Molecular basis of ClC-6 function and its impairment in human disease.


Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
13 10 2023
Historique:
medline: 1 11 2023
pubmed: 13 10 2023
entrez: 13 10 2023
Statut: ppublish

Résumé

ClC-6 is a late endosomal voltage-gated chloride-proton exchanger that is predominantly expressed in the nervous system. Mutated forms of ClC-6 are associated with severe neurological disease. However, the mechanistic role of ClC-6 in normal and pathological states remains largely unknown. Here, we present cryo-EM structures of ClC-6 that guided subsequent functional studies. Previously unrecognized ATP binding to cytosolic ClC-6 domains enhanced ion transport activity. Guided by a disease-causing mutation (p.Y553C), we identified an interaction network formed by Y553/F317/T520 as potential hotspot for disease-causing mutations. This was validated by the identification of a patient with a de novo pathogenic variant p.T520A. Extending these findings, we found contacts between intramembrane helices and connecting loops that modulate the voltage dependence of ClC-6 gating and constitute additional candidate regions for disease-associated gain-of-function mutations. Besides providing insights into the structure, function, and regulation of ClC-6, our work correctly predicts hotspots for

Identifiants

pubmed: 37831762
doi: 10.1126/sciadv.adg4479
pmc: PMC10575590
doi:

Substances chimiques

Chloride Channels 0
CLCN6 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

eadg4479

Références

EMBO J. 2009 Oct 21;28(20):3090-102
pubmed: 19745816
Mol Neurobiol. 2021 Jun;58(6):2990-2999
pubmed: 33590434
Am J Physiol Cell Physiol. 2008 Jan;294(1):C251-62
pubmed: 17977943
Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13362-6
pubmed: 8917596
Neuron. 2001 Jan;29(1):185-96
pubmed: 11182090
Cell. 2012 Oct 12;151(2):372-83
pubmed: 23063126
Cell. 2001 Jan 26;104(2):205-15
pubmed: 11207362
J Biol Chem. 2017 Nov 17;292(46):19055-19065
pubmed: 28972156
Elife. 2020 Apr 20;9:
pubmed: 32310757
EMBO Rep. 2020 Jun 4;21(6):e47872
pubmed: 32390228
J Biol Chem. 2013 Oct 4;288(40):28611-9
pubmed: 23983121
Pflugers Arch. 2013 Oct;465(10):1423-37
pubmed: 23632988
Biophys J. 2023 Mar 21;122(6):1068-1085
pubmed: 36698313
Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13854-9
pubmed: 16950870
J Cell Physiol. 2006 Mar;206(3):792-8
pubmed: 16222710
J Physiol. 2015 Sep 15;593(18):4091-109
pubmed: 25590607
Nature. 1995 Feb 9;373(6514):527-31
pubmed: 7845466
Nat Cell Biol. 2022 Jun;24(6):885-895
pubmed: 35590106
J Biol Chem. 2009 Sep 25;284(39):26526-32
pubmed: 19636075
Nat Nanotechnol. 2021 Jan;16(1):96-103
pubmed: 33139937
J Gen Physiol. 2021 Jan 4;153(1):
pubmed: 33211806
J Physiol. 2001 Aug 15;535(Pt 1):83-93
pubmed: 11507159
J Biol Chem. 2010 Jul 9;285(28):21689-97
pubmed: 20466723
Cell. 2013 Feb 14;152(4):778-790
pubmed: 23394946
Nat Struct Mol Biol. 2014 May;21(5):456-63
pubmed: 24747941
Proc Natl Acad Sci U S A. 1984 May;81(9):2772-5
pubmed: 6326143
Biochem J. 2011 Nov 1;439(3):349-74
pubmed: 21992097
J Physiol. 2004 Jun 1;557(Pt 2):363-78
pubmed: 14724190
J Biol Chem. 1999 Jan 8;274(2):896-902
pubmed: 9873029
J Gen Physiol. 1996 Oct;108(4):237-50
pubmed: 8894974
J Physiol. 2001 Feb 1;530(Pt 3):379-93
pubmed: 11158270
Sci Rep. 2017 Jan 11;7:40319
pubmed: 28074849
Trends Biochem Sci. 2019 Feb;44(2):110-124
pubmed: 30424907
EMBO J. 2020 May 4;39(9):e103358
pubmed: 32118314
Rev Physiol Biochem Pharmacol. 2007;158:23-76
pubmed: 17729441
Hum Mol Genet. 2001 Dec 1;10(25):2861-7
pubmed: 11741829
Am J Hum Genet. 2020 Dec 3;107(6):1062-1077
pubmed: 33217309
Pflugers Arch. 2017 Feb;469(2):183-193
pubmed: 27921211
J Physiol. 2002 Mar 1;539(Pt 2):373-83
pubmed: 11882671
Nature. 2002 Jan 17;415(6869):287-94
pubmed: 11796999
Physiol Rev. 2018 Jul 1;98(3):1493-1590
pubmed: 29845874
J Gen Physiol. 2010 Jun;135(6):653-9
pubmed: 20513761
Mol Psychiatry. 2023 Feb;28(2):668-697
pubmed: 36385166
Philos Trans R Soc Lond B Biol Sci. 2009 Jan 27;364(1514):175-80
pubmed: 18977737
Nature. 1996 Sep 26;383(6598):340-3
pubmed: 8848047
Genet Med. 2015 May;17(5):405-24
pubmed: 25741868
Philos Trans R Soc Lond B Biol Sci. 2009 Jan 27;364(1514):181-7
pubmed: 18957380
J Gen Physiol. 2005 Dec;126(6):563-70
pubmed: 16316975
J Biol Chem. 2005 Sep 16;280(37):32452-8
pubmed: 16027167
J Gen Physiol. 1997 Jan;109(1):105-16
pubmed: 8997669
Science. 2003 Apr 4;300(5616):108-12
pubmed: 12649487
Neuron. 1995 Dec;15(6):1455-63
pubmed: 8845168
J Neurosci Methods. 1994 Jan;51(1):107-16
pubmed: 8189746
J Gen Physiol. 2021 Apr 5;153(4):
pubmed: 33600550
Neuron. 2010 Sep 23;67(6):915-28
pubmed: 20869590
J Physiol. 2022 May;600(9):2147-2164
pubmed: 35262198
Proc Natl Acad Sci U S A. 2012 Jul 17;109(29):11699-704
pubmed: 22753511
J Biol Chem. 2008 Feb 15;283(7):4219-27
pubmed: 18063579
Am J Physiol. 1998 Apr;274(4):C966-73
pubmed: 9575793
J Gen Physiol. 1997 Aug;110(2):165-71
pubmed: 9236209
Science. 2010 Jun 11;328(5984):1401-3
pubmed: 20430974
Nat Struct Mol Biol. 2007 Jan;14(1):60-7
pubmed: 17195847
Nature. 2005 Jul 21;436(7049):420-3
pubmed: 16034421
J Gen Physiol. 2008 Feb;131(2):109-16
pubmed: 18227271
J Physiol. 2003 Dec 15;553(Pt 3):873-9
pubmed: 14617675
Elife. 2020 Aug 04;9:
pubmed: 32749217
Sci Adv. 2020 Aug 12;6(33):eabb4747
pubmed: 32851177
EMBO Rep. 2009 Oct;10(10):1111-6
pubmed: 19713962
EMBO Rep. 2014 Jul;15(7):784-91
pubmed: 24820037
J Gen Physiol. 2008 Oct;132(4):421-8
pubmed: 18824589
FEBS Lett. 1995 Dec 11;377(1):15-20
pubmed: 8543009
Am J Hum Genet. 2021 Aug 5;108(8):1450-1465
pubmed: 34186028
PLoS Biol. 2019 Apr 25;17(4):e3000218
pubmed: 31022181
J Biol Chem. 2023 Feb;299(2):102833
pubmed: 36581207
Biochem J. 1998 Mar 1;330 ( Pt 2):1015-21
pubmed: 9480924
Biophys J. 2011 Mar 2;100(5):1233-41
pubmed: 21354396
Nature. 2005 Jul 21;436(7049):424-7
pubmed: 16034422
Biochem J. 2011 Jun 1;436(2):415-28
pubmed: 21413926
Annu Rev Physiol. 2005;67:809-39
pubmed: 15709979
Elife. 2016 Jan 22;5:
pubmed: 26799336
PLoS One. 2007 May 30;2(5):e474
pubmed: 17534424
Nat Struct Mol Biol. 2006 Dec;13(12):1115-9
pubmed: 17115052
EMBO J. 2011 Jun 1;30(11):2140-52
pubmed: 21527911
Science. 2010 Oct 29;330(6004):635-41
pubmed: 20929736
Nature. 1990 Dec 6;348(6301):510-4
pubmed: 2174129

Auteurs

Bing Zhang (B)

Shanghai Key Laboratory of Maternal Fetal Medicine, Shanghai Institute of Maternal-Fetal Medicine and Gynecologic Oncology, Department of Anesthesiology, Clinical and Translational Research Center, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, 201204 Shanghai, China.

Sensen Zhang (S)

Ministry of Education Key Laboratory of Protein Science, Beijing Advanced Innovation Center for Structural Biology, Beijing Frontier Research Center for Biological Structure, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, 100084 Beijing, China.

Maya M Polovitskaya (MM)

Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP), 13125 Berlin, Germany.
Max-Delbrück-Centrum für Molekulare Medizin (MDC), 13125 Berlin, Germany.

Jingbo Yi (J)

Ministry of Education Key Laboratory of Protein Science, Beijing Advanced Innovation Center for Structural Biology, Beijing Frontier Research Center for Biological Structure, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, 100084 Beijing, China.

Binglu Ye (B)

Shanghai Key Laboratory of Maternal Fetal Medicine, Shanghai Institute of Maternal-Fetal Medicine and Gynecologic Oncology, Department of Anesthesiology, Clinical and Translational Research Center, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, 201204 Shanghai, China.

Ruochong Li (R)

Ministry of Education Key Laboratory of Protein Science, Beijing Advanced Innovation Center for Structural Biology, Beijing Frontier Research Center for Biological Structure, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, 100084 Beijing, China.

Xueying Huang (X)

Shanghai Key Laboratory of Maternal Fetal Medicine, Shanghai Institute of Maternal-Fetal Medicine and Gynecologic Oncology, Department of Anesthesiology, Clinical and Translational Research Center, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, 201204 Shanghai, China.

Jian Yin (J)

Ministry of Education Key Laboratory of Protein Science, Beijing Advanced Innovation Center for Structural Biology, Beijing Frontier Research Center for Biological Structure, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, 100084 Beijing, China.

Sebastian Neuens (S)

Department of Genetics, Hôpital Universitaire des Enfants Reine Fabiola, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Tom Balfroid (T)

Department of Pediatric Neurology, Hôpital Universitaire des Enfants Reine Fabiola, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Julie Soblet (J)

Department of Genetics, Hôpital Universitaire des Enfants Reine Fabiola, Université Libre de Bruxelles (ULB), Brussels, Belgium.
Department of Genetics, Hôpital Erasme, Université Libre de Bruxelles (ULB), Brussels, Belgium.
Interuniversity Institute of Bioinformatics in Brussels, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Daphné Vens (D)

Pediatric Intensive Care Unit, Hôpital Universitaire des Enfants Reine Fabiola, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Alec Aeby (A)

Department of Pediatric Neurology, Hôpital Universitaire des Enfants Reine Fabiola, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Xiaoling Li (X)

Wuya College of Innovation, Shenyang Pharmaceutical University, 110016 Shenyang, China.

Jinjin Cai (J)

Key Laboratory of Receptor Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, 201203 Shanghai, China.

Yingcai Song (Y)

Shanghai Key Laboratory of Maternal Fetal Medicine, Shanghai Institute of Maternal-Fetal Medicine and Gynecologic Oncology, Department of Anesthesiology, Clinical and Translational Research Center, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, 201204 Shanghai, China.

Yuanxi Li (Y)

Institute for Cognitive Neurodynamics, School of Mathematics, East China University of Science and Technology, 200237 Shanghai, China.

Marco Tartaglia (M)

Molecular Genetics and Functional Genomics, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Yang Li (Y)

Key Laboratory of Receptor Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, 201203 Shanghai, China.
National Clinical Research Center for Aging and Medicine, Huashan Hospital, Fudan University, Shanghai 200040, China.

Thomas J Jentsch (TJ)

Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP), 13125 Berlin, Germany.
Max-Delbrück-Centrum für Molekulare Medizin (MDC), 13125 Berlin, Germany.
NeuroCure Cluster of Excellence, Charité Universitätsmedizin Berlin, 10117 Berlin, Germany.

Maojun Yang (M)

Ministry of Education Key Laboratory of Protein Science, Beijing Advanced Innovation Center for Structural Biology, Beijing Frontier Research Center for Biological Structure, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, 100084 Beijing, China.
Cryo-EM Facility Center, Southern University of Science & Technology, 518055 Shenzhen, Guangdong, China.

Zhiqiang Liu (Z)

Shanghai Key Laboratory of Maternal Fetal Medicine, Shanghai Institute of Maternal-Fetal Medicine and Gynecologic Oncology, Department of Anesthesiology, Clinical and Translational Research Center, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, 201204 Shanghai, China.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH