Immune Dysregulation in Human ITCH Deficiency Successfully Treated with Hematopoietic Cell Transplantation.


Journal

The journal of allergy and clinical immunology. In practice
ISSN: 2213-2201
Titre abrégé: J Allergy Clin Immunol Pract
Pays: United States
ID NLM: 101597220

Informations de publication

Date de publication:
07 2021
Historique:
received: 07 08 2020
revised: 24 02 2021
accepted: 03 04 2021
pubmed: 25 4 2021
medline: 23 7 2021
entrez: 24 4 2021
Statut: ppublish

Résumé

Mutations in ITCH, which encodes an E3 ubiquitin-protein ligase, can result in systemic autoimmunity and immunodeficiency. The clinical phenotype and mechanism of disease have not been fully characterized, resulting in a paucity of therapeutic options for this potentially fatal disease. We aimed to (1) expand the understanding about the phenotype of human ITCH deficiency (2) further characterize the associated immune dysregulation, and (3) report the first successful hematopoietic cell transplant (HCT) in a patient with ITCH deficiency. Disease profiling was performed in a patient with multisystem immune dysregulation. Whole exome sequencing with trio analysis and functional validation of candidate disease variants were performed, including mRNA and protein expression. Analyses to further delineate the immunophenotype included quantitative evaluation of lymphoid and myeloid subsets with flow cytometry and mass cytometry. A patient with multisystem immune dysregulation presenting with growth failure, very-early-onset inflammatory bowel disease, arthritis, uveitis, psoriasis, and type 1 diabetes mellitus underwent whole exome sequencing, which identified novel compound heterozygous mutations in ITCH. Reduced expression of ITCH mRNA and absent ITCH protein were found. Abnormalities in both lymphoid and myeloid lineages were identified. The patient underwent HCT. He demonstrated excellent immune reconstitution and resolution of many manifestations of his systemic disease. Here we report ITCH deficiency with unique clinical features of colonic very-early-onset inflammatory bowel disease, arthritis, and uveitis in the setting of immune dysregulation and further characterize the underlying immune dysregulation. We demonstrate that HCT can be an effective, and potentially curative, therapy for ITCH deficiency.

Sections du résumé

BACKGROUND
Mutations in ITCH, which encodes an E3 ubiquitin-protein ligase, can result in systemic autoimmunity and immunodeficiency. The clinical phenotype and mechanism of disease have not been fully characterized, resulting in a paucity of therapeutic options for this potentially fatal disease.
OBJECTIVE
We aimed to (1) expand the understanding about the phenotype of human ITCH deficiency (2) further characterize the associated immune dysregulation, and (3) report the first successful hematopoietic cell transplant (HCT) in a patient with ITCH deficiency.
METHODS
Disease profiling was performed in a patient with multisystem immune dysregulation. Whole exome sequencing with trio analysis and functional validation of candidate disease variants were performed, including mRNA and protein expression. Analyses to further delineate the immunophenotype included quantitative evaluation of lymphoid and myeloid subsets with flow cytometry and mass cytometry.
RESULTS
A patient with multisystem immune dysregulation presenting with growth failure, very-early-onset inflammatory bowel disease, arthritis, uveitis, psoriasis, and type 1 diabetes mellitus underwent whole exome sequencing, which identified novel compound heterozygous mutations in ITCH. Reduced expression of ITCH mRNA and absent ITCH protein were found. Abnormalities in both lymphoid and myeloid lineages were identified. The patient underwent HCT. He demonstrated excellent immune reconstitution and resolution of many manifestations of his systemic disease.
CONCLUSIONS
Here we report ITCH deficiency with unique clinical features of colonic very-early-onset inflammatory bowel disease, arthritis, and uveitis in the setting of immune dysregulation and further characterize the underlying immune dysregulation. We demonstrate that HCT can be an effective, and potentially curative, therapy for ITCH deficiency.

Identifiants

pubmed: 33894394
pii: S2213-2198(21)00450-5
doi: 10.1016/j.jaip.2021.04.010
pmc: PMC9053103
mid: NIHMS1696763
pii:
doi:

Substances chimiques

Repressor Proteins 0
ITCH protein, human EC 2.3.2.26
Ubiquitin-Protein Ligases EC 2.3.2.27

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2885-2893.e3

Subventions

Organisme : NIDDK NIH HHS
ID : K23 DK100461
Pays : United States
Organisme : NIAID NIH HHS
ID : K08 AI135091
Pays : United States
Organisme : NICHD NIH HHS
ID : K12 HD043245
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK111843
Pays : United States
Organisme : NIDDK NIH HHS
ID : K23 DK119585
Pays : United States

Informations de copyright

Copyright © 2021 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

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Auteurs

Trusha Patel (T)

Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa; Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa. Electronic address: patelt3@chop.edu.

Sarah E Henrickson (SE)

Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa; Division of Allergy and Immunology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Emily K Moser (EK)

Division of Pulmonary Critical Care and Sleep Medicine, University of Florida, Gainesville, Fla; Division of Protective Immunity, Children's Hospital of Philadelphia, Philadelphia, Pa.

Natania S Field (NS)

Division of Protective Immunity, Children's Hospital of Philadelphia, Philadelphia, Pa.

Kelly Maurer (K)

Division of Allergy and Immunology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Noor Dawany (N)

Department of Biomedical and Health Informatics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Maire Conrad (M)

Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa; Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa.

Nancy Bunin (N)

Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa; Blood and Marrow Transplant Section, Division of Oncology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Jason L Freedman (JL)

Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa; Blood and Marrow Transplant Section, Division of Oncology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Jennifer Heimall (J)

Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa; Division of Allergy and Immunology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Danielle E Arnold (DE)

Division of Allergy and Immunology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Jing Wang (J)

Division of Genomic Diagnostics, Children's Hospital of Philadelphia, Philadelphia, Pa; Division of Anatomic Pathology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Jonathan E Markowitz (JE)

Pediatric Gastroenterology, Prisma Health Children's Hospital Upstate, Greenville, SC; University of South Carolina School of Medicine-Greenville, Greenville, SC.

Sarah Beth Payne-Poff (SB)

University of South Carolina School of Medicine-Greenville, Greenville, SC; Pediatric Rheumatology, Prisma Health Children's Hospital Upstate, Greenville, SC.

Kelli W Williams (KW)

Division of Pediatric Pulmonology, Allergy and Immunology, Department of Pediatrics, Medical University of South Carolina, Charleston, SC.

Pierre A Russo (PA)

Division of Anatomic Pathology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa; Department of Pathology and Laboratory Medicine, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa.

E John Wherry (EJ)

Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania, Pa; Institute for Immunology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa.

Marcella Devoto (M)

Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa; Division of Human Genetics, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa; Department of Translational and Precision Medicine, Sapienza University, Rome, Italy.

Paula Oliver (P)

Division of Protective Immunity, Children's Hospital of Philadelphia, Philadelphia, Pa; Department of Pathology and Laboratory Medicine, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa.

Kathleen E Sullivan (KE)

Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa; Division of Allergy and Immunology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa.

Judith R Kelsen (JR)

Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, Pa; Department of Pediatrics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa.

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