ETS-1-mediated transcriptional up-regulation of CD44 is required for sphingosine-1-phosphate receptor subtype 3-stimulated chemotaxis

J Biol Chem. 2013 Nov 8;288(45):32126-32137. doi: 10.1074/jbc.M113.495218. Epub 2013 Sep 24.

Abstract

Sphingosine-1-phosphate (S1P)-regulated chemotaxis plays critical roles in various physiological and pathophysiological conditions. S1P-regulated chemotaxis is mediated by the S1P family of G-protein-coupled receptors. However, molecular details of the S1P-regulated chemotaxis are incompletely understood. Cultured human lung adenocarcinoma cell lines abundantly express S1P receptor subtype 3 (S1P3), thus providing a tractable in vitro system to characterize molecular mechanism(s) underlying the S1P3 receptor-regulated chemotactic response. S1P treatment enhances CD44 expression and induces membrane localization of CD44 polypeptides via the S1P3/Rho kinase (ROCK) signaling pathway. Knockdown of CD44 completely diminishes the S1P-stimulated chemotaxis. Promoter analysis suggests that the CD44 promoter contains binding sites of the ETS-1 (v-ets erythroblastosis virus E26 oncogene homolog 1) transcriptional factor. ChIP assay confirms that S1P treatment stimulates the binding of ETS-1 to the CD44 promoter region. Moreover, S1P induces the expression and nuclear translocation of ETS-1. Knockdown of S1P3 or inhibition of ROCK abrogates the S1P-induced ETS-1 expression. Furthermore, knockdown of ETS-1 inhibits the S1P-induced CD44 expression and cell migration. In addition, we showed that S1P3/ROCK signaling up-regulates ETS-1 via the activity of JNK. Collectively, we characterized a novel signaling axis, i.e., ROCK-JNK-ETS-1-CD44 pathway, which plays an essential role in the S1P3-regulated chemotactic response.

Keywords: CD44; Chemotaxis; Ets Family Transcription Factor; Jun N-terminal Kinase (JNK); Lipids; Receptors; Signal Transduction.

Publication types

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

MeSH terms

  • Cell Line, Tumor
  • Chemotaxis / physiology*
  • Gene Knockdown Techniques
  • Humans
  • Hyaluronan Receptors / biosynthesis*
  • Hyaluronan Receptors / genetics
  • Lysophospholipids / genetics
  • Lysophospholipids / metabolism
  • MAP Kinase Kinase 4 / genetics
  • MAP Kinase Kinase 4 / metabolism
  • Proto-Oncogene Protein c-ets-1 / genetics
  • Proto-Oncogene Protein c-ets-1 / metabolism*
  • Receptors, Lysosphingolipid / agonists
  • Receptors, Lysosphingolipid / genetics
  • Receptors, Lysosphingolipid / metabolism*
  • Signal Transduction / physiology*
  • Sphingosine / analogs & derivatives
  • Sphingosine / genetics
  • Sphingosine / metabolism
  • Transcription, Genetic / physiology*
  • Up-Regulation / physiology*
  • rho-Associated Kinases / genetics
  • rho-Associated Kinases / metabolism

Substances

  • CD44 protein, human
  • ETS1 protein, human
  • Hyaluronan Receptors
  • Lysophospholipids
  • Proto-Oncogene Protein c-ets-1
  • Receptors, Lysosphingolipid
  • sphingosine 1-phosphate
  • rho-Associated Kinases
  • MAP Kinase Kinase 4
  • Sphingosine