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Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Review Article

Mitochondrial Proteins as Metabolic Biomarkers and Sites for Therapeutic Intervention in Primary and Metastatic Cancers

Author(s): Diana Xochiquetzal Robledo-Cadena*, Silvia Cecilia Pacheco-Velazquez, Jorge Luis Vargas-Navarro, Joaquín Alberto Padilla-Flores, Rafael Moreno-Sanchez and Sara Rodríguez-Enríquez*

Volume 24, Issue 12, 2024

Published on: 27 November, 2023

Page: [1187 - 1202] Pages: 16

DOI: 10.2174/0113895575254320231030051124

Price: $65

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Abstract

Accelerated aerobic glycolysis is one of the main metabolic alterations in cancer, associated with malignancy and tumor growth. Although glycolysis is one of the most studied properties of tumor cells, recent studies demonstrate that oxidative phosphorylation (OxPhos) is the main ATP provider for the growth and development of cancer. In this last regard, the levels of mRNA and protein of OxPhos enzymes and transporters (including glutaminolysis, acetate and ketone bodies catabolism, free fatty acid β-oxidation, Krebs Cycle, respiratory chain, phosphorylating system- ATP synthase, ATP/ADP translocator, Pi carrier) are altered in tumors and cancer cells in comparison to healthy tissues and organs, and non-cancer cells. Both energy metabolism pathways are tightly regulated by transcriptional factors, oncogenes, and tumor-suppressor genes, all of which dictate their protein levels depending on the micro-environmental conditions and the type of cancer cell, favoring cancer cell adaptation and growth. In the present review paper, variation in the mRNA and protein levels as well as in the enzyme/ transporter activities of the OxPhos machinery is analyzed. An integral omics approach to mitochondrial energy metabolism pathways may allow for identifying their use as suitable, reliable biomarkers for early detection of cancer development and metastasis, and for envisioned novel, alternative therapies.

Graphical Abstract

[1]
Multifactorial Disease In: Kirch, W., Ed.; Encyclopedia of Public Health. ; Dordrecht: Springer, 2008.
[2]
Luo, W. Nasopharyngeal carcinoma ecology theory: Cancer as multidimensional spatiotemporal “unity of ecology and evolution” pathological ecosystem. Theranostics, 2023, 13(5), 1607-1631.
[http://dx.doi.org/10.7150/thno.82690] [PMID: 37056571]
[3]
Global Cancer Observatory https://gco.iarc.fr/ (Accessed May 23, 2018).
[4]
Tobore, T.O. On the need for the development of a cancer early detection, diagnostic, prognosis, and treatment response system. Future Sci. OA, 2020, 6(2), FSO439.
[http://dx.doi.org/10.2144/fsoa-2019-0028] [PMID: 32025328]
[5]
Slodkowska, E.A.; Ross, J.S. MammaPrint™ 70-gene signature: Another milestone in personalized medical care for breast cancer patients. Expert Rev. Mol. Diagn., 2009, 9(5), 417-422.
[http://dx.doi.org/10.1586/erm.09.32] [PMID: 19580427]
[6]
Özaslan, M.S.; Balcı, N.; Demir, Y.; Gürbüz, M.; Küfrevioğlu, Ö.İ. Inhibition effects of some antidepressant drugs on pentose phosphate pathway enzymes. Environ. Toxicol. Pharmacol., 2019, 72, 103244.
[http://dx.doi.org/10.1016/j.etap.2019.103244] [PMID: 31557707]
[7]
Warburg, O. On respiratory impairment in cancer cells. Science, 1956, 124(3215), 269-270.
[http://dx.doi.org/10.1126/science.124.3215.269] [PMID: 13351639]
[8]
Minami, S.; Warburg, O. Versuche an überlebendem Carcinomgewebe. Biochem. Z., 1923, 142, 334-350.
[9]
Chelakkot, C.; Chelakkot, V.S.; Shin, Y.; Song, K. Modulating glycolysis to improve cancer therapy. Int. J. Mol. Sci., 2023, 24(3), 2606.
[http://dx.doi.org/10.3390/ijms24032606] [PMID: 36768924]
[10]
Moreno-Sánchez, R.; Saavedra, E.; Gallardo-Pérez, J.C.; Rumjanek, F.D.; Rodríguez-Enríquez, S. Understanding the cancer cell phenotype beyond the limitations of current omics analyses. FEBS J., 2016, 283(1), 54-73.
[http://dx.doi.org/10.1111/febs.13535] [PMID: 26417966]
[11]
Cantuaria, G.; Fagotti, A.; Ferrandina, G.; Magalhaes, A.; Nadji, M.; Angioli, R.; Penalver, M.; Mancuso, S.; Scambia, G. GLUT-1 expression in ovarian carcinoma. Cancer, 2001, 92(5), 1144-1150.
[http://dx.doi.org/10.1002/1097-0142(20010901)92:5<1144:AID-CNCR1432>3.0.CO;2-T] [PMID: 11571727]
[12]
Koukourakis, M.I.; Giatromanolaki, A.; Sivridis, E.; Bougioukas, G.; Didilis, V.; Gatter, K.C.; Harris, A.L. Lactate dehydrogenase-5 (LDH-5) overexpression in non-small-cell lung cancer tissues is linked to tumour hypoxia, angiogenic factor production and poor prognosis. Br. J. Cancer, 2003, 89(5), 877-885.
[http://dx.doi.org/10.1038/sj.bjc.6601205] [PMID: 12942121]
[13]
Koukourakis, M.I.; Giatromanolaki, A.; Sivridis, E.; Gatter, K.C.; Harris, A.L. Lactate dehydrogenase 5 expression in operable colorectal cancer: Strong association with survival and activated vascular endothelial growth factor pathway--a report of the Tumour Angiogenesis Research Group. J. Clin. Oncol., 2006, 24(26), 4301-4308.
[http://dx.doi.org/10.1200/JCO.2006.05.9501] [PMID: 16896001]
[14]
Altenberg, B.; Greulich, K.O. Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes. Genomics, 2004, 84(6), 1014-1020.
[http://dx.doi.org/10.1016/j.ygeno.2004.08.010] [PMID: 15533718]
[15]
Goldman, N.A.; Katz, E.B.; Glenn, A.S.; Weldon, R.H.; Jones, J.G.; Lynch, U.; Fezzari, M.J.; Runowicz, C.D.; Goldberg, G.L.; Charron, M.J. GLUT1 and GLUT8 in endometrium and endometrial adenocarcinoma. Mod. Pathol., 2006, 19(11), 1429-1436.
[http://dx.doi.org/10.1038/modpathol.3800656] [PMID: 16892013]
[16]
Liu, G.; Zhu, J.; Yu, M.; Cai, C.; Zhou, Y.; Yu, M.; Fu, Z.; Gong, Y.; Yang, B.; Li, Y.; Zhou, Q.; Lin, Q.; Ye, H.; Ye, L.; Zhao, X.; Li, Z.; Chen, R.; Han, F.; Tang, C.; Zeng, B. Glutamate dehydrogenase is a novel prognostic marker and predicts metastases in colorectal cancer patients. J. Transl. Med., 2015, 13(1), 144.
[http://dx.doi.org/10.1186/s12967-015-0500-6] [PMID: 25947346]
[17]
He, X.; Wu, C.; Cui, Y.; Zhu, H.; Gao, Z.; Li, B.; Hua, J.; Zhao, B. The aldehyde group of gossypol induces mitochondrial apoptosis via ROS-SIRT1-p53-PUMA pathway in male germline stem cell. Oncotarget, 2017, 8(59), 100128-100140.
[http://dx.doi.org/10.18632/oncotarget.22044] [PMID: 29245965]
[18]
Sun, Z.; Chen, X.; Wang, G.; Li, L.; Fu, G.; Kuruc, M.; Wang, X. Identification of functional metabolic biomarkers from lung cancer patient serum using PEP technology. Biomark. Res., 2016, 4(1), 11.
[http://dx.doi.org/10.1186/s40364-016-0065-4] [PMID: 27252855]
[19]
Schofield, L.; Lincz, L.F.; Skelding, K.A. Unlikely role of glycolytic enzyme α-enolase in cancer metastasis and its potential as a prognostic biomarker. J. Cancer Metastasis Treat., 2020, 2020(10)
[http://dx.doi.org/10.20517/2394-4722.2019.43]
[20]
Zhu, A.; Lee, D.; Shim, H. Metabolic positron emission tomography imaging in cancer detection and therapy response. Semin. Oncol., 2011, 38(1), 55-69.
[http://dx.doi.org/10.1053/j.seminoncol.2010.11.012] [PMID: 21362516]
[21]
Pavlidis, N.; Briasoulis, E.; Hainsworth, J.; Greco, F.A. Diagnostic and therapeutic management of cancer of an unknown primary. Eur. J. Cancer, 2003, 39(14), 1990-2005.
[http://dx.doi.org/10.1016/S0959-8049(03)00547-1] [PMID: 12957453]
[22]
Podoloff, D.A. PET/CT and occult primary tumors. J. Natl. Compr. Cancer Network, 2009, 7(3), 239-244.
[http://dx.doi.org/10.6004/jnccn.2009.0019] [PMID: 19401059]
[23]
Ozeki, Y.; Abe, Y.; Kita, H.; Tamura, K.; Sakata, I.; Ishida, J.; MacHida, K. A case of primary lung cancer lesion demonstrated by F-18 FDG positron emission tomography/computed tomography (PET/CT) one year after the detection of metastatic brain tumor. Oncol. Lett., 2011, 2(4), 621-623.
[http://dx.doi.org/10.3892/ol.2011.318] [PMID: 22848237]
[24]
Landau, B.R.; Laszlo, J.; Stengle, J.; Burk, D. Certain metabolic and pharmacologic effects in cancer patients given infusions of 2-deoxy-D-glucose. J. Natl. Cancer Inst., 1958, 21(3), 485-494.
[PMID: 13576102]
[25]
Pan, Q.; Sun, Y.; Jin, Q.; Li, Q.; Wang, Q.; Liu, H.; Zhao, S. Hepatotoxicity and nephrotoxicity of 3-bromopyruvate in mice. Acta Cir. Bras., 2016, 31(11), 724-729.
[http://dx.doi.org/10.1590/s0102-865020160110000004] [PMID: 27982259]
[26]
Pacheco-Velázquez, S.C.; Robledo-Cadena, D.X.; Hernández-Reséndiz, I.; Gallardo-Pérez, J.C.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Energy metabolism drugs block triple negative breast metastatic cancer cell phenotype. Mol. Pharm., 2018, 15(6), 2151-2164.
[http://dx.doi.org/10.1021/acs.molpharmaceut.8b00015] [PMID: 29746779]
[27]
Hwa, J.S.; Park, H.J.; Jung, J.H.; Kam, S.C.; Park, H.C.; Kim, C.W.; Kang, K.R.; Hyun, J.S.; Chung, K.H. Identification of proteins differentially expressed in the conventional renal cell carcinoma by proteomic analysis. J. Korean Med. Sci., 2005, 20(3), 450-455.
[http://dx.doi.org/10.3346/jkms.2005.20.3.450] [PMID: 15953868]
[28]
Takadate, T.; Onogawa, T.; Fukuda, T.; Motoi, F.; Suzuki, T.; Fujii, K.; Kihara, M.; Mikami, S.; Bando, Y.; Maeda, S.; Ishida, K.; Minowa, T.; Hanagata, N.; Ohtsuka, H.; Katayose, Y.; Egawa, S.; Nishimura, T.; Unno, M. Novel prognostic protein markers of resectable pancreatic cancer identified by coupled shotgun and targeted proteomics using formalin-fixed paraffin-embedded tissues. Int. J. Cancer, 2013, 132(6), 1368-1382.
[http://dx.doi.org/10.1002/ijc.27797] [PMID: 22915188]
[29]
Huang, F.; Zhang, Q.; Ma, H.; Lv, Q.; Zhang, T. Expression of glutaminase is upregulated in colorectal cancer and of clinical significance. Int. J. Clin. Exp. Pathol., 2014, 7(3), 1093-1100.
[PMID: 24696726]
[30]
Pacheco-Velázquez, S.C.; Gallardo-Pérez, J.C.; Aguilar-Ponce, J.L.; Villarreal, P.; Ruiz-Godoy, L.; Pérez-Sánchez, M.; Marín-Hernández, A.; Ruiz-García, E.; Meneses-García, A.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Identification of a metabolic and canonical biomarker signature in Mexican HR+/HER2−, triple positive and triple-negative breast cancer patients. Int. J. Oncol., 2014, 45(6), 2549-2559.
[http://dx.doi.org/10.3892/ijo.2014.2676] [PMID: 25270118]
[31]
Rodríguez-Enríquez, S.; Hernández-Esquivel, L.; Marín-Hernández, A.; El Hafidi, M.; Gallardo-Pérez, J.C.; Hernández-Reséndiz, I.; Rodríguez-Zavala, J.S.; Pacheco-Velázquez, S.C.; Moreno-Sánchez, R. Mitochondrial free fatty acid β-oxidation supports oxidative phosphorylation and proliferation in cancer cells. Int. J. Biochem. Cell Biol., 2015, 65, 209-221.
[http://dx.doi.org/10.1016/j.biocel.2015.06.010] [PMID: 26073129]
[32]
Sun, X.R.; Sun, Z.; Zhu, Z.; Guan, H.X.; Li, C.Y.; Zhang, J.Y.; Zhang, Y.N.; Zhou, H.; Zhang, H.J.; Xu, H.M.; Sun, M.J. Expression of pyruvate dehydrogenase is an independent prognostic marker in gastric cancer. World J. Gastroenterol., 2015, 21(17), 5336-5344.
[http://dx.doi.org/10.3748/wjg.v21.i17.5336] [PMID: 25954108]
[33]
Williamson, S.R.; Eble, J.N.; Amin, M.B.; Gupta, N.S.; Smith, S.C.; Sholl, L.M.; Montironi, R.; Hirsch, M.S.; Hornick, J.L. Succinate dehydrogenase-deficient renal cell carcinoma: Detailed characterization of 11 tumors defining a unique subtype of renal cell carcinoma. Mod. Pathol., 2015, 28(1), 80-94.
[http://dx.doi.org/10.1038/modpathol.2014.86] [PMID: 25034258]
[34]
Cai, Z.; Deng, Y.; Ye, J.; Zhuo, Y.; Liu, Z.; Liang, Y.; Zhang, H.; Zhu, X.; Luo, Y.; Feng, Y.; Liu, R.; Chen, G.; Wu, Y.; Han, Z.; Liang, Y.; Jiang, F.; Zhong, W. Aberrant expression of citrate synthase is linked to disease progression and clinical outcome in prostate cancer. Cancer Manag. Res., 2020, 12, 6149-6163.
[http://dx.doi.org/10.2147/CMAR.S255817] [PMID: 32801864]
[35]
Ciccarone, F.; Di Leo, L.; Lazzarino, G.; Maulucci, G.; Di Giacinto, F.; Tavazzi, B.; Ciriolo, M.R. Aconitase 2 inhibits the proliferation of MCF-7 cells promoting mitochondrial oxidative metabolism and ROS/FoxO1-mediated autophagic response. Br. J. Cancer, 2020, 122(2), 182-193.
[http://dx.doi.org/10.1038/s41416-019-0641-0] [PMID: 31819175]
[36]
Aggarwal, R.K.; Luchtel, R.A.; Machha, V.; Tischer, A.; Zou, Y.; Pradhan, K.; Ashai, N.; Ramachandra, N.; Albanese, J.M.; Yang, J.; Wang, X.; Aluri, S.; Gordon, S.; Aboumohamed, A.; Gartrell, B.A.; Hafizi, S.; Pullman, J.; Shenoy, N. Functional succinate dehydrogenase deficiency is a common adverse feature of clear cell renal cancer. Proc. Natl. Acad. Sci. USA, 2021, 118(39), e2106947118.
[http://dx.doi.org/10.1073/pnas.2106947118] [PMID: 34551979]
[37]
Ma, Y.C.; Tian, P.F.; Chen, Z.P.; Yue, D.S.; Liu, C.C.; Li, C.G.; Chen, C.; Zhang, H.; Liu, H.L.; Zhang, Z.F.; Chen, L.; Zhang, B.; Wang, C.L. Urinary malate dehydrogenase 2 is a new biomarker for early detection of non-small-cell lung cancer. Cancer Sci., 2021, 112(6), 2349-2360.
[http://dx.doi.org/10.1111/cas.14845] [PMID: 33565687]
[38]
Zu, X.L.; Guppy, M. Cancer metabolism: Facts, fantasy, and fiction. Biochem. Biophys. Res. Commun., 2004, 313(3), 459-465.
[http://dx.doi.org/10.1016/j.bbrc.2003.11.136] [PMID: 14697210]
[39]
Brandon, M.; Baldi, P.; Wallace, D.C. Mitochondrial mutations in cancer. Oncogene, 2006, 25(34), 4647-4662.
[http://dx.doi.org/10.1038/sj.onc.1209607] [PMID: 16892079]
[40]
Moreno-Sánchez, R.; Rodríguez-Enríquez, S.; Marín-Hernández, A.; Saavedra, E. Energy metabolism in tumor cells. FEBS J., 2007, 274(6), 1393-1418.
[http://dx.doi.org/10.1111/j.1742-4658.2007.05686.x] [PMID: 17302740]
[41]
Rodríguez-Enríquez, S.; Marín-Hernández, A.; Gallardo-Pérez, J.C.; Carreño-Fuentes, L.; Moreno-Sánchez, R. Targeting of cancer energy metabolism. Mol. Nutr. Food Res., 2009, 53(1), 29-48.
[http://dx.doi.org/10.1002/mnfr.200700470] [PMID: 19123180]
[42]
Moreno-Sánchez, R.; Robledo-Cadena, D.X.; Pacheco-Velázquez, S.C.; Vargas Navarro, J.L.; Padilla-Flores, J.A.; Rodríguez-Enríquez, S. Estimation of energy pathway fluxes in cancer cells - Beyond the Warburg effect. Arch. Biochem. Biophys., 2023, 739, 109559.
[http://dx.doi.org/10.1016/j.abb.2023.109559] [PMID: 36906097]
[43]
Rodríguezenríquez, S.; Vitalgonzález, P.; Floresrodríguez, F.; Marínhernández, A.; Ruizazuara, L.; Morenosánchez, R. Control of cellular proliferation by modulation of oxidative phosphorylation in human and rodent fast-growing tumor cells. Toxicol. Appl. Pharmacol., 2006, 215(2), 208-217.
[http://dx.doi.org/10.1016/j.taap.2006.02.005] [PMID: 16580038]
[44]
Rodríguez-Enríquez, S.; Hernández-Esquivel, L.; Marín-Hernández, A.; Dong, L.F.; Akporiaye, E.T.; Neuzil, J.; Ralph, S.J.; Moreno-Sánchez, R. Molecular mechanism for the selective impairment of cancer mitochondrial function by a mitochondrially targeted vitamin E analogue. Biochim. Biophys. Acta Bioenerg., 2012, 1817(9), 1597-1607.
[http://dx.doi.org/10.1016/j.bbabio.2012.05.005] [PMID: 22627082]
[45]
Rodríguez-Enríquez, S.; Marín-Hernández, Á.; Gallardo-Pérez, J.C.; Pacheco-Velázquez, S.C.; Belmont-Díaz, J.A.; Robledo-Cadena, D.X.; Vargas-Navarro, J.L.; Corona de la Peña, N.A.; Saavedra, E.; Moreno-Sánchez, R. Transcriptional regulation of energy metabolism in cancer cells. Cells, 2019, 8(10), 1225.
[http://dx.doi.org/10.3390/cells8101225] [PMID: 31600993]
[46]
Ruiz-Azuara, L.; Bastian, G.; Bravo-Gómez, M.E.; Cañas, R.C.; Flores-Alamo, M.; Fuentes, I.; Mejia, C.; García-Ramos, J.C.; Serrano, A. Abstract CT408: Phase I study of one mixed chelates copper(II) compound, Casiopeína CasIIIia with antitumor activity and its mechanism of action. Cancer Res., 2014, 74(19_Supplement), CT408.
[http://dx.doi.org/10.1158/1538-7445.AM2014-CT408]
[47]
Rodríguez-Enríquez, S.; Gallardo-Pérez, J.C.; Avilés-Salas, A.; Marín-Hernández, A.; Carreño-Fuentes, L.; Maldonado-Lagunas, V.; Moreno-Sánchez, R. Energy metabolism transition in multi-cellular human tumor spheroids. J. Cell. Physiol., 2008, 216(1), 189-197.
[http://dx.doi.org/10.1002/jcp.21392] [PMID: 18264981]
[48]
Robledo-Cadena, D.X.; Gallardo-Pérez, J.C.; Dávila-Borja, V.; Pacheco-Velázquez, S.C.; Belmont-Díaz, J.A.; Ralph, S.J.; Blanco-Carpintero, B.A.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Non-steroidal anti-inflammatory drugs increase cisplatin, paclitaxel, and doxorubicin efficacy against human cervix cancer cells. Pharmaceuticals, 2020, 13(12), 463.
[http://dx.doi.org/10.3390/ph13120463] [PMID: 33333716]
[49]
Carew, J.S.; Huang, P. Mitochondrial defects in cancer. Mol. Cancer, 2002, 1(1), 9.
[http://dx.doi.org/10.1186/1476-4598-1-9] [PMID: 12513701]
[50]
Solaini, G.; Sgarbi, G.; Baracca, A. Oxidative phosphorylation in cancer cells. Biochim. Biophys. Acta Bioenerg., 2011, 1807(6), 534-542.
[http://dx.doi.org/10.1016/j.bbabio.2010.09.003] [PMID: 20849810]
[51]
Lim, E.; Wu, D.; Pal, B.; Bouras, T.; Asselin-Labat, M.L.; Vaillant, F.; Yagita, H.; Lindeman, G.J.; Smyth, G.K.; Visvader, J.E. Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res., 2010, 12(2), R21.
[http://dx.doi.org/10.1186/bcr2560] [PMID: 20346151]
[52]
Rodríguez-Enríquez, S.; Carreño-Fuentes, L.; Gallardo-Pérez, J.C.; Saavedra, E.; Quezada, H.; Vega, A.; Marín-Hernández, A.; Olín-Sandoval, V.; Torres-Márquez, M.E.; Moreno-Sánchez, R. Oxidative phosphorylation is impaired by prolonged hypoxia in breast and possibly in cervix carcinoma. Int. J. Biochem. Cell Biol., 2010, 42(10), 1744-1751.
[http://dx.doi.org/10.1016/j.biocel.2010.07.010] [PMID: 20654728]
[53]
Lopaschuk, G.D.; Ussher, J.R.; Folmes, C.D.L.; Jaswal, J.S.; Stanley, W.C. Myocardial fatty acid metabolism in health and disease. Physiol. Rev., 2010, 90(1), 207-258.
[http://dx.doi.org/10.1152/physrev.00015.2009] [PMID: 20086077]
[54]
Hall, C.N.; Klein-Flügge, M.C.; Howarth, C.; Attwell, D. Oxidative phosphorylation, not glycolysis, powers presynaptic and postsynaptic mechanisms underlying brain information processing. J. Neurosci., 2012, 32(26), 8940-8951.
[http://dx.doi.org/10.1523/JNEUROSCI.0026-12.2012] [PMID: 22745494]
[55]
Hitosugi, T.; Fan, J.; Chung, T.W.; Lythgoe, K.; Wang, X.; Xie, J.; Ge, Q.; Gu, T.L.; Polakiewicz, R.D.; Roesel, J.L.; Chen, G.Z.; Boggon, T.J.; Lonial, S.; Fu, H.; Khuri, F.R.; Kang, S.; Chen, J. Tyrosine phosphorylation of mitochondrial pyruvate dehydrogenase kinase 1 is important for cancer metabolism. Mol. Cell, 2011, 44(6), 864-877.
[http://dx.doi.org/10.1016/j.molcel.2011.10.015] [PMID: 22195962]
[56]
Yonashiro, R.; Eguchi, K.; Wake, M.; Takeda, N.; Nakayama, K. Pyruvate dehydrogenase PDH-E1β controls tumor progression by altering the metabolic status of cancer cells. Cancer Res., 2018, 78(7), 1592-1603.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-1751] [PMID: 29436427]
[57]
Lacroix, M.; Rodier, G.; Kirsh, O.; Houles, T.; Delpech, H.; Seyran, B.; Gayte, L.; Casas, F.; Pessemesse, L.; Heuillet, M.; Bellvert, F.; Portais, J.C.; Berthet, C.; Bernex, F.; Brivet, M.; Boutron, A.; Le Cam, L.; Sardet, C. E4F1 controls a transcriptional program essential for pyruvate dehydrogenase activity. Proc. Natl. Acad. Sci. USA, 2016, 113(39), 10998-11003.
[http://dx.doi.org/10.1073/pnas.1602754113] [PMID: 27621446]
[58]
Rodier, G.; Kirsh, O.; Baraibar, M.; Houlès, T.; Lacroix, M.; Delpech, H.; Hatchi, E.; Arnould, S.; Severac, D.; Dubois, E.; Caramel, J.; Julien, E.; Friguet, B.; Le Cam, L.; Sardet, C. The transcription factor E4F1 coordinates CHK1-dependent checkpoint and mitochondrial functions. Cell Rep., 2015, 11(2), 220-233.
[http://dx.doi.org/10.1016/j.celrep.2015.03.024] [PMID: 25843721]
[59]
Hernández-Reséndiz, I.; Román-Rosales, A.; García-Villa, E.; López-Macay, A.; Pineda, E.; Saavedra, E.; Gallardo-Pérez, J.C.; Alvarez-Ríos, E.; Gariglio, P.; Moreno-Sánchez, R.; Rodríguez-Enríquez, S. Dual regulation of energy metabolism by p53 in human cervix and breast cancer cells. Biochim. Biophys. Acta Mol. Cell Res., 2015, 1853(12), 3266-3278.
[http://dx.doi.org/10.1016/j.bbamcr.2015.09.033] [PMID: 26434996]
[60]
Schlichtholz, B.; Turyn, J.; Goyke, E.; Biernacki, M.; Jaskiewicz, K.; Sledzinski, Z.; Swierczynski, J. Enhanced citrate synthase activity in human pancreatic cancer. Pancreas, 2005, 30(2), 99-104.
[http://dx.doi.org/10.1097/01.mpa.0000153326.69816.7d] [PMID: 15714131]
[61]
Herting, B.; Meixensberger, J.; Roggendorf, W.; Reichmann, H. Metabolic patterns in meningiomas. J. Neurooncol., 2003, 65(2), 119-123.
[http://dx.doi.org/10.1023/B:NEON.0000003680.84840.52] [PMID: 14686730]
[62]
Crumbley, C.; Wang, Y.; Banerjee, S.; Burris, T.P. Regulation of expression of citrate synthase by the retinoic acid receptor-related orphan receptor α (RORα). PLoS One, 2012, 7(4), e33804.
[http://dx.doi.org/10.1371/journal.pone.0033804] [PMID: 22485150]
[63]
MacPherson, S.; Horkoff, M.; Gravel, C.; Hoffmann, T.; Zuber, J.; Lum, J.J. STAT3 regulation of citrate synthase is essential during the initiation of lymphocyte cell growth. Cell Rep., 2017, 19(5), 910-918.
[http://dx.doi.org/10.1016/j.celrep.2017.04.012] [PMID: 28467904]
[64]
Ren, M.; Yang, X.; Bie, J.; Wang, Z.; Liu, M.; Li, Y.; Shao, G.; Luo, J. Citrate synthase desuccinylation by SIRT5 promotes colon cancer cell proliferation and migration. Biol. Chem., 2020, 401(9), 1031-1039.
[http://dx.doi.org/10.1515/hsz-2020-0118] [PMID: 32284438]
[65]
Wang, P.; Mai, C.; Wei, Y.; Zhao, J.; Hu, Y.; Zeng, Z.; Yang, J.; Lu, W.; Xu, R.; Huang, P. Decreased expression of the mitochondrial metabolic enzyme aconitase (ACO2) is associated with poor prognosis in gastric cancer. Med. Oncol., 2013, 30(2), 552.
[http://dx.doi.org/10.1007/s12032-013-0552-5] [PMID: 23550275]
[66]
Park, A.; Lee, J.; Mun, S.; Kim, D.J.; Cha, B.H.; Moon, K.T.; Yoo, T.K.; Kang, H.G. Identification of transcription factor YY1 as a regulator of a prostate cancer-specific pathway using proteomic analysis. J. Cancer, 2017, 8(12), 2303-2311.
[http://dx.doi.org/10.7150/jca.19036] [PMID: 28819434]
[67]
de la Cruz López, K.G.; Toledo Guzmán, M.E.; Sánchez, E.O.; García Carrancá, A. mTORC1 as a regulator of mitochondrial functions and a therapeutic target in cancer. Front. Oncol., 2019, 9, 1373.
[http://dx.doi.org/10.3389/fonc.2019.01373] [PMID: 31921637]
[68]
Cunningham, J.T.; Rodgers, J.T.; Arlow, D.H.; Vazquez, F.; Mootha, V.K.; Puigserver, P. mTOR controls mitochondrial oxidative function through a YY1–PGC-1α transcriptional complex. Nature, 2007, 450(7170), 736-740.
[http://dx.doi.org/10.1038/nature06322] [PMID: 18046414]
[69]
Moreno-Sánchez, R.; Marín-Hernández, A.; Saavedra, E.; Pardo, J.P.; Ralph, S.J.; Rodríguez-Enríquez, S. Who controls the ATP supply in cancer cells? Biochemistry lessons to understand cancer energy metabolism. Int. J. Biochem. Cell Biol., 2014, 50, 10-23.
[http://dx.doi.org/10.1016/j.biocel.2014.01.025] [PMID: 24513530]
[70]
Al-Khallaf, H. Isocitrate dehydrogenases in physiology and cancer: Biochemical and molecular insight. Cell Biosci., 2017, 7(1), 37.
[http://dx.doi.org/10.1186/s13578-017-0165-3] [PMID: 28785398]
[71]
Zeng, L.; Morinibu, A.; Kobayashi, M.; Zhu, Y.; Wang, X.; Goto, Y.; Yeom, C.J.; Zhao, T.; Hirota, K.; Shinomiya, K.; Itasaka, S.; Yoshimura, M.; Guo, G.; Hammond, E.M.; Hiraoka, M.; Harada, H. Aberrant IDH3α expression promotes malignant tumor growth by inducing HIF-1-mediated metabolic reprogramming and angiogenesis. Oncogene, 2015, 34(36), 4758-4766.
[http://dx.doi.org/10.1038/onc.2014.411] [PMID: 25531325]
[72]
Tan, F.; Jiang, Y.; Sun, N.; Chen, Z.; Lv, Y.; Shao, K.; Li, N.; Qiu, B.; Gao, Y.; Li, B.; Tan, X.; Zhou, F.; Wang, Z.; Ding, D.; Wang, J.; Sun, J.; Hang, J.; Shi, S.; Feng, X.; He, F.; He, J. Identification of isocitrate dehydrogenase 1 as a potential diagnostic and prognostic biomarker for non-small cell lung cancer by proteomic analysis. Mol. Cell. Proteom., 2012, 11(2), M111.008821.
[http://dx.doi.org/10.1074/mcp.M111.008821]
[73]
Molenaar, R.J.; Radivoyevitch, T.; Maciejewski, J.P.; van Noorden, C.J.; Bleeker, F.E. The driver and passenger effects of isocitrate dehydrogenase 1 and 2 mutations in oncogenesis and survival prolongation. Biochim. Biophys. Acta, 2014, 1846(2), 326-341.
[PMID: 24880135]
[74]
SongTao, Q.; Lei, Y.; Si, G.; YanQing, D.; HuiXia, H.; XueLin, Z; LanXiao, W.; Fei, Y. IDH mutations predict longer survival and response to temozolomide in secondary glioblastoma. Cancer Sci., 2012, 103(2), 269-273.
[http://dx.doi.org/10.1111/j.1349-7006.2011.02134.x] [PMID: 22034964]
[75]
Lu, X.; Wu, N.; Yang, W.; Sun, J.; Yan, K.; Wu, J. OGDH promotes the progression of gastric cancer by regulating mitochondrial bioenergetics and Wnt/β-caten in signal pathway. OncoTargets Ther., 2019, 12, 7489-7500.
[http://dx.doi.org/10.2147/OTT.S208848] [PMID: 31686854]
[76]
Owens, K.M.; Kulawiec, M.; Desouki, M.M.; Vanniarajan, A.; Singh, K.K. Impaired OXPHOS complex III in breast cancer. PLoS One, 2011, 6(8), e23846.
[http://dx.doi.org/10.1371/journal.pone.0023846] [PMID: 21901141]
[77]
Venkatesan, A.M.; Trivedi, H.; Adams, K.T.; Kebebew, E.; Pacak, K.; Hughes, M.S. Comparison of clinical and imaging features in succinate dehydrogenase-positive versus sporadic paragangliomas. Surgery, 2011, 150(6), 1186-1193.
[http://dx.doi.org/10.1016/j.surg.2011.09.026] [PMID: 22136839]
[78]
Smestad, J.A.; Maher, L.J. III Master regulator analysis of paragangliomas carrying SDHx, VHL, or MAML3 genetic alterations. BMC Cancer, 2019, 19(1), 619.
[http://dx.doi.org/10.1186/s12885-019-5813-z] [PMID: 31234811]
[79]
Moreno-Sánchez, R.; Hernández-Esquivel, L.; Rivero-Segura, N.A.; Marín-Hernández, A.; Neuzil, J.; Ralph, S.J.; Rodríguez-Enríquez, S. Reactive oxygen species are generated by the respiratory complex II - evidence for lack of contribution of the reverse electron flow in complex I. FEBS J., 2013, 280(3), n/a..
[http://dx.doi.org/10.1111/febs.12086] [PMID: 23206332]
[80]
Ralph, S.; Pritchard, R.; Rodríguez-Enríquez, S.; Moreno-Sánchez, R.; Ralph, R. Hitting the Bull’s-Eye in metastatic cancers—NSAIDs elevate ROS in mitochondria, inducing malignant cell death. Pharmaceuticals, 2015, 8(1), 62-106.
[http://dx.doi.org/10.3390/ph8010062] [PMID: 25688484]
[81]
Pritchard, R.; Rodríguez-Enríquez, S.; Pacheco-Velázquez, S.C.; Bortnik, V.; Moreno-Sánchez, R.; Ralph, S. Celecoxib inhibits mitochondrial O2 consumption, promoting ROS dependent death of murine and human metastatic cancer cells via the apoptotic signalling pathway. Biochem. Pharmacol., 2018, 154, 318-334.
[http://dx.doi.org/10.1016/j.bcp.2018.05.013] [PMID: 29800556]
[82]
Schrader, A.; Sharaf, R.; Alanee, S.; Kenneth, O. 12- Genetic factors: Hereditary cancer predisposition syndromes in abeloff’s clinical oncology; Elsevier: Amsterdam, 2014, pp. 169-187.
[83]
Chen, T.; Wang, T.; Liang, W.; Zhao, Q.; Yu, Q.; Ma, C.M.; Zhuo, L.; Guo, D.; Zheng, K.; Zhou, C.; Wei, S.; Huang, W.; Jiang, J.; Liu, J.; Li, S.; He, J.; Jiang, Y.; Zhong, N. PAK4 Phosphorylates fumarase and blocks TGFβ-induced cell growth arrest in lung cancer cells. Cancer Res., 2019, 79(7), 1383-1397.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-2575] [PMID: 30683654]
[84]
Zhang, B.; Tornmalm, J.; Widengren, J.; Vakifahmetoglu-Norberg, H.; Norberg, E. Characterization of the role of the malate dehydrogenases to lung tumor cell survival. J. Cancer, 2017, 8(11), 2088-2096.
[http://dx.doi.org/10.7150/jca.19373] [PMID: 28819410]
[85]
Ma, J.T.; Han, C.B.; Zhou, Y.; Zhao, J.Z.; Jing, W.; Zou, H.W. Altered expression of mitochondrial cytochrome c oxidase I and NADH dehydrogenase 4 transcripts associated with gastric tumorigenesis and tumor dedifferentiation. Mol. Med. Rep., 2012, 5(6), 1526-1530.
[PMID: 22407105]
[86]
Wang, P.; Cheng, X.; Fu, Z.; Zhou, C.; Lu, W.; Xie, X. Reduced expression of NDUFS3 and its clinical significance in serous ovarian cancer. Int. J. Gynecol. Cancer, 2013, 23(4), 622-629.
[http://dx.doi.org/10.1097/IGC.0b013e318287a90d] [PMID: 23446378]
[87]
Damm, F.; Bunke, T.; Thol, F.; Markus, B.; Wagner, K.; Göhring, G.; Schlegelberger, B.; Heil, G.; Reuter, C.W.M.; Püllmann, K.; Schlenk, R.F.; Döhner, K.; Heuser, M.; Krauter, J.; Döhner, H.; Ganser, A.; Morgan, M.A. Prognostic implications and molecular associations of NADH dehydrogenase subunit 4 (ND4) mutations in acute myeloid leukemia. Leukemia, 2012, 26(2), 289-295.
[http://dx.doi.org/10.1038/leu.2011.200] [PMID: 21826063]
[88]
Rodríguez-Enríquez, S.; Torres-Márquez, M.E.; Moreno-Sánchez, R. Substrate oxidation and ATP supply in AS-30D hepatoma cells. Arch. Biochem. Biophys., 2000, 375(1), 21-30.
[http://dx.doi.org/10.1006/abbi.1999.1582] [PMID: 10683245]
[89]
Evans, M.J.; Scarpulla, R.C. NRF-1: A trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev., 1990, 4(6), 1023-1034.
[http://dx.doi.org/10.1101/gad.4.6.1023] [PMID: 2166701]
[90]
Lascorz, J.; Bevier, M.; Schönfels, W.V.; Kalthoff, H.; Aselmann, H.; Beckmann, J.; Egberts, J.; Buch, S.; Becker, T.; Schreiber, S.; Hampe, J.; Hemminki, K.; Försti, A.; Schafmayer, C. Polymorphisms in the mitochondrial oxidative phosphorylation chain genes as prognostic markers for colorectal cancer. BMC Med. Genet., 2012, 13(1), 31.
[http://dx.doi.org/10.1186/1471-2350-13-31] [PMID: 22545919]
[91]
Elsner, M.; Rauser, S.; Maier, S.; Schöne, C.; Balluff, B.; Meding, S.; Jung, G.; Nipp, M.; Sarioglu, H.; Maccarrone, G.; Aichler, M.; Feuchtinger, A.; Langer, R.; Jütting, U.; Feith, M.; Küster, B.; Ueffing, M.; Zitzelsberger, H.; Höfler, H.; Walch, A. MALDI imaging mass spectrometry reveals COX7A2, TAGLN2 and S100-A10 as novel prognostic markers in Barrett’s adenocarcinoma. J. Proteom., 2012, 75(15), 4693-4704.
[http://dx.doi.org/10.1016/j.jprot.2012.02.012] [PMID: 22365974]
[92]
Fukuda, R.; Zhang, H.; Kim, J.; Shimoda, L.; Dang, C.V.; Semenza, G.L. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell, 2007, 129(1), 111-122.
[http://dx.doi.org/10.1016/j.cell.2007.01.047] [PMID: 17418790]
[93]
Seelan, R.S.; Grossman, L.I. Structural organization and promoter analysis of the bovine cytochrome c oxidase subunit VIIc gene. A functional role for YY1. J. Biol. Chem., 1997, 272(15), 10175-10181.
[http://dx.doi.org/10.1074/jbc.272.15.10175] [PMID: 9092564]
[94]
Audet-Walsh, É.; Dufour, C.R.; Yee, T.; Zouanat, F.Z.; Yan, M.; Kalloghlian, G.; Vernier, M.; Caron, M.; Bourque, G.; Scarlata, E.; Hamel, L.; Brimo, F.; Aprikian, A.G.; Lapointe, J.; Chevalier, S.; Giguère, V. Nuclear mTOR acts as a transcriptional integrator of the androgen signaling pathway in prostate cancer. Genes Dev., 2017, 31(12), 1228-1242.
[http://dx.doi.org/10.1101/gad.299958.117] [PMID: 28724614]
[95]
Huang, D.; Li, T.; Li, X.; Zhang, L.; Sun, L.; He, X.; Zhong, X.; Jia, D.; Song, L.; Semenza, G.L.; Gao, P.; Zhang, H. HIF-1-mediated suppression of acyl-CoA dehydrogenases and fatty acid oxidation is critical for cancer progression. Cell Rep., 2014, 8(6), 1930-1942.
[http://dx.doi.org/10.1016/j.celrep.2014.08.028] [PMID: 25242319]
[96]
Xiang, L.; Mou, J.; Shao, B.; Wei, Y.; Liang, H.; Takano, N.; Semenza, G.L.; Xie, G. Glutaminase 1 expression in colorectal cancer cells is induced by hypoxia and required for tumor growth, invasion, and metastatic colonization. Cell Death Dis., 2019, 10(2), 40.
[http://dx.doi.org/10.1038/s41419-018-1291-5] [PMID: 30674873]
[97]
Kim, J.H.; Lee, J.; Cho, Y.R.; Lee, S.Y.; Sung, G.J.; Shin, D.M.; Choi, K.C.; Son, J. TFEB Supports pancreatic cancer growth through the transcriptional regulation of glutaminase. Cancers, 2021, 13(3), 483.
[http://dx.doi.org/10.3390/cancers13030483] [PMID: 33513833]
[98]
Lukey, M.J.; Greene, K.S.; Erickson, J.W.; Wilson, K.F.; Cerione, R.A. The oncogenic transcription factor c-Jun regulates glutaminase expression and sensitizes cells to glutaminase-targeted therapy. Nat. Commun., 2016, 7(1), 11321.
[http://dx.doi.org/10.1038/ncomms11321] [PMID: 27089238]
[99]
Juraszek, B.; Nałęcz, K.A. SLC22A5 (OCTN2) carnitine transporter—indispensable for cell metabolism, a jekyll and hyde of human cancer. Molecules, 2019, 25(1), 14.
[http://dx.doi.org/10.3390/molecules25010014] [PMID: 31861504]
[100]
Djouadi, F.; Aubey, F.; Schlemmer, D.; Bastin, J. Peroxisome proliferator activated receptor delta (PPARdelta) agonist but not PPARalpha corrects carnitine palmitoyl transferase 2 deficiency in human muscle cells. J. Clin. Endocrinol. Metab., 2005, 90(3), 1791-1797.
[http://dx.doi.org/10.1210/jc.2004-1936] [PMID: 15613406]
[101]
Yu, D.; Li, H.W.; Wang, Y.; Li, C.Q.; You, D.; Jiang, L.; Song, Y.P.; Li, X.H. Acyl-CoA dehydrogenase long chain expression is associated with esophageal squamous cell carcinoma progression and poor prognosis. OncoTargets Ther., 2018, 11, 7643-7653.
[http://dx.doi.org/10.2147/OTT.S171963] [PMID: 30464513]
[102]
Yu, Y.; Zhao, L.; Li, R. Medium-chain acyl-CoA dehydrogenase enhances invasion and metastasis ability of breast cancer cells Nan Fang Yi Ke Da Xue Xue Bao, 2019, 39(6), 650-656.
[PMID: 31270042]
[103]
Wu, Q.; Yan, T.; Chen, Y.; Chang, J.; Jiang, Y.; Zhu, D.; Wei, Y. Integrated analysis of expression and prognostic values of Acyl-CoA dehydrogenase short-chain in colorectal cancer. Int. J. Med. Sci., 2021, 18(16), 3631-3643.
[http://dx.doi.org/10.7150/ijms.63953] [PMID: 34790035]
[104]
Douglas, D.N.; Pu, C.H.; Lewis, J.T.; Bhat, R.; Anwar-Mohamed, A.; Logan, M.; Lund, G.; Addison, W.R.; Lehner, R.; Kneteman, N.M. Oxidative stress attenuates lipid synthesis and increases mitochondrial fatty acid oxidation in hepatoma cells infected with hepatitis C virus. J. Biol. Chem., 2016, 291(4), 1974-1990.
[http://dx.doi.org/10.1074/jbc.M115.674861] [PMID: 26627833]
[105]
Yeh, C.S.; Wang, J.Y.; Cheng, T.L.; Juan, C.H.; Wu, C.H.; Lin, S.R. Fatty acid metabolism pathway play an important role in carcinogenesis of human colorectal cancers by Microarray-Bioinformatics analysis. Cancer Lett., 2006, 233(2), 297-308.
[http://dx.doi.org/10.1016/j.canlet.2005.03.050] [PMID: 15885896]
[106]
Fan, J.; Lin, R.; Xia, S.; Chen, D.; Elf, S.E.; Liu, S.; Pan, Y.; Xu, H.; Qian, Z.; Wang, M.; Shan, C.; Zhou, L.; Lei, Q.Y.; Li, Y.; Mao, H.; Lee, B.H.; Sudderth, J.; DeBerardinis, R.J.; Zhang, G.; Owonikoko, T.; Gaddh, M.; Arellano, M.L.; Khoury, H.J.; Khuri, F.R.; Kang, S.; Doetsch, P.W.; Lonial, S.; Boggon, T.J.; Curran, W.J.; Chen, J. Tetrameric Acetyl-CoA acetyltransferase 1 is important for tumor growth. Mol. Cell, 2016, 64(5), 859-874.
[http://dx.doi.org/10.1016/j.molcel.2016.10.014] [PMID: 27867011]
[107]
Ayyagari, V.N.; Wang, X.; Diaz-Sylvester, P.L.; Groesch, K.; Brard, L. Assessment of acyl-CoA cholesterol acyltransferase (ACAT-1) role in ovarian cancer progression—An in vitro study. PLoS One, 2020, 15(1), e0228024.
[http://dx.doi.org/10.1371/journal.pone.0228024] [PMID: 31978092]
[108]
Schug, Z.T.; Peck, B.; Jones, D.T.; Zhang, Q.; Grosskurth, S.; Alam, I.S.; Goodwin, L.M.; Smethurst, E.; Mason, S.; Blyth, K.; McGarry, L.; James, D.; Shanks, E.; Kalna, G.; Saunders, R.E.; Jiang, M.; Howell, M.; Lassailly, F.; Thin, M.Z.; Spencer-Dene, B.; Stamp, G.; van den Broek, N.J.F.; Mackay, G.; Bulusu, V.; Kamphorst, J.J.; Tardito, S.; Strachan, D.; Harris, A.L.; Aboagye, E.O.; Critchlow, S.E.; Wakelam, M.J.O.; Schulze, A.; Gottlieb, E. Acetyl-CoA synthetase 2 promotes acetate utilization and maintains cancer cell growth under metabolic stress. Cancer Cell, 2015, 27(1), 57-71.
[http://dx.doi.org/10.1016/j.ccell.2014.12.002] [PMID: 25584894]
[109]
Rodríguez-Enríquez, S.; Robledo-Cadena, D.X.; Gallardo-Pérez, J.C.; Pacheco-Velázquez, S.C.; Vázquez, C.; Saavedra, E.; Vargas-Navarro, J.L.; Blanco-Carpintero, B.A.; Marín-Hernández, Á.; Jasso-Chávez, R.; Encalada, R.; Ruiz-Godoy, L.; Aguilar-Ponce, J.L.; Moreno-Sánchez, R. Acetate promotes a differential energy metabolic response in human HCT 116 and COLO 205 colon cancer cells impacting cancer cell growth and invasiveness. Front. Oncol., 2021, 11, 697408.
[http://dx.doi.org/10.3389/fonc.2021.697408] [PMID: 34414111]
[110]
Mamoor, S. Over-expression of Propionyl-Coa carboxylase beta subunit in human endometrial cancer. OSF Preprints, 2021, 142(3), 649.
[http://dx.doi.org/10.31219/osf.io/qmg4c]
[111]
Ma, S.L.; Li, A.J.; Hu, Z.Y.; Shang, F.S.; Wu, M.C. Co-expression of the carbamoyl-phosphate synthase 1 gene and its long non-coding RNA correlates with poor prognosis of patients with intrahepatic cholangiocarcinoma. Mol. Med. Rep., 2015, 12(6), 7915-7926.
[http://dx.doi.org/10.3892/mmr.2015.4435] [PMID: 26499888]
[112]
Wu, G.; Zhao, Z.; Yan, Y.; Zhou, Y.; Wei, J.; Chen, X.; Lin, W.; Ou, C.; Li, J.; Wang, X.; Xiong, K.; Zhou, J.; Xu, Z. CPS1 expression and its prognostic significance in lung adenocarcinoma. Ann. Transl. Med., 2020, 8(6), 341.
[http://dx.doi.org/10.21037/atm.2020.02.146] [PMID: 32355785]
[113]
Çeliktaş, M.; Tanaka, I.; Chandra Tripathi, S.; Fahrmann, J.F.; Aguilar-Bonavides, C.; Villalobos, P.; Delgado, O.; Dhillon, D.; Dennison, J.B.; Ostrin, E.J.; Wang, H.; Behrens, C.; Do, K.A.; Gazdar, A.F.; Hanash, S.M.; Taguchi, A. Role of CPS1 in cell growth, metabolism, and prognosis in LKB1-Inactivated lung adenocarcinoma. J. Natl. Cancer Inst., 2017, 109(3), djw231.
[http://dx.doi.org/10.1093/jnci/djw231] [PMID: 28376202]
[114]
Hu, Y.; Rosen, D.G.; Zhou, Y.; Feng, L.; Yang, G.; Liu, J.; Huang, P. Mitochondrial manganese-superoxide dismutase expression in ovarian cancer: Role in cell proliferation and response to oxidative stress. J. Biol. Chem., 2005, 280(47), 39485-39492.
[http://dx.doi.org/10.1074/jbc.M503296200] [PMID: 16179351]
[115]
Xu, Y.; Porntadavity, S.; St Clair, D.K. Transcriptional regulation of the human manganese superoxide dismutase gene: The role of specificity protein 1 (Sp1) and activating protein-2 (AP-2). Biochem. J., 2002, 362(2), 401-412.
[http://dx.doi.org/10.1042/bj3620401] [PMID: 11853549]

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