Src regulates cigarette smoke-induced ceramide generation via neutral sphingomyelinase 2 in the airway epithelium

Am J Respir Cell Mol Biol. 2015 Jun;52(6):738-48. doi: 10.1165/rcmb.2014-0122OC.

Abstract

We previously demonstrated that the neutral sphingomyelinase (nSMase) 2 is the sole sphingomyelinase activated during cigarette smoke (CS)-induced oxidative stress of human airway epithelial cells, leading to ceramide generation and subsequent apoptosis of affected cells. Since then, we reported that nSMase2 is a phosphoprotein, the degree of enzymatic activity and stability of which are dictated by its degree of phosphorylation. Simultaneously, the non-receptor tyrosine kinase and proto-oncogene Src has increasingly become a target of interest in both smoking-related lung injury, such as chronic obstructive pulmonary disease, and lung cancer. Within this context, we tested and now present Src as a regulator of ceramide generation via modulation of nSMase2 phosphorylation and activity during CS-induced oxidative stress. Specifically, we provide evidence that Src activity is necessary for both CS-induced ceramide accumulation in vivo (129/Sv mice) and in vitro (human airway epithelial cells) and for nSMase2 activity during CS-induced oxidative stress. Moreover, because nSMase2 is exclusively phosphorylated on serines, we show that this occurs through Src-dependent activation of the serine/threonine kinase p38 mitogen-activated protein kinase during oxidative stress. Finally, we provide evidence that Src and p38 mitogen-activated protein kinase activities are critical for regulating nSMase2 phosphorylation. This study provides insights into a molecular target involved in smoking-related lung injury, represented here as nSMase2, and its modulation by the oncogene Src.

Keywords: Src; ceramide; neutral sphingomyelinase 2; sphingolipids.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Cell Line, Tumor
  • Ceramides / biosynthesis*
  • Enzyme Activation
  • Epithelium / enzymology
  • Humans
  • Lung Diseases / enzymology*
  • Lung Diseases / etiology
  • Lung Diseases / pathology
  • Mice, 129 Strain
  • Oxidative Stress
  • Phosphorylation
  • Protein Processing, Post-Translational
  • Proto-Oncogene Mas
  • Respiratory Mucosa / enzymology*
  • Smoking / adverse effects*
  • Sphingomyelin Phosphodiesterase / physiology*
  • p38 Mitogen-Activated Protein Kinases / metabolism
  • src-Family Kinases / physiology*

Substances

  • Ceramides
  • MAS1 protein, human
  • Proto-Oncogene Mas
  • src-Family Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Smpd3 protein, mouse
  • Sphingomyelin Phosphodiesterase