Evolutionary rate covariation identifies SLC30A9 (ZnT9) as a mitochondrial zinc transporter.


Journal

The Biochemical journal
ISSN: 1470-8728
Titre abrégé: Biochem J
Pays: England
ID NLM: 2984726R

Informations de publication

Date de publication:
17 09 2021
Historique:
received: 12 05 2021
revised: 12 08 2021
accepted: 16 08 2021
pubmed: 17 8 2021
medline: 15 12 2021
entrez: 16 8 2021
Statut: ppublish

Résumé

Recent advances in genome sequencing have led to the identification of new ion and metabolite transporters, many of which have not been characterized. Due to the variety of subcellular localizations, cargo and transport mechanisms, such characterization is a daunting task, and predictive approaches focused on the functional context of transporters are very much needed. Here we present a case for identifying a transporter localization using evolutionary rate covariation (ERC), a computational approach based on pairwise correlations of amino acid sequence evolutionary rates across the mammalian phylogeny. As a case study, we find that poorly characterized transporter SLC30A9 (ZnT9) coevolves with several components of the mitochondrial oxidative phosphorylation chain, suggesting mitochondrial localization. We confirmed this computational finding experimentally using recombinant human SLC30A9. SLC30A9 loss caused zinc mishandling in the mitochondria, suggesting that under normal conditions it acts as a zinc exporter. We therefore propose that ERC can be used to predict the functional context of novel transporters and other poorly characterized proteins.

Identifiants

pubmed: 34397090
pii: 229560
doi: 10.1042/BCJ20210342
pmc: PMC10491466
mid: NIHMS1751066
doi:

Substances chimiques

Carrier Proteins 0
Cation Transport Proteins 0
Cell Cycle Proteins 0
Mitochondrial Proteins 0
SLC30A9 protein, human 0
Transcription Factors 0
zinc-binding protein 0
Zinc J41CSQ7QDS

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

3205-3220

Subventions

Organisme : NHGRI NIH HHS
ID : R01 HG009299
Pays : United States
Organisme : NINDS NIH HHS
ID : R21 NS111944
Pays : United States

Informations de copyright

© 2021 The Author(s). Published by Portland Press Limited on behalf of the Biochemical Society.

Références

Mol Cell Biochem. 2021 Feb;476(2):971-989
pubmed: 33225416
J Neurosci. 2011 Nov 9;31(45):16076-85
pubmed: 22072659
Nucleic Acids Res. 2019 Jul 2;47(W1):W256-W259
pubmed: 30931475
Bioinformatics. 2007 Jan 1;23(1):127-8
pubmed: 17050570
Neuroscience. 2021 Mar 1;457:235-258
pubmed: 33460731
Mol Med. 2007 Jul-Aug;13(7-8):380-7
pubmed: 17622314
Biochem J. 2009 Jul 29;422(1):43-52
pubmed: 19496757
Adv Exp Med Biol. 2020;1131:445-469
pubmed: 31646520
J Neuropathol Exp Neurol. 2019 Jul 1;78(7):655-664
pubmed: 31150090
Sci Rep. 2016 Jan 25;6:19692
pubmed: 26805723
BMC Biol. 2015 Oct 29;13:89
pubmed: 26515107
Proc Natl Acad Sci U S A. 2012 May 8;109(19):7202-7
pubmed: 22529353
Mol Neurobiol. 2021 Apr;58(4):1517-1534
pubmed: 33211252
Bioinformatics. 2015 Dec 1;31(23):3835-7
pubmed: 26243019
J Proteome Res. 2006 Jan;5(1):196-201
pubmed: 16396512
EMBO J. 1995 Feb 15;14(4):639-49
pubmed: 7882967
Biophys J. 2000 Jun;78(6):2798-813
pubmed: 10827963
Proc Natl Acad Sci U S A. 2019 Sep 24;116(39):19593-19599
pubmed: 31501324
J Neuropathol Exp Neurol. 2012 Mar;71(3):211-22
pubmed: 22318122
Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2317-22
pubmed: 11226237
PLoS Comput Biol. 2019 Mar 20;15(3):e1006882
pubmed: 30893306
Int J Mol Sci. 2017 Oct 19;18(10):
pubmed: 29048339
Nucleic Acids Res. 2021 Jan 8;49(D1):D1541-D1547
pubmed: 33174596
Rev Neurosci. 2020 Apr 28;31(3):233-243
pubmed: 31747384
Mol Biol Evol. 2019 May 1;36(5):1022-1036
pubmed: 30785203
Cell. 2000 Mar 3;100(5):551-60
pubmed: 10721992
Nucleic Acids Res. 2001 Jan 1;29(1):137-40
pubmed: 11125071
Brain. 2017 Apr 1;140(4):928-939
pubmed: 28334855
Cell. 2012 Oct 26;151(3):630-44
pubmed: 23101630
Nucleic Acids Res. 2003 Jul 1;31(13):3497-500
pubmed: 12824352
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
PLoS Genet. 2014 Jan;10(1):e1004108
pubmed: 24453993
Biochem J. 2015 Aug 15;470(1):65-76
pubmed: 26251447
J Neurochem. 2021 Mar;156(6):715-752
pubmed: 33616931
Elife. 2020 Dec 14;9:
pubmed: 33315011
Neuron. 2001 Jun;30(3):665-76
pubmed: 11430801
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Neurobiol Dis. 2014 Aug;68:137-44
pubmed: 24787898
J Physiol. 2007 Feb 1;578(Pt 3):633-40
pubmed: 17110406
Front Physiol. 2018 Sep 04;9:1243
pubmed: 30233414
PLoS Genet. 2015 Feb 13;11(2):e1004967
pubmed: 25679399
F1000Res. 2019 Oct 18;8:1774
pubmed: 31819800
Biomol Concepts. 2019 Mar 7;10(1):1-10
pubmed: 30888962
Front Pharmacol. 2017 Mar 23;8:151
pubmed: 28386229
Biochim Biophys Acta. 2006 Oct;1758(10):1696-701
pubmed: 16844077
FEBS J. 2022 Feb;289(3):614-633
pubmed: 33576127
J Biol Chem. 1997 Nov 14;272(46):28875-81
pubmed: 9360955
Neuroscientist. 2019 Apr;25(2):126-138
pubmed: 29742958
Exp Neurol. 2020 Mar;325:113161
pubmed: 31881218
J Exp Biol. 2006 Feb;209(Pt 4):577-89
pubmed: 16449553
Adv Nutr. 2013 Mar 01;4(2):176-90
pubmed: 23493534
Genome Res. 2002 Jun;12(6):996-1006
pubmed: 12045153
Glia. 2004 Nov 1;48(2):145-55
pubmed: 15378655
J Mammary Gland Biol Neoplasia. 2014 Mar;19(1):59-71
pubmed: 24338187
Nucleic Acids Res. 2016 Jan 4;44(D1):D1251-7
pubmed: 26450961
Nucleic Acids Res. 2019 Jul 2;47(W1):W636-W641
pubmed: 30976793
Physiol Rev. 2015 Jul;95(3):749-84
pubmed: 26084690
J Biol Chem. 2010 Jun 18;285(25):19450-9
pubmed: 20404342
Mol Cell. 2014 Mar 6;53(5):726-37
pubmed: 24560927
World J Surg Oncol. 2011 May 20;9:54
pubmed: 21599891
Genome Res. 2012 Apr;22(4):714-20
pubmed: 22287101
Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14934-9
pubmed: 8962159
PLoS Genet. 2019 Feb 14;15(2):e1007720
pubmed: 30763317
Nat Rev Mol Cell Biol. 2015 Jun;16(6):375-88
pubmed: 25991374
Hum Mol Genet. 2014 Jun 1;23(11):2802-15
pubmed: 24399444
EMBO Rep. 2018 Apr;19(4):
pubmed: 29507079
Front Mol Neurosci. 2020 Nov 26;13:600089
pubmed: 33324162
Bioinformatics. 2005 Sep 1;21(17):3482-9
pubmed: 15994190
Biochem J. 2013 Apr 15;451(2):155-63
pubmed: 23368743
J Biol Chem. 2009 Jun 26;284(26):17677-86
pubmed: 19366695
Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1716-21
pubmed: 9990090
Nature. 2020 Jul;583(7816):459-468
pubmed: 32353859
Biochim Biophys Acta Mol Cell Res. 2021 Jun;1868(7):119020
pubmed: 33798602
Int J Mol Sci. 2020 Jan 22;21(3):
pubmed: 31979155
Syst Biol. 2010 May;59(3):307-21
pubmed: 20525638
Sci Rep. 2015 Apr 30;5:9658
pubmed: 25927708
Eur J Biochem. 1996 Nov 1;241(3):779-86
pubmed: 8944766

Auteurs

Amanda Kowalczyk (A)

Joint Carnegie Mellon University-University of Pittsburgh PhD Program in Computational Biology, Pittsburgh, PA 15213, U.S.A.
Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA 15213, U.S.A.

Omotola Gbadamosi (O)

Department of Biological Science, University of Pittsburgh, Pittsburgh, PA 15260, U.S.A.

Kathryn Kolor (K)

Department of Biological Science, University of Pittsburgh, Pittsburgh, PA 15260, U.S.A.

Jahree Sosa (J)

Department of Biological Science, University of Pittsburgh, Pittsburgh, PA 15260, U.S.A.

Livia Andrzejczuk (L)

Department of Biological Science, University of Pittsburgh, Pittsburgh, PA 15260, U.S.A.

Gregory Gibson (G)

Center for Biologic Imaging, University of Pittsburgh, Pittsburgh, PA 15260, U.S.A.

Claudette St Croix (C)

Center for Biologic Imaging, University of Pittsburgh, Pittsburgh, PA 15260, U.S.A.

Maria Chikina (M)

Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA 15213, U.S.A.

Elias Aizenman (E)

Department of Neurobiology and Pittsburgh Institute for Neurodegenerative Diseases, University of Pittsburgh School of Medicine, Pittsburgh, PA 15260, U.S.A.

Nathan Clark (N)

Department of Human Genetics, University of Utah, Utah 84112, U.S.A.

Kirill Kiselyov (K)

Department of Biological Science, University of Pittsburgh, Pittsburgh, PA 15260, U.S.A.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing

[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

Classifications MeSH