Functional analysis of RYR1 variants in patients with confirmed susceptibility to malignant hyperthermia.

calcium release assay malignant hyperthermia next-generation sequencing pre-symptomatic diagnosis ryanodine receptor

Journal

British journal of anaesthesia
ISSN: 1471-6771
Titre abrégé: Br J Anaesth
Pays: England
ID NLM: 0372541

Informations de publication

Date de publication:
12 2022
Historique:
received: 09 05 2022
revised: 20 08 2022
accepted: 22 08 2022
pubmed: 9 10 2022
medline: 23 11 2022
entrez: 8 10 2022
Statut: ppublish

Résumé

A major bottleneck to the introduction of noninvasive presymptomatic diagnostic tests for the pharmacogenetic disorder malignant hyperthermia is the lack of functional data for associated variants. We screened 50 genes having a potential role in skeletal muscle calcium homeostasis using the HaloPlex™ (Agilent Technologies, Santa Clara, CA, USA) target enrichment system and next-generation sequencing. Twenty-one patients with a history of a clinical malignant hyperthermia reaction together with a positive in vitro contracture test were included. Eight variants in RYR1 were subsequently introduced into the cDNA for the human ryanodine receptor gene and tested in cultured human embryonic kidney (HEK293) cells for their effect on calcium release from intracellular stores in response to the ryanodine receptor-1 agonist 4-chloro-m-cresol using fura-2 as calcium indicator. Each variant was subjected to in silico curation using the European Malignant Hyperthermia Group scoring matrix and ClinGen RYR1 variant curation expert panel guidelines. Potentially causative RYR1 variants were identified in 15 patients. Of these, two families carried two RYR1 variants, five variants had been previously reported as 'pathogenic', two variants had been previously reported as 'likely benign', and eight were of 'uncertain significance'. Of these eight variants, four showed hypersensitivity to 4-chloro-m-cresol. Three variants were reclassified as either 'pathogenic' or 'likely pathogenic'. Two were classified as 'benign', whilst three remained of 'uncertain significance'. Three (p.Tyr1711Cys, p.Val2280Ile, and p.Arg4737Gln) additional variants can be added to the list of RYR1 disease-associated variants managed by the European Malignant Hyperthermia Group. These can therefore be used diagnostically in the future. Three variants (p.Glu2348Gly, p.Asn2634Lys, and p.Arg3629Trp) that remained classified as of uncertain significance require further family studies or a different functional test to determine clinical relevance in malignant hyperthermia.

Sections du résumé

BACKGROUND
A major bottleneck to the introduction of noninvasive presymptomatic diagnostic tests for the pharmacogenetic disorder malignant hyperthermia is the lack of functional data for associated variants.
METHODS
We screened 50 genes having a potential role in skeletal muscle calcium homeostasis using the HaloPlex™ (Agilent Technologies, Santa Clara, CA, USA) target enrichment system and next-generation sequencing. Twenty-one patients with a history of a clinical malignant hyperthermia reaction together with a positive in vitro contracture test were included. Eight variants in RYR1 were subsequently introduced into the cDNA for the human ryanodine receptor gene and tested in cultured human embryonic kidney (HEK293) cells for their effect on calcium release from intracellular stores in response to the ryanodine receptor-1 agonist 4-chloro-m-cresol using fura-2 as calcium indicator. Each variant was subjected to in silico curation using the European Malignant Hyperthermia Group scoring matrix and ClinGen RYR1 variant curation expert panel guidelines.
RESULTS
Potentially causative RYR1 variants were identified in 15 patients. Of these, two families carried two RYR1 variants, five variants had been previously reported as 'pathogenic', two variants had been previously reported as 'likely benign', and eight were of 'uncertain significance'. Of these eight variants, four showed hypersensitivity to 4-chloro-m-cresol. Three variants were reclassified as either 'pathogenic' or 'likely pathogenic'. Two were classified as 'benign', whilst three remained of 'uncertain significance'.
CONCLUSIONS
Three (p.Tyr1711Cys, p.Val2280Ile, and p.Arg4737Gln) additional variants can be added to the list of RYR1 disease-associated variants managed by the European Malignant Hyperthermia Group. These can therefore be used diagnostically in the future. Three variants (p.Glu2348Gly, p.Asn2634Lys, and p.Arg3629Trp) that remained classified as of uncertain significance require further family studies or a different functional test to determine clinical relevance in malignant hyperthermia.

Identifiants

pubmed: 36208971
pii: S0007-0912(22)00496-2
doi: 10.1016/j.bja.2022.08.029
pii:
doi:

Substances chimiques

3-cresol GGO4Y809LO
Calcium SY7Q814VUP
Ryanodine Receptor Calcium Release Channel 0
RYR1 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

879-888

Informations de copyright

Copyright © 2022 British Journal of Anaesthesia. All rights reserved.

Auteurs

Ruth White (R)

School of Natural Sciences, Massey University, Palmerston North, New Zealand.

Anja H Schiemann (AH)

School of Natural Sciences, Massey University, Palmerston North, New Zealand.

Sophie M Burling (SM)

School of Natural Sciences, Massey University, Palmerston North, New Zealand.

Andrew Bjorksten (A)

Malignant Hyperthermia Diagnostic Unit, Department of Anaesthesia and Pain Management, Royal Melbourne Hospital, Parkville, VIC, Australia.

Terasa Bulger (T)

Department of Anaesthesia and Intensive Care, Palmerston North Hospital, Palmerston North, New Zealand.

Robyn Gillies (R)

Malignant Hyperthermia Diagnostic Unit, Department of Anaesthesia and Pain Management, Royal Melbourne Hospital, Parkville, VIC, Australia.

Philip M Hopkins (PM)

Leeds Institute of Medical Research at Saint James School of Medicine, University of Leeds, St James's University Hospital, Leeds, UK.

Erik-Jan Kamsteeg (EJ)

Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands.

Roslyn G Machon (RG)

Department of Anaesthesia and Intensive Care, Palmerston North Hospital, Palmerston North, New Zealand.

Sean Massey (S)

School of Natural Sciences, Massey University, Palmerston North, New Zealand; Brain and Mitochondrial Research Group, Murdoch Children's Research Institute, Melbourne, VIC, Australia.

Dorota Miller (D)

Leeds Institute of Medical Research at Saint James School of Medicine, University of Leeds, St James's University Hospital, Leeds, UK.

Margaret Perry (M)

The Children's Hospital at Westmead, Sydney, NSW, Australia.

Marc M J Snoeck (MMJ)

Malignant Hyperthermia Investigation Unit, Department of Anaesthesiology, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands.

Jeremy Stephens (J)

School of Natural Sciences, Massey University, Palmerston North, New Zealand.

Neil Street (N)

The Children's Hospital at Westmead, Sydney, NSW, Australia.

Luuk R van den Bersselaar (LR)

Malignant Hyperthermia Investigation Unit, Department of Anaesthesiology, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands.

Kathryn M Stowell (KM)

School of Natural Sciences, Massey University, Palmerston North, New Zealand. Electronic address: K.M.Stowell@massey.ac.nz.

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Classifications MeSH