HNK-1 sulfotransferase modulates α-dystroglycan glycosylation by 3-O-sulfation of glucuronic acid on matriglycan.
O-mannosylation
congenital muscular dystrophy
glycosylation
sulfotransferase
α-dystroglycan
Journal
Glycobiology
ISSN: 1460-2423
Titre abrégé: Glycobiology
Pays: England
ID NLM: 9104124
Informations de publication
Date de publication:
28 09 2020
28 09 2020
Historique:
received:
14
07
2019
revised:
26
02
2020
accepted:
26
02
2020
pubmed:
10
3
2020
medline:
28
10
2021
entrez:
10
3
2020
Statut:
ppublish
Résumé
Mutations in multiple genes required for proper O-mannosylation of α-dystroglycan are causal for congenital/limb-girdle muscular dystrophies and abnormal brain development in mammals. Previously, we and others further elucidated the functional O-mannose glycan structure that is terminated by matriglycan, [(-GlcA-β3-Xyl-α3-)n]. This repeating disaccharide serves as a receptor for proteins in the extracellular matrix. Here, we demonstrate in vitro that HNK-1 sulfotransferase (HNK-1ST/carbohydrate sulfotransferase) sulfates terminal glucuronyl residues of matriglycan at the 3-hydroxyl and prevents further matriglycan polymerization by the LARGE1 glycosyltransferase. While α-dystroglycan isolated from mouse heart and kidney is susceptible to exoglycosidase digestion of matriglycan, the functional, lower molecular weight α-dystroglycan detected in brain, where HNK-1ST expression is elevated, is resistant. Removal of the sulfate cap by a sulfatase facilitated dual-glycosidase digestion. Our data strongly support a tissue specific mechanism in which HNK-1ST regulates polymer length by competing with LARGE for the 3-position on the nonreducing GlcA of matriglycan.
Identifiants
pubmed: 32149355
pii: 5788508
doi: 10.1093/glycob/cwaa024
pmc: PMC7673472
doi:
Substances chimiques
Dystroglycans
146888-27-9
Glucuronic Acid
8A5D83Q4RW
HNK-1 sulfotransferase
EC 2.8.2.-
Sulfotransferases
EC 2.8.2.-
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
817-829Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM111939
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103390
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103490
Pays : United States
Organisme : NINDS NIH HHS
ID : P50 NS053672
Pays : United States
Organisme : NIGMS NIH HHS
ID : P01 GM107012
Pays : United States
Organisme : NINDS NIH HHS
ID : U54 NS053672
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM130915
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Informations de copyright
© The Author(s) 2020. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Références
Biochim Biophys Acta Gen Subj. 2017 Oct;1861(10):2462-2472
pubmed: 28711406
Curr Opin Struct Biol. 2019 Jun;56:56-63
pubmed: 30530204
Cell. 1991 Sep 20;66(6):1121-31
pubmed: 1913804
J Biol Chem. 2002 May 24;277(21):18928-37
pubmed: 11886875
J Biol Chem. 2010 Nov 26;285(48):37293-301
pubmed: 20855890
Biochem Biophys Res Commun. 2011 Nov 11;415(1):109-13
pubmed: 22020094
Science. 2012 Jan 6;335(6064):93-6
pubmed: 22223806
J Biol Chem. 2002 May 17;277(20):18182-90
pubmed: 11891229
Glycobiology. 2013 Sep;23(9):1066-74
pubmed: 23723439
J Biol Chem. 1997 Apr 4;272(14):8924-31
pubmed: 9083013
J Virol. 2005 Nov;79(22):14282-96
pubmed: 16254363
J Am Chem Soc. 2010 Jan 13;132(1):96-105
pubmed: 19958024
Glycobiology. 2015 Jul;25(7):702-13
pubmed: 25882296
J Clin Invest. 2012 Sep;122(9):3330-42
pubmed: 22922256
EMBO J. 1999 Feb 15;18(4):863-70
pubmed: 10022829
J Biol Chem. 2000 Jul 21;275(29):22082-9
pubmed: 10801892
J Biol Chem. 2013 Feb 15;288(7):5007-16
pubmed: 23269668
J Biol Chem. 2012 Aug 31;287(36):30823-32
pubmed: 22801424
J Biol Chem. 1997 Dec 19;272(51):32092-101
pubmed: 9405406
Glycobiology. 2015 Dec;25(12):1323-4
pubmed: 26543186
Cell Mol Life Sci. 2012 Dec;69(24):4135-47
pubmed: 22669261
Methods Enzymol. 2010;479:73-91
pubmed: 20816160
Nature. 1983 Nov 24-30;306(5941):376-8
pubmed: 6196641
Nat Genet. 2012 May;44(5):575-80
pubmed: 22522420
J Biol Chem. 2013 Mar 8;288(10):6930-5
pubmed: 23329833
Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):598-603
pubmed: 9892679
Elife. 2016 Apr 29;5:
pubmed: 27130732
Biochemistry. 2014 May 20;53(19):3066-78
pubmed: 24786756
Glycobiology. 2013 Mar;23(3):295-302
pubmed: 23125099
Nat Chem Biol. 2016 Oct;12(10):810-4
pubmed: 27526028
Eur J Neurosci. 1993 Jan 1;5(1):34-42
pubmed: 8261088
PLoS One. 2010 Dec 28;5(12):e14434
pubmed: 21203384
Biochem J. 2005 Aug 15;390(Pt 1):303-9
pubmed: 15865602
Nat Rev Neurosci. 2004 Mar;5(3):195-208
pubmed: 14976519
J Biochem. 2018 May 1;163(5):359-369
pubmed: 29394359
J Biol Chem. 2005 May 27;280(21):20851-9
pubmed: 15788414
Eur J Biochem. 1997 May 15;246(1):233-42
pubmed: 9210489
J Biol Chem. 1996 Dec 13;271(50):32321-9
pubmed: 8943294
J Biol Chem. 2013 Nov 29;288(48):34680-98
pubmed: 24155237
Nature. 2002 Jul 25;418(6896):417-22
pubmed: 12140558
Nature. 1984 Sep 13-19;311(5982):153-5
pubmed: 6206400
Chem Biol. 2015 Dec 17;22(12):1643-52
pubmed: 26687144
J Biol Chem. 1986 Sep 5;261(25):11717-25
pubmed: 3017944
Science. 2010 Jan 1;327(5961):88-92
pubmed: 20044576
Glycobiology. 2017 Sep 1;27(9):806-819
pubmed: 28810660
Elife. 2014 Oct 03;3:
pubmed: 25279699
Carbohydr Res. 2006 Jan 16;341(1):49-59
pubmed: 16303119
J Biol Chem. 2011 Sep 23;286(38):33003-11
pubmed: 21828042
J Biol Chem. 2016 Nov 18;291(47):24618-24627
pubmed: 27733679
J Biol Chem. 1996 Sep 20;271(38):22957-60
pubmed: 8798480
Nat Med. 2004 Jul;10(7):696-703
pubmed: 15184894
Elife. 2014 Oct 03;3:
pubmed: 25279697
EMBO J. 2000 Apr 3;19(7):1432-40
pubmed: 10747011
Glycobiology. 2005 Oct;15(10):912-23
pubmed: 15958417
Nat Genet. 2001 Jun;28(2):151-4
pubmed: 11381262
J Cell Biol. 1993 Aug;122(4):809-23
pubmed: 8349731
Nat Commun. 2016 May 19;7:11534
pubmed: 27194101
Nat Genet. 2012 May;44(5):581-5
pubmed: 22522421
Cell Rep. 2016 Mar 8;14(9):2209-2223
pubmed: 26923585
FEBS Lett. 2006 Jun 12;580(14):3381-5
pubmed: 16709410
Matrix Biol. 2005 Aug;24(5):326-32
pubmed: 15979864
Science. 2013 Aug 23;341(6148):896-9
pubmed: 23929950
Nat Chem Biol. 2018 Feb;14(2):156-162
pubmed: 29251719
Glycobiology. 2014 Mar;24(3):314-24
pubmed: 24352591
J Biol Chem. 1997 Nov 21;272(47):29942-6
pubmed: 9368071
J Biol Chem. 2015 Apr 17;290(16):10256-73
pubmed: 25737452
Biochim Biophys Acta Gen Subj. 2017 Oct;1861(10):2455-2461
pubmed: 28709864