Actin dynamics regulation by TTC7A/PI4KIIIα limits DNA damage and cell death under confinement

J Allergy Clin Immunol. 2023 Oct;152(4):949-960. doi: 10.1016/j.jaci.2023.06.016. Epub 2023 Jun 29.

Abstract

Background: The actin cytoskeleton has a crucial role in the maintenance of the immune homeostasis by controlling various cellular processes, including cell migration. Mutations in TTC7A have been described as the cause of a primary immunodeficiency associated to different degrees of gut involvement and alterations in the actin cytoskeleton dynamics.

Objectives: This study investigates the impact of TTC7A deficiency in immune homeostasis. In particular, the role of the TTC7A/phosphatidylinositol 4 kinase type III α pathway in the control of leukocyte migration and actin dynamics.

Methods: Microfabricated devices were leveraged to study cell migration and actin dynamics of murine and patient-derived leukocytes under confinement at the single-cell level.

Results: We show that TTC7A-deficient lymphocytes exhibit an altered cell migration and reduced capacity to deform through narrow gaps. Mechanistically, TTC7A-deficient phenotype resulted from impaired phosphoinositide signaling, leading to the downregulation of the phosphoinositide 3-kinase/AKT/RHOA regulatory axis and imbalanced actin cytoskeleton dynamics. TTC7A-associated phenotype resulted in impaired cell motility, accumulation of DNA damage, and increased cell death in dense 3-dimensional gels in the presence of chemokines.

Conclusions: These results highlight a novel role of TTC7A as a critical regulator of lymphocyte migration. Impairment of this cellular function is likely to contribute to the pathophysiology underlying progressive immunodeficiency in patients.

Keywords: TTC7A; actin dynamics; cell migration; cell survival under confinement; nuclear deformation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1-Phosphatidylinositol 4-Kinase
  • Actins*
  • Animals
  • Cell Death
  • Cell Movement / genetics
  • DNA Damage
  • Humans
  • Mice
  • Mutation
  • Phosphatidylinositol 3-Kinases*
  • Proteins

Substances

  • Actins
  • Phosphatidylinositol 3-Kinases
  • TTC7A protein, human
  • Proteins
  • PI4KIIIalpha protein, human
  • 1-Phosphatidylinositol 4-Kinase