TGF-β1 Evokes Human Airway Smooth Muscle Cell Shortening and Hyperresponsiveness via Smad3

Am J Respir Cell Mol Biol. 2018 May;58(5):575-584. doi: 10.1165/rcmb.2017-0247OC.

Abstract

Transforming growth factor β1 (TGF-β1), a cytokine whose levels are elevated in the airways of patients with asthma, perpetuates airway inflammation and modulates airway structural cell remodeling. However, the role of TGF-β1 in excessive airway narrowing in asthma, or airway hyperresponsiveness (AHR), remains unclear. In this study, we set out to investigate the direct effects of TGF-β1 on human airway smooth muscle (HASM) cell shortening and hyperresponsiveness. The dynamics of AHR and single-cell excitation-contraction coupling were measured in human precision-cut lung slices and in isolated HASM cells using supravital microscopy and magnetic twisting cytometry, respectively. In human precision-cut lung slices, overnight treatment with TGF-β1 significantly augmented basal and carbachol-induced bronchoconstriction. In isolated HASM cells, TGF-β1 increased basal and methacholine-induced cytoskeletal stiffness in a dose- and time-dependent manner. TGF-β1-induced single-cell contraction was corroborated by concomitant increases in myosin light chain and myosin phosphatase target subunit 1 phosphorylation levels, which were attenuated by small interfering RNA-mediated knockdown of Smad3 and pharmacological inhibition of Rho kinase. Strikingly, these physiological effects of TGF-β1 occurred through a RhoA-independent mechanism, with little effect on HASM cell [Ca2+]i levels. Together, our data suggest that TGF-β1 enhances HASM excitation-contraction coupling pathways to induce HASM cell shortening and hyperresponsiveness. These findings reveal a potential link between airway injury-repair responses and bronchial hyperreactivity in asthma, and define TGF-β1 signaling as a potential target to reduce AHR in asthma.

Keywords: asthma; bronchoconstriction; contraction; cytokines; remodeling.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Asthma / metabolism*
  • Asthma / physiopathology
  • Bronchial Hyperreactivity / metabolism*
  • Bronchial Hyperreactivity / physiopathology
  • Bronchoconstriction / drug effects*
  • Calcium Signaling / drug effects*
  • Cells, Cultured
  • Excitation Contraction Coupling / drug effects
  • Humans
  • Muscle, Smooth / drug effects*
  • Muscle, Smooth / metabolism
  • Muscle, Smooth / physiopathology
  • Myocytes, Smooth Muscle / drug effects*
  • Myocytes, Smooth Muscle / metabolism
  • Myosin Light Chains / metabolism
  • Myosin-Light-Chain Phosphatase / metabolism
  • Phosphorylation
  • Smad3 Protein / genetics
  • Smad3 Protein / metabolism*
  • Transforming Growth Factor beta1 / pharmacology*
  • rho-Associated Kinases / metabolism
  • rhoA GTP-Binding Protein / metabolism

Substances

  • Myosin Light Chains
  • SMAD3 protein, human
  • Smad3 Protein
  • Transforming Growth Factor beta1
  • RHOA protein, human
  • rho-Associated Kinases
  • Myosin-Light-Chain Phosphatase
  • PPP1R12A protein, human
  • rhoA GTP-Binding Protein