Phenotype, penetrance, and treatment of 133 cytotoxic T-lymphocyte antigen 4-insufficient subjects

J Allergy Clin Immunol. 2018 Dec;142(6):1932-1946. doi: 10.1016/j.jaci.2018.02.055. Epub 2018 May 4.

Abstract

Background: Cytotoxic T-lymphocyte antigen 4 (CTLA-4) is a negative immune regulator. Heterozygous CTLA4 germline mutations can cause a complex immune dysregulation syndrome in human subjects.

Objective: We sought to characterize the penetrance, clinical features, and best treatment options in 133 CTLA4 mutation carriers.

Methods: Genetics, clinical features, laboratory values, and outcomes of treatment options were assessed in a worldwide cohort of CTLA4 mutation carriers.

Results: We identified 133 subjects from 54 unrelated families carrying 45 different heterozygous CTLA4 mutations, including 28 previously undescribed mutations. Ninety mutation carriers were considered affected, suggesting a clinical penetrance of at least 67%; median age of onset was 11 years, and the mortality rate within affected mutation carriers was 16% (n = 15). Main clinical manifestations included hypogammaglobulinemia (84%), lymphoproliferation (73%), autoimmune cytopenia (62%), and respiratory (68%), gastrointestinal (59%), or neurological features (29%). Eight affected mutation carriers had lymphoma, and 3 had gastric cancer. An EBV association was found in 6 patients with malignancies. CTLA4 mutations were associated with lymphopenia and decreased T-, B-, and natural killer (NK) cell counts. Successful targeted therapies included application of CTLA-4 fusion proteins, mechanistic target of rapamycin inhibitors, and hematopoietic stem cell transplantation. EBV reactivation occurred in 2 affected mutation carriers after immunosuppression.

Conclusions: Affected mutation carriers with CTLA-4 insufficiency can present in any medical specialty. Family members should be counseled because disease manifestation can occur as late as 50 years of age. EBV- and cytomegalovirus-associated complications must be closely monitored. Treatment interventions should be coordinated in clinical trials.

Keywords: Cytotoxic T-lymphocyte antigen 4; abatacept; autoimmunity; common variable immunodeficiency; hematopoietic stem cell transplantation; hypogammaglobulinemia; immune dysregulation; primary immunodeficiency; sirolimus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • CTLA-4 Antigen / genetics*
  • Child
  • Female
  • Humans
  • Immunologic Deficiency Syndromes / diagnostic imaging
  • Immunologic Deficiency Syndromes / genetics*
  • Immunologic Deficiency Syndromes / therapy
  • Male
  • Middle Aged
  • Mutation
  • Phenotype
  • Young Adult

Substances

  • CTLA-4 Antigen
  • CTLA4 protein, human