Linear Integration of ERK Activity Predominates over Persistence Detection in Fra-1 Regulation

Cell Syst. 2017 Dec 27;5(6):549-563.e5. doi: 10.1016/j.cels.2017.10.019. Epub 2017 Nov 29.

Abstract

ERK signaling regulates the expression of target genes, but it is unclear how ERK activity dynamics are interpreted. Here, we investigate this question using simultaneous, live, single-cell imaging of two ERK activity reporters and expression of Fra-1, a target gene controlling epithelial cell identity. We find that Fra-1 is expressed in proportion to the amplitude and duration of ERK activity. In contrast to previous "persistence detector" and "selective filter" models in which Fra-1 expression only occurs when ERK activity persists beyond a threshold duration, our observations demonstrate that the network regulating Fra-1 expression integrates total ERK activity and responds to it linearly. However, exploration of a generalized mathematical model of the Fra-1 coherent feedforward loop demonstrates that it can perform either linear integration or persistence detection, depending on the basal mRNA production rate and protein production delays. Our data indicate that significant basal expression and short delays cause Fra-1 to respond linearly to integrated ERK activity.

Keywords: EGF; EGFR; FOSL1; FRET; KTR; MAPK; Ras; c-Fos degradation; signal transduction dynamics; transcription.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation / genetics
  • Epidermal Growth Factor / metabolism
  • Epithelial Cells / physiology*
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Genes, Reporter
  • Humans
  • MAP Kinase Signaling System*
  • Models, Biological
  • Proto-Oncogene Proteins c-fos / genetics
  • Proto-Oncogene Proteins c-fos / metabolism*
  • Signal Transduction*
  • Single-Cell Analysis

Substances

  • Proto-Oncogene Proteins c-fos
  • fos-related antigen 1
  • Epidermal Growth Factor
  • Extracellular Signal-Regulated MAP Kinases