Structure of the human GlcNAc-1-phosphotransferase αβ subunits reveals regulatory mechanism for lysosomal enzyme glycan phosphorylation.
Journal
Nature structural & molecular biology
ISSN: 1545-9985
Titre abrégé: Nat Struct Mol Biol
Pays: United States
ID NLM: 101186374
Informations de publication
Date de publication:
04 2022
04 2022
Historique:
received:
01
09
2021
accepted:
16
02
2022
pubmed:
26
3
2022
medline:
19
4
2022
entrez:
25
3
2022
Statut:
ppublish
Résumé
Vertebrates use the mannose 6-phosphate (M6P)-recognition system to deliver lysosomal hydrolases to lysosomes. Key to this pathway is N-acetylglucosamine (GlcNAc)-1-phosphotransferase (PTase) that selectively adds GlcNAc-phosphate (P) to mannose residues of hydrolases. Human PTase is an α
Identifiants
pubmed: 35332324
doi: 10.1038/s41594-022-00748-0
pii: 10.1038/s41594-022-00748-0
pmc: PMC9018626
mid: NIHMS1786738
doi:
Substances chimiques
Phosphates
0
Polysaccharides
0
Phosphotransferases
EC 2.7.-
Hydrolases
EC 3.-
Mannose
PHA4727WTP
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
348-356Subventions
Organisme : NCI NIH HHS
ID : R01 CA008759
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA231466
Pays : United States
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
Braulke, T. & Bonifacino, J. S. Sorting of lysosomal proteins. Biochim. Biophys. Acta 1793, 605–614 (2009).
doi: 10.1016/j.bbamcr.2008.10.016
pubmed: 19046998
Burda, P. & Aebi, M. The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1426, 239–257 (1999).
doi: 10.1016/S0304-4165(98)00127-5
pubmed: 9878760
Bai, L. & Li, H. Cryo-EM is uncovering the mechanism of eukaryotic protein N-glycosylation. FEBS J. 286, 1638–1644 (2019).
doi: 10.1111/febs.14705
pubmed: 30450807
Kudo, M. et al. The α- and β-subunits of the human UDP-N-acetylglucosamine:lysosomal enzyme N-acetylglucosamine-1-phosphotransferase [corrected] are encoded by a single cDNA. J. Biol. Chem. 280, 36141–36149 (2005).
doi: 10.1074/jbc.M509008200
pubmed: 16120602
Raas-Rothschild, A. et al. Molecular basis of variant pseudo-Hurler polydystrophy (mucolipidosis IIIC). J. Clin. Invest. 105, 673–681 (2000).
doi: 10.1172/JCI5826
pubmed: 10712439
pmcid: 289169
Sperisen, P., Schmid, C. D., Bucher, P. & Zilian, O. Stealth proteins: in silico identification of a novel protein family rendering bacterial pathogens invisible to host immune defense. PLoS Comput. Biol. 1, e63 (2005).
doi: 10.1371/journal.pcbi.0010063
pubmed: 16299590
pmcid: 1285062
Qian, Y. et al. Functions of the α, β, and γ subunits of UDP-GlcNAc:lysosomal enzyme N-acetylglucosamine-1-phosphotransferase. J. Biol. Chem. 285, 3360–3370 (2010).
doi: 10.1074/jbc.M109.068650
pubmed: 19955174
Marschner, K., Kollmann, K., Schweizer, M., Braulke, T. & Pohl, S. A key enzyme in the biogenesis of lysosomes is a protease that regulates cholesterol metabolism. Science 333, 87–90 (2011).
doi: 10.1126/science.1205677
pubmed: 21719679
Braulke, T., Pohl, S. & Storch, S. Molecular analysis of the GlcNac-1-phosphotransferase. J. Inherit. Metab. Dis. 31, 253–257 (2008).
doi: 10.1007/s10545-008-0862-5
pubmed: 18425436
Qian, Y. et al. Analysis of mucolipidosis II/III GNPTAB missense mutations identifies domains of UDP-GlcNAc:lysosomal enzyme GlcNAc-1-phosphotransferase involved in catalytic function and lysosomal enzyme recognition. J. Biol. Chem. 290, 3045–3056 (2015).
doi: 10.1074/jbc.M114.612507
pubmed: 25505245
Liu, L., Lee, W. S., Doray, B. & Kornfeld, S. Role of spacer-1 in the maturation and function of GlcNAc-1-phosphotransferase. FEBS Lett. 591, 47–55 (2017).
doi: 10.1002/1873-3468.12525
pubmed: 27981560
pmcid: 5235957
Qian, Y., Flanagan-Steet, H., van Meel, E., Steet, R. & Kornfeld, S. A. The DMAP interaction domain of UDP-GlcNAc:lysosomal enzyme N-acetylglucosamine-1-phosphotransferase is a substrate recognition module. Proc. Natl Acad. Sci. USA 110, 10246–10251 (2013).
doi: 10.1073/pnas.1308453110
pubmed: 23733939
pmcid: 3690890
van Meel, E. et al. Multiple domains of GlcNAc-1-phosphotransferase mediate recognition of lysosomal enzymes. J. Biol. Chem. 291, 8295–8307 (2016).
doi: 10.1074/jbc.M116.714568
pubmed: 26833567
pmcid: 4825028
De Pace, R. et al. Subunit interactions of the disease-related hexameric GlcNAc-1-phosphotransferase complex. Hum. Mol. Genet. 24, 6826–6835 (2015).
doi: 10.1093/hmg/ddv387
pubmed: 26385638
Velho, R. V., De Pace, R., Tidow, H., Braulke, T. & Pohl, S. Identification of the interaction domains between α- and γ-subunits of GlcNAc-1-phosphotransferase. FEBS Lett. 590, 4287–4295 (2016).
doi: 10.1002/1873-3468.12456
pubmed: 27736005
Liu, L., Lee, W. S., Doray, B. & Kornfeld, S. Engineering of GlcNAc-1-phosphotransferase for production of highly phosphorylated lysosomal enzymes for enzyme replacement therapy. Mol. Ther. Methods Clin. Dev. 5, 59–65 (2017).
doi: 10.1016/j.omtm.2017.03.006
pubmed: 28480305
pmcid: 5415318
Boustany, R. M. Lysosomal storage diseases—the horizon expands. Nat. Rev. Neurol. 9, 583–598 (2013).
doi: 10.1038/nrneurol.2013.163
pubmed: 23938739
Velho, R. V. et al. The lysosomal storage disorders mucolipidosis type II, type III α/β, and type III γ: update on GNPTAB and GNPTG mutations. Hum. Mutat. 40, 842–864 (2019).
pubmed: 30882951
Appelqvist, H., Waster, P., Kagedal, K. & Ollinger, K. The lysosome: from waste bag to potential therapeutic target. J. Mol. Cell Biol. 5, 214–226 (2013).
doi: 10.1093/jmcb/mjt022
pubmed: 23918283
Marques, A. R. A. & Saftig, P. Lysosomal storage disorders—challenges, concepts and avenues for therapy: beyond rare diseases. J Cell Sci. 132, jcs221739 (2019).
Kudo, M. & Canfield, W. M. Structural requirements for efficient processing and activation of recombinant human UDP-N-acetylglucosamine:lysosomal-enzyme-N-acetylglucosamine-1-phosphotransferase. J. Biol. Chem. 281, 11761–11768 (2006).
doi: 10.1074/jbc.M513717200
pubmed: 16507578
Tiede, S. et al. Mucolipidosis II is caused by mutations in GNPTA encoding the α/β GlcNAc-1-phosphotransferase. Nat. Med. 11, 1109–1112 (2005).
doi: 10.1038/nm1305
pubmed: 16200072
Wang, Y. et al. Identification of predominant GNPTAB gene mutations in Eastern Chinese patients with mucolipidosis II/III and a prenatal diagnosis of mucolipidosis II. Acta Pharmacol. Sin. 40, 279–287 (2019).
doi: 10.1038/s41401-018-0023-9
pubmed: 29872134
Pedersen, L. C. et al. Crystal structure of an α1,4-N-acetylhexosaminyltransferase (EXTL2), a member of the exostosin gene family involved in heparan sulfate biosynthesis. J. Biol. Chem. 278, 14420–14428 (2003).
doi: 10.1074/jbc.M210532200
pubmed: 12562774
Kitagawa, H., Shimakawa, H. & Sugahara, K. The tumor suppressor EXT-like gene EXTL2 encodes an α1, 4-N-acetylhexosaminyltransferase that transfers N-acetylgalactosamine and N-acetylglucosamine to the common glycosaminoglycan–protein linkage region. The key enzyme for the chain initiation of heparan sulfate. J. Biol. Chem. 274, 13933–13937 (1999).
doi: 10.1074/jbc.274.20.13933
pubmed: 10318803
Tiede, S. et al. Missense mutations in N-acetylglucosamine-1-phosphotransferase α/β subunit gene in a patient with mucolipidosis III and a mild clinical phenotype. Am. J. Med. Genet. A 137A, 235–240 (2005).
doi: 10.1002/ajmg.a.30868
pubmed: 16094673
Punjani, A. & Fleet, D. J. 3D variability analysis: resolving continuous flexibility and discrete heterogeneity from single particle cryo-EM. J. Struct. Biol. 213, 107702 (2021).
doi: 10.1016/j.jsb.2021.107702
pubmed: 33582281
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
doi: 10.1038/nmeth.4193
pubmed: 28250466
pmcid: 5494038
Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
doi: 10.1016/j.jsb.2015.08.008
pubmed: 26278980
pmcid: 6760662
Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. eLife 7, e42166 (2018).
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
doi: 10.1038/nmeth.4169
pubmed: 28165473
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).
doi: 10.1107/S0907444910007493
pubmed: 20383002
pmcid: 2852313
Buchan, D. W. A. & Jones, D. T. The PSIPRED Protein Analysis Workbench: 20 years on. Nucleic Acids Res. 47, W402–W407 (2019).
doi: 10.1093/nar/gkz297
pubmed: 31251384
pmcid: 6602445
Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr. D Struct. Biol. 75, 861–877 (2019).
doi: 10.1107/S2059798319011471
pubmed: 31588918
pmcid: 6778852
Williams, C. J. et al. MolProbity: more and better reference data for improved all-atom structure validation. Protein Sci. 27, 293–315 (2018).
doi: 10.1002/pro.3330
pubmed: 29067766
Robert, X. & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320–W324 (2014).
doi: 10.1093/nar/gku316
pubmed: 24753421
pmcid: 4086106
Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2017).