The future of blood-based biomarkers for Alzheimer's disease
Corresponding Author
Kim Henriksen
- [email protected]
- +45 44525219 | Fax: +45 44525251
Nordic Bioscience Biomarkers and Research, Neurodegenerative Diseases, Herlev, Denmark
Corresponding author. Tel.: +45 44525219; Fax: +45 44525251. [email protected]Search for more papers by this authorSid E. O'Bryant
Department of Internal Medicine, University of North Texas Health Science Center, Fort Worth, Texas, USA
Search for more papers by this authorHarald Hampel
Department of Psychiatry, University of Frankfurt, Frankfurt, Germany
Search for more papers by this authorJohn Q. Trojanowski
Institute on Aging, Alzheimer's Disease Core Center, Udall Parkinson's Research Center, Center for Neurodegenerative Disease Research, Department of Pathology and Laboratory Medicine, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, USA
Search for more papers by this authorThomas J. Montine
Department of Pathology, University of Washington, Seattle, WA, USA
Search for more papers by this authorKaj Blennow
Clinical Neurochemistry Laboratory, Department of Neuroscience and Physiology, University of Goteborg, Sahlgrenska University Hospital, Molndal, Sweden
Search for more papers by this authorTony Wyss-Coray
Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, CA, USA
Search for more papers by this authorChantal Bazenet
King's College London, Department of Old Age Psychiatry, Institute of Psychiatry, De Crespigny Park, London, UK
Search for more papers by this authorWilliam Hu
Department of Neurology, Center for Neurodegenerative Disease Research, Emory University School of Medicine, Atlanta, GA, USA
Search for more papers by this authorSimon Lovestone
King's College London, Department of Old Age Psychiatry, Institute of Psychiatry, De Crespigny Park, London, UK
Search for more papers by this authorMorten A. Karsdal
Nordic Bioscience Biomarkers and Research, Neurodegenerative Diseases, Herlev, Denmark
Search for more papers by this authorMichael W. Weiner
Departments of Medicine, Radiology, Psychiatry, and Neurology, University of California, San Francisco, CA, USA
Search for more papers by this authorBlood-Based Biomarker Interest Group
Departments of Medicine, Radiology, Psychiatry, and Neurology, University of California, San Francisco, CA, USA
Additional Blood-Based Biomarker Interest Group members include Howard M. Fillit, Alzheimer's Drug Discovery Foundation, New York, NY, USA; Maria C. Carrillo, Medical & Scientific Relations, Alzheimer's Association, Chicago, IL, USA; Lisa J. Bain, Elverson, PA, USA; David Wholley and Judy Siuciak, The Biomarkers Consortium, Foundation for the National Institutes of Health, USA; David Holtzman, Department of Neurology, Washington University School of Medicine, St. Louis, MO, USA; Gary Kong, Edith Cowan University, Australia; Ralph Martins, Centre of Excellence for Alzheimer's Disease Research and Care, Edith Cowan University, Joondalup, WA, Australia; Jeffrey Roche, Centers for Medicare & Medicaid Services, USA; Andrew Saykin, Indiana University, Center for Neuroimaging, IN, USA; Robert Nagele, University of Medicine and Dentistry of New Jersey School of Osteopathic Medicine, NJ, USA; Les Shaw, Institute on Aging, Alzheimer's Disease Core Center, Udall Parkinson's Research Center, Center for Neurodegenerative Disease Research, Department of Pathology and Laboratory Medicine, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA; Dwight German, Department of Psychiatry, University of Texas Southwestern Medical Center, Dallas, TX, USA; Diane Stephenson, Critical Path Institute, USA; Andrew Watt, Alzheimer's Australia Dementia Research Foundation, Australia; Tatiana Foroud, Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, IN, USA; Holly Soares, Bristol-Myers Squibb, Wallingford, CT, USA; Christoph Laske, Section for Dementia Research, Hertie-Institute of Clinical Brain Research, Department of Psychiatry and Psychotherapy and German Center for Neurodegenerative Diseases (DZNE), University of Tübingen, D-Tübingen, Germany; Monique Breteler, Department of Epidemiology and Biostatistics, Erasmus Medical Center, Rotterdam, Netherlands; Louis Kirby, ZettaScience, USA; Howard Schulman, Caprion Proteomics, USA; Kevin Barnham, Department of Pathology, University of Melbourne, Melbourne, Australia; Pedro Pesini, Araclon Biotech S.L., Spain; Tony Phelps, National Institutes of Aging, USA; Steve Younkin, Mayo Clinic, Jacksonville, FL, USA; Thomas Kodadek, Departments of Chemistry & Cancer Biology, The Scripps Research Institute, Scripps Florida, Jupiter, FL, USA; Joyce Suhy, Synarc Imaging, San Fransisco, CA, USA; Dan Perry, Alliance for Aging Research, Washington, DC, USA; Rachel L. Nosheny, La Jolla, CA, and Stanford, CA, USA; Melissa Edwards, Department of Psychology, Texas Tech University, Lubbock, TX, USA; Hugo Vanderstiechele, ADxNeurosciences, Gent, Belgium.
Search for more papers by this authorCorresponding Author
Kim Henriksen
- [email protected]
- +45 44525219 | Fax: +45 44525251
Nordic Bioscience Biomarkers and Research, Neurodegenerative Diseases, Herlev, Denmark
Corresponding author. Tel.: +45 44525219; Fax: +45 44525251. [email protected]Search for more papers by this authorSid E. O'Bryant
Department of Internal Medicine, University of North Texas Health Science Center, Fort Worth, Texas, USA
Search for more papers by this authorHarald Hampel
Department of Psychiatry, University of Frankfurt, Frankfurt, Germany
Search for more papers by this authorJohn Q. Trojanowski
Institute on Aging, Alzheimer's Disease Core Center, Udall Parkinson's Research Center, Center for Neurodegenerative Disease Research, Department of Pathology and Laboratory Medicine, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, USA
Search for more papers by this authorThomas J. Montine
Department of Pathology, University of Washington, Seattle, WA, USA
Search for more papers by this authorKaj Blennow
Clinical Neurochemistry Laboratory, Department of Neuroscience and Physiology, University of Goteborg, Sahlgrenska University Hospital, Molndal, Sweden
Search for more papers by this authorTony Wyss-Coray
Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, CA, USA
Search for more papers by this authorChantal Bazenet
King's College London, Department of Old Age Psychiatry, Institute of Psychiatry, De Crespigny Park, London, UK
Search for more papers by this authorWilliam Hu
Department of Neurology, Center for Neurodegenerative Disease Research, Emory University School of Medicine, Atlanta, GA, USA
Search for more papers by this authorSimon Lovestone
King's College London, Department of Old Age Psychiatry, Institute of Psychiatry, De Crespigny Park, London, UK
Search for more papers by this authorMorten A. Karsdal
Nordic Bioscience Biomarkers and Research, Neurodegenerative Diseases, Herlev, Denmark
Search for more papers by this authorMichael W. Weiner
Departments of Medicine, Radiology, Psychiatry, and Neurology, University of California, San Francisco, CA, USA
Search for more papers by this authorBlood-Based Biomarker Interest Group
Departments of Medicine, Radiology, Psychiatry, and Neurology, University of California, San Francisco, CA, USA
Additional Blood-Based Biomarker Interest Group members include Howard M. Fillit, Alzheimer's Drug Discovery Foundation, New York, NY, USA; Maria C. Carrillo, Medical & Scientific Relations, Alzheimer's Association, Chicago, IL, USA; Lisa J. Bain, Elverson, PA, USA; David Wholley and Judy Siuciak, The Biomarkers Consortium, Foundation for the National Institutes of Health, USA; David Holtzman, Department of Neurology, Washington University School of Medicine, St. Louis, MO, USA; Gary Kong, Edith Cowan University, Australia; Ralph Martins, Centre of Excellence for Alzheimer's Disease Research and Care, Edith Cowan University, Joondalup, WA, Australia; Jeffrey Roche, Centers for Medicare & Medicaid Services, USA; Andrew Saykin, Indiana University, Center for Neuroimaging, IN, USA; Robert Nagele, University of Medicine and Dentistry of New Jersey School of Osteopathic Medicine, NJ, USA; Les Shaw, Institute on Aging, Alzheimer's Disease Core Center, Udall Parkinson's Research Center, Center for Neurodegenerative Disease Research, Department of Pathology and Laboratory Medicine, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA; Dwight German, Department of Psychiatry, University of Texas Southwestern Medical Center, Dallas, TX, USA; Diane Stephenson, Critical Path Institute, USA; Andrew Watt, Alzheimer's Australia Dementia Research Foundation, Australia; Tatiana Foroud, Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, IN, USA; Holly Soares, Bristol-Myers Squibb, Wallingford, CT, USA; Christoph Laske, Section for Dementia Research, Hertie-Institute of Clinical Brain Research, Department of Psychiatry and Psychotherapy and German Center for Neurodegenerative Diseases (DZNE), University of Tübingen, D-Tübingen, Germany; Monique Breteler, Department of Epidemiology and Biostatistics, Erasmus Medical Center, Rotterdam, Netherlands; Louis Kirby, ZettaScience, USA; Howard Schulman, Caprion Proteomics, USA; Kevin Barnham, Department of Pathology, University of Melbourne, Melbourne, Australia; Pedro Pesini, Araclon Biotech S.L., Spain; Tony Phelps, National Institutes of Aging, USA; Steve Younkin, Mayo Clinic, Jacksonville, FL, USA; Thomas Kodadek, Departments of Chemistry & Cancer Biology, The Scripps Research Institute, Scripps Florida, Jupiter, FL, USA; Joyce Suhy, Synarc Imaging, San Fransisco, CA, USA; Dan Perry, Alliance for Aging Research, Washington, DC, USA; Rachel L. Nosheny, La Jolla, CA, and Stanford, CA, USA; Melissa Edwards, Department of Psychology, Texas Tech University, Lubbock, TX, USA; Hugo Vanderstiechele, ADxNeurosciences, Gent, Belgium.
Search for more papers by this authorAbstract
Treatment of Alzheimer's disease (AD) is significantly hampered by the lack of easily accessible biomarkers that can detect disease presence and predict disease risk reliably. Fluid biomarkers of AD currently provide indications of disease stage; however, they are not robust predictors of disease progression or treatment response, and most are measured in cerebrospinal fluid, which limits their applicability. With these aspects in mind, the aim of this article is to underscore the concerted efforts of the Blood-Based Biomarker Interest Group, an international working group of experts in the field. The points addressed include: (1) the major challenges in the development of blood-based biomarkers of AD, including patient heterogeneity, inclusion of the “right” control population, and the blood–brain barrier; (2) the need for a clear definition of the purpose of the individual markers (e.g., prognostic, diagnostic, or monitoring therapeutic efficacy); (3) a critical evaluation of the ongoing biomarker approaches; and (4) highlighting the need for standardization of preanalytical variables and analytical methodologies used by the field.
References
- [1]N. Herrmann, S.A. Chau, I. Kircanski, K.L. Lanctot. Current and emerging drug treatment options for Alzheimer's disease: a systematic review. Drugs. 71: 2011; 2031–2065
- [2]M. Thambisetty, S. Lovestone. Blood-based biomarkers of Alzheimer's disease: challenging but feasible. Biomark Med. 4: 2010; 65–79
- [3]K. Blennow. Biomarkers in Alzheimer's disease drug development. Nat Med. 16: 2010; 1218–1222
- [4]J.L. Cummings. Biomarkers in Alzheimer's disease drug development. Alzheimers Dement. 7: 2011; e13–e44
- [5]H. Hampel, R. Frank, K. Broich, S.J. Teipel, R.G. Katz, J. Hardy, et al. Biomarkers for Alzheimer's disease: academic, industry and regulatory perspectives. Nat Rev Drug Discov. 9: 2010; 560–574
- [6]R. Mayeux, N. Schupf. Blood-based biomarkers for Alzheimer's disease: plasma Abeta40 and Abeta42, and genetic variants. Neurobiol Aging. 32: 2011; S10–S19
- [7]S. Patel, R.J. Shah, P. Coleman, M. Sabbagh. Potential peripheral biomarkers for the diagnosis of Alzheimer's disease. Int J Alzheimers Dis. 2011: 2011; 572495
10.4061/2011/572495 Google Scholar
- [8]H. Zetterberg. Biomarkers reflecting different facets of Alzheimer's disease. Eur J Neurol. 15: 2008; 1143–1144
- [9]Y. Wang, M.G. Sorensen, Q. Zheng, C. Zhang, M.A. Karsdal, K. Henriksen. Will post-translational modifications of brain proteins provide novel serological markers for dementias? Int J Alzheimers Dis. 2012: 2012; 209409
10.1155/2012/209409 Google Scholar
- [10]C.R. Jack Jr., D.S. Knopman, W.J. Jagust, L.M. Shaw, P.S. Aisen, M.W. Weiner, et al. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol. 9: 2010; 119–128
- [11]J.H. Tanne. US scientists discuss early detection and treatment of Alzheimer's disease. BMJ. 344: 2012; e1068
- [12]K. Blennow, H. Hampel, M. Weiner, H. Zetterberg. Cerebrospinal fluid and plasma biomarkers in Alzheimer disease. Nat Rev Neurol. 6: 2010; 131–144
- [13]H. Hampel, K. Burger, S.J. Teipel, A.L. Bokde, H. Zetterberg, K. Blennow. Core candidate neurochemical and imaging biomarkers of Alzheimer's disease. Alzheimers Dement. 4: 2007; 38–48
- [14]N. Mattsson, K. Blennow, H. Zetterberg. CSF biomarkers: pinpointing Alzheimer pathogenesis. Ann NY Acad Sci. 1180: 2009; 28–35
- [15]S.M. de Almeida, S.D. Shumaker, S.K. LeBlanc, P. Delaney, J. Marquie-Beck, S. Ueland, et al. Incidence of post-dural puncture headache in research volunteers. Headache. 51: 2011; 1503–1510
- [16]P. Schneider, H. Hampel, K. Buerger. Biological marker candidates of Alzheimer's disease in blood, plasma, and serum. CNS Neurosci Ther. 15: 2009; 358–374
- [17]J. Li, D.A. Llano, T. Ellis, D. LeBlond, A. Bhathena, S.S. Jhee, et al. Effect of human cerebrospinal fluid sampling frequency on amyloid-beta levels. Alzheimers Dement. 8: 2012; 295–303
- [18]J.C. Morris, C.M. Roe, E.A. Grant, D. Head, M. Storandt, A.M. Goate, et al. Pittsburgh compound B imaging and prediction of progression from cognitive normality to symptomatic Alzheimer disease. Arch Neurol. 66: 2009; 1469–1475
- [19]A. Forsberg, H. Engler, O. Almkvist, G. Blomquist, G. Hagman, A. Wall, et al. PET imaging of amyloid deposition in patients with mild cognitive impairment. Neurobiol Aging. 29: 2008; 1456–1465
- [20]W.E. Klunk, C.A. Mathis. The future of amyloid-beta imaging: a tale of radionuclides and tracer proliferation. Curr Opin Neurol. 21: 2008; 683–687
- [21]C.M. Clark, M.J. Pontecorvo, T.G. Beach, B.J. Bedell, R.E. Coleman, P.M. Doraiswamy, et al. Cerebral PET with florbetapir compared with neuropathology at autopsy for detection of neuritic amyloid-beta plaques: a prospective cohort study. Lancet Neurol. 11: 2012; 669–678
- [22]H. Hampel, S. Lista, Z.S. Khachaturian. Development of biomarkers to chart all Alzheimer's disease stages: the royal road to cutting the therapeutic Gordian Knot. Alzheimers Dement. 8: 2012; 312–336
- [23]C.B. Jeter, G.W. Hergenroeder, M.J. Hylin, J.B. Redell, A.N. Moore, P.K. Dash. Biomarkers for the diagnosis and prognosis of mild traumatic brain injury/concussion. J Neurotrauma. 30 (8): 2013; 657–670
- [24]L. Papa, M.M. Ramia, J.M. Kelly, S.S. Burks, A. Pawlowicz, R.P. Berger. Systematic Review of Clinical Research on Biomarkers for Pediatric Traumatic Brain Injury. J. Neurotrauma. 30 (5): 2013; 324–338
- [25]U. Ziemann, M. Wahl, E. Hattingen, H. Tumani. Development of biomarkers for multiple sclerosis as a neurodegenerative disorder. Prog Neurobiol. 95: 2011; 670–685
- [26]K.A. Josephs, R.C. Petersen, D.S. Knopman, B.F. Boeve, J.L. Whitwell, J.R. Duffy, et al. Clinicopathologic analysis of frontotemporal and corticobasal degenerations and PSP. Neurology. 66: 2006; 41–48
- [27]L. Yang, D. Rieves, C. Ganley. Brain amyloid imaging–FDA approval of florbetapir F18 injection. N Engl J Med. 367: 2012; 885–887
- [28] World Alzheimer report 2009. 2010; Published by Alzheimer's Disease International, Edited by: Martin Prince & Jim Jackson
- [29]W.T. Hu, D.M. Holtzman, A.M. Fagan, L.M. Shaw, R. Perrin, S.E. Arnold, et al. Plasma multianalyte profiling in mild cognitive impairment and Alzheimer disease. Neurology. 79: 2012; 897–905
- [30]H.D. Soares, W.Z. Potter, E. Pickering, M. Kuhn, F.W. Immermann, D.M. Shera, et al. Plasma Biomarkers Associated With the Apolipoprotein E Genotype and Alzheimer Disease. Arch Neurol. 69 (10): 2012; 1310–1317
- [31]A. Koyama, J. O'Brien, J. Weuve, D. Blacker, A.L. Metti, K. Yaffe. The Role of Peripheral Inflammatory Markers in Dementia and Alzheimer's Disease: A Meta-Analysis. J Gerontol A Biol Sci Med Sci. 68 (4): 2013; 433–440
- [32]K. Blennow, M.J. de Leon, H. Zetterberg. Alzheimer's disease. Lancet. 368: 2006; 387–403
- [33]D.E. Barnes, K. Yaffe. The projected effect of risk factor reduction on Alzheimer's disease prevalence. Lancet Neurol. 10: 2011; 819–828
- [34]G.M. McKhann, M.S. Albert, M. Grossman, B. Miller, D. Dickson, J.Q. Trojanowski. Clinical and pathological diagnosis of frontotemporal dementia: report of the Work Group on Frontotemporal Dementia and Pick's Disease. Arch Neurol. 58: 2001; 1803–1809
- [35]G.D. Rosa, G. Salzano, M. Caraglia, A. Abbruzzese. Nanotechnologies: a strategy to overcome blood-brain barrier. Curr Drug Metab. 13 (1): 2012; 61–69
- [36]S. Chalbot, H. Zetterberg, K. Blennow, T. Fladby, N. Andreasen, I. Grundke-Iqbal, et al. Blood-cerebrospinal fluid barrier permeability in Alzheimer's disease. J Alzheimers Dis. 25: 2011; 505–515
- [37]Z. Cai, B. Zhao, A. Ratka. Oxidative stress and beta-amyloid protein in Alzheimer's disease. Neuromolecular Med. 13: 2011; 223–250
- [38]B.D. Zipser, C.E. Johanson, L. Gonzalez, T.M. Berzin, R. Tavares, C.M. Hulette, et al. Microvascular injury and blood-brain barrier leakage in Alzheimer's disease. Neurobiol Aging. 28: 2007; 977–986
- [39]A. Marcello, O. Wirths, T. Schneider-Axmann, M. German-Gunnarsson, L. Lannfelt, T.A. Bayer. Circulating immune complexes of Abeta and IgM in plasma of patients with Alzheimer's disease. J Neural Transm. 116: 2009; 913–920
10.1007/s00702-009-0224-y Google Scholar
- [40]S.E. O'Bryant, S.C. Waring, V. Hobson, J.R. Hall, C.B. Moore, T. Bottiglieri, et al. Decreased C-reactive protein levels in Alzheimer disease. J Geriatr Psychiatry Neurol. 23: 2010; 49–53
- [41]R. Ghidoni, A. Paterlini, L. Benussi. Translational proteomics in Alzheimer's disease and related disorders. Clin Biochem. 46 (6): 2013; 480–486
- [42]M.A. Karsdal, I. Byrjalsen, A.C. Bay-Jensen, K. Henriksen, B.J. Riis, C. Christiansen. Biochemical markers identify influences on bone and cartilage degradation in osteoarthritis - the effect of sex, Kellgren-Lawrence (KL) score, Body Mass Index (BMI), oral salmon calcitonin (sCT) treatment and diurnal variation BMC. Musculoskelet Disord. 11: 2010; 125
- [43]M.A. Karsdal, K. Henriksen, D.J. Leeming, T. Woodworth, E. Vassiliadis, A.C. Bay-Jensen. Novel combinations of Post-Translational Modification (PTM) neo-epitopes provide tissue-specific biochemical markers-are they the cause or the consequence of the disease? Clin Biochem. 43: 2010; 793–804
- [44]M.A. Karsdal, T. Woodworth, K. Henriksen, W.P. Maksymowych, H. Genant, P. Vergnaud, et al. Biochemical markers of ongoing joint damage in rheumatoid arthritis–current and future applications, limitations and opportunities. Arthritis Res Ther. 13: 2011; 215
- [45]M. Thambisetty, A. Simmons, L. Velayudhan, A. Hye, J. Campbell, Y. Zhang, et al. Association of plasma clusterin concentration with severity, pathology, and progression in Alzheimer disease. Arch Gen Psychiatry. 67: 2010; 739–748
- [46]A. Hye, S. Lynham, M. Thambisetty, M. Causevic, J. Campbell, H.L. Byers, et al. Proteome-based plasma biomarkers for Alzheimer's disease. Brain. 129: 2006; 3042–3050
- [47]S.J. Kiddle, M. Thambisetty, A. Simmons, J. Riddoch-Contreras, A. Hye, E. Westman, et al. Plasma based markers of [11C] PiB-PET brain amyloid burden. PLoS One. 7: 2012; e44260
- [48]M. Thambisetty, A. Simmons, A. Hye, J. Campbell, E. Westman, Y. Zhang, et al. Plasma biomarkers of brain atrophy in Alzheimer's disease. PLoS One. 6: 2011; e28527
- [49]M. Thambisetty, R. Tripaldi, J. Riddoch-Contreras, A. Hye, Y. An, J. Campbell, et al. Proteome-based plasma markers of brain amyloid-beta deposition in non-demented older individuals. J Alzheimers Dis. 22: 2010; 1099–1109
- [50]C. Cruchaga, J.S. Kauwe, K. Mayo, N. Spiegel, S. Bertelsen, P. Nowotny, et al. SNPs associated with cerebrospinal fluid phospho-tau levels influence rate of decline in Alzheimer's disease. PLoS Genet. 6: 2012
- [51]D.C. Bauer, D.J. Hunter, S.B. Abramson, M. Attur, M. Corr, D. Felson, et al. Classification of osteoarthritis biomarkers: a proposed approach. Osteoarthritis Cartilage. 14: 2006; 723–727
- [52]M.A. Karsdal, K. Henriksen, D.J. Leeming, P. Mitchell, K. Duffin, N. Barascuk, et al. Biochemical markers and the FDA Critical Path: how biomarkers may contribute to the understanding of pathophysiology and provide unique and necessary tools for drug development. Biomarkers. 14: 2009; 181–202
- [53]S. Lista, F. Faltraco, H. Hampel. Biological and methodical challenges of blood-based proteomics in the field of neurological research. Prog Neurobiol. 101-102: 2013; 18–34
- [54]S. Ray, M. Britschgi, C. Herbert, Y. Takeda-Uchimura, A. Boxer, K. Blennow, et al. Classification and prediction of clinical Alzheimer's diagnosis based on plasma signaling proteins. Nat Med. 13: 2007; 1359–1362
- [55]M. Britschgi, K. Rufibach, S.L. Huang, C.M. Clark, J.A. Kaye, G. Li, et al. Modeling of pathological traits in Alzheimer's disease based on systemic extracellular signaling proteome. Mol Cell Proteomics. 10: 2011; M111
- [56]H.D. Soares, Y. Chen, M. Sabbagh, A. Roher, E. Schrijvers, M. Breteler. Identifying early markers of Alzheimer's disease using quantitative multiplex proteomic immunoassay panels. Ann NY Acad Sci. 1180: 2009; 56–67
- [57]M. Bjorkqvist, M. Ohlsson, L. Minthon, O. Hansson. Evaluation of a previously suggested plasma biomarker panel to identify Alzheimer's disease. PLoS One. 7: 2012; e29868
- [58]J.D. Doecke, S.M. Laws, N.G. Faux, W. Wilson, S.C. Burnham, C.P. Lam, et al. Blood-Based Protein Biomarkers for Diagnosis of Alzheimer Disease. Arch Neurol. 69 (10): 2012; 1318–1325
- [59]S.E. O'Bryant, G. Xiao, R. Barber, R. Huebinger, K. Wilhelmsen, M. Edwards, et al. A blood-based screening tool for Alzheimer's disease that spans serum and plasma: findings from TARC and ADNI. PLoS One. 6: 2011; e28092
- [60]D.A. Llano, V. Devanarayan, A.J. Simon. Evaluation of Plasma Proteomic Data for Alzheimer Disease State Classification and for the Prediction of Progression From Mild Cognitive Impairment to Alzheimer Disease. Alzheimer Dis Assoc Disord, 2012[Epub ahead of print]
- [61]A.M. Chang, A.S. Maisel, J.E. Hollander. Diagnosis of heart failure. Heart Fail Clin. 5: 2009; 25–35
- [62]C. Sambanis, K. Tziomalos, E. Kountana, N. Kakavas, I. Zografou, A. Balaska, et al. Effect of pioglitazone on heart function and N-terminal pro-brain natriuretic peptide levels of patients with type 2 diabetes. Acta Diabetol. 45: 2008; 23–30
- [63]K. Buerger, A. Ernst, M. Ewers, O. Uspenskaya, M. Omerovic, N.G. Morgenthaler, et al. Blood-based microcirculation markers in Alzheimer's disease-diagnostic value of midregional pro-atrial natriuretic peptide/C-terminal endothelin-1 precursor fragment ratio. Biol Psychiatry. 65: 2009; 979–984
- [64]K. Buerger, O. Uspenskaya, O. Hartmann, O. Hansson, L. Minthon, K. Blennow, et al. Prediction of Alzheimer's disease using midregional proadrenomedullin and midregional proatrial natriuretic peptide: a retrospective analysis of 134 patients with mild cognitive impairment. J Clin Psychiatry. 72: 2011; 556–563
- [65]G. Wu, S. Sankaranarayanan, J. Wong, K. Tugusheva, M.S. Michener, X. Shi, et al. Characterization of plasma beta-secretase (BACE1) activity and soluble amyloid precursor proteins as potential biomarkers for Alzheimer's disease. J Neurosci Res. 90: 2012; 2247–2258
- [66]P.G. Di, T.W. Kim. Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat Rev Neurosci. 12: 2011; 284–296
- [67]P.L. Wood. Lipidomics of Alzheimer's disease: current status. Alzheimers Res Ther. 4: 2012; 5
- [68]X. Han, S. Rozen, S.H. Boyle, C. Hellegers, H. Cheng, J.R. Burke, et al. Metabolomics in early Alzheimer's disease: identification of altered plasma sphingolipidome using shotgun lipidomics. PLoS One. 6: 2011; e21643
- [69]M.M. Mielke, N.J. Haughey, V.V. Bandaru, D.D. Weinberg, E. Darby, N. Zaidi, et al. Plasma Sphingomyelins are Associated with Cognitive Progression in Alzheimer's Disease. J Alzheimers Dis. 27 (2): 2011; 259–269
- [70]B.B. Booij, T. Lindahl, P. Wetterberg, N.V. Skaane, S. Saebo, G. Feten, et al. A gene expression pattern in blood for the early detection of Alzheimer's disease. J Alzheimers Dis. 23: 2011; 109–119
- [71]P.D. Rye, B.B. Booij, G. Grave, T. Lindahl, L. Kristiansen, H.M. Andersen, et al. A novel blood test for the early detection of Alzheimer's disease. J Alzheimers Dis. 23: 2011; 121–129
- [72]P. Fehlbaum-Beurdeley, O. Sol, L. Desire, J. Touchon, T. Dantoine, M. Vercelletto, et al. Validation of AclarusDx, a Blood-Based Transcriptomic Signature for the Diagnosis of Alzheimer's Disease. J Alzheimers Dis. 32: 2012; 169–181
- [73]K. Lunnon, M. Sattlecker, S.J. Furney, G. Coppola, A. Simmons, P. Proitsi, et al. A Blood Gene Expression Marker of Early Alzheimer's Disease. J Alzheimers Dis. 33 (3): 2013; 737–753
- [74]K. Lunnon, Z. Ibrahim, P. Proitsi, A. Lourdusamy, S. Newhouse, M. Sattlecker, et al. Mitochondrial dysfunction and immune activation are detectable in early Alzheimer's disease blood. J Alzheimers Dis. 30: 2012; 685–710
- [75]S.C. Wang, B. Oelze, A. Schumacher. Age-specific epigenetic drift in late-onset Alzheimer's disease. PLoS One. 3: 2008; e2698
- [76]R. Kaddurah-Daouk, S. Rozen, W. Matson, X. Han, C.M. Hulette, J.R. Burke, et al. Metabolomic changes in autopsy-confirmed Alzheimer's disease. Alzheimers Dement. 7: 2011; 309–317
- [77]J.N. Lukens, D.V. Van, C.M. Clark, S.X. Xie, F.B. Johnson. Comparisons of telomere lengths in peripheral blood and cerebellum in Alzheimer's disease. Alzheimers Dement. 5: 2009; 463–469
- [78]T. Hochstrasser, J. Marksteiner, C. Humpel. Telomere length is age-dependent and reduced in monocytes of Alzheimer patients. Exp Gerontol. 47: 2012; 160–163
- [79]Y. Takata, M. Kikukawa, H. Hanyu, S. Koyama, S. Shimizu, T. Umahara, et al. Association between ApoE phenotypes and telomere erosion in Alzheimer's disease. J Gerontol A Biol Sci Med Sci. 67: 2012; 330–335
- [80]D.M. Holtzman, A. Goate, J. Kelly, R. Sperling. Mapping the road forward in Alzheimer's disease. Sci Transl Med. 3: 2011, 114ps48
- [81]T. Colasanti, C. Barbati, G. Rosano, W. Malorni, E. Ortona. Autoantibodies in patients with Alzheimer's disease: pathogenetic role and potential use as biomarkers of disease progression. Autoimmun Rev. 9: 2010; 807–811
- [82]K.A. Gustaw-Rothenberg, S.L. Siedlak, D.J. Bonda, A. Lerner, M. Tabaton, G. Perry, et al. Dissociated amyloid-beta antibody levels as a serum biomarker for the progression of Alzheimer's disease: a population-based study. Exp Gerontol. 45: 2010; 47–52
- [83]M. Maftei, F. Thurm, V.M. Leirer, C.A. von Arnim, T. Elbert, et al. Antigen-Bound and Free beta-Amyloid Autoantibodies in Serum of Healthy Adults. PLoS One. 7: 2012; e44516
- [84]E. Nagele, M. Han, C. Demarshall, B. Belinka, R. Nagele. Diagnosis of Alzheimer's disease based on disease-specific autoantibody profiles in human sera. PLoS One. 6: 2011; e23112
- [85]H. Geekiyanage, G.A. Jicha, P.T. Nelson, C. Chan. Blood serum miRNA: non-invasive biomarkers for Alzheimer's disease. Exp Neurol. 235: 2012; 491–496
- [86]K.S. Sheinerman, V.G. Tsivinsky, F. Crawford, M.J. Mullan, L. Abdullah, S.R. Umansky. Plasma microRNA biomarkers for detection of mild cognitive impairment. Aging (Albany, NY). 4: 2012; 590–605
- [87]J.B. Toledo, H. Vanderstichele, M. Figurski, P.S. Aisen, R.C. Petersen, M.W. Weiner, et al. Factors affecting Abeta plasma levels and their utility as biomarkers in ADNI. Acta Neuropathol. 122: 2011; 401–413
- [88]P.D. Mehta, T. Pirttila, S.P. Mehta, E.A. Sersen, P.S. Aisen, H.M. Wisniewski. Plasma and cerebrospinal fluid levels of amyloid beta proteins 1-40 and 1-42 in Alzheimer disease. Arch Neurol. 57: 2000; 100–105
- [89]A. Koyama, O.I. Okereke, T. Yang, D. Blacker, D.J. Selkoe, F. Grodstein. Plasma amyloid-beta as a predictor of dementia and cognitive decline: a systematic review and meta-analysis. Arch Neurol. 69: 2012; 824–831
- [90]H. Hampel, Y. Shen, D.M. Walsh, P. Aisen, L.M. Shaw, H. Zetterberg, et al. Biological markers of amyloid beta-related mechanisms in Alzheimer's disease. Exp Neurol. 223: 2012; 334–346
- [91]R.A. Rissman, J.Q. Trojanowski, L.M. Shaw, P.S. Aisen. Longitudinal plasma amyloid beta as a biomarker of Alzheimer's disease. J Neural Transm. 119: 2012; 843–850
- [92]F. Song, A. Poljak, M. Valenzuela, R. Mayeux, G.A. Smythe, P.S. Sachdev. Meta-analysis of plasma amyloid-beta levels in Alzheimer's disease. J Alzheimers Dis. 26: 2011; 365–375
- [93]A.D. Watt, K.A. Perez, A.R. Rembach, C.L. Masters, V.L. Villemagne, K.J. Barnham. Variability in blood-based amyloid-beta assays: the need for consensus on pre-analytical processing. J Alzheimers Dis. 30: 2012; 323–336
- [94]K.A. Bruggink, M. Muller, H.B. Kuiperij, M.M. Verbeek. Methods for analysis of amyloid-beta aggregates. J Alzheimers Dis. 28: 2012; 735–758
- [95]W. Xia, T. Yang, G. Shankar, I.M. Smith, Y. Shen, D.M. Walsh, et al. A specific enzyme-linked immunosorbent assay for measuring beta-amyloid protein oligomers in human plasma and brain tissue of patients with Alzheimer disease. Arch Neurol. 66: 2009; 190–199
- [96]M. Noguchi-Shinohara, T. Hamaguchi, I. Nozaki, K. Sakai, M. Yamada. Serum tau protein as a marker for the diagnosis of Creutzfeldt-Jakob disease. J Neurol. 258: 2011; 1464–1468
- [97]J. Bielewicz, J. Kurzepa, E. Czekajska-Chehab, Z. Stelmasiak, H. Bartosik-Psujek. Does serum Tau protein predict the outcome of patients with ischemic stroke? J Mol Neurosci. 43: 2011; 241–245
- [98]P.C. Liliang, C.L. Liang, H.C. Weng, K. Lu, K.W. Wang, H.J. Chen, et al. Tau proteins in serum predict outcome after severe traumatic brain injury. J Surg Res. 160: 2010; 302–307
- [99]J. Randall, E. Mortberg, G.K. Provuncher, D.R. Fournier, D.C. Duffy, S. Rubertsson, et al. Tau proteins in serum predict neurological outcome after hypoxic brain injury from cardiac arrest: Results of a pilot study. Resuscitation. 84 (3): 2013; 351–356
- [100]S. Neselius, H. Zetterberg, K. Blennow, J. Randall, D. Wilson, J. Marcusson, H. Brisby. Brain Injury 2012, In Press
- [101]E. Portelius, R.A. Dean, M.K. Gustavsson, U. Andreasson, H. Zetterberg, E. Siemers, et al. A novel Abeta isoform pattern in CSF reflects gamma-secretase inhibition in Alzheimer disease. Alzheimers Res Ther. 2 (2): 2010; 7
- [102]N. Mattsson, L. Rajendran, H. Zetterberg, M. Gustavsson, U. Andreasson, M. Olsson, et al. BACE1 inhibition induces a specific cerebrospinal fluid beta-amyloid pattern that identifies drug effects in the central nervous system. PLoS One. 7: 2012; e31084
- [103]J. Reifert, D. Hartung-Cranston, S.C. Feinstein. Amyloid {beta}-Mediated Cell Death of Cultured Hippocampal Neurons Reveals Extensive Tau Fragmentation without Increased Full-length Tau Phosphorylation. J Biol Chem. 286: 2011; 20797–20811
- [104]C.A. de, L.M. Fox, R. Pitstick, G.A. Carlson, B.J. Bacskai, T.L. Spires-Jones, et al. Caspase activation precedes and leads to tangles. Nature. 464: 2012; 1201–1204
- [105]T.C. Gamblin, F. Chen, A. Zambrano, A. Abraha, S. Lagalwar, A.L. Guillozet, et al. Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA. 100: 2003; 10032–10037
- [106]T.T. Rohn. Caspase-cleaved TAR DNA-binding protein-43 is a major pathological finding in Alzheimer's disease. Brain Res. 1228: 2008; 189–198
- [107]Y.J. Zhang, Y.F. Xu, C.A. Dickey, E. Buratti, F. Baralle, R. Bailey, et al. Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J Neurosci. 27: 2007; 10530–10534
- [108]M.R. Cookson. alpha-Synuclein and neuronal cell death. Mol Neurodegener. 4: 2009; 9
- [109]B. De Strooper. Proteases and proteolysis in Alzheimer disease: a multifactorial view on the disease process. Physiol Rev. 90: 2010; 465–494
- [110]S. Brunholz, S. Sisodia, A. Lorenzo, C. Deyts, S. Kins, G. Morfini. Axonal transport of APP and the spatial regulation of APP cleavage and function in neuronal cells. Exp Brain Res. 217 (3-4): 2012; 353–364
- [111]M.O. Grimm, T.L. Rothhaar, T. Hartmann. The role of APP proteolytic processing in lipid metabolism. Exp Brain Res. 217 (3-4): 2012; 365–375
- [112]J. Avila. Alzheimer disease: caspases first. Nat Rev Neurol. 6: 2010; 587–588
- [113]R.A. Rissman, W.W. Poon, M. Blurton-Jones, S. Oddo, R. Torp, M.P. Vitek, et al. Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J Clin Invest. 114: 2004; 121–130
- [114]J.Y. Sung, S.M. Park, C.H. Lee, J.W. Um, H.J. Lee, J. Kim, et al. Proteolytic cleavage of extracellular secreted {alpha}-synuclein via matrix metalloproteinases. J Biol Chem. 280: 2005; 25216–25224
- [115]M. Eller, D.R. Williams. alpha-Synuclein in Parkinson disease and other neurodegenerative disorders. Clin Chem Lab Med. 49: 2011; 403–408
- [116]B.M. Dufty, L.R. Warner, S.T. Hou, S.X. Jiang, T. Gomez-Isla, K.M. Leenhouts, et al. Calpain-cleavage of alpha-synuclein: connecting proteolytic processing to disease-linked aggregation. Am J Pathol. 170: 2007; 1725–1738
- [117]C. Yang, W. Tan, C. Whittle, L. Qiu, L. Cao, S. Akbarian, et al. The C-terminal TDP-43 fragments have a high aggregation propensity and harm neurons by a dominant-negative mechanism. PLoS One. 5: 2012; e15878
- [118]I.R. Mackenzie, R. Rademakers, M. Neumann. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol. 9: 2010; 995–1007
- [119]Y.S. Chen, S.C. Lim, M.H. Chen, R.A. Quinlan, M.D. Perng. Alexander disease causing mutations in the C-terminal domain of GFAP are deleterious both to assembly and network formation with the potential to both activate caspase 3 and decrease cell viability. Exp Cell Res. 317: 2011; 2252–2266
- [120]K. Henriksen, Y. Wang, M.G. S⊘rensen, N. Barascuk, J. Suhy, J.T. Pedersen, et al. An enzyme-generated fragment of Tau measured in serum shows an inverse correlation to cognitive function. PLOS One, 2013, In press
- [121]M.L. Andersson, I.F. Petersson, K.E. Karlsson, E.N. Jonsson, B. Mansson, D. Heinegard, et al. Diurnal variation in serum levels of cartilage oligomeric matrix protein in patients with knee osteoarthritis or rheumatoid arthritis. Ann Rheum Dis. 65: 2006; 1490–1494
- [122]M.A. Karsdal, I. Byrjalsen, B.J. Riis, C. Christiansen. Investigation of the diurnal variation in bone resorption for optimal drug delivery and efficacy in osteoporosis with oral calcitonin. BMC Clin Pharmacol. 8: 2008; 12
- [123]S.Y. Kong, T.V. Stabler, L.G. Criscione, A.L. Elliott, J.M. Jordan, V.B. Kraus. Diurnal variation of serum and urine biomarkers in patients with radiographic knee osteoarthritis. Arthritis Rheum. 54: 2006; 2496–2504
- [124]D.J. Quintana, P. Garnero, J.L. Huebner, T.N. Charni-Ben, V.B. Kraus. PIIANP and HELIXII diurnal variation. Osteoarthritis Cartilage. 16: 2008; 1192–1195
10.1016/j.joca.2008.03.006 Google Scholar
- [125]A. Schlemmer, C. Hassager, S.B. Jensen, C. Christiansen. Marked diurnal variation in urinary excretion of pyridinium cross-links in premenopausal women. J Clin Endocrinol Metab. 74: 1992; 476–480
- [126]L.G. Criscione, A.L. Elliott, T. Stabler, J.M. Jordan, C.F. Pieper, V.B. Kraus. Variation of serum hyaluronan with activity in individuals with knee osteoarthritis. Osteoarthritis Cartilage. 13: 2005; 837–840
- [127]M.A. Karsdal, I. Byrjalsen, M. Azria, M. Arnold, L. Choi, B.J. Riis, et al. Influence of food intake on the bioavailability and efficacy of oral calcitonin. Br J Clin Pharmacol. 67: 2009; 413–420
- [128] U.S. Food and Drug Administration. Guidance for industry: bioanalytical method validation. 2001; U.S. Food and Drug Administration: Rockville, MD
- [129]C. Belabani, S. Rajasekharan, V. Poupon, T. Johnson, A. Bar-Or. A condensed performance-validation strategy for multiplex detection kits used in studies of human clinical samples. J Immunol Methods. 387 (1-2): 2013; 1–10
- [130]C.M. Micheel, S.J. Nass, G.J. Omenn. Evolution of translational omics: lessons learned and the path forward. 2012; National Academies Press: Washington, DC
10.17226/13297 Google Scholar
- [131]T.J. Lyons, A. Basu. Biomarkers in diabetes: hemoglobin A1c, vascular and tissue markers. Transl Res. 159: 2012; 303–312
- [132]M. Madjid, J.T. Willerson. Inflammatory markers in coronary heart disease. Br Med Bull. 100: 2011; 23–38
- [133]F. Irie, A.L. Fitzpatrick, O.L. Lopez, L.H. Kuller, R. Peila, A.B. Newman, et al. Enhanced risk for Alzheimer disease in persons with type 2 diabetes and APOE epsilon4: the Cardiovascular Health Study Cognition Study. Arch Neurol. 65: 2008; 89–93
- [134]T.J. Cohen, V.M. Lee, J.Q. Trojanowski. TDP-43 functions and pathogenic mechanisms implicated in TDP-43 proteinopathies. Trends Mol Med. 17: 2011; 659–667
- [135]D. Ito, N. Suzuki. Conjoint pathologic cascades mediated by ALS/FTLD-U linked RNA-binding proteins TDP-43 and FUS. Neurology. 77: 2011; 1636–1643
- [136]V.B. Gupta, S.M. Laws, V.L. Villemagne, D. Ames, A.I. Bush, K.A. Ellis, et al. Plasma apolipoprotein E and Alzheimer disease risk: the AIBL study of aging. Neurology. 76: 2011; 1091–1098
- [137]T. Sunderland, N. Mirza, K.T. Putnam, G. Linker, D. Bhupali, R. Durham, et al. Cerebrospinal fluid beta-amyloid1-42 and tau in control subjects at risk for Alzheimer's disease: the effect of APOE epsilon4 allele. Biol Psychiatry. 56: 2004; 670–676
- [138]C.C. Rowe, K.A. Ellis, M. Rimajova, P. Bourgeat, K.E. Pike, G. Jones, et al. Amyloid imaging results from the Australian Imaging, Biomarkers and Lifestyle (AIBL) study of aging. Neurobiol Aging. 31: 2010; 1275–1283
- [139]C. Cruchaga, J.S. Kauwe, P. Nowotny, K. Bales, E.H. Pickering, K. Mayo, et al. Cerebrospinal fluid APOE levels: an endophenotype for genetic studies for Alzheimer's disease. Hum Mol Genet. 21: 2012; 4558–4571
- [140]J.B. Toledo, J. Brettschneider, M. Grossman, S.E. Arnold, W.T. Hu, S.X. Xie, et al. CSF biomarkers cutoffs: the importance of coincident neuropathological diseases. Acta Neuropathol. 124: 2012; 23–35