Heritable risk for severe anaphylaxis associated with increased α-tryptase-encoding germline copy number at TPSAB1.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
02 2021
Historique:
received: 23 01 2020
revised: 10 06 2020
accepted: 15 06 2020
pubmed: 28 7 2020
medline: 14 9 2021
entrez: 28 7 2020
Statut: ppublish

Résumé

An elevated basal serum tryptase level is associated with severe systemic anaphylaxis, most notably caused by Hymenoptera envenomation. Although clonal mast cell disease is the culprit in some individuals, it does not fully explain this clinical association. Our aim was to determine the prevalence and associated impact of tryptase genotypes on anaphylaxis in humans. Cohorts with systemic mastocytosis (SM) and venom as well as idiopathic anaphylaxis from referral centers in Italy, Slovenia, and the United States, underwent tryptase genotyping by droplet digital PCR. Associated anaphylaxis severity (Mueller scale) was subsequently examined. Healthy volunteers and controls with nonatopic disease were recruited and tryptase was genotyped by droplet digital PCR and in silico analysis of genome sequence, respectively. The effects of pooled and recombinant human tryptases, protease activated receptor 2 agonist and antagonist peptides, and a tryptase-neutralizing mAb on human umbilical vein endothelial cell permeability were assayed using a Transwell system. Hereditary α-tryptasemia (HαT)-a genetic trait caused by increased α-tryptase-encoding Tryptase-α/β1 (TPSAB1) copy number resulting in elevated BST level-was common in healthy individuals (5.6% [n = 7 of 125]) and controls with nonatopic disease (5.3% [n = 21 of 398]). HαT was associated with grade IV venom anaphylaxis (relative risk = 2.0; P < .05) and more prevalent in both idiopathic anaphylaxis (n = 8 of 47; [17%; P = .006]) and SM (n = 10 of 82 [12.2%; P = .03]) relative to the controls. Among patients with SM, concomitant HαT was associated with increased risk for systemic anaphylaxis (relative risk = 9.5; P = .007). In vitro, protease-activated receptor-2-dependent vascular permeability was induced by pooled mature tryptases but not α- or β-tryptase homotetramers. Risk for severe anaphylaxis in humans is associated with inherited differences in α-tryptase-encoding copies at TPSAB1.

Sections du résumé

BACKGROUND
An elevated basal serum tryptase level is associated with severe systemic anaphylaxis, most notably caused by Hymenoptera envenomation. Although clonal mast cell disease is the culprit in some individuals, it does not fully explain this clinical association.
OBJECTIVE
Our aim was to determine the prevalence and associated impact of tryptase genotypes on anaphylaxis in humans.
METHODS
Cohorts with systemic mastocytosis (SM) and venom as well as idiopathic anaphylaxis from referral centers in Italy, Slovenia, and the United States, underwent tryptase genotyping by droplet digital PCR. Associated anaphylaxis severity (Mueller scale) was subsequently examined. Healthy volunteers and controls with nonatopic disease were recruited and tryptase was genotyped by droplet digital PCR and in silico analysis of genome sequence, respectively. The effects of pooled and recombinant human tryptases, protease activated receptor 2 agonist and antagonist peptides, and a tryptase-neutralizing mAb on human umbilical vein endothelial cell permeability were assayed using a Transwell system.
RESULTS
Hereditary α-tryptasemia (HαT)-a genetic trait caused by increased α-tryptase-encoding Tryptase-α/β1 (TPSAB1) copy number resulting in elevated BST level-was common in healthy individuals (5.6% [n = 7 of 125]) and controls with nonatopic disease (5.3% [n = 21 of 398]). HαT was associated with grade IV venom anaphylaxis (relative risk = 2.0; P < .05) and more prevalent in both idiopathic anaphylaxis (n = 8 of 47; [17%; P = .006]) and SM (n = 10 of 82 [12.2%; P = .03]) relative to the controls. Among patients with SM, concomitant HαT was associated with increased risk for systemic anaphylaxis (relative risk = 9.5; P = .007). In vitro, protease-activated receptor-2-dependent vascular permeability was induced by pooled mature tryptases but not α- or β-tryptase homotetramers.
CONCLUSIONS
Risk for severe anaphylaxis in humans is associated with inherited differences in α-tryptase-encoding copies at TPSAB1.

Identifiants

pubmed: 32717252
pii: S0091-6749(20)31029-0
doi: 10.1016/j.jaci.2020.06.035
pii:
doi:

Substances chimiques

Arthropod Venoms 0
TPSAB1 protein, human EC 3.4.21.59
Tryptases EC 3.4.21.59

Types de publication

Journal Article Research Support, N.I.H., Intramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

622-632

Informations de copyright

Published by Elsevier Inc.

Auteurs

Jonathan J Lyons (JJ)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md. Electronic address: jonathan.lyons@nih.gov.

Jack Chovanec (J)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Michael P O'Connell (MP)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Yihui Liu (Y)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Julij Šelb (J)

University Clinic of Respiratory and Allergic Diseases, Golnik, Slovenia.

Roberta Zanotti (R)

Department of Medicine, Section of Hematology, Verona, Italy.

Yun Bai (Y)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Jiwon Kim (J)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Quang T Le (QT)

Department of Internal Medicine, Virginia Commonwealth University, Richmond, Va.

Tom DiMaggio (T)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Lawrence B Schwartz (LB)

Department of Internal Medicine, Virginia Commonwealth University, Richmond, Va.

Hirsh D Komarow (HD)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Matija Rijavec (M)

University Clinic of Respiratory and Allergic Diseases, Golnik, Slovenia.

Melody C Carter (MC)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Joshua D Milner (JD)

Division of Allergy, Immunology and Rheumatology, Columbia University, New York, New York.

Patrizia Bonadonna (P)

Allergy Unit, Verona University Hospital, Verona, Italy.

Dean D Metcalfe (DD)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.

Peter Korošec (P)

University Clinic of Respiratory and Allergic Diseases, Golnik, Slovenia.

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