Differential impairment of cerebrospinal fluid synaptic biomarkers in the genetic forms of frontotemporal dementia
Open accessAbstract
Background: Approximately a third of frontotemporal dementia (FTD) is genetic with mutations in three genes accounting for most of the inheritance: C9orf72 , GRN , and MAPT . Impaired synaptic health is a common mechanism in all three genetic variants, so developing fluid biomarkers of this process could be useful as a readout of cellular dysfunction within therapeutic trials. Methods: A total of 193 cerebrospinal fluid (CSF) samples from the GENetic FTD Initiative including 77 presymptomatic (31 C9orf72 , 23 GRN , 23 MAPT ) and 55 symptomatic (26 C9orf72 , 17 GRN , 12 MAPT ) mutation carriers as well as 61 mutation-negative controls were measured using a microflow LC PRM-MS set-up targeting 15 synaptic proteins: AP-2 complex subunit beta, complexin-2, beta-synuclein, gamma-synuclein, 14–3-3 proteins (eta, epsilon, zeta/delta), neurogranin, Rab GDP dissociation inhibitor alpha (Rab GDI alpha), syntaxin-1B, syntaxin-7, phosphatidylethanolamine-binding protein 1 (PEBP-1), neuronal pentraxin receptor (NPTXR), neuronal pentraxin 1 (NPTX1), and neuronal pentraxin 2 (NPTX2). Mutation carrier groups were compared to each other and to controls using a bootstrapped linear regression model, adjusting for age and sex. Results: CSF levels of eight proteins were increased only in symptomatic MAPT mutation carriers (compared with controls) and not in symptomatic C9orf72 or GRN mutation carriers: beta-synuclein, gamma-synuclein, 14–3-3-eta, neurogranin, Rab GDI alpha, syntaxin-1B, syntaxin-7, and PEBP-1, with three other proteins increased in MAPT mutation carriers compared with the other genetic groups (AP-2 complex subunit beta, complexin-2, and 14–3-3 zeta/delta). In contrast, CSF NPTX1 and NPTX2 levels were affected in all three genetic groups (decreased compared with controls), with NPTXR concentrations being affected in C9orf72 and GRN mutation carriers only (decreased compared with controls). No changes were seen in the CSF levels of these proteins in presymptomatic mutation carriers. Concentrations of the neuronal pentraxins were correlated with brain volumes in the presymptomatic period for the C9orf72 and GRN groups, suggesting that they become abnormal in proximity to symptom onset. Conclusions: Differential synaptic impairment is seen in the genetic forms of FTD, with abnormalities in multiple measures in those with MAPT mutations, but only changes in neuronal pentraxins within the GRN and C9orf72 mutation groups. Such markers may be useful in future trials as measures of synaptic dysfunction, but further work is needed to understand how these markers change throughout the course of the disease.
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Strong associations can be found between some synaptic proteins but not all, and synaptic biomarkers have been reported to lack correlation with CSF neurofilament light levels.
“The diversity of synaptic pathology across several neurodegenerative dementia is further reflected by the fact that strong associations can be found between some synaptic proteins but not all, as well as the reported lack of correlation of synaptic biomarkers with CSF neurofilament light (NfL) levels [1, 9–11].”
The observation that no synaptic proteins were associated with CSF NfL in any clinical group is concurrent with data from other recent cohorts.
“Of particular note is the evidence that no synaptic proteins were not associated with CSF NfL in any clinical group, concurrent with data from other recent cohorts [1, 9, 29].”
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- Authors
- Sogorb-Esteve, A., Nilsson, J., Swift, I. J., Heller, C., Bocchetta, M., Russell, L. L., Peakman, G., Convery, R. S., van Swieten, J. C., Seelaar, H., Borroni, B., Galimberti, D., Sanchez-Valle, R., Laforce, R., Moreno, F., Synofzik, M., Graff, C., Masellis, M., Tartaglia, M. C., Rowe, J. B., Vandenberghe, R., Finger, E., Tagliavini, F., Santana, I., Butler, C. R., Ducharme, S., Gerhard, A., Danek, A., Levin, J., Otto, M., Sorbi, S., Le Ber, I., Pasquier, F., Gobom, J., Brinkmalm, A., Blennow, K., Zetterberg, H., Rohrer, J. D., Initiative, O. B. O. T. G. F., Nelson, A., Bouzigues, A., Greaves, C. V., Cash, D., Thomas, D. L., Todd, E., Benotmane, H., Nicholas, J., Samra, K., Shafei, R., Timberlake, C., Cope, T., Rittman, T., Benussi, A., Premi, E., Gasparotti, R., Archetti, S., Gazzina, S., Cantoni, V., Arighi, A., Fenoglio, C., Scarpini, E., Fumagalli, G., Borracci, V., Rossi, G., Giaccone, G., Di Fede, G., Caroppo, P., Tiraboschi, P., Prioni, S., Redaelli, V., Tang-Wai, D., Rogaeva, E., Castelo-Branco, M., Freedman, M., Keren, R., Black, S., Mitchell, S., Shoesmith, C., Bartha, R., Rademakers, R., Poos, J., Papma, J. M., Giannini, L., van Minkelen, R., Pijnenburg, Y., Nacmias, B., Ferrari, C., Polito, C., Lombardi, G., Bessi, V., Veldsman, M., Andersson, C., Thonberg, H., Öijerstedt, L., Jelic, V., Thompson, P., Langheinrich, T., Lladó, A., Antonell, A., Olives, J., Balasa, M., Bargalló, N., Borrego-Ecija, S., de Mendonça, A., Verdelho, A., Maruta, C., Ferreira, C. B., Miltenberger, G., do Couto, F. S., Gabilondo, A., Gorostidi, A., Villanua, J., Cañada, M., Tainta, M., Zulaica, M., Barandiaran, M., Alves, P., Bender, B., Wilke, C., Graf, L., Vogels, A., Vandenbulcke, M., Van Damme, P., Bruffaerts, R., Poesen, K., Rosa-Neto, P., Gauthier, S., Camuzat, A., Brice, A., Bertrand, A., Funkiewiez, A., Rinaldi, D., Saracino, D., Colliot, O., Sayah, S., Prix, C., Wlasich, E., Wagemann, O., Loosli, S., Schönecker, S., Hoegen, T., Lombardi, J., Anderl-Straub, S., Rollin, A., Kuchcinski, G., Bertoux, M., Lebouvier, T., Deramecourt, V., Santiago, B., Duro, D., Leitão, M. J., Almeida, M. R., Tábuas-Pereira, M., & Afonso, S.
- Affiliations
- University of Gothenburg (SE)
- UK Dementia Research Institute (GB)
- UCL Queen Square Institute of Neurology (GB)
- Erasmus MC (NL)
- University of Brescia (IT)
- University of Milan (IT)
- Centre hospitalier universitaire de Québec (CA)
- German Center for Neurodegenerative Diseases (DE)
- Karolinska University Hospital (SE)
- Sunnybrook Health Science Centre (CA)
- University of Toronto (CA)
- MRC Cognition and Brain Sciences Unit (GB)
- Universitair Ziekenhuis Leuven (BE)
- Western University (CA)
- Fondazione IRCCS Istituto Neurologico Carlo Besta (IT)
- Unidade Local de Saúde de Coimbra (PT)
- Montreal Neurological Institute and Hospital (CA)
- University of Manchester (GB)
- Ludwig-Maximilians-Universität München (DE)
- Universität Ulm (DE)
- Don Carlo Gnocchi Foundation (IT)
- Inserm (FR)
- Sahlgrenska University Hospital (SE)
- Centro de Neurociências e Biologia Celular (PT)
- Munich Cluster for Systems Neurology (DE)
- Corresponding author
- Rohrer, Jonathan D.
- ORCID
- Nilsson, Johanna
- Swift, Imogen J.
- Heller, Carolin
- Bocchetta, Martina
- Russell, Lucy L.
- Peakman, Georgia
- Convery, Rhian S.
- Seelaar, Harro
- Borroni, Barbara
- Galimberti, Daniela
- Laforce, Robert
- Synofzik, Matthis
- Graff, Caroline
- Masellis, Mario
- Tartaglia, Maria Carmela
- Rowe, James B.
- Vandenberghe, Rik
- Finger, Elizabeth
- Tagliavini, Fabrizio
- Santana, Isabel
- Ducharme, Simon
- Gerhard, Alexander
- Danek, Adrian
- Levin, Johannes
- Otto, Markus
- Sorbi, Sandro
- Pasquier, Florence
- Gobom, Johan
- Brinkmalm, Ann
- Blennow, Kaj
- Zetterberg, Henrik
- Rohrer, Jonathan D.
- Bouzigues, Arabella
- Greaves, Caroline V
- Cash, David
- Thomas, David L
- Todd, Emily
- Nicholas, Jennifer
- Samra, Kiran
- Shafei, Rachelle
- Cope, Thomas
- Rittman, Timothy
- Benussi, Alberto
- Premi, Enrico
- Gasparotti, Roberto
- Gazzina, Stefano
- Cantoni, Valentina
- Arighi, Andrea
- Fenoglio, Chiara
- Fumagalli, Giorgio
- Borracci, Vittoria
- Rossi, Giacomina
- Giaccone, Giorgio
- Caroppo, Paola
- Tiraboschi, Pietro
- Prioni, Sara
- Redaelli, Veronica
- Rogaeva, Ekaterina
- Castelo-Branco, Miguel
- Freedman, Morris
- Keren, Ron
- Black, Sandra
- Shoesmith, Christen
- Rademakers, Rosa
- Poos, Jackie
- Papma, Janne M.
- Giannini, Lucia
- Pijnenburg, Yolande
- Nacmias, Benedetta
- Ferrari, Camilla
- Polito, Cristina
- Lombardi, Gemma
- Bessi, Valentina
- Veldsman, Michele
- Öijerstedt, Linn
- Thompson, Paul
- Langheinrich, Tobias
- Lladó, Albert
- Antonell, Anna
- Olives, Jaume
- Balasa, Mircea
- Verdelho, Ana
- Maruta, Carolina
- Ferreira, Catarina B.
- Gabilondo, Alazne
- Gorostidi, Ana
- Tainta, Mikel
- Zulaica, Miren
- Bender, Benjamin
- Wilke, Carlo
- Graf, Lisa
- Vogels, Annick
- Vandenbulcke, Mathieu
- Bruffaerts, Rose
- Poesen, Koen
- Gauthier, Serge
- Brice, Alexis
- Bertrand, Anne
- Saracino, Dario
- Colliot, Olivier
- Sayah, Sabrina
- Prix, Catharina
- Wlasich, Elisabeth
- Wagemann, Olivia
- Loosli, Sandra
- Schönecker, Sonja
- Lombardi, Jolina
- Bertoux, Maxime
- Lebouvier, Thibaud
- Deramecourt, Vincent
- Santiago, Beatriz
- Duro, Diana
- Leitão, Maria João
- Venue
- Alzheimer's Research & Therapy
- Published
- 2022-08-31
- Volume
- 14
- Issue
- 1
- Pages
- 118-118
- ISSN
- 1758-9193 (ISSN-L)
- PMC
- PMC9429339
- OpenAlex
- W4293771139
- Cited by
- 39
- References
- 53
- Citations by year
- 2026: 10 · 2025: 12 · 2024: 10 · 2023: 6 · 2022: 1
- FWCI
- 3.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Alzheimer s Research & Therapy (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, cc-by)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion, cc-by)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion, cc-by)
- Florence Research (University of Florence) (submittedVersion, other-oa)
- Iris (University of Trento) (submittedVersion, cc-by)
- Lirias (KU Leuven) (submittedVersion, other-oa)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, cc-by)
- HAL (submittedVersion, cc-by)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Brunel University Research Archive (BURA) (Brunel University London) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion, cc-by)
- Institutional Research Information System (Università degli Studi di Brescia) (submittedVersion)
- mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion, other-oa)
- Scholarship@Western (Western University) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Alzheimer's Association (ADSF-21-831377-C, 21-831376 -C, ADSF‐21‐831376‐C, #ADSF-21-831381-C, -21-831381-C, ADSF-21-831376-C, #ADSF-21-831381, -21- 831377-C)
- Alzheimer's Drug Discovery Foundation (2016862, 201809, ADSF-21-831381-C, 201809–2016862, ADSF-21-831377-C, 860197, JPND2021-00694, #ADSF-21-831376-C)
- Familjen Erling-Perssons Stiftelse (ADSF-21-831377-C, FO2019-0228, #ADSF-21-831381-C, 860197, #201809-2016862, JPND2021-00694, ADSF-21-831376-C)
- McGill University
- Wellcome Trust (220258/Z/20/Z)
- Stiftelsen för Gamla Tjänarinnor (JPND2021-00694, 860197, FO2019‐0228)
- Sunnybrook Research Institute
- Università degli Studi di Milano
- Weston Brain Institute
- EU Joint Programme – Neurodegenerative Disease Research (JPND 2021-00694, 733 051 042, 529-2014-7504, 2019-02248, 739510, RCN 290173, 02248)
- Brain Research UK (202021-32)
- Université de Lille
- National Brain Appeal (290173, RCN 290173)
- Alzheimer's Society (MR/M008525/1)
- National Institute for Health and Care Research (BRC1215-20014, BRC149/NS/MH, CL-2018-14-007)
- University of Cambridge (BRC-1215-20014)
- Imperial College London
- University of Oxford
- European Commission (ADSF-21-831377-C, 739510, ADSF-21-831381-C, 201809-2016862, JPND2021‐00694, HORIZON2020, 860197, ADSF-21-831376-C)
- Wolfson Foundation (20143810)
- Agence Nationale de la Recherche (ANR-11-LABX-0009)
- Institut National de la Santé et de la Recherche Médicale
- ZonMw (733 051 042, 739510, 20143810)
- Eberhard Karls Universität Tübingen
- Bundesministerium für Bildung und Forschung (739510)
- Cambridge University Hospitals
- Ministero della Salute (2018-, 733 051 042, 739510, No 739510, BRC-1215-20014)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (20014, HCMI 056–13-018, 056-13-018)
- University of Toronto
- Hjärnfonden (JPND2021-00694, 860197, FO2019‐0228)
- KU Leuven
- Stockholms Läns Landsting
- Vetenskapsrådet (Dnr 529-2014-7504, ADSF-21-831377-C, 860197, ADSF-21-831376-C, 2019-02248, 529-2014-7504, 201809-2016862, 681712, BRC-1215-20014, 02532, 2018-, ALFGBG-720931, 2015-02926, #ADSF-21-831381-C, 2018-02532, JPND2021-00694, 2018-02754)
- Università degli Studi di Firenze
- Centre National de la Recherche Scientifique
- Deutsches Zentrum für Neurodegenerative Erkrankungen
- Universidade de Coimbra
- Sahlgrenska Universitetssjukhuset
- Göteborgs Universitet
- Fondazione I.R.C.C.S. Istituto Neurologico Carlo Besta
- Universität Duisburg-Essen
- Universität Ulm
- Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico
- Stichting Dioraphte (09-02-03-00)
- Alzheimer Nederland
- Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (ARUK-CRF2017B-2)
- UK Dementia Research Institute
- Sorbonne Université
- Olav Thon Stiftelsen (#FO2019-0228)
- Canadian Institutes of Health Research (BRC-1215-20014, 201809, 20143810, 327387)
- Medical Research Council (MR/M023664/1, SUAG/051 G101400, ARUK-CRF2017B-2, G101400, MR/T046015/1, MR/M008525/1, MR/K010395/1, BRC-1215-20014)
- Sahlgrenska Akademin
- NIHR Cambridge Biomedical Research Centre ((BRC-1215-20014), 1215-20014, BRC-1215, BRC149/NS/MH, 220258)
- H2020 European Research Council (681712)
- Topics
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- frontotemporal dementia, genetic frontotemporal dementia, cerebrospinal fluid biomarkers, synaptic dysfunction, C9orf72, gene regulatory networks, MAPT, presymptomatic mutation carriers, neurogranin, beta-synuclein, gamma-synuclein, 14-3-3 proteins, syntaxin
- MeSH terms
- C9orf72 Protein, Humans, Mutation, Biomarkers, tau Proteins, Syntaxin 1, Neurogranin, gamma-Synuclein, beta-Synuclein, Frontotemporal Dementia
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