Human ESCRT-III polymers assemble on positively curved membranes and induce helical membrane tube formation

被引:75
作者
Bertin, Aurelie [1 ,2 ]
de Franceschi, Nicola [1 ,2 ,3 ]
de la Mora, Eugenio [1 ,2 ]
Maity, Sourav [4 ]
Alqabandi, Maryam [1 ,2 ]
Miguet, Nolwen [3 ]
di Cicco, Aurelie [1 ,2 ]
Roos, Wouter H. [4 ]
Mangenot, Stephanie [1 ,2 ]
Weissenhorn, Winfried [3 ]
Bassereau, Patricia [1 ,2 ]
机构
[1] PSL Res Univ, Inst Curie, Lab Phys Chim Curie, CNRS,UMR168, F-75005 Paris, France
[2] Sorbonne Univ, F-75005 Paris, France
[3] Univ Grenoble Alpes, Inst Biol Struct IBS, CNRS, CEA, 71 Ave Martyrs, F-38000 Grenoble, France
[4] Univ Groningen, Zernike Inst, Mol Biofys, Nijenborgh 4, NL-9747 AG Groningen, Netherlands
基金
欧盟地平线“2020”;
关键词
STRUCTURAL BASIS; COMPLEX; MACHINERY; FILAMENTS; SUBUNIT; REVEALS; ASSOCIATION; SCISSION; DYNAMO; CARGO;
D O I
10.1038/s41467-020-16368-5
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Endosomal sorting complexes for transport-III (ESCRT-III) assemble in vivo onto membranes with negative Gaussian curvature. How membrane shape influences ESCRT-III polymerization and how ESCRT-III shapes membranes is yet unclear. Human core ESCRT-III proteins, CHMP4B, CHMP2A, CHMP2B and CHMP3 are used to address this issue in vitro by combining membrane nanotube pulling experiments, cryo-electron tomography and AFM. We show that CHMP4B filaments preferentially bind to flat membranes or to tubes with positive mean curvature. Both CHMP2B and CHMP2A/CHMP3 assemble on positively curved membrane tubes. Combinations of CHMP4B/CHMP2B and CHMP4B/CHMP2A/CHMP3 are recruited to the neck of pulled membrane tubes and reshape vesicles into helical "corkscrew-like" membrane tubes. Sub-tomogram averaging reveals that the ESCRT-III filaments assemble parallel and locally perpendicular to the tube axis, highlighting the mechanical stresses imposed by ESCRT-III. Our results underline the versatile membrane remodeling activity of ESCRT-III that may be a general feature required for cellular membrane remodeling processes.
引用
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页数:13
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共 66 条
  • [1] An ESCRT-spastin interaction promotes fission of recycling tubules from the endosome
    Allison, Rachel
    Lumb, Jennifer H.
    Fassier, Coralie
    Connell, James W.
    Ten Martin, Daniel
    Seaman, Matthew N. J.
    Hazan, Jamile
    Reid, Evan
    [J]. JOURNAL OF CELL BIOLOGY, 2013, 202 (03) : 527 - 543
  • [2] Recruitment dynamics of ESCRT-III and Vps4 to endosomes and implications for reverse membrane budding
    Alonso Y Adell, Manuel
    Migliano, Simona M.
    Upadhyayula, Srigokul
    Bykov, Yury S.
    Sprenger, Simon
    Pakdel, Mehrshad
    Vogel, Georg F.
    Jih, Gloria
    Skillern, Wesley
    Behrouzi, Reza
    Babst, Markus
    Schmidt, Oliver
    Hess, Michael W.
    Briggs, John A. G.
    Kirchhausen, Tomas
    Teis, David
    [J]. ELIFE, 2017, 6
  • [3] Alqabandi M., 2019, PREPRINT, DOI [10.1101/756403v1, DOI 10.1101/756403V1]
  • [4] The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function
    Babst, M
    Wendland, B
    Estepa, EJ
    Emr, SD
    [J]. EMBO JOURNAL, 1998, 17 (11) : 2982 - 2993
  • [5] Structural basis for ESCRT-III protein autoinhibition
    Bajorek, Monika
    Schubert, Heidi L.
    McCullough, John
    Langelier, Charles
    Eckert, Debra M.
    Stubblefield, William-May B.
    Uter, Nathan T.
    Myszka, David G.
    Hill, Christopher P.
    Sundquist, Wesley I.
    [J]. NATURE STRUCTURAL & MOLECULAR BIOLOGY, 2009, 16 (07) : 754 - U95
  • [6] Electrostatic lateral interactions drive ESCRT-III heteropolymer assembly
    Banjade, Sudeep
    Tang, Shaogeng
    Shah, Yousuf H.
    Emr, Scott D.
    [J]. ELIFE, 2019, 8
  • [7] Septin-based readout of PI(4,5)P2 incorporation into membranes of giant unilamellar vesicles
    Beber, Alexandre
    Alqabandi, Maryam
    Prevost, Coline
    Viars, Fanny
    Levy, Daniel
    Bassereau, Patricia
    Bertin, Aurelie
    Mangenot, Stephanie
    [J]. CYTOSKELETON, 2019, 76 (01) : 92 - 103
  • [8] Charged Multivesicular Body Protein 2B (CHMP2B) of the Endosomal Sorting Complex Required for Transport-III (ESCRT-III) Polymerizes into Helical Structures Deforming the Plasma Membrane
    Bodon, Gilles
    Chassefeyre, Romain
    Pernet-Gallay, Karin
    Martinelli, Nicolas
    Effantin, Gregory
    Hulsik, David Lutje
    Belly, Agnes
    Goldberg, Yves
    Chatellard-Causse, Christine
    Blot, Beatrice
    Schoehn, Guy
    Weissenhorn, Winfried
    Sadoul, Remy
    [J]. JOURNAL OF BIOLOGICAL CHEMISTRY, 2011, 286 (46) : 40276 - 40286
  • [9] ESCRT Filaments as Spiral Springs
    Carlson, Lars-Anders
    Shen, Qing-Tao
    Pavlin, Mark Remec
    Hurley, James H.
    [J]. DEVELOPMENTAL CELL, 2015, 35 (04) : 397 - 398
  • [10] Structure of cellular ESCRT-III spirals and their relationship to HIV budding
    Cashikar, Anil G.
    Shim, Soomin
    Roth, Robyn
    Maldazys, Michael R.
    Heuser, John E.
    Hanson, Phyllis I.
    [J]. ELIFE, 2014, 3