Synaptic proteins in CSF as potential novel biomarkers for prognosis in prodromal Alzheimer’s disease

Duits, Flora H.; Brinkmalm, Gunnar; Teunissen, Charlotte E.; Brinkmalm, Ann; Scheltens, Philip; Van der Flier, Wiesje M.; Zetterberg, Henrik; Blennow, Kaj

doi:10.1186/s13195-017-0335-x

Cited by 137Dementia and Cognitive Impairment ResearchAlzheimer's disease research and treatmentsAdvanced Proteomics Techniques and Applications

Synaptic proteins in CSF as potential novel biomarkers for prognosis in prodromal Alzheimer’s disease

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Duits, Flora H., Brinkmalm, Gunnar, Teunissen, Charlotte E., Brinkmalm, Ann, Scheltens, Philip, Van der Flier, Wiesje M., Zetterberg, Henrik, Blennow, Kaj·2018·Alzheimer's Research & Therapy

DOI 10.1186/s13195-017-0335-xPMC PMC6389073

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Abstract

BACKGROUND: We investigated whether a panel of 12 potential novel biomarkers consisting of proteins involved in synapse functioning and immunity would be able to distinguish patients with Alzheimer's disease (AD) and patients with mild cognitive impairment (MCI) from control subjects. METHODS: We included 40 control subjects, 40 subjects with MCI, and 40 subjects with AD from the Amsterdam Dementia Cohort who were matched for age and sex (age 65 ± 5 years, 19 [48%] women). The mean follow-up of patients with MCI was 3 years. Two or three tryptic peptides per protein were analyzed in cerebrospinal fluid using parallel reaction monitoring mass spectrometry. Corresponding stable isotope-labeled peptides were added and used as reference peptides. Multilevel generalized estimating equations (GEEs) with peptides clustered per subject and per protein (as within-subject variables) were used to assess differences between diagnostic groups. To assess differential effects of individual proteins, we included the diagnosis × protein interaction in the model. Separate GEE analyses were performed to assess differences between stable patients and patients with progressive MCI (MCI-AD). RESULTS: There was a main effect for diagnosis (p < 0.01) and an interaction between diagnosis and protein (p < 0.01). Analysis stratified according to protein showed higher levels in patients with MCI for most proteins, especially in patients with MCI-AD. Chromogranin A, secretogranin II, neurexin 3, and neuropentraxin 1 showed the largest effect sizes; β values ranged from 0.53 to 0.78 for patients with MCI versus control subjects or patients with AD, and from 0.67 to 0.98 for patients with MCI-AD versus patients with stable MCI. In contrast, neurosecretory protein VGF was lower in patients with AD than in patients with MCI (ß = -0.93 [SE 0.22]) and control subjects (ß = 0.46 [SE 0.19]). CONCLUSIONS: Our results suggest that several proteins involved in vesicular transport and synaptic stability are elevated in patients with MCI, especially in patients with MCI progressing to AD dementia. This may reflect early events in the AD pathophysiological cascade. These proteins may be valuable as disease stage or prognostic markers in an early symptomatic stage of the disease.

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Recent studies in cerebrospinal fluid revealed altered NPTXs levels in several neurodegenerative disorders.
“Recent studies in cerebrospinal fluid (CSF) revealed altered NPTXs levels in several neurodegenerative disorders.”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Duits et al. 2018

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McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984) · Neurology · doi:10.1212/wnl.34.7.939 · Cited by 27,915 · see citing works
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Zetterberg, H., Rüetschi, U., Portelius, E., Brinkmalm, G., Andréasson, U., Blennow, K., & Brinkmalm, A. (2008) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.2007.00985.x · Cited by 112 · see citing works
Self-citation
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Simonsen, A., Mcguire, J., Podust, V., Davies, H., Minthon, L., Skoog, I., Andreasen, N., Wallin, A., Waldemar, G., & Blennow, K. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.01.011 · Cited by 108 · see citing works
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Hölttä, M., Minthon, L., Hansson, O., Holmén-Larsson, J., Pike, I., Ward, M., Kuhn, K., Rüetschi, U., Zetterberg, H., Blennow, K., et al. (2015) · Journal of Proteome Research · doi:10.1021/pr501076j · Cited by 100 · see citing works
Self-citation
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Marksteiner, J., Kaufman, W. A., Gurka, P., & Humpel, C. (2002) · Journal of Molecular Neuroscience · doi:10.1385/jmn:18:1-2:53 · Cited by 54 · see citing works
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Chromogranin peptides in brain diseases
Willis, M., Leitner, I., Jellinger, K. A., & Marksteiner, J. (2011) · Journal of Neural Transmission · doi:10.1007/s00702-011-0648-z · Cited by 32 · see citing works
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Jongbloed, W., Kester, M. I., van der Flier, W. M., Veerhuis, R., Scheltens, P., Blankenstein, M. A., & Teunissen, C. E. (2012) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2012.01.004 · Cited by 29 · see citing works
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Self-citation
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Park, S. A., Han, S. M., & Kim, C. E. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-0418-9 · Cited by 91 · see citing works
VGF-derived peptide TLQP-21 modulates microglial function through C3aR1 signaling pathways and reduces neuropathology in 5xFAD mice
El Gaamouch, F., Audrain, M., Lin, W.-J., Beckmann, N., Jiang, C., Hariharan, S., Heeger, P. S., Schadt, E. E., Gandy, S., Ehrlich, M. E., et al. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-0357-x · Cited by 92 · see citing works
Endo-lysosomal proteins and ubiquitin CSF concentrations in Alzheimer’s and Parkinson’s disease
Sjödin, S., Brinkmalm, G., Öhrfelt, A., Parnetti, L., Paciotti, S., Hansson, O., Hardy, J., Blennow, K., Zetterberg, H., & Brinkmalm, A. (2019) · Alzheimer s Research & Therapy · doi:10.1186/s13195-019-0533-9 · Cited by 91 · see citing works
Self-citation
Cerebrospinal fluid biomarker panel for synaptic dysfunction in Alzheimer's disease
Nilsson, J., Gobom, J., Sjödin, S., Brinkmalm, G., Ashton, N. J., Svensson, J., Johansson, P., Portelius, E., Zetterberg, H., Blennow, K., et al. (2021) · Alzheimer's & Dementia: Diagnosis, Assessment & Disease Monitoring · doi:10.1002/dad2.12179 · Cited by 82 · see citing works
Self-citation
Synaptic vesicle protein 2A as a potential biomarker in synaptopathies
Heurling, K., Ashton, N. J., Leuzy, A., Zimmer, E. R., Blennow, K., Zetterberg, H., Eriksson, J., Lubberink, M., & Schöll, M. (2019) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2019.02.001 · Cited by 77 · see citing works
Self-citation
Multi-analyte proteomic analysis identifies blood-based neuroinflammation, cerebrovascular and synaptic biomarkers in preclinical Alzheimer’s disease
Zeng, X., Lafferty, T. K., Sehrawat, A., Chen, Y., Ferreira, P. C. L., Bellaver, B., Povala, G., Kamboh, M. I., Klunk, W. E., Cohen, A. D., et al. (2024) · Molecular Neurodegeneration · doi:10.1186/s13024-024-00753-5 · Cited by 87 · see citing works
CSF neurogranin as a neuronal damage marker in CJD: a comparative study with AD
Blennow, K., Lucena, D. D., Zetterberg, H., Villar‐Piqué, A., Karch, A., Vidal, E., Hermann, P., Schmitz, M., Ferrer, I., Zerr, I., et al. (2019) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2018-320155 · Cited by 75 · see citing works
Self-citation
A comprehensive systematic review of CSF proteins and peptides that define Alzheimer’s disease
Pedrero-Prieto, C. M., García‐Carpintero, S., Frontiñán-Rubio, J., Llanos-González, E., García, C. A., Alcain, F. J., Lindberg, I., Durán‐Prado, M., Peinado, J. R., & Rabanal‐Ruiz, Y. (2020) · Clinical Proteomics · doi:10.1186/s12014-020-09276-9 · Cited by 61 · see citing works
Neurexin 3 transmembrane and soluble isoform expression and splicing haplotype are associated with neuron inflammasome and Alzheimer’s disease
Hishimoto, A., Pletnikova, O., Lang, D. L., Troncoso, J. C., Egan, J. M., & Liu, Q.-R. (2019) · Alzheimer's Research & Therapy · doi:10.1186/s13195-019-0475-2 · Cited by 62 · see citing works
The Molecular and Neuropathological Consequences of Genetic Risk for Alzheimer's Dementia
Tasaki, S., Gaiteri, C., Mostafavi, S., Jager, P. L. D., & Bennett, D. A. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00699 · Cited by 58 · see citing works
Altered levels of CSF proteins in patients with FTD, presymptomatic mutation carriers and non-carriers
Remnestål, J., Öijerstedt, L., Ullgren, A., Olofsson, J., Bergström, S., Kultima, K., Ingelsson, M., Kilander, L., Uhlén, M., Månberg, A., et al. (2020) · Translational Neurodegeneration · doi:10.1186/s40035-020-00198-y · Cited by 56 · see citing works
Improved Differential Diagnosis of Alzheimer’s Disease by Integrating ELISA and Mass Spectrometry-Based Cerebrospinal Fluid Biomarkers
Khoonsari, P. E., Shevchenko, G., Herman, S., Remnestål, J., Giedraitis, V., Brundin, R., Gunnarsson, M. D., Kilander, L., Zetterberg, H., Nilsson, P., et al. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-180855 · Cited by 51 · see citing works
Self-citation
Neuropeptides in Alzheimer’s Disease: An Update
Petrella, C., Certo, M. G. D., Barbato, C., Gabanella, F., Ralli, M., Greco, A., Possenti, R., & Severini, C. (2019) · Current Alzheimer Research · doi:10.2174/1567205016666190503152555 · Cited by 53 · see citing works
Biomarkers of Dementia with Lewy Bodies: Differential Diagnostic with Alzheimer’s Disease
Bousiges, O., & Blanc, F. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126371 · Cited by 53 · see citing works
The Novel Omega-6 Fatty Acid Docosapentaenoic Acid Positively Modulates Brain Innate Immune Response for Resolving Neuroinflammation at Early and Late Stages of Humanized APOE-Based Alzheimer's Disease Models
Ma, Q., Zhu, C., Morselli, M., Su, T., Pelligrini, M., Lu, Z., Jones, M. R., Denver, P., Castro, D., Gu, X., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.558036 · Cited by 48 · see citing works
Exploring advancements in early detection of Alzheimer's disease with molecular assays and animal models
Sethi, P., Bhaskar, R., Singh, D. K. K., Gupta, S., Han, S. S., Avinash, D., Abomughaid, M. M., Koul, A., Rani, B., Ghosh, S., et al. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102411 · Cited by 43 · see citing works
Pathologically Decreased CSF Levels of Synaptic Marker NPTX2 in DLB Are Correlated with Levels of Alpha-Synuclein and VGF
Boiten, W., van Steenoven, I., Xiao, M.-F., Worley, P., Noli, B., Cocco, C., Ferri, G.-L., Lemstra, A., & Teunissen, C. (2020) · Cells · doi:10.3390/cells10010038 · Cited by 42 · see citing works
Self-citation
Shed CNTNAP2 ectodomain is detectable in CSF and regulates Ca2+ homeostasis and network synchrony via PMCA2/ATP2B2
Martin‐de‐Saavedra, M. D., Santos, M. D., Culotta, L., Varea, O., Spielman, B. P., Parnell, E., Forrest, M. P., Gao, R., Yoon, S., McCoig, E., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.11.025 · Cited by 46 · see citing works
VGF Peptides in Cerebrospinal Fluid of Patients with Dementia with Lewy Bodies
van Steenoven, I., Noli, B., Cocco, C., Ferri, G., Oeckl, P., Otto, M., Koel‐Simmelink, M. J. A., Bridel, C., van der Flier, W. M., Lemstra, A. W., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20194674 · Cited by 42 · see citing works
Self-citation
Quantitative proteomics of synaptosome <i>S</i>‐nitrosylation in Alzheimer’s disease
Wijasa, T. S., Sylvester, M., Brocke‐Ahmadinejad, N., Schwartz, S., Santarelli, F., Gieselmann, V., Klockgether, T., Brosseron, F., & Heneka, M. T. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.14870 · Cited by 41 · see citing works
Blood-brain barrier and innate immunity in the pathogenesis of Alzheimer's disease
Šimić, G., Španić, E., Horvat, L. L., & Hof, P. R. (2019) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2019.06.003 · Cited by 39 · see citing works
Structure, function, and pathology of Neurexin-3
Zhang, R., Jiang, H., Liu, Y., & He, G. (2022) · Genes & Diseases · doi:10.1016/j.gendis.2022.04.008 · Cited by 37 · see citing works
Finding memo: versatile interactions of the VPS10p-Domain receptors in Alzheimer’s disease
Salašová, A., Monti, G., Andersen, O. M., & Nykjær, A. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00576-2 · Cited by 35 · see citing works
A panel of CSF proteins separates genetic frontotemporal dementia from presymptomatic mutation carriers: a GENFI study
Bergström, S., Öijerstedt, L., Remnestål, J., Olofsson, J., Ullgren, A., Seelaar, H., Swieten, J. C. V., Synofzik, M., Sánchez‐Valle, R., Moreno, F., et al. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00499-4 · Cited by 36 · see citing works
VGF in Cerebrospinal Fluid Combined With Conventional Biomarkers Enhances Prediction of Conversion From MCI to AD
Llano, D. A., Devanarayan, P., & Devanarayan, V. (2019) · Alzheimer Disease & Associated Disorders · doi:10.1097/wad.0000000000000328 · Cited by 35 · see citing works
Omics-based Biomarkers for the Early Alzheimer Disease Diagnosis and Reliable Therapeutic Targets Development
Peña‐Bautista, C., Baquero, M., Vento, M., & Cháfer‐Pericás, C. (2018) · Current Neuropharmacology · doi:10.2174/1570159x16666180926123722 · Cited by 34 · see citing works
VGF: A prospective biomarker and therapeutic target for neuroendocrine and nervous system disorders
Wang, Y., Qin, X., Han, Y. J., & Li, B. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113099 · Cited by 33 · see citing works
Skull bone marrow and skull meninges channels: redefining the landscape of central nervous system immune surveillance
Liu, L., Zhang, X., Chai, Y., Zhang, J., Deng, Q., & Chen, X. (2025) · Cell Death and Disease · doi:10.1038/s41419-025-07336-2 · Cited by 32 · see citing works
The role of synaptic biomarkers in the spectrum of neurodegenerative diseases
Mazzucchi, S., Palermo, G., Campese, N., Galgani, A., Vecchia, A. D., Vergallo, A., Siciliano, G., Ceravolo, R., Hampel, H. J., & Baldacci, F. (2020) · Expert Review of Proteomics · doi:10.1080/14789450.2020.1831388 · Cited by 32 · see citing works
Systematic Review: microRNAs as Potential Biomarkers in Mild Cognitive Impairment Diagnosis
Ogonowski, N. S., Salcidua, S., León, T., Chamorro-Veloso, N., Valls, C., Avalos, C., Bisquertt, A., Rentería, M. E., Orellana, P., & Duran-Aniotz, C. A. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.807764 · Cited by 32 · see citing works
SWATH-MS analysis of cerebrospinal fluid to generate a robust battery of biomarkers for Alzheimer’s disease
Park, S. A., Jung, J. M., Park, J. S., Lee, J. H., Park, B., Kim, H. J., Park, J., Chae, W. S., Jeong, J. H., Choi, S. H., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-64461-y · Cited by 30 · see citing works
Multimodal data integration via mediation analysis with high‐dimensional exposures and mediators
Zhao, Y., Li, L., & Initiative, A. D. N. (2022) · Human Brain Mapping · doi:10.1002/hbm.25800 · Cited by 25 · see citing works
Long-Term DL-3-n-Butylphthalide Treatment Alleviates Cognitive Impairment Correlate With Improving Synaptic Plasticity in SAMP8 Mice
Lv, C., Ma, Q., Han, B., Li, J., Geng, Y., Zhang, X., & Wang, M. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00200 · Cited by 28 · see citing works
Chromogranin A in the early steps of the neurosecretory pathway
Laguerre, F., Anouar, Y., & Montero‐Hadjadje, M. (2019) · IUBMB Life · doi:10.1002/iub.2218 · Cited by 27 · see citing works
Has the time arrived for cerebrospinal fluid biomarkers in psychiatric disorders?
Lleó, A., Parnetti, L., Belbin, O., & Wiltfang, J. (2019) · Clinica Chimica Acta · doi:10.1016/j.cca.2019.01.019 · Cited by 26 · see citing works
Cerebrospinal fluid shotgun proteomics identifies distinct proteomic patterns in cerebral amyloid angiopathy rodent models and human patients
Vervuurt, M., Schrader, J. M., de Kort, A. M., Kersten, I., Wessels, H. J. C. T., Klijn, C. J. M., Schreuder, F. H. B. M., Kuiperij, H. B., Gloerich, J., Nostrand, W. E. V., et al. (2024) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01698-4 · Cited by 26 · see citing works
Complement C3aR signaling: Immune and metabolic modulation and its impact on Alzheimer's disease
Gedam, M., & Zheng, H. (2024) · European Journal of Immunology · doi:10.1002/eji.202350815 · Cited by 23 · see citing works
Synaptic Pruning in Alzheimer’s Disease: Role of the Complement System
Brucato, F. H., & Benjamin, D. E. (2020) · Global Journal of Medical Research · doi:10.34257/gjmrfvol20is6pg1 · Cited by 22 · see citing works
Risk Factors, Pathological Changes, and Potential Treatment of Diabetes‐Associated Cognitive Dysfunction
Meng, X., Du, H., Li, D., Guo, Y., Luo, P., Pan, L., Kan, R., Yu, P., Xiang, Y., Mao, B., et al. (2025) · Journal of Diabetes · doi:10.1111/1753-0407.70089 · Cited by 23 · see citing works
Endosomal-Lysosomal and Autophagy Pathway in Alzheimer’s Disease: A Systematic Review and Meta-Analysis
Krance, S. H., Wu, C., Chan, A. C. Y., Kwong, S., Song, B. X., Xiong, L. Y., Ouk, M., Chen, M. H., Zhang, J., Yung, A., et al. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-220360 · Cited by 25 · see citing works
Fluid‐based proteomics targeted on pathophysiological processes and pathologies in neurodegenerative diseases
Brinkmalm, A., Portelius, E., Brinkmalm, G., Pannee, J., Dahlén, R., Gobom, J., Blennow, K., & Zetterberg, H. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14594 · Cited by 21 · see citing works
Self-citation
Evaluation of cerebrospinal fluid levels of synaptic vesicle protein, VAMP-2, across the sporadic Alzheimer’s disease continuum
Goossens, J., González, A. C., Dewit, N., Lidón, L., Fortea, J., Alcolea, D. A., Lleó, A., Belbin, O., & Vanmechelen, E. (2023) · Alzheimer s Research & Therapy · doi:10.1186/s13195-023-01336-0 · Cited by 18 · see citing works
Alzheimer's Disease Biomarker Analysis Using Targeted Mass Spectrometry
Gobom, J., Brinkmalm, A., Brinkmalm, G., Blennow, K., & Zetterberg, H. (2024) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2024.100721 · Cited by 18 · see citing works
Self-citation
Peripheral transcriptomic biomarkers for early detection of sporadic Alzheimer disease?
Hadar, A., & Gurwitz, D. (2018) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2018.20.4/dgurwitz · Cited by 18 · see citing works
Association of CSF proteins with tau and amyloid β levels in asymptomatic 70-year-olds
Remnestål, J., Bergström, S., Olofsson, J., Sjöstedt, E., Uhlén, M., Blennow, K., Zetterberg, H., Zettergren, A., Kern, S., Skoog, I. G., et al. (2021) · Alzheimer s Research & Therapy · doi:10.1186/s13195-021-00789-5 · Cited by 16 · see citing works
Self-citation
Proteomics Landscape of Alzheimer’s Disease
Jain, A., & Sathe, G. J. (2021) · Proteomes · doi:10.3390/proteomes9010013 · Cited by 18 · see citing works
Nanoplasmonic immunosensor for the detection of SCG2, a candidate serum biomarker for the early diagnosis of neurodevelopmental disorder
Lim, S., Sung, Y.-J., Jo, N., Lee, N.-Y., Kim, K., Lee, D. Y., Kim, N.-S., Lee, J., Byun, J., Shin, Y., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-02262-7 · Cited by 17 · see citing works
Synaptic Proteins as Fluid Biomarkers in Alzheimer’s Disease: A Systematic Review and Meta-Analysis
Roveta, F., Cermelli, A., Boschi, S., Ferrandes, F., Grassini, A., Marcinnò, A., Spina, M., Rubino, E., Borsello, T., Vercelli, A., et al. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-220515 · Cited by 17 · see citing works
Dense core vesicle markers in CSF and cortical tissues of patients with Alzheimer’s disease
Barranco, N., Plá, V., Alcolea, D. A., Sánchez-Domínguez, I., Fischer‐Colbrie, R., Ferrer, I., Lleó, A., & Aguado, F. (2021) · Translational Neurodegeneration · doi:10.1186/s40035-021-00263-0 · Cited by 15 · see citing works
Probe-dependent Proximity Profiling (ProPPr) Uncovers Similarities and Differences in Phospho-Tau-Associated Proteomes Between Tauopathies
Morderer, D., Wren, M. C., Liu, F., Kouri, N., Maistrenko, A., Khalil, B., Pobitzer, N., Salemi, M., Phinney, B. S., Bu, G., et al. (2025) · Molecular Neurodegeneration · doi:10.1186/s13024-025-00817-0 · Cited by 19 · see citing works
Pathogenic tau induces an adaptive elevation in mRNA translation rate at early stages of disease
Zuniga, G., Katsumura, S., Mange, J. D., Ramirez, P., Atrian, F., Morita, M., & Frost, B. E. (2024) · Aging Cell · doi:10.1111/acel.14245 · Cited by 15 · see citing works
Pathophysiological subtypes of Alzheimer’s disease based on cerebrospinal fluid proteomicsPreprint
Tijms, B. M., Gobom, J., Reus, L. M., Jansen, I. E., Hong, S., Dobričić, V., Kilpert, F., ten Kate, M., Barkhof, F., Tsolaki, M., et al. (2020) · medRxiv · doi:10.1101/2020.03.25.20043158 · Cited by 14 · see citing works
Self-citation
Cerebrospinal fluid NPTX2 changes and relationship with regional brain metabolism metrics across mild cognitive impairment due to Alzheimer's disease
Massa, F., Martinuzzo, C., José, N. G. D. S., Pelagotti, V., Kreshpa, W., Abu‐Rumeileh, S., Barba, L., Mattioli, P., Orso, B., Brugnolo, A., et al. (2023) · Journal of Neurology · doi:10.1007/s00415-023-12154-7 · Cited by 13 · see citing works
Quantification of the trans-synaptic partners neurexin-neuroligin in CSF of neurodegenerative diseases by parallel reaction monitoring mass spectrometry
Camporesi, E., Nilsson, J., Vrillon, A., Cognat, E., Hourrègue, C., Zetterberg, H., Blennow, K., Becker, B., Brinkmalm, A., Paquet, C., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2021.103793 · Cited by 13 · see citing works
Self-citation
CSF proteomic signature predicts progression to Alzheimer's disease dementia
Vromen, E. M., del Campo, M., Scheltens, P., Teunissen, C. E., Visser, P. J., & Tijms, B. M. (2022) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1002/trc2.12240 · Cited by 11 · see citing works
Self-citation
Moyamoya disease: A human model for chronic hypoperfusion and intervention in Alzheimer's disease
Zou, X., Yuan, Y., Liao, Y., Jiang, C., Zhao, F., Ding, D., Gu, Y., Chen, L., Chu, Y., Hsu, Y., et al. (2022) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1002/trc2.12285 · Cited by 12 · see citing works
Translating Alzheimer’s Disease Mechanisms into Therapeutic Opportunities
Li, J., Wang, L., Zhang, X., Shi, J., Zhu, Y. Z., Wang, H., Zhu, X., Zhu, Q., & Luo, J. (2025) · Biomolecules · doi:10.3390/biom15091290 · Cited by 12 · see citing works
Using Proteomics to Understand Alzheimer’s Disease Pathogenesis
Drummond, E., & Wısnıewskı, T. (2019) · Codon Publications eBooks · doi:10.15586/alzheimersdisease.2019.ch3 · Cited by 12 · see citing works
Multiscale causal network models of Alzheimer’s disease identify VGF as a key regulator of diseasePreprint
Beckmann, N. D., Lin, W., Wang, M., Cohain, A. T., Wang, P., Ma, W., Wang, Y., Jiang, C. S., Audrain, M., Comella, P., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/458430 · Cited by 12 · see citing works
Shifting the balance: soluble ADAM10 as a potential treatment for Alzheimer's disease
Hershkovits, A. S., Gelley, S., Hanna, R., Kleifeld, O., Shulman, A., & Fishman, A. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1171123 · Cited by 12 · see citing works
Biological Significance of the Protein Changes Occurring in the Cerebrospinal Fluid of Alzheimer’s Disease Patients: Getting Clues from Proteomic Studies
Pedrero-Prieto, C. M., Frontiñán-Rubio, J., Alcain, F. J., Durán‐Prado, M., Peinado, J. R., & Rabanal‐Ruiz, Y. (2021) · Diagnostics · doi:10.3390/diagnostics11091655 · Cited by 12 · see citing works
Serial Cerebrospinal Fluid Sampling Reveals Trajectories of Potential Synaptic Biomarkers in Early Stages of Alzheimer’s Disease
Duits, F. H., Nilsson, J., Zetterberg, H., Blennow, K., van der Flier, W. M., Teunissen, C. E., & Brinkmalm, A. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-240610 · Cited by 10 · see citing works
Self-citation
Precision Medicine: Role of Biomarkers in Early Prediction and Diagnosis of Alzheimer’s Disease
Shen, L., Xia, S., Zhang, H., Yao, F., Liu, X., Zhao, Y., Ying, M., Iqbal, J., & Liu, Q. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.82035 · Cited by 10 · see citing works
Increased apolipoprotein E and decreased TNF‐α in the cerebrospinal fluid of nondemented APOE‐ε4 carriers
Sasayama, D., Hattori, K., Yokota, Y., Matsumura, R., Teraishi, T., Yoshida, S., & Kunugi, H. (2020) · Neuropsychopharmacology Reports · doi:10.1002/npr2.12110 · Cited by 10 · see citing works
Large-scale cerebrospinal fluid proteomic analysis in Alzheimer’s disease patients reveals five molecular subtypes with distinct genetic risk profiles
Tijms, B. M., Vromen, E. M., Mjaavatten, O., Holstege, H., Reus, L. M., van der Lee, S., Wesenhagen, K. E., Lorenzini, L., Vermunt, L., Venkatraghavan, V., et al. (2023) · doi:10.1101/2023.05.10.23289793 · Cited by 10 · see citing works
Self-citation
Proteomic analysis of the human hippocampus identifies neuronal pentraxin 1 ( NPTX1 ) as synapto‐axonal target in late‐stage Parkinson's disease
Arias, C. C. W. P., Silbern, I., Gomes, L. C., Wartmann, H., Dambeck, V., Fanz, J., Neuenroth, L., Bähr, M., Outeiro, T. F., Bonn, S., et al. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15924 · Cited by 9 · see citing works
Cerebrospinal Fluid Panel of Synaptic Proteins in Cerebral Amyloid Angiopathy and Alzheimer’s Disease
van den Berg, E., Nilsson, J., Kersten, I., Brinkmalm, G., de Kort, A. M., Klijn, C. J. M., Schreuder, F. H. B. M., Jäkel, L., Gobom, J., Portelius, E., et al. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-220977 · Cited by 8 · see citing works
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14-3-3 $$\upzeta /\updelta$$-reported early synaptic injury in Alzheimer’s disease is independently mediated by sTREM2
Woo, M. S., Nilsson, J., Therriault, J., Rahmouni, N., Brinkmalm, A., Benedet, A. L., Ashton, N. J., Macedo, A. C., Servaes, S., Wang, Y.-T., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02962-z · Cited by 8 · see citing works
Self-citation
FastCAT Accelerates Absolute Quantification of Proteins Using Multiple Short Nonpurified Chimeric Standards
Rzagalinski, I., Bogdanova, A. I., Raghuraman, B. K., Geertsma, E. R., Hersemann, L., Ziemssen, T., & Shevchenko, A. (2022) · Journal of Proteome Research · doi:10.1021/acs.jproteome.2c00014 · Cited by 7 · see citing works
Cerebrospinal fluid VGF is associated with the onset and progression of Alzheimer's disease
Lu, Y., Li, D., Yu, Y., Wang, Q., Li, A., Quan, Y., Xing, Y., & Initiative, A. D. N. (2025) · Journal of Alzheimer s Disease · doi:10.1177/13872877251323002 · Cited by 8 · see citing works
Identifying the joint signature of brain atrophy and gene variant scores in Alzheimer’s Disease
Cruciani, F., Aparo, A., Brusini, L., Combi, C., Storti, S. F., Giugno, R., Menegaz, G., & Galazzo, I. B. (2023) · Journal of Biomedical Informatics · doi:10.1016/j.jbi.2023.104569 · Cited by 8 · see citing works
Association of region‐specific hippocampal reduction of neurogranin with inflammasome proteins in post mortem brains of Alzheimer's disease
Vontell, R., Gober, R., Dallmeier, J., Brzostowicki, D. J., Barreda, A., Blennow, K., Zetterberg, H., Kvartsberg, H., Gultekin, S. H., Vaccari, J. P. D. R., et al. (2024) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1002/trc2.12444 · Cited by 7 · see citing works
Self-citation
Cognitive Resilience in Preclinical Alzheimer's Disease: Higher Nptx2 and Vgf Levels are Associated with Reduced Cognitive Decline
Anderson, C. L., Gross, A. L., Pettigrew, C. A., Vazquez, J. P., Moghekar, A., Oh, S., Na, C. H., Albert, M., Worley, P. F., & Soldan, A. (2025) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2025.09.002 · Cited by 7 · see citing works
CSF-Targeted Proteomics Indicate Amyloid-Beta Ratios in Patients with Alzheimer’s Dementia Spectrum
Behzad, M., Zirak, N., Madani, G. H., Baidoo, L., Rezaei, A., Karbasi, S., Sadeghi, M. R., Shafie, M., Mayeli, M., & Initiative, A. D. N. (2023) · International Journal of Alzheimer s Disease · doi:10.1155/2023/5336273 · Cited by 7 · see citing works
Diagnostic value of CSF chromogranin A to discriminate between Alzheimer's disease and dementia with Lewy bodies
Bousiges, O., Lavaux, T., Demuynck, C., Schaeffer‐Agalède, C., Philippi, N., Muller, C., Cretin, B., & Blanc, F. (2024) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12961 · Cited by 6 · see citing works
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Barba, L., Bellomo, G., Oeckl, P., Chiasserini, D., Gaetani, L., Torrigiani, E. G., Paoletti, F. P., Steinacker, P., Abu‐Rumeileh, S., Parnetti, L., et al. (2024) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2024.123059 · Cited by 6 · see citing works
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Chowdhury, U. N., Islam, M. B., Ahmad, S., & Moni, M. A. (2020) · Informatics in Medicine Unlocked · doi:10.1016/j.imu.2020.100439 · Cited by 6 · see citing works
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Colín-Martínez, E., & Arias, C. (2024) · Reviews in the Neurosciences · doi:10.1515/revneuro-2024-0110 · Cited by 5 · see citing works
Transcriptome Signatures for Cognitive Resilience Among Individuals with Pathologically Confirmed Alzheimer Disease
Li, D., Han, X., Farrer, L. A., Stein, T. D., & Jun, G. (2024) · Alzheimer s & Dementia · doi:10.1002/alz.090972 · Cited by 5 · see citing works
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Wu, C., Ruan, T., Yuan, Y., Xu, C., Du, L., Wang, F., & Xu, S. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-240123 · Cited by 5 · see citing works
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de Geus, M. B., Nairn, A. C., Arnold, S. E., & Carlyle, B. C. (2025) · Brain Communications · doi:10.1093/braincomms/fcaf202 · Cited by 3 · see citing works
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Dai, L., Kirsebom, B., Wang, C., Zhang, M., Wang, Q., Ni, M., González‐Ortiz, F., Blennow, K., Shi, J., Fladby, T., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-70472-6 · Cited by 3 · see citing works
Self-citation
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Nassar, A., Nampoothiri, M., Gurram, P. C., Satarker, S., Upadhya, D., Shamabhat, G., & Mahammad, F. S. (2023) · Journal of Applied Pharmaceutical Science · doi:10.7324/japs.2023.152245 · Cited by 3 · see citing works
Integrated Proteomics Identifies Neuritin (NRN1) as a Mediator of Cognitive Resilience to Alzheimer’s DiseasePreprint
Hurst, C. D., Pugh, D. A., Abreha, M. H., Duong, D. M., Dammer, E. B., Bennett, D. A., Herskowitz, J. H., & Seyfried, N. T. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.15.496285 · Cited by 3 · see citing works
Heterogeneity of cerebral atrophic rate in mild cognitive impairment and its interactive association with proteins related to microglia activity on longitudinal cognitive changes
Tang, J., Cao, Z., Lei, M., Yu, Q., Mai, Y., Xu, J., Liao, W., Ruan, Y., Shi, L., Yang, L., et al. (2024) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2024.105582 · Cited by 2 · see citing works

O3‐14‐06: DISSECTION OF SYNAPTIC PATHWAYS THROUGH THE ANALYSIS OF BIOMARKERS IN THE CSF: A COMBINING TOOL FOR THE DIAGNOSIS OF ALZHEIMER'S DISEASE
Tible, M., Persson, A., Höglund, K., Brinkmalm, A., Cognat, E., Hugon, J., Dumurgier, J., Zetterberg, H., Paquet, C., & Blennow, K. (2018) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2018.06.2854
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Simonsen, A. H., Danborg, P. B., Bourbouli, M., Kapaki, E. N., & Waldemar, G. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2014.05.774
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Simonsen, A., Mcguire, J., Hansson, O., Zetterberg, H., Podust, V., Davies, H., Waldemar, G., Minthon, L., & Blennow, K. (2007) · Archives of Neurology · doi:10.1001/archneur.64.3.366 · Cited by 151 · see citing works
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Begcevic, I., Brinc, D., Brown, M., Martinez-Morillo, E., Goldhardt, O., Grimmer, T., Magdolen, V., Batruch, I., & Diamandis, E. P. (2018) · Journal of Proteomics · doi:10.1016/j.jprot.2018.04.027 · Cited by 81 · see citing works
Multi‐cohort profiling reveals elevated CSF levels of brain‐enriched proteins in Alzheimer’s disease
Bergström, S., Remnestål, J., Yousef, J., Olofsson, J., Markaki, I., Carvalho, S., Corvol, J., Kultima, K., Kilander, L., Löwenmark, M., et al. (2021) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51402 · Cited by 48 · see citing works
Self-citation

Authors: Duits, F. H., Brinkmalm, G., Teunissen, C. E., Brinkmalm, A., Scheltens, P., Van der Flier, W. M., Zetterberg, H., & Blennow, K.
Affiliations: Amsterdam Neuroscience (NL)
Sahlgrenska University Hospital (SE)
Corresponding author: Duits, Flora H.
ORCID: Duits, Flora H.
Brinkmalm, Gunnar
Teunissen, Charlotte E.
Brinkmalm, Ann
Scheltens, Philip
Zetterberg, Henrik
Blennow, Kaj
Venue: Alzheimer's Research & Therapy
Publisher: Springer Science and Business Media LLC
Published: 2018-01-15
Volume: 10
Issue: 1
Pages: 5-5
ISSN: 1758-9193 (ISSN-L)
DOI: 10.1186/s13195-017-0335-x
PMC: PMC6389073
OpenAlex: W2796923525
Cited by: 137
References: 50
Citations by year: 2026: 7 · 2025: 8 · 2024: 22 · 2023: 12 · 2022: 15 · 2021: 30 · 2020: 19 · 2019: 18 · 2018: 6
FWCI: 14.56
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Alzheimer s Research & Therapy (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
Pure Amsterdam UMC (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
UCL Discovery (University College London) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders: Alzheimer Nederland (WE.15-2013-08)
Swedish research council
European Research Council
Åhlén-stiftelsen
Swedish state support for clinical research
Hjärnfonden
Swedish alzheimer foundation
Knut och Alice Wallenbergs Stiftelse
Torsten Söderbergs Stiftelse
Frimurarestiftelsen
Stiftelsen för Gamla Tjänarinnor
Gun och Bertil Stohnes Stiftelse
Magnus Bergvalls Stiftelse
Stichting Dioraphte
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
Keywords: prodromal Alzheimer's disease, mild cognitive impairment, cerebrospinal fluid biomarkers, synaptic proteins, chromogranin A, secretogranin II, NRXN3, VGF, vesicle trafficking, synapse stability, disease progression, prognosis
MeSH terms: Mental Status and Dementia Tests, Aged, Alzheimer Disease, Apolipoproteins E, Female, Follow-Up Studies, Humans, Male, Middle Aged, Nerve Tissue Proteins, Peptide Fragments, Phosphorylation, Prognosis, Mass Spectrometry, Synapses, Biomarkers, Amyloid beta-Peptides, tau Proteins, Cognitive Dysfunction, Prodromal Symptoms

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Synaptic proteins in CSF as potential novel biomarkers for prognosis in prodromal Alzheimer’s disease

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