L-plastin associated syndrome of immune deficiency and hematologic cytopenia

J Allergy Clin Immunol. 2024 Sep;154(3):767-777. doi: 10.1016/j.jaci.2024.05.001. Epub 2024 May 6.

Abstract

Background: LCP1 encodes L-plastin, an actin-bundling protein primarily expressed in hematopoietic cells. In mouse and fish models, LCP1 deficiency has been shown to result in hematologic and immune defects.

Objective: This study aimed to determine the nature of a human inborn error of immunity resulting from a novel genetic variant of LCP1.

Methods: We performed genetic, protein, and cellular analysis of PBMCs from a kindred with apparent autosomal dominant immune deficiency. We identified a candidate causal mutation in LCP1, which we evaluated by engineering the orthologous mutation in mice and Jurkat cells.

Results: A splice-site variant in LCP1 segregated with lymphopenia, neutropenia, and thrombocytopenia. The splicing defect resulted in at least 2 aberrant transcripts, producing an in-frame deletion of 24 nucleotides, and a frameshift deletion of exon 8. Cellular analysis of the kindred revealed a proportionate reduction of T and B cells and a mild expansion of transitional B cells. Similarly, mice carrying the orthologous genetic variant exhibited the same in-frame aberrant transcript, reduced expression Lcp1 and gene dose-dependent leukopenia, mild thrombocytopenia, and lymphopenia, with a significant reduction of T-cell populations. Functional analysis revealed that LCP1c740-1G>A confers a defect in platelet development and function with aberrant spreading on collagen. Immunologic analysis revealed defective actin organization in T cells, reduced migration of PBMCs from patients, splenocytes from mutant mice, and a mutant Jurkat cell line in response to CXCL12; impaired germinal center B-cell expansion after immunization; and reduced cytokinesis during T cell proliferation.

Conclusions: We describe a unique human hematopoietic defect affecting neutrophils, lymphocytes, and platelets arising from partial LCP1 deficiency.

Keywords: CRISPR/cas9; Immune deficiency; L-plastin; neutropenia; thrombocytopenia.

MeSH terms

  • Animals
  • Cytopenia
  • Female
  • Humans
  • Immunologic Deficiency Syndromes / genetics
  • Immunologic Deficiency Syndromes / immunology
  • Jurkat Cells
  • Lymphopenia / genetics
  • Lymphopenia / immunology
  • Male
  • Membrane Glycoproteins
  • Mice
  • Microfilament Proteins* / deficiency
  • Microfilament Proteins* / genetics
  • Mutation
  • Neutropenia / genetics
  • Neutropenia / immunology
  • Pedigree
  • Thrombocytopenia / genetics
  • Thrombocytopenia / immunology

Substances

  • plastin
  • Microfilament Proteins
  • Membrane Glycoproteins