Mechanism of homodimeric cytokine receptor activation and dysregulation by oncogenic mutations.


Journal

Science (New York, N.Y.)
ISSN: 1095-9203
Titre abrégé: Science
Pays: United States
ID NLM: 0404511

Informations de publication

Date de publication:
07 02 2020
Historique:
received: 12 12 2018
revised: 08 10 2019
accepted: 20 12 2019
entrez: 8 2 2020
pubmed: 8 2 2020
medline: 17 4 2020
Statut: ppublish

Résumé

Homodimeric class I cytokine receptors are assumed to exist as preformed dimers that are activated by ligand-induced conformational changes. We quantified the dimerization of three prototypic class I cytokine receptors in the plasma membrane of living cells by single-molecule fluorescence microscopy. Spatial and spatiotemporal correlation of individual receptor subunits showed ligand-induced dimerization and revealed that the associated Janus kinase 2 (JAK2) dimerizes through its pseudokinase domain. Oncogenic receptor and hyperactive JAK2 mutants promoted ligand-independent dimerization, highlighting the formation of receptor dimers as the switch responsible for signal activation. Atomistic modeling and molecular dynamics simulations based on a detailed energetic analysis of the interactions involved in dimerization yielded a mechanistic blueprint for homodimeric class I cytokine receptor activation and its dysregulation by individual mutations.

Identifiants

pubmed: 32029621
pii: 367/6478/643
doi: 10.1126/science.aaw3242
pmc: PMC8117407
mid: NIHMS1694456
doi:

Substances chimiques

Ligands 0
Nitriles 0
Pyrazoles 0
Pyrimidines 0
Receptors, Erythropoietin 0
Receptors, Somatotropin 0
Receptors, Thrombopoietin 0
Phenylalanine 47E5O17Y3R
ruxolitinib 82S8X8XX8H
Janus Kinase 2 EC 2.7.10.2
Valine HG18B9YRS7

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

643-652

Subventions

Organisme : European Research Council
Pays : International
Organisme : NIAID NIH HHS
ID : R37 AI051321
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI101256
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI051321
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom

Informations de copyright

Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.

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Auteurs

Stephan Wilmes (S)

Department of Biology and Center of Cellular Nanoanalytics, University of Osnabrück, 49076 Osnabrück, Germany.
Division of Cell Signalling and Immunology, School of Life Sciences, University of Dundee, Dundee, UK.

Maximillian Hafer (M)

Department of Biology and Center of Cellular Nanoanalytics, University of Osnabrück, 49076 Osnabrück, Germany.

Joni Vuorio (J)

Department of Physics, University of Helsinki, Helsinki, Finland.
Computational Physics Laboratory, Tampere University, Tampere, Finland.

Julie A Tucker (JA)

York Biomedical Research Institute and Department of Biology, University of York, Heslington, York YO10 5DD, UK.

Hauke Winkelmann (H)

Department of Biology and Center of Cellular Nanoanalytics, University of Osnabrück, 49076 Osnabrück, Germany.

Sara Löchte (S)

Department of Biology and Center of Cellular Nanoanalytics, University of Osnabrück, 49076 Osnabrück, Germany.

Tess A Stanly (TA)

York Biomedical Research Institute and Department of Biology, University of York, Heslington, York YO10 5DD, UK.

Katiuska D Pulgar Prieto (KD)

York Biomedical Research Institute and Department of Biology, University of York, Heslington, York YO10 5DD, UK.

Chetan Poojari (C)

Department of Physics, University of Helsinki, Helsinki, Finland.

Vivek Sharma (V)

Department of Physics, University of Helsinki, Helsinki, Finland.
Institute of Biotechnology, University of Helsinki, Helsinki, Finland.

Christian P Richter (CP)

Department of Biology and Center of Cellular Nanoanalytics, University of Osnabrück, 49076 Osnabrück, Germany.

Rainer Kurre (R)

Department of Biology and Center of Cellular Nanoanalytics, University of Osnabrück, 49076 Osnabrück, Germany.

Stevan R Hubbard (SR)

Skirball Institute and Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY, USA.

K Christopher Garcia (KC)

Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA, USA.
Department of Molecular and Cellular Physiology and Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA.

Ignacio Moraga (I)

Division of Cell Signalling and Immunology, School of Life Sciences, University of Dundee, Dundee, UK.

Ilpo Vattulainen (I)

Department of Physics, University of Helsinki, Helsinki, Finland. ilpo.vattulainen@helsinki.fi ian.hitchcock@york.ac.uk piehler@uos.de.
Computational Physics Laboratory, Tampere University, Tampere, Finland.

Ian S Hitchcock (IS)

York Biomedical Research Institute and Department of Biology, University of York, Heslington, York YO10 5DD, UK. ilpo.vattulainen@helsinki.fi ian.hitchcock@york.ac.uk piehler@uos.de.

Jacob Piehler (J)

Department of Biology and Center of Cellular Nanoanalytics, University of Osnabrück, 49076 Osnabrück, Germany. ilpo.vattulainen@helsinki.fi ian.hitchcock@york.ac.uk piehler@uos.de.

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Classifications MeSH