IL-13 and IL-17A activate β1 integrin through an NF-kB/Rho kinase/PIP5K1γ pathway to enhance force transmission in airway smooth muscle

Proc Natl Acad Sci U S A. 2024 Aug 20;121(34):e2401251121. doi: 10.1073/pnas.2401251121. Epub 2024 Aug 13.

Abstract

Integrin activation resulting in enhanced adhesion to the extracellular matrix plays a key role in fundamental cellular processes. Although integrin activation has been extensively studied in circulating cells such as leukocytes and platelets, much less is known about the regulation and functional impact of integrin activation in adherent cells such as smooth muscle. Here, we show that two different asthmagenic cytokines, IL-13 and IL-17A, activate type I and IL-17 cytokine receptor families, respectively, to enhance adhesion of airway smooth muscle. These cytokines also induce activation of β1 integrins detected by the conformation-specific antibody HUTS-4. Moreover, HUTS-4 binding is increased in the smooth muscle of patients with asthma compared to nonsmokers without lung disease, suggesting a disease-relevant role for integrin activation in smooth muscle. Indeed, integrin activation induced by the β1-activating antibody TS2/16, the divalent cation manganese, or the synthetic peptide β1-CHAMP that forces an extended-open integrin conformation dramatically enhances force transmission in smooth muscle cells and airway rings even in the absence of cytokines. We demonstrate that cytokine-induced activation of β1 integrins is regulated by a common pathway of NF-κB-mediated induction of RhoA and its effector Rho kinase, which in turn stimulates PIP5K1γ-mediated synthesis of PIP2 at focal adhesions, resulting in β1 integrin activation. Taken together, these data identify a pathway by which type I and IL-17 cytokine receptor family stimulation induces functionally relevant β1 integrin activation in adherent smooth muscle and help to explain the exaggerated force transmission that characterizes chronic airway diseases such as asthma.

Keywords: force transmission; integrin activation; smooth muscle.

MeSH terms

  • Animals
  • Asthma* / metabolism
  • Cell Adhesion
  • Humans
  • Integrin beta1* / metabolism
  • Interleukin-13* / metabolism
  • Interleukin-17* / metabolism
  • Muscle, Smooth* / metabolism
  • Myocytes, Smooth Muscle / metabolism
  • NF-kappa B* / metabolism
  • Signal Transduction
  • rho-Associated Kinases* / metabolism

Substances

  • Integrin beta1
  • Interleukin-17
  • NF-kappa B
  • rho-Associated Kinases
  • Interleukin-13
  • IL17A protein, human