Mitochondrial oxidative phosphorylation TRAP(1)ped in tumor cells
Open accessAbstract
Many tumors undergo a dramatic metabolic shift known as the Warburg effect in which glucose utilization is favored and oxidative phosphorylation is downregulated, even when oxygen availability is plentiful. However, the mechanistic basis for this switch has remained unclear. Recently several independent groups identified tumor necrosis factor receptor-associated protein 1 (TRAP1), a mitochondrial molecular chaperone of the heat shock protein 90 (Hsp90) family, as a key modulator of mitochondrial respiration. Although all reports agree that this activity of TRAP1 has important implications for neoplastic progression, data from the different groups only partially overlap, suggesting that TRAP1 may have complex and possibly contextual effects on tumorigenesis. In this review we analyze these recent findings and attempt to reconcile these observations.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
A hypoxia response element exists in the IL-1β promoter.
“The finding that hypoxia was capable of inducing IL-1β production in astrocytes in an NF-κB-independent, HIF-1α-dependent, mechanism 28 led to the discovery of a HRE in the IL-1β promoter 2.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [28]
Succinate production is enhanced during inflammation, acting as a signal from mitochondria to cytosol to activate pro-inflammatory gene expression and generating ROS as a pro-inflammatory redox signal.
“The production of succinate is also enhanced during inflammation13, acting as a signal from mitochondria to the cytosol to activate pro-inflammatory gene expression while also generating ROS as a further pro-inflammatory redox signal28.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [28]
DMM decreases inflammation in a mouse model of sepsis.
“DMM could also decrease inflammation in a mouse model of sepsis28.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [28]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation
Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1160809 · Cited by 16,197 · see citing works
Warburg, O. (1956) · Science · doi:10.1126/science.123.3191.309 · Cited by 13,425 · see citing works
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 · see citing works
The metabolism of tumors in the body
Warburg, O., Wind, F., & Negelein, E. (1927) · Journal of General Physiology · doi:10.1085/jgp.8.6.519 · Cited by 4,416 · see citing works
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 · see citing works
Dang, C. V. (2012) · Cell · doi:10.1016/j.cell.2012.03.003 · Cited by 3,390 · see citing works
Metabolic Reprogramming: A Cancer Hallmark Even Warburg Did Not Anticipate
Ward, P. S., & Thompson, C. B. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.02.014 · Cited by 3,233 · see citing works
Cancer cell metabolism: warburg and beyond
Hsu, P. P., & Sabatini, D. M. (2008) · Cell · doi:10.1016/j.cell.2008.08.021 · Cited by 2,452 · see citing works
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 · see citing works
Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity
Weinberg, F., Hamanaka, R., Wheaton, W. W., Weinberg, S., Joseph, J., Lopez, M., Kalyanaraman, B., Mutlu, G. M., Budinger, G. R. S., & Chandel, N. S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003428107 · Cited by 1,742 · see citing works
Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics
Semenza, G. L. (2010) · Oncogene · doi:10.1038/onc.2009.441 · Cited by 1,712 · see citing works
Hypoxia, HIF1 and glucose metabolism in the solid tumour
Denko, N. C. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2468 · Cited by 1,707 · see citing works
HIF-1: upstream and downstream of cancer metabolism
Semenza, G. L. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.10.009 · Cited by 1,381 · see citing works
Glutamine and cancer: cell biology, physiology, and clinical opportunities
Hensley, C. T., Wasti, A. T., & DeBerardinis, R. J. (2013) · Journal of Clinical Investigation · doi:10.1172/jci69600 · Cited by 1,262 · see citing works
The Control of the Metabolic Switch in Cancers by Oncogenes and Tumor Suppressor Genes
Levine, A. J., & Puzio-Kuter, A. M. (2010) · Science · doi:10.1126/science.1193494 · Cited by 1,243 · see citing works
Links between metabolism and cancerPreprint
Dang, C. V. (2012) · Genes & Development · doi:10.1101/gad.189365.112 · Cited by 991 · see citing works
Vousden, K. H., & Ryan, K. M. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2715 · Cited by 959 · see citing works
Isaacs, J. S., Jung, Y. J., Mole, D. R., Lee, S., Torres-Cabala, C., Chung, Y.-L., Merino, M., Trepel, J., Zbar, B., Toro, J., et al. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.06.017 · Cited by 958 · see citing works
Self-citationHow cancer metabolism is tuned for proliferation and vulnerable to disruption
Schulze, A., & Harris, A. L. (2012) · Nature · doi:10.1038/nature11706 · Cited by 927 · see citing works
Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70
Young, J. C., Hoogenraad, N. J., & Hartl, F. U. (2003) · Cell · doi:10.1016/s0092-8674(02)01250-3 · Cited by 915 · see citing works
Observations on the carbohydrate metabolism of tumours
Crabtree, H. G. (1929) · Biochemical Journal · doi:10.1042/bj0230536 · Cited by 864 · see citing works
Miller, D. M., Thomas, S. D., Islam, A., Muench, D. E., & Sedoris, K. C. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-0977 · Cited by 844 · see citing works
mtDNA mutations increase tumorigenicity in prostate cancer
Petros, J. A., Baumann, A. K., Ruiz‐Pesini, E., Amin, M. B., Sun, C. Q., Hall, J., Lim, S.-D., Issa, M. M., Flanders, W. D., Hosseini, S. H., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408894102 · Cited by 834 · see citing works
Coller, H. A., Grandori, C., Tamayo, P., Colbert, T., Lander, E. S., Eisenman, R. N., & Golub, T. R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3260 · Cited by 823 · see citing works
Mathupala, S. P., Ko, Y. H., & Pedersen, P. L. (2006) · Oncogene · doi:10.1038/sj.onc.1209603 · Cited by 766 · see citing works
Exner, N., Lutz, A. K., Haass, C., & Winklhofer, K. F. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.170 · Cited by 652 · see citing works
Disrupting proton dynamics and energy metabolism for cancer therapy
Parks, S. K., Chiche, J., & Pouysségur, J. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3579 · Cited by 613 · see citing works
PINK1 Protects against Oxidative Stress by Phosphorylating Mitochondrial Chaperone TRAP1
Pridgeon, J. W., Olzmann, J. A., Chin, L.-S., & Li, L. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050172 · Cited by 596 · see citing works
Mitochondrial permeability transition in Ca2+-dependent apoptosis and necrosis
Rasola, A., & Bernardi, P. (2011) · Cell Calcium · doi:10.1016/j.ceca.2011.04.007 · Cited by 563 · see citing works
Self-citationMitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt
Robey, R. B., & Hay, N. (2006) · Oncogene · doi:10.1038/sj.onc.1209595 · Cited by 534 · see citing works
Metabolic Signatures Uncover Distinct Targets in Molecular Subsets of Diffuse Large B Cell Lymphoma
Caro, P., Kishan, A. U., Norberg, E., Stanley, I. A., Chapuy, B., Ficarro, S. B., Polak, K. Z., Tondera, D., Gounarides, J., Yin, H. X., et al. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.08.014 · Cited by 522 · see citing works
Diaz-Ruiz, R., Rigoulet, M., & Devin, A. (2011) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.08.010 · Cited by 486 · see citing works
Oncogenic Isocitrate Dehydrogenase Mutations: Mechanisms, Models, and Clinical Opportunities
Cairns, R. A., & Mak, T. W. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0083 · Cited by 452 · see citing works
Regulation of Tumor Cell Mitochondrial Homeostasis by an Organelle-Specific Hsp90 Chaperone Network
Kang, B. H., Plescia, J., Dohi, T., Rosa, J., Doxsey, S., & Altieri, D. C. (2007) · Cell · doi:10.1016/j.cell.2007.08.028 · Cited by 445 · see citing works
Oncometabolites: linking altered metabolism with cancer
Yang, M. H., Soga, T., & Pollard, P. J. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67228 · Cited by 424 · see citing works
The hsp90-related Protein TRAP1 Is a Mitochondrial Protein with Distinct Functional Properties
Felts, S. J., Owen, B. A. L., Nguyen, P., Trepel, J. B., Donner, D. B., & Toft, D. O. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.5.3305 · Cited by 371 · see citing works
Chen, J., & Russo, J. (2012) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2012.06.004 · Cited by 330 · see citing works
Chiara, F., Castellaro, D., Marin, O., Petronilli, V., Brusilow, W. S. A., Juhaszova, M., Sollott, S. J., Forte, M. A., Bernardi, P., & Rasola, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001852 · Cited by 291 · see citing works
Self-citationYoshida, S., Tsutsumi, S., Mühlebach, G., Sourbier, C., Lee, M.-J., Lee, S., Vartholomaiou, E., Tatokoro, M., Beebe, K. E., Miyajima, N., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220659110 · Cited by 281 · see citing works
Self-citationThe 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 269 · see citing works
Self-citationThe chaperone Hsp90: changing partners for demanding clients
Röhl, A., Rohrberg, J., & Büchner, J. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.02.003 · Cited by 268 · see citing works
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 267 · see citing works
Song, H. Y., Dunbar, J. D., Zhang, Y. X., Guo, D., & Donner, D. B. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.8.3574 · Cited by 266 · see citing works
Hypoxia and energetic tumour metabolism
Brahimi-Horn, M. C., Bellot, G. L., & Pouysségur, J. (2010) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2010.10.006 · Cited by 228 · see citing works
Rasola, A., Sciacovelli, M., Chiara, F., Pantic, B., Brusilow, W. S. A., & Bernardi, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912742107 · Cited by 225 · see citing works
Self-citationHua, G., Zhang, Q., & Fan, Z. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m703196200 · Cited by 188 · see citing works
Mathupala, S. P., Ko, Y. H., & Pedersen, P. L. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.03.025 · Cited by 186 · see citing works
Moreno‐Sánchez, R., Marín‐Hernández, Á., Saavedra, E., Pardo, J. P., Ralph, S. J., & Rodríguez‐Enríquez, S. (2014) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2014.01.025 · Cited by 185 · see citing works
Metabolic stress regulates cytoskeletal dynamics and metastasis of cancer cells
Caino, M. C., Chae, Y. C., Vaira, V., Ferrero, S., Nosotti, M., Martin, N., Weeraratna, A. T., O’Connell, M. P., Jernigan, D. L., Fatatis, A., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67841 · Cited by 181 · see citing works
Redox regulation of cancer cell migration and invasion.
Tochhawng, L., Deng, S., Pervaiz, S., & Yap, C. (2013) · Mitochondrion (Amsterdam. Print) · doi:10.1016/j.mito.2012.08.002 · Cited by 175 · see citing works
Gesualdi, N. M., Chirico, G., Pirozzi, G., et al. (2007) · Stress · doi:10.1080/10253890701314863 · Cited by 173 · see citing works
Xu, L., Voloboueva, L. A., Ouyang, Y., & Giffard, R. G. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.125 · Cited by 166 · see citing works
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 158 · see citing works
Lavery, L. A., Partridge, J. R., Ramelot, T. A., Elnatan, D., Kennedy, M. A., & Agard, D. A. (2014) · Molecular Cell · doi:10.1016/j.molcel.2013.12.023 · Cited by 158 · see citing works
Gasparre, G., Hervouet, É., de Laplanche, E., Demont, J., Pennisi, L. F., Colombel, M. C., Mège‐Lechevallier, F., Scoazec, J., Bonora, E., Smeets, R., et al. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm371 · Cited by 150 · see citing works
Masuda, Y., Shima, G., Aiuchi, T., Horie, M., Hori, K., Nakajo, S., Kajimoto, S., Shibayama‐Imazu, T., & Nakaya, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404256200 · Cited by 142 · see citing works
The Mitochondrial Chaperone Protein TRAP1 Mitigates α-Synuclein Toxicity
Butler, E. K., Voigt, A., Lutz, A. K., Toegel, J. P., Gerhardt, E., Karsten, P., Falkenburger, B. H., Reinartz, A., Winklhofer, K. F., & Schulz, J. B. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002488 · Cited by 142 · see citing works
Costantino, E., Maddalena, F., Calise, S. J., et al. (2009) · Cancer Letters · doi:10.1016/j.canlet.2009.01.018 · Cited by 139 · see citing works
Saisawat, P., Kohl, S., Hilger, A. C., Hwang, D., Gee, H. Y., Dworschak, G. C., Tasic, V. B., Pennimpede, T., NATARAJAN, S., Sperry, E. D., et al. (2013) · Kidney International · doi:10.1038/ki.2013.417 · Cited by 131 · see citing works
Costa, A. C., Loh, S. H. Y., & Martins, L. M. (2013) · Cell Death and Disease · doi:10.1038/cddis.2012.205 · Cited by 129 · see citing works
Leav, I., Plescia, J., Goel, H. L., Li, J., Jiang, Z., Cohen, R. J., Languino, L. R., & Altieri, D. C. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090521 · Cited by 128 · see citing works
Metabolic reprogramming of the tumor
Ferreira, L. M. R., Hébrant, A., & Dumont, J. E. (2012) · Oncogene · doi:10.1038/onc.2011.576 · Cited by 125 · see citing works
Icard, P., & Lincet, H. (2012) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2012.07.001 · Cited by 123 · see citing works
Tumor Biology and Prognostic Factors in Renal Cell Carcinoma
Finley, D. S., Pantuck, A. J., & Belldegrun, A. S. (2011) · The Oncologist · doi:10.1634/theoncologist.2011-s2-04 · Cited by 112 · see citing works
Control of Tumor Bioenergetics and Survival Stress Signaling by Mitochondrial HSP90s
Chae, Y. C., Caino, M. C., Lisanti, S., Ghosh, J. C., Dohi, T., Danial, N. N., Villanueva, J., Ferrero, S., Vaira, V., Santambrogio, L., et al. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.07.015 · Cited by 111 · see citing works
TRAP1 rescues PINK1 loss-of-function phenotypes
Zhang, L., Karsten, P., Hamm, S., Pogson, J. H., Müller-Rischart, A. K., Exner, N., Haass, C., Whitworth, A. J., Winklhofer, K. F., Schulz, J. B., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt132 · Cited by 109 · see citing works
Fan, A. C. Y., Bhangoo, M. K., & Young, J. C. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605250200 · Cited by 103 · see citing works
Cechetto, J. D., & Gupta, R. S. (2000) · Experimental Cell Research · doi:10.1006/excr.2000.4983 · Cited by 98 · see citing works
The ATPase Cycle of the Mitochondrial Hsp90 Analog Trap1
Leskovar, A., Wegele, H., Werbeck, N. D., Büchner, J., & Reinstein, J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709516200 · Cited by 97 · see citing works
Corti, O., & Brice, A. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.002 · Cited by 76 · see citing works
Mitochondrial remodeling in cancer metabolism and survival: Potential for new therapies
Barbosa, I. A., Machado, N. G., Skildum, A. J., Scott, P. M., & Oliveira, P. J. (2012) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2012.04.005 · Cited by 75 · see citing works
Fei, X., Huang, Y., Shi, X., & Zhang, Q. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07615.x · Cited by 74 · see citing works
Matassa, D. S., Amoroso, M. R., Agliarulo, I., Maddalena, F., Sisinni, L., Paladino, S., Romano, S., Romano, M. F., Sagar, V., Loreni, F., et al. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.379 · Cited by 73 · see citing works
Abu‐Amero, K. K., Alzahrani, A. S., Zou, M., et al. (2004) · Oncogene · doi:10.1038/sj.onc.1208292 · Cited by 71 · see citing works
Faou, P., & Hoogenraad, N. (2012) · Biochimica et Biophysica Acta · doi:10.1016/j.bbamcr.2011.12.001 · Cited by 68 · see citing works
Mitochondrial carrier protein biogenesis: role of the chaperones Hsc70 and Hsp90
Zara, V., Ferramosca, A., Robitaille-Foucher, P., Palmieri, F., & Young, J. C. (2009) · Biochemical Journal · doi:10.1042/bj20082270 · Cited by 64 · see citing works
Pantic, B., Trevisan, E., Citta, A., Rigobello, M. P., Marin, O., Bernardi, P., Salvatori, S., & Rasola, A. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.385 · Cited by 63 · see citing works
Self-citationCompartmentalized cancer drug discovery targeting mitochondrial Hsp90 chaperones
Kang, B. H., & Altieri, D. C. (2009) · Oncogene · doi:10.1038/onc.2009.227 · Cited by 57 · see citing works
The role of mitochondria in the oncogenic signal transduction
Frezza, C. (2014) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.12.013 · Cited by 52 · see citing works
Kubota, K., Inoue, K., Hashimoto, R., Kumamoto, N., Kosuga, A., Tatsumi, M., Kamijima, K., Kunugi, H., Iwata, N., Ozaki, N., et al. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06099.x · Cited by 49 · see citing works
Correlation between mitochondrial TRAP-1 expression and lymph node metastasis in colorectal cancer
Gao, J. (2012) · World Journal of Gastroenterology · doi:10.3748/wjg.v18.i41.5965 · Cited by 42 · see citing works
Aust, S., Bachmayr-Heyda, A., Pateisky, P., et al. (2012) · Molecular Cancer · doi:10.1186/1476-4598-11-69 · Cited by 42 · see citing works
TRAP1 Controls Mitochondrial Fusion/Fission Balance through Drp1 and Mff Expression
Takamura, H., Koyama, Y., Matsuzaki, S., Yamada, K., Hattori, T., Miyata, S., Takemoto, K., Tohyama, M., & Katayama, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051912 · Cited by 39 · see citing works
Picard, D. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.02.004 · Cited by 26 · see citing works
Self-citationRodríguez‐Enríquez, S., Gallardo‐Pérez, J. C., Marín‐Hernández, Á., et al. (2012) · Current Pharmaceutical Biotechnology · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The HSP90 Family: Structure, Regulation, Function, and Implications in Health and Disease
Hoter, A., El-Sabban, M. E., & Naim, H. Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092560 · Cited by 693 · see citing works
Coupling Krebs cycle metabolites to signalling in immunity and cancer
Ryan, D. G., Murphy, M. P., Frezza, C., Prag, H. A., Chouchani, E. T., O’Neill, L. A., & Mills, E. L. (2018) · Nature Metabolism · doi:10.1038/s42255-018-0014-7 · Cited by 398 · see citing works
Sung, N., Lee, J., Kim, J.-H., Chang, C., Tsai, F. T. F., & Lee, S. (2016) · Acta Crystallographica Section D Structural Biology · doi:10.1107/s2059798316009906 · Cited by 15 · see citing works
- Authors
- Rasola, A., Neckers, L., & Picard, D.
- Affiliations
- University of Padua (IT)
- National Cancer Institute (US)
- University of Geneva (CH)
- Corresponding author
- Rasola, Andrea
- Venue
- Trends in Cell Biology
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 24
- Issue
- 8
- Pages
- 455-463
- ISSN
- 0962-8924 (ISSN-L)
- PMC
- PMC7670877
- OpenAlex
- W2029103952
- Cited by
- 129
- References
- 86
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 13 · 2023: 13 · 2022: 11 · 2021: 19 · 2020: 9 · 2019: 5 · 2018: 14 · 2017: 11 · 2016: 10 · 2015: 7 · 2014: 7
- FWCI
- 1.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Trends in Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- PubMed Central (acceptedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Canton de Genève
- National Institutes of Health
- National Cancer Institute (Z01BC011032)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- TRAP1, mitochondrial oxidative phosphorylation, Warburg effect, cancer metabolism, mitochondrial respiration, HSP90, mitochondrial chaperone, glucose utilization, carcinogenesis
- MeSH terms
- Animals, Energy Metabolism, Humans, Mitochondria, Neoplasms, Oxidative Phosphorylation, HSP90 Heat-Shock Proteins, Carcinogenesis
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
