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Current Molecular Medicine

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ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

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Review Article

Ferroptosis and Cancer Immunotherapy

Author(s): Jumei Yin, Xingqi Meng, Lixuan Peng, Wei Xie, Xuan Liu, Weiguo He* and Suyun Li*

Volume 23, Issue 5, 2023

Published on: 05 August, 2022

Page: [401 - 409] Pages: 9

DOI: 10.2174/1566524022666220509124608

Price: $65

Abstract

Traditional treatment strategies for cancer are unsatisfactory. As a nonapoptotic cell death process and owning to the characteristics of iron-dependent lipid peroxide accumulation, ferroptosis has become a new target of tumor treatment. Numerous studies have proved that ferroptosis could enhance the immunogenicity of cancer and interact with immune cells. Cancer antigens, exposed to cancer cells that underwent ferroptosis, effectively improve the immunogenicity of the tumor microenvironment and promote the activation and maturation of immune cells. Meantime, immune cells release immunostimulatory cytokines including TNF-α and IFN-γ to downregulate the expression of SLC7A11 and SLC3A2, and reduce the absorption of cysteine, leading to lipid peroxidation and iron deposition in cancer cells. Consequently, induction of ferroptosis via iron deposition-based combination strategies could stimulate and activate natural and adaptive immune responses which release immune-stimulating factors to induce iron deposition in cancer cells. In this review, we provided a critical analysis of the correlation between ferroptosis and the immune responses, providing a novel way to effectively induce ferroptosis in cancer, which may be one of the focuses in future to improve the development of new therapeutic strategies of cancer.

Keywords: Ferroptosis, iron deposition, immunotherapy, immunogenicity, immune cells, cancer.

« Previous Next »
[1]
Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell 2012; 149(5): 1060-72.
[http://dx.doi.org/10.1016/j.cell.2012.03.042] [PMID: 22632970]
[2]
Gao M, Yi J, Zhu J, et al. Role of mitochondria in ferroptosis. Mol Cell 2019; 73(2): 354-363.e3.
[http://dx.doi.org/10.1016/j.molcel.2018.10.042] [PMID: 30581146]
[3]
Du J, Zhou Y, Li Y, et al. Identification of frataxin as a regulator of ferroptosis. Redox Biol 2020; 32: 101483.
[http://dx.doi.org/10.1016/j.redox.2020.101483] [PMID: 32169822]
[4]
Jelinek A, Heyder L, Daude M, et al. Mitochondrial rescue prevents glutathione peroxidase-dependent ferroptosis. Free Radic Biol Med 2018; 117: 45-57.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.01.019] [PMID: 29378335]
[5]
Neitemeier S, Jelinek A, Laino V, et al. BID links ferroptosis to mitochondrial cell death pathways. Redox Biol 2017; 12: 558-70.
[http://dx.doi.org/10.1016/j.redox.2017.03.007] [PMID: 28384611]
[6]
Riegman M, Sagie L, Galed C, et al. Ferroptosis occurs through an osmotic mechanism and propagates independently of cell rupture. Nat Cell Biol 2020; 22(9): 1042-8.
[http://dx.doi.org/10.1038/s41556-020-0565-1] [PMID: 32868903]
[7]
Agmon E, Solon J, Bassereau P, Stockwell BR. Modeling the effects of lipid peroxidation during ferroptosis on membrane properties. Sci Rep 2018; 8(1): 5155.
[http://dx.doi.org/10.1038/s41598-018-23408-0] [PMID: 29581451]
[8]
Stockwell BR, Friedmann Angeli JP, et al. Ferroptosis: A Regulated cell death nexus linking metabolism, redox biology, and Disease. Cell 2017; 171(2): 273-85.
[http://dx.doi.org/10.1016/j.cell.2017.09.021] [PMID: 28985560]
[9]
Li W, Feng G, Gauthier JM, et al. Ferroptotic cell death and TLR4/Trif signaling initiate neutrophil recruitment after heart transplantation. J Clin Invest 2019; 129(6): 2293-304.
[http://dx.doi.org/10.1172/JCI126428] [PMID: 30830879]
[10]
Wu J, Minikes AM, Gao M, et al. Intercellular interaction dictates cancer cell ferroptosis via NF2-YAP signalling. Nature 2019; 572(7769): 402-6.
[http://dx.doi.org/10.1038/s41586-019-1426-6] [PMID: 31341276]
[11]
Llabani E, Hicklin RW, Lee HY, et al. Diverse compounds from pleuromutilin lead to a thioredoxin inhibitor and inducer of ferroptosis. Nat Chem 2019; 11(6): 521-32.
[http://dx.doi.org/10.1038/s41557-019-0261-6] [PMID: 31086302]
[12]
Zhang D, Cui P, Dai Z, et al. Tumor microenvironment responsive FePt/MoS2 nanocomposites with chemotherapy and photothermal therapy for enhancing cancer immunotherapy. Nanoscale 2019; 11(42): 19912-22.
[http://dx.doi.org/10.1039/C9NR05684J] [PMID: 31599915]
[13]
Yoon HY, Selvan ST, Yang Y, et al. Engineering nanoparticle strategies for effective cancer immunotherapy. Biomaterials 2018; 178: 597-607.
[http://dx.doi.org/10.1016/j.biomaterials.2018.03.036] [PMID: 29576282]
[14]
Mohme M, Riethdorf S, Pantel K. Circulating and disseminated tumour cells - mechanisms of immune surveillance and escape. Nat Rev Clin Oncol 2017; 14(3): 155-67.
[http://dx.doi.org/10.1038/nrclinonc.2016.144] [PMID: 27644321]
[15]
Guerrouahen BS, Maccalli C, Cugno C, Rutella S, Akporiaye ET. Reverting Immune suppression to enhance cancer immunotherapy. Front Oncol 2020; 9: 1554.
[http://dx.doi.org/10.3389/fonc.2019.01554] [PMID: 32039024]
[16]
Koebel CM, Vermi W, Swann JB, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007; 450(7171): 903-7.
[http://dx.doi.org/10.1038/nature06309] [PMID: 18026089]
[17]
Papaioannou NE, Beniata OV, Vitsos P, Tsitsilonis O, Samara P. Harnessing the immune system to improve cancer therapy. Ann Transl Med 2016; 4(14): 261.
[http://dx.doi.org/10.21037/atm.2016.04.01] [PMID: 27563648]
[18]
McGranahan N, Rosenthal R, Hiley CT, et al. Allele-specific HLA loss and immune escape in lung cancer evolution. Cell 2017; 171(6): 1259-1271.e11.
[http://dx.doi.org/10.1016/j.cell.2017.10.001] [PMID: 29107330]
[19]
Naing A, Infante JR, Papadopoulos KP, et al. PEGylated IL-10 (Pegilodecakin) induces systemic immune activation, CD8+ T cell invigoration and polyclonal T cell expansion in cancer patients. Cancer Cell 2018; 34(5): 775-791.e3.
[http://dx.doi.org/10.1016/j.ccell.2018.10.007] [PMID: 30423297]
[20]
Vanpouille-Box C, Alard A, Aryankalayil MJ, et al. DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity. Nat Commun 2017; 8(1): 15618.
[http://dx.doi.org/10.1038/ncomms15618] [PMID: 28598415]
[21]
Xu T, Ding W, Ji X, et al. Molecular mechanisms of ferroptosis and its role in cancer therapy. J Cell Mol Med 2019; 23(8): 4900-12.
[http://dx.doi.org/10.1111/jcmm.14511] [PMID: 31232522]
[22]
Blankenstein T, Coulie PG, Gilboa E, Jaffee EM. The determinants of tumour immunogenicity. Nat Rev Cancer 2012; 12(4): 307-13.
[http://dx.doi.org/10.1038/nrc3246] [PMID: 22378190]
[23]
Wang W, Green M, Choi JE, et al. CD8+ T cells regulate tumour ferroptosis during cancer immunotherapy. Nature 2019; 569(7755): 270-4.
[http://dx.doi.org/10.1038/s41586-019-1170-y] [PMID: 31043744]
[24]
Berglund A, Mills M, Putney RM, Hamaidi I, Mulé J, Kim S. Methylation of immune synapse genes modulates tumor immunogenicity. J Clin Invest 2020; 130(2): 974-80.
[http://dx.doi.org/10.1172/JCI131234] [PMID: 31714899]
[25]
Wang Z, Chen J, Hu J, et al. cGAS/STING axis mediates a topoisomerase II inhibitor-induced tumor immunogenicity. J Clin Invest 2019; 129(11): 4850-62.
[http://dx.doi.org/10.1172/JCI127471] [PMID: 31408442]
[26]
Garrido G, Schrand B, Rabasa A, et al. Tumor-targeted silencing of the peptide transporter TAP induces potent antitumor immunity. Nat Commun 2019; 10(1): 3773.
[http://dx.doi.org/10.1038/s41467-019-11728-2] [PMID: 31434881]
[27]
Zhang F, Li F, Lu GH, et al. Engineering magnetosomes for ferroptosis/immunomodulation synergism in cancer. ACS Nano 2019; 13(5): 5662-73.
[http://dx.doi.org/10.1021/acsnano.9b00892] [PMID: 31046234]
[28]
Jiang Q, Wang K, Zhang X, et al. Platelet membrane-camouflaged magnetic nanoparticles for ferroptosis-enhanced cancer immunotherapy. Small 2020; 16(22): e2001704.
[http://dx.doi.org/10.1002/smll.202001704] [PMID: 32338436]
[29]
Gordon SR, Maute RL, Dulken BW, et al. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature 2017; 545(7655): 495-9.
[http://dx.doi.org/10.1038/nature22396] [PMID: 28514441]
[30]
Pozzi C, Cuomo A, Spadoni I, et al. The EGFR-specific antibody cetuximab combined with chemotherapy triggers immunogenic cell death. Nat Med 2016; 22(6): 624-31.
[http://dx.doi.org/10.1038/nm.4078] [PMID: 27135741]
[31]
Galluzzi L, Buqué A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol 2017; 17(2): 97-111.
[http://dx.doi.org/10.1038/nri.2016.107] [PMID: 27748397]
[32]
Wen X, Li Y, Hamblin MR. Photodynamic therapy in dermatology beyond non-melanoma cancer: An update. Photodiagn Photodyn Ther 2017; 19: 140-52.
[http://dx.doi.org/10.1016/j.pdpdt.2017.06.010] [PMID: 28647616]
[33]
Turan IS, Yildiz D, Turksoy A, Gunaydin G, Akkaya EU. A bifunctional photosensitizer for enhanced fractional photodynamic therapy: Singlet oxygen generation in the presence and absence of light. Angew Chem Int Ed Engl 2016; 55(8): 2875-8.
[http://dx.doi.org/10.1002/anie.201511345] [PMID: 26799149]
[34]
Yu B, Choi B, Li W, Kim DH. Magnetic field boosted ferroptosis-like cell death and responsive MRI using hybrid vesicles for cancer immunotherapy. Nat Commun 2020; 11(1): 3637.
[http://dx.doi.org/10.1038/s41467-020-17380-5] [PMID: 32686685]
[35]
Turubanova VD, Balalaeva IV, Mishchenko TA, et al. Immunogenic cell death induced by a new photodynamic therapy based on photosens and photodithazine. J Immunother Cancer 2019; 7(1): 350.
[http://dx.doi.org/10.1186/s40425-019-0826-3] [PMID: 31842994]
[36]
Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418(6894): 191-5.
[http://dx.doi.org/10.1038/nature00858] [PMID: 12110890]
[37]
Bustin M. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol 1999; 19(8): 5237-46.
[http://dx.doi.org/10.1128/MCB.19.8.5237] [PMID: 10409715]
[38]
Wang H, Bloom O, Zhang M, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999; 285(5425): 248-51.
[http://dx.doi.org/10.1126/science.285.5425.248] [PMID: 10398600]
[39]
Degryse B, Bonaldi T, Scaffidi P, et al. The high Mobility Group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J Cell Biol 2001; 152(6): 1197-206.
[http://dx.doi.org/10.1083/jcb.152.6.1197] [PMID: 11257120]
[40]
Xu D, Young J, Song D, Esko JD. Heparan sulfate is essential for High Mobility Group protein 1 (HMGB1) signaling by the receptor for advanced glycation end products (RAGE). J Biol Chem 2011; 286(48): 41736-44.
[http://dx.doi.org/10.1074/jbc.M111.299685] [PMID: 21990362]
[41]
Wen Q, Liu J, Kang R, Zhou B, Tang D. The release and activity of HMGB1 in ferroptosis. Biochem Biophys Res Commun 2019; 510(2): 278-83.
[http://dx.doi.org/10.1016/j.bbrc.2019.01.090] [PMID: 30686534]
[42]
Gao Q, Wang S, Chen X, et al. Cancer-cell-secreted CXCL11 promoted CD8+ T cells infiltration through docetaxel-induced-release of HMGB1 in NSCLC. J Immunother Cancer 2019; 7(1): 42.
[http://dx.doi.org/10.1186/s40425-019-0511-6] [PMID: 30744691]
[43]
Li X, Liu Z, Zhang A, et al. NQO1 targeting prodrug triggers innate sensing to overcome checkpoint blockade resistance. Nat Commun 2019; 10(1): 3251.
[http://dx.doi.org/10.1038/s41467-019-11238-1] [PMID: 31324798]
[44]
Mascaux C, Angelova M, Vasaturo A, et al. Immune evasion before tumour invasion in early lung squamous carcinogenesis. Nature 2019; 571(7766): 570-5.
[http://dx.doi.org/10.1038/s41586-019-1330-0] [PMID: 31243362]
[45]
Miao Y, Yang H, Levorse J, et al. Adaptive immune resistance emerges from tumor-initiating stem cells. Cell 2019; 177(5): 1172-1186.e14.
[http://dx.doi.org/10.1016/j.cell.2019.03.025] [PMID: 31031009]
[46]
Böttcher JP, Bonavita E, Chakravarty P, et al. NK Cells Stimulate Recruitment of cDC1 into the tumor microenvironment promoting cancer immune control. Cell 2018; 172(5): 1022-1037.e14.
[http://dx.doi.org/10.1016/j.cell.2018.01.004] [PMID: 29429633]
[47]
Di Pilato M, Kim EY, Cadilha BL, et al. Targeting the CBM complex causes Treg cells to prime tumours for immune checkpoint therapy. Nature 2019; 570(7759): 112-6.
[http://dx.doi.org/10.1038/s41586-019-1215-2] [PMID: 31092922]
[48]
Petrausch U, Poehlein CH, Jensen SM, et al. Cancer immunotherapy: The role regulatory T cells play and what can be done to overcome their inhibitory effects. Curr Mol Med 2009; 9(6): 673-82.
[http://dx.doi.org/10.2174/156652409788970670] [PMID: 19689294]
[49]
Rodell CB, Arlauckas SP, Cuccarese MF, et al. TLR7/8-agonist-loaded nanoparticles promote the polarization of tumour-associated macrophages to enhance cancer immunotherapy. Nat Biomed Eng 2018; 2(8): 578-88.
[http://dx.doi.org/10.1038/s41551-018-0236-8] [PMID: 31015631]
[50]
Walsh SR, Simovic B, Chen L, et al. Endogenous T cells prevent tumor immune escape following adoptive T cell therapy. J Clin Invest 2019; 129(12): 5400-10.
[http://dx.doi.org/10.1172/JCI126199] [PMID: 31682239]
[51]
Muri J, Thut H, Bornkamm GW, Kopf M. B1 and marginal zone B cells but not follicular B2 cells require Gpx4 to prevent lipid peroxidation and ferroptosis. Cell Rep 2019; 29(9): 2731-2744.e4.
[http://dx.doi.org/10.1016/j.celrep.2019.10.070] [PMID: 31775041]
[52]
Matsushita M, Freigang S, Schneider C, Conrad M, Bornkamm GW, Kopf M. T cell lipid peroxidation induces ferroptosis and prevents immunity to infection. J Exp Med 2015; 212(4): 555-68.
[http://dx.doi.org/10.1084/jem.20140857] [PMID: 25824823]
[53]
Kinowaki Y, Kurata M, Ishibashi S, et al. Glutathione peroxidase 4 overexpression inhibits ROS-induced cell death in diffuse large B-cell lymphoma. Lab Invest 2018; 98(5): 609-19.
[http://dx.doi.org/10.1038/s41374-017-0008-1] [PMID: 29463878]
[54]
Simanshu DK, Nissley DV, McCormick F. RAS Proteins and Their regulators in human disease. Cell 2017; 170(1): 17-33.
[http://dx.doi.org/10.1016/j.cell.2017.06.009] [PMID: 28666118]
[55]
Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: Weaving a tumorigenic web. Nat Rev Cancer 2011; 11(11): 761-74.
[http://dx.doi.org/10.1038/nrc3106] [PMID: 21993244]
[56]
Waters AM, Der CJ. KRAS: The critical driver and therapeutic target for pancreatic cancer. Cold Spring Harb Perspect Med 2018; 8(9): a031435.
[http://dx.doi.org/10.1101/cshperspect.a031435] [PMID: 29229669]
[57]
Dai E, Han L, Liu J, et al. Autophagy-dependent ferroptosis drives tumor-associated macrophage polarization via release and uptake of oncogenic KRAS protein. Autophagy 2020; 16(11): 2069-83.
[http://dx.doi.org/10.1080/15548627.2020.1714209] [PMID: 31920150]
[58]
Wei G, Sun J, Luan W, et al. Natural product albiziabioside a conjugated with pyruvate dehydrogenase kinase inhibitor dichloroacetate to induce apoptosis-ferroptosis-m2-tams polarization for combined cancer therapy. J Med Chem 2019; 62(19): 8760-72.
[http://dx.doi.org/10.1021/acs.jmedchem.9b00644] [PMID: 31509699]
[59]
Wan C, Sun Y, Tian Y, et al. Irradiated tumor cell-derived microparticles mediate tumor eradication via cell killing and immune reprogramming. Sci Adv 2020; 6(13): eaay9789.
[http://dx.doi.org/10.1126/sciadv.aay9789] [PMID: 32232155]
[60]
Xu T, Ma Y, Yuan Q, et al. Enhanced ferroptosis by oxygen-boosted phototherapy based on a 2-in-1 nanoplatform of ferrous hemoglobin for tumor synergistic therapy. ACS Nano 2020; 14(3): 3414-25.
[http://dx.doi.org/10.1021/acsnano.9b09426] [PMID: 32155051]
[61]
Ingold I, Berndt C, Schmitt S, et al. Selenium utilization by gpx4 is required to prevent hydroperoxide-induced ferroptosis. Cell 2018; 172(3): 409-22.
[http://dx.doi.org/10.1016/j.cell.2017.11.048] [PMID: 29290465]
[62]
Shen Z, Liu T, Li Y, et al. Fenton-Reaction-acceleratable magnetic nanoparticles for ferroptosis therapy of orthotopic brain tumors. ACS Nano 2018; 12(11): 11355-65.
[http://dx.doi.org/10.1021/acsnano.8b06201] [PMID: 30375848]
[63]
Wan X, Song L, Pan W, Zhong H, Li N, Tang B. Tumor-Targeted cascade nanoreactor based on metal-organic frameworks for synergistic ferroptosis-starvation anticancer therapy. ACS Nano 2020; 14(9): 11017-28.
[http://dx.doi.org/10.1021/acsnano.9b07789] [PMID: 32786253]
[64]
He H, Du L, Guo H, et al. Redox responsive metal organic framework nanoparticles induces ferroptosis for cancer therapy. Small 2020; 16(33): e2001251.
[http://dx.doi.org/10.1002/smll.202001251] [PMID: 32677157]
[65]
Yu M, Gai C, Li Z, et al. Targeted exosome-encapsulated erastin induced ferroptosis in triple negative breast cancer cells. Cancer Sci 2019; 110(10): 3173-82.
[http://dx.doi.org/10.1111/cas.14181] [PMID: 31464035]
[66]
Xue CC, Li MH, Zhao Y, et al. Tumor microenvironment-activatable Fe-doxorubicin preloaded amorphous CaCO3 nanoformulation triggers ferroptosis in target tumor cells. Sci Adv 2020; 6(18): eaax1346.
[http://dx.doi.org/10.1126/sciadv.aax1346] [PMID: 32494659]
[67]
Wang S, Li F, Qiao R, et al. Arginine-Rich manganese silicate nanobubbles as a ferroptosis-inducing agent for tumor-targeted theranostics. ACS Nano 2018; 12(12): 12380-92.
[http://dx.doi.org/10.1021/acsnano.8b06399] [PMID: 30495919]
[68]
Tang H, Chen D, Li C, et al. Dual GSH-exhausting sorafenib loaded manganese-silica nanodrugs for inducing the ferroptosis of hepatocellular carcinoma cells. Int J Pharm 2019; 572: 118782.
[http://dx.doi.org/10.1016/j.ijpharm.2019.118782] [PMID: 31678528]
[69]
Hu Z, Wang S, Dai Z, Zhang H, Zheng X. A novel theranostic nano-platform (PB@FePt-HA-g-PEG) for tumor chemodynamic-photothermal co-therapy and triple-modal imaging (MR/CT/PI) diagnosis. J Mater Chem B Mater Biol Med 2020; 8(24): 5351-60.
[http://dx.doi.org/10.1039/D0TB00708K] [PMID: 32458958]
[70]
He S, Jiang Y, Li J, Pu K. Semiconducting polycomplex nanoparticles for photothermal ferrotherapy of cancer. Angew Chem Int Ed Engl 2020; 59(26): 10633-8.
[http://dx.doi.org/10.1002/anie.202003004] [PMID: 32207214]
[71]
Jiang Y, Zhao X, Huang J, et al. Transformable hybrid semiconducting polymer nanozyme for second near-infrared photothermal ferrotherapy. Nat Commun 2020; 11(1): 1857.
[http://dx.doi.org/10.1038/s41467-020-15730-x] [PMID: 32312987]
[72]
Ye LF, Chaudhary KR, Zandkarimi F, et al. Radiation-induced lipid peroxidation triggers ferroptosis and synergizes with ferroptosis inducers. ACS Chem Biol 2020; 15(2): 469-84.
[http://dx.doi.org/10.1021/acschembio.9b00939] [PMID: 31899616]
[73]
Shibata Y, Yasui H, Higashikawa K, Miyamoto N, Kuge Y. Erastin, a ferroptosis-inducing agent, sensitized cancer cells to X-ray irradiation via glutathione starvation in vitro and in vivo. PLoS One 2019; 14(12): e0225931.
[http://dx.doi.org/10.1371/journal.pone.0225931] [PMID: 31800616]
[74]
Gao Z, He T, Zhang P, et al. Polypeptide-based theranostics with tumor-microenvironment-activatable cascade reaction for chemo-ferroptosis combination therapy. ACS Appl Mater Interfaces 2020; 12(18): 20271-80.
[http://dx.doi.org/10.1021/acsami.0c03748] [PMID: 32283924]
[75]
Zhu T, Shi L, Yu C, et al. Ferroptosis promotes photodynamic therapy: Supramolecular photosensitizer-Inducer nanodrug for enhanced cancer treatment. Theranostics 2019; 9(11): 3293-307.
[http://dx.doi.org/10.7150/thno.32867] [PMID: 31244955]
[76]
Zhang P, Hou Y, Zeng J, et al. Coordinatively Unsaturated Fe3+ Based activatable probes for enhanced MRI and therapy of tumors. Angew Chem Int Ed Engl 2019; 58(32): 11088-96.
[http://dx.doi.org/10.1002/anie.201904880] [PMID: 31131511]
[77]
Luo X, Gong X, Su L, et al. Activatable mitochondria-targeting organoarsenic prodrugs for bioenergetic cancer therapy. Angew Chem Int Ed Engl 2021; 60(3): 1403-10.
[http://dx.doi.org/10.1002/anie.202012237] [PMID: 33029903]
[78]
Jia X, Zhang Y, Zou Y, et al. Dual intratumoral redox/enzyme-responsive no-releasing nanomedicine for the specific, high-efficacy, and low-toxic cancer therapy. Adv Mater 2018; 30(30): e1704490.
[http://dx.doi.org/10.1002/adma.201704490] [PMID: 29889325]

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