Chronic Cigarette Smoke Exposure Subdues PP2A Activity by Enhancing Expression of the Oncogene CIP2A

Am J Respir Cell Mol Biol. 2018 Dec;59(6):695-705. doi: 10.1165/rcmb.2018-0173OC.

Abstract

Phosphatase activity of the major serine threonine phosphatase, protein phosphatase 2A (PP2A), is blunted in the airways of individuals with chronic obstructive pulmonary disease (COPD), which results in heightened inflammation and proteolytic responses. The objective of this study was to investigate how PP2A activity is modulated in COPD airways. PP2A activity and endogenous inhibitors of PP2A were investigated in animal and cell models of COPD. In primary human bronchial epithelial (HBE) cells isolated from smokers and donors with COPD, we observed enhanced expression of cancerous inhibitor of PP2A (CIP2A), an oncoprotein encoded by the KIAA1524 gene, compared with cells from nonsmokers. CIP2A expression was induced by chronic cigarette smoke exposure in mice that coincided with a reduction in PP2A activity, airspace enlargements, and loss of lung function, as determined by PP2A phosphatase activity, mean linear intercept analysis, and forced expiratory volume in 0.05 second/forced vital capacity. Modulating CIP2A expression in HBE cells by silencing RNA or chemically with erlotinib enhanced PP2A activity, reduced extracellular-signal-regulated kinase phosphorylation, and reduced the responses of matrix metalloproteinases 1 and 9 in HBE cells isolated from subjects with COPD. Enhanced epithelial growth factor receptor responses in cells from subjects with COPD were observed to modulate CIP2A expression levels. Our study indicates that chronic cigarette smoke induction of epithelial growth factor receptor signaling and CIP2A expression can impair PP2A responses that are associated with loss of lung function and enhancement of proteolytic responses. Augmenting PP2A activity by manipulating CIP2A expression may represent a feasible therapeutic approach to counter smoke-induced lung disease.

Keywords: cancerous inhibitor of PP2A; chronic obstructive pulmonary disease; cigarette smoke; protein phosphatase 2A.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autoantigens / metabolism*
  • Cells, Cultured
  • Cigarette Smoking / adverse effects*
  • Environmental Exposure / adverse effects*
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Oncogene Proteins / metabolism
  • Protein Phosphatase 2 / metabolism*
  • Proteolysis
  • Pulmonary Disease, Chronic Obstructive / etiology
  • Pulmonary Disease, Chronic Obstructive / metabolism*
  • Pulmonary Disease, Chronic Obstructive / pathology

Substances

  • Autoantigens
  • CIP2A protein, human
  • Intracellular Signaling Peptides and Proteins
  • KIAA1524 protein, mouse
  • Membrane Proteins
  • Oncogene Proteins
  • Protein Phosphatase 2