Home LiteratureArticle Details
PMID: 26522593 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Relaxation of Loaded ESCRT-III Spiral Springs Drives Membrane Deformation.

Cell ·Vol. 163 ·No. 4 ·2015-11-05 ·Pages 866-79

Chiaruttini N, Redondo-Morata L, Colom A, Humbert F, Lenz M, Scheuring S, Roux A

Abstract

ESCRT-III is required for lipid membrane remodeling in many cellular processes, from abscission to viral budding and multi-vesicular body biogenesis. However, how ESCRT-III polymerization generates membrane curvature remains debated. Here, we show that Snf7, the main component of ESCRT-III, polymerizes into spirals at the surface of lipid bilayers. When covering the entire membrane surface, these spirals stopped growing when densely packed: they had a polygonal shape, suggesting that lateral compression could deform them. We reasoned that Snf7 spirals could function as spiral springs. By measuring the polymerization energy and the rigidity of Snf7 filaments, we showed that they were deformed while growing in a confined area. Furthermore, we observed that the elastic expansion of compressed Snf7 spirals generated an area difference between the two sides of the membrane and thus curvature. This spring-like activity underlies the driving force by which ESCRT-III could mediate membrane deformation and fission.

MeSH Terms
Endosomal Sorting Complexes Required for Transport/chemistry,ultrastructure Intracellular Membranes/chemistry Lipid Bilayers/chemistry Models, Molecular Virus Release Yeasts/cytology,metabolism
Chemicals
Endosomal Sorting Complexes Required for Transport Lipid Bilayers
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Chiaruttini Nicolas
University of Geneva, Department of Biochemistry, quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland.
Redondo-Morata Lorena
U1006 INSERM, Aix-Marseille Université, Parc Scientifique et Technologique de Luminy, 163 avenue de Luminy, 13009 Marseille, France.
Colom Adai
University of Geneva, Department of Biochemistry, quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland; Swiss National Centre for Competence in Research Programme Chemical Biology, 1211 Geneva, Switzerland; U1006 INSERM, Aix-Marseille Université, Parc Scientifique et Technologique de Luminy, 163 avenue de Luminy, 13009 Marseille, France.
Humbert Frédéric
University of Geneva, Department of Biochemistry, quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland.
Lenz Martin
LPTMS,CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91405 Orsay, France.
Scheuring Simon
U1006 INSERM, Aix-Marseille Université, Parc Scientifique et Technologique de Luminy, 163 avenue de Luminy, 13009 Marseille, France. Electronic address: simon.scheuring@inserm.fr.
Roux Aurélien
University of Geneva, Department of Biochemistry, quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland; Swiss National Centre for Competence in Research Programme Chemical Biology, 1211 Geneva, Switzerland. Electronic address: aurelien.roux@unige.ch.
References (34)
34 references, click to expand
  1. Structure of the ESCRT-II endosomal trafficking complex.
    Nature. 2004 Sep 9;431(7005):221-5 PMID: 15329733
  2. The protein network of HIV budding.
    Cell. 2003 Sep 19;114(6):701-13 PMID: 14505570
  3. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release.
    Proc Natl Acad Sci U S A. 2008 Jul 29;105(30):10541-6 PMID: 18641129
  4. Coalescence of membrane tethers: experiments, theory, and applications.
    Biophys J. 2005 Apr;88(4):2714-26 PMID: 15695629
  5. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments.
    J Cell Biol. 2008 Jan 28;180(2):389-402 PMID: 18209100
  6. Helical structures of ESCRT-III are disassembled by VPS4.
    Science. 2008 Sep 5;321(5894):1354-7 PMID: 18687924
  7. Functional reconstitution of ESCRT-III assembly and disassembly.
    Cell. 2009 Jan 9;136(1):97-109 PMID: 19135892
  8. Membrane scission by the ESCRT-III complex.
    Nature. 2009 Mar 12;458(7235):172-7 PMID: 19234443
  9. Bursting of sensitive polymersomes induced by curling.
    Proc Natl Acad Sci U S A. 2009 May 5;106(18):7294-8 PMID: 19383800
  10. A crescent-shaped ALIX dimer targets ESCRT-III CHMP4 filaments.
    Structure. 2009 Jun 10;17(6):843-56 PMID: 19523902
  11. Membrane buckling induced by curved filaments.
    Phys Rev Lett. 2009 Jul 17;103(3):038101 PMID: 19659322
  12. Computational model of membrane fission catalyzed by ESCRT-III.
    PLoS Comput Biol. 2009 Nov;5(11):e1000575 PMID: 19936052
  13. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes.
    Nature. 2010 Apr 8;464(7290):864-9 PMID: 20305637
  14. The yeast vps class E mutants: the beginning of the molecular genetic analysis of multivesicular body biogenesis.
    Mol Biol Cell. 2010 Dec;21(23):4057-60 PMID: 21115849
  15. Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission.
    Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):4846-51 PMID: 21383202
  16. Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments.
    Science. 2011 Mar 25;331(6024):1616-20 PMID: 21310966
  17. Membrane bending by protein-protein crowding.
    Nat Cell Biol. 2012 Sep;14(9):944-9 PMID: 22902598
  18. Characterization of the motion of membrane proteins using high-speed atomic force microscopy.
    Nat Nanotechnol. 2012 Aug;7(8):525-9 PMID: 22772862
  19. The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III helices.
    Cell. 2012 Oct 12;151(2):356-71 PMID: 23063125
  20. Membrane shape at the edge of the dynamin helix sets location and duration of the fission reaction.
    Cell. 2012 Oct 26;151(3):619-29 PMID: 23101629
  21. Red blood cell membrane dynamics during malaria parasite egress.
    Biophys J. 2012 Dec 19;103(12):2475-83 PMID: 23260049
  22. Membrane fission reactions of the mammalian ESCRT pathway.
    Annu Rev Biochem. 2013;82:663-92 PMID: 23527693
  23. Membrane bending: the power of protein imbalance.
    Trends Biochem Sci. 2013 Nov;38(11):576-84 PMID: 24054463
  24. Essential N-terminal insertion motif anchors the ESCRT-III filament during MVB vesicle formation.
    Dev Cell. 2013 Oct 28;27(2):201-14 PMID: 24139821
  25. ALIX and the multivesicular endosome: ALIX in Wonderland.
    Trends Cell Biol. 2014 Jan;24(1):19-25 PMID: 24287454
  26. ESCRT machinery is required for plasma membrane repair.
    Science. 2014 Feb 28;343(6174):1247136 PMID: 24482116
  27. Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation.
    J Cell Biol. 2014 Apr 14;205(1):33-49 PMID: 24711499
  28. A dynamin mutant defines a superconstricted prefission state.
    Cell Rep. 2014 Aug 7;8(3):734-42 PMID: 25088425
  29. Structural analysis and modeling reveals new mechanisms governing ESCRT-III spiral filament assembly.
    J Cell Biol. 2014 Sep 15;206(6):763-77 PMID: 25202029
  30. Structure of cellular ESCRT-III spirals and their relationship to HIV budding.
    Elife. 2014;3. doi: 10.7554/eLife.02184 PMID: 24878737
  31. Constitutively active ESCRT-II suppresses the MVB-sorting phenotype of ESCRT-0 and ESCRT-I mutants.
    Mol Biol Cell. 2015 Feb 1;26(3):554-68 PMID: 25501366
  32. A balance between membrane elasticity and polymerization energy sets the shape of spherical clathrin coats.
    Nat Commun. 2015;6:6249 PMID: 25695735
  33. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting.
    Dev Cell. 2002 Aug;3(2):271-82 PMID: 12194857
  34. Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM. Atomic force microscopy.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1690-3 PMID: 12574504
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
Published
2015-11-05
Epub
2015-00-29
Pages
866-79
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC4644223
Subset
IM
Corrections
CommentIn
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