Model Predicts That MKP1 and TAB1 Regulate p38α Nuclear Pulse and Its Basal Activity through Positive and Negative Feedback Loops in Response to IL-1

PLoS One. 2016 Jun 17;11(6):e0157572. doi: 10.1371/journal.pone.0157572. eCollection 2016.

Abstract

Interleukin-1 mediates inflammation and stress response through nuclear activity of p38α. Although IL-1 receptor is not degraded, p38α activation is transient. IL-1 also causes cell migration and EMT by modulating cell-cell junctions. Although molecules involved in p38 activation are known, mechanism of the transient nuclear response and its basal activity remains unknown. By mathematical modeling of IL1/p38 signaling network, we show that IL-1 induces robust p38α activation both in the nucleus and in the cytoplasm/membrane. While nuclear response consists of an acute phase, membrane response resembles a step change. Following stimulation, p38α activity returns to a basal level in absence of receptor degradation. While nuclear pulse is controlled by MKP1 through a negative feedback to pp38, its basal activity is controlled by both TAB1 and MKP1 through a positive feedback loop. Our model provides insight into the mechanism of p38α activation, reason for its transient nuclear response, and explanation of the basal activity of MKK3/6 and p38α, which has been experimentally observed by other groups.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics*
  • Adaptor Proteins, Signal Transducing / metabolism
  • Amino Acid Sequence / genetics
  • Cell Movement / genetics
  • Cytoplasm / enzymology
  • Enzyme Activation / genetics
  • Feedback, Physiological
  • Humans
  • Inflammation / enzymology
  • Inflammation / genetics*
  • Inflammation / pathology
  • Intercellular Junctions / genetics
  • MAP Kinase Kinase 3 / genetics
  • Mitogen-Activated Protein Kinase Phosphatases / genetics*
  • Models, Theoretical
  • Nuclear Envelope / enzymology
  • Phosphorylation
  • Signal Transduction
  • Stress, Physiological / genetics*
  • p38 Mitogen-Activated Protein Kinases / biosynthesis*
  • p38 Mitogen-Activated Protein Kinases / genetics

Substances

  • Adaptor Proteins, Signal Transducing
  • TAB1 protein, human
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 3
  • MAP2K3 protein, human
  • Mitogen-Activated Protein Kinase Phosphatases

Grants and funding

This work was supported by Indian Institute of Technology Kanpur grant IITK/CHE/20090282 to RS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.