Beyond being an energy supplier, ATP synthase is a sculptor of mitochondrial cristae.

ATP synthase; F(1)-F(O) ATPase; Lineage-specific subunits; Mitochondrial ATPase; Adenosine Triphosphate; Glycogen Synthase; Mitochondrial Proton-Translocating ATPases; Adenosine Triphosphate/metabolism; Mitochondria/metabolism; Mitochondrial Membranes/metabolism; Glycogen Synthase/metabolism; Mitochondrial Proton-Translocating ATPases/metabolism; F1-FO ATPase; Mitochondria; Mitochondrial Membranes; Biophysics; Biochemistry; Cell Biology

Abstract :

[en] Mitochondrial F1FO-ATP synthase plays a key role in cellular bioenergetics; this enzyme is present in all eukaryotic linages except in amitochondriate organisms. Despite its ancestral origin, traceable to the alpha proteobacterial endosymbiotic event, the actual structural diversity of these complexes, due to large differences in their polypeptide composition, reflects an important evolutionary divergence between eukaryotic lineages. We discuss the effect of these structural differences on the oligomerization of the complex and the shape of mitochondrial cristae.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Miranda-Astudillo, Héctor; Departamento de Biología Molecular y Biotecnología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Mexico City, Mexico

Ostolga-Chavarría, Marcos; Departamento de Genética Molecular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City, Mexico

Cardol, Pierre ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues

González-Halphen, Diego; Departamento de Genética Molecular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City, Mexico. Electronic address: dhalphen@ifc.unam.mx

Language :

English

Title :

Beyond being an energy supplier, ATP synthase is a sculptor of mitochondrial cristae.

Publication date :

01 August 2022

Journal title :

Biochimica et Biophysica Acta. Bioenergetics

ISSN :

0005-2728

eISSN :

1879-2650

Publisher :

Elsevier B.V., Netherlands

Volume :

1863

Issue :

Pages :

148569

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S000527282200038X?httpAccept=text/xml

Funding text :

The authors are grateful to Dr. Mauro Degli Esposti (CGG, UNAM) for critically reading the manuscript, and acknowledge the technical expertise of Q.B.P. Miriam Vázquez-Acevedo and Dr. José Luis Santillán Torres (IFC, UNAM) in our ongoing research. H.M.-A.´s research is supported by grant IA204122 ( PAPIIT , DGAPA, UNAM ). P.C. acknowledges financial support from the Belgian Fonds de la Recherche Scientifique FRS- FNRS ( PDR T.0032 ). PC is Senior Research Associate from FNRS. D.G.-H. acknowledges the financial support from grant 21856 (Frontiers of Science, CONACyT , Mexico) and IN209220 (PAPIIT, DGAPA, UNAM ). M. O.-C. is a Ph.D. student at Programa de Maestría y Doctorado en Ciencias Bioquímicas (UNAM) and recipient of a CONACyT fellowship ( 710287 ).

Available on ORBi :

since 12 January 2023

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Bibliography

Muench, S.P., Trinick, J., Harrison, M.A., Structural Divergence of the Rotary ATPases. 2011, 10.1017/S0033583510000338.
Wächter, A., Bi, Y., Dunn, S.D., Cain, B.D., Sielaff, H., Wintermann, F., Engelbrecht, S., Junge, W., Two rotary motors in F-ATP synthase are elastically coupled by a flexible rotor and a stiff stator stalk. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 3924–3929, 10.1073/pnas.1011581108.
Stock, D., Gibbons, C., Arechaga, I., Leslie, A.G.W., Walker, J.E., The rotary mechanism of ATP-synthase. Curr. Opin. Struct. Biol. 10 (2000), 672–679, 10.1016/j.abb.2008.05.004.
Grüber, G., Wieczorek, H., Harvey, W.R., Müller, V., Structure – function relationships of A-, F- and V-ATPases. J. Exp. Biol. 204 (2001), 2597–2605.
Nishi, T., Forgac, M., The vacuolar (H+)-Atpases — nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3 (2002), 94–103, 10.1038/nrm729.
Boyer, P.D., A perspective of the binding change mechanism for ATP synthesis. FASEB J. 3 (1989), 2164–2178, 10.1096/fj.1530-6860.
Kühlbrandt, W., Davies, K.M., Rotary ATPases: a new twist to an ancient machine. Trends Biochem. Sci. 41 (2016), 106–116, 10.1016/j.tibs.2015.10.006.
Iwabe, N., Kuma, K.-I., Hasegawa, M., Osawa, S., Source, T.M., Hasegawat, M., Osawat, S., Miyata, T., Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Natl. Acad. Sci. U. S. A. 86 (1989), 9355–9359 http://www.jstor.org/stable/35080.
Wieczorek, H., Grber, G., Harvey, W.R., Huss, M., Merzendorfer, H., Zeiske, W., Structure and regulation of insect plasma membrane H(+)V-ATPase. J. Exp. Biol. 203 (2000), 127–135.
Colina-Tenorio, L., Dautant, A., Miranda-Astudillo, H., Giraud, M.-F., González-Halphen, D., The peripheral stalk of rotary ATPases. Front. Physiol. 9 (2018), 1–19, 10.3389/fphys.2018.01243.
Cross, R.L., Müller, V., The evolution of A-, F-, and V-type ATP synthases and ATPases: reversals in function and changes in the H+/ATP coupling ratio. FEBS Lett. 576 (2004), 1–4, 10.1016/j.febslet.2004.08.065.
Cross, R.L., Taiz, L., Gene duplication as a means for altering H+/ATP ratios during the evolution of fo F1 ATPases and synthases. FEBS Lett. 259 (1990), 227–229, 10.1016/0014-5793(90)80014-A.
Gogarten, J.P., Kibak, H., Dittrich, P., Taiz, L., Bowman, E.J., Bowman, B.J., Manolson, M.F., Poole, R.J., Date, T., Oshima, T., Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc. Natl. Acad. Sci. U. S. A. 86 (1989), 6661–6665, 10.1073/pnas.86.17.6661.
Hilario, E., Gogarten, J.P., Horizontal transfer of ATPase genes - the tree of life becomes a net of life. Biosystems 31 (1993), 111–119.
Lapierre, P., Shial, R., Gogarten, J.P., Distribution of F- and A/V-type ATPases in Thermus scotoductus and other closely related species. Syst. Appl. Microbiol. 29 (2006), 15–23, 10.1016/j.syapm.2005.06.004.
Forterre, P., Benachenhou-Lahfa, N., Confalonieri, F., Duguet, M., Elie, C., Labedan, B., The nature of the last universal ancestor and the root of the tree of life, still open questions. Biosystems 28 (1992), 15–32, 10.1016/0303-2647(92)90004-I.
Burki, F., Roger, A.J., Brown, M.W., Simpson, A.G.B., The new tree of eukaryotes. Trends Ecol. Evol. 35 (2020), 43–55, 10.1016/j.tree.2019.08.008.
Keeling, P.J., Burki, F., Progress towards the tree of eukaryotes. Curr. Biol. 29 (2019), R808–R817, 10.1016/j.cub.2019.07.031.
Keeling, P.J., Slamovits, C.H., Causes and effects of nuclear genome reduction. Curr. Opin. Genet. Dev. 15 (2005), 601–608, 10.1016/j.gde.2005.09.003.
Corradi, N., Pombert, J.F., Farinelli, L., Didier, E.S., Keeling, P.J., The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat. Commun., 1, 2010, 10.1038/ncomms1082.
Margulis, L., The origin of plant and animal cells. Am. Sci. 59 (1971), 230–235.
Leister, D., Origin, evolution and genetic effects of nuclear insertions of organelle DNA. Trends Genet. 21 (2005), 655–663, 10.1016/j.tig.2005.09.004.
Archibald, J.M., The puzzle of plastid evolution. Curr. Biol. 19 (2009), R81–R88, 10.1016/j.cub.2008.11.067.
Maruyama, S., Kim, E., Evolution of photosynthetic eukaryotes; current opinion, perplexity, and a new perspective. Results Probl. Cell Differ. 69 (2020), 337–351, 10.1007/978-3-030-51849-3_12.
Boyer, P.D., The ATP synthase–a splendid molecular machine. Annu. Rev. Biochem. 66 (1997), 717–749, 10.1146/annurev.biochem.66.1.717.
Junge, W., Protons, proteins and ATP. Photosynth. Res. 80 (2004), 197–221, 10.1023/B:PRES.0000030677.98474.74.
Pedersen, P.L., The machine that makes ATP. Curr. Biol. 4 (1994), 1138–1141.
Walker, J.E., The ATP synthase: the understood, the uncertain and the unknown. Biochim. Biophys. Acta - Bioenerg., 1817, 2012, S1, 10.1016/j.bbabio.2012.06.013.
Walker, J.E., Collinson, I.R., The role of the stalk in the coupling mechanism of F1F0-ATPases. FEBS Lett. 346 (1994), 39–43, 10.1016/0014-5793(94)00368-8.
Yoshida, M., Muneyuki, E., Hisabori, T., ATP synthase–a marvellous rotary engine of the cell. Nat. Rev. Mol. Cell Biol. 2 (2001), 669–677, 10.1038/35089509.
Sobti, M., Walshe, J.L., Wu, D., Ishmukhametov, R., Zeng, Y.C., Robinson, C.V., Berry, R.M., Stewart, A.G., Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch. Nat. Commun. 11 (2020), 1–10, 10.1038/s41467-020-16387-2.
Morales-Rios, E., Montgomery, M.G., Leslie, A.G.W., Walker, J.E., Structure of ATP synthase from Paracoccus denitrificans determined by X-ray crystallography at 4.0 Å resolution. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 13231–13236, 10.1073/pnas.1517542112.
Guo, H., Suzuki, T., Rubinstein, J.L., Structure of a bacterial atp synthase. elife 8 (2019), 1–17, 10.7554/eLife.43128.
Montgomery, M.G., Petri, J., Spikes, T.E., Walker, J.E., Structure of the ATP synthase from mycobacterium smegmatis provides targets for treating tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 118 (2021), 1–9, 10.1073/pnas.2111899118.
Hahn, A., Vonck, J., Mills, D.J., Meier, T., Kühlbrandt, W., Structure, mechanism, and regulation of the chloroplast ATP synthase. Science, 360, 2018, eaat4318, 10.1126/science.aat4318.
Hahn, A., Parey, K., Bublitz, M., Mills, D.J., Zickermann, V., Vonck, J., Kühlbrandt, W., Meier, T., Structure of a complete ATP synthase dimer reveals the molecular basis of inner mitochondrial membrane morphology. Mol. Cell 63 (2016), 445–456, 10.1016/j.molcel.2016.05.037.
Guo, H., Bueler, S.A., Rubinstein, J.L., Atomic model for the dimeric Fo region of mitochondrial ATP synthase. Science 358 (2017), 936–940, 10.1126/science.aao4815.
Vinothkumar, K.R., Montgomery, M.G., Liu, S., Walker, J.E., Structure of the mitochondrial ATP synthase from Pichia angusta determined by electron cryo-microscopy. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 12709–12714, 10.1073/pnas.1615902113.
Zhou, A., Rohou, A., Schep, D.G., Bason, J.V., Montgomery, M.G., Walker, J.E., Grigorieff, N., Rubinstein, J.L., Structure and conformational states of the bovine mitochondrial ATP synthase by cryo-EM. elife 4 (2015), 1–15, 10.7554/eLife.10180.
Spikes, T.E., Montgomery, M.G., Walker, J.E., Structure of the dimeric ATP synthase from bovine mitochondria. Proc. Natl. Acad. Sci. U. S. A. 117 (2020), 23519–23526, 10.1073/pnas.2013998117.
Gu, J., Zhang, L., Zong, S., Guo, R., Liu, T., Yi, J., Wang, P., Zhuo, W., Yang, M., Cryo-EM structure of the mammalian ATP synthase tetramer bound with inhibitory protein IF1. Science 364 (2019), 1068–1075, 10.1126/science.aaw4852.
Murphy, B.J., Klusch, N., Langer, J., Mills, D.J., Yildiz, Ö., Kühlbrandt, W., Rotary substates of mitochondrial ATP synthase reveal the basis of flexible F 1 -F. Science, 364, 2019, 10.1126/science.aaw9128.
Vázquez-Acevedo, M., Vega-deLuna, F., Sánchez-Vásquez, L., Colina-Tenorio, L., Remacle, C., Cardol, P., Miranda-Astudillo, H., González-Halphen, D., Dissecting the peripheral stalk of the mitochondrial ATP synthase of chlorophycean algae. Biochim. Biophys. Acta - Bioenerg. 2016 (1857), 1183–1190, 10.1016/j.bbabio.2016.02.003.
Flygaard, R.K., Mühleip, A., Tobiasson, V., Amunts, A., Type III ATP synthase is a symmetry-deviated dimer that induces membrane curvature through tetramerization. Nat. Commun., 11, 2020, 10.1038/s41467-020-18993-6.
Balabaskaran Nina, P., Dudkina, N.V., Kane, L.A., van Eyk, J.E., Boekema, E.J., Mather, M.W., Vaidya, A.B., Highly divergent mitochondrial ATP synthase complexes in Tetrahymena thermophila. PLoS Biol. 8 (2010), 3–6, 10.1371/journal.pbio.1000418.
Mühleip, A.W., Joos, F., Wigge, C., Frangakis, A.S., Kühlbrandt, W., Davies, K.M., Helical arrays of U-shaped ATP synthase dimers form tubular cristae in ciliate mitochondria. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 8442–8447, 10.1073/pnas.1525430113.
Mühleip, A., Kock Flygaard, R., Ovciarikova, J., Lacombe, A., Fernandes, P., Sheiner, L., Amunts, A., ATP synthase hexamer assemblies shape cristae of Toxoplasma mitochondria. Nat. Commun., 12, 2021, 10.1038/s41467-020-20381-z.
Zíková, A., Schnaufer, A., Dalley, R.A., Panigrahi, A.K., Stuart, K.D., The F0F1-ATP synthase complex contains novel subunits and is essential for procyclic Trypanosoma brucei. PLoS Pathog., 5, 2009, e1000436, 10.1371/journal.ppat.1000436.
Gahura, O., Mühleip, A., Hierro-Yap, C., Panicucci, B., Jain, M., Hollaus, D., Slapničková, M., Zíková, A., Amunts, A., An Ancestral Interaction Module Promotes Oligomerization in Divergent Mitochondrial ATP Synthases. 2021, BioRxiv, 10.1101/2021.10.10.463820 2021.10.10.463820.
Mühleip, A., McComas, S.E., Amunts, A., Structure of a mitochondrial ATP synthase with bound native cardiolipin. elife 8 (2019), 1–23, 10.7554/eLife.51179.
Yadav, K.N.S., Miranda-Astudillo, H.V., Colina-Tenorio, L., Bouillenne, F., Degand, H., Morsomme, P., González-Halphen, D., Boekema, E.J., Cardol, P., Atypical composition and structure of the mitochondrial dimeric ATP synthase from Euglena gracilis. Biochim. Biophys. Acta - Bioenerg. 2017 (1858), 267–275, 10.1016/j.bbabio.2017.01.007.
Dittrich, M., Schulten, K., Zooming in on ATP hydrolysis in F1. J. Bioenerg. Biomembr. 37 (2005), 441–444, 10.1007/s10863-005-9487-7.
Cheuk, A., Meier, T., Rotor subunits adaptations in ATP synthases from photosynthetic organisms. Biochem. Soc. Trans. 49 (2021), 541–550, 10.1042/BST20190936.
Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R.A., Schägger, H., Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J. 17 (1998), 7170–7178, 10.1093/emboj/17.24.7170.
Wagner, K., Rehling, P., Szklarz, L.K.Sanjuán, Taylor, R.D., Pfanner, N., van der Laan, M., Mitochondrial F1Fo-ATP synthase: the small subunits e and g associate with monomeric complexes to trigger dimerization. J. Mol. Biol. 392 (2009), 855–861, 10.1016/j.jmb.2009.07.059.
Kühlbrandt, W., Structure and mechanisms of F-type ATP synthases. Annu. Rev. Biochem., 88, 2019, 10.1146/annurev-biochem-013118-110903.
Atteia, A., Dreyfus, G., González-Halphen, D., Characterization of the alpha and beta-subunits of the F0F1-ATPase from the alga Polytomella spp., a colorless relative of Chlamydomonas reinhardtii. Biochim. Biophys. Acta - Bioenerg. 1320 (1997), 275–284, 10.1016/S0005-2728(97)00031-5.
van Lis, R., Atteia, A., Mendoza-hernández, G., González-halphen, D., Identification of novel mitochondrial protein components of Chlamydomonas reinhardtii. A proteomic approach 1. Plant Physiol. 132 (2003), 318–330, 10.1104/pp.102.018325.proteins.
Villavicencio-Queijeiro, A., Vázquez-Acevedo, M., Cano-Estrada, A., Zarco-Zavala, M., Tuena De Gómez, M., Mignaco, J.A., Freire, M.M., Scofano, H.M., Foguel, D., Cardol, P., Remacle, C., González-Halphen, D., The fully-active and structurally-stable form of the mitochondrial ATP synthase of Polytomella sp. is dimeric. J. Bioenerg. Biomembr. 41 (2009), 1–13, 10.1007/s10863-009-9203-0.
Lapaille, M., Escobar-Ramírez, A., Degand, H., Baurain, D., Rodríguez-Salinas, E., Coosemans, N., Boutry, M., Gonzalez-Halphen, D., Remacle, C., Cardol, P., Atypical subunit composition of the chlorophycean mitochondrial F 1FO-ATP synthase and role of asa7 protein in stability and oligomycin resistance of the enzyme. Mol. Biol. Evol. 27 (2010), 1630–1644, 10.1093/molbev/msq049.
Allegretti, M., Klusch, N., Mills, D.J., Vonck, J., Kühlbrandt, W., Davies, K.M., Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase. Nature 521 (2015), 237–240, 10.1038/nature14185.
Colina-Tenorio, L., Miranda-Astudillo, H., Dautant, A., Vázquez-Acevedo, M., Giraud, M.-F., González-Halphen, D., Subunit Asa3 ensures the attachment of the peripheral stalk to the membrane sector of the dimeric ATP synthase of Polytomella sp. Biochem. Biophys. Res. Commun. 509 (2019), 341–347, 10.1016/j.bbrc.2018.12.142.
Miranda-Astudillo, H., Colina-Tenorio, L., Jiménez-Suárez, A., Vázquez-Acevedo, M., Salin, B., Giraud, M.-F., Remacle, C., Cardol, P., González-Halphen, D., Oxidative phosphorylation supercomplexes and respirasome reconstitution of the colorless alga Polytomella sp. Biochim. Biophys. Acta - Bioenerg. 1859 (2018), 434–444, 10.1016/j.bbabio.2018.03.004.
Röhricht, H., Schwartzmann, J., Meyer, E.H., Complexome profiling reveals novel insights into the composition and assembly of the mitochondrial ATP synthase of Arabidopsis thaliana. Biochim. Biophys. Acta - Bioenerg., 1862, 2021, 10.1016/j.bbabio.2021.148425.
Perez, E., Lapaille, M., Degand, H., Cilibrasi, L., Villavicencio-Queijeiro, A., Morsomme, P., González-Halphen, D., Field, M.C., Remacle, C., Baurain, D., Cardol, P., The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae. Mitochondrion 19 (2014), 338–349, 10.1016/j.mito.2014.02.001.
Mühleip, A.W., Dewar, C.E., Schnaufer, A., Kühlbrandt, W., Davies, K.M., In-situ structure of trypanosomal ATP synthase dimer reveals unique arrangement of catalytic subunits. PNAS, 2017, 10.1073/pnas.1612386114.
Miranda-Astudillo, H.V., Yadav, K.N.S., Boekema, E.J., Cardol, P., Supramolecular associations between atypical oxidative phosphorylation complexes of Euglena gracilis. J. Bioenerg. Biomembr., 2021, 10.1007/s10863-021-09882-8.
Funes, S., Davidson, E., Gonzalo Claros, M., Van Lis, R., Pérez-Martínez, X., Vázquez-Acevedo, M., King, M.P., González-Halphen, D., The typically mitochondrial DNA-encoded ATP6 subunit of the F1F0-ATPase is encoded by a nuclear gene in Chlamydomonas reinhardtii. J. Biol. Chem. 277 (2002), 6051–6058, 10.1074/jbc.M109993200.
Ariga, T., Muneyuki, E., Yoshida, M., F1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits. Nat. Struct. Mol. Biol. 14 (2007), 841–846, 10.1038/nsmb1296.
Zarco-Zavala, M., Watanabe, R., McMillan, D.G.G., Suzuki, T., Ueno, H., Mendoza-Hoffmann, F., García-Trejo, J.J., Noji, H., The 3 × 120° rotary mechanism of Paracoccus denitrificans F1-ATPase is different from that of the bacterial and mitochondrial F1-ATPases. Proc. Natl. Acad. Sci. U. S. A. 117 (2020), 29647–29657, 10.1073/pnas.2003163117.
Noji, H., Ueno, H., Kobayashi, R., Correlation between the numbers of rotation steps in the ATPase and proton-conducting domains of F- and V-ATPases. Biophys. Rev. 12 (2020), 303–307, 10.1007/s12551-020-00668-7.
Zarco-Zavala, M., Mendoza-Hoffmann, F., García-Trejo, J.J., Unidirectional regulation of the F 1 F O -ATP synthase nanomotor by the ζ pawl-ratchet inhibitor protein of paracoccus denitrificans and related α-proteobacteria. Biochim. Biophys. Acta - Bioenerg. 2018 (1859), 762–774, 10.1016/j.bbabio.2018.06.005.
Miranda-Astudillo, H., Zarco-Zavala, M., García-Trejo, J.J., González-Halphen, D., Regulation of bacterial ATP synthase activity: a gear-shifting or a pawl–ratchet mechanism?. FEBS J. 288 (2021), 3159–3163, 10.1111/febs.15671.
Davies, K.M., Strauss, M., Daum, B., Kief, J.H., Osiewacz, H.D., Rycovska, A., Zickermann, V., Kuhlbrandt, W., Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc. Natl. Acad. Sci. 108 (2011), 14121–14126, 10.1073/pnas.1103621108.
Blum, T.B., Hahn, A., Meier, T., Davies, K.M., Kühlbrandt, W., Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows. Proc. Natl. Acad. Sci. 116 (2019), 4250–4255, 10.1073/pnas.1816556116.
Khosravi, S., Harner, M.E., The MICOS complex, a structural element of mitochondria with versatile functions. Biol. Chem. 401 (2020), 765–778, 10.1515/hsz-2020-0103.
Muñoz-Gómez, S.A., Slamovits, C.H., Dacks, J.B., Wideman, J.G., The evolution of MICOS: ancestral and derived functions and interactions. Commun.Integr. Biol. 8 (2015), 1–5, 10.1080/19420889.2015.1094593.
Huynen, M.A., Mühlmeister, M., Gotthardt, K., Guerrero-Castillo, S., Brandt, U., Evolution and structural organization of the mitochondrial contact site (MICOS) complex and the mitochondrial intermembrane space bridging (MIB) complex. Biochim. Biophys. Acta - Mol. Cell Res. 2016 (1863), 91–101, 10.1016/j.bbamcr.2015.10.009.
Pfanner, N., van der Laan, M., Amati, P., Capaldi, R.A., Caudy, A.A., Chacinska, A., Darshi, M., Deckers, M., Hoppins, S., Icho, T., Jakobs, S., Ji, J., Kozjak-Pavlovic, V., Meisinger, C., Odgren, P.R., Park, S.K., Rehling, P., Reichert, A.S., Sheikh, M.S., Taylor, S.S., Tsuchida, N., van der Bliek, A.M., van der Klei, I.J., Weissman, J.S., Westermann, B., Zha, J., Neupert, W., Nunnari, J., Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J. Cell Biol. 204 (2014), 1083–1086, 10.1083/jcb.201401006.
Harner, M., Körner, C., Walther, D., Mokranjac, D., Kaesmacher, J., Welsch, U., Griffith, J., Mann, M., Reggiori, F., Neupert, W., The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J. 30 (2011), 4356–4370, 10.1038/emboj.2011.379.
Wideman, J.G., Muñoz-Gómez, S.A., Cell biology: functional conservation, structural divergence, and surprising convergence in the MICOS complex of trypanosomes. Curr. Biol. 28 (2018), R1245–R1248, 10.1016/j.cub.2018.09.057.
Rampelt, H., Bohnert, M., Zerbes, R.M., Horvath, S.E., Warscheid, B., Pfanner, N., van der Laan, M., Mic10, a core subunit of the mitochondrial contact site and cristae organizing system, interacts with the dimeric F1Fo-ATP synthase. J. Mol. Biol. 429 (2017), 1162–1170, 10.1016/j.jmb.2017.03.006.
Eydt, K., Davies, K.M., Behrendt, C., Wittig, I., Reichert, A.S., Cristae architecture is determined by an interplay of the MICOS complex and the F1Fo ATP synthase via Mic27 and Mic10. Microb.Cell 4 (2017), 259–272, 10.15698/mic2017.08.585.
Cadena, L.R., Gahura, O., Panicucci, B., Zíková, A., Hashimi, H., Mitochondrial contact site and cristae organization system and F 1 F O -ATP synthase crosstalk is a fundamental property of mitochondrial cristae. MSphere, 6, 2021, 10.1128/msphere.00327-21.
Rampelt, H., Wollweber, F., Licheva, M., de Boer, R., Perschil, I., Steidle, L., Becker, T., Bohnert, M., van der Klei, I., Kraft, C., van der Laan, M., Pfanner, N., Dual role of Mic10 in mitochondrial cristae organization and ATP synthase-linked metabolic adaptation and respiratory growth. Cell Rep., 38, 2022, 110290, 10.1016/j.celrep.2021.110290.
Muñoz-Gómez, S.A., Slamovits, C.H., Dacks, J.B., Baier, K.A., Spencer, K.D., Wideman, J.G., Ancient homology of the mitochondrial contact site and cristae organizing system points to an endosymbiotic origin of mitochondrial cristae. Curr. Biol. 25 (2015), 1489–1495, 10.1016/j.cub.2015.04.006.
Fernández-Morán, H., Oda, T., Blair, P.V., Green, D.E., A macromolecular repeating unit of mitochondrial structure and function: correlated electron microscopic and biochemical studies of isolated mitochondria and submitochondrial particles of beef heart muscle. J. Cell Biol. 22 (1964), 63–100, 10.1083/jcb.22.1.63.
Allen, R.D., Schroeder, C.C., Fok, A.K., An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J. Cell Biol. 108 (1989), 2233–2240, 10.1083/jcb.108.6.2233.
Dudkina, N.V., Sunderhaus, S., Braun, H.P., Boekema, E.J., Characterization of dimeric ATP synthase and cristae membrane ultrastructure from Saccharomyces and Polytomella mitochondria. FEBS Lett. 580 (2006), 3427–3432, 10.1016/j.febslet.2006.04.097.
Nicastro, D., Frangakis, A.S., Typke, D., Baumeister, W., Cryo-electron tomography of Neurospora mitochondria. J. Struct. Biol. 129 (2000), 48–56, 10.1006/jsbi.1999.4204.
Schägger, H., Pfeiffer, K., Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19 (2000), 1777–1783, 10.1093/emboj/19.8.1777.
Buzhynskyy, N., Sens, P., Prima, V., Sturgis, J.N., Scheuring, S., Rows of ATP synthase dimers in native mitochondrial inner membranes. Biophys. J. 93 (2007), 2870–2876, 10.1529/biophysj.107.109728.
Wittig, I., Schägger, H., Supramolecular organization of ATP synthase and respiratory chain in mitochondrial membranes. Biochim. Biophys. Acta 1787 (2009), 672–680, 10.1016/j.bbabio.2008.12.016.
Vonck, J., Schäfer, E., Supramolecular organization of protein complexes in the mitochondrial inner membrane. Biochim. Biophys. Acta 1793 (2009), 117–124, 10.1016/j.bbamcr.2008.05.019.
Paumard, P., Vaillier, J., Coulary, B., Schaeffer, J., Soubannier, V., Mueller, D.M., Brèthes, D., Di Rago, J.P., Velours, J., The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21 (2002), 221–230, 10.1093/emboj/21.3.221.
Giraud, M.F., Paumard, P., Soubannier, V., Vaillier, J., Arselin, G., Salin, B., Schaeffer, J., Brèthes, D., Di Rago, J.P., Velours, J., Is there a relationship between the supramolecular organization of the mitochondrial ATP synthase and the formation of cristae?. Biochim. Biophys. Acta - Bioenerg. 1555 (2002), 174–180, 10.1016/S0005-2728(02)00274-8.
Thomas, D., Bron, P., Weimann, T., Dautant, A., Giraud, M.-F., Paumard, P., Salin, B., Cavalier, A., Velours, J., Brèthes, D., Supramolecular organization of the yeast F1Fo-ATP synthase. Biol. Cell. 100 (2008), 591–601, 10.1042/BC20080022.
Strauss, M., Hofhaus, G., Schröder, R.R., Kühlbrandt, W., Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 27 (2008), 1154–1160, 10.1038/emboj.2008.35.
Allen, R.D., Membrane tubulation and proton pumps. Protoplasma 189 (1995), 1–8, 10.1007/BF01280286.
Bornhövd, C., Vogel, F., Neupert, W., Reichert, A.S., Mitochondrial membrane potential is dependent on the oligomeric state of F1F0-ATP synthase supracomplexes. J. Biol. Chem. 281 (2006), 13990–13998, 10.1074/jbc.M512334200.
Anselmi, C., Davies, K.M., Gómez, J.D.F., Mitochondrial ATP synthase dimers spontaneously associate due to a long-range membrane-induced force. J. Gen. Physiol. 150 (2018), 763–770.
Davies, K.M., Anselmi, C., Wittig, I., Faraldo-Gomez, J.D., Kuhlbrandt, W., Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. 109 (2012), 13602–13607, 10.1073/pnas.1204593109.
Arselin, G., Vaillier, J., Salin, B., Schaeffer, J., Giraud, M.F., Dautant, A., Brèthes, D., Velours, J., The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology. J. Biol. Chem. 279 (2004), 40392–40399, 10.1074/jbc.M404316200.
Gavin, P.D., Prescott, M., Luff, S.E., Devenish, R.J., Cross-linking ATP synthase complexes in vivo eliminates mitochondrial cristae. J. Cell Sci. 117 (2004), 2333–2343, 10.1242/jcs.01074.
Goyon, V., Fronzes, R., Salin, B., Di-Rago, J.P., Velours, J., Brèthes, D., Yeast cells depleted in Atp14p fail to assemble Atp6p within the ATP synthase and exhibit altered mitochondrial cristae morphology. J. Biol. Chem. 283 (2008), 9749–9758, 10.1074/jbc.M800204200.
Russ, W.P., Engelman, D.M., The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296 (2000), 911–919, 10.1006/jmbi.1999.3489.
Arselin, G., Giraud, M.F., Dautant, A., Vaillier, J., Brèthes, D., Coulary-Salin, B., Schaeffer, J., Velours, J., The GxxxG motif of the transmembrane domain of subunit e is involved in the dimerization/oligomerization of the yeast ATP synthase complex in the mitochondrial membrane. Eur. J. Biochem. 270 (2003), 1875–1884, 10.1046/j.1432-1033.2003.03557.x.
Bazán, S., Mileykovskaya, E., Mallampalli, V.K.P.S., Heacock, P., Sparagna, G.C., Dowhan, W., Cardiolipin-dependent reconstitution of respiratory supercomplexes from purified Saccharomyces cerevisiae complexes III and IV. J. Biol. Chem. 288 (2013), 401–411, 10.1074/jbc.M112.425876.
Pfeiffer, K., Gohil, V., Stuart, R.A., Hunte, C., Brandt, U., Greenberg, M.L., Schägger, H., Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278 (2003), 52873–52880, 10.1074/jbc.M308366200.
Gupta, K., Donlan, J.A.C., Hopper, J.T.S., Uzdavinys, P., Landreh, M., Struwe, W.B., Drew, D., Baldwin, A.J., Stansfeld, P.J., Robinson, C.V., The role of interfacial lipids in stabilizing membrane protein oligomers. Nature 541 (2017), 421–424, 10.1038/nature20820.
Chaban, Y., Boekema, E.J., Dudkina, N.V., Structures of mitochondrial oxidative phosphorylation supercomplexes and mechanisms for their stabilisation. Biochim. Biophys. Acta - Bioenerg. 2014 (1837), 418–426, 10.1016/j.bbabio.2013.10.004.
Genova, M.L., Lenaz, G., Functional role of mitochondrial respiratory supercomplexes. Biochim. Biophys. Acta 1837 (2014), 427–443, 10.1016/j.bbabio.2013.11.002.
Letts, J.A., Fiedorczuk, K., Sazanov, L.A., The architecture of respiratory supercomplexes. Nature 537 (2016), 644–648, 10.1038/nature19774.
Lobo-Jarne, T., Ugalde, C., Respiratory chain supercomplexes: structures, function and biogenesis. Semin. Cell Dev. Biol. 76 (2018), 179–190, 10.1016/j.semcdb.2017.07.021.
Lenaz, G., Tioli, G., Falasca, A.I., Genova, M.L., Complex i function in mitochondrial supercomplexes. Biochim. Biophys. Acta - Bioenerg. 2016 (1857), 991–1000, 10.1016/j.bbabio.2016.01.013.
Milenkovic, D., Blaza, J.N., Larsson, N.G., Hirst, J., The enigma of the respiratory chain supercomplex. Cell Metab. 25 (2017), 765–776, 10.1016/j.cmet.2017.03.009.
Acin-Perez, R., Enriquez, J.A., The function of the respiratory supercomplexes: the plasticity model. Biochim. Biophys. Acta - Bioenerg. 2014 (1837), 444–450, 10.1016/j.bbabio.2013.12.009.
Winge, D.R., Sealing the mitochondrial respirasome. Mol. Cell. Biol. 32 (2012), 2647–2652, 10.1128/MCB.00573-12.
Reyes-Galindo, M., Suarez, R., Esparza-Perusquía, M., de Lira-Sánchez, J., Pardo, J.P., Martínez, F., Flores-Herrera, O., Mitochondrial respirasome works as a single unit and the cross-talk between complexes I, III2 and IV stimulates NADH dehydrogenase activity. Biochim. Biophys. Acta - Bioenerg. 2019 (1860), 618–627, 10.1016/j.bbabio.2019.06.017.
Berndtsson, J., Aufschnaiter, A., Rathore, S., Marin-Buera, L., Dawitz, H., Diessl, J., Kohler, V., Barrientos, A., Büttner, S., Fontanesi, F., Ott, M., Respiratory supercomplexes enhance electron transport by decreasing cytochrome c diffusion distance. EMBO Rep. 21 (2020), 1–13, 10.15252/embr.202051015.
Stroh, A., Anderka, O., Pfeiffer, K., Yagi, T., Finel, M., Ludwig, B., Schägger, H., Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans. J. Biol. Chem. 279 (2004), 5000–5007, 10.1074/jbc.M309505200.
Franco, L.V.R., Su, C.H., Tzagoloff, A., Modular assembly of yeast mitochondrial ATP synthase and cytochrome oxidase. Biol. Chem. 401 (2020), 835–853, 10.1515/hsz-2020-0112.
Azuma, K., Ikeda, K., Inoue, S., Functional mechanisms of mitochondrial respiratory chain supercomplex assembly factors and their involvement in muscle quality. Int. J. Mol. Sci. 21 (2020), 1–17, 10.3390/ijms21093182.
Bultema, J.B., Braun, H.P., Boekema, E.J., Kouril, R., Megacomplex organization of the oxidative phosphorylation system by structural analysis of respiratory supercomplexes from potato. Biochim. Biophys. Acta - Bioenerg. 1787 (2009), 60–67, 10.1016/j.bbabio.2008.10.010.
Nubel, E., Wittig, I., Kerscher, S., Brandt, U., Schägger, H., Two-dimensional native electrophoretic analysis of respiratory supercomplexes from Yarrowia lipolytica. Proteomics 9 (2009), 2408–2418, 10.1002/pmic.200800632.
Strecker, V., Wumaier, Z., Wittig, I., Schägger, H., Large pore gels to separate mega protein complexes larger than 10MDa by blue native electrophoresis: isolation of putative respiratory strings or patches. Proteomics 10 (2010), 3379–3387, 10.1002/pmic.201000343.
Seelert, H., Dencher, N.A., ATP synthase superassemblies in animals and plants: two or more are better. Biochim. Biophys. Acta - Bioenerg. 2011 (1807), 1185–1197, 10.1016/j.bbabio.2011.05.023.
Nesterov, S., Chesnokov, Y., Kamyshinsky, R., Panteleeva, A., Lyamzaev, K., Vasilov, R., Yaguzhinsky, L., Ordered clusters of the complete oxidative phosphorylation system in cardiac mitochondria. Int. J. Mol. Sci. 22 (2021), 1–10, 10.3390/ijms22031462.
Ukolova, I., Kondakova, M., Kondratov, I., Sidorov, A., Borovskii, G., Voinikov, V., New insights into the organisation of the oxidative phosphorylation system in the example of pea shoot mitochondria. Biochim. Biophys. Acta - Bioenerg., 1861, 2020, 148264, 10.1016/j.bbabio.2020.148264.
Tsukihara, T., Aoyama, H., Tomizaki, T., Yamashita, E., Takashi, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., Yoshikawa, S., The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272 (1996), 1136–1144.
Hartley, A.M., Lukoyanova, N., Zhang, Y., Cabrera-Orefice, A., Arnold, S., Meunier, B., Pinotsis, N., Maréchal, A., Structure of yeast cytochrome c oxidase in a supercomplex with cytochrome bc 1. Nat. Struct. Mol. Biol. 26 (2019), 78–83, 10.1038/s41594-018-0172-z.
Kadenbach, B., Complex IV – the regulatory center of mitochondrial oxidative phosphorylation. Mitochondrion 58 (2021), 296–302, 10.1016/j.mito.2020.10.004.
Zhou, L., Sazanov, L.A., Structure and conformational plasticity of the intact Thermus thermophilus V/A-type ATPase. Science, 2019, 365, 10.1126/science.aaw9144.
Wang, R., Long, T., Hassan, A., Wang, J., Sun, Y., Xie, X.S., Li, X., Cryo-EM structures of intact V-ATPase from bovine brain. Nat. Commun. 11 (2020), 1–9, 10.1038/s41467-020-17762-9.
Sehnal, D., Bittrich, S., Deshpande, M., Svobodová, R., Berka, K., Bazgier, V., Velankar, S., Burley, S.K., Koča, J., Rose, A.S., Mol∗Viewer: modern web app for 3D visualization and analysis of large biomolecular structures. Nucleic Acids Res. 49 (2021), W431–W437, 10.1093/nar/gkab314.
Guo, H., Bueler, S.A., Rubinstein, J.L., Atomic model for the dimeric Fo región of mitochondrial ATP synthase. Science 358 (2017), 936–940, 10.1126/science.aao4815.