Zinc transport via ZNT5-6 and ZNT7 is critical for cell surface glycosylphosphatidylinositol-anchored protein expression.

ER quality control ZNT cell surface early secretory pathway ectoenzyme glycosylphosphatidylinositol (GPI anchor) phosphatidylinositol glycan anchor biosynthesis (PIG) transporter zinc

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:
06 2022
Historique:
received: 14 01 2022
revised: 20 04 2022
accepted: 27 04 2022
pubmed: 8 5 2022
medline: 30 6 2022
entrez: 7 5 2022
Statut: ppublish

Résumé

Glycosylphosphatidylinositol (GPI)-anchored proteins play crucial roles in various enzyme activities, cell signaling and adhesion, and immune responses. While the molecular mechanism underlying GPI-anchored protein biosynthesis has been well studied, the role of zinc transport in this process has not yet been elucidated. Zn transporter (ZNT) proteins mobilize cytosolic zinc to the extracellular space and to intracellular compartments. Here, we report that the early secretory pathway ZNTs (ZNT5-ZNT6 heterodimers [ZNT5-6] and ZNT7-ZNT7 homodimers [ZNT7]), which supply zinc to the lumen of the early secretory pathway compartments are essential for GPI-anchored protein expression on the cell surface. We show, using overexpression and gene disruption/re-expression strategies in cultured human cells, that loss of ZNT5-6 and ZNT7 zinc transport functions results in significant reduction in GPI-anchored protein levels similar to that in mutant cells lacking phosphatidylinositol glycan anchor biosynthesis (PIG) genes. Furthermore, medaka fish with disrupted Znt5 and Znt7 genes show touch-insensitive phenotypes similar to zebrafish Pig mutants. These findings provide a previously unappreciated insight into the regulation of GPI-anchored protein expression and protein quality control in the early secretory pathway.

Identifiants

pubmed: 35525268
pii: S0021-9258(22)00451-3
doi: 10.1016/j.jbc.2022.102011
pmc: PMC9168625
pii:
doi:

Substances chimiques

Cation Transport Proteins 0
GPI-Linked Proteins 0
Glycosylphosphatidylinositols 0
Membrane Proteins 0
Zinc J41CSQ7QDS

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

102011

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest The authors declare that they have no conflicts of interest with the contents of this article.

Références

PLoS Genet. 2014 Sep 18;10(9):e1004641
pubmed: 25233454
Arch Biochem Biophys. 2016 Dec 1;611:37-42
pubmed: 27046342
Dev Growth Differ. 2020 Dec;62(9):554-567
pubmed: 33155277
Development. 2010 May;137(10):1689-98
pubmed: 20392743
Cell. 1993 May 21;73(4):703-11
pubmed: 8500164
Metallomics. 2018 Dec 12;10(12):1755-1776
pubmed: 30358795
Open Biol. 2020 Mar;10(3):190290
pubmed: 32156170
Trends Pharmacol Sci. 2002 Apr;23(4):177-83
pubmed: 11931993
Nucleic Acids Res. 2015 Jan;43(Database issue):D204-12
pubmed: 25348405
Am J Physiol Cell Physiol. 2022 May 1;322(5):C948-C959
pubmed: 35294847
J Biol Chem. 2002 Jan 11;277(2):1375-80
pubmed: 11689569
J Biol Chem. 1991 May 15;266(14):9002-8
pubmed: 1851160
J Virol. 2007 Oct;81(19):10831-4
pubmed: 17652383
Biomed Res. 2011 Dec;32(6):407-11
pubmed: 22199132
Clin Genet. 2019 Jan;95(1):112-121
pubmed: 30054924
Biochem Soc Trans. 2020 Jun 30;48(3):1129-1138
pubmed: 32573677
Biol Pharm Bull. 2021;44(6):804-815
pubmed: 34078812
Eur J Hum Genet. 2021 May;29(5):808-815
pubmed: 33547425
Biochemistry. 2001 Feb 6;40(5):1205-13
pubmed: 11170445
J Biol Chem. 2012 Feb 24;287(9):6318-25
pubmed: 22228761
J Biol Chem. 1995 Oct 6;270(40):23641-7
pubmed: 7559531
PLoS One. 2015 Sep 18;10(9):e0138553
pubmed: 26383639
Proteins. 2001 Dec 1;45(4):318-24
pubmed: 11746679
J Lipid Res. 2016 Jan;57(1):6-24
pubmed: 26563290
Cell. 2014 Jul 31;158(3):522-33
pubmed: 25083867
Nat Protoc. 2009;4(11):1582-90
pubmed: 19816421
J Biol Chem. 2017 Feb 10;292(6):2159-2173
pubmed: 28028180
J Biol Chem. 2021 Jan-Jun;296:100320
pubmed: 33485965
Commun Biol. 2018 Aug 22;1:113
pubmed: 30271993
Biochem J. 2016 Sep 1;473(17):2611-21
pubmed: 27303047
Mol Cell Proteomics. 2012 Jun;11(6):O111.016717
pubmed: 22261725
J Biol Chem. 2011 May 6;286(18):16363-73
pubmed: 21402707
J Biol Chem. 2020 Apr 24;295(17):5669-5684
pubmed: 32179649
Nat Rev Mol Cell Biol. 2008 Dec;9(12):944-57
pubmed: 19002207
Blood. 1998 Feb 15;91(4):1185-95
pubmed: 9454748
EMBO J. 2001 Aug 1;20(15):4088-98
pubmed: 11483512
J Cell Biol. 2004 Aug 2;166(3):325-35
pubmed: 15277543
Dev Growth Differ. 2000 Oct;42(5):469-78
pubmed: 11041488
Nat Commun. 2019 Feb 5;10(1):603
pubmed: 30723194
EMBO J. 2001 Oct 1;20(19):5383-91
pubmed: 11574470
Genome Biol. 2003;4(8):225
pubmed: 12914653
Biochemistry. 2020 Jan 14;59(1):74-79
pubmed: 31718170
Am J Hum Genet. 2012 Jul 13;91(1):146-51
pubmed: 22683086
Sci Rep. 2020 Jul 9;10(1):11271
pubmed: 32647189
J Biol Chem. 2005 Sep 2;280(35):30956-62
pubmed: 15994300
Mol Biol Cell. 2008 Aug;19(8):3463-76
pubmed: 18508914
J Neurophysiol. 2015 Aug;114(2):1146-57
pubmed: 26133798
J Neurochem. 2022 Mar;160(6):662-674
pubmed: 35064931
Commun Biol. 2021 Jun 23;4(1):777
pubmed: 34162996
Biol Chem. 2015 Jun;396(6-7):707-36
pubmed: 25803076
Nat Commun. 2020 Feb 26;11(1):1058
pubmed: 32103002
Curr Opin Chem Biol. 2020 Apr;55:145-150
pubmed: 32114317
Nucleic Acids Res. 2022 Jan 7;50(D1):D543-D552
pubmed: 34723319
EMBO J. 2014 Nov 3;33(21):2444-6
pubmed: 25190517
FEBS Lett. 2010 May 3;584(9):1895-900
pubmed: 19944693
J Biol Chem. 2006 Jun 30;281(26):17743-50
pubmed: 16636052

Auteurs

Takumi Wagatsuma (T)

Division of Integrated Life Science, Graduate School of Biostudies, Kyoto University, Kyoto, Japan.

Keiko Shimotsuma (K)

Division of Integrated Life Science, Graduate School of Biostudies, Kyoto University, Kyoto, Japan.

Akiko Sogo (A)

Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.

Risa Sato (R)

Division of Membrane Transport and Drug Targeting, Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai, Japan.

Naoya Kubo (N)

Division of Integrated Life Science, Graduate School of Biostudies, Kyoto University, Kyoto, Japan.

Sachiko Ueda (S)

Division of Integrated Life Science, Graduate School of Biostudies, Kyoto University, Kyoto, Japan.

Yasuo Uchida (Y)

Division of Membrane Transport and Drug Targeting, Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai, Japan.

Masato Kinoshita (M)

Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.

Taiho Kambe (T)

Division of Integrated Life Science, Graduate School of Biostudies, Kyoto University, Kyoto, Japan. Electronic address: kambe.taiho.7z@kyoto-u.ac.jp.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH