Mutations affecting the actin regulator WD repeat-containing protein 1 lead to aberrant lymphoid immunity

J Allergy Clin Immunol. 2018 Nov;142(5):1589-1604.e11. doi: 10.1016/j.jaci.2018.04.023. Epub 2018 May 8.

Abstract

Background: The actin-interacting protein WD repeat-containing protein 1 (WDR1) promotes cofilin-dependent actin filament turnover. Biallelic WDR1 mutations have been identified recently in an immunodeficiency/autoinflammatory syndrome with aberrant morphology and function of myeloid cells.

Objective: Given the pleiotropic expression of WDR1, here we investigated to what extent it might control the lymphoid arm of the immune system in human subjects.

Methods: Histologic and detailed immunologic analyses were performed to elucidate the role of WDR1 in the development and function of B and T lymphocytes.

Results: Here we identified novel homozygous and compound heterozygous WDR1 missense mutations in 6 patients belonging to 3 kindreds who presented with respiratory tract infections, skin ulceration, and stomatitis. In addition to defective adhesion and motility of neutrophils and monocytes, WDR1 deficiency was associated with aberrant T-cell activation and B-cell development. T lymphocytes appeared to develop normally in the patients, except for the follicular helper T-cell subset. However, peripheral T cells from the patients accumulated atypical actin structures at the immunologic synapse and displayed reduced calcium flux and mildly impaired proliferation on T-cell receptor stimulation. WDR1 deficiency was associated with even more severe abnormalities of the B-cell compartment, including peripheral B-cell lymphopenia, paucity of B-cell progenitors in the bone marrow, lack of switched memory B cells, reduced clonal diversity, abnormal B-cell spreading, and increased apoptosis on B-cell receptor/Toll-like receptor stimulation.

Conclusion: Our study identifies a novel role for WDR1 in adaptive immunity, highlighting WDR1 as a central regulator of actin turnover during formation of the B-cell and T-cell immunologic synapses.

Keywords: WD repeat–containing protein 1; actin cytoskeleton; immunodeficiency; immunologic synapse; lymphocytes.

Publication types

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

MeSH terms

  • Adaptive Immunity
  • Adult
  • B-Lymphocytes / immunology*
  • Child
  • Female
  • Humans
  • Immunological Synapses*
  • Male
  • Microfilament Proteins / genetics*
  • Microfilament Proteins / immunology*
  • Mutation
  • T-Lymphocytes / immunology*
  • Young Adult

Substances

  • Microfilament Proteins
  • WDR1 protein, human