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

Venkatraman, Kailash; Lee, Christopher T.; Garcia, Guadalupe C.; Mahapatra, Arijit; Milshteyn, Daniel; Perkins, Guy; Kim, Keun‐Young; Pasolli, H. Amalia; Phan, Sebastien; Lippincott‐Schwartz, Jennifer; Ellisman, Mark H.; Rangamani, Padmini; Budin, Itay

doi:10.15252/embj.2023114054

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

DOI:https://doi.org/10.15252/embj.2023114054· OSTI ID:2204905

^[1]; ^[2]; ^[3]; Mahapatra, Arijit ^[2]; Milshteyn, Daniel ^[1]; Perkins, Guy ^[4]; Kim, Keun‐Young ^[4]; ^[5]; ^[4]; Lippincott‐Schwartz, Jennifer ^[5]; ^[4]; ^[2]; ^[1]

Department of Chemistry and Biochemistry University of California San Diego La Jolla CA USA
Department of Mechanical and Aerospace Engineering University of California San Diego La Jolla CA USA
Computational Neurobiology Laboratory Salk Institute for Biological Studies La Jolla CA USA
National Center for Microscopy and Imaging Research, Center for Research in Biological Systems University of California San Diego La Jolla CA USA
Howard Hughes Medical Institute Ashburn VA USA

Abstract

Cristae are high‐curvature structures in the inner mitochondrial membrane (IMM) that are crucial for ATP production. While cristae‐shaping proteins have been defined, analogous lipid‐based mechanisms have yet to be elucidated. Here, we combine experimental lipidome dissection with multi‐scale modeling to investigate how lipid interactions dictate IMM morphology and ATP generation. When modulating phospholipid (PL) saturation in engineered yeast strains, we observed a surprisingly abrupt breakpoint in IMM topology driven by a continuous loss of ATP synthase organization at cristae ridges. We found that cardiolipin (CL) specifically buffers the inner mitochondrial membrane against curvature loss, an effect that is independent of ATP synthase dimerization. To explain this interaction, we developed a continuum model for cristae tubule formation that integrates both lipid and protein‐mediated curvatures. This model highlighted a snapthrough instability, which drives IMM collapse upon small changes in membrane properties. We also showed that cardiolipin is essential in low‐oxygen conditions that promote PL saturation. These results demonstrate that the mechanical function of cardiolipin is dependent on the surrounding lipid and protein components of the IMM.

View Journal Article

Research Organization:: University of California, San Diego, La Jolla, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0022954

OSTI ID:: 2204905

Alternate ID(s):: OSTI ID: 2472223
OSTI ID: 2204907

Journal Information:: EMBO Journal, Journal Name: EMBO Journal Journal Issue: 24 Vol. 42; ISSN 0261-4189

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (129)

The phosphatidylcholine to phosphatidylethanolamine ratio ofSaccharomyces cerevisiae varies with the growth phase Janssen, Marjolein J. F. W.; Koorengevel, Martijn C.; de Kruijff, Ben Yeast, Vol. 16, Issue 7 https://doi.org/10.1002/(SICI)1097-0061(200005)16:7<641::AID-YEA578>3.0.CO;2-U	journal	May 2000
Rapid and reliable protein extraction from yeast Kushnirov, Vitaly V. Yeast, Vol. 16, Issue 9 https://doi.org/10.1002/1097-0061(20000630)16:9<857::AID-YEA561>3.0.CO;2-B	journal	January 2000
Barth syndrome: Clinical features and confirmation of gene localisation to distal Xq28 Adès, L. C.; Gedeon, A. K.; Wilson, M. J. American Journal of Medical Genetics, Vol. 45, Issue 3 https://doi.org/10.1002/ajmg.1320450309	journal	February 1993
Morphological principles of neuronal mitochondria Mendelsohn, Rachel; Garcia, Guadalupe C.; Bartol, Thomas M. Journal of Comparative Neurology, Vol. 530, Issue 6 https://doi.org/10.1002/cne.25254	journal	November 2021
An automated shotgun lipidomics platform for high throughput, comprehensive, and quantitative analysis of blood plasma intact lipids Surma, Michal A.; Herzog, Ronny; Vasilj, Andrej European Journal of Lipid Science and Technology, Vol. 117, Issue 10 https://doi.org/10.1002/ejlt.201500145	journal	July 2015
Mammalian ATPsynthase monomerversus dimer profiled by blue native PAGE and activity stain Bisetto, Elena; Di Pancrazio, Francesca; Simula, Maria Paola ELECTROPHORESIS, Vol. 28, Issue 18 https://doi.org/10.1002/elps.200700066	journal	September 2007
The internal compartmentation of rat-liver mitochondria: Tomographic study using the high-voltage transmission electron microscope Mannella, Carmen A.; Marko, Michael; Penczek, Pawel Microscopy Research and Technique, Vol. 27, Issue 4 https://doi.org/10.1002/jemt.1070270403	journal	March 1994
Electron Tomography of Neuronal Mitochondria: Three-Dimensional Structure and Organization of Cristae and Membrane Contacts Perkins, G.; Renken, C.; Martone, M. E. Journal of Structural Biology, Vol. 119, Issue 3 https://doi.org/10.1006/jsbi.1997.3885	journal	August 1997
Purification of Functional F-ATP Synthase from Blue Native PAGE Galber, Chiara; Valente, Giulia; von Stockum, Sophia Calcium Signalling https://doi.org/10.1007/978-1-4939-9018-4_20	book	January 2019
Improved Technique for Electron Microscope Visualization of Yeast Membrane Structure Bauer, Christoph; Herzog, Volker; Bauer, Matthias F. Microscopy and Microanalysis, Vol. 7, Issue 6 https://doi.org/10.1007/S10005-001-0020-4	journal	November 2001
Mitochondrial phospholipids: role in mitochondrial function Mejia, Edgard M.; Hatch, Grant M. Journal of Bioenergetics and Biomembranes, Vol. 48, Issue 2 https://doi.org/10.1007/s10863-015-9601-4	journal	January 2015
VolRoverN: Enhancing Surface and Volumetric Reconstruction for Realistic Dynamical Simulation of Cellular and Subcellular Function Edwards, John; Daniel, Eric; Kinney, Justin Neuroinformatics, Vol. 12, Issue 2 https://doi.org/10.1007/s12021-013-9205-2	journal	October 2013
Effects of fatty acids on mitochondria: implications for cell death Penzo, Daniele; Tagliapietra, Chiara; Colonna, Raffaele Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1555, Issue 1-3 https://doi.org/10.1016/S0005-2728(02)00272-4	journal	September 2002
Phosphatidylserine decarboxylase Voelker, Dennis R. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 1348, Issue 1-2 https://doi.org/10.1016/S0005-2760(97)00101-X	journal	September 1997
Effect of Chain Length and Unsaturation on Elasticity of Lipid Bilayers Rawicz, W.; Olbrich, K. C.; McIntosh, T. Biophysical Journal, Vol. 79, Issue 1 https://doi.org/10.1016/S0006-3495(00)76295-3	journal	July 2000
The Effects of Acyl Chain Length and Saturation of Diacylglycerols and Phosphatidylcholines on Membrane Monolayer Curvature Szule, Joseph A.; Fuller, Nola L.; Peter Rand, R. Biophysical Journal, Vol. 83, Issue 2 https://doi.org/10.1016/S0006-3495(02)75223-5	journal	August 2002
The Effect of Cholesterol on the Lateral Diffusion of Phospholipids in Oriented Bilayers Filippov, Andrey; Orädd, Greger; Lindblom, Göran Biophysical Journal, Vol. 84, Issue 5 https://doi.org/10.1016/S0006-3495(03)70033-2	journal	May 2003
Isolation and characterization of OLE1, a gene affecting fatty acid desaturation from Saccharomyces cerevisiae Stukey, J. E.; McDonough, V. M.; Martin, C. E. Journal of Biological Chemistry, Vol. 264, Issue 28 https://doi.org/10.1016/S0021-9258(19)84740-3	journal	October 1989
Shape and attachment of the cristae mitochondriales in mouse hepatic cell mitochondria Daems, W. Th.; Wisse, E. Journal of Ultrastructure Research, Vol. 16, Issue 1-2 https://doi.org/10.1016/S0022-5320(66)80027-8	journal	September 1966
Cryomethods for thin section electron microscopy McDonald, Kent; Müller-Reichert, Thomas Guide to Yeast Genetics and Molecular and Cell Biology Part C https://doi.org/10.1016/S0076-6879(02)51843-7	book	January 2002
The internal structure of mitochondria Frey, Terrence G.; Mannella, Carmen A. Trends in Biochemical Sciences, Vol. 25, Issue 7 https://doi.org/10.1016/S0968-0004(00)01609-1	journal	July 2000
Reconsidering mitochondrial structure: new views of an old organelle Mannella, Carmen A.; Marko, Michael; Buttle, Karolyn Trends in Biochemical Sciences, Vol. 22, Issue 2 https://doi.org/10.1016/S0968-0004(96)30050-9	journal	February 1997
Quantifying mitochondrial content in living cells Viana, Matheus Palhares; Lim, Swee; Rafelski, Susanne M. Methods in Cell Biology https://doi.org/10.1016/bs.mcb.2014.10.003	book	January 2015
Functional role of cardiolipin in mitochondrial bioenergetics Paradies, Giuseppe; Paradies, Valeria; De Benedictis, Valentina Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 4 https://doi.org/10.1016/j.bbabio.2013.10.006	journal	April 2014
The relevance of mitochondrial membrane topology to mitochondrial function Mannella, Carmen A. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1762, Issue 2 https://doi.org/10.1016/j.bbadis.2005.07.001	journal	February 2006
Effects of siRNA-dependent knock-down of cardiolipin synthase and tafazzin on mitochondria and proliferation of glioma cells Ohlig, Theresa; Le, Do Viet; Gardemann, Andreas Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1863, Issue 4 https://doi.org/10.1016/j.bbalip.2018.01.003	journal	April 2018
Structure and dynamics of the mitochondrial inner membrane cristae Mannella, Carmen A. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1763, Issue 5-6 https://doi.org/10.1016/j.bbamcr.2006.04.006	journal	May 2006
Cristae formation—linking ultrastructure and function of mitochondria Zick, Michael; Rabl, Regina; Reichert, Andreas S. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1793, Issue 1 https://doi.org/10.1016/j.bbamcr.2008.06.013	journal	January 2009
Evolution and structural organization of the mitochondrial contact site (MICOS) complex and the mitochondrial intermembrane space bridging (MIB) complex Huynen, Martijn A.; Mühlmeister, Mareike; Gotthardt, Katherina Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1863, Issue 1 https://doi.org/10.1016/j.bbamcr.2015.10.009	journal	January 2016
Lipid packing variations induced by pH in cardiolipin-containing bilayers: The driving force for the cristae-like shape instability Khalifat, Nada; Fournier, Jean-Baptiste; Angelova, Miglena I. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1808, Issue 11 https://doi.org/10.1016/j.bbamem.2011.07.013	journal	November 2011
Cardiolipin and mitochondrial cristae organization Ikon, Nikita; Ryan, Robert O. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1859, Issue 6 https://doi.org/10.1016/j.bbamem.2017.03.013	journal	June 2017
OPA1 Controls Apoptotic Cristae Remodeling Independently from Mitochondrial Fusion Frezza, Christian; Cipolat, Sara; Martins de Brito, Olga Cell, Vol. 126, Issue 1 https://doi.org/10.1016/j.cell.2006.06.025	journal	July 2006
Mitochondria: In Sickness and in Health Nunnari, Jodi; Suomalainen, Anu Cell, Vol. 148, Issue 6 https://doi.org/10.1016/j.cell.2012.02.035	journal	March 2012
Decoding Information in Cell Shape Rangamani, Padmini; Lipshtat, Azi; Azeloglu, Evren U. Cell, Vol. 154, Issue 6 https://doi.org/10.1016/j.cell.2013.08.026	journal	September 2013
Optic Atrophy 1 Is Epistatic to the Core MICOS Component MIC60 in Mitochondrial Cristae Shape Control Glytsou, Christina; Calvo, Enrique; Cogliati, Sara Cell Reports, Vol. 17, Issue 11 https://doi.org/10.1016/j.celrep.2016.11.049	journal	December 2016
Triglycerides Promote Lipid Homeostasis during Hypoxic Stress by Balancing Fatty Acid Saturation Ackerman, Daniel; Tumanov, Sergey; Qiu, Bo Cell Reports, Vol. 24, Issue 10 https://doi.org/10.1016/j.celrep.2018.08.015	journal	September 2018
Lipid monolayer spontaneous curvatures: A collection of published values Dymond, Marcus K. Chemistry and Physics of Lipids, Vol. 239 https://doi.org/10.1016/j.chemphyslip.2021.105117	journal	September 2021
Returning to the Fold for Lessons in Mitochondrial Crista Diversity and Evolution Pánek, Tomáš; Eliáš, Marek; Vancová, Marie Current Biology, Vol. 30, Issue 10 https://doi.org/10.1016/j.cub.2020.02.053	journal	May 2020
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
Regulation of mitochondrial cristae remodelling by acetylcholine alleviates palmitate-induced cardiomyocyte hypertrophy Xue, Run-Qing; Zhao, Ming; Wu, Qing Free Radical Biology and Medicine, Vol. 145 https://doi.org/10.1016/j.freeradbiomed.2019.09.025	journal	December 2019
A Eukaryotic Sensor for Membrane Lipid Saturation Covino, Roberto; Ballweg, Stephanie; Stordeur, Claudius Molecular Cell, Vol. 63, Issue 1 https://doi.org/10.1016/j.molcel.2016.05.015	journal	July 2016
Lipids of mitochondria Horvath, Susanne E.; Daum, Günther Progress in Lipid Research, Vol. 52, Issue 4 https://doi.org/10.1016/j.plipres.2013.07.002	journal	October 2013
Metabolism and function of mitochondrial cardiolipin Ren, Mindong; Phoon, Colin K. L.; Schlame, Michael Progress in Lipid Research, Vol. 55 https://doi.org/10.1016/j.plipres.2014.04.001	journal	July 2014
The complexity of cardiolipin in health and disease Claypool, Steven M.; Koehler, Carla M. Trends in Biochemical Sciences, Vol. 37, Issue 1 https://doi.org/10.1016/j.tibs.2011.09.003	journal	January 2012
Mitochondrial Cristae: Where Beauty Meets Functionality Cogliati, Sara; Enriquez, Jose A.; Scorrano, Luca Trends in Biochemical Sciences, Vol. 41, Issue 3 https://doi.org/10.1016/j.tibs.2016.01.001	journal	March 2016
Protocol for the Analysis of Yeast and Human Mitochondrial Respiratory Chain Complexes and Supercomplexes by Blue Native Electrophoresis Timón-Gómez, Alba; Pérez-Pérez, Rafael; Nyvltova, Eva STAR Protocols, Vol. 1, Issue 2 https://doi.org/10.1016/j.xpro.2020.100089	journal	September 2020
Lipid engineering reveals regulatory roles for membrane fluidity in yeast flocculation and oxygen-limited growth Degreif, Daniel; de Rond, Tristan; Bertl, Adam Metabolic Engineering, Vol. 41 https://doi.org/10.1016/j.ymben.2017.03.002	journal	May 2017
Computational Modeling of Realistic Cell Membranes Marrink, Siewert J.; Corradi, Valentina; Souza, Paulo C. T. Chemical Reviews, Vol. 119, Issue 9 https://doi.org/10.1021/acs.chemrev.8b00460	journal	January 2019
Buckling Under Pressure: Curvature-Based Lipid Segregation and Stability Modulation in Cardiolipin-Containing Bilayers Boyd, Kevin J.; Alder, Nathan N.; May, Eric R. Langmuir, Vol. 33, Issue 27 https://doi.org/10.1021/acs.langmuir.7b01185	journal	June 2017
On the Structure of Cardiolipin ^* LeCocq, Jean; Ballou, Clinton E. Biochemistry, Vol. 3, Issue 7 https://doi.org/10.1021/bi00895a023	journal	July 1964
Mechanical Properties of Coarse-Grained Bilayers Formed by Cardiolipin and Zwitterionic Lipids Dahlberg, Martin; Maliniak, Arnold Journal of Chemical Theory and Computation, Vol. 6, Issue 5 https://doi.org/10.1021/ct900654e	journal	April 2010
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
The mitochondrial contact site complex, a determinant of mitochondrial architecture: Molecular architecture of mitochondria Harner, Max; Körner, Christian; Walther, Dirk The EMBO Journal, Vol. 30, Issue 21 https://doi.org/10.1038/emboj.2011.379	journal	October 2011
Comparison of lymphoblast mitochondria from normal subjects and patients with Barth syndrome using electron microscopic tomography Acehan, Devrim; Xu, Yang; Stokes, David L. Laboratory Investigation, Vol. 87, Issue 1 https://doi.org/10.1038/labinvest.3700480	journal	October 2006
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
A novel X-linked gene, G4.5. is responsible for Barth syndrome Bione, Silvia; D'Adamo, Patrizia; Maestrini, Elena Nature Genetics, Vol. 12, Issue 4 https://doi.org/10.1038/ng0496-385	journal	April 1996
Hypoxia-inducible factors enhance the effector responses of CD8+ T cells to persistent antigen Doedens, Andrew L.; Phan, Anthony T.; Stradner, Martin H. Nature Immunology, Vol. 14, Issue 11 https://doi.org/10.1038/ni.2714	journal	September 2013
OPA1 and MICOS Regulate mitochondrial crista dynamics and formation Hu, Chao; Shu, Li; Huang, Xiaoshuai Cell Death & Disease, Vol. 11, Issue 10 https://doi.org/10.1038/s41419-020-03152-y	journal	October 2020
Regulation of lipid saturation without sensing membrane fluidity Ballweg, Stephanie; Sezgin, Erdinc; Doktorova, Milka Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14528-1	journal	February 2020
Author Correction: Understanding the diversity of membrane lipid composition Harayama, Takeshi; Riezman, Howard Nature Reviews Molecular Cell Biology, Vol. 20, Issue 11 https://doi.org/10.1038/s41580-019-0171-x	journal	September 2019
Metabolic programs of T cell tissue residency empower tumour immunity Reina-Campos, Miguel; Heeg, Maximilian; Kennewick, Kelly Nature, Vol. 621, Issue 7977 https://doi.org/10.1038/s41586-023-06483-w	journal	August 2023
Geometric principles of second messenger dynamics in dendritic spines Cugno, Andrea; Bartol, Thomas M.; Sejnowski, Terrence J. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-48028-0	journal	August 2019
Mitochondrial morphology provides a mechanism for energy buffering at synapses Garcia, Guadalupe C.; Bartol, Thomas M.; Phan, Sébastien Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-54159-1	journal	December 2019
Cell shape regulates subcellular organelle location to control early Ca2+ signal dynamics in vascular smooth muscle cells Calizo, R. C.; Bell, M. K.; Ron, A. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-74700-x	journal	October 2020
Membrane curvature induces cardiolipin sorting Beltrán-Heredia, Elena; Tsai, Feng-Ching; Salinas-Almaguer, Samuel Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0471-x	journal	June 2019
Cardiolipin deficiency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis Choi, S-Y; Gonzalvez, F.; Jenkins, G. M. Cell Death & Differentiation, Vol. 14, Issue 3 https://doi.org/10.1038/sj.cdd.4402020	journal	August 2006
Differential dependencies on [Ca²⁺] and temperature of the monolayer spontaneous curvatures of DOPE, DOPA and cardiolipin: effects of modulating the strength of the inter-headgroup repulsion Chen, Y. -F.; Tsang, K. -Y.; Chang, W. -F. Soft Matter, Vol. 11, Issue 20 https://doi.org/10.1039/C5SM00577A	journal	January 2015
A mechanical model reveals that non-axisymmetric buckling lowers the energy barrier associated with membrane neck constriction Vasan, R.; Rudraraju, S.; Akamatsu, M. Soft Matter, Vol. 16, Issue 3 https://doi.org/10.1039/C9SM01494B	journal	January 2020
Formation of protein-mediated bilayer tubes is governed by a snapthrough transition Mahapatra, Arijit; Rangamani, Padmini Soft Matter, Vol. 19, Issue 23 https://doi.org/10.1039/D2SM01676A	journal	January 2023
Perspective on the Martini model Marrink, Siewert J.; Tieleman, D. Peter Chemical Society Reviews, Vol. 42, Issue 16 https://doi.org/10.1039/c3cs60093a	journal	January 2013
Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems Al-Fageeh, Mohamed B.; Smales, C. Mark Biochemical Journal, Vol. 397, Issue 2 https://doi.org/10.1042/BJ20060166	journal	June 2006
Asymmetrical distribution of cardiolipin in yeast inner mitochondrial membrane triggered by carbon catabolite repression Gallet, Paul François; Petit, Jean-Michel; Maftah, Abderrahman Biochemical Journal, Vol. 324, Issue 2 https://doi.org/10.1042/bj3240627	journal	June 1997
Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non‐fermentable carbon sources Jiang, Feng; Rizavi, Hooriyah S.; Greenberg, Miriam L. Molecular Microbiology, Vol. 26, Issue 3 https://doi.org/10.1046/j.1365-2958.1997.5841950.x	journal	October 1997
Impaired Mitochondrial Activity in the Insulin-Resistant Offspring of Patients with Type 2 Diabetes Petersen, Kitt Falk; Dufour, Sylvie; Befroy, Douglas New England Journal of Medicine, Vol. 350, Issue 7 https://doi.org/10.1056/NEJMoa031314	journal	February 2004
Tuning genetic control through promoter engineering Alper, H.; Fischer, C.; Nevoigt, E. Proceedings of the National Academy of Sciences, Vol. 102, Issue 36, p. 12678-12683 https://doi.org/10.1073/pnas.0504604102	journal	August 2005
Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry Ejsing, C. S.; Sampaio, J. L.; Surendranath, V. Proceedings of the National Academy of Sciences, Vol. 106, Issue 7 https://doi.org/10.1073/pnas.0811700106	journal	January 2009
F1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase Rak, M.; Tzagoloff, A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 44 https://doi.org/10.1073/pnas.0910351106	journal	October 2009
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
Hypoxic and Ras-transformed cells support growth by scavenging unsaturated fatty acids from lysophospholipids Kamphorst, J. J.; Cross, J. R.; Fan, J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 22 https://doi.org/10.1073/pnas.1307237110	journal	May 2013
Endocytic proteins drive vesicle growth via instability in high membrane tension environment Walani, Nikhil; Torres, Jennifer; Agrawal, Ashutosh Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1418491112	journal	March 2015
Design principles for robust vesiculation in clathrin-mediated endocytosis Hassinger, Julian E.; Oster, George; Drubin, David G. Proceedings of the National Academy of Sciences, Vol. 114, Issue 7 https://doi.org/10.1073/pnas.1617705114	journal	January 2017
Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows Blum, Thorsten B.; Hahn, Alexander; Meier, Thomas Proceedings of the National Academy of Sciences, Vol. 116, Issue 10 https://doi.org/10.1073/pnas.1816556116	journal	February 2019
Oxygen sensing in yeast: Evidence for the involvement of the respiratory chain in regulating the transcription of a subset of hypoxic genes Kwast, Kurt E.; Burke, Patricia V.; Staahl, Brett T. Proceedings of the National Academy of Sciences, Vol. 96, Issue 10 https://doi.org/10.1073/pnas.96.10.5446	journal	May 1999
Identification and Characterization of a Low Oxygen Response Element Involved in the Hypoxic Induction of a Family ofSaccharomyces cerevisiae Genes Vasconcelles, Michael J.; Jiang, Yide; McDaid, Kevin Journal of Biological Chemistry, Vol. 276, Issue 17 https://doi.org/10.1074/jbc.M009546200	journal	April 2001
ChChd3, an Inner Mitochondrial Membrane Protein, Is Essential for Maintaining Crista Integrity and Mitochondrial Function Darshi, Manjula; Mendiola, Vincent L.; Mackey, Mason R. Journal of Biological Chemistry, Vol. 286, Issue 4 https://doi.org/10.1074/jbc.M110.171975	journal	January 2011
Unremodeled and Remodeled Cardiolipin Are Functionally Indistinguishable in Yeast Baile, Matthew G.; Sathappa, Murugappan; Lu, Ya-Wen Journal of Biological Chemistry, Vol. 289, Issue 3 https://doi.org/10.1074/jbc.M113.525733	journal	January 2014
Phosphatidylethanolamine Is a Key Regulator of Membrane Fluidity in Eukaryotic Cells Dawaliby, Rosie; Trubbia, Cataldo; Delporte, Cédric Journal of Biological Chemistry, Vol. 291, Issue 7 https://doi.org/10.1074/jbc.M115.706523	journal	December 2015
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
Cardiolipin Is Essential for Organization of Complexes III and IV into a Supercomplex in Intact Yeast Mitochondria Zhang, Mei; Mileykovskaya, Eugenia; Dowhan, William Journal of Biological Chemistry, Vol. 280, Issue 33 https://doi.org/10.1074/jbc.M504955200	journal	August 2005
Temperature-sensitive yeast mutants defective in mitochondrial inheritance. McConnell, S. J.; Stewart, L. C.; Talin, A. The Journal of cell biology, Vol. 111, Issue 3 https://doi.org/10.1083/jcb.111.3.967	journal	September 1990
A role for unsaturated fatty acids in mitochondrial movement and inheritance. Stewart, L. C.; Yaffe, M. P. The Journal of cell biology, Vol. 115, Issue 5 https://doi.org/10.1083/jcb.115.5.1249	journal	December 1991
Observations on Mitochondrial Structure Revel, J. P.; Fawcett, D. W.; Philpott, C. W. The Journal of Cell Biology, Vol. 16, Issue 1 https://doi.org/10.1083/jcb.16.1.187	journal	January 1963
Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane Claypool, Steven M.; Oktay, Yavuz; Boontheung, Pinmanee The Journal of Cell Biology, Vol. 182, Issue 5 https://doi.org/10.1083/jcb.200801152	journal	September 2008
Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g Rabl, Regina; Soubannier, Vincent; Scholz, Roland Journal of Cell Biology, Vol. 185, Issue 6 https://doi.org/10.1083/jcb.200811099	journal	June 2009
A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria Hoppins, Suzanne; Collins, Sean R.; Cassidy-Stone, Ann Journal of Cell Biology, Vol. 195, Issue 2 https://doi.org/10.1083/jcb.201107053	journal	October 2011
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
Specific requirements of nonbilayer phospholipids in mitochondrial respiratory chain function and formation Baker, Charli D.; Basu Ball, Writoban; Pryce, Erin N. Molecular Biology of the Cell, Vol. 27, Issue 14 https://doi.org/10.1091/mbc.E15-12-0865	journal	July 2016
Mgm1p, a Dynamin-related GTPase, Is Essential for Fusion of the Mitochondrial Outer Membrane Sesaki, Hiromi; Southard, Sheryl M.; Yaffe, Michael P. Molecular Biology of the Cell, Vol. 14, Issue 6 https://doi.org/10.1091/mbc.e02-12-0788	journal	June 2003
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 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
Bacterial membrane lipids: diversity in structures and pathways Sohlenkamp, Christian; Geiger, Otto FEMS Microbiology Reviews, Vol. 40, Issue 1 https://doi.org/10.1093/femsre/fuv008	journal	April 2015
Cardiolipin is essential for early embryonic viability and mitochondrial integrity of neurons in mammals Kasahara, Takaoki; Kubota‐Sakashita, Mie; Nagatsuka, Yasuko The FASEB Journal, Vol. 34, Issue 1 https://doi.org/10.1096/fj.201901598R	journal	December 2019
Mitochondrial Membranes: Model Lipid Compositions, Material Properties and the Changing Curvature of Cardiolipin Konar, Sukanya; Arif, Hina; Allolio, Christoph https://doi.org/10.1101/2023.02.06.527315	preprint	February 2023
Curvature-Driven Lipid Sorting in Biomembranes Callan-Jones, A.; Sorre, B.; Bassereau, P. Cold Spring Harbor Perspectives in Biology, Vol. 3, Issue 2 https://doi.org/10.1101/cshperspect.a004648	journal	January 2011
Direct analysis and significance of cardiolipin transverse distribution in mitochondrial inner membranes Petit, Jean‐Michel; Huet, Olivier; Gallet, Paul François European Journal of Biochemistry, Vol. 220, Issue 3 https://doi.org/10.1111/j.1432-1033.1994.tb18690.x	journal	March 1994
Phospholipid Synthesis and Transport in Mammalian Cells Vance, Jean E. Traffic, Vol. 16, Issue 1 https://doi.org/10.1111/tra.12230	journal	October 2014
Mitochondrial Dysfunction and Type 2 Diabetes Lowell, Bradford B.; Shulman, Gerald I. Science, Vol. 307, Issue 5708 https://doi.org/10.1126/science.1104343	journal	January 2005
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
Impact of Membrane Phospholipid Alterations in Escherichia coli on Cellular Function and Bacterial Stress Adaptation Rowlett, Veronica W.; Mallampalli, Venkata K. P. S.; Karlstaedt, Anja Journal of Bacteriology, Vol. 199, Issue 13 https://doi.org/10.1128/JB.00849-16	journal	April 2017
Mitochondrial Fission Contributes to Mitochondrial Dysfunction and Insulin Resistance in Skeletal Muscle Jheng, Huei-Fen; Tsai, Pei-Jane; Guo, Syue-Maio Molecular and Cellular Biology, Vol. 32, Issue 2 https://doi.org/10.1128/MCB.05603-11	journal	January 2012
Biochemical and Genetic Aspects of Nystatin Resistance in Saccharomyces cerevisiae Bard, Martin Journal of Bacteriology, Vol. 111, Issue 3 https://doi.org/10.1128/jb.111.3.649-657.1972	journal	September 1972
Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. Zinser, E.; Sperka-Gottlieb, C. D.; Fasch, E. V. Journal of Bacteriology, Vol. 173, Issue 6 https://doi.org/10.1128/jb.173.6.2026-2034.1991	journal	March 1991
Geometric Methods in the Elastic Theory of Membranes in Liquid Crystal Phases Zhong-Can, Ou-Yang; Ji-Xing, Liu; Yu-Zhang, Xie https://doi.org/10.1142/3579	book	March 1999
Physiologic hypoxia and oxygen homeostasis in the healthy intestine. A Review in the Theme: Cellular Responses to Hypoxia Zheng, Leon; Kelly, Caleb J.; Colgan, Sean P. American Journal of Physiology-Cell Physiology, Vol. 309, Issue 6 https://doi.org/10.1152/ajpcell.00191.2015	journal	September 2015
A metabolic role for mitochondria in palmitate-induced cardiac myocyte apoptosis Sparagna, Genevieve C.; Hickson-Bick, Diane L.; Buja, L. Maximilian American Journal of Physiology-Heart and Circulatory Physiology, Vol. 279, Issue 5 https://doi.org/10.1152/ajpheart.2000.279.5.H2124	journal	November 2000
A novel informatics concept for high-throughput shotgun lipidomics based on the molecular fragmentation query language Herzog, Ronny; Schwudke, Dominik; Schuhmann, Kai Genome Biology, Vol. 12, Issue 1 https://doi.org/10.1186/gb-2011-12-1-r8	journal	January 2011
Depth- and temperature-specific fatty acid adaptations in ctenophores from extreme habitats Winnikoff, Jacob R.; Haddock, Steven H. D.; Budin, Itay Journal of Experimental Biology, Vol. 224, Issue 21 https://doi.org/10.1242/jeb.242800	journal	November 2021
3D mesh processing using GAMer 2 to enable reaction-diffusion simulations in realistic cellular geometries Lee, Christopher T.; Laughlin, Justin G.; Angliviel de La Beaumelle, Nils PLOS Computational Biology, Vol. 16, Issue 4 https://doi.org/10.1371/journal.pcbi.1007756	journal	April 2020
LipidXplorer: A Software for Consensual Cross-Platform Lipidomics Herzog, Ronny; Schuhmann, Kai; Schwudke, Dominik PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0029851	journal	January 2012
Flexibility of a Eukaryotic Lipidome – Insights from Yeast Lipidomics Klose, Christian; Surma, Michal A.; Gerl, Mathias J. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035063	journal	April 2012
OPA1‐dependent cristae modulation is essential for cellular adaptation to metabolic demand Patten, David A.; Wong, Jacob; Khacho, Mireille The EMBO Journal, Vol. 33, Issue 22 https://doi.org/10.15252/embj.201488349	journal	October 2014
Cardiolipin remodeling enables protein crowding in the inner mitochondrial membrane Xu, Yang; Erdjument‐Bromage, Hediye; Phoon, Colin K. L. The EMBO Journal, Vol. 40, Issue 23 https://doi.org/10.15252/embj.2021108428	journal	October 2021
Membrane Deformation under Local pH Gradient: Mimicking Mitochondrial Cristae Dynamics Khalifat, Nada; Puff, Nicolas; Bonneau, Stéphanie Biophysical Journal, Vol. 95, Issue 10 https://doi.org/10.1529/biophysj.108.136077	journal	November 2008
Cardiolipin externalization mediates prion protein (PrP) peptide 106–126-associated mitophagy and mitochondrial dysfunction Yang, Dongming; Li, Jie; Li, Zhiping Frontiers in Molecular Neuroscience, Vol. 16 https://doi.org/10.3389/fnmol.2023.1163981	journal	June 2023
Role of Cardiolipin in Mitochondrial Function and Dynamics in Health and Disease: Molecular and Pharmacological Aspects Paradies, Giuseppe; Paradies, Valeria; Ruggiero, Francesca M. Cells, Vol. 8, Issue 7 https://doi.org/10.3390/cells8070728	journal	July 2019
The dimerization equilibrium of a ClC Cl−/H+ antiporter in lipid bilayers Chadda, Rahul; Krishnamani, Venkatramanan; Mersch, Kacey eLife, Vol. 5 https://doi.org/10.7554/eLife.17438	journal	August 2016
An evidence based hypothesis on the existence of two pathways of mitochondrial crista formation Harner, Max E.; Unger, Ann-Katrin; Geerts, Willie JC eLife, Vol. 5 https://doi.org/10.7554/eLife.18853	journal	November 2016
Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage Manni, Marco M.; Tiberti, Marion L.; Pagnotta, Sophie eLife, Vol. 7 https://doi.org/10.7554/eLife.34394	journal	March 2018
Membrane transporter dimerization driven by differential lipid solvation energetics of dissociated and associated states Chadda, Rahul; Bernhardt, Nathan; Kelley, Elizabeth G. eLife, Vol. 10 https://doi.org/10.7554/eLife.63288	journal	April 2021

Similar Records

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

Journal Article · Tue Feb 12 19:00:00 EST 2019 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1559185

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biochemistry & Molecular Biology
Cardiolipin
Cell Biology
Cristae
Lipids
Mechanics
Mitochondria

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

Citation Formats

References (129)

Similar Records

Related Subjects