Bypassing a kinase activity with an ATP-competitive drug

Science. 2003 Nov 28;302(5650):1533-7. doi: 10.1126/science.1090031. Epub 2003 Oct 16.

Abstract

Unfolded proteins in the endoplasmic reticulum cause trans-autophosphorylation of the bifunctional transmembrane kinase Ire1, which induces its endoribonuclease activity. The endoribonuclease initiates nonconventional splicing of HAC1 messenger RNA to trigger the unfolded-protein response (UPR). We explored the role of Ire1's kinase domain by sensitizing it through site-directed mutagenesis to the ATP-competitive inhibitor 1NM-PP1. Paradoxically, rather than being inhibited by 1NM-PP1, drug-sensitized Ire1 mutants required 1NM-PP1 as a cofactor for activation. In the presence of 1NM-PP1, drug-sensitized Ire1 bypassed mutations that inactivate its kinase activity and induced a full UPR. Thus, rather than through phosphorylation per se, a conformational change in the kinase domain triggered by occupancy of the active site with a ligand leads to activation of all known downstream functions.

Publication types

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

MeSH terms

  • Adenosine Diphosphate / pharmacology
  • Adenosine Triphosphate / analogs & derivatives
  • Adenosine Triphosphate / chemistry
  • Adenosine Triphosphate / metabolism*
  • Adenosine Triphosphate / pharmacology
  • Basic-Leucine Zipper Transcription Factors
  • Binding Sites
  • Binding, Competitive
  • Cytosol / metabolism
  • Dithiothreitol / pharmacology
  • Endoplasmic Reticulum / metabolism*
  • Endoribonucleases / metabolism
  • Enzyme Activation
  • Ligands
  • Membrane Glycoproteins / antagonists & inhibitors
  • Membrane Glycoproteins / chemistry*
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Models, Biological
  • Mutagenesis, Site-Directed
  • Phosphorylation
  • Protein Conformation
  • Protein Folding*
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Protein Serine-Threonine Kinases / chemistry*
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Structure, Tertiary
  • Pyrazoles / chemistry
  • Pyrazoles / metabolism*
  • Pyrazoles / pharmacology*
  • Pyrimidines / chemistry
  • Pyrimidines / metabolism*
  • Pyrimidines / pharmacology*
  • RNA Splicing
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Saccharomyces cerevisiae Proteins / antagonists & inhibitors
  • Saccharomyces cerevisiae Proteins / chemistry*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Signal Transduction
  • Structure-Activity Relationship
  • Substrate Specificity
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Up-Regulation

Substances

  • 1-tert-butyl-3-naphthalen-1-ylmethyl-1H-pyrazolo(3,4-d)pyrimidin-4-ylemine
  • Basic-Leucine Zipper Transcription Factors
  • HAC1 protein, S cerevisiae
  • Ligands
  • Membrane Glycoproteins
  • Pyrazoles
  • Pyrimidines
  • RNA, Messenger
  • Repressor Proteins
  • Saccharomyces cerevisiae Proteins
  • Transcription Factors
  • Adenosine Diphosphate
  • Adenosine Triphosphate
  • IRE1 protein, S cerevisiae
  • Protein Serine-Threonine Kinases
  • Endoribonucleases
  • Dithiothreitol
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