IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29850-z.html
   My bibliography  Save this article

Snf7 spirals sense and alter membrane curvature

Author

Listed:
  • Nebojsa Jukic

    (Physiology, Biophysics and Systems Biology Graduate Program, Weill Cornell Medicine)

  • Alma P. Perrino

    (Weill Cornell Medicine)

  • Frédéric Humbert

    (University of Geneva)

  • Aurélien Roux

    (University of Geneva
    Swiss National Centre for Competence in Research Programme Chemical Biology)

  • Simon Scheuring

    (Weill Cornell Medicine
    Weill Cornell Medicine
    Cornell University, Ithaca)

Abstract

Endosomal Sorting Complex Required for Transport III (ESCRT-III) is a conserved protein system involved in many cellular processes resulting in membrane deformation and scission, topologically away from the cytoplasm. However, little is known about the transition of the planar membrane-associated protein assembly into a 3D structure. High-speed atomic force microscopy (HS-AFM) provided insights into assembly, structural dynamics and turnover of Snf7, the major ESCRT-III component, on planar supported lipid bilayers. Here, we develop HS-AFM experiments that remove the constraints of membrane planarity, crowdedness, and support rigidity. On non-planar membranes, Snf7 monomers are curvature insensitive, but Snf7-spirals selectively adapt their conformation to membrane geometry. In a non-crowded system, Snf7-spirals reach a critical radius, and remodel to minimize internal stress. On non-rigid supports, Snf7-spirals compact and buckle, deforming the underlying bilayer. These experiments provide direct evidence that Snf7 is sufficient to mediate topological transitions, in agreement with the loaded spiral spring model.

Suggested Citation

  • Nebojsa Jukic & Alma P. Perrino & Frédéric Humbert & Aurélien Roux & Simon Scheuring, 2022. "Snf7 spirals sense and alter membrane curvature," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29850-z
    DOI: 10.1038/s41467-022-29850-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29850-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-29850-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Thomas Wollert & James H. Hurley, 2010. "Molecular mechanism of multivesicular body biogenesis by ESCRT complexes," Nature, Nature, vol. 464(7290), pages 864-869, April.
    2. Aitor Hierro & Ji Sun & Alexander S. Rusnak & Jaewon Kim & Gali Prag & Scott D. Emr & James H. Hurley, 2004. "Structure of the ESCRT-II endosomal trafficking complex," Nature, Nature, vol. 431(7005), pages 221-225, September.
    3. Aurélie Bertin & Nicola Franceschi & Eugenio Mora & Sourav Maity & Maryam Alqabandi & Nolwen Miguet & Aurélie Cicco & Wouter H. Roos & Stéphanie Mangenot & Winfried Weissenhorn & Patricia Bassereau, 2020. "Human ESCRT-III polymers assemble on positively curved membranes and induce helical membrane tube formation," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    4. Sina Ghaemmaghami & Won-Ki Huh & Kiowa Bower & Russell W. Howson & Archana Belle & Noah Dephoure & Erin K. O'Shea & Jonathan S. Weissman, 2003. "Global analysis of protein expression in yeast," Nature, Nature, vol. 425(6959), pages 737-741, October.
    5. Tobias Baumgart & Samuel T. Hess & Watt W. Webb, 2003. "Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension," Nature, Nature, vol. 425(6960), pages 821-824, October.
    6. Thomas Wollert & Christian Wunder & Jennifer Lippincott-Schwartz & James H. Hurley, 2009. "Membrane scission by the ESCRT-III complex," Nature, Nature, vol. 458(7235), pages 172-177, March.
    7. Aurélie Bertin & Nicola Franceschi & Eugenio Mora & Sourav Maity & Maryam Alqabandi & Nolwen Miguet & Aurélie Cicco & Wouter H. Roos & Stéphanie Mangenot & Winfried Weissenhorn & Patricia Bassereau, 2020. "Author Correction: Human ESCRT-III polymers assemble on positively curved membranes and induce helical membrane tube formation," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    8. Joachim Moser von Filseck & Luca Barberi & Nathaniel Talledge & Isabel E. Johnson & Adam Frost & Martin Lenz & Aurélien Roux, 2020. "Anisotropic ESCRT-III architecture governs helical membrane tube formation," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    9. Won-Ki Huh & James V. Falvo & Luke C. Gerke & Adam S. Carroll & Russell W. Howson & Jonathan S. Weissman & Erin K. O'Shea, 2003. "Global analysis of protein localization in budding yeast," Nature, Nature, vol. 425(6959), pages 686-691, October.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Joke J F A van Vugt & Martijn de Jager & Magdalena Murawska & Alexander Brehm & John van Noort & Colin Logie, 2009. "Multiple Aspects of ATP-Dependent Nucleosome Translocation by RSC and Mi-2 Are Directed by the Underlying DNA Sequence," PLOS ONE, Public Library of Science, vol. 4(7), pages 1-14, July.
    2. B. Vijayalakshmi Ayyar & Khalil Ettayebi & Wilhelm Salmen & Umesh C. Karandikar & Frederick H. Neill & Victoria R. Tenge & Sue E. Crawford & Erhard Bieberich & B. V. Venkataram Prasad & Robert L. Atma, 2023. "CLIC and membrane wound repair pathways enable pandemic norovirus entry and infection," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Louis-François Handfield & Yolanda T Chong & Jibril Simmons & Brenda J Andrews & Alan M Moses, 2013. "Unsupervised Clustering of Subcellular Protein Expression Patterns in High-Throughput Microscopy Images Reveals Protein Complexes and Functional Relationships between Proteins," PLOS Computational Biology, Public Library of Science, vol. 9(6), pages 1-19, June.
    4. Anneke Brümmer & Carlos Salazar & Vittoria Zinzalla & Lilia Alberghina & Thomas Höfer, 2010. "Mathematical Modelling of DNA Replication Reveals a Trade-off between Coherence of Origin Activation and Robustness against Rereplication," PLOS Computational Biology, Public Library of Science, vol. 6(5), pages 1-13, May.
    5. Emma Pierson & the GTEx Consortium & Daphne Koller & Alexis Battle & Sara Mostafavi, 2015. "Sharing and Specificity of Co-expression Networks across 35 Human Tissues," PLOS Computational Biology, Public Library of Science, vol. 11(5), pages 1-19, May.
    6. Maya Dinur-Mills & Merav Tal & Ophry Pines, 2008. "Dual Targeted Mitochondrial Proteins Are Characterized by Lower MTS Parameters and Total Net Charge," PLOS ONE, Public Library of Science, vol. 3(5), pages 1-8, May.
    7. Zhdanov, Vladimir P., 2011. "Periodic perturbation of the bistable kinetics of gene expression," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 390(1), pages 57-64.
    8. Shinsuke Ohnuki & Yoshikazu Ohya, 2018. "High-dimensional single-cell phenotyping reveals extensive haploinsufficiency," PLOS Biology, Public Library of Science, vol. 16(5), pages 1-23, May.
    9. Verena Kohler & Andreas Kohler & Lisa Larsson Berglund & Xinxin Hao & Sarah Gersing & Axel Imhof & Thomas Nyström & Johanna L. Höög & Martin Ott & Claes Andréasson & Sabrina Büttner, 2024. "Nuclear Hsp104 safeguards the dormant translation machinery during quiescence," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    10. Brian J. Caldwell & Andrew S. Norris & Caroline F. Karbowski & Alyssa M. Wiegand & Vicki H. Wysocki & Charles E. Bell, 2022. "Structure of a RecT/Redβ family recombinase in complex with a duplex intermediate of DNA annealing," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Jian Cui & Jinghua Liu & Yuhua Li & Tieliu Shi, 2011. "Integrative Identification of Arabidopsis Mitochondrial Proteome and Its Function Exploitation through Protein Interaction Network," PLOS ONE, Public Library of Science, vol. 6(1), pages 1-16, January.
    12. Xiaomei Wu & Erli Pang & Kui Lin & Zhen-Ming Pei, 2013. "Improving the Measurement of Semantic Similarity between Gene Ontology Terms and Gene Products: Insights from an Edge- and IC-Based Hybrid Method," PLOS ONE, Public Library of Science, vol. 8(5), pages 1-11, May.
    13. Marc S Sherman & Barak A Cohen, 2014. "A Computational Framework for Analyzing Stochasticity in Gene Expression," PLOS Computational Biology, Public Library of Science, vol. 10(5), pages 1-13, May.
    14. Kiyan Shabestary & Cinzia Klemm & Benedict Carling & James Marshall & Juline Savigny & Marko Storch & Rodrigo Ledesma-Amaro, 2024. "Phenotypic heterogeneity follows a growth-viability tradeoff in response to amino acid identity," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Jason W Locasale & Arup K Chakraborty, 2008. "Regulation of Signal Duration and the Statistical Dynamics of Kinase Activation by Scaffold Proteins," PLOS Computational Biology, Public Library of Science, vol. 4(6), pages 1-12, June.
    16. Michelle Lindström & Lihua Chen & Shan Jiang & Dan Zhang & Yuan Gao & Ju Zheng & Xinxin Hao & Xiaoxue Yang & Arpitha Kabbinale & Johannes Thoma & Lisa C. Metzger & Deyuan Y. Zhang & Xuefeng Zhu & Huis, 2022. "Lsm7 phase-separated condensates trigger stress granule formation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    17. Alex N Nguyen Ba & Bob Strome & Jun Jie Hua & Jonathan Desmond & Isabelle Gagnon-Arsenault & Eric L Weiss & Christian R Landry & Alan M Moses, 2014. "Detecting Functional Divergence after Gene Duplication through Evolutionary Changes in Posttranslational Regulatory Sequences," PLOS Computational Biology, Public Library of Science, vol. 10(12), pages 1-15, December.
    18. Morgane Boone & Pathmanaban Ramasamy & Jasper Zuallaert & Robbin Bouwmeester & Berre Moer & Davy Maddelein & Demet Turan & Niels Hulstaert & Hannah Eeckhaut & Elien Vandermarliere & Lennart Martens & , 2021. "Massively parallel interrogation of protein fragment secretability using SECRiFY reveals features influencing secretory system transit," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    19. Rower, David A. & Atzberger, Paul J., 2023. "Coarse-grained methods for heterogeneous vesicles with phase-separated domains: Elastic mechanics of shape fluctuations, plate compression, and channel insertion," Mathematics and Computers in Simulation (MATCOM), Elsevier, vol. 209(C), pages 342-361.
    20. Yosuke Ito & Yuhei Chadani & Tatsuya Niwa & Ayako Yamakawa & Kodai Machida & Hiroaki Imataka & Hideki Taguchi, 2022. "Nascent peptide-induced translation discontinuation in eukaryotes impacts biased amino acid usage in proteomes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29850-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.