Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows
Abstract
Mitochondrial ATP synthases form dimers, which assemble into long ribbons at the rims of the inner membrane cristae. We reconstituted detergent-purified mitochondrial ATP synthase dimers from the green algae Polytomella sp. and the yeast Yarrowia lipolytica into liposomes and examined them by electron cryotomography. Tomographic volumes revealed that ATP synthase dimers from both species self-assemble into rows and bend the lipid bilayer locally. The dimer rows and the induced degree of membrane curvature closely resemble those in the inner membrane cristae. Monomers of mitochondrial ATP synthase reconstituted into liposomes do not bend membrane visibly and do not form rows. No specific lipids or proteins other than ATP synthase dimers are required for row formation and membrane remodelling. Long rows of ATP synthase dimers are a conserved feature of mitochondrial inner membranes. They are required for cristae formation and a main factor in mitochondrial morphogenesis.
- Authors:
-
- Max Planck Institute of Biophysics, Frankfurt (Germany)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1559185
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 116; Journal Issue: 10; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences, Washington, DC (United States)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; mitochondria; ATP synthase; membrane curvature; electron cryotomography; subtomogram averaging
Citation Formats
Blum, Thorsten B., Hahn, Alexander, Meier, Thomas, Davies, Karen M., and Kühlbrandt, Werner. Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows. United States: N. p., 2019.
Web. doi:10.1073/pnas.1816556116.
Blum, Thorsten B., Hahn, Alexander, Meier, Thomas, Davies, Karen M., & Kühlbrandt, Werner. Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows. United States. https://doi.org/10.1073/pnas.1816556116
Blum, Thorsten B., Hahn, Alexander, Meier, Thomas, Davies, Karen M., and Kühlbrandt, Werner. Wed .
"Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows". United States. https://doi.org/10.1073/pnas.1816556116. https://www.osti.gov/servlets/purl/1559185.
@article{osti_1559185,
title = {Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows},
author = {Blum, Thorsten B. and Hahn, Alexander and Meier, Thomas and Davies, Karen M. and Kühlbrandt, Werner},
abstractNote = {Mitochondrial ATP synthases form dimers, which assemble into long ribbons at the rims of the inner membrane cristae. We reconstituted detergent-purified mitochondrial ATP synthase dimers from the green algae Polytomella sp. and the yeast Yarrowia lipolytica into liposomes and examined them by electron cryotomography. Tomographic volumes revealed that ATP synthase dimers from both species self-assemble into rows and bend the lipid bilayer locally. The dimer rows and the induced degree of membrane curvature closely resemble those in the inner membrane cristae. Monomers of mitochondrial ATP synthase reconstituted into liposomes do not bend membrane visibly and do not form rows. No specific lipids or proteins other than ATP synthase dimers are required for row formation and membrane remodelling. Long rows of ATP synthase dimers are a conserved feature of mitochondrial inner membranes. They are required for cristae formation and a main factor in mitochondrial morphogenesis.},
doi = {10.1073/pnas.1816556116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 10,
volume = 116,
place = {United States},
year = {2019},
month = {2}
}
Web of Science
Works referenced in this record:
High-resolution cryo-EM analysis of the yeast ATP synthase in a lipid membrane
journal, April 2018
- Srivastava, Anurag P.; Luo, Min; Zhou, Wenchang
- Science, Vol. 360, Issue 6389
A visualization and segmentation toolbox for electron microscopy
journal, October 2008
- Pruggnaller, Sabine; Mayr, Matthias; Frangakis, Achilleas S.
- Journal of Structural Biology, Vol. 164, Issue 1
Polytomella spp. growth on ethananol: Extracellular pH affects the accumulation of mitochondrial cytochrome c550
journal, May 2000
- Atteia, Ariane; van Lis, Robert; Ramírez, Jorge
- European Journal of Biochemistry, Vol. 267, Issue 10
Membrane tubulation and proton pumps
journal, March 1995
- Allen, R. D.
- Protoplasma, Vol. 189, Issue 1-2
Structure and Mechanisms of F-Type ATP Synthases
journal, June 2019
- Kühlbrandt, Werner
- Annual Review of Biochemistry, Vol. 88, Issue 1
The Modulation in Subunits e and g Amounts of Yeast ATP Synthase Modifies Mitochondrial Cristae Morphology
journal, July 2004
- Arselin, Geneviève; Vaillier, Jacques; Salin, Bénédicte
- Journal of Biological Chemistry, Vol. 279, Issue 39
Visualization of ATP Synthase Dimers in Mitochondria by Electron Cryo-tomography
journal, January 2014
- Davies, Karen M.; Daum, Bertram; Gold, Vicki A. M.
- Journal of Visualized Experiments, Issue 91
Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase
journal, February 2015
- Allegretti, Matteo; Klusch, Niklas; Mills, Deryck J.
- Nature, Vol. 521, Issue 7551
Helical arrays of U-shaped ATP synthase dimers form tubular cristae in ciliate mitochondria
journal, July 2016
- Mühleip, Alexander W.; Joos, Friederike; Wigge, Christoph
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 30
Lateral pH gradient between OXPHOS complex IV and F0F1 ATP-synthase in folded mitochondrial membranes
journal, January 2014
- Rieger, Bettina; Junge, Wolfgang; Busch, Karin B.
- Nature Communications, Vol. 5, Issue 1
Mitochondrial ATP synthase dimers spontaneously associate due to a long-range membrane-induced force
journal, April 2018
- Anselmi, Claudio; Davies, Karen M.; Faraldo-Gómez, José D.
- The Journal of General Physiology, Vol. 150, Issue 5
Atomic model for the dimeric F O region of mitochondrial ATP synthase
journal, October 2017
- Guo, Hui; Bueler, Stephanie A.; Rubinstein, John L.
- Science, Vol. 358, Issue 6365
A thermodynamic model describing the nature of the crista junction: a structural motif in the mitochondrion
journal, April 2002
- Renken, Christian; Siragusa, Gino; Perkins, Guy
- Journal of Structural Biology, Vol. 138, Issue 1-2
In situ structure of trypanosomal ATP synthase dimer reveals a unique arrangement of catalytic subunits
journal, January 2017
- Mühleip, Alexander W.; Dewar, Caroline E.; Schnaufer, Achim
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 5
Structure of dimeric mitochondrial ATP synthase: Novel F0 bridging features and the structural basis of mitochondrial cristae biogenesis
journal, August 2005
- Minauro-Sanmiguel, F.; Wilkens, S.; Garcia, J. J.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 35
Structural basis of proton translocation and force generation in mitochondrial ATP synthase
journal, December 2017
- Klusch, Niklas; Murphy, Bonnie J.; Mills, Deryck J.
- eLife, Vol. 6
Dimer ribbons of ATP synthase shape the inner mitochondrial membrane
journal, March 2008
- Strauss, Mike; Hofhaus, Götz; Schröder, Rasmus R.
- The EMBO Journal, Vol. 27, Issue 7
Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae
journal, August 2012
- Davies, K. M.; Anselmi, C.; Wittig, I.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 34
Structure of a Complete ATP Synthase Dimer Reveals the Molecular Basis of Inner Mitochondrial Membrane Morphology
journal, August 2016
- Hahn, Alexander; Parey, Kristian; Bublitz, Maike
- Molecular Cell, Vol. 63, Issue 3
Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM
journal, July 2012
- Baker, L. A.; Watt, I. N.; Runswick, M. J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 29
The ATP synthase is involved in generating mitochondrial cristae morphology
journal, February 2002
- Paumard, Patrick; Vaillier, Jacques; Coulary, Bénédicte
- The EMBO Journal, Vol. 21, Issue 3
Macromolecular organization of ATP synthase and complex I in whole mitochondria
journal, August 2011
- Davies, K. M.; Strauss, M.; Daum, B.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 34
Row-like organization of ATP synthase in intact mitochondria determined by cryo-electron tomography
journal, February 2010
- Dudkina, Natalya V.; Oostergetel, Gert T.; Lewejohann, Dagmar
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 2
Structure of Dimeric F 1 F 0 -ATP Synthase
journal, September 2010
- Couoh-Cardel, Sergio J.; Uribe-Carvajal, Salvador; Wilkens, Stephan
- Journal of Biological Chemistry, Vol. 285, Issue 47
ATP Synthase of Yeast Mitochondria: ISOLATION OF SUBUNIT j AND DISRUPTION OF THE
journal, January 1999
- Arnold, Isabel; Pfeiffer, Kathy; Neupert, Walter
- Journal of Biological Chemistry, Vol. 274, Issue 1
Structure of dimeric ATP synthase from mitochondria: An angular association of monomers induces the strong curvature of the inner membrane
journal, October 2005
- Dudkina, Natalya V.; Heinemeyer, Jesco; Keegstra, Wilko
- FEBS Letters, Vol. 579, Issue 25
Supramolecular organization of the yeast F1Fo-ATP synthase
journal, October 2008
- Thomas, Daniel; Bron, Patrick; Weimann, Théodore
- Biology of the Cell, Vol. 100, Issue 10
Bovine F1Fo ATP synthase monomers bend the lipid bilayer in 2D membrane crystals
journal, March 2015
- Jiko, Chimari; Davies, Karen M.; Shinzawa-Itoh, Kyoko
- eLife, Vol. 4
Changes of mitochondrial ultrastructure and function during ageing in mice and Drosophila
journal, July 2017
- Brandt, Tobias; Mourier, Arnaud; Tain, Luke S.
- eLife, Vol. 6
GRecon: A Method for the Lipid Reconstitution of Membrane Proteins
journal, July 2012
- Althoff, Thorsten; Davies, Karen M.; Schulze, Sabrina
- Angewandte Chemie International Edition, Vol. 51, Issue 33
Atypical Subunit Composition of the Chlorophycean Mitochondrial F1FO-ATP Synthase and Role of Asa7 Protein in Stability and Oligomycin Resistance of the Enzyme
journal, February 2010
- Lapaille, M.; Escobar-Ramirez, A.; Degand, H.
- Molecular Biology and Evolution, Vol. 27, Issue 7
Computer Visualization of Three-Dimensional Image Data Using IMOD
journal, January 1996
- Kremer, James R.; Mastronarde, David N.; McIntosh, J. Richard
- Journal of Structural Biology, Vol. 116, Issue 1
Characterization of dimeric ATP synthase and cristae membrane ultrastructure from Saccharomyces and Polytomella mitochondria
journal, May 2006
- Dudkina, Natalya V.; Sunderhaus, Stephanie; Braun, Hans-Peter
- FEBS Letters, Vol. 580, Issue 14
Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits
journal, December 1998
- Arnold, I.
- The EMBO Journal, Vol. 17, Issue 24
The mitochondrial ATP synthase of chlorophycean algae contains eight subunits of unknown origin involved in the formation of an atypical stator-stalk and in the dimerization of the complex
journal, December 2006
- Vázquez-Acevedo, Miriam; Cardol, Pierre; Cano-Estrada, Araceli
- Journal of Bioenergetics and Biomembranes, Vol. 38, Issue 5-6
Morphogenesis of membrane invaginations in spherical confinement
journal, March 2012
- Kahraman, O.; Stoop, N.; Müller, M. M.
- EPL (Europhysics Letters), Vol. 97, Issue 6
GRecon: A Method for the Lipid Reconstitution of Membrane Proteins
journal, July 2012
- Althoff, Thorsten; Davies, Karen M.; Schulze, Sabrina
- Angewandte Chemie, Vol. 124, Issue 33
Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules.
text, January 2019
- Roth, Ronelle; Hillmer, Stefan; Funaya, Charlotta
- Apollo - University of Cambridge Repository
Morphogenesis of membrane invaginations in spherical confinement
text, January 2012
- Kahraman, Osman; Stoop, Norbert; Mueller, Martin Michael
- arXiv
Works referencing / citing this record:
Purified F-ATP synthase forms a Ca2+-dependent high-conductance channel matching the mitochondrial permeability transition pore
journal, September 2019
- Urbani, Andrea; Giorgio, Valentina; Carrer, Andrea
- Nature Communications, Vol. 10, Issue 1
A mitochondrial megachannel resides in monomeric F1FO ATP synthase
journal, December 2019
- Mnatsakanyan, Nelli; Llaguno, Marc C.; Yang, Youshan
- Nature Communications, Vol. 10, Issue 1
Structural insights into tetraspanin CD9 function
journal, March 2020
- Umeda, Rie; Satouh, Yuhkoh; Takemoto, Mizuki
- Nature Communications, Vol. 11, Issue 1
Live-cell STED nanoscopy of mitochondrial cristae
journal, August 2019
- Stephan, Till; Roesch, Axel; Riedel, Dietmar
- Scientific Reports, Vol. 9, Issue 1
Kinetic coupling of the respiratory chain with ATP synthase, but not proton gradients, drives ATP production in cristae membranes
journal, January 2020
- Toth, Alexandra; Meyrat, Axel; Stoldt, Stefan
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 5
Single organelle function and organization as estimated from Arabidopsis mitochondrial proteomics
journal, November 2019
- Fuchs, Philippe; Rugen, Nils; Carrie, Chris
- The Plant Journal, Vol. 101, Issue 2
Cryo-EM structure of the mammalian ATP synthase tetramer bound with inhibitory protein IF1
journal, June 2019
- Gu, Jinke; Zhang, Laixing; Zong, Shuai
- Science, Vol. 364, Issue 6445
Response to Comment on “Protein assemblies ejected directly from native membranes yield complexes for mass spectrometry”
journal, November 2019
- Chorev, Dror S.; Robinson, Carol V.
- Science, Vol. 366, Issue 6466
Functional Interplay between Cristae Biogenesis, Mitochondrial Dynamics and Mitochondrial DNA Integrity
journal, September 2019
- Kondadi, Arun Kumar; Anand, Ruchika; Reichert, Andreas S.
- International Journal of Molecular Sciences, Vol. 20, Issue 17
The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015
- Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
- Nature Protocols, Vol. 10, Issue 6
Kinetic coupling of the respiratory chain with ATP synthase, but not proton gradients, drives ATP production in cristae membranes.
text, January 2020
- Toth, Alexandra; Meyrat, Axel; Stoldt, Stefan
- National Academy of Sciences NAS
Single organelle function and organization as estimated from Arabidopsis mitochondrial proteomics
other, January 2020
- Fuchs, Philippe; Rugen, Nils; Carrie, Chris
- Oxford [u.a.] : Wiley-Blackwell