A Novel Pathogenic Variant in CARMIL2 (RLTPR) Causing CARMIL2 Deficiency and EBV-Associated Smooth Muscle Tumors

Front Immunol. 2020 Jun 18:11:884. doi: 10.3389/fimmu.2020.00884. eCollection 2020.

Abstract

CARMIL2 deficiency is a rare combined immunodeficiency (CID) characterized by defective CD28-mediated T cell co-stimulation, altered cytoskeletal dynamics, and susceptibility to Epstein Barr Virus smooth muscle tumors (EBV-SMTs). Case reports associated with EBV-SMTs are limited. We describe herein a novel homozygous CARMIL2 variant (c.1364_1393del) in two Saudi Arabian male siblings born to consanguineous parents who developed EBV-SMTs. CARMIL2 protein expression was significantly reduced in CD4+ T cells and CD8+ T cells. T cell proliferation on stimulation with soluble (s) anti-CD3 or (s) anti-CD3 plus anti-CD28 antibodies was close to absent in the proband, confirming altered CD28-mediated co-signaling. CD28 expression was substantially reduced in the proband's T cells, and was diminished to a lesser degree in the T cells of the younger sibling, who has a milder clinical phenotype. Defects in both T and B cell compartments were observed, including absent central memory CD8+ T cells, and decreased frequencies of total and class-switched memory B cells. FOXP3+ regulatory T cells (Treg) were also quantitatively decreased, and furthermore CD25 expression within the Treg subset was substantially reduced. These data confirm the pathogenicity of this novel loss-of-function (LOF) variant in CARMIL2 and expand the genotypic and phenotypic spectrum of CIDs associated with EBV-SMTs.

Keywords: CARMIL2 deficiency; DOCK8 deficiency; EBV-associated smooth muscle tumor; Early-onset inflammatory bowel disease (IBD); RLTPR; immune dysregulation; primary immunodeficiencies.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • CD28 Antigens / metabolism
  • Cells, Cultured
  • Cytoskeleton / metabolism
  • Epstein-Barr Virus Infections / genetics*
  • Herpesvirus 4, Human / physiology*
  • Humans
  • Lymphocyte Activation
  • Male
  • Microfilament Proteins / genetics*
  • Pedigree
  • Primary Immunodeficiency Diseases / genetics*
  • Saudi Arabia
  • Siblings
  • Smooth Muscle Tumor
  • T-Lymphocytes / physiology*

Substances

  • CARMIL1 protein, human
  • CD28 Antigens
  • Microfilament Proteins