Successful treatment of severe MSUD in Bckdhb

AAV8 BCKDH BCKDHB EF1α MSUD adeno associated virus branched-chain 2-keto acid dehydrogenase gene therapy maple syrup urine disease mouse model

Journal

Journal of inherited metabolic disease
ISSN: 1573-2665
Titre abrégé: J Inherit Metab Dis
Pays: United States
ID NLM: 7910918

Informations de publication

Date de publication:
07 Mar 2023
Historique:
revised: 11 02 2023
received: 30 11 2022
accepted: 02 03 2023
pubmed: 8 3 2023
medline: 8 3 2023
entrez: 7 3 2023
Statut: aheadofprint

Résumé

Maple syrup urine disease (MSUD) is rare autosomal recessive metabolic disorder caused by the dysfunction of the mitochondrial branched-chain 2-ketoacid dehydrogenase (BCKD) enzyme complex leading to massive accumulation of branched-chain amino acids and 2-keto acids. MSUD management, based on a life-long strict protein restriction with nontoxic amino acids oral supplementation represents an unmet need as it is associated with a poor quality of life, and does not fully protect from acute life-threatening decompensations or long-term neuropsychiatric complications. Orthotopic liver transplantation is a beneficial therapeutic option, which shows that restoration of only a fraction of whole-body BCKD enzyme activity is therapeutic. MSUD is thus an ideal target for gene therapy. We and others have tested AAV gene therapy in mice for two of the three genes involved in MSUD, BCKDHA and DBT. In this study, we developed a similar approach for the third MSUD gene, BCKDHB. We performed the first characterization of a Bckdhb

Identifiants

pubmed: 36880392
doi: 10.1002/jimd.12604
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Conseil Régional, Île-de-France
ID : DIM Thérapie Génique

Informations de copyright

© 2023 The Authors. Journal of Inherited Metabolic Disease published by John Wiley & Sons Ltd on behalf of SSIEM.

Références

Chuang DT, Shih VE. Maple syrup urine disease (branched-chain ketoaciduria). The Metabolic and Molecular Bases of Inherited Disease 1971-2006. McGraw-Hill; 2001.
Strauss KA, Puffenberger EG, Morton DH. Maple syrup urine disease. In: Adam MP et al., eds. GeneReviews®. University of Washington; 2013.
Muelly ER, Moore GJ, Bunce SC, et al. Biochemical correlates of neuropsychiatric illness in maple syrup urine disease. J Clin Invest. 2013;123:1809-1820.
Strauss KA, Carson VJ, Soltys K, et al. Branched-chain α-ketoacid dehydrogenase deficiency (maple syrup urine disease): treatment, biomarkers, and outcomes. Mol Genet Metab. 2020;129:193-206.
Bouchereau J, Leduc-Leballeur J, Pichard S, et al. Neurocognitive profiles in MSUD school-age patients. J Inherit Metab Dis. 2017;40:377-383.
Abi-Wardé M-T, Roda C, Arnoux JB, et al. Long-term metabolic follow-up and clinical outcome of 35 patients with maple syrup urine disease. J Inherit Metab Dis. 2017;40:783-792.
Mazariegos GV, Morton DH, Sindhi R, et al. Liver transplantation for classical maple syrup urine disease: long-term follow-up in 37 patients and comparative united network for organ sharing experience. J Pediatr. 2012;160:116-121.e1.
Bodner-Leidecker A, Wendel U, Saudubray JM, Schadewaldt P. Branched-chain L-amino acid metabolism in classical maple syrup urine disease after orthotopic liver transplantation. J Inherit Metab Dis. 2000;23:805-818.
Wendel U, Saudubray JM, Bodner A, Schadewaldt P. Liver transplantation in maple syrup urine disease. Eur J Pediatr. 1999;158(Suppl 2):S60-S64.
Suryawan A, Hawes JW, Harris RA, Shimomura Y, Jenkins AE, Hutson SM. A molecular model of human branched-chain amino acid metabolism. Am J Clin Nutr. 1998;68:72-81.
Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet. 2011;12:341-355.
Baruteau J, Perocheau DP, Hanley J, et al. Argininosuccinic aciduria fosters neuronal nitrosative stress reversed by Asl gene transfer. Nat Commun. 2018;9:3505.
Cunningham SC, Spinoulas A, Carpenter KH, Wilcken B, Kuchel PW, Alexander IE. AAV2/8-mediated correction of OTC deficiency is robust in adult but not neonatal Spf(ash) mice. Mol Ther J Am Soc Gene Ther. 2009;17:1340-1346.
Chandler RJ, Tarasenko TN, Cusmano-Ozog K, et al. Liver-directed adeno-associated virus serotype 8 gene transfer rescues a lethal murine model of citrullinemia type 1. Gene Ther. 2013;20:1188-1191.
Nitzahn M, Allegri G, Khoja S, et al. Split AAV-mediated gene therapy restores ureagenesis in a murine model of carbamoyl phosphate synthetase 1 deficiency. Mol Ther J Am Soc Gene Ther. 2020;28:1717-1730.
Sonaimuthu P, Senkevitch E, Haskins N, et al. Gene delivery corrects N-acetylglutamate synthase deficiency and enables insights in the physiological impact of L-arginine activation of N-acetylglutamate synthase. Sci Rep. 2021;11:3580.
Chandler RJ, Chandrasekaran S, Carrillo-Carrasco N, et al. Adeno-associated virus serotype 8 gene transfer rescues a neonatal lethal murine model of propionic acidemia. Hum Gene Ther. 2011;22:477-481.
Chandler RJ, Venditti CP. Gene therapy for methylmalonic acidemia: past, present, and future. Hum Gene Ther. 2019;30:1236-1244. doi:10.1089/hum.2019.113
Grisch-Chan HM, Schwank G, Harding CO, Thöny B. State-of-the-art 2019 on gene therapy for phenylketonuria. Hum Gene Ther. 2019;30:1274-1283. doi:10.1089/hum.2019.111
Pontoizeau C, Simon-Sola M, Gaborit C, et al. Neonatal gene therapy achieves sustained disease rescue of maple syrup urine disease in mice. Nat Commun. 2022;13:3278.
Greig JA, Jennis M, Dandekar A, et al. Muscle-directed AAV gene therapy rescues the maple syrup urine disease phenotype in a mouse model. Mol Genet Metab. 2021;134:139-146. doi:10.1016/j.ymgme.2021.08.003
Homanics GE, Skvorak K, Ferguson C, Watkins S, Paul HS. Production and characterization of murine models of classic and intermediate maple syrup urine disease. BMC Med Genet. 2006;7:33.
Bortolussi G, Zentillin L, Vaníkova J, et al. Life-long correction of hyperbilirubinemia with a neonatal liver-specific AAV-mediated gene transfer in a lethal mouse model of Crigler-Najjar syndrome. Hum Gene Ther. 2014;25:844-855.
Ronzitti G, Bortolussi G, van Dijk R, et al. A translationally optimized AAV-UGT1A1 vector drives safe and long-lasting correction of Crigler-Najjar syndrome. Mol Ther Methods Clin Dev. 2016;3:16049.
Wang L, Bell P, Lin J, Calcedo R, Tarantal AF, Wilson JM. AAV8-mediated hepatic gene transfer in infant rhesus monkeys (Macaca mulatta). Mol Ther. 2011;19:2012-2020.
Collaud F, Bortolussi G, Guianvarc'h L, et al. Preclinical development of an AAV8-hUGT1A1 vector for the treatment of Crigler-Najjar syndrome. Mol Ther - Methods Clin Dev. 2019;12:157-174.
Colella P, Sellier P, Costa Verdera H, et al. AAV gene transfer with tandem promoter design prevents anti-transgene immunity and provides persistent efficacy in neonate Pompe mice. Mol. Ther. - Methods Clin. Dev. 2019;12:85-101.
Corrà S, Cerutti R, Balmaceda V, Viscomi C, Zeviani M. Double administration of self-complementary AAV9NDUFS4 prevents Leigh disease in Ndufs4−/− mice. Brain J Neurol. 2022;145:3405-3414.
Mendell JR, Sahenk Z, Lehman K, et al. Assessment of systemic delivery of rAAVrh74.MHCK7.Micro-dystrophin in children with Duchenne muscular dystrophy: a nonrandomized controlled trial. JAMA Neurol. 2020;77:1122-1131. doi:10.1001/jamaneurol.2020.1484

Auteurs

Clément Pontoizeau (C)

Necker Hospital, APHP, Biochemistry, Metabolomics Unit, University Paris Cité, Paris, France.
Necker Hospital, APHP, Reference Center for Inborn Error of Metabolism, Pediatrics Department, University Paris Cité, Paris, France.
Inserm UMR_S1163, Institut Imagine, Paris, France.

Clovis Gaborit (C)

Inserm UMR_S1163, Institut Imagine, Paris, France.

Nolan Tual (N)

Inserm UMR_S1163, Institut Imagine, Paris, France.

Marcelo Simon-Sola (M)

Inserm UMR_S1163, Institut Imagine, Paris, France.

Irina Rotaru (I)

Inserm UMR_S1163, Institut Imagine, Paris, France.

Marion Benoist (M)

Inserm UMR_S1163, Institut Imagine, Paris, France.

Pasqualina Colella (P)

Généthon INTEGRARE UMR-S951, University of Evry, Evry, France.

Antonin Lamazière (A)

CRSA, St Antoine Hospital, Paris, France.

Anaïs Brassier (A)

Necker Hospital, APHP, Reference Center for Inborn Error of Metabolism, Pediatrics Department, University Paris Cité, Paris, France.

Jean-Baptiste Arnoux (JB)

Necker Hospital, APHP, Reference Center for Inborn Error of Metabolism, Pediatrics Department, University Paris Cité, Paris, France.

Agnès Rötig (A)

Inserm UMR_S1163, Institut Imagine, Paris, France.

Chris Ottolenghi (C)

Necker Hospital, APHP, Biochemistry, Metabolomics Unit, University Paris Cité, Paris, France.
Necker Hospital, APHP, Reference Center for Inborn Error of Metabolism, Pediatrics Department, University Paris Cité, Paris, France.
Inserm UMR_S1163, Institut Imagine, Paris, France.

Pascale de Lonlay (P)

Necker Hospital, APHP, Reference Center for Inborn Error of Metabolism, Pediatrics Department, University Paris Cité, Paris, France.
Inserm U1151, Institut Necker Enfants Malades, Paris, France.

Federico Mingozzi (F)

Généthon INTEGRARE UMR-S951, University of Evry, Evry, France.

Marina Cavazzana (M)

Inserm UMR_S1163, Institut Imagine, Paris, France.
Necker Hospital, APHP, Biotherapies Department and Clinical Investigation Center, Inserm, University Paris Cité, Paris, France.

Manuel Schiff (M)

Necker Hospital, APHP, Reference Center for Inborn Error of Metabolism, Pediatrics Department, University Paris Cité, Paris, France.
Inserm UMR_S1163, Institut Imagine, Paris, France.

Classifications MeSH