disease and aging brain Neurobiol. Dis. 20 2005 858 870
55. 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
56. S. Musunuri, M. Wetterhall, M. Ingelsson, L. Lannfelt, K. Artemenko, J. Bergquist, K. Kultima, and G. Shevchenko Quantification of the brain proteome in Alzheimer's disease using multiplexed mass spectrometry J. Proteome Res. 13 2014 2056 2068
57. M. Perluigi, R. Sultana, G. Cenini, F. Di Domenico, M. Memo, W.M. Pierce, R. Coccia, and D.A. Butterfield Redox proteomics identification of 4-hydroxynonenal-modified brain proteins in Alzheimer's disease: role of lipid peroxidation in Alzheimer's disease pathogenesis Proteomics Clin. Appl. 3 2009 682 693
58. S.J. Schonberger, P.F. Edgar, R. Kydd, R.L. Faull, and G.J. Cooper Proteomic analysis of the brain in Alzheimer's disease: molecular phenotype of a complex disease process Proteomics 1 2001 1519 1528
59. 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
60. R. Sultana, D. Boyd-Kimball, H.F. Poon, J. Cai, W.M. Pierce, J.B. Klein, M. Merchant, W.R. Markesbery, and D.A. Butterfield Redox proteomics identification of oxidized proteins in Alzheimer's disease hippocampus and cerebellum: an approach to understand pathological and biochemical alterations in AD Neurobiol. Aging 27 2006 1564 1576
61. R. Sultana, H.F. Poon, J. Cai, W.M. Pierce, M. Merchant, J.B. Klein, W.R. Markesbery, and D.A. Butterfield Identification of nitrated proteins in Alzheimer's disease brain using a redox proteomics approach Neurobiol. Dis. 22 2006 76 87
62. 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
63. T. Tsuji, A. Shiozaki, R. Kohno, K. Yoshizato, and S. Shimohama Proteomic profiling and neurodegeneration in Alzheimer's disease Neurochem. Res. 27 2002 1245 1253
64. S. Zahid, M. Oellerich, A.R. Asif, and N. Ahmed Differential expression of proteins in brain regions of Alzheimer's disease patients Neurochem. Res. 39 2014 208 215
65. N.L. Anderson, and N.G. Anderson The human plasma proteome: history, character, and diagnostic prospects Mol. Cell. Proteomics 1 2002 845 867
66. U. Andreasson, E. Portelius, M.E. Andersson, K. Blennow, and H. Zetterberg Aspects of beta-amyloid as a biomarker for Alzheimer's disease Biomark. Med 1 2007 59 78
67. R. Vassar, and P.C. Kandalepas The beta-secretase enzyme BACE1 as a therapeutic target for Alzheimer's disease Alzheimers Res. Ther. 3 2011 20
68. H. Steiner, R. Fluhrer, and C. Haass Intramembrane proteolysis by gamma-secretase J. Biol. Chem. 283 2008 29627 29631
69. E. Portelius, E. Price, G. Brinkmalm, M. Stiteler, M. Olsson, R. Persson, A. Westman-Brinkmalm, H. Zetterberg, A.J. Simon, and K. Blennow A novel pathway for amyloid precursor protein processing Neurobiol. Aging 32 2011 1090 1098
70. G.G. Glenner, and C.W. Wong Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein Biochem. Biophys. Res. Commun. 120 1984 885 890
71. P. Seubert, C. Vigo-Pelfrey, F. Esch, M. Lee, H. Dovey, D. Davis, S. Sinha, M. Schlossmacher, J. Whaley, and C. Swindlehurst Isolation and quantification of soluble Alzheimer's beta-peptide from biological fluids Nature 359 1992 325 327
72. R. Motter, C. Vigo-Pelfrey, D. Kholodenko, R. Barbour, K. Johnson-Wood, D. Galasko, L. Chang, B. Miller, C. Clark, and R. Green Reduction of beta-amyloid peptide42 in the cerebrospinal fluid of patients with Alzheimer's disease Ann. Neurol. 38 1995 643 648
73. M. Tabaton, M.G. Nunzi, R. Xue, M. Usiak, L. Autilio-Gambetti, and P. Gambetti Soluble amyloid beta-protein is a marker of Alzheimer amyloid in brain but not in cerebrospinal fluid Biochem. Biophys. Res. Commun. 200 1994 1598 1603
74. W.E. Van Nostrand, S.L. Wagner, W.R. Shankle, J.S. Farrow, M. Dick, J.M. Rozemuller, M.A. Kuiper, E.C. Wolters, J. Zimmerman, and C.W. Cotman Decreased levels of soluble amyloid beta-protein precursor in cerebrospinal fluid of live Alzheimer disease patients Proc. Natl. Acad. Sci. U. S. A. 89 1992 2551 2555
75. M.S. Albert, S.T. DeKosky, D. Dickson, B. Dubois, H.H. Feldman, N.C. Fox, A. Gamst, D.M. Holtzman, W.J. Jagust, R.C. Petersen, P.J. Snyder, M.C. Carrillo, B. Thies, and C.H. Phelps The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease Alzheimers Dement. 7 2011 270 279
76. N.N. Nalivaeva, C. Beckett, N.D. Belyaev, and A.J. Turner Are amyloid-degrading enzymes viable therapeutic targets in Alzheimer's disease? J. Neurochem. 120 Suppl. 1 2012 167 185
77. E. Portelius, N. Mattsson, U. Andreasson, K. Blennow, and H. Zetterberg Novel abeta isoforms in Alzheimer's disease - their role in diagnosis and treatment Curr. Pharm. Des. 17 2011 2594 2602
78. C. Vigo-Pelfrey, D. Lee, P. Keim, I. Lieberburg, and D.B. Schenk Characterization of beta-amyloid peptide from human cerebrospinal fluid J. Neurochem. 61 1993 1965 1968
79. G. Brinkmalm, E. Portelius, A. Ohrfelt, N. Mattsson, R. Persson, M.K. Gustavsson, C.H. Vite, J. Gobom, J.E. Mansson, J. Nilsson, A. Halim, G. Larson, U. Ruetschi, H. Zetterberg, K. Blennow, and A. Brinkmalm An online nano-LC-ESI-FTICR-MS method for comprehensive characterization of endogenous fragments from amyloid beta and amyloid precursor protein in human and cat cerebrospinal fluid J. Mass Spectrom. 47 2012 591 603
80. V. Coric, C.H. van Dyck, S. Salloway, N. Andreasen, M. Brody, R.W. Richter, H. Soininen, S. Thein, T. Shiovitz, G. Pilcher, S. Colby, L. Rollin, R. Dockens, C. Pachai, E. Portelius, U. Andreasson, K. Blennow, H. Soares, C. Albright, H.H. Feldman, and R.M. Berman Safety and tolerability of the gamma-secretase inhibitor avagacestat in a phase 2 study of mild to moderate Alzheimer disease Arch. Neurol. 69 2012 1430 1440
81. E. Portelius, R.A. Dean, M.K. Gustavsson, U. Andreasson, H. Zetterberg, E. Siemers, and K. Blennow A novel Abeta isoform pattern in CSF reflects gamma-secretase inhibition in Alzheimer disease Alzheimers Res. Ther. 2 2010 7
82. M. Korecka, T. Waligorska, M. Figurski, J.B. Toledo, S.E. Arnold, M. Grossman, J.Q. Trojanowski, and L.M. Shaw Qualification of a surrogate matrix-based absolute quantification method for amyloid-beta(4)(2) in human cerebrospinal fluid using 2D UPLC-tandem mass spectrometry J. Alzheimers Dis. 41 2014 441 451
83. M.E. Lame, E.E. Chambers, and M. Blatnik Quantitation of amyloid beta peptides Abeta(1-38), Abeta(1-40), and Abeta(1-42) in human cerebrospinal fluid by ultra-performance liquid chromatography-tandem mass spectrometry Anal. Biochem. 419 2011 133 139
84. J. Pannee, E. Portelius, M. Oppermann, A. Atkins, M. Hornshaw, I. Zegers, P. Hojrup, L. Minthon, O. Hansson, H. Zetterberg, K. Blennow, and J. Gobom A selected reaction monitoring (SRM)-based method for absolute quantification of Abeta38, Abeta40, and Abeta42 in cerebrospinal fluid of Alzheimer's disease patients and healthy controls J. Alzheimers Dis. 33 2013 1021 1032
85. A. Leinenbach, J. Pannee, T. Dulffer, A. Huber, T. Bittner, U. Andreasson, J. Gobom, H. Zetterberg, U. Kobold, E. Portelius, and K. Blennow Mass spectrometry-based candidate reference measurement procedure for quantification of amyloid-beta in cerebrospinal fluid Clin. Chem. 60 7 2014 987 994
86. G. Brinkmalm, A. Brinkmalm, P. Bourgeois, R. Persson, O. Hansson, E. Portelius, M. Mercken, U. Andreasson, S. Parent, F. Lipari, A. Ohrfelt, M. Bjerke, L. Minthon, H. Zetterberg, K. Blennow, and M. Nutu Soluble amyloid precursor protein alpha and beta in CSF in Alzheimer's disease Brain Res. 1513 2013 117 126
87. S. Schedin-Weiss, B. Winblad, and L.O. Tjernberg The role of protein glycosylation in Alzheimer disease FEBS J. 281 2014 46 62
88. A. Halim, G. Brinkmalm, U. Ruetschi, A. Westman-Brinkmalm, E. Portelius, H. Zetterberg, K. Blennow, G. Larson, and J. Nilsson Site-specific characterization of threonine, serine, and tyrosine glycosylations of amyloid precursor protein/amyloid beta-peptides in human cerebrospinal fluid Proc. Natl. Acad. Sci. U. S. A. 108 2011 11848 11853
89. I. Perdivara, R. Petrovich, B. Allinquant, L.J. Deterding, K.B. Tomer, and M. Przybylski Elucidation of O-glycosylation structures of the beta-amyloid precursor protein by liquid chromatography-mass spectrometry using electron transfer dissociation and collision induced dissociation J. Proteome Res. 8 2009 631 642
90. E. Portelius, G. Brinkmalm, A. Tran, U. Andreasson, H. Zetterberg, A. Westman-Brinkmalm, K. Blennow, and A. Ohrfelt Identification of novel N-terminal fragments of amyloid precursor protein in cerebrospinal fluid Exp. Neurol. 223 2010 351 358
91. J. Chen, M. Wang, and I.V. Turko Quantification of amyloid precursor protein isoforms using quantification concatamer internal standard Anal. Chem. 85 2013 303 307
92. G. Utermann, M. Hees, and A. Steinmetz Polymorphism of apolipoprotein E and occurrence of dysbetalipoproteinaemia in man Nature 269 1977 604 607
93. S.C. Rall Jr., K.H. Weisgraber, and R.W. Mahley Human apolipoprotein E. The complete amino acid sequence J. Biol. Chem. 257 1982 4171 4178
94. K.H. Weisgraber, S.C. Rall Jr., and R.W. Mahley Human E apoprotein heterogeneity. Cysteine-arginine interchanges in the amino acid sequence of the apo-E isoforms J. Biol. Chem. 256 1981 9077 9083
95. C.C. Liu, T. Kanekiyo, H. Xu, and G. Bu Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy Nat. Rev. Neurol. 9 2013 106 118
96. C. Cruchaga, J.S. Kauwe, P. Nowotny, K. Bales, E.H. Pickering, K. Mayo, S. Bertelsen, A. Hinrichs, A.M. Fagan, D.M. Holtzman, J.C. Morris, and A.M. Goate Cerebrospinal fluid APOE levels: an endophenotype for genetic studies for Alzheimer's disease Hum. Mol. Genet. 21 2012 4558 4571
97. E. Martinez-Morillo, O. Hansson, Y. Atagi, G. Bu, L. Minthon, E.P. Diamandis, and H.M. Nielsen Total apolipoprotein E levels and specific isoform composition in cerebrospinal fluid and plasma from Alzheimer's disease patients and controls Acta Neuropathol. 127 2014 633 643
98. E. Vanmechelen, H. Vanderstichele, P. Davidsson, E. Van Kerschaver, B. Van Der Perre, M. Sjogren, N. Andreasen, and K. Blennow Quantification of tau phosphorylated at threonine 181 in human cerebrospinal fluid: a sandwich ELISA with a synthetic phosphopeptide for standardization Neurosci. Lett. 285 2000 49 52
99. E. Portelius, S.F. Hansson, A.J. Tran, H. Zetterberg, P. Grognet, E. Vanmechelen, K. Hoglund, G. Brinkmalm, A. Westman-Brinkmalm, E. Nordhoff, K. Blennow, and J. Gobom Characterization of tau in cerebrospinal fluid using mass spectrometry J. Proteome Res. 7 2008 2114 2120
100. T. McAvoy, M.E. Lassman, D.S. Spellman, Z. Ke, B.J. Howell, O. Wong, L. Zhu, M. Tanen, A. Struyk, and O.F. Laterza Quantification of tau in cerebrospinal fluid by immunoaffinity enrichment and tandem mass spectrometry Clin. Chem. 60 2014 683 689
101. A. Brinkmalm, G. Brinkmalm, W.G. Honer, J.A. Moreno, J. Jakobsson, G.R. Mallucci, H. Zetterberg, K. Blennow, and A. Ohrfelt Targeting synaptic pathology with a novel affinity mass spectrometry approach Mol. Cell. Proteomics 13 2014 2584 2592
102. A. Brinkmalm, G. Brinkmalm, W.G. Honer, L. Frolich, L. Hausner, L. Minthon, O. Hansson, A. Wallin, H. Zetterberg, K. Blennow, and A. Ohrfelt SNAP-25 is a promising novel cerebrospinal fluid biomarker for synapse degeneration in Alzheimer's disease Mol. Neurodegener. 9 2014 53
103. H. Kvartsberg, F.H. Duits, M. Ingelsson, N. Andreasen, A. Öhrfelt, K. Andersson, G. Brinkmalm, L. Lannfelt, L. Minthon, O. Hansson, U. Andreasson, C.E. Teunissen, P. Scheltens, W.M. Van der Flier, H. Zetterberg, E. Portelius, and K. Blennow Cerebrospinal Fluid Levels of the Synaptic Protein Neurogranin Predict Cognitive Decline in Prodromal Alzheimer's Disease, Alzheimers Dement 2014
104. R.Y. Chang, N. Etheridge, P. Dodd, and A. Nouwens Quantitative multiple reaction monitoring analysis of synaptic proteins from human brain J. Neurosci. Methods 227 2014 189 210
105. R.Y. Chang, N. Etheridge, P.R. Dodd, and A.S. Nouwens Targeted quantitative analysis of synaptic proteins in Alzheimer's disease brain Neurochem. Int. 75 2014 66 75
106. Y.V. Skorobogatko, J. Deuso, J. Adolf-Bryfogle, M.G. Nowak, Y. Gong, C.F. Lippa, and K. Vosseller Human Alzheimer's disease synaptic O-GlcNAc site mapping and iTRAQ expression proteomics with ion trap mass spectrometry Amino Acids 40 2011 765 779
107. R. Guerreiro, A. Wojtas, J. Bras, M. Carrasquillo, E. Rogaeva, E. Majounie, C. Cruchaga, C. Sassi, J.S. Kauwe, S. Younkin, L. Hazrati, J. Collinge, J. Pocock, T. Lashley, J. Williams, J.C. Lambert, P. Amouyel, A. Goate, R. Rademakers, K. Morgan, J. Powell, P. St George-Hyslop, A. Singleton, and J. Hardy TREM2 variants in Alzheimer's disease N. Engl. J. Med. 368 2013 117 127
108. T. Jonsson, H. Stefansson, S. Steinberg, I. Jonsdottir, P.V. Jonsson, J. Snaedal, S. Bjornsson, J. Huttenlocher, A.I. Levey, J.J. Lah, D. Rujescu, H. Hampel, I. Giegling, O.A. Andreassen, K. Engedal, I. Ulstein, S. Djurovic, C. Ibrahim-Verbaas, A. Hofman, M.A. Ikram, C.M. van Duijn, U. Thorsteinsdottir, A. Kong, and K. Stefansson Variant of TREM2 associated with the risk of Alzheimer's disease N. Engl. J. Med. 368 2013 107 116
109. N. Mattsson, S. Tabatabaei, P. Johansson, O. Hansson, U. Andreasson, J.E. Mansson, J.O. Johansson, B. Olsson, A. Wallin, J. Svensson, K. Blennow, and H. Zetterberg Cerebrospinal fluid microglial markers in Alzheimer's disease: elevated chitotriosidase activity but lack of diagnostic utility Neruomol. Med. 13 2011 151 159
110. B. Olsson, J. Hertze, R. Lautner, H. Zetterberg, K. Nagga, K. Hoglund, H. Basun, P. Annas, L. Lannfelt, N. Andreasen, L. Minthon, K. Blennow, and O. Hansson Microglial markers are elevated in the prodromal phase of Alzheimer's disease and vascular dementia J. Alzheimers Dis. 33 2013 45 53
111. A.M. Varghese, A. Sharma, P. Mishra, K. Vijayalakshmi, H.C. Harsha, T.N. Sathyaprabha, S.M. Bharath, A. Nalini, P.A. Alladi, and T.R. Raju Chitotriosidase - a putative biomarker for sporadic amyotrophic lateral sclerosis Clin. Proteomics 10 2013 19
112. J. Chen, R.Y. Huang, and I.V. Turko Mass spectrometry assessment of ubiquitin carboxyl-terminal hydrolase L1 partitioning between soluble and particulate brain homogenate fractions Anal. Chem. 85 2013 6011 6017
113. S. Mondello, R. Constantinescu, H. Zetterberg, U. Andreasson, B. Holmberg, and A. Jeromin CSF alpha-synuclein and UCH-L1 levels in Parkinson's disease and atypical parkinsonian disorders Parkinsonism Relat. Disord. 20 2014 382 387
114. J. Chen, M. Wang, and I.V. Turko Mass spectrometry quantification of clusterin in the human brain Mol. Neurodegener. 7 2012 41
115. K. Zhang, M. Schrag, A. Crofton, R. Trivedi, H. Vinters, and W. Kirsch Targeted proteomics for quantification of histone acetylation in Alzheimer's disease Proteomics 12 2012 1261 1268
116. Y.S. Choi, S. Hou, L.H. Choe, and K.H. Lee Targeted human cerebrospinal fluid proteomics for the validation of multiple Alzheimer's disease biomarker candidates J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 930 2013 129 135
117. A.N. Fonteh, R.J. Harrington, A. Tsai, P. Liao, and M.G. Harrington Free amino acid and dipeptide changes in the body fluids from Alzheimer's disease subjects Amino Acids 32 2007 213 224
118. B. Krastins, A. Prakash, D.A. Sarracino, D. Nedelkov, E.E. Niederkofler, U.A. Kiernan, R. Nelson, M.S. Vogelsang, G. Vadali, A. Garces, J.N. Sutton, S. Peterman, G. Byram, B. Darbouret, J.R. Perusse, N.G. Seidah, B. Coulombe, J. Gobom, E. Portelius, J. Pannee, K. Blennow, V. Kulasingam, L. Couchman, C. Moniz, and M.F. Lopez Rapid development of sensitive, high-throughput, quantitative and highly selective mass spectrometric targeted immunoassays for clinically important proteins in human plasma and serum Clin. Biochem. 46 2013 399 410
119. 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
120. J. Eriksson, and D. Fenyo Improving the success rate of proteome analysis by modeling protein-abundance distributions and experimental designs Nat. Biotechnol. 25 2007 651 655
121. G.C. McAlister, E.L. Huttlin, W. Haas, L. Ting, M.P. Jedrychowski, J.C. Rogers, K. Kuhn, I. Pike, R.A. Grothe, J.D. Blethrow, and S.P. Gygi Increasing the multiplexing capacity of TMTs using reporter ion isotopologues with isobaric masses Anal. Chem. 84 2012 7469 7478
122. P. Lescuyer, D. Hochstrasser, and T. Rabilloud How shall we use the proteomics toolbox for biomarker discovery? J. Proteome Res. 6 2007 3371 3376
123. B. Hernandez, A. Parnell, and S.R. Pennington Why have so few proteomic biomarkers "survived" validation? (Sample size and independent validation considerations) Proteomics 14 2014 1587 1592
124. R. Nuzzo Scientific method: statistical errors Nature 506 2014 150 152
125. N.L. Anderson The roles of multiple proteomic platforms in a pipeline for new diagnostics Mol. Cell. Proteomics 4 2005 1441 1444
126. N. Rifai, M.A. Gillette, and S.A. Carr Protein biomarker discovery and validation: the long and uncertain path to clinical utility Nat. Biotechnol. 24 2006 971 983
127. P.M. Bossuyt, J.B. Reitsma, D.E. Bruns, C.A. Gatsonis, P.P. Glasziou, L.M. Irwig, J.G. Lijmer, D. Moher, D. Rennie, and H.C. de Vet Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative. Standards for reporting of diagnostic accuracy Clin. Chem. 49 2003 1 6
128. A.H. Noel-Storr, J.M. McCleery, E. Richard, C.W. Ritchie, L. Flicker, S.J. Cullum, D. Davis, T.J. Quinn, C. Hyde, A.W. Rutjes, N. Smailagic, S. Marcus, S. Black, K. Blennow, C. Brayne, M. Fiorivanti, J.K. Johnson, S. Kopke, L.S. Schneider, A. Simmons, N. Mattsson, H. Zetterberg, P.M. Bossuyt, G. Wilcock, and R. McShane Reporting standards for studies of diagnostic test accuracy in dementia: the STARDdem initiative Neurology 83 2014 364 373
129. E.M. Castano, A.E. Roher, C.L. Esh, T.A. Kokjohn, and T. Beach Comparative proteomics of cerebrospinal fluid in neuropathologically-confirmed Alzheimer's disease and non-demented elderly subjects Neurol. Res. 28 2006 155 163
130. P. Davidsson, A. Westman-Brinkmalm, C.L. Nilsson, M. Lindbjer, L. Paulson, N. Andreasen, M. Sjogren, and K. Blennow Proteome analysis of cerebrospinal fluid proteins in Alzheimer patients Neuroreport 13 2002 611 615
131. M. Puchades, S.F. Hansson, C.L. Nilsson, N. Andreasen, K. Blennow, and P. Davidsson Proteomic studies of potential cerebrospinal fluid protein markers for Alzheimer's disease Brain Res. Mol. Brain Res. 118 2003 140 146
132. M.A. Korolainen, T.A. Nyman, P. Nyyssonen, E.S. Hartikainen, and T. Pirttila Multiplexed proteomic analysis of oxidation and concentrations of cerebrospinal fluid proteins in Alzheimer disease Clin. Chem. 53 2007 657 665
133. M.S. Cheon, M. Fountoulakis, N.J. Cairns, M. Dierssen, K. Herkner, and G. Lubec Decreased protein levels of stathmin in adult brains with Down syndrome and Alzheimer's disease J. Neural Transm. Suppl. 2001 281 288
134. 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
135. R. Sultana, D. Boyd-Kimball, H.F. Poon, J. Cai, W.M. Pierce, J.B. Klein, W.R. Markesbery, X.Z. Zhou, K.P. Lu, and D.A. Butterfield Oxidative modification and down-regulation of Pin1 in Alzheimer's disease hippocampus: a redox proteomics analysis Neurobiol. Aging 27 2006 918 925
136. R. Pamplona, E. Dalfo, V. Ayala, M.J. Bellmunt, J. Prat, I. Ferrer, and M. Portero-Otin Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation. Effects of Alzheimer disease and identification of lipoxidation targets J. Biol. Chem. 280 2005 21522 21530
137. A. Papassotiropoulos, M. Fountoulakis, T. Dunckley, D.A. Stephan, and E.M. Reiman Genetics, transcriptomics, and proteomics of Alzheimer's disease J. Clin. Psychiatry 67 2006 652 670
138. L. Emilsson, P. Saetre, and E. Jazin Alzheimer's disease: mRNA expression profiles of multiple patients show alterations of genes involved with calcium signaling Neurobiol. Dis. 21 2006 618 625
139. N.A. Twine, K. Janitz, M.R. Wilkins, and M. Janitz Whole transcriptome sequencing reveals gene expression and splicing differences in brain regions affected by Alzheimer's disease PLoS One 6 2011 e16266
140. J. Zhang, D.R. Goodlett, J.F. Quinn, E. Peskind, J.A. Kaye, Y. Zhou, C. Pan, E. Yi, J. Eng, Q. Wang, R.H. Aebersold, and T.J. Montine Quantitative proteomics of cerebrospinal fluid from patients with Alzheimer disease J. Alzheimers Dis. 7 2005 125 133 (discussion 173-180)
141. S. Baig, S.A. Joseph, H. Tayler, R. Abraham, M.J. Owen, J. Williams, P.G. Kehoe, and S. Love Distribution and expression of picalm in Alzheimer disease J. Neuropathol. Exp. Neurol. 69 2010 1071 1077
142. S. Vogelgesang, R.W. Warzok, I. Cascorbi, C. Kunert-Keil, E. Schroeder, H.K. Kroemer, W. Siegmund, L.C. Walker, and J. Pahnke The role of P-glycoprotein in cerebral amyloid angiopathy; implications for the early pathogenesis of Alzheimer's disease Curr. Alzheimer Res. 1 2004 121 125
143. S. Vogelgesang, I. Cascorbi, E. Schroeder, J. Pahnke, H.K. Kroemer, W. Siegmund, C. Kunert-Keil, L.C. Walker, and R.W. Warzok Deposition of Alzheimer's beta-amyloid is inversely correlated with P-glycoprotein expression in the brains of elderly non-demented humans Pharmacogenetics 12 2002 535 541