Home LiteratureArticle Details
PMID: 33637534 Published · epublish English Journal Article

Molecular architecture of the endocytic TPLATE complex.

Science advances ·Vol. 7 ·No. 9 ·2021-02-00

Yperman K, Wang J, Eeckhout D, Winkler J, Vu LD, Vandorpe M, Grones P, Mylle E, Kraus M, Merceron R, Nolf J, Mor E, De Bruyn P, Loris R, Potocký M, Savvides SN, De Rybel B, De Jaeger G, Van Damme D, Pleskot R

Abstract

Eukaryotic cells rely on endocytosis to regulate their plasma membrane proteome and lipidome. Most eukaryotic groups, except fungi and animals, have retained the evolutionary ancient TSET complex as an endocytic regulator. Unlike other coatomer complexes, structural insight into TSET is lacking. Here, we reveal the molecular architecture of plant TSET [TPLATE complex (TPC)] using an integrative structural approach. We identify crucial roles for specific TSET subunits in complex assembly and membrane interaction. Our data therefore generate fresh insight into the differences between the hexameric TSET in Dictyostelium and the octameric TPC in plants. Structural elucidation of this ancient adaptor complex represents the missing piece in the coatomer puzzle and vastly advances our functional as well as evolutionary insight into the process of endocytosis.

Authors & Affiliations
20 authors, click to expand affiliations / ORCID
Yperman Klaas ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Wang Jie ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Eeckhout Dominique ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Winkler Joanna ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Vu Lam Dai ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Vandorpe Michael ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Grones Peter ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Mylle Evelien
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Kraus Michael ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Merceron Romain
Department of Biochemistry and Microbiology, Ghent University, 9052 Ghent, Belgium. | VIB Center for Inflammation Research, 9052 Ghent, Belgium.
Nolf Jonah ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Mor Eliana ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
De Bruyn Pieter ORCID
Vrije Universiteit Brussel, Structural Biology Brussels, Department of Biotechnology, 1050 Brussels, Belgium. | VIB-VUB Center for Structural Biology, Structural Biology Research Center, Molecular Recognition Unit, 1050 Brussels, Belgium.
Loris Remy ORCID
VIB-VUB Center for Structural Biology, Structural Biology Research Center, Molecular Recognition Unit, 1050 Brussels, Belgium. | Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Rozvojová 263, 16502 Prague 6, Czech Republic.
Potocký Martin ORCID
Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Rozvojová 263, 16502 Prague 6, Czech Republic.
Savvides Savvas N ORCID
Department of Biochemistry and Microbiology, Ghent University, 9052 Ghent, Belgium. | VIB Center for Inflammation Research, 9052 Ghent, Belgium.
De Rybel Bert ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
De Jaeger Geert ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Van Damme Daniël ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. daniel.vandamme@psb.vib-ugent.be pleskot@ueb.cas.cz. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
Pleskot Roman ORCID
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium. daniel.vandamme@psb.vib-ugent.be pleskot@ueb.cas.cz. | VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium. | Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Rozvojová 263, 16502 Prague 6, Czech Republic.
References (66)
66 references, click to expand
  1. The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis.
    Proc Natl Acad Sci U S A. 2015 Oct 13;112(41):12870-5 PMID: 26417106
  2. Multiple lipid binding sites determine the affinity of PH domains for phosphoinositide-containing membranes.
    Sci Adv. 2020 Feb 19;6(8):eaay5736 PMID: 32128410
  3. The Cellulose Synthases Are Cargo of the TPLATE Adaptor Complex.
    Mol Plant. 2018 Feb 5;11(2):346-349 PMID: 29221860
  4. Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins.
    Plant Cell. 2006 Dec;18(12):3502-18 PMID: 17189342
  5. An improved toolbox to unravel the plant cellular machinery by tandem affinity purification of Arabidopsis protein complexes.
    Nat Protoc. 2015 Jan;10(1):169-87 PMID: 25521792
  6. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization.
    Brief Bioinform. 2019 Jul 19;20(4):1160-1166 PMID: 28968734
  7. Molecular basis for recognition of dilysine trafficking motifs by COPI.
    Dev Cell. 2012 Dec 11;23(6):1255-62 PMID: 23177648
  8. Plant AtEH/Pan1 proteins drive autophagosome formation at ER-PM contact sites with actin and endocytic machinery.
    Nat Commun. 2019 Nov 13;10(1):5132 PMID: 31723129
  9. 9Å structure of the COPI coat reveals that the Arf1 GTPase occupies two contrasting molecular environments.
    Elife. 2017 Jun 16;6: PMID: 28621666
  10. Evolution: On a bender--BARs, ESCRTs, COPs, and finally getting your coat.
    J Cell Biol. 2011 Jun 13;193(6):963-72 PMID: 21670211
  11. High Temporal Resolution Reveals Simultaneous Plasma Membrane Recruitment of TPLATE Complex Subunits.
    Plant Physiol. 2020 Jul;183(3):986-997 PMID: 32321842
  12. The MARTINI Coarse-Grained Force Field: Extension to Proteins.
    J Chem Theory Comput. 2008 May;4(5):819-34 PMID: 26621095
  13. An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins.
    J Biol Chem. 2007 Apr 13;282(15):11356-64 PMID: 17277311
  14. Conformational regulation of AP1 and AP2 clathrin adaptor complexes.
    Traffic. 2019 Oct;20(10):741-751 PMID: 31313456
  15. Establishment of Proximity-Dependent Biotinylation Approaches in Different Plant Model Systems.
    Plant Cell. 2020 Nov;32(11):3388-3407 PMID: 32843435
  16. A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core.
    J Mol Biol. 2018 Jul 20;430(15):2237-2243 PMID: 29258817
  17. A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants.
    Nat Plants. 2016 Jun 20;2:16089 PMID: 27322096
  18. A Combinatorial Lipid Code Shapes the Electrostatic Landscape of Plant Endomembranes.
    Dev Cell. 2018 May 21;45(4):465-480.e11 PMID: 29754803
  19. VMD: visual molecular dynamics.
    J Mol Graph. 1996 Feb;14(1):33-8, 27-8 PMID: 8744570
  20. UCSF Chimera--a visualization system for exploratory research and analysis.
    J Comput Chem. 2004 Oct;25(13):1605-12 PMID: 15264254
  21. Protein secondary structure prediction based on position-specific scoring matrices.
    J Mol Biol. 1999 Sep 17;292(2):195-202 PMID: 10493868
  22. Lipid organization of the plasma membrane.
    J Am Chem Soc. 2014 Oct 15;136(41):14554-9 PMID: 25229711
  23. Comparative protein modelling by satisfaction of spatial restraints.
    J Mol Biol. 1993 Dec 5;234(3):779-815 PMID: 8254673
  24. Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode.
    J Cell Sci. 2007 Sep 1;120(Pt 17):2977-85 PMID: 17715154
  25. Evolution and Natural History of Membrane Trafficking in Eukaryotes.
    Curr Biol. 2020 May 18;30(10):R553-R564 PMID: 32428497
  26. The structures of natively assembled clathrin-coated vesicles.
    Sci Adv. 2020 Jul 22;6(30):eaba8397 PMID: 32743076
  27. CHARMM-GUI Martini Maker for modeling and simulation of complex bacterial membranes with lipopolysaccharides.
    J Comput Chem. 2017 Oct 15;38(27):2354-2363 PMID: 28776689
  28. Molecular architecture and function of the SEA complex, a modulator of the TORC1 pathway.
    Mol Cell Proteomics. 2014 Nov;13(11):2855-70 PMID: 25073740
  29. Principles for Integrative Structural Biology Studies.
    Cell. 2019 May 30;177(6):1384-1403 PMID: 31150619
  30. Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1.
    Cell. 2013 Feb 14;152(4):755-67 PMID: 23415225
  31. Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase.
    Nat Plants. 2019 Mar;5(3):316-327 PMID: 30833711
  32. Building blocks for plant gene assembly.
    Plant Physiol. 2007 Dec;145(4):1183-91 PMID: 17965171
  33. VESICULAR TRANSPORT. A structure of the COPI coat and the role of coat proteins in membrane vesicle assembly.
    Science. 2015 Jul 10;349(6244):195-8 PMID: 26160949
  34. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification.
    Nat Biotechnol. 2008 Dec;26(12):1367-72 PMID: 19029910
  35. Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis.
    Curr Biol. 2011 Jun 21;21(12):1055-60 PMID: 21658946
  36. Characterization of TSET, an ancient and widespread membrane trafficking complex.
    Elife. 2014 May 27;3:e02866 PMID: 24867644
  37. Computer-assisted protein domain boundary prediction using the DomPred server.
    Curr Protein Pept Sci. 2007 Apr;8(2):181-8 PMID: 17430199
  38. Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins.
    Plant J. 2004 Nov;40(3):386-98 PMID: 15469496
  39. Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains.
    Elife. 2017 Jul 31;6: PMID: 28758890
  40. The PSIPRED Protein Analysis Workbench: 20 years on.
    Nucleic Acids Res. 2019 Jul 2;47(W1):W402-W407 PMID: 31251384
  41. FCHo proteins are nucleators of clathrin-mediated endocytosis.
    Science. 2010 Jun 4;328(5983):1281-4 PMID: 20448150
  42. Assembly of COPI and COPII Vesicular Coat Proteins on Membranes.
    Annu Rev Biophys. 2018 May 20;47:63-83 PMID: 29345989
  43. A high-speed search engine pLink 2 with systematic evaluation for proteome-scale identification of cross-linked peptides.
    Nat Commun. 2019 Jul 30;10(1):3404 PMID: 31363125
  44. Combining an Elastic Network With a Coarse-Grained Molecular Force Field: Structure, Dynamics, and Intermolecular Recognition.
    J Chem Theory Comput. 2009 Sep 8;5(9):2531-43 PMID: 26616630
  45. A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs.
    PLoS One. 2010 Mar 29;5(3):e9788 PMID: 20360960
  46. Polyphosphoinositides are enriched in plant membrane rafts and form microdomains in the plasma membrane.
    Plant Physiol. 2010 Apr;152(4):2173-87 PMID: 20181756
  47. Putting the pieces together: integrative modeling platform software for structure determination of macromolecular assemblies.
    PLoS Biol. 2012 Jan;10(1):e1001244 PMID: 22272186
  48. Jalview Version 2--a multiple sequence alignment editor and analysis workbench.
    Bioinformatics. 2009 May 1;25(9):1189-91 PMID: 19151095
  49. Assessing Exhaustiveness of Stochastic Sampling for Integrative Modeling of Macromolecular Structures.
    Biophys J. 2017 Dec 5;113(11):2344-2353 PMID: 29211988
  50. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis.
    Dev Cell. 2013 Feb 25;24(4):426-37 PMID: 23415953
  51. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  52. The ClusPro web server for protein-protein docking.
    Nat Protoc. 2017 Feb;12(2):255-278 PMID: 28079879
  53. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants.
    Nat Protoc. 2006;1(4):2019-25 PMID: 17487191
  54. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants.
    Cell. 2014 Feb 13;156(4):691-704 PMID: 24529374
  55. Template-based protein structure modeling using the RaptorX web server.
    Nat Protoc. 2012 Jul 19;7(8):1511-22 PMID: 22814390
  56. Architecture of the AP2/clathrin coat on the membranes of clathrin-coated vesicles.
    Sci Adv. 2020 Jul 22;6(30):eaba8381 PMID: 32743075
  57. DISOPRED3: precise disordered region predictions with annotated protein-binding activity.
    Bioinformatics. 2015 Mar 15;31(6):857-63 PMID: 25391399
  58. xVis: a web server for the schematic visualization and interpretation of crosslink-derived spatial restraints.
    Nucleic Acids Res. 2015 Jul 1;43(W1):W362-9 PMID: 25956653
  59. Molecular architecture and functional model of the endocytic AP2 complex.
    Cell. 2002 May 17;109(4):523-35 PMID: 12086608
  60. The Evolution of Organellar Coat Complexes and Organization of the Eukaryotic Cell.
    Annu Rev Biochem. 2017 Jun 20;86:637-657 PMID: 28471691
  61. UCSF ChimeraX: Meeting modern challenges in visualization and analysis.
    Protein Sci. 2018 Jan;27(1):14-25 PMID: 28710774
  62. Syp1 is a conserved endocytic adaptor that contains domains involved in cargo selection and membrane tubulation.
    EMBO J. 2009 Oct 21;28(20):3103-16 PMID: 19713939
  63. Improved Parameters for the Martini Coarse-Grained Protein Force Field.
    J Chem Theory Comput. 2013 Jan 8;9(1):687-97 PMID: 26589065
  64. The MARTINI force field: coarse grained model for biomolecular simulations.
    J Phys Chem B. 2007 Jul 12;111(27):7812-24 PMID: 17569554
  65. BeStSel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra.
    Nucleic Acids Res. 2018 Jul 2;46(W1):W315-W322 PMID: 29893907
  66. Transient Fcho1/2⋅Eps15/R⋅AP-2 Nanoclusters Prime the AP-2 Clathrin Adaptor for Cargo Binding.
    Dev Cell. 2016 Jun 6;37(5):428-43 PMID: 27237791
Article Info
Journal
Science advances
Abbr.
Sci Adv
ISSN
2375-2548
DOI
10.1126/sciadv.abe7999
Email
daniel.vandamme@psb.vib-ugent.be
pleskot@ueb.cas.cz
Published
2021-02-00
Epub
2021-00-26
Language
English
Region
United States
NLM ID
101653440
PMCID
PMC7909872
Subset
IM
Grants
European Research Council · 682436 · International
External Links
PubMed source DOI: 10.1126/sciadv.abe7999 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2