Structural basis for malfunction in complex II
Open accessAbstract
Complex II couples oxidoreduction of succinate and fumarate at one active site with that of quinol/quinone at a second distinct active site over 40 Å away. This process links the Krebs cycle to oxidative phosphorylation and ATP synthesis. The pathogenic mutation or inhibition of human complex II or its assembly factors is often associated with neurodegeneration or tumor formation in tissues derived from the neural crest. This brief overview of complex II correlates the clinical presentations of a large number of symptom-associated alterations in human complex II activity and assembly with the biochemical manifestations of similar alterations in the complex II homologs from Escherichia coli. These analyses provide clues to the molecular basis for diseases associated with aberrant complex II function.
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Loss of complex II function can cause succinate accumulation and increased ROS generation in mammalian cells.
“It has been observed that loss of function of complex II can lead to the accumulation of succinate and increased ROS generation in mammalian cells (overview in [14,36]).”
From Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning (2013) · cites this paper as [14]
Mutations in complex II subunits C and D near the Qp site are associated with hereditary paragangliomas and pheochromocytomas, and SdhA mutations can cause Leigh syndrome.
“This seems to be especially the case for mutations in complex II subunits C and D located in the vicinity of the Qp site that have been associated with specific forms of cancer such as hereditary paragangliomas and pheochromocytomas (overview in [13,14,36]) and in SdhA that can cause Leigh syndrome, a progressive neurodegenerative disease [14,94].”
From Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning (2013) · cites this paper as [14]
Cites
Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase
Selak, M. A., Armour, S. M., MacKenzie, E. D., Boulahbel, H., Watson, D. G., Mansfield, K. D., Pan, Y., Simon, M. C., Thompson, C. B., & Gottlieb, E. (2005) · Cancer Cell · doi:10.1016/j.ccr.2004.11.022 · Cited by 2,108 · cited 2× · see citing works
“Interestingly, in yeast, themutants secreted succinate (65), consistent with reduced complex II activity elevating succinate levels and stabilizing hypoxia-inducible factor-1 , leading to a pseudohypoxic phenotype (40, 42).”
BackgroundMutations in <i>SDHD</i> , a Mitochondrial Complex II Gene, in Hereditary Paraganglioma
Baysal, B. E., Ferrell, R. E., Willett-Brozick, J. E., Lawrence, E. C., Myssiorek, D., Bosch, A., Mey, A. V. D., Taschner, P. E. M., Rubinstein, W. S., Myers, E. N., et al. (2000) · Science · doi:10.1126/science.287.5454.848 · Cited by 1,638 · see citing works
Germ-Line Mutations in Nonsyndromic Pheochromocytoma
Neumann, H. P. H., Bausch, B., McWhinney, S. R., Bender, B., Gimm, O., Franke, G., Schipper, J., Klisch, J., Altehoefer, C., Zerres, K., et al. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa020152 · Cited by 1,350 · 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 · see citing works
Self-citationCrystal Structure of Mitochondrial Respiratory Membrane Protein Complex II
Sun, F., Huo, X., Zhai, Y., Wang, A., Xu, J., Su, D., Bartlam, M., & Rao, Z. (2005) · Cell · doi:10.1016/j.cell.2005.05.025 · Cited by 881 · see citing works
WARBURN, O., & Dickens, F. (1931) · The American Journal of the Medical Sciences · doi:10.1097/00000441-193107000-00022 · Cited by 813 · see citing works
Bourgeron, T., Rustin, P., Chretien, D., Birch-Machin, M., Bourgeois, M., Viegas-Péquignot, E., Munnich, A., & Rötig, A. (1995) · Nature Genetics · doi:10.1038/ng1095-144 · Cited by 730 · cited 4× · see citing works
“The enhanced sensitivity of complex II to oxaloacetate likely reduces enzyme activity to 50% of wild-type levels in patients harboring the R554Wmutation (2).”
BackgroundInfluentialHao, H.-X., Khalimonchuk, O., Schraders, M., Dephoure, N., Bayley, J.-P., Kunst, H., Devilee, P., Cremers, C. W. R. J., Schiffman, J. D., Bentz, B. G., et al. (2009) · Science · doi:10.1126/science.1175689 · Cited by 702 · see citing works
A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes.
Ishii, N., Fujii, M., Hartman, P. S., Tsuda, M., Yasuda, K., Senoo-Matsuda, N., Yanase, S., Ayusawa, D., & Suzuki, K. (1998) · Nature · doi:10.1038/29331 · Cited by 687 · cited 1× · see citing works
“elegans had a shortened life span phenotypically similar to the SdhC mev-1 mutant, in which the [3Fe-4S]/quinone-binding domain is perturbed (63).”
BackgroundSuccinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer
King, A., Selak, M. A., & Gottlieb, E. (2006) · Oncogene · doi:10.1038/sj.onc.1209594 · Cited by 672 · see citing works
SDHA is a tumor suppressor gene causing paraganglioma
Burnichon, N., Brière, J.-J., Libé, R., Vescovo, L., Rivière, J., Tissier, F., Jouanno, E., Jeunemaı̂tre, X., Bénit, P., Tzagoloff, A., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq206 · Cited by 645 · see citing works
Clinical Presentation and Penetrance of Pheochromocytoma/Paraganglioma Syndromes
Benn, D. E., Gimenez‐Roqueplo, A., Reilly, J. R., Bertherat, J. Y., Burgess, J. R., Byth, K., CROXSON, M. S., Dahia, P. L. M., Elston, M. S., Gimm, O., et al. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1862 · Cited by 565 · see citing works
Function and Structure of Complex II of the Respiratory Chain
Cecchini, G. (2003) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.72.121801.161700 · Cited by 556 · see citing works
Self-citationInhibition of Hypoxia-inducible Factor (HIF) Hydroxylases by Citric Acid Cycle Intermediates
Koivunen, P., Hirsilä, M., Remes, A. M., Hassinen, I. E., Kivirikko, K. I., & Myllyharju, J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m610415200 · Cited by 521 · see citing works
Structure of the Escherichia coli Fumarate Reductase Respiratory Complex
Iverson, T. M., Luna-Chavez, C., Cecchini, G., & Rees, D. C. (1999) · Science · doi:10.1126/science.284.5422.1961 · Cited by 416 · see citing works
Self-citationReplicating Huntington's disease phenotype in experimental animals
Brouillet, E. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00005-2 · Cited by 413 · see citing works
Bardella, C., Pollard, P. J., & Tomlinson, I. (2011) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2011.07.003 · Cited by 395 · see citing works
Alston, T. A., Mela, L., & Bright, H. J. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.9.3767 · Cited by 380 · see citing works
Burnichon, N., Rohmer, V., Amar, L., Herman, P., Leboulleux, S., Darrouzet, V., Niccoli, P., Gaillard, D. A., Chabrier, G., Chabolle, F., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-2504 · Cited by 374 · see citing works
Structure of fumarate reductase from Wolinella succinogenes at 2.2 Å resolution
Lancaster, C. R. D., Kröger, A., Auer, M., & Michel, H. (1999) · Nature · doi:10.1038/46483 · Cited by 339 · see citing works
Brouwers, F. M., Eisenhofer, G., Tao, J. J., Kant, J. A., Adams, K. T., Linehan, W. M., & Pacák, K. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0423 · Cited by 314 · see citing works
Horsefield, R., Yankovskaya, V., Sexton, G., Whittingham, W., Shiomi, K., Ōmura, S., Byrne, B., Cecchini, G., & Iwata, S. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m508173200 · Cited by 292 · see citing works
Self-citationKorpershoek, E., Favier, J., Gaal, J., Burnichon, N., van Gessel, B., Oudijk, L., Badoual, C., Gadessaud, N., Venisse, A., Bayley, J.-P., et al. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1043 · Cited by 277 · see citing works
Ghezzi, D., Goffrini, P., Uziel, G., Horváth, R., Klopstock, T., Lochmüller, H., D’Adamo, P., Gasparini, P., Strom, T. M., Prokisch, H., et al. (2009) · Nature Genetics · doi:10.1038/ng.378 · Cited by 244 · see citing works
Túnez, I., Tasset, I., de la Cruz, V. P., & Santamarı́a, A. (2010) · Molecules · doi:10.3390/molecules15020878 · Cited by 220 · see citing works
Parfait, B., Chrétien, D., Rötig, A., Marsac, C., Münnich, A., & Rustin, P. (2000) · Human Genetics · doi:10.1007/s004399900218 · Cited by 211 · see citing works
Bayley, J., Devilee, P., & Taschner, P. E. M. (2005) · BMC Medical Genetics · doi:10.1186/1471-2350-6-39 · Cited by 183 · see citing works
Succinate inhibition of α-ketoglutarate-dependent enzymes in a yeast model of paraganglioma
Smith, E. H., Janknecht, R., & Maher, L. J. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm275 · Cited by 169 · see citing works
Inhibition of succinate dehydrogenase dysregulates histone modification in mammalian cells
Cervera, A. M., Bayley, J.-P., Devilee, P., & McCreath, K. J. (2009) · Molecular Cancer · doi:10.1186/1476-4598-8-89 · Cited by 156 · see citing works
Pantaleo, M. A., Astolfi, A., Indio, V., Moore, R. A., Thiessen, N., Heinrich, M. C., Gnocchi, C., Santini, D., Catena, F., Formica, S., et al. (2011) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djr130 · Cited by 150 · see citing works
Inborn and acquired metabolic defects in cancer
Frezza, C., Pollard, P. J., & Gottlieb, E. (2011) · Journal of Molecular Medicine · doi:10.1007/s00109-011-0728-4 · Cited by 146 · see citing works
Maklashina, E., Berthold, D. A., & Cecchini, G. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.22.5989-5996.1998 · Cited by 144 · see citing works
Self-citationHorváth, R. (2005) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2005.067041 · Cited by 133 · see citing works
Tzagoloff, A., Jang, J., Glerum, D. M., & Wu, M. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.13.7392 · Cited by 120 · see citing works
Bayley, J., & Devilee, P. (2010) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2010.02.008 · Cited by 117 · see citing works
Levitas, A., Muhammad, E., Harel, G., Saada, A., Caspi, V. C., Manor, E., Beck, J. S., Sheffield, V. C., & Parvari, R. (2010) · European Journal of Human Genetics · doi:10.1038/ejhg.2010.83 · Cited by 113 · see citing works
Fumarate Reductase Mutants of Escherichia coli That Lack Covalently Bound Flavin
Blaut, M., Whittaker, K. M., Valdovinos, A., Ackrell, B. A. C., Gunsalus, R. P., & Cecchini, G. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)80039-4 · Cited by 107 · see citing works
Self-citationSzeto, S. S. W., Reinke, S. N., Sykes, B. D., & Lemire, B. D. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700601200 · Cited by 104 · see citing works
Guo, J., & Lemire, B. D. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306312200 · Cited by 103 · see citing works
Role of Oxalacetate in the Regulation of Mammalian Succinate Dehydrogenase
Ackrell, B. A. C., Kearney, E. B., & Mayr, M. (1974) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)42790-7 · Cited by 102 · see citing works
Studies on Succinate Dehydrogenase
Kimura, T., HAUBER, J., & Singer, T. P. (1967) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)99466-4 · Cited by 99 · see citing works
Guest, J. R. (1981) · Microbiology · doi:10.1099/00221287-122-2-171 · Cited by 93 · see citing works
Glutaric aciduria type I: Pathomechanisms of neurodegeneration
Ullrich, K., Flott-Rahmel, B., Schluff, P., Mußhoff, U., Das, A. M., Lücke, T., Steinfeld, R., Christensen, E., Jakobs, C., Ludolph, A. C., et al. (1999) · Journal of Inherited Metabolic Disease · doi:10.1023/a:1005595921323 · Cited by 91 · see citing works
Ruprecht, J. J., Yankovskaya, V., Maklashina, E., Iwata, S., & Cecchini, G. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.010058 · Cited by 90 · see citing works
Self-citationCoster, R. V., Seneca, S., Smet, J., Hecke, R. V., Gerlo, E., Devreese, B. V., BEEUMEN, J. V., Leroy, J. G., Meırleır, L. D., & Lissens, W. (2003) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.10202 · Cited by 83 · see citing works
Dibrov, E., Fu, S., & Lemire, B. D. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.48.32042 · Cited by 82 · see citing works
Srirangalingam, U., Walker, L., Khoo, B. C. E., MacDonald, F., Gardner, D. S.-L., Wilkin, T. J., Skelly, R. H., George, E., Spooner, D. A., Monson, J. P., et al. (2008) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2008.03274.x · Cited by 82 · see citing works
Manodori, A. B., Cecchini, G., Schröder, I., Gunsalus, R. P., Werth, M. T., & Johnson, M. K. (1992) · Biochemistry · doi:10.1021/bi00125a010 · Cited by 78 · see citing works
Self-citationHead and neck paragangliomas: genetic spectrum and clinical variability in 79 consecutive patients
Piccini, V., Rapizzi, E., Bacca, A., Trapani, G. D., Pulli, R., Giaché, V., Zampetti, B., Cordisco, E. L., Canu, L., Corsini, E., et al. (2012) · Endocrine Related Cancer · doi:10.1530/erc-11-0369 · Cited by 78 · see citing works
Milunsky, J. M., Maher, T. A., Michels, V. V., & Milunsky, A. (2001) · American Journal of Medical Genetics · doi:10.1002/ajmg.1270 · Cited by 77 · see citing works
Werth, M. T., Cecchini, G., Manodori, A. B., Ackrell, B. A. C., Schröder, I., Gunsalus, R. P., & Johnson, M. K. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.22.8965 · Cited by 73 · see citing works
Self-citationHuang, J., & Lemire, B. D. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.02.028 · Cited by 73 · see citing works
Selective pathological changes of the periaqueductal gray matter in Alzheimer's disease
Parvizi, J., Hoesen, G. W. V., & Damásio, A. R. (2000) · Annals of Neurology · doi:10.1002/1531-8249(200009)48:3 · Cited by 70 · see citing works
Huang, L.-S., Shen, J. T., Wang, A. C., & Berry, E. A. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.06.015 · Cited by 65 · see citing works
Kowal, A. T., Werth, M. T., Manodori, A. B., Cecchini, G., Schroeder, I., Gunsalus, R. P., & Johnson, M. K. (1995) · Biochemistry · doi:10.1021/bi00038a024 · Cited by 65 · see citing works
Self-citationTran, Q. M., Rothery, R. A., Maklashina, E., Cecchini, G., & Weiner, J. H. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607476200 · Cited by 64 · see citing works
Self-citationMitochondrial Syndromes with Leukoencephalopathies
Wong, L. (2012) · Seminars in Neurology · doi:10.1055/s-0032-1306387 · Cited by 63 · see citing works
SdhE Is a Conserved Protein Required for Flavinylation of Succinate Dehydrogenase in Bacteria
McNeil, M. B., Clulow, J. S., Wilf, N. M., Salmond, G. P. C., & Fineran, P. C. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.293803 · Cited by 63 · see citing works
The Saccharomyces cerevisiae succinate dehydrogenase does not require heme for ubiquinone reduction
Oyedotun, K. S., Sit, C. S., & Lemire, B. D. (2007) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2007.09.008 · Cited by 54 · see citing works
Phenotypic variability of mitochondrial disease caused by a nuclear mutation in complex II
Pagnamenta, A. T., Hargreaves, I. P., Duncan, A. J., Taanman, J., Heales, S., Land, J. M., Bitner-Glindzicz, M. A. K., Leonard, J. V., & Rahman, S. (2006) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2006.05.003 · Cited by 54 · see citing works
Lima, J. P., Feijão, T., da Silva, A. F., Pereira‐Castro, I., Fernandez-Ballester, G. J., Máximo, V., Herrero, A., Serrano, L., Sobrinho-Simões, M. A., & García‐Rostán, G. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0640 · Cited by 53 · see citing works
<i>Escherichia coli</i> succinate dehydrogenase variant lacking the heme <i>b</i>
Tran, Q. M., Rothery, R. A., Maklashina, E., Cecchini, G., & Weiner, J. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707732104 · Cited by 51 · see citing works
Self-citationDifferences in Protonation of Ubiquinone and Menaquinone in Fumarate Reductase from Escherichia coli
Maklashina, E., Hellwig, P., Rothery, R. A., Kotlyar, V., Sher, Y. I., Weiner, J. H., & Cecchini, G. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602938200 · Cited by 50 · see citing works
Self-citationInteractions of oxaloacetate with Escherichia coli fumarate reductase
Ackrell, B. A. C., Cochran, B. C., & Cecchini, G. (1989) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(89)90561-4 · Cited by 39 · see citing works
Self-citationShimizu, H., Osanai, A., Sakamoto, K., Inaoka, D. K., Shiba, T., Harada, S., & Kita, K. (2012) · The Journal of Biochemistry · doi:10.1093/jb/mvs051 · Cited by 39 · see citing works
Candidate gene mutation analysis in bilateral adrenal pheochromocytoma and sympathetic paraganglioma
Korpershoek, E., Petri, B., van Nederveen, F. H., Dinjens, W. N. M., Verhofstad, A. A. J., de Herder, W. W., Schmid, S., Perren, A. A., Komminoth, P., & de Krijger, R. R. (2007) · Endocrine Related Cancer · doi:10.1677/erc-06-0044 · Cited by 38 · see citing works
Schiavi, F., Savvoukidis, T., Trabalzini, F., Grego, F., Piazza, M., Amistà, P., Demattè, S., Piano, A. D., Cecchini, M. E., Erlic, Z., et al. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1353.020 · Cited by 37 · see citing works
Cecchini, G., Sices, H. J., Schröder, I., & Gunsalus, R. P. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.16.4587-4592.1995 · Cited by 35 · see citing works
Self-citationSilkin, Y. A., Oyedotun, K. S., & Lemire, B. D. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.11.017 · Cited by 32 · see citing works
Tomasiak, T. M., Maklashina, E., Cecchini, G., & Iverson, T. M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m801372200 · Cited by 30 · see citing works
Self-citationSpectroscopy of succinate dehydrogenases, a historical perspective
Beinert, H. (2002) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(01)00235-3 · Cited by 30 · see citing works
Giancaspero, T. A., Wait, R., Boles, E., & Barile, M. (2008) · FEBS Journal · doi:10.1111/j.1742-4658.2008.06270.x · Cited by 26 · see citing works
Tomasiak, T. M., Archuleta, T. L., Andréll, J., Luna-Chavez, C., Davis, T. A., Sarwar, M., Ham, A. L., McDonald, W. H., Yankovskaya, V., Stern, H. A., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.192849 · Cited by 25 · see citing works
Self-citationSystematic screening and treatment evaluation of hereditary neck paragangliomas
Fish, J., Klein-Weigel, P. F., Biebl, M., Janecke, A., Tauscher, T., & Fraedrich, G. (2007) · Head & Neck · doi:10.1002/hed.20638 · Cited by 22 · see citing works
Lim, K., Doseeva, V., Demirkan, E., Pullalarevu, S., Krajewski, W. W., Galkin, A. G., Howard, A. J., & Herzberg, O. (2004) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.20337 · Cited by 20 · see citing works
Chromosomal changes in sporadic and familial head and neck paragangliomas
Sevilla, M. A., Hermsen, M. A. J. A., Weiss, M. M., Grimbergen, A., Balbı́n, M., Llorente, J. L., Rodrigo, J. P., & Suarez, C. M. (2009) · Otolaryngology · doi:10.1016/j.otohns.2009.01.004 · Cited by 20 · see citing works
Role of the Genetic Study in the Management of Carotid Body Tumor in Paraganglioma Syndrome
Antonello, M., Piazza, M., Menegolo, M., Opocher, G., Deriu, G. P., & Grego, F. (2008) · European Journal of Vascular and Endovascular Surgery · doi:10.1016/j.ejvs.2008.06.021 · Cited by 19 · see citing works
No evidence for involvement of SDHD in neuroblastoma pathogenesis
Preter, K. D., Vandesompele, J., Hoebeeck, J., Vandenbroecke, C., Smet, J., Nuyts, A., Laureys, G., Combaret, V., Roy, N. V., Roels, F., et al. (2004) · BMC Cancer · doi:10.1186/1471-2407-4-55 · Cited by 17 · see citing works
Poeppel, T. D., Yuece, A., Boy, C., Metz, K. A., Kaminsky, E., Neumann, H. P. H., Rosenbaum, S. J., Mann, K., & Moeller, L. C. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2011.36.2269 · Cited by 13 · see citing works
Bacca, A., Franceschini, S. S., Carrara, D., Bernini, M., Zampa, V., Taddei, S., Miccoli, P., Congregati, C., Simi, P., Ferrari, M., et al. (2012) · Head & Neck · doi:10.1002/hed.22910 · Cited by 10 · see citing works
Huang, L.-S., Sun, G., Cobessi, D., Wang, A. C., Shen, J. T., Tung, E. Y., Anderson, V. E., & Berry, E. A. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m511270200 · Cited by 10 · see citing works
Liu, G., Sukumaran, D. K., Xu, D., Chiang, Y., Acton, T., Goldsmith‐Fischman, S., Honig, B. H., Montelione, G. T., & Szyperski, T. (2004) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.20009 · Cited by 7 · see citing works
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Siebels, I., & Dröse, S. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.06.005 · Cited by 130 · see citing works
Lalève, A., Gamet, S., Walker, A. S., Debieu, D., Toquin, V., & Fillinger, S. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12282 · Cited by 125 · see citing works
Sharma, S., Bhattarai, S., Ara, H., Sun, G. E. C., Clair, D. K. S., Bhuiyan, M. S., Kevil, C. G., Watts, M. N., Dominic, P. S., Shimizu, T., et al. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101740 · Cited by 90 · see citing works
Chen, W., Wei, L., Zhao, W., Wang, B., Zheng, H., Zhang, P., Lou, T., Duan, Y., Hou, Y., Zhou, M., et al. (2020) · Pest Management Science · doi:10.1002/ps.6053 · Cited by 87 · see citing works
Huang, S., Braun, H., Gawryluk, R. M. R., & Millar, A. H. (2019) · The Plant Journal · doi:10.1111/tpj.14227 · Cited by 84 · see citing works
Lanciano, P., Khalfaoui-Hassani, B., Selamoglu, N., Ghelli, A. M., Rugolo, M., & Daldal, F. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.03.009 · Cited by 80 · see citing works
Catalytic mechanisms of complex II enzymes: A structural perspective
Iverson, T. M. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.09.008 · Cited by 80 · see citing works
Self-citationSivley, R. M., Kropski, J., Sheehan, J., Cogan, J., Dou, X., Blackwell, T. S., Phillips, J., Meiler, J., Bush, W. S., & Capra, J. A. (2018) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2018.01.017 · Cited by 75 · see citing works
Emerging concepts in the flavinylation of succinate dehydrogenase
Kim, H. J., & Winge, D. R. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.01.012 · Cited by 74 · see citing works
Sharma, P., Maklashina, E., Cecchini, G., & Iverson, T. M. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2007391117 · Cited by 58 · see citing works
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Pei, H., Yang, Y., Zhao, H., Li, X., Yang, D., Li, D., & Yang, Y. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/5470457 · Cited by 55 · see citing works
Chen, W., Wei, L., Li, X., Ma, H., Lou, T., Zhang, P., Zheng, H., Zhu, X., Zhang, Y. L., Liu, F., et al. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c04363 · Cited by 52 · see citing works
Iverson, T. M., Singh, P. K., & Cecchini, G. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104761 · Cited by 51 · see citing works
Self-citationCao, F., Souders, C. L., Perez‐Rodriguez, V., & Martyniuk, C. J. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2018.00701 · Cited by 48 · see citing works
Mitochondrial protein dysfunction in pathogenesis of neurological diseases
Wang, L., Yang, Z., He, X., Pu, S., Yang, C., Wu, Q., Zhou, Z., Cen, X., & Zhao, H. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.974480 · Cited by 46 · see citing works
Role of Mitochondrial Dysfunctions in Neurodegenerative Disorders: Advances in Mitochondrial Biology
Kathiresan, D. S., Balasubramani, R., Marudhachalam, K., Jaiswal, P., Ramesh, N., Suruthi, G. S., Moorthi, P. V., & Vijayan, M. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04469-x · Cited by 46 · see citing works
Woodman, A. G., Mah, R., Keddie, D., Noble, R. M. N., Panahi, S., Gragasin, F. S., Lemieux, H., & Bourque, S. L. (2018) · The FASEB Journal · doi:10.1096/fj.201701080r · Cited by 42 · see citing works
Defining a direction: Electron transfer and catalysis in Escherichia coli complex II enzymes
Maklashina, E., Cecchini, G., & Dikanov, S. A. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.01.010 · Cited by 41 · see citing works
Self-citationMaturation of the respiratory complex II flavoprotein
Sharma, P., Maklashina, E., Cecchini, G., & Iverson, T. M. (2019) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2019.01.027 · Cited by 37 · see citing works
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Kim, E., Rath, E. M., Tsang, V., Duff, A. P., Robinson, B. G., Church, W. B., Benn, D. E., Dwight, T., & Clifton-Bligh, R. J. (2015) · Endocrine Related Cancer · doi:10.1530/erc-15-0099 · Cited by 37 · see citing works
Molecular pathogenesis of tumorigenesis caused by succinate dehydrogenase defect
Moosavi, B., Zhu, X., Yang, W., & Yang, G. (2019) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2019.151057 · Cited by 36 · see citing works
Chen, W., Li, X., Wei, L., Chen, B., Han, C., Duan, Y., & Chen, C. (2024) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.4c02179 · Cited by 33 · see citing works
Maklashina, E., Rajagukguk, S., Iverson, T. M., & Cecchini, G. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.001977 · Cited by 30 · see citing works
Self-citationZhang, L., Qiu, L., Xu, S., Cheng, X. F., Wu, J., Wang, Y., Gao, W., Bao, J., & Yu, H. (2023) · Toxicology in Vitro · doi:10.1016/j.tiv.2023.105669 · Cited by 24 · see citing works
Anderson, R. F., Shinde, S. S., Hille, R., Rothery, R. A., Weiner, J. H., Rajagukguk, S., Maklashina, E., & Cecchini, G. (2014) · Biochemistry · doi:10.1021/bi401630m · Cited by 24 · see citing works
Self-citationHuang, L.-S., Lümmen, P., & Berry, E. A. (2021) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2021.140679 · Cited by 23 · see citing works
Selective striatal mtDNA depletion in end-stage Huntington's disease R6/2 mice
Hering, T., Birth, N., Taanman, J., & Orth, M. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.02.004 · Cited by 23 · see citing works
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Maklashina, E., Rajagukguk, S., Starbird, C. A., McDonald, W. H., Koganitsky, A., Eisenbach, M., Iverson, T. M., & Cecchini, G. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.690396 · Cited by 19 · see citing works
Self-citationSakai, C., Tomitsuka, E., Miyagishi, M., Harada, S., & Kita, K. (2013) · Mitochondrion · doi:10.1016/j.mito.2013.08.009 · Cited by 18 · see citing works
Xu, X. M., Huang, Z., Han, H., Yu, Z., Ye, L., Zhao, Z., Qian, Y., Li, Y., Zhao, R., Zhang, T., et al. (2025) · Cancer Letters · doi:10.1016/j.canlet.2025.217566 · Cited by 16 · see citing works
How an assembly factor enhances covalent FAD attachment to the flavoprotein subunit of complex II
Maklashina, E., Iverson, T. M., & Cecchini, G. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102472 · Cited by 15 · see citing works
Self-citationSha, D., Wang, L., Zhang, J., Qian, L., Li, Q., Li, J., Qian, J., Gu, S., Han, L., Xu, P., et al. (2014) · Brain Research · doi:10.1016/j.brainres.2014.07.043 · Cited by 15 · see citing works
ROS control in human iPS cells reveals early events in spontaneous carcinogenesis
Oka, S., Hayashi, M., Taguchi, K., Hidaka, M., Tsuzuki, T., & Sekiguchi, M. (2019) · Carcinogenesis · doi:10.1093/carcin/bgz081 · Cited by 14 · see citing works
Sharma, P., Maklashina, E., Voehler, M., Balintova, S., Dvorakova, S., Kraus, M., Vanova, K. H., Nahácka, Z., Zobalová, R., Boukalová, Š., et al. (2024) · Nature Communications · doi:10.1038/s41467-023-44563-7 · Cited by 11 · see citing works
Self-citationKent, J. D., Klug, L. R., & Heinrich, M. C. (2024) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-24-1601 · Cited by 8 · see citing works
Electron Transport Chain, Oxidative Phosphorylation, and Other Oxygen-Consuming Systems
Bhagavan, N. V., & Ha, C. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-416687-5.00013-0 · Cited by 7 · see citing works
Kumar, R., Chinala, A., & Gullapalli, R. R. (2026) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2026.104943 · Cited by 5 · see citing works
Zheng, J., Liu, S., Wang, D., Li, L., Sarsaiya, S., Zhou, H., & Cai, H. J. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1246842 · Cited by 5 · see citing works
Kim, Y., Kim, J., Hwang, K., Park, K. C., Cheong, J., & Sim, T. (2025) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2025.118081 · Cited by 3 · see citing works
Electron transport chain, oxidative phosphorylation, and reactive oxygen species
Ha, C. E., & Bhagavan, N. V. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-88541-6.00005-3 · Cited by 3 · see citing works
Electron Transport Chain, Oxidative Phosphorylation, and Other Oxygen-Consuming Systems
Bhagavan, N. V., & Ha, C. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-095461-2.00013-8 · Cited by 2 · see citing works
Neurodegenerative Diseases and Succinate Dehydrogenase: A Therapeutics Avenue for Treatment
Viswalingam, V., & Kumar, D. (2025) · Springer eBooks · doi:10.1007/978-981-96-6831-1_9 · Cited by 1 · see citing works
Liu, Z., Hu, J., Lin, Y., Ge, C., Shao, Y., Bao, M., Liu, M., Jia, S., Li, Y., Xu, X., et al. (2025) · Liver International · doi:10.1111/liv.70433 · Cited by 1 · see citing works
Sharma, P., Maklashina, E., Voehler, M., Balintova, S., Dvorakova, S., Kraus, M., Vanova, K. H., Nahácka, Z., Zobalová, R., Boukalová, Š., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-2070392/v1 · Cited by 1 · see citing works
Self-citationMitochondrial Complex II in Cancer
Kľučková, K., Neužil, J., & Rohlena, J. (2014) · Springer eBooks · doi:10.1007/978-94-017-8984-4_4
(Re)defining the concept of "pathogenic mutation" : translational analysis of an unusual lhon case
Guiomar, P. F. R. (2014) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Saucedo-Rodríguez, M. J., Pecina, P., Tauchmannová, K., Čunátová, K., Vrbacký, M., Čajka, T., Houštěk, J., Mráček, T., & Pecinová, A. (2026) · Research Square · doi:10.21203/rs.3.rs-8568560/v1
- Authors
- Iverson, T. M., Maklashina, E., & Cecchini, G.
- Affiliations
- Vanderbilt University Medical Center (US)
- San Francisco VA Medical Center (US)
- Corresponding author
- Iverson, Tina M.
- Cecchini, Gary
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2012-10
- Volume
- 287
- Issue
- 42
- Pages
- 35430-35438
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3471735
- OpenAlex
- W2029913956
- Cited by
- 53
- References
- 83
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 7 · 2018: 3 · 2017: 1 · 2016: 1 · 2015: 4 · 2014: 4 · 2013: 7 · 2012: 1
- FWCI
- 0.21
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01 BX001077)
- National Institute of General Medical Sciences (GM79419, GM61606, R01GM061606, R01GM079419)
- Topics
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Biochemical Acid Research Studies
- Keywords
- complex II, mitochondrial electron transport chain, pathogenic variants, neurodegeneration, neural crest tumors, oxidative phosphorylation, TCA cycle
- MeSH terms
- Adenosine Triphosphate, Animals, Citric Acid Cycle, Escherichia coli, Humans, Phosphorylation, Structure-Activity Relationship, Escherichia coli Proteins, Electron Transport Complex II
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