p38 MAPK down-regulates fibulin 3 expression through methylation of gene regulatory sequences: role in migration and invasion

J Biol Chem. 2015 Feb 13;290(7):4383-97. doi: 10.1074/jbc.M114.582239. Epub 2014 Dec 29.

Abstract

p38 MAPKs regulate migration and invasion. However, the mechanisms involved are only partially known. We had previously identified fibulin 3, which plays a role in migration, invasion, and tumorigenesis, as a gene regulated by p38α. We have characterized in detail how p38 MAPK regulates fibulin 3 expression and its role. We describe here for the first time that p38α, p38γ, and p38δ down-regulate fibulin 3 expression. p38α has a stronger effect, and it does so through hypermethylation of CpG sites in the regulatory sequences of the gene. This would be mediated by the DNA methylase, DNMT3A, which is down-regulated in cells lacking p38α, but once re-introduced represses Fibulin 3 expression. p38α through HuR stabilizes dnmt3a mRNA leading to an increase in DNMT3A protein levels. Moreover, by knocking-down fibulin 3, we have found that Fibulin 3 inhibits migration and invasion in MEFs by mechanisms involving p38α/β inhibition. Hence, p38α pro-migratory/invasive effect might be, at least in part, mediated by fibulin 3 down-regulation in MEFs. In contrast, in HCT116 cells, Fibulin 3 promotes migration and invasion through a mechanism dependent on p38α and/or p38β activation. Furthermore, Fibulin 3 promotes in vitro and in vivo tumor growth of HCT116 cells through a mechanism dependent on p38α, which surprisingly acts as a potent inducer of tumor growth. At the same time, p38α limits fibulin 3 expression, which might represent a negative feed-back loop.

Keywords: cancer biology; cell signaling; fibulin 3; invasion; migration; p38 MAPK.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Adhesion
  • Cell Movement*
  • Cell Proliferation
  • Cells, Cultured
  • Colonic Neoplasms / genetics
  • Colonic Neoplasms / metabolism
  • Colonic Neoplasms / pathology*
  • DNA Methylation*
  • Down-Regulation
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / metabolism*
  • Extracellular Matrix Proteins / genetics*
  • Extracellular Matrix Proteins / metabolism
  • Fibroblasts / cytology
  • Fibroblasts / metabolism*
  • Gene Expression Regulation*
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Mice, Nude
  • Mitogen-Activated Protein Kinase 14 / physiology*
  • Neoplasm Invasiveness
  • Promoter Regions, Genetic / genetics
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Response Elements / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Wound Healing
  • Xenograft Model Antitumor Assays

Substances

  • Efemp1 protein, mouse
  • Extracellular Matrix Proteins
  • RNA, Messenger
  • Mitogen-Activated Protein Kinase 14