Phospho-regulation, nucleotide binding and ion access control in potassium-chloride cotransporters.


Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
15 07 2021
Historique:
revised: 29 03 2021
received: 12 11 2020
accepted: 11 04 2021
pubmed: 26 5 2021
medline: 18 11 2021
entrez: 25 5 2021
Statut: ppublish

Résumé

Potassium-coupled chloride transporters (KCCs) play crucial roles in regulating cell volume and intracellular chloride concentration. They are characteristically inhibited under isotonic conditions via phospho-regulatory sites located within the cytoplasmic termini. Decreased inhibitory phosphorylation in response to hypotonic cell swelling stimulates transport activity, and dysfunction of this regulatory process has been associated with various human diseases. Here, we present cryo-EM structures of human KCC3b and KCC1, revealing structural determinants for phospho-regulation in both N- and C-termini. We show that phospho-mimetic KCC3b is arrested in an inward-facing state in which intracellular ion access is blocked by extensive contacts with the N-terminus. In another mutant with increased isotonic transport activity, KCC1Δ19, this interdomain interaction is absent, likely due to a unique phospho-regulatory site in the KCC1 N-terminus. Furthermore, we map additional phosphorylation sites as well as a previously unknown ATP/ADP-binding pocket in the large C-terminal domain and show enhanced thermal stabilization of other CCCs by adenine nucleotides. These findings provide fundamentally new insights into the complex regulation of KCCs and may unlock innovative strategies for drug development.

Identifiants

pubmed: 34031912
doi: 10.15252/embj.2020107294
pmc: PMC8280820
doi:

Substances chimiques

Chlorides 0
Nucleotides 0
Symporters 0
Potassium RWP5GA015D

Banques de données

PDB
['6Y5V', '7AIN', '7AIO', '7AIP', '7AIQ', '7AIR', '7NGB']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e107294

Subventions

Organisme : Medical Research Council
ID : MC_PC_17137
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 060208/Z/00/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_17136
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 093305/Z/10/Z
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2021 The Authors. Published under the terms of the CC BY 4.0 license.

Références

Cold Spring Harb Mol Case Stud. 2016 Nov;2(6):a001289
pubmed: 27900370
Blood. 2015 Dec 24;126(26):2863-70
pubmed: 26450986
Nat Rev Neurosci. 2014 Oct;15(10):637-54
pubmed: 25234263
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Cell Chem Biol. 2020 Aug 20;27(8):1073-1083.e12
pubmed: 32521230
EMBO Rep. 2014 Jul;15(7):766-74
pubmed: 24928908
J Biol Chem. 2010 May 7;285(19):14115-21
pubmed: 20223824
J Physiol. 2019 Aug;597(16):4263-4276
pubmed: 31216057
Cell. 2017 Mar 23;169(1):85-95.e8
pubmed: 28340353
Science. 2019 Oct 25;366(6464):505-508
pubmed: 31649201
J Neurosci. 2007 Jun 20;27(25):6751-9
pubmed: 17581962
Nucleic Acids Res. 2010 Jul;38(Web Server issue):W545-9
pubmed: 20457744
Nature. 2019 Aug;572(7770):488-492
pubmed: 31367042
Am J Physiol. 1988 Apr;254(4 Pt 1):C582-6
pubmed: 3354657
Sci Signal. 2019 Oct 15;12(603):
pubmed: 31615901
J Chem Phys. 2005 Sep 8;123(10):104501
pubmed: 16178604
J Biol Chem. 2013 Nov 1;288(44):31468-76
pubmed: 24043619
J Neurol Neurosurg Psychiatry. 2018 Oct;89(10):1123-1125
pubmed: 29269506
Proc Natl Acad Sci U S A. 2005 Nov 15;102(46):16777-82
pubmed: 16275913
J Biol Chem. 2012 Jan 13;287(3):2210-20
pubmed: 22121194
Physiol Rev. 2005 Apr;85(2):423-93
pubmed: 15788703
Nat Genet. 2002 Nov;32(3):384-92
pubmed: 12368912
Am J Physiol. 1996 Feb;270(2 Pt 1):C437-48
pubmed: 8779905
Neurology. 2007 Sep 25;69(13):1350-5
pubmed: 17893295
Mol Genet Genomic Med. 2019 Sep;7(9):e892
pubmed: 31393094
Spine J. 2014 May 1;14(5):777-81
pubmed: 24239489
Acta Crystallogr D Struct Biol. 2018 Jun 1;74(Pt 6):531-544
pubmed: 29872004
Biochemistry. 2010 Mar 16;49(10):2194-204
pubmed: 20113006
Neurology. 2006 Apr 11;66(7):1044-8
pubmed: 16606917
Nat Genet. 1996 Jun;13(2):183-8
pubmed: 8640224
Acta Crystallogr D Struct Biol. 2019 Oct 1;75(Pt 10):878-881
pubmed: 31588919
Trends Mol Med. 2015 Aug;21(8):513-23
pubmed: 26142773
Mol Aspects Med. 2013 Apr-Jun;34(2-3):288-98
pubmed: 23506871
Cell. 2009 Aug 7;138(3):525-36
pubmed: 19665974
ACS Cent Sci. 2018 Oct 24;4(10):1334-1343
pubmed: 30410971
Sci Signal. 2016 Aug 02;9(439):ra77
pubmed: 27485015
Cell Res. 2021 Apr;31(4):482-484
pubmed: 33199848
Neurochem Int. 2019 Feb;123:114-124
pubmed: 29366908
J Gen Physiol. 2014 Apr;143(4):419-35
pubmed: 24638992
Sci Adv. 2020 Dec 11;6(50):
pubmed: 33310850
J Struct Biol. 2014 Jul;187(1):58-65
pubmed: 24821279
Trends Neurosci. 2013 Dec;36(12):726-737
pubmed: 24139641
Biochem J. 2014 Mar 15;458(3):559-73
pubmed: 24393035
Bioinformatics. 2003 Jul 1;19(10):1290-1
pubmed: 12835274
News Physiol Sci. 1998 Aug;13:177-182
pubmed: 11390785
Sci Signal. 2019 Oct 15;12(603):
pubmed: 31615899
Physiol Rev. 2000 Jan;80(1):211-76
pubmed: 10617769
Front Cell Neurosci. 2015 Jul 09;9:255
pubmed: 26217182
J Biol Chem. 2007 Oct 12;282(41):29777-84
pubmed: 17693402
J Biol Chem. 1995 Dec 1;270(48):28955-61
pubmed: 7499426
Structure. 2009 Apr 15;17(4):538-46
pubmed: 19368887
Am J Physiol. 1990 May;258(5 Pt 1):C933-43
pubmed: 2333985
Nat Commun. 2020 Feb 21;11(1):1016
pubmed: 32081947
Elife. 2020 Apr 14;9:
pubmed: 32286222
Protein Sci. 2014 Jan;23(1):47-55
pubmed: 24265211
EMBO J. 2021 Jul 15;40(14):e107294
pubmed: 34031912
Annu Rev Physiol. 2000;62:515-34
pubmed: 10845101
Am J Physiol Cell Physiol. 2013 Apr 15;304(8):C693-714
pubmed: 23325410
Brain Res Mol Brain Res. 2002 Jun 30;103(1-2):91-105
pubmed: 12106695
Structure. 2020 Sep 1;28(9):1051-1060.e4
pubmed: 32679039

Auteurs

Gamma Chi (G)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Rebecca Ebenhoch (R)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Henry Man (H)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Haiping Tang (H)

Physical and Theoretical Chemistry Laboratory, University of Oxford, Oxford, UK.

Laurence E Tremblay (LE)

Department of Medicine, Nephrology Research Group, Faculty of Medicine, Laval University, Quebec City, QC, Canada.

Gabriella Reggiano (G)

Department of Biochemistry, University of Washington, Seattle, WA, USA.

Xingyu Qiu (X)

Physical and Theoretical Chemistry Laboratory, University of Oxford, Oxford, UK.

Tina Bohstedt (T)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Idlir Liko (I)

OMass Therapeutics, Ltd., Oxford, UK.

Fernando G Almeida (FG)

OMass Therapeutics, Ltd., Oxford, UK.

Alexandre P Garneau (AP)

Department of Medicine, Nephrology Research Group, Faculty of Medicine, Laval University, Quebec City, QC, Canada.
Cardiometabolic Axis, School of Kinesiology and Physical Activity Sciences, University of Montréal, Montréal, QC, Canada.

Dong Wang (D)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Gavin McKinley (G)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Christophe P Moreau (CP)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.

Kiran D Bountra (KD)

OMass Therapeutics, Ltd., Oxford, UK.

Patrizia Abrusci (P)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Shubhashish M M Mukhopadhyay (SMM)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Alejandra Fernandez-Cid (A)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Samira Slimani (S)

Department of Medicine, Nephrology Research Group, Faculty of Medicine, Laval University, Quebec City, QC, Canada.

Julie L Lavoie (JL)

Cardiometabolic Axis, School of Kinesiology and Physical Activity Sciences, University of Montréal, Montréal, QC, Canada.

Nicola A Burgess-Brown (NA)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Ben Tehan (B)

OMass Therapeutics, Ltd., Oxford, UK.

Frank DiMaio (F)

Department of Biochemistry, University of Washington, Seattle, WA, USA.

Ali Jazayeri (A)

OMass Therapeutics, Ltd., Oxford, UK.

Paul Isenring (P)

Department of Medicine, Nephrology Research Group, Faculty of Medicine, Laval University, Quebec City, QC, Canada.

Carol V Robinson (CV)

Physical and Theoretical Chemistry Laboratory, University of Oxford, Oxford, UK.

Katharina L Dürr (KL)

Nuffield Department of Medicine, Centre of Medicines Discovery, University of Oxford, Oxford, UK.
Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Oxford, UK.
OMass Therapeutics, Ltd., Oxford, UK.

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