Targeting glycolysis for cancer therapy using drug delivery systems

Journal of Controlled Release - Tập 353 - Trang 650-662 - 2023
Yongzhuo Huang1,2
1Zhongshan Institute for Drug Discovery, SIMM, CAS, China
2Shanghai Institute of Materia Medica Chinese Academy of Science, China

Tài liệu tham khảo

Ward, 2012, Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate, Cancer Cell, 21, 297, 10.1016/j.ccr.2012.02.014 Hanahan, 2011, Hallmarks of cancer: the next generation, Cell, 144, 646, 10.1016/j.cell.2011.02.013 Pavlova, 2016, The emerging hallmarks of Cancer metabolism, Cell Metab., 23, 27, 10.1016/j.cmet.2015.12.006 Liberti, 2016, The Warburg effect: how does it benefit Cancer cells?, Trends Biochem. Sci., 41, 211, 10.1016/j.tibs.2015.12.001 Warburg, 1956, On the origin of cancer cells, Science, 123, 309, 10.1126/science.123.3191.309 Schell, 2014, A role for the mitochondrial pyruvate carrier as a repressor of the Warburg effect and colon cancer cell growth, Mol. Cell, 56, 400, 10.1016/j.molcel.2014.09.026 Jose, 1807, Choosing between glycolysis and oxidative phosphorylation: a tumor’s dilemma?, Biochim. Biophys. Acta, 2011, 552 Hargreaves, 2020, Skeletal muscle energy metabolism during exercise, Nat. Metab., 2, 817, 10.1038/s42255-020-0251-4 Mookerjee, 2017, Quantifying intracellular rates of glycolytic and oxidative ATP production and consumption using extracellular flux measurements, J. Biol. Chem., 292, 7189, 10.1074/jbc.M116.774471 Hayes, 2021, The oncogenic and clinical implications of lactate induced immunosuppression in the tumour microenvironment, Cancer Lett., 500, 75, 10.1016/j.canlet.2020.12.021 Feng, 2017, Tumor cell-derived lactate induces TAZ-dependent upregulation of PD-L1 through GPR81 in human lung cancer cells, Oncogene, 36, 5829, 10.1038/onc.2017.188 Colegio, 2014, Functional polarization of tumour-associated macrophages by tumour-derived lactic acid, Nature, 513, 559, 10.1038/nature13490 Brand, 2016, LDHA-associated lactic acid production blunts tumor immunosurveillance by T and NK cells, Cell Metab., 24, 657, 10.1016/j.cmet.2016.08.011 Watson, 2021, Metabolic support of tumour-infiltrating regulatory T cells by lactic acid, Nature, 591, 645, 10.1038/s41586-020-03045-2 Zhang, 2019, Metabolic regulation of gene expression by histone lactylation, Nature, 574, 575, 10.1038/s41586-019-1678-1 Noe, 2021, Lactate supports a metabolic-epigenetic link in macrophage polarization, Sci. Adv., 7, eabi8602, 10.1126/sciadv.abi8602 Wen, 2021, Lactate anions participate in T cell cytokine production and function, Sci. China Life Sci., 64, 1895, 10.1007/s11427-020-1887-7 Rundqvist, 2019, Lactate potentiates differentiation and expansion of cytotoxic T cells, bioRxiv, 571745 Li, 2020, Cancer cells don’t live alone: metabolic communication within tumor microenvironments, Dev. Cell, 54, 183, 10.1016/j.devcel.2020.06.018 Hui, 2017, Glucose feeds the TCA cycle via circulating lactate, Nature, 551, 115, 10.1038/nature24057 Pinheiro, 2016, The metabolic microenvironment of melanomas: prognostic value of MCT1 and MCT4, Cell Cycle, 15, 1462, 10.1080/15384101.2016.1175258 Eilertsen, 2014, Monocarboxylate transporters 1-4 in NSCLC: MCT1 is an independent prognostic marker for survival, PLoS One, 9, 10.1371/journal.pone.0105038 Miranda-Goncalves, 2021, MCT1 is a new prognostic biomarker and its therapeutic inhibition boosts response to temozolomide in human glioblastoma, Cancers (Basel), 13, 3468, 10.3390/cancers13143468 Puri, 2020, Monocarboxylate transporter 1 and 4 inhibitors as potential therapeutics for treating solid tumours: a review with structure-activity relationship insights, Eur. J. Med. Chem., 199, 10.1016/j.ejmech.2020.112393 Pavlides, 2009, The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma, Cell Cycle, 8, 3984, 10.4161/cc.8.23.10238 Bonuccelli, 2010, Ketones and lactate “fuel” tumor growth and metastasis: evidence that epithelial cancer cells use oxidative mitochondrial metabolism, Cell Cycle, 9, 3506, 10.4161/cc.9.17.12731 Bhattacharya, 2016, The Warburg effect and drug resistance, Br. J. Pharmacol., 173, 970, 10.1111/bph.13422 Marcucci, 2021, Glycolysis-induced drug resistance in tumors-a response to danger signals?, Neoplasia, 23, 234, 10.1016/j.neo.2020.12.009 Abacka, 2021, Targeting GLUT1 in acute myeloid leukemia to overcome cytarabine resistance, Haematologica, 106, 1163, 10.3324/haematol.2020.246843 Wang, 2018, Glycolysis is essential for chemoresistance induced by transient receptor potential channel C5 in colorectal cancer, BMC Cancer, 18, 207, 10.1186/s12885-018-4123-1 Li, 2017, Genistein suppresses aerobic glycolysis and induces hepatocellular carcinoma cell death, Br. J. Cancer, 117, 1518, 10.1038/bjc.2017.323 Wang, 2019, Wnt1-inducible signaling protein 1 regulates laryngeal squamous cell carcinoma glycolysis and chemoresistance via the YAP1/TEAD1/GLUT1 pathway, J. Cell. Physiol., 234, 15941, 10.1002/jcp.28253 Martin, 2020, PKM2 inhibition may reverse therapeutic resistance to transarterial chemoembolization in hepatocellular carcinoma, J. Exp. Clin. Cancer Res., 39, 99, 10.1186/s13046-020-01605-y de la Cruz-Lopez, 2019, Lactate in the regulation of tumor microenvironment and therapeutic approaches, Front. Oncol., 9, 1143, 10.3389/fonc.2019.01143 Dong, 2020, Lactate-induced MRP1 expression contributes to metabolism-based etoposide resistance in non-small cell lung cancer cells, Cell Commun. Signal., 18, 167, 10.1186/s12964-020-00653-3 Franklin, 2020, MEK activation modulates glycolysis and supports suppressive myeloid cells in TNBC, JCI Insight, 5, 10.1172/jci.insight.134290 Apicella, 2018, Increased lactate secretion by cancer cells sustains non-cell-autonomous adaptive resistance to MET and EGFR targeted therapies, Cell Metab., 28, 848, 10.1016/j.cmet.2018.08.006 Barnes, 2020, Lactic acidosis induces resistance to the pan-Akt inhibitor uprosertib in colon cancer cells, Br. J. Cancer, 122, 1298, 10.1038/s41416-020-0777-y Li, 2020, N(6)-methyladenosine regulates glycolysis of cancer cells through PDK4, Nat. Commun., 11, 2578, 10.1038/s41467-020-16306-5 Li, 2020, ALKBH5 regulates anti-PD-1 therapy response by modulating lactate and suppressive immune cell accumulation in tumor microenvironment, Proc. Natl. Acad. Sci. U. S. A., 117, 20159, 10.1073/pnas.1918986117 Daneshmandi, 2019, Blockade of lactate dehydrogenase-a (LDH-A) improves efficacy of anti-programmed cell Death-1 (PD-1) therapy in melanoma, Cancers (Basel), 11, 450, 10.3390/cancers11040450 Yang, 2020, The enhancement of glycolysis regulates pancreatic cancer metastasis, Cell. Mol. Life Sci., 77, 305, 10.1007/s00018-019-03278-z Jia, 2021, Towards decoding the coupled decision-making of metabolism and epithelial-to-mesenchymal transition in cancer, Br. J. Cancer, 124, 1902, 10.1038/s41416-021-01385-y Shiraishi, 2015, Glycolysis is the primary bioenergetic pathway for cell motility and cytoskeletal remodeling in human prostate and breast cancer cells, Oncotarget, 6, 130, 10.18632/oncotarget.2766 Liu, 2016, Epithelial-mesenchymal transition induction is associated with augmented glucose uptake and lactate production in pancreatic ductal adenocarcinoma, Cancer Metab., 4, 19, 10.1186/s40170-016-0160-x Dong, 2021, Long non-coding RNA DLEU2 drives EMT and glycolysis in endometrial cancer through HK2 by competitively binding with miR-455 and by modulating the EZH2/miR-181a pathway, J. Exp. Clin. Cancer Res., 40, 216, 10.1186/s13046-021-02018-1 Hamabe, 2014, Role of pyruvate kinase M2 in transcriptional regulation leading to epithelial-mesenchymal transition, Proc. Natl. Acad. Sci. U. S. A., 111, 15526, 10.1073/pnas.1407717111 Fan, 2014, PKM2 regulates hepatocellular carcinoma cell epithelial-mesenchymal transition and migration upon EGFR activation, Asian Pac. J. Cancer Prev., 15, 1961, 10.7314/APJCP.2014.15.5.1961 Hou, 2019, LDH-A promotes malignant behavior via activation of epithelial-to-mesenchymal transition in lung adenocarcinoma, Biosci. Rep., 39, 10.1042/BSR20181476 Zetter, 1998, Angiogenesis and tumor metastasis, Annu. Rev. Med., 49, 407, 10.1146/annurev.med.49.1.407 Weidner, 1991, Tumor angiogenesis and metastasis—correlation in invasive breast carcinoma, N. Engl. J. Med., 324, 1, 10.1056/NEJM199101033240101 Schwickert, 1995, Correlation of high lactate levels in human cervical cancer with incidence of metastasis, Cancer Res., 55, 4757 Phypers, 2006, Lactate physiology in health and disease, Continuing Educ. Anaesthesia Crit. Care Pain, 6, 128, 10.1093/bjaceaccp/mkl018 Vegran, 2011, Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kappaB/IL-8 pathway that drives tumor angiogenesis, Cancer Res., 71, 2550, 10.1158/0008-5472.CAN-10-2828 Sonveaux, 2012, Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis, PLoS One, 7, 10.1371/journal.pone.0033418 Ruan, 2013, Lactate engages receptor tyrosine kinases Axl, Tie2, and vascular endothelial growth factor receptor 2 to activate phosphoinositide 3-kinase/Akt and promote angiogenesis, J. Biol. Chem., 288, 21161, 10.1074/jbc.M113.474619 Butler, 1975, Quantitation of cell shedding into efferent blood of mammary adenocarcinoma, Cancer Res., 35, 512 Fidler, 1970, Metastasis: quantitative analysis of distribution and fate of tumor emboli labeled with 125 I-5-iodo-2′-deoxyuridine, J. Natl. Cancer Inst., 45, 773 Liu, 2015, PKM2 promotes metastasis by recruiting myeloid-derived suppressor cells and indicates poor prognosis for hepatocellular carcinoma, Oncotarget, 6, 846, 10.18632/oncotarget.2749 Morrissey, 2021, Tumor-derived exosomes drive immunosuppressive macrophages in a pre-metastatic niche through glycolytic dominant metabolic reprogramming, Cell Metab., 33, 2040, 10.1016/j.cmet.2021.09.002 Sun, 2019, Oxidized ATM-mediated glycolysis enhancement in breast cancer-associated fibroblasts contributes to tumor invasion through lactate as metabolic coupling, EBioMedicine, 41, 370, 10.1016/j.ebiom.2019.02.025 Oh, 2017, Glut1 promotes cell proliferation, migration and invasion by regulating epidermal growth factor receptor and integrin signaling in triple-negative breast cancer cells, BMB Rep., 50, 132, 10.5483/BMBRep.2017.50.3.189 Koch, 2015, Glucose transporter isoform 1 expression enhances metastasis of malignant melanoma cells, Oncotarget, 6, 32748, 10.18632/oncotarget.4977 Qian, 2021, Lactic acid promotes metastatic niche formation in bone metastasis of colorectal cancer, Cell Commun. Signal., 19, 9, 10.1186/s12964-020-00667-x Papadaki, 2020, Correlation of PKM2 and CD44 protein expression with poor prognosis in platinum-treated epithelial ovarian Cancer: a retrospective study, Cancers (Basel), 12, 1013, 10.3390/cancers12041013 Li, 2021, Expression and clinical significance of pyruvate kinase M2 in breast cancer: a protocol for meta-analysis and bioinformatics validation analysis, Medicine (Baltimore), 100 Sfakianaki, 2020, PKM2 expression as biomarker for resistance to Oxaliplatin-based chemotherapy in colorectal Cancer, Cancers (Basel), 12, 10.3390/cancers12082058 Chen, 2011, Shikonin and its analogs inhibit cancer cell glycolysis by targeting tumor pyruvate kinase-M2, Oncogene, 30, 4297, 10.1038/onc.2011.137 Li, 2014, Sensitizing the therapeutic efficacy of taxol with shikonin in human breast cancer cells, PLoS One, 9 Liu, 2020, Experimental study of hepatocellular carcinoma treatment by Shikonin through regulating PKM2, J. Hepatocell. Carcinoma, 7, 19, 10.2147/JHC.S237614 Wang, 2019, Reprogramming tumor immune microenvironment (TIME) and metabolism via biomimetic targeting Codelivery of Shikonin/JQ1, Nano Lett., 19, 2935, 10.1021/acs.nanolett.9b00021 Mo, 2018, Antiglioma via regulating oxidative stress and remodeling tumor-associated macrophage using lactoferrin-mediated biomimetic codelivery of simvastatin/fenretinide, J. Control. Release, 287, 12, 10.1016/j.jconrel.2018.08.012 Zhao, 2022, Anti-alcoholism drug disulfiram for targeting glioma energy metabolism using BBB-penetrating delivery of fixed-dose combination, Nano Today, 44, 10.1016/j.nantod.2022.101448 Mossmann, 2018, mTOR signalling and cellular metabolism are mutual determinants in cancer, Nat. Rev. Cancer, 18, 744, 10.1038/s41568-018-0074-8 Howell, 2013, A growing role for mTOR in promoting anabolic metabolism, Biochem. Soc. Trans., 41, 906, 10.1042/BST20130041 Poulain, 2017, High mTORC1 activity drives glycolysis addiction and sensitivity to G6PD inhibition in acute myeloid leukemia cells, Leukemia, 31, 2326, 10.1038/leu.2017.81 Chen, 2020, Metabolic modulation via mTOR pathway and anti-angiogenesis remodels tumor microenvironment using PD-L1-targeting codelivery, Biomaterials, 255, 10.1016/j.biomaterials.2020.120187 Mecca, 2018, Targeting mTOR in glioblastoma: rationale and preclinical/clinical evidence, Dis. Markers, 2018, 9230479, 10.1155/2018/9230479 Crane, 2009, Honokiol-mediated inhibition of PI3K/mTOR pathway: a potential strategy to overcome immunoresistance in glioma, breast, and prostate carcinoma without impacting T cell function, J. Immunother., 32, 585, 10.1097/CJI.0b013e3181a8efe6 Zheng, 2020, Remodeling tumor immune microenvironment (TIME) for glioma therapy using multi-targeting liposomal codelivery, J. Immunother. Cancer, 8, 10.1136/jitc-2019-000207 Skrott, 2017, Alcohol-abuse drug disulfiram targets cancer via p97 segregase adaptor NPL4, Nature, 552, 194, 10.1038/nature25016 Terashima, 2020, Targeting FROUNT with disulfiram suppresses macrophage accumulation and its tumor-promoting properties, Nat. Commun., 11, 609, 10.1038/s41467-020-14338-5 Ciscato, 2021, Hexokinase 2 in Cancer: a Prima Donna playing multiple characters, Int. J. Mol. Sci., 22, 4716, 10.3390/ijms22094716 Sasaki, 2021, Nanoparticle-mediated delivery of 2-deoxy-D-glucose induces antitumor immunity and cytotoxicity in liver tumors in mice, cell Mol, Gastroenterol. Hepatol., 11, 739 Andrzejewski, 2018, Metabolic profiles associated with metformin efficacy in Cancer, Front. Endocrinol. (Lausanne), 9, 372, 10.3389/fendo.2018.00372 Salani, 2014, Metformin, cancer and glucose metabolism, Endocr. Relat. Cancer, 21, R461, 10.1530/ERC-14-0284 Elgogary, 2016, Combination therapy with BPTES nanoparticles and metformin targets the metabolic heterogeneity of pancreatic cancer, Proc. Natl. Acad. Sci. U. S. A., 113, E5328, 10.1073/pnas.1611406113 Fan, 2019, Tumor energy metabolism and potential of 3-Bromopyruvate as an inhibitor of aerobic glycolysis: implications in tumor treatment, Cancers (Basel), 11, 317, 10.3390/cancers11030317 Zhang, 2018, Suppression of tumor energy supply by liposomal nanoparticle-mediated inhibition of aerobic glycolysis, ACS Appl. Mater. Interfaces, 10, 2347, 10.1021/acsami.7b16685 Lis, 2016, The HK2 dependent “Warburg effect” and mitochondrial oxidative phosphorylation in cancer: targets for effective therapy with 3-bromopyruvate, Molecules, 21, 1730, 10.3390/molecules21121730 Khatami, 2022, Glucose oxidase: applications, sources, and recombinant production, Biotechnol. Appl. Biochem., 69, 939, 10.1002/bab.2165 Zhao, 2017, Glucose oxidase-polymer Nanogels for synergistic Cancer-starving and oxidation therapy, ACS Appl. Mater. Interfaces, 9, 23528, 10.1021/acsami.7b06814 Wang, 2021, Hypoxia modulation by dual-drug nanoparticles for enhanced synergistic sonodynamic and starvation therapy, J. Nanobiotechnol., 19, 87, 10.1186/s12951-021-00837-0 Zhang, 2021, Metal-phenolic network-enabled lactic acid consumption reverses immunosuppressive tumor microenvironment for sonodynamic therapy, ACS Nano, 15, 16934, 10.1021/acsnano.1c08026 Robey, 2009, Bicarbonate increases tumor pH and inhibits spontaneous metastases, Cancer Res., 69, 2260, 10.1158/0008-5472.CAN-07-5575 Lam, 2021, Calcium carbonate nanoparticles stimulate cancer cell reprogramming to suppress tumor growth and invasion in an organ-on-a-chip system, Sci. Rep., 11, 9246, 10.1038/s41598-021-88687-6 Phan, 2017, Metabolic and epigenetic coordination of T cell and macrophage immunity, Immunity, 46, 714, 10.1016/j.immuni.2017.04.016 Nguyen, 2020, HDAC inhibitors elicit metabolic reprogramming by targeting super-enhancers in glioblastoma models, J. Clin. Invest., 130, 3699, 10.1172/JCI129049 Medon, 2017, HDAC inhibitor panobinostat engages host innate immune defenses to promote the tumoricidal effects of trastuzumab in HER2(+) tumors, Cancer Res., 77, 2594, 10.1158/0008-5472.CAN-16-2247 Oki, 2014, Immune regulatory effects of panobinostat in patients with Hodgkin lymphoma through modulation of serum cytokine levels and T-cell PD1 expression, Blood Cancer J., 4, 10.1038/bcj.2014.58 Zhu, 2016, BET Bromodomain inhibition promotes anti-tumor immunity by suppressing PD-L1 expression, Cell Rep., 16, 2829, 10.1016/j.celrep.2016.08.032 Hogg, 2017, BET-bromodomain inhibitors engage the host immune system and regulate expression of the immune checkpoint ligand PD-L1, Cell Rep., 18, 2162, 10.1016/j.celrep.2017.02.011 Fan, 2018, PES1 is transcriptionally regulated by BRD4 and promotes cell proliferation and glycolysis in hepatocellular carcinoma, Int. J. Biochem. Cell Biol., 104, 1, 10.1016/j.biocel.2018.08.014 Qiu, 2015, JQ1 suppresses tumor growth through downregulating LDHA in ovarian cancer, Oncotarget, 6, 6915, 10.18632/oncotarget.3126 He, 2022, Remodeling “cold” tumor immune microenvironment via epigenetic-based therapy using targeted liposomes with in situ formed albumin corona, Acta Pharm. Sin. B, 12, 2057, 10.1016/j.apsb.2021.09.022 Shen, 2020, M(6)A-dependent glycolysis enhances colorectal cancer progression, Mol. Cancer, 19, 72, 10.1186/s12943-020-01190-w Du, 2021, Gold Nanorods exhibit intrinsic therapeutic activity via controlling N6-Methyladenosine-based Epitranscriptomics in acute myeloid leukemia, ACS Nano, 15, 17689, 10.1021/acsnano.1c05547 Lu, 2022, G6PD functions as a metabolic checkpoint to regulate granzyme B expression in tumor-specific cytotoxic T lymphocytes, J. Immunother. Cancer, 10, 10.1136/jitc-2021-003543 Ho, 2015, Phosphoenolpyruvate is a metabolic checkpoint of anti-tumor T cell responses, Cell, 162, 1217, 10.1016/j.cell.2015.08.012 Garber, 2017, First metabolic oncology inhibitor gets FDA green light, with record price tag, Nat. Biotechnol., 35, 895, 10.1038/nbt1017-895 Mullard, 2016, Cancer metabolism pipeline breaks new ground, Nat. Rev. Drug Discov., 15, 735, 10.1038/nrd.2016.223 Hu, 2019, Nanoparticles targeting macrophages as potential clinical therapeutic agents against Cancer and inflammation, Front. Immunol., 10, 1998, 10.3389/fimmu.2019.01998 Musser, 1988, The effect of photodynamic therapy (PDT) on glucose levels within the SMT-F mouse tumor, Res. Commun. Chem. Pathol. Pharmacol., 60, 361 Zhu, 2020, A dual functional Nanoreactor for synergistic starvation and photodynamic therapy, ACS Appl. Mater. Interfaces, 12, 18309, 10.1021/acsami.0c01039 Chen, 2021, Glucose/glutathione co-triggered tumor hypoxia relief and Chemodynamic therapy to enhance Photothermal therapy in bladder Cancer, ACS Appl. Bio. Mater., 4, 7485, 10.1021/acsabm.1c00741 Guerra, 2018, Targeting tumor metabolism with plant-derived natural products: emerging trends in Cancer therapy, J. Agric. Food Chem., 66, 10663, 10.1021/acs.jafc.8b04104 Zhong, 2016, Chinese herbs interfering with Cancer reprogramming metabolism, Evid. Based Complement. Alternat. Med., 2016, 9282813, 10.1155/2016/9282813 Wang, 2020, Combination therapy based on nano codelivery for overcoming cancer drug resistance, Med. Drug Discov., 6, 10.1016/j.medidd.2020.100024