Polyglutamine-Expanded Ataxin-3: A Target Engagement Marker for Spinocerebellar Ataxia Type 3 in Peripheral Blood.

ataxin-3; Machado-Joseph disease; spinocerebellar ataxia type 3; singulex technology; target engagement biomarker

Journal

Movement disorders : official journal of the Movement Disorder Society
ISSN: 1531-8257
Titre abrégé: Mov Disord
Pays: United States
ID NLM: 8610688

Informations de publication

Date de publication:
11 2021
Historique:
revised: 27 06 2021
received: 14 04 2021
accepted: 21 07 2021
pubmed: 17 8 2021
medline: 17 3 2022
entrez: 16 8 2021
Statut: ppublish

Résumé

Spinocerebellar ataxia type 3 is a rare neurodegenerative disease caused by a CAG repeat expansion in the ataxin-3 gene. Although no curative therapy is yet available, preclinical gene-silencing approaches to reduce polyglutamine (polyQ) toxicity demonstrate promising results. In view of upcoming clinical trials, quantitative and easily accessible molecular markers are of critical importance as pharmacodynamic and particularly as target engagement markers. We aimed at developing an ultrasensitive immunoassay to measure specifically polyQ-expanded ataxin-3 in plasma and cerebrospinal fluid (CSF). Using the novel single molecule counting ataxin-3 immunoassay, we analyzed cross-sectional and longitudinal patient biomaterials. Statistical analyses revealed a correlation with clinical parameters and a stability of polyQ-expanded ataxin-3 during conversion from the pre-ataxic to the ataxic phases. The novel immunoassay is able to quantify polyQ-expanded ataxin-3 in plasma and CSF, whereas ataxin-3 levels in plasma correlate with disease severity. Longitudinal analyses demonstrated a high stability of polyQ-expanded ataxin-3 over a short period. © 2021 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Sections du résumé

BACKGROUND
Spinocerebellar ataxia type 3 is a rare neurodegenerative disease caused by a CAG repeat expansion in the ataxin-3 gene. Although no curative therapy is yet available, preclinical gene-silencing approaches to reduce polyglutamine (polyQ) toxicity demonstrate promising results. In view of upcoming clinical trials, quantitative and easily accessible molecular markers are of critical importance as pharmacodynamic and particularly as target engagement markers.
OBJECTIVE
We aimed at developing an ultrasensitive immunoassay to measure specifically polyQ-expanded ataxin-3 in plasma and cerebrospinal fluid (CSF).
METHODS
Using the novel single molecule counting ataxin-3 immunoassay, we analyzed cross-sectional and longitudinal patient biomaterials.
RESULTS
Statistical analyses revealed a correlation with clinical parameters and a stability of polyQ-expanded ataxin-3 during conversion from the pre-ataxic to the ataxic phases.
CONCLUSIONS
The novel immunoassay is able to quantify polyQ-expanded ataxin-3 in plasma and CSF, whereas ataxin-3 levels in plasma correlate with disease severity. Longitudinal analyses demonstrated a high stability of polyQ-expanded ataxin-3 over a short period. © 2021 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Identifiants

pubmed: 34397117
doi: 10.1002/mds.28749
doi:

Substances chimiques

Peptides 0
polyglutamine 26700-71-0
Ataxin-3 EC 3.4.19.12

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2675-2681

Subventions

Organisme : Medical Research Council
ID : MR/N028767/1
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn
Type : CommentIn

Informations de copyright

© 2021 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Références

Klockgether T, Mariotti C, Paulson HL. Spinocerebellar Ataxia. Nat Rev Dis Primers 2019;5:24.
Prudencio M, Garcia-Moreno H, Jansen-West KR, et al. Towards allele-specific targeting therapy and pharmacodynamic marker for spinocerebellar ataxia type 3. Sci Transl Med 2020;12:eabb7086.
Gonsior K, Kaucher AG, Pelz P, et al. PolyQ-expanded ataxin-3 protein levels in peripheral blood mononuclear cells correlate with clinical parameters in SCA3: a pilot study. J Neurol 2021;268:1304-1315.
Tezenas du Montcel S, Durr A, Rakowicz M, et al. Prediction of age at onset in spinocerebellar ataxia type 1, 2, 3 and 6. J Med Genet 2014;51:479-486.
Schmitz-Hübsch T, du Montcel ST, Baliko L, et al. Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology 2006;66:1717-1720.
Hwang J, Banerjee M, Venable AS, et al. Quantitation of low abundant soluble biomarkers using high sensitivity single molecule counting technology. Methods 2019;158:69-76.
Ko J, Ou S, Patterson PH. New anti-huntingtin monoclonal antibodies: implications for huntingtin conformation and its binding proteins. Brain Res Bull 2001;56:319-329.
Jiao S, Wang P, Chen Z, et al. Age is an important independent modifier of SCA3 phenotype severity. Neurosci Lett 2021;741:135510.
Leotti VB, de Vries JJ, Oliveira CM, et al. CAG repeat size influences the progression rate of Spinocerebellar ataxia type 3. Ann Neurol 2021;89:66-73.
Meeter LHH, Gendron TF, Sias AC, et al. Poly(GP), neurofilament and grey matter deficits in C9orf72 expansion carriers. Ann Clin Transl Neurol 2018;5(5):583-597.

Auteurs

Jeannette Hübener-Schmid (J)

Institute of Medical Genetics and Applied Genomics, University of Tübingen, Tübingen, Germany.
Centre for Rare Diseases, University of Tübingen, Tübingen, Germany.

Kirsten Kuhlbrodt (K)

Evotec SE, Hamburg, Germany.

Julien Peladan (J)

Evotec SE, Hamburg, Germany.

Jennifer Faber (J)

DZNE, German Center for Neurodegenerative Diseases, Bonn, Germany.
Department of Neurology, University Hospital Bonn, Bonn, Germany.

Magda M Santana (MM)

Center for Neuroscience and Cell Biology (CNC), University of Coimbra, Coimbra, Portugal.
Center for Innovation in Biomedicine and Biotechnology (CIBB), University of Coimbra, Coimbra, Portugal.
IIIUC-Institute for Interdisciplinary Research, University of Coimbra, Coimbra, Portugal.

Holger Hengel (H)

Department of Neurodegenerative Diseases and Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
German Centre for Neurodegenerative Diseases (DZNE), Tübingen, Germany.

Heike Jacobi (H)

Department of Neurology, University Hospital of Heidelberg, Heidelberg, Germany.

Kathrin Reetz (K)

Department of Neurology, RWTH Aachen University, Aachen, Germany.
JARA-Brain Institute Molecular Neuroscience and Neuroimaging, Jülich, Germany.

Hector Garcia-Moreno (H)

Department of Clinical and Movement Neuroscience, Ataxia Centre, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom.
Department of Neurogenetics, National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Foundation Trust, London, UK.

Mafalda Raposo (M)

Faculdade de Ciências e Tecnologia, Universidade dos Açores, Ponta Delgada, Portugal & Instituto de Biologia Molecular e Celular (IBMC), Instituto de Investigação e Inovação em Saúde (i3S), Universidade do Porto, Porto, Portugal.

Judith van Gaalen (J)

Department of Neurology, Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands.

Jon Infante (J)

Service of Neurology, University Hospital Marqués de Valdecilla (IDIVAL), University of Cantabria (UC), Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Santander, Spain.

Katharina M Steiner (KM)

Department of Neurology, Center for Translational Neuro- and Behavioral Sciences, Essen University Hospital, University of Duisburg-Essen, Essen, Germany.

Jeroen de Vries (J)

Department of Neurology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.

Marcel M Verbeek (MM)

Department of Neurology, Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands.
Department of Laboratory Medicine, Radboud University Medical Centre, Nijmegen, The Netherlands.

Paola Giunti (P)

Department of Clinical and Movement Neuroscience, Ataxia Centre, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom.
Department of Neurogenetics, National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Foundation Trust, London, UK.

Luis Pereira de Almeida (L)

Center for Neuroscience and Cell Biology (CNC), University of Coimbra, Coimbra, Portugal.
Center for Innovation in Biomedicine and Biotechnology (CIBB), University of Coimbra, Coimbra, Portugal.
Faculty of Pharmacy, University of Coimbra, Coimbra, Portugal.

Manuela Lima (M)

Faculdade de Ciências e Tecnologia, Universidade dos Açores, Ponta Delgada, Portugal & Instituto de Biologia Molecular e Celular (IBMC), Instituto de Investigação e Inovação em Saúde (i3S), Universidade do Porto, Porto, Portugal.

Bart van de Warrenburg (B)

Department of Neurology, Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands.

Ludger Schöls (L)

Department of Neurodegenerative Diseases and Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
German Centre for Neurodegenerative Diseases (DZNE), Tübingen, Germany.

Thomas Klockgether (T)

DZNE, German Center for Neurodegenerative Diseases, Bonn, Germany.
Department of Neurology, University Hospital Bonn, Bonn, Germany.

Matthis Synofzik (M)

Department of Neurodegenerative Diseases and Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
German Centre for Neurodegenerative Diseases (DZNE), Tübingen, Germany.

Olaf Riess (O)

Institute of Medical Genetics and Applied Genomics, University of Tübingen, Tübingen, Germany.
Centre for Rare Diseases, University of Tübingen, Tübingen, Germany.

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