Cardiolipin-based respiratory complex activation in bacteria
Open accessAbstract
Anionic lipids play a variety of key roles in membrane function, including functional and structural effects on respiratory complexes. However, little is known about the molecular basis of these lipid–protein interactions. In this study, NarGHI, an anaerobic respiratory complex of Escherichia coli , has been used to investigate the relations in between membrane-bound proteins with phospholipids. Activity of the NarGHI complex is enhanced by anionic phospholipids both in vivo and in vitro. The anionic cardiolipin tightly associates with the NarGHI complex and is the most effective phospholipid to restore functionality of a nearly inactive detergent-solubilized enzyme complex. A specific cardiolipin-binding site is identified on the basis of the available X-ray diffraction data and of site-directed mutagenesis experiment. One acyl chain of cardiolipin is in close proximity to the heme b D center and is responsible for structural adjustments of b D and of the adjacent quinol substrate binding site. Finally, cardiolipin binding tunes the interaction with the quinol substrate. Together, our results provide a molecular basis for the activation of a bacterial respiratory complex by cardiolipin.
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Translated NapD is a dedicated chaperone protein with a defined role in NapA maturation.
“Translated NapD is a dedicated chaperone protein as it has a defined role in NapA maturation.263”
From Nitrate and periplasmic nitrate reductases (2014) · cites this paper as [263]
Cites
A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/o59-099 · Cited by 54,751 · see citing works
<i>Coot</i> : model-building tools for molecular graphics
Emsley, P., & Cowtan, K. (2004) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444904019158 · Cited by 30,571 · see citing works
A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/y59-099 · Cited by 23,189 · see citing works
Refinement of Macromolecular Structures by the Maximum-Likelihood Method
Murshudov, G. N., Vagin, A. A., & Dodson, E. J. (1997) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444996012255 · Cited by 14,671 · see citing works
MOLECULAR BASIS FOR MEMBRANE PHOSPHOLIPID DIVERSITY: Why Are There So Many Lipids?
Dowhan, W. (1997) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.66.1.199 · Cited by 1,007 · see citing works
Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside
Pebay‐Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trézéguet, V., Lauquin, G. J. ‐., & Brandolin, G. (2003) · Nature · doi:10.1038/nature02056 · Cited by 998 · see citing works
Architecture of succinate dehydrogenase and reactive oxygen species generation
Yankovskaya, V., Horsefield, R., Törnroth, S., Luna-Chavez, C., Miyoshi, H., Léger, C., Byrne, B., Cecchini, G., & Iwata, S. (2003) · Science · doi:10.1126/science.1079605 · Cited by 927 · cited 2× · see citing works
“In particular, cardiolipin, which consists of two phosphatidyl residues linked by a glycerol moiety, has been observed at the interface of adjacent monomers in the dimeric succinate dehydrogenase (19) or in the trimeric formate dehydrogenase N (FdnGHI) (20).”
BackgroundMolecular Basis of Proton Motive Force Generation: Structure of Formate Dehydrogenase-N
Jormakka, M., Törnroth‐Horsefield, S., Byrne, B., & Iwata, S. (2002) · Science · doi:10.1126/science.1068186 · Cited by 502 · see citing works
Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A
Bertero, M. G., Rothery, R. A., Palak, M., Hou, C., Lim, D., Blasco, F., Weiner, J. H., & Strynadka, N. C. J. (2003) · Nature Structural & Molecular Biology · doi:10.1038/nsb969 · Cited by 494 · see citing works
Specific roles of protein–phospholipid interactions in the yeast cytochrome bc1 complex structure
Lange, C. M., Nett, J. H., Trumpower, B. L., & Hunte, C. (2001) · The EMBO Journal · doi:10.1093/emboj/20.23.6591 · Cited by 444 · see citing works
Mileykovskaya, E., & Dowhan, W. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.4.1172-1175.2000 · Cited by 434 · see citing works
Mitochondrial Respiratory Chain Supercomplexes Are Destabilized in Barth Syndrome Patients
McKenzie, M., Lazarou, M., Thorburn, D. R., & Ryan, M. T. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.06.057 · Cited by 426 · see citing works
Lipids in membrane protein structures
Pálsdóttir, H., & Hunte, C. (2004) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2004.06.012 · Cited by 424 · see citing works
Fry, M., & Green, D. E. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)69888-1 · Cited by 405 · see citing works
Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase
Shinzawa‐Itoh, K., Aoyama, H., Muramoto, K., Terada, H., Kurauchi, T., Tadehara, Y., Yamasaki, A., Sügimura, T., Kurono, S., Tsujimoto, K., et al. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601618 · Cited by 378 · see citing works
Jones, R. W., & Garland, P. B. (1977) · Biochemical Journal · doi:10.1042/bj1640199 · Cited by 268 · see citing works
Lipid-Dependent Membrane Protein Topogenesis
Dowhan, W., & Bogdanov, M. V. (2009) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.77.060806.091251 · Cited by 265 · see citing works
The role of cardiolipin in the structural organization of mitochondrial membranes
Schlame, M., & Ren, M. (2009) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2009.04.019 · Cited by 248 · see citing works
DeChavigny, A., Heacock, P. N., & Dowhan, W. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)67791-4 · Cited by 238 · see citing works
Structural details of an interaction between cardiolipin and an integral membrane protein
McAuley, K. E., Fyfe, P. K., Ridge, J. P., Isaacs, N. W., Cogdell, R. J., & Jones, M. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.14706 · Cited by 236 · see citing works
Brandner, K., Mick, D. U., Frazier, A. E., Taylor, R. D., Meisinger, C., & Rehling, P. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-03-0256 · Cited by 209 · see citing works
Lipids and membrane protein structures
Hunte, C., & Richers, S. (2008) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2008.03.008 · Cited by 196 · see citing works
Sharpley, M. S., Shannon, R. J., Draghi, F., & Hirst, J. (2005) · Biochemistry · doi:10.1021/bi051809x · Cited by 193 · see citing works
Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli
Romantsov, T., Helbig, S., Culham, D. E., Gill, C., Stalker, L., & Wood, J. M. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05727.x · Cited by 177 · see citing works
Effects of Phospholipid Composition on MinD-Membrane Interactions in Vitro and in Vivo
Mileykovskaya, E., Fishov, I., Fu, X., Corbin, B. D., Margolin, W., & Dowhan, W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302603200 · Cited by 175 · see citing works
The action of cardiolipin on the bacterial translocon.
Gold, V. A. M., Robson, A., Bao, H., Romantsov, T., Duong, F., & Collinson, I. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914680107 · Cited by 168 · see citing works
Cellular functions of cardiolipin in yeast
Joshi, A., Zhou, J., Gohil, V. M., Chen, S., & Greenberg, M. L. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.07.024 · Cited by 157 · see citing works
Phospholipid modifications in bacteria
Cronan, J. E. (2002) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(02)00297-7 · Cited by 156 · see citing works
Role of phospholipids in respiratory cytochrome bc1 complex catalysis and supercomplex formation
Wenz, T., Hielscher, R., Hellwig, P., Schägger, H., Richers, S., & Hunte, C. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.02.012 · Cited by 154 · see citing works
Bogdanov, M. V., Mileykovskaya, E., & Dowhan, W. (2008) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-1-4020-8831-5_8 · Cited by 141 · see citing works
Yung, B. Y., & Kornberg, A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.19.7202 · Cited by 137 · see citing works
Short, S. A., & White, D. C. S. (1971) · Journal of Bacteriology · doi:10.1128/jb.108.1.219-226.1971 · Cited by 131 · see citing works
Koch, H.-G., Renate, H. A. A. S., & Fischer, W. (1984) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1984.tb07923.x · Cited by 130 · see citing works
The coordination and function of the redox centres of the membrane-bound nitrate reductases
Blasco, F., Guigliarelli, B., Magalon, A., Asso, M., Giordano, G., & Rothery, R. A. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000846 · Cited by 113 · see citing works
Self-citationBooth, P. J., & Curran, A. R. (1999) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(99)80015-3 · Cited by 96 · see citing works
Phospholipid specificity of bovine heart bc1 complex
Schägger, H., HAGEN, T., Brigitte, R. O. T. H., Brandt, U., Link, T. A., & von JAGOW, G. (1990) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1990.tb15554.x · Cited by 96 · see citing works
Cardiolipin in energy transducing membranes
Mileykovskaya, E., Zhang, M., & Dowhan, W. (2005) · Biochemistry (Moscow) · doi:10.1007/s10541-005-0095-2 · Cited by 94 · see citing works
Bertero, M. G., Rothery, R. A., Boroumand, N., Palak, M., Blasco, F., Ginet, N., Weiner, J. H., & Strynadka, N. C. J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m410457200 · Cited by 88 · see citing works
Dröse, S., Zwicker, K., & Brandt, U. (2002) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(02)00307-9 · Cited by 76 · see citing works
Richardson, D. J., & Sawers, R. G. (2002) · Science · doi:10.1126/science.1070366 · Cited by 71 · see citing works
The role of lipids in membrane insertion and translocation of bacterial proteins
van Dalen, A., & KRUIJFF, B. D. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2004.03.007 · Cited by 70 · see citing works
Biogenesis of a Respiratory Complex Is Orchestrated by a Single Accessory Protein
Lanciano, P., Vergnes, A., Grimaldi, S., Guigliarelli, B., & Magalon, A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700994200 · Cited by 66 · see citing works
Self-citationNeosynthesis of Cardiolipin in Rhodobacter sphaeroides under Osmotic Stress
Catucci, L., Depalo, N., Lattanzio, V. M. T., Agostiano, A., & Corcelli, A. (2004) · Biochemistry · doi:10.1021/bi048802k · Cited by 55 · see citing works
Mikhaleva, N. I., Santini, C., Giordano, G., Nesmeyanova, M. A., & Wu, L. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01661-0 · Cited by 51 · see citing works
Self-citationIs There a Conserved Interaction between Cardiolipin and the Type II Bacterial Reaction Center?
Wakeham, M. C., Sessions, R. B., Jones, M. R., & Fyfe, P. K. (2001) · Biophysical Journal · doi:10.1016/s0006-3495(01)76112-7 · Cited by 46 · see citing works
Berry, E. A., & Walker, F. A. (2008) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-008-0372-9 · Cited by 44 · see citing works
Lanciano, P., Savoyant, A., Grimaldi, S., Magalon, A., Guigliarelli, B., & Bertrand, P. (2007) · The Journal of Physical Chemistry B · doi:10.1021/jp075243t · Cited by 37 · see citing works
Self-citationMore, C., Belle, V., Asso, M., Fournel, A., Roger, G., Guigliarelli, B., & Bertrand, P. (1999) · Biospectroscopy · doi:10.1002/(sici)1520-6343(1999)5:5+ · Cited by 36 · see citing works
Self-citationGrimaldi, S., Arias-Cartín, R., Lanciano, P., Lyubenova, S., Endeward, B., Prisner, T. F., Magalon, A., & Guigliarelli, B. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.060251 · Cited by 36 · see citing works
Self-citationGiordani, R., Buc, J., Cornish-Bowden, A. J., & Cárdenas, M. L. (1997) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1997.0567a.x · Cited by 34 · see citing works
Lanciano, P., Magalon, A., Bertrand, P., Guigliarelli, B., & Grimaldi, S. (2007) · Biochemistry · doi:10.1021/bi700074y · Cited by 34 · see citing works
Self-citationHielscher, R., Wenz, T., Hunte, C., & Hellwig, P. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.01.006 · Cited by 33 · see citing works
Genetic regulation of cardiolipin synthase in Escherichia coli
Heber, S., & Tropp, B. E. (1991) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/0167-4781(91)90206-2 · Cited by 31 · see citing works
Grimaldi, S., Lanciano, P., Bertrand, P., Blasco, F., & Guigliarelli, B. (2004) · Biochemistry · doi:10.1021/bi048009r · Cited by 30 · see citing works
Self-citationvan Gestel, R. A., Rijken, P. J., Šurinová, S., O’Flaherty, M. C., Heck, A. J. R., Killian, J. A., de Kroon, A. I. P. M., & Slijper, M. (2009) · Journal of Proteomics · doi:10.1016/j.jprot.2009.11.009 · Cited by 29 · see citing works
Arias-Cartín, R., Lyubenova, S., Ceccaldi, P., Prisner, T. F., Magalon, A., Guigliarelli, B., & Grimaldi, S. (2010) · Journal of the American Chemical Society · doi:10.1021/ja1009234 · Cited by 23 · see citing works
Self-citationRoszak, A. W., Gardiner, A. T., Isaacs, N. W., & Cogdell, R. J. (2007) · Biochemistry · doi:10.1021/bi062154i · Cited by 19 · see citing works
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Sparacino-Watkins, C., Stolz, J. F., & Basu, P. (2014) · Chem. Soc. Rev. · doi:10.1039/c3cs60249d · Cited by 426 · see citing works
Tan, B. K., Bogdanov, M. V., Zhao, J., Dowhan, W., Raetz, C. R. H., & Guan, Z. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1212797109 · Cited by 249 · see citing works
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Evidence for Cardiolipin Binding Sites on the Membrane-Exposed Surface of the Cytochrome bc 1
Arnarez, C., Mazat, J., Elezgaray, J., Marrink, . J., & Périole, X. (2013) · Journal of the American Chemical Society · doi:10.1021/ja310577u · Cited by 162 · see citing works
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Self-citationThe stability and activity of respiratory Complex II is cardiolipin-dependent
Schwall, C. T., Greenwood, V., & Alder, N. N. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.04.015 · Cited by 127 · see citing works
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Cardiolipin binding in bacterial respiratory complexes: Structural and functional implications
Arias-Cartin, R., Grimaldi, S., Arnoux, P., Guigliarelli, B., & Magalon, A. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.04.005 · Cited by 117 · see citing works
Self-citationThe lipid basis of cell death and autophagy
Lin, Z., Long, F., Kang, R., Klionsky, D. J., Yang, M., & Tang, D. (2023) · Autophagy · doi:10.1080/15548627.2023.2259732 · Cited by 106 · see citing works
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Wang, X., Dong, H., Zeng, Q., Xia, Q., Zhang, L., & Zhou, Z. (2017) · Environmental Science & Technology · doi:10.1021/acs.est.7b00726 · Cited by 99 · see citing works
Chen, W., Chao, Y.-J., Chang, W.-H., Chan, J.-F., & Hsu, Y. (2018) · Scientific Reports · doi:10.1038/s41598-018-23190-z · Cited by 77 · see citing works
Different Modes of Lipid Binding to Membrane Proteins Probed by Mass Spectrometry
Bechara, C., & Robinson, C. V. (2015) · Journal of the American Chemical Society · doi:10.1021/jacs.5b00420 · Cited by 70 · see citing works
Subramani, S., Perdreau‐Dahl, H., & Morth, J. P. (2016) · eLife · doi:10.7554/elife.11407 · Cited by 59 · see citing works
Saxena, R., Fingland, N., Patil, D., Sharma, A., & Crooke, E. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14048517 · Cited by 54 · see citing works
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Douglass, M. V., Cléon, F., & Trent, M. S. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2018329118 · Cited by 50 · see citing works
Tian, H., Feng, J.-M., & Wen, J. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-32 · Cited by 49 · see citing works
Distribution and dynamics of OXPHOS complexes in the bacterial cytoplasmic membrane
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Self-citationDiscovery of a bifunctional cardiolipin/phosphatidylethanolamine synthase in bacteria
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Studying Biomolecule Localization by Engineering Bacterial Cell Wall Curvature
Renner, L. D., Eswara, P. J., Ramamurthi, K. S., & Weibel, D. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0084143 · Cited by 35 · see citing works
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Self-citationRcs Phosphorelay Activation in Cardiolipin-Deficient Escherichia coli Reduces Biofilm Formation
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Ma, Y., Guo, C., Li, H., & Peng, X. (2013) · Journal of Proteomics · doi:10.1016/j.jprot.2013.05.019 · Cited by 27 · see citing works
Swain, J., Khoury, M. E., Kempf, J., Briée, F., Smissen, P. V. D., Décout, J., & Mingeot‐Leclercq, M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201752 · Cited by 27 · see citing works
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Noguchi, F., Tanifuji, G., Brown, M. W., Fujikura, K., & Takishita, K. (2016) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2016.05.011 · Cited by 23 · see citing works
Chan, C. S., Bay, D. C., Leach, T., Winstone, T. M. L., Kuzniatsova, L., Tran, V. A., & Turner, R. J. (2014) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2014.08.020 · Cited by 22 · see citing works
Makowski, M., Felício, M. R., Fensterseifer, I. C. M., Franco, O. L., Santos, N. C., & Gonçalves, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239104 · Cited by 22 · see citing works
Exterkate, M., de Kok, N. A. W., Andringa, R. L. H., Wolbert, N. H. J., Minnaard, A. J., & Driessen, A. J. M. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100691 · Cited by 22 · see citing works
Nathoo, S., Litzenberger, J. K., Bay, D. C., Turner, R. J., & Prenner, E. J. (2013) · Chemistry and Physics of Lipids · doi:10.1016/j.chemphyslip.2013.01.007 · Cited by 21 · see citing works
Rendon, J., Pilet, E., Fahs, Z., Seduk, F., Sylvi, L., Chehade, M. H., Pierrel, F., Guigliarelli, B., Magalon, A., & Grimaldi, S. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.05.001 · Cited by 21 · see citing works
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Bulot, S., Audebert, S., Pieulle, L., Seduk, F., Baudelet, É., Espinosa, L., Pizay, M.-C., Camoin, L., & Magalon, A. (2019) · mBio · doi:10.1128/mbio.01832-19 · Cited by 21 · see citing works
Self-citationRoger, M., de Poulpiquet, A., Ciaccafava, A., Ilbert, M., Guiral, M., Giudici‐Orticoni, M., & Lojou, É. (2013) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-013-7465-1 · Cited by 20 · see citing works
Grimaldi, S., Arias-Cartín, R., Lanciano, P., Lyubenova, S., Szenes, R., Endeward, B., Prisner, T. F., Guigliarelli, B., & Magalon, A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.325100 · Cited by 20 · see citing works
Self-citationBian, J., Zhao, J., Zhang, Z., Liu, D., Lan, X., Liao, Y., An, X., Lu, D., Liang, M., Liu, R., et al. (2025) · Journal of the American Chemical Society · doi:10.1021/jacs.5c07315 · Cited by 19 · see citing works
Oxidative stress in ageing and disease development studied by FT-IR spectroscopy
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Schlattner, U., Tokarska-Schlattner, M., Epand, R. M., Boissan, M., Lacombe, M., Klein‐Seetharaman, J., & Kagan, V. E. (2014) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-014-1047-4 · Cited by 17 · see citing works
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Morales‐Ríos, E., Watt, I. N., Zhang, Q., Ding, S., Fearnley, I. M., Montgomery, M. G., Wakelam, M. J. O., & Walker, J. E. (2015) · Open Biology · doi:10.1098/rsob.150119 · Cited by 17 · see citing works
Cardiolipin deficiency causes a dissociation of the b 6 c:caa 3 megacomplex in B. subtilis membranes
de, L. Y. J. G. M., Cabellos-Avelar, T., Garrido, G. I. P., Chagoya-López, A., de la Vara, L. E. G., Delgado‐Buenrostro, N. L., Chirino, Y. I., Gómez‐Lojero, C., & Gutiérrez-Cirlos, E. B. (2016) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-016-9671-y · Cited by 15 · see citing works
Relationship between cardiolipin metabolism and oxygen availability in Bacillus subtilis
Lobasso, S., Palese, L. L., Angelini, R., & Corcelli, A. (2013) · FEBS Open Bio · doi:10.1016/j.fob.2013.02.002 · Cited by 14 · see citing works
Bacterial Electron Transfer Chains Primed by Proteomics
Wessels, H. J. C. T., de Almeida, N. M., Kartal, B., & Keltjens, J. T. (2016) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2016.02.006 · Cited by 14 · see citing works
Caliskan, M., Poschmann, G., Gudzuhn, M., Waldera-Lupa, D. M., Molitor, R., Strunk, C. H., Streit, W. R., Jaeger, K., Stühler, K., & Kovačić, F. (2023) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2023.159317 · Cited by 12 · see citing works
Asseri, A. H., Godoy-Hernández, A., Goojani, H. G., Lill, H., Sakamoto, J., McMillan, D. G. G., & Bald, D. (2021) · Scientific Reports · doi:10.1038/s41598-021-87354-0 · Cited by 11 · see citing works
Promiscuous phospholipid biosynthesis enzymes in the plant pathogen Pseudomonas syringae
Vasilopoulos, G., Moser, R., Petersen, J., Aktas, M., & Narberhaus, F. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2021.158926 · Cited by 10 · see citing works
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Fedor, J. G., Rothery, R. A., & Weiner, J. H. (2014) · Biochemistry · doi:10.1021/bi500394m · Cited by 9 · see citing works
Villanueva, J. A., Crooks, A. L., Nagy, T. A., Quintana, J. L. J., Dalebroux, Z. D., & Detweiler, C. S. (2022) · mBio · doi:10.1128/mbio.01790-22 · Cited by 8 · see citing works
Catucci, L., Leo, V. D., Milano, F., Giotta, L., Vitale, R., Agostiano, A., & Corcelli, A. (2012) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-012-9447-y · Cited by 8 · see citing works
Interaction of Terminal Oxidases with Amphipathic Molecules
Azarkina, N. V., Borisov, V. B., Oleynikov, I. P., Sudakov, R. V., & Vygodina, T. V. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076428 · Cited by 7 · see citing works
Bacterial Iron Homeostasis Regulation by sRNAs
Chareyre, S., & Mandin, P. (2018) · ASM Press eBooks · doi:10.1128/9781683670247.ch16 · Cited by 7 · see citing works
Fiorentino, F., Cervoni, M., Wang, Y., Urner, L. H., Sauer, J. B., Tran, T. A., Corey, R. A., Rotili, D., Mai, A., Stansfeld, P. J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-66182-0 · Cited by 6 · see citing works
Q-Site Occupancy Defines Heme Heterogeneity in Escherichia coli Nitrate Reductase A (NarGHI)
Fedor, J. G., Rothery, R. A., Giraldi, K. S., & Weiner, J. H. (2014) · Biochemistry · doi:10.1021/bi500121x · Cited by 6 · see citing works
Makowski, M., Almendro‐Vedia, V. G., Domingues, M. M., Franco, O. L., López‐Montero, I., Melo, M. N., & Santos, N. C. (2023) · iScience · doi:10.1016/j.isci.2023.107004 · Cited by 5 · see citing works
Liu, L., Li, A., Shi, C., Hrynsphan, D., Savitskaya, T., Wang, Z., & Chen, J. (2024) · Critical Reviews in Environmental Science and Technology · doi:10.1080/10643389.2024.2333716 · Cited by 4 · see citing works
Kristensen, S. S., Lukassen, M. V., Siebenhaar, S., Diep, D. B., Morth, J. P., & Mathiesen, G. (2023) · Scientific Reports · doi:10.1038/s41598-023-41559-7 · Cited by 3 · see citing works
Herrera, C. M., Demey, L. M., Ellison, C. K., & Trent, M. S. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2524588123 · Cited by 3 · see citing works
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Calisto, F., Todorović, S., Louro, R. O., & Pereira, M. M. (2023) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2023.148983 · Cited by 3 · see citing works
A splendid molecular factory: De- and reconstruction of the mammalian respiratory chain
Rimle, L., Phillips, B. P., Barra, I. M. C. C., Arnold, N., Hennebert, C., Meier, T. W., & von Ballmoos, C. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2416162122 · Cited by 3 · see citing works
Kovačić, F., & Batra, R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-22222-1.00019-2 · Cited by 2 · see citing works
Aerobic denitrification with an electrode as the sole electron and energy source
Simón, C. N. R., Pedetta, A., Busalmen, J. P., & Bonanni, P. S. (2023) · Environmental Science Water Research & Technology · doi:10.1039/d3ew00600j · Cited by 2 · see citing works
Anand, P., & Akhter, Y. (2026) · Journal of Cellular Biochemistry · doi:10.1002/jcb.70095 · Cited by 1 · see citing works
Heo, K., Jung, D.-J., Yoo, J., Goh, B., Kasper, D. L., & Oh, S. F. (2026) · Cell · doi:10.1016/j.cell.2026.08.011 · Cited by 1 · see citing works
Sawasato, K., & Bogdanov, M. V. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2024.159483 · Cited by 1 · see citing works
Membrane-bound respiratory nitrate reductase functioning: It takes two to tango
Arias-Cartín, R., Grimaldi, S., Lanciano, P., Arnoux, P., Guigliarelli, B., & Magalon, A. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.06.337 · Cited by 1 · see citing works
Self-citationMikulovich, Y. L., Sorokoumova, G. M., Селищева, А. А., & Швец, В. И. (2016) · Fine Chemical Technologies · doi:10.32362/2410-6593-2016-11-3-64-73 · Cited by 1 · see citing works
Sustainable membrane biosynthesis for synthetic minimal cells
Exterkate, M. (2019) · doi:10.33612/diss.98704569 · Cited by 1 · see citing works
Bacterial glycosphingolipids orchestrate colonization and immune modulation in neonatal hostPreprint
Heo, K., Jung, D.-J., Yoo, J., Goh, B., Kasper, D. L., & Oh, S. F. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.02.651985 · Cited by 1 · see citing works
Shaigec, E. R., Cho, T. H. S., Tsviklist, V., Bishop, J., & Raivio, T. L. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.22.696046 · Cited by 1 · see citing works
Promoter Order Strategy and Bacterial PspF Regulon Evolution
Jovanović, G., Mehta, P. D., McDonald, C., & Buck, M. (2015) · Springer eBooks · doi:10.1007/978-3-319-19932-0_14
Caliskan, M., Poschmann, G., Gudzuhn, M., Waldera-Lupa, D. M., Streit, W. R., Jaeger, K., Stühler, K., & Kovačić, F. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.25.517918
Piksa, M., Bromke, M. A., Marques, C. M., Lecuyer, S., Daira, P., Fourmaux, B., Samuel, I. D. W., Matczyszyn, K., & Pawlik, K. J. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.26.701284
Membrane composition and thermodynamic identity as boundaries of life for synthetic cell research
Presutti, C., & Poolman, B. (2026) · FEBS Letters · doi:10.1002/1873-3468.70476
- Authors
- Arias-Cartin, R., Grimaldi, S., Pommier, J., Lanciano, P., Schaefer, C., Arnoux, P., Giordano, G., Guigliarelli, B., & Magalon, A.
- Affiliations
- Laboratoire de Chimie Bactérienne, Unité Propre de Recherche 9043, Institut de Microbiologie de la Méditerranée, Centre National de la Recherche Scientifique and Aix-Marseille Université, 31, Chemin Joseph Aiguier, 13009 Marseille, France;
- Centre National de la Recherche Scientifique (FR)
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- Corresponding author
- Magalon, Axel
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-04-25
- Volume
- 108
- Issue
- 19
- Pages
- 7781-7786
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3093509
- OpenAlex
- W2023186532
- Cited by
- 78
- References
- 57
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 3 · 2023: 7 · 2022: 3 · 2021: 4 · 2020: 3 · 2019: 3 · 2018: 6 · 2017: 2 · 2016: 6 · 2015: 6 · 2014: 6 · 2013: 9 · 2012: 7
- FWCI
- 3.25
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- cardiolipin, Escherichia coli, anionic phospholipids, protein-lipid interactions, bacterial respiratory chain
- MeSH terms
- Binding Sites, Cardiolipins, Electron Spin Resonance Spectroscopy, Escherichia coli, Heme, Membrane Lipids, Models, Molecular, Multienzyme Complexes, Oxidoreductases, Phospholipids, Proteolipids, Mutagenesis, Site-Directed, Escherichia coli Proteins, Electron Transport Chain Complex Proteins, Mutant Proteins, Nitrate Reductase, Protein Interaction Domains and Motifs, Static Electricity
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