Prion protein monoclonal antibody (PRN100) therapy for Creutzfeldt-Jakob disease: evaluation of a first-in-human treatment programme.


Journal

The Lancet. Neurology
ISSN: 1474-4465
Titre abrégé: Lancet Neurol
Pays: England
ID NLM: 101139309

Informations de publication

Date de publication:
04 2022
Historique:
received: 22 10 2021
revised: 07 01 2022
accepted: 14 02 2022
pubmed: 20 3 2022
medline: 26 4 2022
entrez: 19 3 2022
Statut: ppublish

Résumé

Human prion diseases, including Creutzfeldt-Jakob disease (CJD), are rapidly progressive, invariably fatal neurodegenerative conditions with no effective therapies. Their pathogenesis involves the obligate recruitment of cellular prion protein (PrP We generated a fully humanised anti-PrP We treated six patients (two men; four women) with CJD for 7-260 days at UCLH between Oct 9, 2018, and July 31, 2019. Repeated intravenous dosing of PRN100 was well tolerated and reached the target CSF drug concentration (50 nM) in four patients after 22-70 days; no clinically significant adverse reactions were seen. All patients showed progressive neurological decline on serial assessments with the MRC Scales. Neuropathological examination was done in two patients (patients 2 and 3) and showed no evidence of cytotoxicity. Patient 2, who was treated for 140 days, had the longest clinical duration we have yet documented for iatrogenic CJD and showed patterns of disease-associated PrP that differed from untreated patients with CJD, consistent with drug effects. Patient 3, who had sporadic CJD and only received one therapeutic dose of 80 mg/kg, had weak PrP synaptic labelling in the periventricular regions, which was not a feature of untreated patients with sporadic CJD. Brain tissue-bound drug concentrations across multiple regions in patient 2 ranged from 9·9 μg per g of tissue (SD 0·3) in the thalamus to 27·4 μg per g of tissue (1·5) in the basal ganglia (equivalent to 66-182 nM). Our academic-led programme delivered what is, to our knowledge, the first rationally designed experimental treatment for human prion disease to a small number of patients with CJD. The treatment appeared to be safe and reached encouraging CSF and brain tissue concentrations. These findings justify the need for formal efficacy trials in patients with CJD at the earliest possible clinical stages and as prophylaxis in those at risk of prion disease due to PRNP mutations or prion exposure. The Cure CJD Campaign, the National Institute for Health Research UCLH Biomedical Research Centre, the Jon Moulton Charitable Trust, and the UK MRC.

Sections du résumé

BACKGROUND
Human prion diseases, including Creutzfeldt-Jakob disease (CJD), are rapidly progressive, invariably fatal neurodegenerative conditions with no effective therapies. Their pathogenesis involves the obligate recruitment of cellular prion protein (PrP
METHODS
We generated a fully humanised anti-PrP
FINDINGS
We treated six patients (two men; four women) with CJD for 7-260 days at UCLH between Oct 9, 2018, and July 31, 2019. Repeated intravenous dosing of PRN100 was well tolerated and reached the target CSF drug concentration (50 nM) in four patients after 22-70 days; no clinically significant adverse reactions were seen. All patients showed progressive neurological decline on serial assessments with the MRC Scales. Neuropathological examination was done in two patients (patients 2 and 3) and showed no evidence of cytotoxicity. Patient 2, who was treated for 140 days, had the longest clinical duration we have yet documented for iatrogenic CJD and showed patterns of disease-associated PrP that differed from untreated patients with CJD, consistent with drug effects. Patient 3, who had sporadic CJD and only received one therapeutic dose of 80 mg/kg, had weak PrP synaptic labelling in the periventricular regions, which was not a feature of untreated patients with sporadic CJD. Brain tissue-bound drug concentrations across multiple regions in patient 2 ranged from 9·9 μg per g of tissue (SD 0·3) in the thalamus to 27·4 μg per g of tissue (1·5) in the basal ganglia (equivalent to 66-182 nM).
INTERPRETATION
Our academic-led programme delivered what is, to our knowledge, the first rationally designed experimental treatment for human prion disease to a small number of patients with CJD. The treatment appeared to be safe and reached encouraging CSF and brain tissue concentrations. These findings justify the need for formal efficacy trials in patients with CJD at the earliest possible clinical stages and as prophylaxis in those at risk of prion disease due to PRNP mutations or prion exposure.
FUNDING
The Cure CJD Campaign, the National Institute for Health Research UCLH Biomedical Research Centre, the Jon Moulton Charitable Trust, and the UK MRC.

Identifiants

pubmed: 35305340
pii: S1474-4422(22)00082-5
doi: 10.1016/S1474-4422(22)00082-5
pii:
doi:

Substances chimiques

Antibodies, Monoclonal 0
Prion Proteins 0
Prions 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

342-354

Subventions

Organisme : Medical Research Council
ID : G0400713
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00024/9
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Published by Elsevier Ltd.. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests JC is a director and shareholder of D-Gen, an academic spinout in the field of prion disease diagnosis and therapeutics; D-Gen owns intellectual property relating to PRN100. All other authors declare no competing interests.

Auteurs

Simon Mead (S)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK; National Prion Clinic, National Hospital for Neurology and Neurosurgery, London, UK.

Azadeh Khalili-Shirazi (A)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK; National Prion Clinic, National Hospital for Neurology and Neurosurgery, London, UK.

Caroline Potter (C)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Tzehow Mok (T)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK; National Prion Clinic, National Hospital for Neurology and Neurosurgery, London, UK.

Akin Nihat (A)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK; National Prion Clinic, National Hospital for Neurology and Neurosurgery, London, UK.

Harpreet Hyare (H)

Department of Neuroradiology, National Hospital for Neurology and Neurosurgery, London, UK.

Stephanie Canning (S)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Christian Schmidt (C)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Tracy Campbell (T)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Lee Darwent (L)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Nicola Muirhead (N)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Nicolette Ebsworth (N)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Patrick Hextall (P)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Madeleine Wakeling (M)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Jacqueline Linehan (J)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK.

Vincenzo Libri (V)

NIHR, Biomedical Research Centre, University College London Hospitals, London, UK; Clinical Research Facility, University College London Hospitals, London, UK.

Bryan Williams (B)

NIHR, Biomedical Research Centre, University College London Hospitals, London, UK.

Zane Jaunmuktane (Z)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, London, UK; Division of Neuropathology, National Hospital for Neurology and Neurosurgery, London, UK.

Sebastian Brandner (S)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK; Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, UK; Division of Neuropathology, National Hospital for Neurology and Neurosurgery, London, UK.

Peter Rudge (P)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK; National Prion Clinic, National Hospital for Neurology and Neurosurgery, London, UK.

John Collinge (J)

MRC Prion Unit at UCL, UCL Institute of Prion Diseases, University College London, London, UK; National Prion Clinic, National Hospital for Neurology and Neurosurgery, London, UK. Electronic address: jc@prion.ucl.ac.uk.

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