Glucose starvation greatly enhances antiproliferative and antiestrogenic potency of oligomycin A in MCF-7 breast cancer cells

Biochimie - Tập 186 - Trang 51-58 - 2021
Alexander M. Scherbakov1, Danila V. Sorokin1, Olga A. Omelchuk2, Andrey E. Shchekotikhin2, Mikhail A. Krasil’nikov1
1Blokhin National Medical Research Center of Oncology, Moscow, 115522, Russia
2Gause Institute of New Antibiotics, Moscow, 119021, Russia

Tài liệu tham khảo

Capuano, 1997, Oxidative phosphorylation enzymes in normal and neoplastic cell growth, J. Bioenerg. Biomembr., 29, 379, 10.1023/A:1022402915431 Warburg, 1927, The metabolism OF tumors IN the body, J. Gen. Physiol., 8, 519, 10.1085/jgp.8.6.519 Jurisic, 2015, The actual role of LDH as tumor marker, biochemical and clinical aspects, Adv. Exp. Med. Biol., 867, 115, 10.1007/978-94-017-7215-0_8 Radenkovic, 2013, Lactate dehydrogenase, catalase, and superoxide dismutase in tumor tissue of breast cancer patients in respect to mammographic findings, Cell Biochem. Biophys., 66, 287, 10.1007/s12013-012-9482-7 Naik, 2020, Lactate metabolism and immune modulation in breast cancer: a focused review on triple negative breast tumors, Front. Oncol., 10, 598626, 10.3389/fonc.2020.598626 Thakur, 2018, Metformin targets mitochondrial glycerophosphate dehydrogenase to control rate of oxidative phosphorylation and growth of thyroid cancer in vitro and in vivo, clinical cancer research : an, Off. J. Am. Assoc. Canc. Res., 24, 4030, 10.1158/1078-0432.CCR-17-3167 Scherbakov, 2016, The phenomenon of acquired resistance to metformin in breast cancer cells: the interaction of growth pathways and estrogen receptor signaling, IUBMB Life, 68, 281, 10.1002/iub.1481 Kafkova, 2020 Samuel, 2019, Metformin: the answer to cancer in a flower? Current knowledge and future prospects of metformin as an anti-cancer agent in breast cancer, Biomolecules, 9 Berstein, 2011, Isolated and combined action of tamoxifen and metformin in wild-type, tamoxifen-resistant, and estrogen-deprived MCF-7 cells, Breast Canc. Res. Treat., 128, 109, 10.1007/s10549-010-1072-z Narang, 2019, Recent advancements in mechanistic studies and structure activity relationship of F(o)F(1) ATP synthase inhibitor as antimicrobial agent, Eur. J. Med. Chem., 182, 111644, 10.1016/j.ejmech.2019.111644 Griffiths, 1994, Venturicidin titrates a redox cofactor of mitochondrial ATP synthase, Biochem. Soc. Trans., 22, 321S, 10.1042/bst022321s Lysenkova, 2019, Synthesis, antimicrobial and antiproliferative properties of epi-oligomycin A, the (33S)-diastereomer of oligomycin A, Nat. Prod. Res., 1 Salomon, 2001, Apoptolidin, a selective cytotoxic agent, is an inhibitor of F0F1-ATPase, Chem. Biol., 8, 71, 10.1016/S1074-5521(00)00057-0 Vatlin, 2020, Bioinformatic analysis of genes of Streptomyces xinghaiensis (fradiae) ATCC 19609 with a focus on mutations conferring resistance to oligomycin A and its derivatives, J. Global Antimicrob. Resist., 22, 47, 10.1016/j.jgar.2020.01.026 Hearne, 2020, Oligomycin-induced proton uncoupling, Toxicol. Vitro, 104907, 10.1016/j.tiv.2020.104907 Beechey, 1966, Dicyclohexylcarbodiimide--an inhibitor of oxidative phosphorylation, Biochem. Biophys. Res. Commun., 23, 75, 10.1016/0006-291X(66)90271-3 Toei, 2013, Single-molecule analysis of F0F1-ATP synthase inhibited by N,N-dicyclohexylcarbodiimide, J. Biol. Chem., 288, 25717, 10.1074/jbc.M113.482455 Salomon, 2000, Understanding and exploiting the mechanistic basis for selectivity of polyketide inhibitors of F(0)F(1)-ATPase, Proc. Natl. Acad. Sci. U.S.A., 97, 14766, 10.1073/pnas.97.26.14766 Serrill, 2015, Apoptolidins A and C activate AMPK in metabolically sensitive cell types and are mechanistically distinct from oligomycin A, Biochem. Pharmacol., 93, 251, 10.1016/j.bcp.2014.11.015 Hao, 2010, Oligomycin-induced bioenergetic adaptation in cancer cells with heterogeneous bioenergetic organization, J. Biol. Chem., 285, 12647, 10.1074/jbc.M109.084194 De Luca, 2015, Mitochondrial biogenesis is required for the anchorage-independent survival and propagation of stem-like cancer cells, Oncotarget, 6, 14777, 10.18632/oncotarget.4401 Symersky, 2012, Oligomycin frames a common drug-binding site in the ATP synthase, Proc. Natl. Acad. Sci. U.S.A., 109, 13961, 10.1073/pnas.1207912109 Momose, 2010, Mitochondrial inhibitors show preferential cytotoxicity to human pancreatic cancer PANC-1 cells under glucose-deprived conditions, Biochem. Biophys. Res. Commun., 392, 460, 10.1016/j.bbrc.2010.01.050 Danilenko, 2012, vol. 57, 3 Kuznetsov, 2018, New estrogen receptor antagonists. 3,20-Dihydroxy-19-norpregna-1,3,5(10)-trienes: synthesis, molecular modeling, and biological evaluation, Eur. J. Med. Chem., 143, 670, 10.1016/j.ejmech.2017.11.042 Reid, 2003, Cyclic, proteasome-mediated turnover of unliganded and liganded ERalpha on responsive promoters is an integral feature of estrogen signaling, Mol. Cell., 11, 695, 10.1016/S1097-2765(03)00090-X Buravchenko, 2020, Discovery of derivatives of 6(7)-amino-3-phenylquinoxaline-2-carbonitrile 1,4-dioxides: novel, hypoxia-selective HIF-1α inhibitors with strong antiestrogenic potency, Bioorg. Chem., 104, 104324, 10.1016/j.bioorg.2020.104324 Scherbakov, 2017, Steroidal pyrimidines and dihydrotriazines as novel classes of anticancer agents against hormone-dependent breast cancer cells, Front. Pharmacol., 8, 979, 10.3389/fphar.2017.00979 Scherbakov, 2019, Biological evaluation of a new brassinosteroid: antiproliferative effects and targeting estrogen receptor α pathways, Chem. Biodivers., 16, 10.1002/cbdv.201900332 Mruk, 2011, Enhanced chemiluminescence (ECL) for routine immunoblotting: an inexpensive alternative to commercially available kits, Spermatogenesis, 1, 121, 10.4161/spmg.1.2.16606 Radde, 2015, Bioenergetic differences between MCF-7 and T47D breast cancer cells and their regulation by oestradiol and tamoxifen, Biochem. J., 465, 49, 10.1042/BJ20131608 Sun, 2015, Mechanisms underlying 3-bromopyruvate-induced cell death in colon cancer, J. Bioenerg. Biomembr., 47, 319, 10.1007/s10863-015-9612-1 Parniak, 1985, Incorporation of glucose into glycogen in primary cultures of rat hepatocytes, Canad. J. Biochem. Cell. Biol. = Revue canadienne de biochimie et biologie cellulaire, 63, 333 Zhong, 2009, The glycolytic inhibitor 2-deoxyglucose activates multiple prosurvival pathways through IGF1R, J. Biol. Chem., 284, 23225, 10.1074/jbc.M109.005280 Pajak, 2019, 2-Deoxy-d-Glucose and its analogs: from diagnostic to therapeutic agents, Int. J. Mol. Sci., 21, 10.3390/ijms21010234 Hamilton, 2018, Quercetin inhibits glucose transport by binding to an exofacial site on GLUT1, Biochimie, 151, 107, 10.1016/j.biochi.2018.05.012 Cunningham, 2006, Docking studies show that D-glucose and quercetin slide through the transporter GLUT1, J. Biol. Chem., 281, 5797, 10.1074/jbc.M509422200 Coloff, 2011, Akt-dependent glucose metabolism promotes Mcl-1 synthesis to maintain cell survival and resistance to Bcl-2 inhibition, Canc. Res., 71, 5204, 10.1158/0008-5472.CAN-10-4531 Isakovic, 2007, Dual antiglioma action of metformin: cell cycle arrest and mitochondria-dependent apoptosis, Cell. Mol. Life Sci. : CMLS, 64, 1290, 10.1007/s00018-007-7080-4 Imamura, 2001, Cell cycle regulation via p53 phosphorylation by a 5’-AMP activated protein kinase activator, 5-aminoimidazole- 4-carboxamide-1-beta-D-ribofuranoside, in a human hepatocellular carcinoma cell line, Biochem. Biophys. Res. Commun., 287, 562, 10.1006/bbrc.2001.5627 Zou, 2020, mTOR signaling pathway and mTOR inhibitors in cancer: progress and challenges, Cell Biosci., 10, 31, 10.1186/s13578-020-00396-1 Popova, 2021, The role of mTOR signaling as a therapeutic target in cancer, Int. J. Mol. Sci., 22, 10.3390/ijms22041743 Raught, 2001, The target of rapamycin (TOR) proteins, Proc. Natl. Acad. Sci. U.S.A., 98, 7037, 10.1073/pnas.121145898 Raphael, 2020, Everolimus in advanced breast cancer: a systematic review and meta-analysis, Targeted Oncol., 15, 723, 10.1007/s11523-020-00770-6 Bundschuh, 2019, Therapy of patients with neuroendocrine neoplasia-evidence-based approaches and new horizons, J. Clin. Med., 8 Seo, 2003, Decrease of estrogen receptor expression and associated ERE-dependent transcription in MCF-7 breast cancer cells after oligomycin treatment, Steroids, 68, 257, 10.1016/S0039-128X(02)00179-4 Lardy, 1958, Antibiotics as tools for metabolic studies. I. A survey of toxic antibiotics in respiratory, phosphorylative and glycolytic systems, Arch. Biochem. Biophys., 78, 587, 10.1016/0003-9861(58)90383-7 Racker, 1969, Resolution and reconstitution of a Mammalian membrane, J. Gen. Physiol., 54, 38, 10.1085/jgp.54.1.38 Kobayashi, 1987, A new antitumor antibiotic produced by Streptomyces sp. MCI-2225, J. Antibiot., 40, 1053, 10.7164/antibiotics.40.1053 Mirabelli, 1985, Application of a tissue culture microtiter test for the detection of cytotoxic agents from natural products, J. Antibiot., 38, 758, 10.7164/antibiotics.38.758 Jurisic, 2011, TNF-α induced apoptosis is accompanied with rapid CD30 and slower CD45 shedding from K-562 cells, J. Membr. Biol., 239, 115, 10.1007/s00232-010-9309-7 Ratajczak, 2019, Monitoring of dynamic ATP level changes by oligomycin-modulated ATP synthase inhibition in SW480 cancer cells using fluorescent "On-Off" switching DNA aptamer, Anal. Bioanal. Chem., 411, 6899, 10.1007/s00216-019-02061-0 Souders, 2021, Mitochondria of teleost radial glia: a novel target of neuroendocrine disruption by environmental chemicals?, Comparative biochemistry and physiology, Toxicol. & Pharmacol. : CBP, 243, 108995 Yamazaki, 1992, 44-Homooligomycins A and B, new antitumor antibiotics from Streptomyces bottropensis. Producing organism, fermentation, isolation, structure elucidation and biological properties, J. Antibiot., 45, 171, 10.7164/antibiotics.45.171 Seo, 2003, Decrease of estrogen receptor expression and associated ERE-dependent transcription in MCF-7 breast cancer cells after oligomycin treatment, Steroids, 68, 257, 10.1016/S0039-128X(02)00179-4 Yang, 2015, Estrogen activates AMP-activated protein kinase in human endothelial cells via ERβ/Ca(2+)/calmodulin-dependent protein kinase kinase β pathway, Cell Biochem. Biophys., 72, 701, 10.1007/s12013-015-0521-z Lipovka, 2014, Estradiol activates AMPK through interaction with extrogen receptor beta (15.4), Faseb. J., 28, 10.1096/fasebj.28.1_supplement.15.4 Kim, 2016, Anticancer effect of metformin on estrogen receptor-positive and tamoxifen-resistant breast cancer cell lines, Oncol. Rep., 35, 2553, 10.3892/or.2016.4675 Lui, 2016, Everolimus downregulates estrogen receptor and induces autophagy in aromatase inhibitor-resistant breast cancer cells, BMC Canc., 16, 487, 10.1186/s12885-016-2490-z Irwin, 2008, Progesterone and estrogen regulate oxidative metabolism in brain mitochondria, Endocrinology, 149, 3167, 10.1210/en.2007-1227 Wang, 2001, Estradiol protects against ATP depletion, mitochondrial membrane potential decline and the generation of reactive oxygen species induced by 3-nitroproprionic acid in SK-N-SH human neuroblastoma cells, J. Neurochem., 77, 804, 10.1046/j.1471-4159.2001.00271.x Massart, 2002, Dose-dependent inhibition of mitochondrial ATP synthase by 17 beta-estradiol, Gynecol. Endocrinol. : Off. J. Int. Soc. Gynecol. Endocrinol., 16, 373, 10.1080/gye.16.5.373.377 Varghese, 2019, High glucose represses the anti-proliferative and pro-apoptotic effect of metformin in triple negative breast cancer cells, Biomolecules, 9, 10.3390/biom9010016 Litchfield, 2015, Hyperglycemia-induced metabolic compensation inhibits metformin sensitivity in ovarian cancer, Oncotarget, 6, 23548, 10.18632/oncotarget.4556 Zhu, 2016, Targeting cancer cell metabolism: the combination of metformin and 2-Deoxyglucose regulates apoptosis in ovarian cancer cells via p38 MAPK/JNK signaling pathway, Am. J. Tourism Res., 8, 4812 Ben Sahra, 2010, Targeting cancer cell metabolism: the combination of metformin and 2-deoxyglucose induces p53-dependent apoptosis in prostate cancer cells, Canc. Res., 70, 2465, 10.1158/0008-5472.CAN-09-2782