The DOI matches its Crossref record; 61 of the 61 references it cites were found in a registry or an index.
Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer
Abstract
The phenomenon of enhanced glycolysis in tumours has been acknowledged for decades, but biochemical evidence to explain it is only just beginning to emerge. A significant hint as to the triggers and advantages of enhanced glycolysis in tumours was supplied by the recent discovery that succinate dehydrogenase (SDH) and fumarate hydratase (FH) are tumour suppressors and which associated, for the first time, mitochondrial enzymes and their dysfunction with tumorigenesis. Further steps forward showed that the substrates of SDH and FH, succinate and fumarate, respectively, can mediate a 'metabolic signalling' pathway. Succinate or fumarate, which accumulate in mitochondria owing to the inactivation of SDH or FH, leak out to the cytosol, where they inhibit a family of prolyl hydroxylase enzymes (PHDs). Depending on the PHD inhibited, two newly recognized pathways that support tumour maintenance may ensue: affected cells become resistant to certain apoptotic signals and/or activate a pseudohypoxic response that enhances glycolysis and is conveyed by hypoxia-inducible factor.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“In animal models, fumarate hydratase inactivation induces a precancerous phenotype associated with chronic HIF pathway activation, highlighting the intersection of mitochondrial metabolism, redox homeostasis, and HIF regulation [229,230].”
From HIF inhibition: Current strategies and clinical challenges (2026) · cites this paper as [230]
In the citing paper
“These metabolic perturbations, which are tightly linked to altered cellular redox balance, result in pseudohypoxic signaling and increased cancer susceptibility [229,230].”
From HIF inhibition: Current strategies and clinical challenges (2026) · cites this paper as [230]
In the citing paper
“Mitochondrial dysfunction could impair oxidative phosphorylation, the TCA cycle, fatty acid oxidation, the urea cycle, gluconeogenesis, and apoptotic pathways (King et al., 2006; Modica-Napolitano and Singh, 2004).”
From Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism (2016) · cites this paper as King et al., 2006
In the citing paper
“Loss-of-function mutations in SDH and FH cause a build-up of succinate and fumarate, respectively87. Accordingly, increased levels of succinate and fumarate caused by mutations in these genes can compete with αKG and inhibit activity of HIF hydroxylases and thus induce normoxic HIF1α activity in vitro88,89.”
From Targeting cancer vulnerabilities with high-dose vitamin C (2019) · cites this paper as [87]
In the citing paper
“Interestingly, inherited mutations in fumarate hydratase, another Krebs cycle enzyme, have also been linked to a separate and equally rare inherited cancer syndrome 96 .”
From The common biology of cancer and ageing (2007) · cites this paper as [96]
Citations
Cites
Why Do Cancers Have High Aerobic Glycolysis?
Gatenby, R. A., & Gillies, R. J. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1478 · Cited by 4,784
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 4×
“Although both molecules were shown to mediate HIF induction (Isaacs et al., 2005; Selak et al., 2005), it is possible that they inhibit different PHDs with different efficiency.”
BackgroundInfluentialSelf-citationOxygen sensing by HIF hydroxylases
Schofield, C. J., & Ratcliffe, P. J. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1366 · Cited by 2,068
Mutations in SDHD , 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
The Multiple Leiomyoma Consortium (2002) · Nature Genetics · doi:10.1038/ng849 · Cited by 1,635
The key role of anaplerosis and cataplerosis for citric acid cycle function
Owen, O. E., Kalhan, S. C., & Hanson, R. W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.r200006200 · Cited by 1,172 · cited 1×
“Moreover, enhanced glucose breakdown provides building blocks for the synthesis of nucleotides (via the pentose phosphate pathway), and amino and fatty acids (from glycolytic and TCA cycle intermediates) (Figure 1) (Owen et al., 2002).”
BackgroundOncogenic alterations of metabolism
Dang, C. V., & Semenza, G. L. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(98)01344-9 · Cited by 1,106
Astuti, D., Latif, F., Dallol, A., Dahia, P. L. M., Douglas, F., George, E., Sköldberg, F., Husebye, E. S., Eng, C., & Maher, E. R. (2001) · The American Journal of Human Genetics · doi:10.1086/321282 · Cited by 1,087
Mitochondria, oxygen free radicals, disease and ageing
Raha, S., & Robinson, B. H. (2000) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(00)01674-1 · Cited by 1,066 · cited 1×
“These are reactive oxygen species (ROS), which can be generated by the ETC, especially in complex I and III (Raha and Robinson, 2000).”
BackgroundDysregulation of the TSC-mTOR pathway in human disease
Inoki, K., Corradetti, M. N., & Guan, K. (2004) · Nature Genetics · doi:10.1038/ng1494 · Cited by 980
Cited by
Sorted by citations
Regulation of cancer cell metabolism
Cairns, R. A., Harris, I. S., & Mak, T. W. (2011) · Nature Reviews Cancer · doi:10.1038/nrc2981 · Cited by 4,744
Otto Warburg's contributions to current concepts of cancer metabolism
Koppenol, W. H., Bounds, P. L., & Dang, C. V. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3038 · Cited by 3,427
Hypoxia-inducible factors and the response to hypoxic stress
Majmundar, A. J., Wong, W. J., & Simon, M. C. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.022 · Cited by 2,380
Role of Mitochondria in Ferroptosis
Gao, M., Yi, J., Zhu, J., Minikes, A. M., Monian, P., Thompson, C. B., & Jiang, X. (2019) · Molecular Cell · doi:10.1016/j.molcel.2018.10.042 · Cited by 2,120
Cellular Adaptation to Hypoxia through Hypoxia Inducible Factors and beyond
Lee, P., Chandel, N. S., & Simon, M. C. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0227-y · Cited by 1,272
Xiao, M., Yang, H., Xu, W., Ma, S., Lin, H., Zhu, H., Liu, L., Liu, Y., Yang, C., Xu, Y., et al. (2012) · Genes & Development · doi:10.1101/gad.191056.112 · Cited by 1,188
Glucose-Independent Glutamine Metabolism via TCA Cycling for Proliferation and Survival in B Cells
Le, A., Lane, A. N., Hamaker, M., Bose, S., Gouw, A., Barbi, J., Tsukamoto, T., Rojas, C. J., Slusher, B. S., Zhang, H., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2011.12.009 · Cited by 1,095
Links between metabolism and cancerPreprint
Dang, C. V. (2012) · Genes & Development · doi:10.1101/gad.189365.112 · Cited by 1,021
The common biology of cancer and ageing
Finkel, T., Serrano, M., & Blasco, M. A. (2007) · Nature · doi:10.1038/nature05985 · Cited by 988
Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism
Zhao, H., Yang, L., Baddour, J., Achreja, A., Bernard, V., Moss, T., Marini, J. C., Tudawe, T., Seviour, E. G., San Lucas, F. A., et al. (2016) · eLife · doi:10.7554/elife.10250 · Cited by 927
Oncogenic BRAF Regulates Oxidative Metabolism via PGC1α and MITF
Haq, R., Shoag, J., Andreu-Perez, P., Yokoyama, S., Edelman, H., Rowe, G. C., Frederick, D. T., Hurley, A. D., Nellore, A., Kung, A. L., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.02.003 · Cited by 818
Revisiting the Warburg effect: historical dogma versus current understanding
Vaupel, P. W., & Multhoff, G. (2020) · The Journal of Physiology · doi:10.1113/jp278810 · Cited by 862
With TOR, Less Is More: A Key Role for the Conserved Nutrient-Sensing TOR Pathway in Aging
Kapahi, P., Chen, D., Rogers, A. N., Katewa, S. D., Li, P. W.-L., Thomas, E., & Kockel, L. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.05.001 · Cited by 678
Seyfried, T. N., & Shelton, L. M. (2010) · Nutrition & Metabolism · doi:10.1186/1743-7075-7-7 · Cited by 675
Bonora, M., Patergnani, S., Rimessi, A., De Marchi, E., Suski, J. M., Bononi, A., Giorgi, C., Marchi, S., Missiroli, S., Poletti, F., et al. (2012) · Purinergic Signalling · doi:10.1007/s11302-012-9305-8 · Cited by 644
What a difference a hydroxyl makes: mutant IDH, (R)-2-hydroxyglutarate, and cancer
Losman, J.-A., & Kaelin, W. G. (2013) · Genes & Development · doi:10.1101/gad.217406.113 · Cited by 570
Reitman, Z. J., & Yan, H. (2010) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djq187 · Cited by 562
Wu, J.-Y., Huang, T., Hsieh, Y.-T., Wang, Y., Yen, C.-C., Lee, G.-L., Yeh, C., Peng, Y., Kuo, Y.-Y., Wen, H.-T., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.10.023 · Cited by 549
Mitochondrial DNA copy number variation across human cancers
Reznik, E., Miller, M. L., Şenbabaoğlu, Y., Riaz, N., Sarungbam, J., Tickoo, S. K., Al‐Ahmadie, H. A., Lee, W., Seshan, V., Hakimi, A. A., et al. (2016) · eLife · doi:10.7554/elife.10769 · Cited by 530
Mitochondrial dysfunction and the inflammatory response
López-Armada, M. J., Riveiro-Naveira, R. R., Vaamonde‐García, C., & Valcarcel‐Ares, M. N. (2013) · Mitochondrion · doi:10.1016/j.mito.2013.01.003 · Cited by 528
Cancer Cell Metabolism in Hypoxia: Role of HIF-1 as Key Regulator and Therapeutic Target
Infantino, V., Santarsiero, A., Convertini, P., Todisco, S., & Iacobazzi, V. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115703 · Cited by 541
The evolving metabolic landscape of chromatin biology and epigenetics
Dai, Z., Ramesh, V., & Locasale, J. W. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0270-8 · Cited by 508
Therapeutic targeting of the hypoxic tumour microenvironment
Singleton, D. C., Macann, A., & Wilson, W. R. (2021) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-021-00539-4 · Cited by 507
Regulation of Succinate Dehydrogenase Activity by SIRT3 in Mammalian Mitochondria
Çimen, H., Han, M., Yang, Y., Tong, Q., Koc, H., & Koc, E. C. (2009) · Biochemistry · doi:10.1021/bi901627u · Cited by 483
Roles of p53, MYC and HIF-1 in regulating glycolysis–the seventh hallmark of cancer
Yeung, S. J., Pan, J., & Lee, M.-H. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8224-x · Cited by 514
Succinate dehydrogenase – Assembly, regulation and role in human disease
Rutter, J. P., Winge, D. R., & Schiffman, J. D. (2010) · Mitochondrion · doi:10.1016/j.mito.2010.03.001 · Cited by 459
Mitochondrial dysfunction and mitochondrial dynamics-The cancer connection
Srinivasan, S., Guha, M., Kashina, A., & Avadhani, N. G. (2017) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2017.01.004 · Cited by 452
Fan, T. W. ‐., Lane, A. N., Higashi, R. M., Farag, M. A., Gao, H. T., Bousamra, M., & Miller, D. M. (2009) · Molecular Cancer · doi:10.1186/1476-4598-8-41 · Cited by 438
Targeting cancer vulnerabilities with high-dose vitamin C
Ngo, B., Van Riper, J. M., Cantley, L. C., & Yun, J. (2019) · Nature Reviews Cancer · doi:10.1038/s41568-019-0135-7 · Cited by 423
Puisségur, M.-P., Mazure, N. M., Bertero, T., Pradelli, L. A., Grosso, S., Robbe-Sermesant, K., Maurin, T., Lebrigand, K., Cardinaud, B., Hofman, V., et al. (2010) · Cell Death and Differentiation · doi:10.1038/cdd.2010.119 · Cited by 430
Iron–sulfur cluster biogenesis and human disease
Rouault, T. A., & Tong, W. H. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.05.008 · Cited by 391
Potential contribution of the uterine microbiome in the development of endometrial cancer
Walther-Antonio, M. R. S., Chen, J., Multinu, F., Hokenstad, A., Distad, T. J., Cheek, E. H., Keeney, G. L., Creedon, D. J., Nelson, H., Mariani, A., et al. (2016) · Genome Medicine · doi:10.1186/s13073-016-0368-y · Cited by 395
The Significance of Mitochondrial Dysfunction in Cancer
Luo, Y., Ma, J., & Lu, W. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165598 · Cited by 380
Succinate Dehydrogenase-Deficient GISTs
Miettinen, M., Wang, Z.-F., Sarlomo‐Rikala, M., Osuch, C., Rutkowski, P. L., & Lasota, J. P. (2011) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e3182260752 · Cited by 361
MacKenzie, E. D., Selak, M. A., Tennant, D. A., Payne, L. J., Crosby, S., Frederiksen, C. M., Watson, D. G., & Gottlieb, E. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01927-06 · Cited by 359
Self-citationMetabolic Reprogramming in Glioma
Strickland, M., & Stoll, E. A. (2017) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2017.00043 · Cited by 357
The enhancement of glycolysis regulates pancreatic cancer metastasis
Yang, J., Ren, B., Yang, G., Wang, H., Chen, G., You, L., Zhang, T., & Zhao, Y. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03278-z · Cited by 347
CircACC1 Regulates Assembly and Activation of AMPK Complex under Metabolic Stress
Li, Q., Wang, Y., Wu, S., Zhou, Z., Ding, X., Shi, R., Thorne, R. F., Zhang, X. D., Hu, W., & Wu, M. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.05.009 · Cited by 344
Favaro, E., Ramachandran, A., McCormick, R., Gee, H., Blancher, C., Crosby, M., Devlin, C., Blick, C., Buffa, F., Li, J.-L., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010345 · Cited by 324
“Mutations in many of these Fe-S cluster enzymes including succinate dehydrogenase subunits SDHD, SDHB and SDHC [35] and fumarate hydratase [36] are implicated in hyperproliferative disorders and cancer, demonstrating an important link between cellular metabolism and subsequent transformation and highlights a role for…”
BackgroundBensaad, K., & Vousden, K. H. (2007) · Trends in Cell Biology · doi:10.1016/j.tcb.2007.04.004 · Cited by 317
Hypoxia signalling controls metabolic demand
Brahimi-Horn, M. C., Chiche, J., & Pouysségur, J. (2007) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2007.02.003 · Cited by 298
The Redox Basis of Epigenetic Modifications: From Mechanisms to Functional Consequences
Cyr, A. R., & Domann, F. E. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3492 · Cited by 301
Cancer-associated IDH mutations: biomarker and therapeutic opportunities
Yen, K. E., Bittinger, M. A., Su, S. M., & Fantin, V. R. (2010) · Oncogene · doi:10.1038/onc.2010.444 · Cited by 296
Cancer metabolism: The Warburg effect today
Ferreira, L. M. R. (2010) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2010.08.006 · Cited by 290
Biswas, S., Dodwadkar, N. S., Deshpande, P. P., & Torchilin, V. P. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.01.009 · Cited by 281
Jia, D., Park, J. E., Jung, K., Levine, H., & Kaipparettu, B. A. (2018) · Cells · doi:10.3390/cells7030021 · Cited by 283
The Influence of Metabolism on Drug Response in Cancer
Zaal, E. A., & Berkers, C. R. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00500 · Cited by 272
Eichner, L. J., Perry, M.-C., Dufour, C. R., Bertos, N., Park, M., St‐Pierre, J., & Giguère, V. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.09.002 · Cited by 284
Liao, M., Yao, D., Wu, L., Luo, C., Wang, Z., Zhang, J., & Liu, B. (2023) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2023.12.003 · Cited by 299
Mitochondria in cancer: Not just innocent bystanders
Frezza, C., & Gottlieb, E. (2008) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2008.11.008 · Cited by 275
Self-citationBersten, D. C., Sullivan, A. E., Peet, D. J., & Whitelaw, M. L. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3621 · Cited by 267
The Mitochondrial Chaperone TRAP1 Promotes Neoplastic Growth by Inhibiting Succinate Dehydrogenase
Sciacovelli, M., Guzzo, G., Morello, V., Frezza, C., Zheng, L., Nannini, N., Calabrese, F., Laudiero, G., Esposito, F., Landriscina, M., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.04.019 · Cited by 272
Pathania, D., Millard, M., & Neamati, N. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.05.010 · Cited by 269
Li, L., & Li, W. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.01.004 · Cited by 257
Jung, S., Yang, W. K., Kim, J., Kim, H. S., Kim, E. J., Yun, H., Park, H., Kim, S. S., Choe, W., Kang, I., et al. (2008) · Carcinogenesis · doi:10.1093/carcin/bgn032 · Cited by 257
Tricarboxylic Acid (TCA) Cycle Intermediates: Regulators of Immune Responses
Choi, I., Son, H., & Baek, J.-H. (2021) · Life · doi:10.3390/life11010069 · Cited by 262
Meiser, J., Krämer, L., Sapcariu, S. C., Battello, N., Ghelfi, J., D'Herouel, A. F., Skupin, A., & Hiller, K. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.676817 · Cited by 243
Cancer metabolism: Key players in metabolic reprogramming
Soga, T. (2012) · Cancer Science · doi:10.1111/cas.12085 · Cited by 247
Metabolic rearrangements in primary liver cancers: cause and consequences
Satriano, L., Lewińska, M., Rodrigues, P. M., Bañales, J. M., & Andersen, J. B. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0217-8 · Cited by 245
The Role of Mitochondria in Inflammation: From Cancer to Neurodegenerative Disorders
Missiroli, S., Genovese, I., Perrone, M., Vezzani, B., Vitto, V. A. M., & Giorgi, C. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9030740 · Cited by 235
The Warburg effect is genetically determined in inherited pheochromocytomas
Favier, J., Brière, J.-J., Burnichon, N., Rivière, J., Vescovo, L., Benit, P., Giscos-Douriez, I., De Reyniès, A., Bertherat, J., Badoual, C., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007094 · Cited by 232
Sayin, V. I., LeBoeuf, S. E., Singh, S. X., Davidson, S. M., Biancur, D., Guzelhan, B. S., Alvarez, S. W., Wu, W. L., Karakousi, T. R., Zavitsanou, A. M., et al. (2017) · eLife · doi:10.7554/elife.28083 · Cited by 231
Oxidative phosphorylation in cancer cells
Solaini, G., Sgarbi, G., & Baracca, A. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.09.003 · Cited by 233
Cancer Metabolism: Current Understanding and Therapies
Counihan, J. L., Grossman, E. A., & Nomura, D. K. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00775 · Cited by 236
Succinate dehydrogenase: the complex roles of a simple enzyme
Huang, S., & Millar, A. H. (2013) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2013.02.007 · Cited by 226
Morgan, N. V., Morris, M. R., Cangül, H., Gleeson, D., Straatman-Iwanowska, A. A., Davies, N. P., Keenan, S., Pasha, S. S., Rahman, F., Gentle, D., et al. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000833 · Cited by 225
Waves of gene regulation suppress and then restore oxidative phosphorylation in cancer cells
Smolková, K., Plecitá‐Hlavatá, L., Bellancé, N., Bénard, G., Rossignol, R., & Ježek, P. (2010) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2010.05.003 · Cited by 232
Cancer Cell MetabolismPreprint
Cairns, R. A., Harris, I. S., McCracken, S. A., & Mak, T. W. (2011) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2011.76.012856 · Cited by 229
Zdzisińska, B., Żurek, A., & Kandefer-Szerszeń, M. (2017) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-016-0406-x · Cited by 221
Metabolic enzymes as oncogenes or tumor suppressors
Thompson, C. B. (2009) · New England Journal of Medicine · doi:10.1056/nejme0810213 · Cited by 213
Tong, W.-H., Sourbier, C., Kovtunovych, G., Jeong, S. Y., Vira, M., Ghosh, M., Romero, V. V., Sougrat, R., Vaulont, S., Viollet, B., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.07.018 · Cited by 212
Lactate dehydrogenase A silencing in IDH mutant gliomas
Chesnelong, C., Chaumeil, M. M., Blough, M. D., Al-Najjar, M., Stechishin, O. D., Chan, J. A., Pieper, R. O., Ronen, S. M., Weiss, S., Luchman, H. A., et al. (2014) · Neuro-Oncology · doi:10.1093/neuonc/not243 · Cited by 210
Stable isotope-resolved metabolomics and applications for drug development
Fan, T. W. ‐., Lorkiewicz, P., Sellers, K., Moseley, H., Higashi, R. M., & Lane, A. N. (2011) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2011.12.007 · Cited by 215
Wilson, G. K., Tennant, D. A., & McKeating, J. A. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.08.025 · Cited by 205
The hypoxic microenvironment: A determinant of cancer stem cell evolution
Carnero, A., & LLeonart, M. E. (2016) · BioEssays · doi:10.1002/bies.201670911 · Cited by 204
Dong, L.-F., Jameson, V. J. A., Tilly, D., Cerny, J., Mahdavian, E., Marín-Hernández, A., Hernández-Esquivel, L., Rodríguez-Enríquez, S., Stursa, J., Witting, P. K., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.186643 · Cited by 200
How does cancer cell metabolism affect tumor migration and invasion?
Han, T., Kang, D., Ji, D., Wang, X., Zhan, W., Fu, M., Xin, H.-B., & Wang, J.-B. (2013) · Cell Adhesion & Migration · doi:10.4161/cam.26345 · Cited by 198
Analysis of Cell Metabolism Using LC-MS and Isotope Tracers
Mackay, G., Zheng, L., van den Broek, N. J. F., & Gottlieb, E. (2015) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2015.05.016 · Cited by 195
Self-citationTea tree oil exhibits antifungal activity against Botrytis cinerea by affecting mitochondria
Li, Y., Shao, X., Xu, J., Wei, Y., Xu, F., & Wang, H. (2017) · Food Chemistry · doi:10.1016/j.foodchem.2017.04.172 · Cited by 196
microRNA‐122 as a regulator of mitochondrial metabolic gene network in hepatocellular carcinoma
Burchard, J., Zhang, C., Liu, A. M., Poon, R. T. P., Lee, N. P. Y., Wong, K., Sham, P. C., Lam, B., Ferguson, M. D., Tokiwa, G. Y., et al. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.58 · Cited by 197
Reactive Oxygen Species Regulate Hypoxia-Inducible Factor 1α Differentially in Cancer and Ischemia
Qutub, A. A., & Popel, A. S. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00060-08 · Cited by 196
Joyal, J., Gantner, M. L., & Smith, L. E. H. (2017) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2017.11.002 · Cited by 193
Aspuria, P.-J. P., Lunt, S. Y., Väremo, L., Vergnes, L., Gozo, M. C., Beach, J. A., Salumbides, B. C., Reue, K., Wiedemeyer, W. R., Nielsen, J., et al. (2014) · Cancer & Metabolism · doi:10.1186/2049-3002-2-21 · Cited by 192
Morscher, R. J., Aminzadeh-Gohari, S., Feichtinger, R. G., Mayr, J. A., Lang, R., Neureiter, D., Sperl, W., & Kofler, B. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129802 · Cited by 191
Mitochondrial dynamics and cancer
Grandemange, S., Herzig, S., & Martinou, J. (2008) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2008.12.001 · Cited by 180
Metabolic therapy: A new paradigm for managing malignant brain cancer
Seyfried, T. N., Flores, R. E., Poff, A. M., D’Agostino, D. P., & Mukherjee, P. (2014) · Cancer Letters · doi:10.1016/j.canlet.2014.07.015 · Cited by 183
Mei-An, S., Huang, Y., Chen, I.-T., Lee, D., Yun-Chieh, H., Li, C.-Y., Ng, T. H., Liang, S., Lin, S., Huang, S.-W., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004196 · Cited by 181
Metabolic changes in cancer: beyond the Warburg effect
Wu, W., & Zhao, S. (2013) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gms104 · Cited by 173
Ripoli, M. C., D’Aprile, A., Quarato, G., Sinnreich, M. F., Gouttenoire, J., Scrima, R., Cela, O., Boffoli, D., Heim, M. H., Moradpour, D., et al. (2009) · Journal of Virology · doi:10.1128/jvi.00769-09 · Cited by 174
Bisphenol-A Affects Male Fertility via Fertility-related Proteins in Spermatozoa
Rahman, M. S., Kwon, W., Lee, J.-S., Yoon, S., Ryu, B., & Pang, M. (2015) · Scientific Reports · doi:10.1038/srep09169 · Cited by 172
Mitochondrial dynamics in the central regulation of metabolism
Nasrallah, C. M., & Horváth, T. L. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2014.160 · Cited by 176
Kaadige, M. R., Looper, R., Kamalanaadhan, S., & Ayer, D. E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901221106 · Cited by 168
TCA Cycle Defects and Cancer: When Metabolism Tunes Redox State
Cardaci, S., & Ciriolo, M. R. (2012) · International Journal of Cell Biology · doi:10.1155/2012/161837 · Cited by 169
Landscape of the mitochondrial Hsp90 metabolome in tumours
Chae, Y. C., Angelin, A., Lisanti, S., Kossenkov, A. V., Speicher, K. D., Wang, H., Powers, J. F., Tischler, A. S., Pacák, K., Fliedner, S. M. J., et al. (2013) · Nature Communications · doi:10.1038/ncomms3139 · Cited by 162
Dimethyl fumarate, a two‐edged drug: Current status and future directions
Saidu, N. E. B., Kavian, N., Leroy, K., Jacob, C., Nicco, C., Batteux, F., & Alexandre, J. (2019) · Medicinal Research Reviews · doi:10.1002/med.21567 · Cited by 166
Malonate Promotes Adult Cardiomyocyte Proliferation and Heart Regeneration
Bae, J., Salamon, R. J., Brandt, E. B., Paltzer, W. G., Zhang, Z., Britt, E. C., Hacker, T. A., Fan, J., & Mahmoud, A. I. (2021) · Circulation · doi:10.1161/circulationaha.120.049952 · Cited by 161
Metabolic consequences of oncogenic IDH mutations
Parker, S. J., & Metallo, C. M. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.05.003 · Cited by 162
Lin, C.-C., Cheng, T., Tsai, W., Tsai, H.-J., Hu, K.-H., Chang, H., Yeh, C., Chen, Y.-C., Liao, C.-C., & Chang, W. (2012) · Scientific Reports · doi:10.1038/srep00785 · Cited by 163
Mutant Metabolic Enzymes Are at the Origin of Gliomas
Yan, H., Bigner, D. D., Velculescu, V. E., & Parsons, D. W. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-2650 · Cited by 156
Pyruvate and metabolic flexibility: illuminating a path toward selective cancer therapies
Olson, K. A., Schell, J. C., & Rutter, J. (2016) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2016.01.002 · Cited by 154
Metadata
- Authors
- King, A., Selak, M. A., & Gottlieb, E.
- Affiliations
- Cancer Research UK Scotland Institute (GB)
- Corresponding author
- Gottlieb, E
- Venue
- Oncogene
- Published
- 2006-08-07
- Volume
- 25
- Issue
- 34
- Pages
- 4675-4682
- ISSN
- 0950-9232 (ISSN-L)
- 1476-5594
- OpenAlex
- W2005828644
- Semantic Scholar
- 960f2f114b8beb17db8bd6d91cd79f788b80738a
- Cited by
- 672
- References
- 61
- Citations by year
- 2026: 21 · 2025: 22 · 2024: 19 · 2023: 25 · 2022: 42 · 2021: 39 · 2020: 38 · 2019: 37 · 2018: 37 · 2017: 42 · 2016: 39 · 2015: 37 · 2014: 42 · 2013: 37 · 2012: 52
- FWCI
- 1.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Oncogene (publishedVersion)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Ferroptosis and cancer prognosis
- Keywords
- succinate dehydrogenase, fumarate hydratase, mitochondrial dysfunction, tumour suppressor, succinic acid, fumarate, metabolic signalling, prolyl hydroxylase inhibition, pseudohypoxia, hypoxia-inducible factor, apoptosis resistance, carcinogenesis
- MeSH terms
- Fumarate Hydratase, Humans, Mitochondria, Neoplasms, Succinate Dehydrogenase, Genes, Tumor Suppressor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review