Cardiac myosin-binding protein C interaction with actin is inhibited by compounds identified in a high-throughput fluorescence lifetime screen.

actin cardiac muscle cardiac myosin-binding protein C (cMyBP-C) contractile proteins fluorescence lifetime high-throughput screening (HTS) library of pharmacologically active compounds (LOPAC) phosphorylation protein kinase A (PKA) site-directed spectroscopy

Journal

The Journal of biological chemistry
ISSN: 1083-351X
Titre abrégé: J Biol Chem
Pays: United States
ID NLM: 2985121R

Informations de publication

Date de publication:
07 2021
Historique:
received: 04 03 2021
revised: 19 05 2021
accepted: 26 05 2021
pubmed: 31 5 2021
medline: 26 8 2021
entrez: 30 5 2021
Statut: ppublish

Résumé

Cardiac myosin-binding protein C (cMyBP-C) interacts with actin and myosin to modulate cardiac muscle contractility. These interactions are disfavored by cMyBP-C phosphorylation. Heart failure patients often display decreased cMyBP-C phosphorylation, and phosphorylation in model systems has been shown to be cardioprotective against heart failure. Therefore, cMyBP-C is a potential target for heart failure drugs that mimic phosphorylation or perturb its interactions with actin/myosin. Here we have used a novel fluorescence lifetime-based assay to identify small-molecule inhibitors of actin-cMyBP-C binding. Actin was labeled with a fluorescent dye (Alexa Fluor 568, AF568) near its cMyBP-C binding sites; when combined with the cMyBP-C N-terminal fragment, C0-C2, the fluorescence lifetime of AF568-actin decreases. Using this reduction in lifetime as a readout of actin binding, a high-throughput screen of a 1280-compound library identified three reproducible hit compounds (suramin, NF023, and aurintricarboxylic acid) that reduced C0-C2 binding to actin in the micromolar range. Binding of phosphorylated C0-C2 was also blocked by these compounds. That they specifically block binding was confirmed by an actin-C0-C2 time-resolved FRET (TR-FRET) binding assay. Isothermal titration calorimetry (ITC) and transient phosphorescence anisotropy (TPA) confirmed that these compounds bind to cMyBP-C, but not to actin. TPA results were also consistent with these compounds inhibiting C0-C2 binding to actin. We conclude that the actin-cMyBP-C fluorescence lifetime assay permits detection of pharmacologically active compounds that affect cMyBP-C-actin binding. We now have, for the first time, a validated high-throughput screen focused on cMyBP-C, a regulator of cardiac muscle contractility and known key factor in heart failure.

Identifiants

pubmed: 34052227
pii: S0021-9258(21)00638-4
doi: 10.1016/j.jbc.2021.100840
pmc: PMC8233204
pii:
doi:

Substances chimiques

Actins 0
Carrier Proteins 0
myosin-binding protein C 0

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

100840

Subventions

Organisme : NIA NIH HHS
ID : R01 AG026160
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR032961
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL141564
Pays : United States
Organisme : NIA NIH HHS
ID : R37 AG026160
Pays : United States

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest D. D. T. holds equity in and serves as President of Photonic Pharma LLC. This relationship has been reviewed and managed by the University of Minnesota. Photonic Pharma had no role in this study, except to provide some instrumentation, as stated in Experimental procedures. B. A. C. filed a PCT patent application based on this work (patent pending, serial no. PCT/US21/14142). The other authors declare no competing financial interests.

Auteurs

Thomas A Bunch (TA)

Department of Cellular & Molecular Medicine, University of Arizona, Tucson Arizona, USA.

Piyali Guhathakurta (P)

Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, Minnesota, USA.

Victoria C Lepak (VC)

Department of Cellular & Molecular Medicine, University of Arizona, Tucson Arizona, USA.

Andrew R Thompson (AR)

Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, Minnesota, USA.

Rhye-Samuel Kanassatega (RS)

Department of Cellular & Molecular Medicine, University of Arizona, Tucson Arizona, USA.

Anna Wilson (A)

Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, Minnesota, USA.

David D Thomas (DD)

Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, Minnesota, USA.

Brett A Colson (BA)

Department of Cellular & Molecular Medicine, University of Arizona, Tucson Arizona, USA. Electronic address: bcolson@arizona.edu.

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Classifications MeSH