Fibrinogen isoforms as potential blood-based biomarkers of Alzheimer’s disease using a proteomics approach

References

• Dong R, Wang H, Ye J, et al. Publication trends for Alzheimer's disease worldwide and in China: a 30-year bibliometric analysis. Front Hum Neurosci. 2019;13:259,
   PubMed Web of Science ®Google Scholar
• Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science. 2002;297(5580):353–356.
   PubMed Web of Science ®Google Scholar
• Kametani F, Hasegawa M. Reconsideration of amyloid hypothesis and tau hypothesis in Alzheimer's disease. Front Neurosci. 2018;12.DOI:10.3389/fnins.2018.00025
   PubMed Web of Science ®Google Scholar
• Heneka MT, Carson MJ, Khoury JE, et al. Neuroinflammation in Alzheimer's disease. Lancet Neurol. 2015;14(4):388–405.,
   PubMed Web of Science ®Google Scholar
• Heppner FL, Ransohoff RM, Becher B. Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci. 2015;16(6):358–372.
   PubMed Web of Science ®Google Scholar
• Rius-Pérez S, Tormos AM, Pérez S, et al. Vascular pathology: cause or effect in Alzheimer disease? Neurologia. 2018;33(2):112–120.,
   PubMed Web of Science ®Google Scholar
• Long JM, Holtzman DM. Alzheimer disease: an update on pathobiology and treatment strategies. Cell. 2019;179(2):312–339. )
   PubMed Web of Science ®Google Scholar
• Doody RS, Thomas RG, Farlow M, Solanezumab Study Group, et al. Phase 3 trials of solanezumab for mild-to-moderate Alzheimer's disease. N Engl J Med. 2014;370(4):311–321.,
   PubMed Web of Science ®Google Scholar
• Schneider P, Hampel H, Buerger K. Biological marker candidates of Alzheimer's disease in blood, plasma, and serum. CNS Neurosci Ther. 2009;15(4):358–374.
   PubMed Web of Science ®Google Scholar
• Jellinger KA, Janetzky B, Attems J, et al. Biomarkers for early diagnosis of Alzheimer disease: ‘Alzheimer associated gene’-a new blood biomarker? J Cell Mol Med. 2008;12(4):1094–1117.,
   PubMed Web of Science ®Google Scholar
• McKhann GM, Knopman DS, Chertkow H, et al. The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's Dement. 2011;7(3):263–269.,
   PubMed Web of Science ®Google Scholar
• Leinenbach A, Pannee J, Dülffer T, IFCC Scientific Division Working Group on CSF proteins, et al. Mass spectrometry-based candidate reference measurement procedure for quantification of amyloid-β in cerebrospinal fluid . Clin Chem. 2014;60(7):987–994.
   PubMed Web of Science ®Google Scholar
• Zipser BD, Johanson CE, Gonzalez L, et al. Microvascular injury and blood-brain barrier leakage in Alzheimer's disease. Neurobiol Aging. 2007;28(7):977–986.,
   PubMed Web of Science ®Google Scholar
• Sweeney MD, Sagare AP, Zlokovic BV. Blood-brain barrier breakdown in Alzheimer disease and other neurodegenerative disorders. Nat Rev Neurol. 2018;14(3):133–150.
   PubMed Web of Science ®Google Scholar
• O'Bryant SE, Mielke MM, Rissman RA, Biofluid Based Biomarker Professional Interest Area, et al. Blood-based biomarkers in Alzheimer disease: current state of the science and a novel collaborative paradigm for advancing from discovery to clinic. Alzheimers Dement. 2017;13(1):45–58.,
   PubMed Web of Science ®Google Scholar
• Henriksen K, O'Bryant SE, Hampel H, Blood-Based Biomarker Interest Group, et al. The future of blood-based biomarkers for Alzheimer's disease. Alzheimers Dement. 2014;10(1):115–131.,
   PubMed Web of Science ®Google Scholar
• Gauthier S, Reisberg B, Zaudig M, et al. Mild cognitive impairment. Lancet. 2006;367(9518):1262–1270.,
   PubMed Web of Science ®Google Scholar
• Sperling RA, Jack CR, Aisen PS. Testing the right target and right drug at the right stage. Sci Transl Med. 2011;3(111):111cm33–111cm33.
   PubMed Web of Science ®Google Scholar
• Lista S, Faltraco F, Prvulovic D, et al. Blood and plasma-based proteomic biomarker research in Alzheimer's disease. Prog Neurobiol. 2013;101/102:1–17.
   PubMed Web of Science ®Google Scholar
• Omenn GS, Lane L, Overall CM, et al. Progress on identifying and characterizing the Human Proteome: 2019 metrics from the HUPO Human Proteome Project. J Proteome Res. 2019;18(12):4098–4107.
   PubMed Web of Science ®Google Scholar
• Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteom. 2002;1(11):845–867.
   PubMed Web of Science ®Google Scholar
• Arentz G, Weiland F, Oehler MK, et al. State of the art of 2D DIGE. Proteomics Clin Appl. 2015;9(3/4):277–288.,
   PubMed Web of Science ®Google Scholar
• Beckett P. The basics of 2D DIGE. In: R. Cramerand R. Westermeier, Editors. Difference gel electrophoresis (DIGE). Methods in Molecular Biology (Methods and Protocols). New York: Humana Press; 2012. p. 9–19.
   Google Scholar
• Issaq HJ, Veenstra TD. Two-dimensional difference in gel electrophoresis for biomarker discovery. In: Proteomic and metabolomic approaches to biomarker discovery. Amsterdam: Elsevier; 2020. p. 209–214.
   Google Scholar
• Domon B, Aebersold R. Mass spectrometry and protein analysis. Science. 2006;312(5771):212–217.
   PubMed Web of Science ®Google Scholar
• Carlson RV, Boyd KM, Webb DJ. The revision of the Declaration of Helsinki: past, present and future. Br J Clin Pharmacol. 2004;57(6):695–713.
   PubMed Web of Science ®Google Scholar
• Bell CC. DSM-IV: diagnostic and statistical manual of mental disorders. JAMA. 1994;272(10):828–829.
   Google Scholar
• McKhann G, Drachman D, Folstein M, et al. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease . Neurology. 1984;34(7):939–939.,
   PubMed Web of Science ®Google Scholar
• Petersen RC, Smith GE, Waring SC, et al. Mild cognitive impairment: clinical characterization and outcome. Arch Neurol. 1999;56(3):303–308.,
   PubMed Web of Science ®Google Scholar
• Cockrell JR, Folstein MF. Mini-mental state examination. In: Copeland JRM, Abou‐Saleh MT, Blazer DG, editors. Principles and practice of geriatric psychiatry. John Wiley & Sons, Ltd West Sussex; 2002. p. 140–141.
   Google Scholar
• Hughes CP, Berg L, Danziger WL, et al. A new clinical scale for the staging of dementia. Br J Psychiatry. 1982;140(6):566–572.,
   PubMed Web of Science ®Google Scholar
• Yesavage JA, Brink TL, Rose TL, et al. Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res. 1982;17(1):37–49.
   PubMed Web of Science ®Google Scholar
• Kahn RL, Zarit SH, Hilbert NM, et al. Memory complaint and impairment in the aged. The effect of depression and altered brain function. Arch Gen Psychiatry. 1975;32(12):1569–1573.,
   PubMed Web of Science ®Google Scholar
• Katz S, Ford AB, Moskowitz RW, et al. Studies of illness in the aged. the index of ADL: a standardized measure of biological and psychosocial function. JAMA. 1963;185(12):914–919.,
   PubMed Web of Science ®Google Scholar
• Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 1969;9(3):179–186.
   PubMed Web of Science ®Google Scholar
• Mohd Hasni DS, Lim SM, Chin AV, et al. Peripheral cytokines, C‐X‐C motif ligand10 and interleukin‐13, are associated with Malaysian Alzheimer's disease. Geriatr Gerontol Int. 2017;17(5):839–846.,
   PubMed Web of Science ®Google Scholar
• Tannu NS, Hemby SE. Two-dimensional fluorescence difference gel electrophoresis for comparative proteomics profiling. Nat Protoc. 2006;1(4):1732–1742.
   PubMed Web of Science ®Google Scholar
• Timms JF, Cramer R. Difference gel electrophoresis. Proteomics. 2008;8(23/24):4886–4897.
   PubMed Web of Science ®Google Scholar
• Görg A, Obermaier C, Boguth G, et al. The current state of two‐dimensional electrophoresis with immobilized pH gradients. Electrophoresis. 2000;21(6):1037–1053.
   PubMed Web of Science ®Google Scholar
• Fodor IK, Nelson DO, Alegria-Hartman M, et al. Statistical challenges in the analysis of two-dimensional difference gel electrophoresis experiments using DeCyder™. Bioinformatics. 2005;21(19):3733–3740.,
   PubMed Web of Science ®Google Scholar
• Gharbi S, Gaffney P, Yang A, et al. Evaluation of two-dimensional differential gel electrophoresis for proteomic expression analysis of a model breast cancer cell system. Mol Cell Proteomics. 2002;1(2):91–98.,
   PubMed Web of Science ®Google Scholar
• Karp NA, Kreil DP, Lilley KS. Determining a significant change in protein expression with DeCyder during a pair-wise comparison using two-dimensional difference gel electrophoresis. Proteomics. 2004;4(5):1421–1432.
   PubMed Web of Science ®Google Scholar
• Shevchenko A, Tomas H, Havlis J, et al. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc. 2006;1(6):2856–2860.
   PubMed Web of Science ®Google Scholar
• Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature. 2003;422(6928):198–207.
   PubMed Web of Science ®Google Scholar
• Perkins DN, Pappin DJC, Creasy DM, et al. Probability‐based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis. 1999;20(18):3551–3567.,
   PubMed Web of Science ®Google Scholar
• Lu M, Jin Y, Cerny R, et al. Combining 2-DE immunoblots and mass spectrometry to identify putative soybean (Glycine max) allergens. Food Chem Toxicol. 2018;116(Pt B):207–215.,
   PubMed Web of Science ®Google Scholar
• Zweig MH, Campbell G. Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem. 1993;39(4):561–577.
   PubMed Web of Science ®Google Scholar
• Cocciolo A, Di Domenico F, Coccia R, et al. Decreased expression and increased oxidation of plasma haptoglobin in Alzheimer disease: Insights from redox proteomics. Free Radic Biol Med. 2012;53(10):1868–1876.,
   PubMed Web of Science ®Google Scholar
• Muenchhoff J, Poljak A, Song F, et al. Plasma protein profiling of mild cognitive impairment and Alzheimer's disease across two independent cohorts. J Alzheimers Dis. 2015;43(4):1355–1373.,
   PubMed Web of Science ®Google Scholar
• Kitamura Y, Usami R, Ichihara S, et al. Plasma protein profiling for potential biomarkers in the early diagnosis of Alzheimer's disease. Neurol Res. 2017;39(3):231–238.,
   PubMed Web of Science ®Google Scholar
• Xu G, Zhang H, Zhang S, et al. Plasma fibrinogen is associated with cognitive decline and risk for dementia in patients with mild cognitive impairment. International Journal of Clinical Practice. 2007;62(7):1070–1075.,
   PubMed Web of Science ®Google Scholar
• Mosesson M. Fibrinogen and fibrin structure and functions. J Thromb Haemost. 2005;3(8):1894–1904.
   PubMed Web of Science ®Google Scholar
• Tomimoto H, Akiguchi I, Suenaga T, et al. Alterations of the blood-brain barrier and glial cells in white-matter lesions in cerebrovascular and Alzheimer's disease patients. Stroke. 1996;27(11):2069–2074.,
   PubMed Web of Science ®Google Scholar
• Erickson MA, Banks WA. Blood-brain barrier dysfunction as a cause and consequence of Alzheimer's disease. J Cereb Blood Flow Metab. 2013;33(10):1500–1513.
   PubMed Web of Science ®Google Scholar
• Ryu JK, McLarnon JG. A leaky blood-brain barrier, fibrinogen infiltration and microglial reactivity in inflamed Alzheimer's disease brain. J Cell Mol Med. 2009;13(9A):2911–2925.
   PubMed Web of Science ®Google Scholar
• Viggars AP, Wharton SB, Simpson JE, et al. Alterations in the blood brain barrier in ageing cerebral cortex in relationship to Alzheimer-type pathology: a study in the MRC-CFAS population neuropathology cohort. Neurosci Lett. 2011;505(1):25–30.
   PubMed Web of Science ®Google Scholar
• Cooper AV, Standeven KF, Ariëns RA. Fibrinogen gamma-chain splice variant gamma' alters fibrin formation and structure. Blood. 2003;102(2):535–540.
   PubMed Web of Science ®Google Scholar
• Mosesson MW, Antithrombin I. Inhibition of thrombin generation in plasma by fibrin formation. Thromb Haemost. 2003;89(1):9–12.
   PubMed Web of Science ®Google Scholar
• Bennett JS. Platelet-fibrinogen interactions. Ann N Y Acad Sci. 2001;936(1):340–354.
   PubMed Web of Science ®Google Scholar
• de Willige SU, et al. Genetic variation in the fibrinogen gamma gene increases the risk for deep venous thrombosis by reducing plasma fibrinogen γ′ levels. Blood. 2005;106(13):4176–4183.,
   PubMed Web of Science ®Google Scholar
• Wood H. Fibrinogen links vascular pathology to cognitive decline. Nat Rev Neurol. 2019;15(4):187–187.
   PubMed Web of Science ®Google Scholar
• Ahn HJ, Zamolodchikov D, Cortes-Canteli M, et al. Alzheimer's disease peptide beta-amyloid interacts with fibrinogen and induces its oligomerization . Proc Natl Acad Sci U S A. 2010;107(50):21812–21817.,
   PubMed Web of Science ®Google Scholar
• Cortes-Canteli M, Zamolodchikov D, Ahn HJ, et al. Fibrinogen and altered hemostasis in Alzheimer's disease. J Alzheimers Dis. 2012;32(3):599–608.
   PubMed Web of Science ®Google Scholar
• Cortes-Canteli M, Mattei L, Richards AT, et al. Fibrin deposited in the Alzheimer's disease brain promotes neuronal degeneration. Neurobiol Aging. 2015;36(2):608–617.,
   PubMed Web of Science ®Google Scholar
• Shi X, Ohta Y, Liu X, et al. Coagulation and complement change in Alzheimer's disease with hypoperfusion. Neuroscience. 2019;416:126–136., )
   PubMed Web of Science ®Google Scholar
• Merlini M, Rafalski VA, Rios Coronado PE, et al. Fibrinogen induces microglia-mediated spine elimination and cognitive impairment in an Alzheimer's Disease Model. Neuron. 2019;101(6):1099–1108. e6.,
   PubMed Web of Science ®Google Scholar
• The Ronald and Nancy Reagan Research Institute of the Alzheimer's Association and The National Institute on Aging Working Group, Consensus report of the working group on: “Molecular and biochemical markers of Alzheimer’s disease”. Neurobiol Aging. 1998;19(2):109–116.
   PubMed Web of Science ®Google Scholar
• Andreasson U, Vanmechelen E, Shaw LM, et al. Analytical aspects of molecular Alzheimer's disease biomarkers. Biomark Med. 2012;6(4):377–389.
   PubMed Web of Science ®Google Scholar
• Ahn HJ, Glickman JF, Poon KL, et al. A novel Aβ-fibrinogen interaction inhibitor rescues altered thrombosis and cognitive decline in Alzheimer's disease mice. J Exp Med. 2014;211(6):1049–1062.
   PubMed Web of Science ®Google Scholar
• Chiam JTW, Dobson RJB, Kiddle SJ, et al. Are blood-based protein biomarkers for Alzheimer's disease also involved in other brain disorders? A systematic review. J Alzheimers Dis. 2015;43(1):303–314.,
   PubMed Web of Science ®Google Scholar
• Davinelli S, et al. The “Alzheimer's disease signature”: potential perspectives for novel biomarkers. Immun Ageing. 2011;8(1). DOI:10.1186/1742-4933-8-7
   PubMed Web of Science ®Google Scholar
• Gupta VB, Sundaram R, Martins RN. Multiplex biomarkers in blood. Alzheimer's Res Therap. 2013;5(3). DOI: 10.1186/alzrt185
   Google Scholar
• Hampel H, O'Bryant SE, Molinuevo JL, et al. Blood-based biomarkers for Alzheimer disease: mapping the road to the clinic. Nat Rev Neurol. 2018;14(11):639–652.,
   PubMed Web of Science ®Google Scholar
• Henkel AW, Müller K, Lewczuk P, et al. Multidimensional plasma protein separation technique for identification of potential Alzheimer's disease plasma biomarkers: a pilot study. J Neural Transm (Vienna). 2012;119(7):779–788.,
   PubMed Web of Science ®Google Scholar
• Amieva H, Mokri H, Le Goff M, et al. Compensatory mechanisms in higher-educated subjects with Alzheimer's disease: a study of 20 years of cognitive decline. Brain. 2014;137(Pt 4):1167–1175.,
   PubMed Web of Science ®Google Scholar
• O'Bryant SE, Gupta V, Henriksen K, STAR-B and BBBIG working groups, et al. Guidelines for the standardization of preanalytic variables for blood-based biomarker studies in Alzheimer's disease research. Alzheimers Dement. 2015;11(5):549–560.,
   PubMed Web of Science ®Google Scholar
• Mielke MM, Rosenberg PB, Tschanz J, et al. Vascular factors predict rate of progression in Alzheimer disease. Neurology. 2007;69(19):1850–1858.,
   PubMed Web of Science ®Google Scholar
• Rock PL, Roiser JP, Riedel WJ, et al. Cognitive impairment in depression: a systematic review and meta-analysis. Psychol Med. 2014;44(10):2029–2040.,
   PubMed Web of Science ®Google Scholar
• Lubec G, Afjehi-Sadat L. Limitations and pitfalls in protein identification by mass spectrometry. Chem Rev. 2007;107(8):3568–3584.
   PubMed Web of Science ®Google Scholar