Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling

Biochem Pharmacol. 2002 Sep;64(5-6):755-63. doi: 10.1016/s0006-2952(02)01135-8.

Abstract

Extracellular signals transduced via receptor tyrosine kinases, G-protein-coupled receptors or integrins activate Ras, a key switch in cellular signalling. Although Ras can activate multiple downstream effectors (PI3K, Ral em leader ) one of the major activated pathway is a conserved sequential protein kinase cascade referred to as the mitogen activated protein (MAP) kinase module: Raf>MEK>ERK. The fidelity of signalling among protein kinases and the spatio-temporal activation are certainly key determinants for generating precise biological responses. The fidelity is ensured by scaffold proteins, a sort of protein kinase "insulators" and/or specific docking sites among the members of the signalling cascade. These docking sites are found in upstream and downstream regulators and MAPK substrates [Nat Cell Biol 2 2000 110]. The duration and the intensity of the response are in part controlled by the compartmentalisation of the signalling molecules. Growth factors promote nuclear accumulation and persistent activation of ERK (p42/p44 MAP kinases) during the entire G1 period with an extinction during S-phase. These features are exquisitely well controlled by (i) the temporal induction of the MAP kinase phosphatases, MKP1-3, and (ii) the compartmentalisation of the signalling molecules. We have shown that MKP1-2 induction is strictly controlled by the activation of the MAP kinase module providing evidence for an autoregulatory mechanism. This negative regulatory loop was further enhanced by the capacity of ERK to phosphorylate MKP1 and 2. This action reduced the degradation rate of these MKPs through the ubiquitin-proteasomal system [Science 286 1999 2514]. Whereas the two upstream kinases of the module, Raf and MEK remained cytoplasmic, ERK anchored to MEK in the cytoplasm of resting cells, rapidly translocated to the nucleus upon mitogenic stimulation. This process was rapid, reversible, and controlled by the strict activation of the MAPK cascade. Prevention of this nuclear translocation, by overexpression of a cytoplasmic ERK-docking molecule (inactive MKP3) prevented growth factor-stimulated DNA replication [EMBO J 18 1999 664]. Following long term stimulation, ERK progressively accumulated in the nucleus in an inactive form. This nuclear retention relied on the neosynthesis of short-lived nuclear anchoring proteins. Nuclear inactivation and sequestration was likely to be controlled by MAP kinase phosphatases 1 and 2. Therefore we propose that the nucleus represents a site for ERK action, sequestration and signal termination [J Cell Sci 114 2001 3433]. In addition, with the generation of mice invalidated for each of the ERK isoforms, we will illustrate that besides controlling cell proliferation the ERK cascade also controls cell differentiation and cell behaviour [Science 286 1999 1374].

Publication types

  • Review

MeSH terms

  • Animals
  • Cell Nucleus / metabolism
  • Enzyme Activation
  • Humans
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases / metabolism*
  • Phosphoric Monoester Hydrolases / metabolism
  • Signal Transduction / physiology*
  • Subcellular Fractions

Substances

  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases
  • Phosphoric Monoester Hydrolases