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Cited by 5ATP Synthase and ATPases ResearchPhotosynthetic Processes and MechanismsEnzyme Structure and Function

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I-Shaped Dimers of a Plant Chloroplast FOF1-ATP Synthase in Response to Changes in Ionic Strength

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Osipov, Stepan D., Ryzhykau, Yury L., Zinovev, Egor V., Minaeva, Andronika V., Ivashchenko, Sergey D., Verteletskiy, Dmitry P., Sudarev, Vsevolod V., Kuklina, Daria D., Nikolaev, Mikhail Yu., Semenov, Yury S., Zagryadskaya, Yuliya A., Okhrimenko, Ivan S., Gette, Margarita S., Dronova, Elizaveta A., Shishkin, Aleksei Yu., Dencher, Norbert A., Kuklin, Alexander I., Ivanovich, Valentin, Uversky, Vladimir N., Vlasov, Alexey V.·2023·International Journal of Molecular Sciences
DOI 10.3390/ijms241310720PMC PMC10341776

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Abstract

F-type ATP synthases play a key role in oxidative and photophosphorylation processes generating adenosine triphosphate (ATP) for most biochemical reactions in living organisms. In contrast to the mitochondrial FOF1-ATP synthases, those of chloroplasts are known to be mostly monomers with approx. 15% fraction of oligomers interacting presumably non-specifically in a thylakoid membrane. To shed light on the nature of this difference we studied interactions of the chloroplast ATP synthases using small-angle X-ray scattering (SAXS) method. Here, we report evidence of I-shaped dimerization of solubilized FOF1-ATP synthases from spinach chloroplasts at different ionic strengths. The structural data were obtained by SAXS and demonstrated dimerization in response to ionic strength. The best model describing SAXS data was two ATP-synthases connected through F1/F1′ parts, presumably via their δ-subunits, forming “I” shape dimers. Such I-shaped dimers might possibly connect the neighboring lamellae in thylakoid stacks assuming that the FOF1 monomers comprising such dimers are embedded in parallel opposing stacked thylakoid membrane areas. If this type of dimerization exists in nature, it might be one of the pathways of inhibition of chloroplast FOF1-ATP synthase for preventing ATP hydrolysis in the dark, when ionic strength in plant chloroplasts is rising. Together with a redox switch inserted into a γ-subunit of chloroplast FOF1 and lateral oligomerization, an I-shaped dimerization might comprise a subtle regulatory process of ATP synthesis and stabilize the structure of thylakoid stacks in chloroplasts.

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Research works printed but not linked: 66

  1. Vlasov, 2022, ATP synthase FOF1 structure, function, and structure-based drug design, Cell. Mol. Life Sci., 79, 179, 10.1007/s00018-022-04153-0 · DOI
  2. 2019, Structure and Mechanisms of F-Type ATP Synthases, Annu. Rev. Biochem., 88, 515, 10.1146/annurev-biochem-013118-110903 · DOI
  3. Daum, 2010, Arrangement of Photosystem II and ATP Synthase in Chloroplast Membranes of Spinach and Pea, Plant Cell, 22, 1299, 10.1105/tpc.109.071431 · DOI
  4. Rexroth, 2004, Dimeric H+-ATP synthase in the chloroplast of Chlamydomonas reinhardtii, Biochim. Biophys. Acta Bioenerg., 1658, 202, 10.1016/j.bbabio.2004.05.014 · DOI
  5. Rexroth, 2007, Metabolism controls dimerization of the chloroplast FoF1ATP synthase in Chlamydomonas reinhardtii, FEBS Lett., 581, 1391, 10.1016/j.febslet.2007.02.057 · DOI
  6. Seelert, 2011, ATP synthase superassemblies in animals and plants: Two or more are better, Biochim. Biophys. Acta Bioenerg., 1807, 1185, 10.1016/j.bbabio.2011.05.023 · DOI
  7. Robinson, 1984, Potassium, sodium, and chloride content of isolated intact chloroplasts in relation to ionic compartmentation in leaves, Arch. Biochem. Biophys., 228, 197, 10.1016/0003-9861(84)90061-4 · DOI
  8. Chow, 1976, Light-dependent Redistribution of Ions in Isolated Spinach Chloroplasts, Funct. Plant Biol., 3, 853, 10.1071/PP9760853 · DOI
  9. Nobel, 1969, Light-induced changes in the ionic content of chloroplasts in Pisum sativum, Biochim. Biophys. Acta (BBA) Bioenerg., 172, 134, 10.1016/0005-2728(69)90098-X · DOI
  10. Ryzhykau, 2021, Molecular model of a sensor of two-component signaling system, Sci. Rep., 11, 10774, 10.1038/s41598-021-89613-6 · DOI
  11. Ryzhykau, 2021, Ambiguities in and completeness of SAS data analysis of membrane proteins: The case of the sensory rhodopsin II–transducer complex, Acta Crystallogr. Sect. D Struct. Biol., 77, 1386, 10.1107/S2059798321009542 · DOI
  12. Vlasov, 2019, Unusual features of the c-ring of F1FO ATP synthases, Sci. Rep., 9, 18547, 10.1038/s41598-019-55092-z · DOI
  13. Balakrishna, 2014, Crystallographic structure of the turbine C-ring from spinach chloroplast F-ATP synthase, Biosci. Rep., 34, e00102, 10.1042/BSR20130114 · DOI
  14. Hahn, 2018, Structure, mechanism, and regulation of the chloroplast ATP synthase, Science, 360, eaat4318, 10.1126/science.aat4318 · DOI
  15. Koutsioubas, 2015, Memprot: A program to model the detergent corona around a membrane protein based on SEC–SAXS data, Acta Crystallogr. D Biol. Crystallogr., 71, 86, 10.1107/S1399004714016678 · DOI
  16. Glatter, 1982, General Theory, Small-Angle X-ray Scatt., 36, 17
  17. Yan, 2020, The HDOCK server for integrated protein–protein docking, Nat. Protoc., 15, 1829, 10.1038/s41596-020-0312-x · DOI
  18. Krissinel, 2007, Inference of Macromolecular Assemblies from Crystalline State, J. Mol. Biol., 372, 774, 10.1016/j.jmb.2007.05.022 · DOI
  19. Minges, 2020, Structure and supramolecular architecture of chloroplast ATP synthase, Adv. Bot. Res., 96, 27, 10.1016/bs.abr.2020.07.004 · DOI
  20. Molodenskiy, 2021, MPBuilder: A PyMOL Plugin for Building and Refinement of Solubilized Membrane Proteins Against Small Angle X-ray Scattering Data, J. Mol. Biol., 433, 166888, 10.1016/j.jmb.2021.166888 · DOI
  21. Disfani, 2012, MoRFpred, a computational tool for sequence-based prediction and characterization of short disorder-to-order transitioning binding regions in proteins, Bioinformatics, 28, i75, 10.1093/bioinformatics/bts209 · DOI
  22. Cheng, 2007, Mining α-Helix-Forming Molecular Recognition Features with Cross Species Sequence Alignments, Biochemistry, 46, 13468, 10.1021/bi7012273 · DOI
  23. Oldfield, 2005, Coupled Folding and Binding with α-Helix-Forming Molecular Recognition Elements, Biochemistry, 44, 12454, 10.1021/bi050736e · DOI
  24. Garner, 1999, Predicting Binding Regions within Disordered Proteins, Genome Inf. Ser. Workshop Genome Inf., 10, 41
  25. DeForte, 2016, Resolving the ambiguity: Making sense of intrinsic disorder when PDB structures disagree, Protein Sci., 25, 676, 10.1002/pro.2864 · DOI
  26. Romero, 2007, Intrinsic Disorder in the Protein Data Bank, J. Biomol. Struct. Dyn., 24, 325, 10.1080/07391102.2007.10507123 · DOI
  27. Varadi, 2022, AlphaFold Protein Structure Database: Massively expanding the structural coverage of protein-sequence space with high-accuracy models, Nucleic Acids Res., 50, D439, 10.1093/nar/gkab1061 · DOI · Paper page
  28. Romero, 2001, Sequence Complexity of Disordered Protein, Proteins, 42, 38, 10.1002/1097-0134(20010101)42:1<38::AID-PROT50>3.0.CO;2-3 · DOI
  29. Peng, K., Radivojac, P., Vucetic, S., Dunker, A.K., and Obradovic, Z. (2006). Length-dependent prediction of protein intrinsic disorder. BMC Bioinform., 7. · DOI
  30. Peng, 2005, Optimizing long intrinsic disorder predictors with protein evolutionary information, J. Bioinform. Comput. Biol., 3, 35, 10.1142/S0219720005000886 · DOI
  31. Xue, 2010, PONDR-FIT: A meta-predictor of intrinsically disordered amino acids, Biochim. Biophys. Acta, 1804, 996, 10.1016/j.bbapap.2010.01.011 · DOI
  32. 2018, IUPred2A: Context-dependent prediction of protein disorder as a function of redox state and protein binding, Nucleic Acids Res., 46, W329, 10.1093/nar/gky384 · DOI
  33. Hu, 2021, flDPnn: Accurate intrinsic disorder prediction with putative propensities of disorder functions, Nat. Commun., 12, 4438, 10.1038/s41467-021-24773-7 · DOI
  34. Dayhoff, 2022, Rapid prediction and analysis of protein intrinsic disorder, Protein Sci., 31, e4496, 10.1002/pro.4496 · DOI
  35. Caffrey, 2009, Crystallizing membrane proteins using lipidic mesophases, Nat. Protoc., 4, 706, 10.1038/nprot.2009.31 · DOI
  36. Faham, 2002, Bicelle crystallization: A new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure, J. Mol. Biol., 316, 1, 10.1006/jmbi.2001.5295 · DOI
  37. Murugova, 2022, Mechanisms of membrane protein crystallization in ‘bicelles’, Sci. Rep., 12, 11109, 10.1038/s41598-022-13945-0 · DOI
  38. Morgan, 2014, Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP, Nat. Struct. Mol. Biol., 21, 489, 10.1038/nsmb.2803 · DOI
  39. Noinaj, 2013, Structural insight into the biogenesis of β-barrel membrane proteins, Nature, 501, 385, 10.1038/nature12521 · DOI
  40. Lin, 2015, Crystal structures of a polypeptide processing and secretion transporter, Nature, 523, 425, 10.1038/nature14623 · DOI
  41. Stock, 1999, Molecular Architecture of the Rotary Motor in ATP Synthase, Science, 286, 1700, 10.1126/science.286.5445.1700 · DOI · Paper page
  42. Dautant, 2010, Crystal Structure of the Mg·ADP-inhibited State of the Yeast F1c10-ATP Synthase, J. Biol. Chem., 285, 29502, 10.1074/jbc.M110.124529 · DOI
  43. Watt, 2010, Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria, Proc. Natl. Acad. Sci. USA, 107, 16823, 10.1073/pnas.1011099107 · DOI · Paper page
  44. Giraud, 2012, Rotor architecture in the yeast and bovine F1-c-ring complexes of F-ATP synthase, J. Struct. Biol., 177, 490, 10.1016/j.jsb.2011.10.015 · DOI
  45. Montgomery, 2015, Structure of ATP synthase from Paracoccus denitrificans determined by X-ray crystallography at 4.0 Å resolution, Proc. Natl. Acad. Sci. USA, 112, 13231, 10.1073/pnas.1517542112 · DOI
  46. Hahn, 2016, Structure of a Complete ATP Synthase Dimer Reveals the Molecular Basis of Inner Mitochondrial Membrane Morphology, Mol. Cell, 63, 445, 10.1016/j.molcel.2016.05.037 · DOI
  47. Zabelskii, 2018, Ambiguities and completeness of SAS data analysis: Investigations of apoferritin by SAXS/SANS EID and SEC-SAXS methods, J. Phys. Conf. Ser., 994, 012017, 10.1088/1742-6596/994/1/012017 · DOI
  48. 2000, The structure of the H+-ATP synthase from chloroplasts and its subcomplexes as revealed by electron microscopy, Biochim. Biophys. Acta Bioenerg., 1458, 404, 10.1016/S0005-2728(00)00090-6 · DOI
  49. Vlasov, 2017, Photo-Voltage of Highly-Oriented Bacteriorhodopsin in Purple Membranes: Possibilities for Bio Solar Cells, Optoelectron. Adv. Mater. Rapid Commun., 11, 65
  50. Engel, 2015, Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography, eLife, 4, e04889, 10.7554/eLife.04889 · DOI
  51. 1991, Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form, Anal. Biochem., 199, 223, 10.1016/0003-2697(91)90094-A · DOI
  52. Hartwig, 2016, Oxygen and differentiation status modulate the effect of X-ray irradiation on physiology and mitochondrial proteome of human neuroblastoma cells, Arch. Physiol. Biochem., 122, 257, 10.1080/13813455.2016.1218518 · DOI
  53. Kuklin, 2021, Small-Angle Neutron Scattering at the Pulsed Reactor IBR-2: Current Status and Prospects, Crystallogr. Rep., 66, 231, 10.1134/S1063774521020085 · DOI
  54. Kuklin, 2005, Scientific Reviews: Two-Detector System for Small-Angle Neutron Scattering Instrument, Neutron News, 16, 16, 10.1080/10448630500454361 · DOI
  55. Kuklin, 2011, New opportunities provided by modernized small-angle neutron scattering two-detector system instrument (YuMO), J. Phys. Conf. Ser., 291, 012013, 10.1088/1742-6596/291/1/012013 · DOI
  56. Covington, 1968, Use of the glass electrode in deuterium oxide and the relation between the standardized pD (paD) scale and the operational pH in heavy water, Anal. Chem., 40, 700, 10.1021/ac60260a013 · DOI
  57. Tsoraev, 2022, Anti-Stokes fluorescence excitation reveals conformational mobility of the C-phycocyanin chromophores, Struct. Dyn., 9, 054701, 10.1063/4.0000164 · DOI
  58. Soloviov, 2012, Silver behenate and silver stearate powders for calibration of SAS instruments, J. Phys. Conf. Ser., 351, 012024, 10.1088/1742-6596/351/1/012024 · DOI
  59. Soloviev, 2017, SAS program for two-detector system: Seamless curve from both detectors, J. Phys. Conf. Ser., 848, 012020, 10.1088/1742-6596/848/1/012020 · DOI
  60. Konarev, 2021, ATSAS 3.0: Expanded functionality and new tools for small-angle scattering data analysis, J. Appl. Crystallogr., 54, 343, 10.1107/S1600576720013412 · DOI
  61. Franke, 2017, ATSAS 2.8: A comprehensive data analysis suite for small-angle scattering from macromolecular solutions, J. Appl. Crystallogr., 50, 1212, 10.1107/S1600576717007786 · DOI
  62. DeLano, 2002, Pymol: An Open-Source Molecular Graphics Tool, CCP4 Newsl. Protein Crystallogr., 40, 82
  63. Lomize, 2012, OPM database and PPM web server: Resources for positioning of proteins in membranes, Nucleic Acids Res., 40, D370, 10.1093/nar/gkr703 · DOI
  64. Konarev, 2003, PRIMUS: A Windows PC-based system for small-angle scattering data analysis, J. Appl. Crystallogr., 36, 1277, 10.1107/S0021889803012779 · DOI
  65. Svergun, 1992, Determination of the regularization parameter in indirect-transform methods using perceptual criteria, J. Appl. Crystallogr., 25, 495, 10.1107/S0021889892001663 · DOI
  66. Clote, 2005, DiANNA: A web server for disulfide connectivity prediction, Nucleic Acids Res., 33, W230, 10.1093/nar/gki412 · DOI

Metadata

Authors
Osipov, S. D., Ryzhykau, Y. L., Zinovev, E. V., Minaeva, A. V., Ivashchenko, S. D., Verteletskiy, D. P., Sudarev, V. V., Kuklina, D. D., Nikolaev, M. Y., Semenov, Y. S., Zagryadskaya, Y. A., Okhrimenko, I. S., Gette, M. S., Dronova, E. A., Shishkin, A. Y., Dencher, N. A., Kuklin, A. I., Ivanovich, V., Uversky, V. N., & Vlasov, A. V.
Affiliations
  • Moscow Institute of Physics and Technology (RU)
  • University of South Florida (US)
Corresponding author
Uversky, Vladimir N.
ORCID
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2023-06-27
Volume
24
Issue
13
Pages
10720
ISSN
1422-0067 (ISSN-L)
DOI
10.3390/ijms241310720
PMC
PMC10341776
OpenAlex
W4382582818
Cited by
5
References
2
Citations by year
2025: 1 · 2024: 2 · 2023: 2
FWCI
0.44
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Molecular Sciences (publishedVersion, cc-by)
  • Preprints.org (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Russian Science Foundation (RSF) (22-74-00044, FSMG-2021-0002, 075-03-2023-106, 075-15-2021-1354)
  • Ministry of Science and Higher Education of the Russian Federation (22-74-00044, FSMG-2021-0002, 075-03-2023-106, 075-15-2021-1354)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
Keywords
oligomerization, ionic strength, thylakoid membranes, spinach chloroplasts, delta subunit, redox switch, thylakoid stacking, small-angle X-ray scattering
MeSH terms
Adenosine Triphosphate, Chloroplasts, Proton-Translocating ATPases, Polymers, X-Ray Diffraction, Nitric Oxide Synthase, Scattering, Small Angle

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