Mislocalization of protein kinase A drives pathology in Cushing's syndrome.

CP: Cell biology CP: Metabolism PRKACA adrenal anchoring cortisol photoactivation proteomics proximity biotinylation scaffold signaling stress hormone

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
12 07 2022
Historique:
received: 27 01 2022
revised: 20 04 2022
accepted: 17 06 2022
entrez: 13 7 2022
pubmed: 14 7 2022
medline: 16 7 2022
Statut: ppublish

Résumé

Mutations in the catalytic subunit of protein kinase A (PKAc) drive the stress hormone disorder adrenal Cushing's syndrome. We define mechanisms of action for the PKAc-L205R and W196R variants. Proximity proteomic techniques demonstrate that both Cushing's mutants are excluded from A kinase-anchoring protein (AKAP)-signaling islands, whereas live-cell photoactivation microscopy reveals that these kinase mutants indiscriminately diffuse throughout the cell. Only cAMP analog drugs that displace native PKAc from AKAPs enhance cortisol release. Rescue experiments that incorporate PKAc mutants into AKAP complexes abolish cortisol overproduction, indicating that kinase anchoring restores normal endocrine function. Analyses of adrenal-specific PKAc-W196R knockin mice and Cushing's syndrome patient tissue reveal defective signaling mechanisms of the disease. Surprisingly each Cushing's mutant engages a different mitogenic-signaling pathway, with upregulation of YAP/TAZ by PKAc-L205R and ERK kinase activation by PKAc-W196R. Thus, aberrant spatiotemporal regulation of each Cushing's variant promotes the transmission of distinct downstream pathogenic signals.

Identifiants

pubmed: 35830806
pii: S2211-1247(22)00871-3
doi: 10.1016/j.celrep.2022.111073
pmc: PMC9311266
mid: NIHMS1823265
pii:
doi:

Substances chimiques

Cyclic AMP-Dependent Protein Kinases EC 2.7.11.11
Hydrocortisone WI4X0X7BPJ

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

111073

Subventions

Organisme : Cancer Research UK
ID : C1443/A22095
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R01 GM129090
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK119192
Pays : United States
Organisme : NIDDK NIH HHS
ID : F32 DK121415
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/S018514/1
Pays : United Kingdom
Organisme : NIH HHS
ID : S10 OD021502
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK119186
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/T018127/1
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : T32 GM007270
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK123694
Pays : United States

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Mitchell H Omar (MH)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA. Electronic address: mho6@uw.edu.

Dominic P Byrne (DP)

Department of Biochemistry & Systems Biology, University of Liverpool, Liverpool L69 7ZB, UK.

Kiana N Jones (KN)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

Tyler M Lakey (TM)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

Kerrie B Collins (KB)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

Kyung-Soon Lee (KS)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

Leonard A Daly (LA)

Centre for Proteome Research, Department of Biochemistry and Systems Biology, University of Liverpool, Liverpool L69 7ZB, UK.

Katherine A Forbush (KA)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

Ho-Tak Lau (HT)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

Martin Golkowski (M)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

G Stanley McKnight (GS)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

David T Breault (DT)

Division of Endocrinology, Boston Children's Hospital, Boston, MA 02115, USA.

Anne-Marie Lefrançois-Martinez (AM)

Génétique, Reproduction et Développement (GReD), CNRS, INSERM, Université Clermont Auvergne, 63001 Clermont-Ferrand, France.

Antoine Martinez (A)

Génétique, Reproduction et Développement (GReD), CNRS, INSERM, Université Clermont Auvergne, 63001 Clermont-Ferrand, France.

Claire E Eyers (CE)

Centre for Proteome Research, Department of Biochemistry and Systems Biology, University of Liverpool, Liverpool L69 7ZB, UK.

Geoffrey S Baird (GS)

Department of Laboratory Medicine and Pathology, University of Washington, Seattle, WA 98195, USA.

Shao-En Ong (SE)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

F Donelson Smith (FD)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA.

Patrick A Eyers (PA)

Department of Biochemistry & Systems Biology, University of Liverpool, Liverpool L69 7ZB, UK.

John D Scott (JD)

Department of Pharmacology, University of Washington, Seattle, WA 98195, USA. Electronic address: scottjdw@uw.edu.

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