Literature DB >> 29903914

Ligand binding to a remote site thermodynamically corrects the F508del mutation in the human cystic fibrosis transmembrane conductance regulator.

Chi Wang1, Andrei A Aleksandrov2, Zhengrong Yang3, Farhad Forouhar1, Elizabeth A Proctor2, Pradeep Kota2, Jianli An3, Anna Kaplan1, Netaly Khazanov4, Grégory Boël1, Brent R Stockwell5, Hanoch Senderowitz4, Nikolay V Dokholyan2, John R Riordan2, Christie G Brouillette3, John F Hunt6.   

Abstract

Many disease-causing mutations impair protein stability. Here, we explore a thermodynamic strategy to correct the disease-causing F508del mutation in the human cystic fibrosis transmembrane conductance regulator (hCFTR). F508del destabilizes nucleotide-binding domain 1 (hNBD1) in hCFTR relative to an aggregation-prone intermediate. We developed a fluorescence self-quenching assay for compounds that prevent aggregation of hNBD1 by stabilizing its native conformation. Unexpectedly, we found that dTTP and nucleotide analogs with exocyclic methyl groups bind to hNBD1 more strongly than ATP and preserve electrophysiological function of full-length F508del-hCFTR channels at temperatures up to 37 °C. Furthermore, nucleotides that increase open-channel probability, which reflects stabilization of an interdomain interface to hNBD1, thermally protect full-length F508del-hCFTR even when they do not stabilize isolated hNBD1. Therefore, stabilization of hNBD1 itself or of one of its interdomain interfaces by a small molecule indirectly offsets the destabilizing effect of the F508del mutation on full-length hCFTR. These results indicate that high-affinity binding of a small molecule to a remote site can correct a disease-causing mutation. We propose that the strategies described here should be applicable to identifying small molecules to help manage other human diseases caused by mutations that destabilize native protein conformation.
© 2018 by The American Society for Biochemistry and Molecular Biology, Inc.

Entities:  

Keywords:  F508del mutation; calorimetry; cystic fibrosis; cystic fibrosis transmembrane conductance regulator (CFTR); deoxythymidine; electrophysiology; fluorescence resonance energy transfer (FRET); high-throughput screening (HTS); isothermal titration calorimetry (ITC); protein aggregation; thermodynamics

Mesh:

Substances:

Year:  2018        PMID: 29903914      PMCID: PMC6240863          DOI: 10.1074/jbc.RA117.000819

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  101 in total

1.  The First Nucleotide Binding Domain of Cystic Fibrosis Transmembrane Conductance Regulator Is a Site of Stable Nucleotide Interaction, whereas the Second Is a Site of Rapid Turnover.

Authors:  Luba Aleksandrov; Andrei A Aleksandrov; Xiu-Bao Chang; John R Riordan
Journal:  J Biol Chem       Date:  2002-02-22       Impact factor: 5.157

2.  Structures of a minimal human CFTR first nucleotide-binding domain as a monomer, head-to-tail homodimer, and pathogenic mutant.

Authors:  Shane Atwell; Christie G Brouillette; Kris Conners; Spencer Emtage; Tarun Gheyi; William B Guggino; Jorg Hendle; John F Hunt; Hal A Lewis; Frances Lu; Irina I Protasevich; Logan A Rodgers; Rich Romero; Stephen R Wasserman; Patricia C Weber; Diana Wetmore; Feiyu F Zhang; Xun Zhao
Journal:  Protein Eng Des Sel       Date:  2010-02-11       Impact factor: 1.650

3.  High affinity ATP/ADP analogues as new tools for studying CFTR gating.

Authors:  Zhen Zhou; Xiaohui Wang; Min Li; Yoshiro Sohma; Xiaoqin Zou; Tzyh-Chang Hwang
Journal:  J Physiol       Date:  2005-10-13       Impact factor: 5.182

4.  Ab initio folding of proteins with all-atom discrete molecular dynamics.

Authors:  Feng Ding; Douglas Tsao; Huifen Nie; Nikolay V Dokholyan
Journal:  Structure       Date:  2008-07       Impact factor: 5.006

5.  Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the CFTR 3D structure crucial to assembly and channel function.

Authors:  Adrian W R Serohijos; Tamás Hegedus; Andrei A Aleksandrov; Lihua He; Liying Cui; Nikolay V Dokholyan; John R Riordan
Journal:  Proc Natl Acad Sci U S A       Date:  2008-02-27       Impact factor: 11.205

6.  Mechanism-based corrector combination restores ΔF508-CFTR folding and function.

Authors:  Tsukasa Okiyoneda; Guido Veit; Johanna F Dekkers; Miklos Bagdany; Naoto Soya; Haijin Xu; Ariel Roldan; Alan S Verkman; Mark Kurth; Agnes Simon; Tamas Hegedus; Jeffrey M Beekman; Gergely L Lukacs
Journal:  Nat Chem Biol       Date:  2013-05-12       Impact factor: 15.040

7.  ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer.

Authors:  Paul C Smith; Nathan Karpowich; Linda Millen; Jonathan E Moody; Jane Rosen; Philip J Thomas; John F Hunt
Journal:  Mol Cell       Date:  2002-07       Impact factor: 17.970

8.  CFTR gating I: Characterization of the ATP-dependent gating of a phosphorylation-independent CFTR channel (DeltaR-CFTR).

Authors:  Silvia G Bompadre; Tomohiko Ai; Jeong Han Cho; Xiaohui Wang; Yoshiro Sohma; Min Li; Tzyh-Chang Hwang
Journal:  J Gen Physiol       Date:  2005-03-14       Impact factor: 4.086

9.  Emergence of protein fold families through rational design.

Authors:  Feng Ding; Nikolay V Dokholyan
Journal:  PLoS Comput Biol       Date:  2006-05-26       Impact factor: 4.475

10.  CFTR gating II: Effects of nucleotide binding on the stability of open states.

Authors:  Silvia G Bompadre; Jeong Han Cho; Xiaohui Wang; Xiaoqin Zou; Yoshiro Sohma; Min Li; Tzyh-Chang Hwang
Journal:  J Gen Physiol       Date:  2005-03-14       Impact factor: 4.086

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  3 in total

1.  Triangulating variation in the population to define mechanisms for precision management of genetic disease.

Authors:  Chao Wang; Frédéric Anglès; William E Balch
Journal:  Structure       Date:  2022-06-16       Impact factor: 5.871

2.  Short-term consequences of F508del-CFTR thermal instability on CFTR-dependent transepithelial currents in human airway epithelial cells.

Authors:  Lionel Froux; Christelle Coraux; Edouard Sage; Frédéric Becq
Journal:  Sci Rep       Date:  2019-09-24       Impact factor: 4.379

Review 3.  Recent Strategic Advances in CFTR Drug Discovery: An Overview.

Authors:  Marco Rusnati; Pasqualina D'Ursi; Nicoletta Pedemonte; Chiara Urbinati; Robert C Ford; Elena Cichero; Matteo Uggeri; Alessandro Orro; Paola Fossa
Journal:  Int J Mol Sci       Date:  2020-03-31       Impact factor: 5.923

  3 in total

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