Cross-species efficacy of enzyme replacement therapy for CLN1 disease in mice and sheep.


Journal

The Journal of clinical investigation
ISSN: 1558-8238
Titre abrégé: J Clin Invest
Pays: United States
ID NLM: 7802877

Informations de publication

Date de publication:
17 10 2022
Historique:
received: 29 06 2022
accepted: 25 08 2022
pubmed: 31 8 2022
medline: 19 10 2022
entrez: 30 8 2022
Statut: epublish

Résumé

CLN1 disease, also called infantile neuronal ceroid lipofuscinosis (NCL) or infantile Batten disease, is a fatal neurodegenerative lysosomal storage disorder resulting from mutations in the CLN1 gene encoding the soluble lysosomal enzyme palmitoyl-protein thioesterase 1 (PPT1). Therapies for CLN1 disease have proven challenging because of the aggressive disease course and the need to treat widespread areas of the brain and spinal cord. Indeed, gene therapy has proven less effective for CLN1 disease than for other similar lysosomal enzyme deficiencies. We therefore tested the efficacy of enzyme replacement therapy (ERT) by administering monthly infusions of recombinant human PPT1 (rhPPT1) to PPT1-deficient mice (Cln1-/-) and CLN1R151X sheep to assess how to potentially scale up for translation. In Cln1-/- mice, intracerebrovascular (i.c.v.) rhPPT1 delivery was the most effective route of administration, resulting in therapeutically relevant CNS levels of PPT1 activity. rhPPT1-treated mice had improved motor function, reduced disease-associated pathology, and diminished neuronal loss. In CLN1R151X sheep, i.c.v. infusions resulted in widespread rhPPT1 distribution and positive treatment effects measured by quantitative structural MRI and neuropathology. This study demonstrates the feasibility and therapeutic efficacy of i.c.v. rhPPT1 ERT. These findings represent a key step toward clinical testing of ERT in children with CLN1 disease and highlight the importance of a cross-species approach to developing a successful treatment strategy.

Identifiants

pubmed: 36040802
pii: 163107
doi: 10.1172/JCI163107
pmc: PMC9566914
doi:
pii:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NINDS NIH HHS
ID : R43 NS107079
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS124655
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/P013732/1 ISP
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : R44 NS107079
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS100779
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/J004316/1
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : R56 NS117635
Pays : United States

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Auteurs

Hemanth R Nelvagal (HR)

Department of Pediatrics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.

Samantha L Eaton (SL)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Sophie H Wang (SH)

Department of Pediatrics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.

Elizabeth M Eultgen (EM)

Department of Pediatrics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.

Keigo Takahashi (K)

Department of Pediatrics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.

Steven Q Le (SQ)

Department of Pediatrics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.

Rachel Nesbitt (R)

Department of Medicine, Washington University in St. Louis, School of Medicine, St .Louis, Missouri, USA.

Joshua T Dearborn (JT)

Department of Medicine, Washington University in St. Louis, School of Medicine, St .Louis, Missouri, USA.

Nicholas Siano (N)

Discovery Science Division, Amicus Therapeutics Inc., Philadelphia, Pennsylvania, USA.

Ana C Puhl (AC)

Collaborations Pharmaceuticals Inc., Lab 3510, Raleigh, North Carolina, USA.

Patricia I Dickson (PI)

Department of Pediatrics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.
Department of Genetics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.

Gerard Thompson (G)

Centre for Clinical Brain Sciences, University of Edinburgh, Chancellor's Building, Edinburgh, Scotland, United Kingdom.
Department of Clinical Neurosciences, NHS Lothian, Edinburgh, Scotland, United Kingdom.

Fraser Murdoch (F)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Paul M Brennan (PM)

Centre for Clinical Brain Sciences, University of Edinburgh, Chancellor's Building, Edinburgh, Scotland, United Kingdom.
Department of Clinical Neurosciences, NHS Lothian, Edinburgh, Scotland, United Kingdom.

Mark Gray (M)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.
The Large Animal Research and Imaging Facility (LARIF), Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Stephen N Greenhalgh (SN)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.
The Large Animal Research and Imaging Facility (LARIF), Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Peter Tennant (P)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.
The Large Animal Research and Imaging Facility (LARIF), Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Rachael Gregson (R)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.
The Large Animal Research and Imaging Facility (LARIF), Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Eddie Clutton (E)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.
The Large Animal Research and Imaging Facility (LARIF), Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

James Nixon (J)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.
The Large Animal Research and Imaging Facility (LARIF), Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Chris Proudfoot (C)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.
The Large Animal Research and Imaging Facility (LARIF), Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Stefano Guido (S)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Simon G Lillico (SG)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

C Bruce A Whitelaw (CBA)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Jui-Yun Lu (JY)

Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, Texas, USA.

Sandra L Hofmann (SL)

Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, Texas, USA.

Sean Ekins (S)

Collaborations Pharmaceuticals Inc., Lab 3510, Raleigh, North Carolina, USA.

Mark S Sands (MS)

Department of Medicine, Washington University in St. Louis, School of Medicine, St .Louis, Missouri, USA.
Department of Genetics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.

Thomas M Wishart (TM)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Easter Bush, Scotland, United Kingdom.

Jonathan D Cooper (JD)

Department of Pediatrics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.
Department of Genetics, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.
Department of Neurology, Washington University in St. Louis, School of Medicine, St. Louis, Missouri, USA.

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