Glypicans shield the Wnt lipid moiety to enable signalling at a distance.
Adaptor Proteins, Signal Transducing
/ chemistry
Animals
Cell Cycle Proteins
/ chemistry
Drosophila Proteins
/ chemistry
Drosophila melanogaster
Fatty Acids, Monounsaturated
/ chemistry
Female
Glypicans
/ chemistry
Humans
Hydrophobic and Hydrophilic Interactions
Lipids
/ chemistry
Male
Models, Molecular
Mutation
Nuclear Proteins
/ chemistry
Protein Binding
/ genetics
Protein Domains
Protein Transport
Signal Transduction
Solubility
Wnt Proteins
/ chemistry
Wnt1 Protein
/ chemistry
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
08
08
2019
accepted:
23
04
2020
pubmed:
24
7
2020
medline:
6
10
2020
entrez:
24
7
2020
Statut:
ppublish
Résumé
A relatively small number of proteins have been suggested to act as morphogens-signalling molecules that spread within tissues to organize tissue repair and the specification of cell fate during development. Among them are Wnt proteins, which carry a palmitoleate moiety that is essential for signalling activity
Identifiants
pubmed: 32699409
doi: 10.1038/s41586-020-2498-z
pii: 10.1038/s41586-020-2498-z
pmc: PMC7610841
mid: EMS124251
doi:
Substances chimiques
Adaptor Proteins, Signal Transducing
0
Cell Cycle Proteins
0
Daxx protein, Drosophila
0
Drosophila Proteins
0
Fatty Acids, Monounsaturated
0
Glypicans
0
Lipids
0
Nuclear Proteins
0
TXNL4B protein, human
0
Wnt Proteins
0
Wnt1 Protein
0
wg protein, Drosophila
0
palmitoleic acid
209B6YPZ4I
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
85-90Subventions
Organisme : Arthritis Research UK
ID : FC001204
Pays : United Kingdom
Organisme : Wellcome Trust
ID : FC001204
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 102164/B/13/Z
Pays : United Kingdom
Organisme : Cancer Research UK
ID : FC001204
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : FC001204
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203141/Z/16/Z
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Type : CommentIn
Références
Willert, K. et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448–452 (2003).
pubmed: 12717451
Takada, R. et al. Monounsaturated fatty acid modification of Wnt protein: its role in Wnt secretion. Dev. Cell 11, 791–801 (2006).
pubmed: 17141155
Janda, C. Y., Waghray, D., Levin, A. M., Thomas, C. & Garcia, K. C. Structural basis of Wnt recognition by Frizzled. Science 337, 59–64 (2012).
pubmed: 22653731
pmcid: 3577348
Panáková, D., Sprong, H., Marois, E., Thiele, C. & Eaton, S. Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435, 58–65 (2005).
pubmed: 15875013
Gross, J. C., Chaudhary, V., Bartscherer, K. & Boutros, M. Active Wnt proteins are secreted on exosomes. Nat. Cell Biol. 14, 1036–1045 (2012).
pubmed: 22983114
Mulligan, K. A. et al. Secreted Wingless-interacting molecule (Swim) promotes long-range signaling by maintaining Wingless solubility. Proc. Natl Acad. Sci. USA 109, 370–377 (2012).
pubmed: 22203956
Kiecker, C. & Niehrs, C. A morphogen gradient of Wnt/β-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development 128, 4189–4201 (2001).
pubmed: 11684656
Farin, H. F. et al. Visualization of a short-range Wnt gradient in the intestinal stem-cell niche. Nature 530, 340–343 (2016).
pubmed: 26863187
Alexandre, C., Baena-Lopez, A. & Vincent, J. P. Patterning and growth control by membrane-tethered Wingless. Nature 505, 180–185 (2014).
pubmed: 24390349
Tian, A., Duwadi, D., Benchabane, H. & Ahmed, Y. Essential long-range action of Wingless/Wnt in adult intestinal compartmentalization. PLoS Genet. 15, e1008111 (2019).
pubmed: 31194729
pmcid: 6563961
Zecca, M., Basler, K. & Struhl, G. Direct and long-range action of a wingless morphogen gradient. Cell 87, 833–844 (1996).
pubmed: 8945511
Harmansa, S., Hamaratoglu, F., Affolter, M. & Caussinus, E. Dpp spreading is required for medial but not for lateral wing disc growth. Nature 527, 317–322 (2015).
pubmed: 26550827
Yan, D., Wu, Y., Feng, Y., Lin, S. C. & Lin, X. The core protein of glypican Dally-like determines its biphasic activity in wingless morphogen signaling. Dev. Cell 17, 470–481 (2009).
pubmed: 19853561
pmcid: 3326419
Franch-Marro, X. et al. Glypicans shunt the Wingless signal between local signalling and further transport. Development 132, 659–666 (2005).
pubmed: 15647318
Stanganello, E. et al. Filopodia-based Wnt transport during vertebrate tissue patterning. Nat. Commun. 6, 5846 (2015).
pubmed: 25556612
Baeg, G. H., Selva, E. M., Goodman, R. M., Dasgupta, R. & Perrimon, N. The Wingless morphogen gradient is established by the cooperative action of Frizzled and Heparan Sulfate Proteoglycan receptors. Dev. Biol. 276, 89–100 (2004).
pubmed: 15531366
Reichsman, F., Smith, L. & Cumberledge, S. Glycosaminoglycans can modulate extracellular localization of the wingless protein and promote signal transduction. J. Cell Biol. 135, 819–827 (1996).
pubmed: 8909553
Baena-Lopez, L. A., Franch-Marro, X. & Vincent, J. P. Wingless promotes proliferative growth in a gradient-independent manner. Sci. Signal. 2, ra60 (2009).
pubmed: 19809090
pmcid: 3000546
Tang, X. et al. Roles of N-glycosylation and lipidation in Wg secretion and signaling. Dev. Biol. 364, 32–41 (2012).
pubmed: 22285813
pmcid: 3315154
Kakugawa, S. et al. Notum deacylates Wnt proteins to suppress signalling activity. Nature 519, 187–192 (2015).
pubmed: 25731175
pmcid: 4376489
Fuerer, C., Habib, S. J. & Nusse, R. A study on the interactions between heparan sulfate proteoglycans and Wnt proteins. Dev. Dyn. 239, 184–190 (2010).
pubmed: 19705435
pmcid: 2846786
Mihara, E. et al. Active and water-soluble form of lipidated Wnt protein is maintained by a serum glycoprotein afamin/α-albumin. eLife 5, e11621 (2016).
pubmed: 26902720
pmcid: 4775226
Kim, M. S., Saunders, A. M., Hamaoka, B. Y., Beachy, P. A. & Leahy, D. J. Structure of the protein core of the glypican Dally-like and localization of a region important for hedgehog signaling. Proc. Natl Acad. Sci. USA 108, 13112–13117 (2011).
pubmed: 21828006
Pei, J. & Grishin, N. V. Cysteine-rich domains related to Frizzled receptors and Hedgehog-interacting proteins. Protein Sci. 21, 1172–1184 (2012).
pubmed: 22693159
pmcid: 3537238
Hirai, H., Matoba, K., Mihara, E., Arimori, T. & Takagi, J. Crystal structure of a mammalian Wnt-frizzled complex. Nat. Struct. Mol. Biol. 26, 372–379 (2019).
pubmed: 31036956
Awad, W. et al. Structural Aspects of N-Glycosylations and the C-terminal Region in Human Glypican-1. J. Biol. Chem. 290, 22991–23008 (2015).
pubmed: 26203194
pmcid: 4645609
Sivasankaran, R., Calleja, M., Morata, G. & Basler, K. The Wingless target gene Dfz3 encodes a new member of the Drosophila Frizzled family. Mech. Dev. 91, 427–431 (2000).
pubmed: 10704878
Schilling, S., Steiner, S., Zimmerli, D. & Basler, K. A regulatory receptor network directs the range and output of the Wingless signal. Development 141, 2483–2493 (2014).
pubmed: 24917503
Mii, Y. & Taira, M. Secreted Frizzled-related proteins enhance the diffusion of Wnt ligands and expand their signalling range. Development 136, 4083–4088 (2009).
pubmed: 19906850
Hayashi, Y., Kobayashi, S. & Nakato, H. Drosophila glypicans regulate the germline stem cell niche. J. Cell Biol. 187, 473–480 (2009).
pubmed: 19948496
pmcid: 2779228
Wang, X. & Page-McCaw, A. A matrix metalloproteinase mediates long-distance attenuation of stem cell proliferation. J. Cell Biol. 206, 923–936 (2014).
pubmed: 25267296
pmcid: 4178971
Serralbo, O. & Marcelle, C. Migrating cells mediate long-range WNT signaling. Development 141, 2057–2063 (2014).
pubmed: 24803654
González-Méndez, L., Gradilla, A. C. & Guerrero, I. The cytoneme connection: direct long-distance signal transfer during development. Development 146, dev174607 (2019).
pubmed: 31068374
Elegheert, J. et al. Lentiviral transduction of mammalian cells for fast, scalable and high-level production of soluble and membrane proteins. Nat. Protocols 13, 2991–3017 (2018).
pubmed: 30455477
Reeves, P. J., Callewaert, N., Contreras, R. & Khorana, H. G. Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl Acad. Sci. USA 99, 13419–13424 (2002).
pubmed: 12370423
Aricescu, A. R., Lu, W. & Jones, E. Y. A time- and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr. D 62, 1243–1250 (2006).
pubmed: 17001101
Chang, V. T. et al. Glycoprotein structural genomics: solving the glycosylation problem. Structure 15, 267–273 (2007).
pubmed: 17355862
pmcid: 1885966
Walter, T. S. et al. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr. D 61, 651–657 (2005).
pubmed: 15930615
Newman, J. Novel buffer systems for macromolecular crystallization. Acta Crystallogr. D 60, 610–612 (2004).
pubmed: 14993709
Winter, G., Lobley, C. M. & Prince, S. M. Decision making in xia2. Acta Crystallogr. D 69, 1260–1273 (2013).
pubmed: 23793152
Winter, G. et al. DIALS: implementation and evaluation of a new integration package. Acta Crystallogr. D 74, 85–97 (2018).
Evans, P. R. & Murshudov, G. N. How good are my data and what is the resolution? Acta Crystallogr. D 69, 1204–1214 (2013).
pubmed: 23793146
Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235–242 (2011).
pubmed: 21460441
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
pubmed: 19461840
pmcid: 2483472
Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D 68, 352–367 (2012).
pubmed: 22505256
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
pubmed: 20383002
Smart, O. S. Grade v.1.105; http://grade.globalphasing.org (2012).
Williams, C. J. et al. MolProbity: More and better reference data for improved all-atom structure validation. Protein Sci. 27, 293–315 (2018).
pubmed: 29067766
Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797 (2007).
pubmed: 17681537
Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M. & Barton, G. J. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009).
pubmed: 19151095
pmcid: 2672624
Tian, W., Chen, C., Lei, X., Zhao, J. & Liang, J. CASTp 3.0: computed atlas of surface topography of proteins. Nucleic Acids Res. 46 (W1), W363–W367 (2018).
pubmed: 29860391
pmcid: 6031066
Beckett, D., Kovaleva, E. & Schatz, P. J. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci. 8, 921–929 (1999).
pubmed: 10211839
pmcid: 2144313
Port, F., Chen, H. M., Lee, T. & Bullock, S. L. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc. Natl Acad. Sci. USA 111, E2967–E2976 (2014).
pubmed: 25002478
Liebschner, D. et al. Polder maps: improving OMIT maps by excluding bulk solvent. Acta Crystallogr. D 73, 148–157 (2017).