Germline LCP1 mutations cause immunodeficiency with neutropenia, monocytopenia, lymphopenia and defective cytokinesis

  • Thijs van Bergen
  • , Dennis Bosch
  • , Christine Bellanné-Chantelot
  • , Roger Mulet-Lazaro
  • , Jacob R Bledsoe
  • , Lanpeng Chen
  • , Hans W J de Looper
  • , Claire van Dijk
  • , Mariëtte Ter Borg
  • , Eric Bindels
  • , Remco Hoogenboezem
  • , Onno Roovers
  • , Patricia A Olofsen
  • , Marije Bartels
  • , Joris M van Montfrans
  • , Puck Breed
  • , Elisabeth Salzer
  • , Marloes G Holierhoek
  • , Brigittie Nelken
  • , Blandine Beaupain
  • Mark Daniel Fleming, Akiko Shimamura, Marc H G P Raaijmakers, Jean Donadieu, Peter E Newburger, Ivo P Touw, Anna M Aalbers*
*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Severe congenital neutropenia (SCN) is characterized by neutropenia, recurrent infections, and an increased leukemia risk. Multiple genetic defects that underlie SCN have been identified, but a genetic diagnosis is still lacking in a significant proportion of patients. In this study, we report 4 independent pedigrees with heterozygous variants in LCP1. Variants c.740-1G>T and c.740-20_744del produced the same alternatively spliced RNA product, causing an in-frame deletion (p.A247_E254del). Variant c.509C>T in the third pedigree produced p.S170L, and variant c.806T>C in the fourth pedigree produced p.L269P. Affected individuals suffered from neutropenia, poor or complete lack of response to granulocyte colony–stimulating factor (G-CSF) treatment, and variable degrees of lymphopenia, hypogammaglobulinemia, and monocytopenia. Patients with A247_E254del and p.L269P presented with tetraploid cells in the bone marrow, indicative of disturbed cytokinesis. In one of these kindreds, 2 individuals developed acute leukemia. G-CSF nonresponsiveness and defective cell cycling were repaired upon correction of the LCP1 A247_E254del variant in patient-derived induced pluripotent stem cells, supporting the monogenic origin of the disease. Indicative of their gain-of-function effect, both the A247_E254del and S170L variants increased F-actin bundling and the formation of abnormal protrusions. Single-cell transcriptome analysis of A247_E254del bone marrow-derived hematopoietic stem and progenitor cells (HSPCs) showed deregulation of signaling pathways that control mitosis in multilineage and lymphoid-primed HSPC subsets. We concluded that activating LCP1 variants cause a new hematopoietic disorder with autosomal dominant inheritance. Depending on the consequences of the LCP1 variants in terms of protein structure, patients may suffer from G-CSF refractory severe neutropenia, lymphopenia, hypogammaglobulinemia, monocytopenia, and defective cytokinesis.

Original languageEnglish
Pages (from-to)627-641
Number of pages15
JournalBlood Advances
Volume10
Issue number3
Early online date7 Oct 2025
DOIs
Publication statusPublished - 10 Feb 2026

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