Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows

Blum, Thorsten B.; Hahn, Alexander; Meier, Thomas; Davies, Karen M.; Kühlbrandt, Werner

doi:10.1073/pnas.1816556116

Title: Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows

Journal Article · Wed Feb 13 00:00:00 EST 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1816556116· OSTI ID:1559185

Blum, Thorsten B. ^[1]; Hahn, Alexander ^[1];

^[1]; Davies, Karen M. ^[1];

^[1]

Max Planck Institute of Biophysics, Frankfurt (Germany)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1559185

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, Issue 10; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 119 works

Citation information provided by
Web of Science

References (40)

High-resolution cryo-EM analysis of the yeast ATP synthase in a lipid membrane Srivastava, Anurag P.; Luo, Min; Zhou, Wenchang Science, Vol. 360, Issue 6389 https://doi.org/10.1126/science.aas9699	journal	April 2018
A visualization and segmentation toolbox for electron microscopy Pruggnaller, Sabine; Mayr, Matthias; Frangakis, Achilleas S. Journal of Structural Biology, Vol. 164, Issue 1 https://doi.org/10.1016/j.jsb.2008.05.003	journal	October 2008
Polytomella spp. growth on ethananol: Extracellular pH affects the accumulation of mitochondrial cytochrome c550 Atteia, Ariane; van Lis, Robert; Ramírez, Jorge European Journal of Biochemistry, Vol. 267, Issue 10 https://doi.org/10.1046/j.1432-1327.2000.01288.x	journal	May 2000
Membrane tubulation and proton pumps Allen, R. D. Protoplasma, Vol. 189, Issue 1-2 https://doi.org/10.1007/BF01280286	journal	March 1995
Structure and Mechanisms of F-Type ATP Synthases Kühlbrandt, Werner Annual Review of Biochemistry, Vol. 88, Issue 1 https://doi.org/10.1146/annurev-biochem-013118-110903	journal	June 2019
Visualization of ATP Synthase Dimers in Mitochondria by Electron Cryo-tomography Davies, Karen M.; Daum, Bertram; Gold, Vicki A. M. Journal of Visualized Experiments, Issue 91 https://doi.org/10.3791/51228	journal	January 2014
Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase Allegretti, Matteo; Klusch, Niklas; Mills, Deryck J. Nature, Vol. 521, Issue 7551 https://doi.org/10.1038/nature14185	journal	February 2015
Helical arrays of U-shaped ATP synthase dimers form tubular cristae in ciliate mitochondria Mühleip, Alexander W.; Joos, Friederike; Wigge, Christoph Proceedings of the National Academy of Sciences, Vol. 113, Issue 30 https://doi.org/10.1073/pnas.1525430113	journal	July 2016
Lateral pH gradient between OXPHOS complex IV and F0F1 ATP-synthase in folded mitochondrial membranes Rieger, Bettina; Junge, Wolfgang; Busch, Karin B. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4103	journal	January 2014
Mitochondrial ATP synthase dimers spontaneously associate due to a long-range membrane-induced force Anselmi, Claudio; Davies, Karen M.; Faraldo-Gómez, José D. The Journal of General Physiology, Vol. 150, Issue 5 https://doi.org/10.1085/jgp.201812033	journal	April 2018
Atomic model for the dimeric F _O region of mitochondrial ATP synthase Guo, Hui; Bueler, Stephanie A.; Rubinstein, John L. Science, Vol. 358, Issue 6365 https://doi.org/10.1126/science.aao4815	journal	October 2017
In situ structure of trypanosomal ATP synthase dimer reveals a unique arrangement of catalytic subunits Mühleip, Alexander W.; Dewar, Caroline E.; Schnaufer, Achim Proceedings of the National Academy of Sciences, Vol. 114, Issue 5 https://doi.org/10.1073/pnas.1612386114	journal	January 2017
Structure of dimeric mitochondrial ATP synthase: Novel F0 bridging features and the structural basis of mitochondrial cristae biogenesis Minauro-Sanmiguel, F.; Wilkens, S.; Garcia, J. J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 35 https://doi.org/10.1073/pnas.0503893102	journal	August 2005
Structural basis of proton translocation and force generation in mitochondrial ATP synthase Klusch, Niklas; Murphy, Bonnie J.; Mills, Deryck J. eLife, Vol. 6 https://doi.org/10.7554/eLife.33274	journal	December 2017
Dimer ribbons of ATP synthase shape the inner mitochondrial membrane Strauss, Mike; Hofhaus, Götz; Schröder, Rasmus R. The EMBO Journal, Vol. 27, Issue 7 https://doi.org/10.1038/emboj.2008.35	journal	March 2008
Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae Davies, K. M.; Anselmi, C.; Wittig, I. Proceedings of the National Academy of Sciences, Vol. 109, Issue 34 https://doi.org/10.1073/pnas.1204593109	journal	August 2012
Structure of a Complete ATP Synthase Dimer Reveals the Molecular Basis of Inner Mitochondrial Membrane Morphology Hahn, Alexander; Parey, Kristian; Bublitz, Maike Molecular Cell, Vol. 63, Issue 3 https://doi.org/10.1016/j.molcel.2016.05.037	journal	August 2016
Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM Baker, L. A.; Watt, I. N.; Runswick, M. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 29 https://doi.org/10.1073/pnas.1204935109	journal	July 2012
The ATP synthase is involved in generating mitochondrial cristae morphology Paumard, Patrick; Vaillier, Jacques; Coulary, Bénédicte The EMBO Journal, Vol. 21, Issue 3 https://doi.org/10.1093/emboj/21.3.221	journal	February 2002
Macromolecular organization of ATP synthase and complex I in whole mitochondria Davies, K. M.; Strauss, M.; Daum, B. Proceedings of the National Academy of Sciences, Vol. 108, Issue 34 https://doi.org/10.1073/pnas.1103621108	journal	August 2011
Row-like organization of ATP synthase in intact mitochondria determined by cryo-electron tomography Dudkina, Natalya V.; Oostergetel, Gert T.; Lewejohann, Dagmar Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 2 https://doi.org/10.1016/j.bbabio.2009.11.004	journal	February 2010
ATP Synthase of Yeast Mitochondria: ISOLATION OF SUBUNIT j AND DISRUPTION OF THE Arnold, Isabel; Pfeiffer, Kathy; Neupert, Walter Journal of Biological Chemistry, Vol. 274, Issue 1 https://doi.org/10.1074/jbc.274.1.36	journal	January 1999
Structure of dimeric ATP synthase from mitochondria: An angular association of monomers induces the strong curvature of the inner membrane Dudkina, Natalya V.; Heinemeyer, Jesco; Keegstra, Wilko FEBS Letters, Vol. 579, Issue 25 https://doi.org/10.1016/j.febslet.2005.09.065	journal	October 2005
Changes of mitochondrial ultrastructure and function during ageing in mice and Drosophila Brandt, Tobias; Mourier, Arnaud; Tain, Luke S. eLife, Vol. 6 https://doi.org/10.7554/eLife.24662	journal	July 2017
GRecon: A Method for the Lipid Reconstitution of Membrane Proteins Althoff, Thorsten; Davies, Karen M.; Schulze, Sabrina Angewandte Chemie International Edition, Vol. 51, Issue 33 https://doi.org/10.1002/anie.201202094	journal	July 2012
Atypical Subunit Composition of the Chlorophycean Mitochondrial F1FO-ATP Synthase and Role of Asa7 Protein in Stability and Oligomycin Resistance of the Enzyme Lapaille, M.; Escobar-Ramirez, A.; Degand, H. Molecular Biology and Evolution, Vol. 27, Issue 7 https://doi.org/10.1093/molbev/msq049	journal	February 2010
Computer Visualization of Three-Dimensional Image Data Using IMOD Kremer, James R.; Mastronarde, David N.; McIntosh, J. Richard Journal of Structural Biology, Vol. 116, Issue 1 https://doi.org/10.1006/jsbi.1996.0013	journal	January 1996
Characterization of dimeric ATP synthase and cristae membrane ultrastructure from Saccharomyces and Polytomella mitochondria Dudkina, Natalya V.; Sunderhaus, Stephanie; Braun, Hans-Peter FEBS Letters, Vol. 580, Issue 14 https://doi.org/10.1016/j.febslet.2006.04.097	journal	May 2006
Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits Arnold, I. The EMBO Journal, Vol. 17, Issue 24 https://doi.org/10.1093/emboj/17.24.7170	journal	December 1998
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 Vázquez-Acevedo, Miriam; Cardol, Pierre; Cano-Estrada, Araceli Journal of Bioenergetics and Biomembranes, Vol. 38, Issue 5-6 https://doi.org/10.1007/s10863-006-9046-x	journal	December 2006
Morphogenesis of membrane invaginations in spherical confinement Kahraman, O.; Stoop, N.; Müller, M. M. EPL (Europhysics Letters), Vol. 97, Issue 6 https://doi.org/10.1209/0295-5075/97/68008	journal	March 2012
GRecon: A Method for the Lipid Reconstitution of Membrane Proteins Althoff, Thorsten; Davies, Karen M.; Schulze, Sabrina Angewandte Chemie, Vol. 124, Issue 33 https://doi.org/10.1002/ange.201202094	journal	July 2012
Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. Roth, Ronelle; Hillmer, Stefan; Funaya, Charlotta Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52956	text	January 2019
Morphogenesis of membrane invaginations in spherical confinement Kahraman, Osman; Stoop, Norbert; Mueller, Martin Michael arXiv https://doi.org/10.48550/arxiv.1201.2518	text	January 2012
A thermodynamic model describing the nature of the crista junction: a structural motif in the mitochondrion Renken, Christian; Siragusa, Gino; Perkins, Guy Journal of Structural Biology, Vol. 138, Issue 1-2 https://doi.org/10.1016/s1047-8477(02)00012-6	journal	April 2002
Supramolecular organization of the yeast F1Fo-ATP synthase Thomas, Daniel; Bron, Patrick; Weimann, Théodore Biology of the Cell, Vol. 100, Issue 10 https://doi.org/10.1042/bc20080022	journal	October 2008
Structure of Dimeric F ₁ F ₀ -ATP Synthase Couoh-Cardel, Sergio J.; Uribe-Carvajal, Salvador; Wilkens, Stephan Journal of Biological Chemistry, Vol. 285, Issue 47 https://doi.org/10.1074/jbc.m110.144907	journal	September 2010
The Modulation in Subunits e and g Amounts of Yeast ATP Synthase Modifies Mitochondrial Cristae Morphology Arselin, Geneviève; Vaillier, Jacques; Salin, Bénédicte Journal of Biological Chemistry, Vol. 279, Issue 39 https://doi.org/10.1074/jbc.m404316200	journal	July 2004
Energy powerhouses of cells come into focus Kane, Patricia M. Science, Vol. 360, Issue 6389 https://doi.org/10.1126/science.aat6275	journal	May 2018
Bovine F1Fo ATP synthase monomers bend the lipid bilayer in 2D membrane crystals Jiko, Chimari; Davies, Karen M.; Shinzawa-Itoh, Kyoko eLife, Vol. 4 https://doi.org/10.7554/elife.06119	journal	March 2015

Cited By (17)

Purified F-ATP synthase forms a Ca2+-dependent high-conductance channel matching the mitochondrial permeability transition pore Urbani, Andrea; Giorgio, Valentina; Carrer, Andrea Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12331-1	journal	September 2019
A mitochondrial megachannel resides in monomeric F1FO ATP synthase Mnatsakanyan, Nelli; Llaguno, Marc C.; Yang, Youshan Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13766-2	journal	December 2019
Structural insights into tetraspanin CD9 function Umeda, Rie; Satouh, Yuhkoh; Takemoto, Mizuki Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15459-7	journal	March 2020
Live-cell STED nanoscopy of mitochondrial cristae Stephan, Till; Roesch, Axel; Riedel, Dietmar Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-48838-2	journal	August 2019
Kinetic coupling of the respiratory chain with ATP synthase, but not proton gradients, drives ATP production in cristae membranes Toth, Alexandra; Meyrat, Axel; Stoldt, Stefan Proceedings of the National Academy of Sciences, Vol. 117, Issue 5 https://doi.org/10.1073/pnas.1917968117	journal	January 2020
Single organelle function and organization as estimated from Arabidopsis mitochondrial proteomics Fuchs, Philippe; Rugen, Nils; Carrie, Chris The Plant Journal, Vol. 101, Issue 2 https://doi.org/10.1111/tpj.14534	journal	November 2019
Cryo-EM structure of the mammalian ATP synthase tetramer bound with inhibitory protein IF1 Gu, Jinke; Zhang, Laixing; Zong, Shuai Science, Vol. 364, Issue 6445 https://doi.org/10.1126/science.aaw4852	journal	June 2019
Response to Comment on “Protein assemblies ejected directly from native membranes yield complexes for mass spectrometry” Chorev, Dror S.; Robinson, Carol V. Science, Vol. 366, Issue 6466 https://doi.org/10.1126/science.aax3102	journal	November 2019
Functional Interplay between Cristae Biogenesis, Mitochondrial Dynamics and Mitochondrial DNA Integrity Kondadi, Arun Kumar; Anand, Ruchika; Reichert, Andreas S. International Journal of Molecular Sciences, Vol. 20, Issue 17 https://doi.org/10.3390/ijms20174311	journal	September 2019
The Phyre2 web portal for protein modeling, prediction and analysis Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M. Nature Protocols, Vol. 10, Issue 6 https://doi.org/10.1038/nprot.2015.053	journal	May 2015
Kinetic coupling of the respiratory chain with ATP synthase, but not proton gradients, drives ATP production in cristae membranes. Toth, Alexandra; Meyrat, Axel; Stoldt, Stefan National Academy of Sciences NAS https://doi.org/10.7892/boris.147126	text	January 2020
Single organelle function and organization as estimated from Arabidopsis mitochondrial proteomics Fuchs, Philippe; Rugen, Nils; Carrie, Chris Oxford [u.a.] : Wiley-Blackwell https://doi.org/10.15488/11679	other	January 2020
The Unique Cysteine of F-ATP Synthase OSCP Subunit Participates in Modulation of the Permeability Transition Pore Carraro, Michela; Jones, Kristen; Sartori, Geppo Cell Reports, Vol. 32, Issue 9 https://doi.org/10.1016/j.celrep.2020.108095	journal	September 2020
Rcf2 revealed in cryo-EM structures of hypoxic isoforms of mature mitochondrial III-IV supercomplexes Hartley, Andrew M.; Meunier, Brigitte; Pinotsis, Nikos Proceedings of the National Academy of Sciences, Vol. 117, Issue 17 https://doi.org/10.1073/pnas.1920612117	journal	April 2020
Consequences of Folding the Mitochondrial Inner Membrane Mannella, Carmen A. Frontiers in Physiology, Vol. 11 https://doi.org/10.3389/fphys.2020.00536	journal	June 2020
VDAC—A Primal Perspective Mannella, Carmen A. International Journal of Molecular Sciences, Vol. 22, Issue 4 https://doi.org/10.3390/ijms22041685	journal	February 2021
ATP synthase: evolution, energetics, and membrane interactions Nirody, Jasmine A.; Budin, Itay; Rangamani, Padmini arXiv https://doi.org/10.48550/arxiv.2006.09357	text	January 2020

Similar Records

Effect of the ATPase inhibitor protein IF{sub 1} on H{sup +} translocation in the mitochondrial ATP synthase complex

Journal Article · Fri Jun 19 00:00:00 EDT 2009 · Biochemical and Biophysical Research Communications · OSTI ID:1559185

Zanotti, Franco; Gnoni, Antonio; Mangiullo, Roberto; +1 more

Cristae formation is a mechanical buckling event controlled by the inner mitochondrial membrane lipidome

Journal Article · Tue Nov 07 00:00:00 EST 2023 · EMBO Journal · OSTI ID:1559185

Venkatraman, Kailash; Lee, Christopher T.; Garcia, Guadalupe C.; +10 more

Cristae architecture is determined by an interplay of the MICOS complex and the F₁F_o ATP synthase via Mic27 and Mic10

Journal Article · Mon Aug 07 00:00:00 EDT 2017 · Microbial Cell · OSTI ID:1559185

Eydt, Katharina; Davis, Karen M.; Behrendt, Christina; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
mitochondria
ATP synthase
membrane curvature
electron cryotomography
subtomogram averaging

Title: Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows

Citation Formats

References (40)

Cited By (17)

Similar Records

Related Subjects