TorsinA folding and N-linked glycosylation are sensitive to redox homeostasis.
Dystonia
N-linked glycosylation
Post-translational modifications
Protein disulfide isomerase
Protein folding
torsinA
Journal
Biochimica et biophysica acta. Molecular cell research
ISSN: 1879-2596
Titre abrégé: Biochim Biophys Acta Mol Cell Res
Pays: Netherlands
ID NLM: 101731731
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
17
06
2020
revised:
18
05
2021
accepted:
26
05
2021
pubmed:
2
6
2021
medline:
30
11
2021
entrez:
1
6
2021
Statut:
ppublish
Résumé
The Endoplasmic Reticulum (ER) is responsible for the folding and post-translational modification of secretory proteins, as well as for triaging misfolded proteins. During folding, there is a complex yet only partially understood interplay between disulfide bond formation, which is an enzyme catalyzed event in the oxidizing environment of the ER, along with other post-translational modifications (PTMs) and chaperone-supported protein folding. Here, we used the glycoprotein torsinA as a model substrate to explore the impact of ER redox homeostasis on PTMs and protein biogenesis. TorsinA is a AAA+ ATPase with unusual oligomeric properties and controversial functions. The deletion of a C-terminal glutamic acid residue (∆E) is associated with the development of Early-Onset Torsion Dystonia, a severe movement disorder. TorsinA differs from other AAA+ ATPases since it is an ER resident, and as a result of its entry into the ER torsinA contains two N-linked glycans and at least one disulfide bond. The role of these PTMs on torsinA biogenesis and function and the identity of the enzymes that catalyze them are poorly defined. Using a yeast torsinA expression system, we demonstrate that a specific protein disulfide isomerase, Pdi1, affects the folding and N-linked glycosylation of torsinA and torsinA∆E in a redox-dependent manner, suggesting that the acquisition of early torsinA folding intermediates is sensitive to perturbed interactions between Cys residues and the quality control machinery. We also highlight the role of specific Cys residues during torsinA biogenesis and demonstrate that torsinA∆E is more sensitive than torsinA when these Cys residues are mutated.
Identifiants
pubmed: 34062155
pii: S0167-4889(21)00127-0
doi: 10.1016/j.bbamcr.2021.119073
pmc: PMC8889903
mid: NIHMS1778999
pii:
doi:
Substances chimiques
Saccharomyces cerevisiae Proteins
0
Adenosine Triphosphatases
EC 3.6.1.-
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
119073Subventions
Organisme : NIDDK NIH HHS
ID : P30 DK079307
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM131732
Pays : United States
Informations de copyright
Copyright © 2021 The Authors. Published by Elsevier B.V. All rights reserved.
Références
Front Cell Dev Biol. 2015 May 21;3:30
pubmed: 26052512
Neurobiol Dis. 2019 Jul;127:233-241
pubmed: 30877032
Antioxid Redox Signal. 2010 Dec 15;13(12):1955-89
pubmed: 20560784
J Cell Biol. 1999 Dec 27;147(7):1443-56
pubmed: 10613903
Proc Natl Acad Sci U S A. 2013 Apr 23;110(17):E1545-54
pubmed: 23569223
Biochim Biophys Acta. 2013 Nov;1833(11):2430-7
pubmed: 23583305
J Biol Chem. 1996 Oct 11;271(41):25590-7
pubmed: 8810333
Proc Natl Acad Sci U S A. 2004 Jan 20;101(3):847-52
pubmed: 14711988
J Neurochem. 2007 Aug;102(3):783-8
pubmed: 17550429
Neurobiol Dis. 2011 May;42(2):136-47
pubmed: 21134457
Mol Cell Proteomics. 2016 Jul;15(7):2435-47
pubmed: 27094473
Biochem Biophys Res Commun. 2004 Jul 23;320(2):359-65
pubmed: 15219835
Cell. 1993 Jun 18;73(6):1197-206
pubmed: 8513503
EMBO J. 1999 Nov 1;18(21):5972-82
pubmed: 10545109
Mol Biol Cell. 2010 Mar 15;21(6):1047-58
pubmed: 20110346
Traffic. 2016 Apr;17(4):308-26
pubmed: 26676362
Nat Rev Mol Cell Biol. 2005 Jul;6(7):519-29
pubmed: 16072036
Biochem J. 2007 Jun 15;404(3):353-63
pubmed: 17521290
Genome Res. 1999 Jan;9(1):27-43
pubmed: 9927482
Mol Gen Genet. 1982;186(2):253-8
pubmed: 7050632
Curr Opin Cell Biol. 2020 Apr;63:125-134
pubmed: 32088611
J Cell Biol. 1993 Dec;123(6 Pt 1):1355-63
pubmed: 8253836
Elife. 2016 Aug 04;5:
pubmed: 27490483
J Neurosci Res. 2003 Apr 15;72(2):158-68
pubmed: 12671990
Annu Rev Biochem. 2011;80:71-99
pubmed: 21495850
Exp Mol Med. 2020 Mar;52(3):390-399
pubmed: 32203104
Am J Hum Genet. 1992 Mar;50(3):619-28
pubmed: 1347197
J Proteome Res. 2012 Nov 2;11(11):5376-83
pubmed: 23038983
Mol Biol Cell. 2012 Feb;23(4):520-32
pubmed: 22190736
J Biol Chem. 2000 Sep 8;275(36):27933-9
pubmed: 10871631
J Cell Biol. 1982 Apr;93(1):97-102
pubmed: 7068762
Sci Rep. 2016 Feb 11;6:20946
pubmed: 26864433
Semin Cell Dev Biol. 2015 May;41:71-8
pubmed: 25460543
J Biol Chem. 2015 Sep 25;290(39):23631-45
pubmed: 26170458
EMBO J. 2003 Aug 1;22(15):3792-802
pubmed: 12881414
Mol Biol Cell. 2017 Oct 15;28(21):2765-2772
pubmed: 28814508
J Biol Chem. 2000 Jun 23;275(25):18759-66
pubmed: 10764757
J Cell Biol. 2019 Oct 7;218(10):3171-3187
pubmed: 31537714
Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6229-33
pubmed: 7541532
Hum Genomics. 2012 Jul 05;6:6
pubmed: 23245351
EMBO J. 1996 Jul 15;15(14):3538-46
pubmed: 8670857
Mol Biol Cell. 1992 Feb;3(2):129-42
pubmed: 1550957
J Biol Chem. 2012 Jan 2;287(1):43-47
pubmed: 22105075
Genetics. 2011 Nov;189(3):695-704
pubmed: 22084421
J Biol Chem. 2016 Apr 29;291(18):9469-81
pubmed: 26953341
J Biol Chem. 2008 Mar 21;283(12):7568-79
pubmed: 18167355
PLoS Biol. 2011 Apr;9(4):e1001052
pubmed: 21541368
Eur J Biochem. 1995 Jul 15;231(2):312-6
pubmed: 7635143
FEBS Lett. 2015 Nov 14;589(22):3379-87
pubmed: 26226420
FEBS J. 2015 May;282(10):2045-59
pubmed: 25754985
Cell. 2009 Jan 23;136(2):272-83
pubmed: 19167329
Neurosci Lett. 2003 Oct 30;350(3):153-6
pubmed: 14550917
Ann Neurol. 1989 Nov;26(5):612-20
pubmed: 2817837
J Neurosci. 2005 Apr 13;25(15):3801-12
pubmed: 15829632
J Virol. 1997 Apr;71(4):3083-9
pubmed: 9060670
Hum Mol Genet. 2010 Sep 15;19(18):3502-15
pubmed: 20584926
Annu Rev Biochem. 2015;84:435-64
pubmed: 25784053
J Neurosci. 2004 Mar 17;24(11):2593-601
pubmed: 15028751
Mol Biol Cell. 2001 May;12(5):1303-14
pubmed: 11359923
Free Radic Biol Med. 2015 Jun;83:305-13
pubmed: 25697778
Crit Rev Biochem Mol Biol. 2015;50(6):532-49
pubmed: 26592310
Semin Cell Dev Biol. 2010 Jul;21(5):491-9
pubmed: 20045480
Neuroscience. 2009 Dec 15;164(3):1127-37
pubmed: 19761814
J Biol Chem. 2003 Nov 21;278(47):46895-905
pubmed: 12954632
Proc Am Thorac Soc. 2010 Nov;7(6):363-7
pubmed: 21030514
J Biochem. 1991 Aug;110(2):306-13
pubmed: 1761527
Hum Mutat. 2014 Sep;35(9):1114-22
pubmed: 24931141
Front Chem. 2014 Aug 26;2:70
pubmed: 25207270
Cell. 1999 Feb 5;96(3):341-52
pubmed: 10025400
Am J Physiol Renal Physiol. 2011 Jul;301(1):F1-11
pubmed: 21490136
Glycobiology. 2019 Apr 1;29(4):320-331
pubmed: 30689864
Hum Mol Genet. 2000 May 22;9(9):1403-13
pubmed: 10814722
J Biol Chem. 1995 Mar 3;270(9):4797-804
pubmed: 7876253
Proc Natl Acad Sci U S A. 2019 May 14;116(20):9865-9870
pubmed: 31036665
Hum Mol Genet. 2008 Sep 1;17(17):2712-22
pubmed: 18552369
Nat Rev Mol Cell Biol. 2008 Dec;9(12):944-57
pubmed: 19002207
Biochem J. 2007 Jan 15;401(2):607-12
pubmed: 17037984
FEBS Lett. 1989 Sep 25;255(2):265-8
pubmed: 2551733
EMBO Rep. 2005 Jan;6(1):28-32
pubmed: 15643448
Mol Cell Proteomics. 2009 Feb;8(2):357-64
pubmed: 18854577
J Neurosci Methods. 2020 Jun 1;339:108728
pubmed: 32289333
Nat Commun. 2019 Jul 22;10(1):3262
pubmed: 31332180
Science. 1999 Dec 3;286(5446):1882-8
pubmed: 10583943
Nat Commun. 2011 Jul 12;2:393
pubmed: 21750546
Biochem J. 2003 Aug 15;374(Pt 1):117-22
pubmed: 12780349
Semin Cell Dev Biol. 2010 Jul;21(5):472-8
pubmed: 20026282
Neuroscience. 2008 Dec 2;157(3):588-95
pubmed: 18940237
Microbiol Mol Biol Rev. 2012 Jun;76(2):115-58
pubmed: 22688810
Biotechnol J. 2008 Mar;3(3):325-38
pubmed: 18228539
J Biol Chem. 2014 May 2;289(18):12727-47
pubmed: 24627482
Adv Neurol. 1998;78:93-105
pubmed: 9750906
Mol Biol Cell. 2003 Jun;14(6):2559-69
pubmed: 12808051
Biochem Biophys Res Commun. 1997 Oct 29;239(3):710-4
pubmed: 9367834
EMBO J. 2020 May 18;39(10):e103841
pubmed: 32149426
J Neurochem. 2004 Feb;88(4):1019-25
pubmed: 14756824
Mol Ther Nucleic Acids. 2020 Sep 4;21:1-12
pubmed: 32502938
Annu Rev Nutr. 2016 Jul 17;36:511-42
pubmed: 27296502
Mol Biol Cell. 2009 Jun;20(11):2661-72
pubmed: 19339278
Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15650-5
pubmed: 15505207
Springerplus. 2014 Dec 16;3:743
pubmed: 25674472
Mol Cell Biol. 2001 Sep;21(18):6139-50
pubmed: 11509657
Hum Mol Genet. 2010 Mar 1;19(5):888-900
pubmed: 20015956
J Neurochem. 2008 Oct;107(1):20-34
pubmed: 18643792
Trends Genet. 2018 Jun;34(6):466-476
pubmed: 29606283
Nat Genet. 1997 Sep;17(1):40-8
pubmed: 9288096
Front Mol Biosci. 2020 Oct 02;7:585643
pubmed: 33134321
Biochim Biophys Acta. 2008 Jul;1783(7):1381-95
pubmed: 18298958
Arch Neurol. 2000 Aug;57(8):1129-34
pubmed: 10927792
Glycobiology. 2000 Jan;10(1):77-87
pubmed: 10570226
Biochim Biophys Acta. 2008 Apr;1783(4):549-56
pubmed: 18191641
Elife. 2014 Aug 22;3:e03239
pubmed: 25149450
Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11061-6
pubmed: 19549845
Mol Cells. 2010 Dec;30(6):497-506
pubmed: 21340671
Mol Biol Cell. 2008 Aug;19(8):3599-612
pubmed: 18550799
Biochim Biophys Acta. 2005 Nov 15;1726(2):121-37
pubmed: 16126345
Annu Rev Biochem. 2004;73:1019-49
pubmed: 15189166
Cell Stress Chaperones. 2010 Sep;15(5):605-17
pubmed: 20169475
Semin Cell Dev Biol. 2007 Dec;18(6):751-61
pubmed: 17964199
Eur J Neurol. 2010 Jul;17 Suppl 1:81-7
pubmed: 20590813
J Neurochem. 2013 Jan;124(1):45-58
pubmed: 23043510
Pharmacol Ther. 2020 Jun;210:107525
pubmed: 32201313
Mol Cell Neurosci. 2004 Dec;27(4):417-26
pubmed: 15555920
Mol Cell. 1998 Jan;1(2):161-70
pubmed: 9659913
J Cell Biol. 2001 Feb 5;152(3):553-62
pubmed: 11157982
Cold Spring Harb Perspect Biol. 2020 May 1;12(5):
pubmed: 31088828
Lancet Neurol. 2002 Sep;1(5):316-25
pubmed: 12849429
Proc Natl Acad Sci U S A. 2014 Nov 11;111(45):E4822-31
pubmed: 25352667
Cold Spring Harb Perspect Biol. 2019 Aug 1;11(8):
pubmed: 30670468
Mol Cell. 1998 Jan;1(2):171-82
pubmed: 9659914
Science. 2008 Jul 25;321(5888):569-72
pubmed: 18653895
J Cell Biol. 2014 Aug 18;206(4):525-39
pubmed: 25135935
Cell. 1993 Sep 10;74(5):899-908
pubmed: 8374956
Mol Neurobiol. 2014 Apr;49(2):796-807
pubmed: 24091828
Science. 2003 Dec 5;302(5651):1769-72
pubmed: 14657499
Parkinsonism Relat Disord. 2007;13 Suppl 3:S347-55
pubmed: 18267263
Curr Opin Struct Biol. 2011 Oct;21(5):576-82
pubmed: 21978957
EMBO J. 2011 Jul 22;30(16):3217-31
pubmed: 21785409
J Biol Chem. 2010 Nov 26;285(48):37271-80
pubmed: 20861018
Mol Cell Biol. 1992 Oct;12(10):4601-11
pubmed: 1406650
Dis Model Mech. 2017 Sep 1;10(9):1129-1140
pubmed: 28768697
Antioxid Redox Signal. 2009 Nov;11(11):2807-50
pubmed: 19476414
EMBO J. 1992 May;11(5):1717-22
pubmed: 1582407
Neurochem Res. 2011 Mar;36(3):452-9
pubmed: 21161590
J Cell Biol. 2005 Mar 14;168(6):855-62
pubmed: 15767459
Science. 2018 Aug 3;361(6401):
pubmed: 30072511
J Biochem. 1990 Nov;108(5):846-51
pubmed: 2081737
Physiol Rev. 1999 Apr;79(2):425-49
pubmed: 10221986
J Clin Invest. 2014 Jul;124(7):3080-92
pubmed: 24937429
Prog Mol Biol Transl Sci. 2019;168:351-379
pubmed: 31699326
FEBS Lett. 1995 Aug 7;369(2-3):212-6
pubmed: 7649260
Glycoconj J. 2016 Jun;33(3):359-76
pubmed: 26638212
Exp Neurol. 2008 Apr;210(2):719-30
pubmed: 18299128
J Biol Chem. 2019 Sep 13;294(37):13638-13656
pubmed: 31337704
Front Cell Neurosci. 2014 Jul 29;8:213
pubmed: 25120434
Hum Mutat. 2014 Sep;35(9):1101-13
pubmed: 24930953
Mol Cell. 2011 Jun 24;42(6):782-93
pubmed: 21700223
Glycobiology. 2017 Jan;27(1):3-49
pubmed: 27558841
Front Mol Biosci. 2017 May 11;4:29
pubmed: 28553638
J Cell Biol. 2019 Aug 5;218(8):2782-2796
pubmed: 31296534