Targeted Proteomics upon Treatment with Tofersen Identifies Novel Response Markers for Superoxide Dismutase 1-Linked Amyotrophic Lateral Sclerosis

Research output: Contribution to journal › Research article › Contributed › peer-review

Contributors

  • Christina Steffke - , Ulm University (Author)
  • Karthik Baskar - , Ulm University (Author)
  • Franziska Bachhuber - , Ulm University (Author)
  • Maximilian Wiesenfarth - , Ulm University (Author)
  • Johannes Dorst - , Ulm University (Author)
  • Joachim Schuster - , Ulm University, German Center for Neurodegenerative Diseases (DZNE) (Author)
  • Florian Schöberl - , Ludwig Maximilian University of Munich (Author)
  • Peter Reilich - , Ludwig Maximilian University of Munich (Author)
  • Martin Regensburger - , Friedrich-Alexander University Erlangen-Nürnberg (Author)
  • Alexander German - , Friedrich-Alexander University Erlangen-Nürnberg (Author)
  • René Günther - , Department of Neurology, University Hospital Carl Gustav Carus Dresden, German Center for Neurodegenerative Diseases (DZNE) - Partner Site Dresden (Author)
  • Maximilian Vidovic - , Department of Neurology, University Hospital Carl Gustav Carus Dresden (Author)
  • Susanne Petri - , Hannover Medical School (MHH) (Author)
  • Thomas Meyer - , Berlin Institute of Health at Charité (Author)
  • Tim Hagenacker - , University Hospital Essen (Author)
  • Julian Grosskreutz - , University of Lübeck (Author)
  • Ute Weyen - , Ruhr University Bochum (Author)
  • Patrick Weydt - , University of Bonn, German Center for Neurodegenerative Diseases (DZNE) (Author)
  • Thomas Haarmeier - , Helios Hospital Group (Author)
  • Paul Lingor - , Klinikum Rechts der Isar (MRI TUM), German Center for Neurodegenerative Diseases (DZNE), Munich Cluster for Systems Neurology (SyNergy) (Author)
  • Joachim Wolf - , Diakonissenhospital Flensburg (Author)
  • Andreas Hermann - , University of Rostock, German Center for Neurodegenerative Diseases (DZNE) (Author)
  • Johannes Prudlo - , German Center for Neurodegenerative Diseases (DZNE), University of Rostock (Author)
  • Kornelia Günther - , Ulm University (Author)
  • Antje Knehr - , Ulm University (Author)
  • Zeynep Elmas - , Ulm University (Author)
  • Zeljko Uzelac - , Ulm University (Author)
  • Simon Witzel - , Ulm University (Author)
  • Wolfgang Philipp Ruf - , Ulm University, German Center for Neurodegenerative Diseases (DZNE) (Author)
  • Axel Freischmidt - , Ulm University (Author)
  • Ritchie Ho - , Cedars-Sinai Medical Center (Author)
  • Albert C. Ludolph - , Ulm University, German Center for Neurodegenerative Diseases (DZNE) (Author)
  • Jochen H. Weishaupt - , Ulm University, Heidelberg University  (Author)
  • Hayrettin Tumani - , Ulm University, German Center for Neurodegenerative Diseases (DZNE) (Author)
  • Patrick Oeckl - , Ulm University, German Center for Neurodegenerative Diseases (DZNE) (Author)
  • David Brenner - , Ulm University, German Center for Neurodegenerative Diseases (DZNE) (Author)
  • Alberto Catanese - , Ulm University, German Center for Neurodegenerative Diseases (DZNE), University of Freiburg (Author)

Abstract

Objective: Tofersen is the first effective and approved therapy for superoxide dismutase 1 (SOD1)-associated amyotrophic lateral sclerosis (ALS [SOD1-ALS]). Following treatment with tofersen, neurofilament levels in patients' cerebrospinal fluid (CSF) and serum seem to respond earlier than clinical parameters. This evidence prompted us to hypothesize that this novel treatment could provide an opportunity to identify additional biomarkers responsive to therapy in SOD1-ALS. Methods: We investigated a panel of 120 neural, glial, and inflammatory markers in CSF and serum samples longitudinally collected from a total of 28 SOD1-ALS patients at baseline, and after 3, 6 and 12 months of treatment with tofersen, followed by validation with conventional methodology. Results: We identified a set of proteins, including neurofilament light chain, neurofilament heavy chain, amyloid-beta 1–40 and amyloid-beta 1–42, neuropeptide Y (NPY), and ubiquitin C-terminal hydrolase L1 (UCHL1), whose CSF levels both differed between SOD1-ALS and the control group, and were responsive to tofersen at 3 and 6 months after treatment initiation. Another group of markers, including the neuropentraxin (NPTX) family members NPTX1, NPTX2 and NPTXR, did not separate untreated SOD1-ALS from controls, but was responsive to tofersen. At 12 months on tofersen the levels of neurofilament light chain, neurofilament heavy chain, NPTX1, NPTX2, and NPTXR remained reduced compared with baseline, and correlated with the clinical response to tofersen. Consistent with increasing CSF pleocytosis and intrathecal immunoglobulin production, inflammatory markers were significantly increased after 12 months of treatment. Interpretation: Our results highlight a complex, time-dependent differential response of CSF biomarkers to tofersen treatment, and may pave the way for developing a panel of responsive proteins to make biomarker endpoints more robust in clinical trials for SOD1-ALS and beyond. ANN NEUROL 2025;98:1318–1334.

Details

Original languageEnglish
Pages (from-to)1318-1334
Number of pages17
JournalAnnals of neurology
Volume98
Issue number6
Publication statusPublished - Dec 2025
Peer-reviewedYes

External IDs

PubMed 40781905

Keywords

ASJC Scopus subject areas