Emerging Therapeutic Approaches Targeting Ferroptosis in Cancer: Focus on Immunotherapy and Nanotechnology


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Abstract

:Ferroptosis is a newly discovered form of programmed cell death characterized by iron overload, ROS accumulation, and lipid peroxidation. It is distinguished by unique morphological, biochemical, and genetic features and stands apart from other known regulated cell death mechanisms. Studies have demonstrated a close association between ferroptosis and various cancers, including liver cancer, lung cancer, renal cell carcinoma, colorectal cancer, pancreatic cancer, and ovarian cancer. Inducing ferroptosis has shown promising results in inhibiting tumor growth and reversing tumor progression. However, the challenge lies in regulating ferroptosis in vivo due to the scarcity of potent compounds that can activate it. Integrating emerging biomedical discoveries and technological innovations with conventional therapies is imperative. Notably, considerable progress has been made in cancer treatment by leveraging immunotherapy and nanotechnology to trigger ferroptosis. This review explores the relationship between ferroptosis and emerging immunotherapies and nanotechnologies, along with their potential underlying mechanisms, offering valuable insights for developing novel cancer treatment strategies.

About the authors

Zongchao Yu

Department of General Surgery, he Affiliated Nanhua Hospital, Hengyang Medical School, University of South China

Email: info@benthamscience.net

Zhongcheng Mo

Department of Histology and Embryology, Guangxi Key Laboratory of Diabetic Systems Medicine, Guilin Medical University

Email: info@benthamscience.net

Yuan Qiu

Department of General Surgery, he Affiliated Nanhua Hospital, Hengyang Medical School, University of South China

Email: info@benthamscience.net

Hengzhe Lu

Department of General Surgery, he Affiliated Nanhua Hospital, Hengyang Medical School, University of South China

Email: info@benthamscience.net

Biao Zheng

Department of Histology and Embryology, Guangxi Key Laboratory of Diabetic Systems Medicine, Guilin Medical University

Email: info@benthamscience.net

Longfei Liu

Department of General Surgery, he Affiliated Nanhua Hospital, Hengyang Medical School, University of South China

Author for correspondence.
Email: info@benthamscience.net

References

  1. Vinay, D.S.; Ryan, E.P.; Pawelec, G.; Talib, W.H.; Stagg, J.; Elkord, E.; Lichtor, T.; Decker, W.K.; Whelan, R.L.; Kumara, H. Immune evasion in cancer: Mechanistic basis and therapeutic strategies. Semin. Cancer Biol., 2015, 35, S185-S198.
  2. Wellenstein, M.D.; de Visser, K.E. Cancer-cell-intrinsic mechanisms shaping the tumor immune landscape. Immunity, 2018, 48(3), 399-416. doi: 10.1016/j.immuni.2018.03.004 PMID: 29562192
  3. Okusaka, T.; Furuse, J. Recent advances in chemotherapy for pancreatic cancer: evidence from Japan and recommendations in guidelines. J. Gastroenterol., 2020, 55(4), 369-382. doi: 10.1007/s00535-020-01666-y PMID: 31997007
  4. Pugh, T.J.; Nguyen, B.N.; Kanke, J.E.; Johnson, J.L.; Hoffman, K.E. Radiation therapy modalities in prostate cancer. J. Natl. Compr. Canc. Netw., 2013, 11(4), 414-421. doi: 10.6004/jnccn.2013.0056 PMID: 23584344
  5. Wang, L.; Qin, W.; Huo, Y.J.; Li, X.; Shi, Q.; Rasko, J.E.J.; Janin, A.; Zhao, W.L. Advances in targeted therapy for malignant lymphoma. Signal Transduct. Target. Ther., 2020, 5(1), 15. doi: 10.1038/s41392-020-0113-2 PMID: 32296035
  6. Tang, Z.; Zeng, Q.; Li, Y.; Zhang, X.; Ma, J.; Suto, M.J.; Xu, B.; Yi, N. Development of a radiosensitivity gene signature for patients with soft tissue sarcoma. Oncotarget, 2017, 8(16), 27428-27439. doi: 10.18632/oncotarget.16194 PMID: 28404969
  7. Zraik, I.M.; Heß-Busch, Y. Management of chemotherapy side effects and their long-term sequelae. Urologe A, 2021, 60(7), 862-871. doi: 10.1007/s00120-021-01569-7 PMID: 34185118
  8. Lev, S. Targeted therapy and drug resistance in triple-negative breast cancer: the EGFR axis. Biochem. Soc. Trans., 2020, 48(2), 657-665. doi: 10.1042/BST20191055 PMID: 32311020
  9. Dixon, S.J.; Lemberg, K.M.; Lamprecht, M.R.; Skouta, R.; Zaitsev, E.M.; Gleason, C.E.; Patel, D.N.; Bauer, A.J.; Cantley, A.M.; Yang, W.S.; Morrison, B., III; Stockwell, B.R. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell, 2012, 149(5), 1060-1072. doi: 10.1016/j.cell.2012.03.042 PMID: 22632970
  10. Dolma, S.; Lessnick, S.L.; Hahn, W.C.; Stockwell, B.R. Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell, 2003, 3(3), 285-296. doi: 10.1016/S1535-6108(03)00050-3 PMID: 12676586
  11. Yang, W.S.; Stockwell, B.R. Synthetic lethal screening identifies compounds activating iron-dependent, nonapoptotic cell death in oncogenic-RAS-harboring cancer cells. Chem. Biol., 2008, 15(3), 234-245. doi: 10.1016/j.chembiol.2008.02.010 PMID: 18355723
  12. Yu, H.; Guo, P.; Xie, X.; Wang, Y.; Chen, G. Ferroptosis, a new form of cell death, and its relationships with tumourous diseases. J. Cell. Mol. Med., 2017, 21(4), 648-657. doi: 10.1111/jcmm.13008 PMID: 27860262
  13. Djulbegovic, M.B.; Uversky, V.N. Ferroptosis – An iron- and disorder-dependent programmed cell death. Int. J. Biol. Macromol., 2019, 135, 1052-1069. doi: 10.1016/j.ijbiomac.2019.05.221 PMID: 31175900
  14. Cotter, T.G. Apoptosis and cancer: The genesis of a research field. Nat. Rev. Cancer, 2009, 9(7), 501-507. doi: 10.1038/nrc2663 PMID: 19550425
  15. Czabotar, P.E.; Lessene, G.; Strasser, A.; Adams, J.M. Control of apoptosis by the BCL-2 protein family: Implications for physiology and therapy. Nat. Rev. Mol. Cell Biol., 2014, 15(1), 49-63. doi: 10.1038/nrm3722 PMID: 24355989
  16. Luna-Vargas, M.P.A.; Chipuk, J.E. Physiological and pharmacological control of BAK, BAX, and beyond. Trends Cell Biol., 2016, 26(12), 906-917. doi: 10.1016/j.tcb.2016.07.002 PMID: 27498846
  17. Murphy, J.M.; Czabotar, P.E.; Hildebrand, J.M.; Lucet, I.S.; Zhang, J.G.; Alvarez-Diaz, S.; Lewis, R.; Lalaoui, N.; Metcalf, D.; Webb, A.I.; Young, S.N.; Varghese, L.N.; Tannahill, G.M.; Hatchell, E.C.; Majewski, I.J.; Okamoto, T.; Dobson, R.C.J.; Hilton, D.J.; Babon, J.J.; Nicola, N.A.; Strasser, A.; Silke, J.; Alexander, W.S. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity, 2013, 39(3), 443-453. doi: 10.1016/j.immuni.2013.06.018 PMID: 24012422
  18. Xu, D.; Zou, C.; Yuan, J. Genetic regulation of RIPK1 and necroptosis. Annu. Rev. Genet., 2021, 55(1), 235-263. doi: 10.1146/annurev-genet-071719-022748 PMID: 34813352
  19. Zhang, T.; Wang, Y.; Inuzuka, H.; Wei, W. Necroptosis pathways in tumorigenesis. Semin. Cancer Biol., 2022, 86(Pt 3), 32-40. doi: 10.1016/j.semcancer.2022.07.007 PMID: 35908574
  20. Jorgensen, I.; Miao, E.A. Pyroptotic cell death defends against intracellular pathogens. Immunol. Rev., 2015, 265(1), 130-142. doi: 10.1111/imr.12287 PMID: 25879289
  21. Miao, E.A.; Leaf, I.A.; Treuting, P.M.; Mao, D.P.; Dors, M.; Sarkar, A.; Warren, S.E.; Wewers, M.D.; Aderem, A. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol., 2010, 11(12), 1136-1142. doi: 10.1038/ni.1960 PMID: 21057511
  22. Galluzzi, L.; Baehrecke, E.H.; Ballabio, A.; Boya, P.; Bravo-San Pedro, J.M.; Cecconi, F.; Choi, A.M.; Chu, C.T.; Codogno, P.; Colombo, M.I.; Cuervo, A.M.; Debnath, J.; Deretic, V.; Dikic, I.; Eskelinen, E.L.; Fimia, G.M.; Fulda, S.; Gewirtz, D.A.; Green, D.R.; Hansen, M.; Harper, J.W.; Jäättelä, M.; Johansen, T.; Juhasz, G.; Kimmelman, A.C.; Kraft, C.; Ktistakis, N.T.; Kumar, S.; Levine, B.; Lopez-Otin, C.; Madeo, F.; Martens, S.; Martinez, J.; Melendez, A.; Mizushima, N.; Münz, C.; Murphy, L.O.; Penninger, J.M.; Piacentini, M.; Reggiori, F.; Rubinsztein, D.C.; Ryan, K.M.; Santambrogio, L.; Scorrano, L.; Simon, A.K.; Simon, H.U.; Simonsen, A.; Tavernarakis, N.; Tooze, S.A.; Yoshimori, T.; Yuan, J.; Yue, Z.; Zhong, Q.; Kroemer, G. Molecular definitions of autophagy and related processes. EMBO J., 2017, 36(13), 1811-1836. doi: 10.15252/embj.201796697 PMID: 28596378
  23. Pietrocola, F.; Izzo, V.; Niso-Santano, M.; Vacchelli, E.; Galluzzi, L.; Maiuri, M.C.; Kroemer, G. Regulation of autophagy by stress-responsive transcription factors. Semin. Cancer Biol., 2013, 23(5), 310-322. doi: 10.1016/j.semcancer.2013.05.008 PMID: 23726895
  24. Wang, H.; Liu, C.; Zhao, Y.; Gao, G. Mitochondria regulation in ferroptosis. Eur. J. Cell Biol., 2020, 99(1), 151058. doi: 10.1016/j.ejcb.2019.151058 PMID: 31810634
  25. Li, Y.; Zeng, X.; Lu, D.; Yin, M.; Shan, M.; Gao, Y. Erastin induces ferroptosis via ferroportin-mediated iron accumulation in endometriosis. Hum. Reprod., 2021, 36(4), 951-964. doi: 10.1093/humrep/deaa363 PMID: 33378529
  26. Haschka, D.; Hoffmann, A.; Weiss, G. Iron in immune cell function and host defense. Semin. Cell Dev. Biol., 2021, 115, 27-36. doi: 10.1016/j.semcdb.2020.12.005 PMID: 33386235
  27. Zhu, J.; Xiong, Y.; Zhang, Y.; Wen, J.; Cai, N.; Cheng, K.; Liang, H.; Zhang, W. The molecular mechanisms of regulating oxidative stress-induced ferroptosis and therapeutic strategy in tumors. Oxid. Med. Cell. Longev., 2020, 2020, 1-14. doi: 10.1155/2020/8810785 PMID: 33425217
  28. Xie, Y.; Hou, W.; Song, X.; Yu, Y.; Huang, J.; Sun, X.; Kang, R.; Tang, D. Ferroptosis: Process and function. Cell Death Differ., 2016, 23(3), 369-379. doi: 10.1038/cdd.2015.158 PMID: 26794443
  29. Dixon, S.J.; Pratt, D.A. Ferroptosis: A flexible constellation of related biochemical mechanisms. Mol. Cell, 2023, 83(7), 1030-1042. doi: 10.1016/j.molcel.2023.03.005 PMID: 36977413
  30. Koppula, P.; Zhuang, L.; Gan, B. Cystine transporter SLC7A11/xCT in cancer: Ferroptosis, nutrient dependency, and cancer therapy. Protein Cell, 2021, 12(8), 599-620. doi: 10.1007/s13238-020-00789-5 PMID: 33000412
  31. Dixon, S.J.; Winter, G.E.; Musavi, L.S.; Lee, E.D.; Snijder, B.; Rebsamen, M.; Superti-Furga, G.; Stockwell, B.R. Human haploid cell genetics reveals roles for lipid metabolism genes in nonapoptotic cell death. ACS Chem. Biol., 2015, 10(7), 1604-1609. doi: 10.1021/acschembio.5b00245 PMID: 25965523
  32. Friedmann Angeli, J.P.; Schneider, M.; Proneth, B.; Tyurina, Y.Y.; Tyurin, V.A.; Hammond, V.J.; Herbach, N.; Aichler, M.; Walch, A.; Eggenhofer, E.; Basavarajappa, D.; Rådmark, O.; Kobayashi, S.; Seibt, T.; Beck, H.; Neff, F.; Esposito, I.; Wanke, R.; Förster, H.; Yefremova, O.; Heinrichmeyer, M.; Bornkamm, G.W.; Geissler, E.K.; Thomas, S.B.; Stockwell, B.R.; O’Donnell, V.B.; Kagan, V.E.; Schick, J.A.; Conrad, M. Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat. Cell Biol., 2014, 16(12), 1180-1191. doi: 10.1038/ncb3064 PMID: 25402683
  33. Li, Y.; Feng, D.; Wang, Z.; Zhao, Y.; Sun, R.; Tian, D.; Liu, D.; Zhang, F.; Ning, S.; Yao, J.; Tian, X. Ischemia-induced ACSL4 activation contributes to ferroptosis-mediated tissue injury in intestinal ischemia/reperfusion. Cell Death Differ., 2019, 26(11), 2284-2299. doi: 10.1038/s41418-019-0299-4 PMID: 30737476
  34. Liu, W.; Östberg, N.; Yalcinkaya, M.; Dou, H.; Endo-Umeda, K.; Tang, Y.; Hou, X.; Xiao, T.; Fidler, T.P.; Abramowicz, S.; Yang, Y.G.; Soehnlein, O.; Tall, A.R.; Wang, N. Erythroid lineage Jak2V617F expression promotes atherosclerosis through erythrophagocytosis and macrophage ferroptosis. J. Clin. Invest., 2022, 132(13), e155724. doi: 10.1172/JCI155724 PMID: 35587375
  35. Derry, P.J.; Hegde, M.L.; Jackson, G.R.; Kayed, R.; Tour, J.M.; Tsai, A.L.; Kent, T.A. Revisiting the intersection of amyloid, pathologically modified tau and iron in Alzheimer’s disease from a ferroptosis perspective. Prog. Neurobiol., 2020, 184, 101716. doi: 10.1016/j.pneurobio.2019.101716 PMID: 31604111
  36. Jiang, X.; Stockwell, B.R.; Conrad, M. Ferroptosis: Mechanisms, biology and role in disease. Nat. Rev. Mol. Cell Biol., 2021, 22(4), 266-282. doi: 10.1038/s41580-020-00324-8 PMID: 33495651
  37. Stockwell, B.R.; Jiang, X.; Gu, W. Emerging mechanisms and disease relevance of ferroptosis. Trends Cell Biol., 2020, 30(6), 478-490.
  38. Yang, W.S. SriRamaratnam, R.; Welsch, M.E.; Shimada, K.; Skouta, R.; Viswanathan, V.S.; Cheah, J.H.; Clemons, P.A.; Shamji, A.F.; Clish, C.B.; Brown, L.M.; Girotti, A.W.; Cornish, V.W.; Schreiber, S.L.; Stockwell, B.R. Regulation of ferroptotic cancer cell death by GPX4. Cell, 2014, 156(1-2), 317-331. doi: 10.1016/j.cell.2013.12.010 PMID: 24439385
  39. Dixon, S.J.; Patel, D.N.; Welsch, M.; Skouta, R.; Lee, E.D.; Hayano, M.; Thomas, A.G.; Gleason, C.E.; Tatonetti, N.P.; Slusher, B.S.; Stockwell, B.R. Pharmacological inhibition of cystine–glutamate exchange induces endoplasmic reticulum stress and ferroptosis. eLife, 2014, 3, e02523. doi: 10.7554/eLife.02523 PMID: 24844246
  40. Toyokuni, S.; Ito, F.; Yamashita, K.; Okazaki, Y.; Akatsuka, S. Iron and thiol redox signaling in cancer: An exquisite balance to escape ferroptosis. Free Radic. Biol. Med., 2017, 108, 610-626. doi: 10.1016/j.freeradbiomed.2017.04.024 PMID: 28433662
  41. Lin, R.; Zhang, Z.; Chen, L.; Zhou, Y.; Zou, P.; Feng, C.; Wang, L.; Liang, G. Dihydroartemisinin (DHA) induces ferroptosis and causes cell cycle arrest in head and neck carcinoma cells. Cancer Lett., 2016, 381(1), 165-175. doi: 10.1016/j.canlet.2016.07.033 PMID: 27477901
  42. Devisscher, L.; Van Coillie, S.; Hofmans, S.; Van Rompaey, D.; Goossens, K.; Meul, E.; Maes, L.; De Winter, H.; Van Der Veken, P.; Vandenabeele, P.; Berghe, T.V.; Augustyns, K. Discovery of novel, drug-like ferroptosis inhibitors with in vivo efficacy. J. Med. Chem., 2018, 61(22), 10126-10140. doi: 10.1021/acs.jmedchem.8b01299 PMID: 30354101
  43. Niki, E. Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence. Free Radic. Biol. Med., 2014, 66, 3-12. doi: 10.1016/j.freeradbiomed.2013.03.022 PMID: 23557727
  44. Doll, S.; Proneth, B.; Tyurina, Y.Y.; Panzilius, E.; Kobayashi, S.; Ingold, I.; Irmler, M.; Beckers, J.; Aichler, M.; Walch, A.; Prokisch, H.; Trümbach, D.; Mao, G.; Qu, F.; Bayir, H.; Füllekrug, J.; Scheel, C.H.; Wurst, W.; Schick, J.A.; Kagan, V.E.; Angeli, J.P.F.; Conrad, M. ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat. Chem. Biol., 2017, 13(1), 91-98. doi: 10.1038/nchembio.2239 PMID: 27842070
  45. Louandre, C.; Ezzoukhry, Z.; Godin, C.; Barbare, J.C.; Mazière, J.C.; Chauffert, B.; Galmiche, A. Iron‐dependent cell death of hepatocellular carcinoma cells exposed to sorafenib. Int. J. Cancer, 2013, 133(7), 1732-1742. doi: 10.1002/ijc.28159 PMID: 23505071
  46. Ye, L.F.; Chaudhary, K.R.; Zandkarimi, F.; Harken, A.D.; Kinslow, C.J.; Upadhyayula, P.S.; Dovas, A.; Higgins, D.M.; Tan, H.; Zhang, Y.; Buonanno, M.; Wang, T.J.C.; Hei, T.K.; Bruce, J.N.; Canoll, P.D.; Cheng, S.K.; Stockwell, B.R. Radiation-induced lipid peroxidation triggers ferroptosis and synergizes with ferroptosis inducers. ACS Chem. Biol., 2020, 15(2), 469-484. doi: 10.1021/acschembio.9b00939 PMID: 31899616
  47. Li, Y.; Wei, X.; Tao, F.; Deng, C.; Lv, C.; Chen, C.; Cheng, Y. The potential application of nanomaterials for ferroptosis-based cancer therapy. Biomed. Mater., 2021, 16(4), 042013. doi: 10.1088/1748-605X/ac058a PMID: 34038885
  48. Lang, X.; Green, M.D.; Wang, W.; Yu, J.; Choi, J.E.; Jiang, L.; Liao, P.; Zhou, J.; Zhang, Q.; Dow, A.; Saripalli, A.L.; Kryczek, I.; Wei, S.; Szeliga, W.; Vatan, L.; Stone, E.M.; Georgiou, G.; Cieslik, M.; Wahl, D.R.; Morgan, M.A.; Chinnaiyan, A.M.; Lawrence, T.S.; Zou, W. Radiotherapy and immunotherapy promote tumoral lipid oxidation and ferroptosis via synergistic repression of SLC7A11. Cancer Discov., 2019, 9(12), 1673-1685. doi: 10.1158/2159-8290.CD-19-0338 PMID: 31554642
  49. Li, Z.; Rong, L. Cascade reaction-mediated efficient ferroptosis synergizes with immunomodulation for high-performance cancer therapy. Biomater. Sci., 2020, 8(22), 6272-6285. doi: 10.1039/D0BM01168A PMID: 33016289
  50. Hao, X.; Zheng, Z.; Liu, H.; Zhang, Y.; Kang, J.; Kong, X.; Rong, D.; Sun, G.; Sun, G.; Liu, L.; Yu, H.; Tang, W.; Wang, X. Inhibition of APOC1 promotes the transformation of M2 into M1 macrophages via the ferroptosis pathway and enhances anti-PD1 immunotherapy in hepatocellular carcinoma based on single-cell RNA sequencing. Redox Biol., 2022, 56, 102463. doi: 10.1016/j.redox.2022.102463 PMID: 36108528
  51. Liao, P.; Wang, W.; Wang, W.; Kryczek, I.; Li, X.; Bian, Y.; Sell, A.; Wei, S.; Grove, S.; Johnson, J.K.; Kennedy, P.D.; Gijón, M.; Shah, Y.M.; Zou, W. CD8+ T cells and fatty acids orchestrate tumor ferroptosis and immunity via ACSL4. Cancer Cell, 2022, 40(4), 365-378.e6. doi: 10.1016/j.ccell.2022.02.003 PMID: 35216678
  52. Wang, W.; Green, M.; Choi, J.E.; Gijón, M.; Kennedy, P.D.; Johnson, J.K.; Liao, P.; Lang, X.; Kryczek, I.; Sell, A.; Xia, H.; Zhou, J.; Li, G.; Li, J.; Li, W.; Wei, S.; Vatan, L.; Zhang, H.; Szeliga, W.; Gu, W.; Liu, R.; Lawrence, T.S.; Lamb, C.; Tanno, Y.; Cieslik, M.; Stone, E.; Georgiou, G.; Chan, T.A.; Chinnaiyan, A.; Zou, W. CD8+ T cells regulate tumour ferroptosis during cancer immunotherapy. Nature, 2019, 569(7755), 270-274. doi: 10.1038/s41586-019-1170-y PMID: 31043744
  53. Tao, C.; Rouhi, J. A biosensor based on graphene oxide nanocomposite for determination of carcinoembryonic antigen in colorectal cancer biomarker. Environ. Res., 2023, 238(Pt 1), 117113. doi: 10.1016/j.envres.2023.117113 PMID: 37696325
  54. Deng, S.; Gu, J.; Jiang, Z.; Cao, Y.; Mao, F.; Xue, Y.; Wang, J.; Dai, K.; Qin, L.; Liu, K.; Wu, K.; He, Q.; Cai, K. Application of nanotechnology in the early diagnosis and comprehensive treatment of gastrointestinal cancer. J. Nanobiotechnology, 2022, 20(1), 415. doi: 10.1186/s12951-022-01613-4 PMID: 36109734
  55. Xiong, Y.; Xiao, C.; Li, Z.; Yang, X. Engineering nanomedicine for glutathione depletion-augmented cancer therapy. Chem. Soc. Rev., 2021, 50(10), 6013-6041. doi: 10.1039/D0CS00718H PMID: 34027953
  56. Xu, Y.; Qin, Z.; Ma, J.; Cao, W.; Zhang, P. Recent progress in nanotechnology based ferroptotic therapies for clinical applications. Eur. J. Pharmacol., 2020, 880, 173198. doi: 10.1016/j.ejphar.2020.173198 PMID: 32473167
  57. Zhu, T.; Shi, L.; Yu, C.; Dong, Y.; Qiu, F.; Shen, L.; Qian, Q.; Zhou, G.; Zhu, X. Ferroptosis promotes photodynamic therapy: Supramolecular photosensitizer-inducer nanodrug for enhanced cancer treatment. Theranostics, 2019, 9(11), 3293-3307. doi: 10.7150/thno.32867 PMID: 31244955
  58. Su, L.J.; Zhang, J.H.; Gomez, H.; Murugan, R.; Hong, X.; Xu, D.; Jiang, F.; Peng, Z.Y. Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid. Med. Cell. Longev., 2019, 2019, 1-13. doi: 10.1155/2019/5080843 PMID: 31737171
  59. Valashedi, M.R.; Najafi-Ghalehlou, N.; Nikoo, A.; Bamshad, C.; Tomita, K.; Kuwahara, Y.; Sato, T.; Roushandeh, A.M.; Roudkenar, M.H. Cashing in on ferroptosis against tumor cells: Usher in the next chapter. Life Sci., 2021, 285, 119958. doi: 10.1016/j.lfs.2021.119958 PMID: 34534562
  60. Zorov, D.B.; Juhaszova, M.; Sollott, S.J. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev., 2014, 94(3), 909-950. doi: 10.1152/physrev.00026.2013 PMID: 24987008
  61. Breuer, W.; Shvartsman, M.; Cabantchik, Z.I. Intracellular labile iron. Int. J. Biochem. Cell Biol., 2008, 40(3), 350-354. doi: 10.1016/j.biocel.2007.03.010 PMID: 17451993
  62. Hassannia, B.; Vandenabeele, P.; Vanden, B.T. Targeting ferroptosis to iron out cancer. Cancer Cell, 2019, 35(6), 830-849. doi: 10.1016/j.ccell.2019.04.002 PMID: 31105042
  63. Kagan, V.E.; Mao, G.; Qu, F.; Angeli, J.P.F.; Doll, S.; Croix, C.S.; Dar, H.H.; Liu, B.; Tyurin, V.A.; Ritov, V.B.; Kapralov, A.A.; Amoscato, A.A.; Jiang, J.; Anthonymuthu, T.; Mohammadyani, D.; Yang, Q.; Proneth, B.; Klein-Seetharaman, J.; Watkins, S.; Bahar, I.; Greenberger, J.; Mallampalli, R.K.; Stockwell, B.R.; Tyurina, Y.Y.; Conrad, M.; Bayır, H. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat. Chem. Biol., 2017, 13(1), 81-90. doi: 10.1038/nchembio.2238 PMID: 27842066
  64. Tsoi, J.; Robert, L.; Paraiso, K.; Galvan, C.; Sheu, K.M.; Lay, J.; Wong, D.J.L.; Atefi, M.; Shirazi, R.; Wang, X.; Braas, D.; Grasso, C.S.; Palaskas, N.; Ribas, A.; Graeber, T.G. Multi-stage differentiation defines melanoma subtypes with differential vulnerability to drug-induced iron-dependent oxidative stress. Cancer Cell, 2018, 33(5), 890-904.e5. doi: 10.1016/j.ccell.2018.03.017 PMID: 29657129
  65. Conrad, M.; Pratt, D.A. The chemical basis of ferroptosis. Nat. Chem. Biol., 2019, 15(12), 1137-1147. doi: 10.1038/s41589-019-0408-1 PMID: 31740834
  66. Golej, D.L.; Askari, B.; Kramer, F.; Barnhart, S.; Vivekanandan-Giri, A.; Pennathur, S.; Bornfeldt, K.E. Long-chain acyl-CoA synthetase 4 modulates prostaglandin E2 release from human arterial smooth muscle cells. J. Lipid Res., 2011, 52(4), 782-793. doi: 10.1194/jlr.M013292 PMID: 21242590
  67. Yan, B.; Ai, Y.; Sun, Q.; Ma, Y.; Cao, Y.; Wang, J.; Zhang, Z.; Wang, X. Membrane damage during ferroptosis is caused by oxidation of phospholipids catalyzed by the oxidoreductases POR and CYB5R1. Mol. Cell, 2021, 81(2), 355-369.e10. doi: 10.1016/j.molcel.2020.11.024 PMID: 33321093
  68. Zou, Y.; Li, H.; Graham, E.T.; Deik, A.A.; Eaton, J.K.; Wang, W.; Sandoval-Gomez, G.; Clish, C.B.; Doench, J.G.; Schreiber, S.L. Cytochrome P450 oxidoreductase contributes to phospholipid peroxidation in ferroptosis. Nat. Chem. Biol., 2020, 16(3), 302-309. doi: 10.1038/s41589-020-0472-6 PMID: 32080622
  69. Bersuker, K.; Hendricks, J.M.; Li, Z.; Magtanong, L.; Ford, B.; Tang, P.H.; Roberts, M.A.; Tong, B.; Maimone, T.J.; Zoncu, R.; Bassik, M.C.; Nomura, D.K.; Dixon, S.J.; Olzmann, J.A. The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis. Nature, 2019, 575(7784), 688-692. doi: 10.1038/s41586-019-1705-2 PMID: 31634900
  70. Kraft, V.A.N.; Bezjian, C.T.; Pfeiffer, S.; Ringelstetter, L.; Müller, C.; Zandkarimi, F.; Merl-Pham, J.; Bao, X.; Anastasov, N.; Kössl, J.; Brandner, S.; Daniels, J.D.; Schmitt-Kopplin, P.; Hauck, S.M.; Stockwell, B.R.; Hadian, K.; Schick, J.A. GTP cyclohydrolase 1/tetrahydrobiopterin counteract ferroptosis through lipid remodeling. ACS Cent. Sci., 2020, 6(1), 41-53. doi: 10.1021/acscentsci.9b01063 PMID: 31989025
  71. Mao, C.; Liu, X.; Zhang, Y.; Lei, G.; Yan, Y.; Lee, H.; Koppula, P.; Wu, S.; Zhuang, L.; Fang, B.; Poyurovsky, M.V.; Olszewski, K.; Gan, B. DHODH-mediated ferroptosis defence is a targetable vulnerability in cancer. Nature, 2021, 593(7860), 586-590. doi: 10.1038/s41586-021-03539-7 PMID: 33981038
  72. Stockwell, B.R.; Friedmann Angeli, J.P.; Bayir, H.; Bush, A.I.; Conrad, M.; Dixon, S.J.; Fulda, S.; Gascón, S.; Hatzios, S.K.; Kagan, V.E.; Noel, K.; Jiang, X.; Linkermann, A.; Murphy, M.E.; Overholtzer, M.; Oyagi, A.; Pagnussat, G.C.; Park, J.; Ran, Q.; Rosenfeld, C.S.; Salnikow, K.; Tang, D.; Torti, F.M.; Torti, S.V.; Toyokuni, S.; Woerpel, K.A.; Zhang, D.D. Ferroptosis: A regulated cell death nexus linking metabolism, redox biology, and disease. Cell, 2017, 171(2), 273-285. doi: 10.1016/j.cell.2017.09.021 PMID: 28985560
  73. Liang, C.; Zhang, X.; Yang, M.; Dong, X. Recent progress in ferroptosis inducers for cancer therapy. Adv. Mater., 2019, 31(51), 1904197. doi: 10.1002/adma.201904197 PMID: 31595562
  74. Guo, J.; Xu, B.; Han, Q.; Zhou, H.; Xia, Y.; Gong, C.; Dai, X.; Li, Z.; Wu, G. Ferroptosis: A novel anti-tumor action for cisplatin. Cancer Res. Treat., 2018, 50(2), 445-460. doi: 10.4143/crt.2016.572 PMID: 28494534
  75. Ma, S.; Henson, E.S.; Chen, Y.; Gibson, S.B. Ferroptosis is induced following siramesine and lapatinib treatment of breast cancer cells. Cell Death Dis., 2016, 7(7), e2307. doi: 10.1038/cddis.2016.208 PMID: 27441659
  76. Sato, M.; Kusumi, R.; Hamashima, S.; Kobayashi, S.; Sasaki, S.; Komiyama, Y.; Izumikawa, T.; Conrad, M.; Bannai, S.; Sato, H. The ferroptosis inducer erastin irreversibly inhibits system xc− and synergizes with cisplatin to increase cisplatin’s cytotoxicity in cancer cells. Sci. Rep., 2018, 8(1), 968. doi: 10.1038/s41598-018-19213-4 PMID: 29343855
  77. Viswanathan, V.S.; Ryan, M.J.; Dhruv, H.D.; Gill, S.; Eichhoff, O.M.; Seashore-Ludlow, B.; Kaffenberger, S.D.; Eaton, J.K.; Shimada, K.; Aguirre, A.J.; Viswanathan, S.R.; Chattopadhyay, S.; Tamayo, P.; Yang, W.S.; Rees, M.G.; Chen, S.; Boskovic, Z.V.; Javaid, S.; Huang, C.; Wu, X.; Tseng, Y.Y.; Roider, E.M.; Gao, D.; Cleary, J.M.; Wolpin, B.M.; Mesirov, J.P.; Haber, D.A.; Engelman, J.A.; Boehm, J.S.; Kotz, J.D.; Hon, C.S.; Chen, Y.; Hahn, W.C.; Levesque, M.P.; Doench, J.G.; Berens, M.E.; Shamji, A.F.; Clemons, P.A.; Stockwell, B.R.; Schreiber, S.L. Dependency of a therapy-resistant state of cancer cells on a lipid peroxidase pathway. Nature, 2017, 547(7664), 453-457. doi: 10.1038/nature23007 PMID: 28678785
  78. Chen, X.; Kang, R.; Kroemer, G.; Tang, D. Broadening horizons: The role of ferroptosis in cancer. Nat. Rev. Clin. Oncol., 2021, 18(5), 280-296. doi: 10.1038/s41571-020-00462-0 PMID: 33514910
  79. Hangauer, M.J.; Viswanathan, V.S.; Ryan, M.J.; Bole, D.; Eaton, J.K.; Matov, A.; Galeas, J.; Dhruv, H.D.; Berens, M.E.; Schreiber, S.L.; McCormick, F.; McManus, M.T. Drug-tolerant persister cancer cells are vulnerable to GPX4 inhibition. Nature, 2017, 551(7679), 247-250. doi: 10.1038/nature24297 PMID: 29088702
  80. Lei, G.; Zhang, Y.; Koppula, P.; Liu, X.; Zhang, J.; Lin, S.H.; Ajani, J.A.; Xiao, Q.; Liao, Z.; Wang, H.; Gan, B. The role of ferroptosis in ionizing radiation-induced cell death and tumor suppression. Cell Res., 2020, 30(2), 146-162. doi: 10.1038/s41422-019-0263-3 PMID: 31949285
  81. Bai, X.; Ni, J.; Beretov, J.; Wasinger, V.C.; Wang, S.; Zhu, Y.; Graham, P.; Li, Y. Activation of the eIF2α/ATF4 axis drives triple-negative breast cancer radioresistance by promoting glutathione biosynthesis. Redox Biol., 2021, 43, 101993. doi: 10.1016/j.redox.2021.101993 PMID: 33946018
  82. Bukowski, K.; Kciuk, M.; Kontek, R. Mechanisms of multidrug resistance in cancer chemotherapy. Int. J. Mol. Sci., 2020, 21(9), 3233. doi: 10.3390/ijms21093233 PMID: 32370233
  83. Ravindran Menon, D.; Hammerlindl, H.; Torrano, J.; Schaider, H.; Fujita, M. Epigenetics and metabolism at the crossroads of stress-induced plasticity, stemness and therapeutic resistance in cancer. Theranostics, 2020, 10(14), 6261-6277. doi: 10.7150/thno.42523 PMID: 32483452
  84. Zhang, M.X.; Wang, L.; Zeng, L.; Tu, Z.W. LCN2 is a potential biomarker for radioresistance and recurrence in nasopharyngeal carcinoma. Front. Oncol., 2021, 10, 605777. doi: 10.3389/fonc.2020.605777 PMID: 33604288
  85. Demuynck, R.; Efimova, I.; Catanzaro, E.; Krysko, D.V. Ferroptosis: Friend or foe in cancer immunotherapy? OncoImmunology, 2023, 12(1), 2182992. doi: 10.1080/2162402X.2023.2182992 PMID: 36875549
  86. Du, S.; Zeng, F.; Deng, G. Tumor neutrophils ferroptosis: A targetable immunosuppressive mechanism for cancer immunotherapy. Signal Transduct. Target. Ther., 2023, 8(1), 77. doi: 10.1038/s41392-023-01357-z PMID: 36813764
  87. Chen, D.S.; Mellman, I. Elements of cancer immunity and the cancer–immune set point. Nature, 2017, 541(7637), 321-330. doi: 10.1038/nature21349 PMID: 28102259
  88. Sharma, P.; Allison, J.P. The future of immune checkpoint therapy. Science, 2015, 348(6230), 56-61. doi: 10.1126/science.aaa8172 PMID: 25838373
  89. Wei, S.C.; Levine, J.H.; Cogdill, A.P.; Zhao, Y.; Anang, N.A.A.S.; Andrews, M.C.; Sharma, P.; Wang, J.; Wargo, J.A.; Pe’er, D.; Allison, J.P. Distinct cellular mechanisms underlie anti-CTLA-4 and anti-PD-1 checkpoint blockade. Cell, 2017, 170(6), 1120-1133.e17. doi: 10.1016/j.cell.2017.07.024 PMID: 28803728
  90. Morad, G.; Helmink, B.A.; Sharma, P.; Wargo, J.A. Hallmarks of response, resistance, and toxicity to immune checkpoint blockade. Cell, 2021, 184(21), 5309-5337. doi: 10.1016/j.cell.2021.09.020 PMID: 34624224
  91. Yuen, V.W.H.; Chiu, D.K.C.; Law, C.T.; Cheu, J.W.S.; Chan, C.Y.K.; Wong, B.P.Y.; Goh, C.C.; Zhang, M.S.; Xue, H.D.G.; Tse, A.P.W.; Zhang, Y.; Lau, H.Y.H.; Lee, D.; Au-Yeung, R.K.H.; Wong, C.M.; Wong, C.C.L. Using mouse liver cancer models based on somatic genome editing to predict immune checkpoint inhibitor responses. J. Hepatol., 2023, 78(2), 376-389. doi: 10.1016/j.jhep.2022.10.037 PMID: 36455783
  92. Bonaventura, P.; Shekarian, T.; Alcazer, V.; Valladeau-Guilemond, J.; Valsesia-Wittmann, S.; Amigorena, S.; Caux, C.; Depil, S. Cold tumors: A therapeutic challenge for immunotherapy. Front. Immunol., 2019, 10, 168. doi: 10.3389/fimmu.2019.00168 PMID: 30800125
  93. Galon, J.; Bruni, D. Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat. Rev. Drug Discov., 2019, 18(3), 197-218. doi: 10.1038/s41573-018-0007-y PMID: 30610226
  94. Zhang, J.; Huang, D.; Saw, P.E.; Song, E. Turning cold tumors hot: from molecular mechanisms to clinical applications. Trends Immunol., 2022, 43(7), 523-545. doi: 10.1016/j.it.2022.04.010 PMID: 35624021
  95. Daei Sorkhabi, A.; Mohamed Khosroshahi, L.; Sarkesh, A.; Mardi, A.; Aghebati-Maleki, A.; Aghebati-Maleki, L.; Baradaran, B. The current landscape of CAR T-cell therapy for solid tumors: Mechanisms, research progress, challenges, and counterstrategies. Front. Immunol., 2023, 14, 1113882. doi: 10.3389/fimmu.2023.1113882 PMID: 37020537
  96. Ma, S.; Li, X.; Wang, X.; Cheng, L.; Li, Z.; Zhang, C.; Ye, Z.; Qian, Q. Current progress in CAR-T cell therapy for solid tumors. Int. J. Biol. Sci., 2019, 15(12), 2548-2560. doi: 10.7150/ijbs.34213 PMID: 31754328
  97. Szakács, G.; Paterson, J.K.; Ludwig, J.A.; Booth-Genthe, C.; Gottesman, M.M. Targeting multidrug resistance in cancer. Nat. Rev. Drug Discov., 2006, 5(3), 219-234. doi: 10.1038/nrd1984 PMID: 16518375
  98. Yin, W.; Chang, J.; Sun, J.; Zhang, T.; Zhao, Y.; Li, Y.; Dong, H. Nanomedicine-mediated ferroptosis targeting strategies for synergistic cancer therapy. J. Mater. Chem. B Mater. Biol. Med., 2023, 11(6), 1171-1190. doi: 10.1039/D2TB02161G PMID: 36650960
  99. Xie, S.; Sun, W.; Zhang, C.; Dong, B.; Yang, J.; Hou, M.; Xiong, L.; Cai, B.; Liu, X.; Xue, W. Metabolic control by heat stress determining cell fate to ferroptosis for effective cancer therapy. ACS Nano, 2021, 15(4), 7179-7194. doi: 10.1021/acsnano.1c00380 PMID: 33861924
  100. An, Y.; Zhu, J.; Liu, F.; Deng, J.; Meng, X.; Liu, G.; Wu, H.; Fan, A.; Wang, Z.; Zhao, Y. Boosting the ferroptotic antitumor efficacy via site-specific amplification of tailored lipid peroxidation. ACS Appl. Mater. Interfaces, 2019, 11(33), 29655-29666. doi: 10.1021/acsami.9b10954 PMID: 31359759
  101. Ma, P.; Xiao, H.; Yu, C.; Liu, J.; Cheng, Z.; Song, H.; Zhang, X.; Li, C.; Wang, J.; Gu, Z.; Lin, J. Enhanced cisplatin chemotherapy by iron oxide nanocarrier-mediated generation of highly toxic reactive oxygen species. Nano Lett., 2017, 17(2), 928-937. doi: 10.1021/acs.nanolett.6b04269 PMID: 28139118
  102. Yao, X.; Yang, P.; Jin, Z.; Jiang, Q.; Guo, R.; Xie, R.; He, Q.; Yang, W. Multifunctional nanoplatform for photoacoustic imaging-guided combined therapy enhanced by CO induced ferroptosis. Biomaterials, 2019, 197, 268-283. doi: 10.1016/j.biomaterials.2019.01.026 PMID: 30677556
  103. Isola, A.L.; Chen, S. Exosomes: The messengers of health and disease. Curr. Neuropharmacol., 2017, 15(1), 157-165. doi: 10.2174/1570159X14666160825160421 PMID: 27568544
  104. Kalluri, R.; LeBleu, V.S. The biology, function, and biomedical applications of exosomes. Science, 2020, 367(6478), eaau6977. doi: 10.1126/science.aau6977 PMID: 32029601
  105. Batrakova, E.V.; Kim, M.S. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J. Control. Release, 2015, 219, 396-405. doi: 10.1016/j.jconrel.2015.07.030 PMID: 26241750
  106. Liang, Y.; Duan, L.; Lu, J.; Xia, J. Engineering exosomes for targeted drug delivery. Theranostics, 2021, 11(7), 3183-3195. doi: 10.7150/thno.52570 PMID: 33537081
  107. Qiu, X.; Li, Z.; Han, X.; Zhen, L.; Luo, C.; Liu, M.; Yu, K.; Ren, Y. Tumor-derived nanovesicles promote lung distribution of the therapeutic nanovector through repression of Kupffer cell-mediated phagocytosis. Theranostics, 2019, 9(9), 2618-2636. doi: 10.7150/thno.32363 PMID: 31131057
  108. Du, J.; Wan, Z.; Wang, C.; Lu, F.; Wei, M.; Wang, D.; Hao, Q. Designer exosomes for targeted and efficient ferroptosis induction in cancer via chemo-photodynamic therapy. Theranostics, 2021, 11(17), 8185-8196. doi: 10.7150/thno.59121 PMID: 34373736
  109. Chen, X.; Kang, R.; Kroemer, G.; Tang, D. Ferroptosis in infection, inflammation, and immunity. J. Exp. Med., 2021, 218(6), e20210518. doi: 10.1084/jem.20210518 PMID: 33978684
  110. Fang, X.; Ardehali, H.; Min, J.; Wang, F. The molecular and metabolic landscape of iron and ferroptosis in cardiovascular disease. Nat. Rev. Cardiol., 2023, 20(1), 7-23. doi: 10.1038/s41569-022-00735-4 PMID: 35788564
  111. Stockwell, B.R. Ferroptosis turns 10: Emerging mechanisms, physiological functions, and therapeutic applications. Cell, 2022, 185(14), 2401-2421. doi: 10.1016/j.cell.2022.06.003 PMID: 35803244
  112. Ma, L.; Hostetler, A.; Morgan, D.M.; Maiorino, L.; Sulkaj, I.; Whittaker, C.A.; Neeser, A.; Pires, I.S.; Yousefpour, P.; Gregory, J.; Qureshi, K.; Dye, J.; Abraham, W.; Suh, H.; Li, N.; Love, J.C.; Irvine, D.J.; Vaccine-boosted, C.A.R. Vaccine-boosted CAR T crosstalk with host immunity to reject tumors with antigen heterogeneity. Cell, 2023, 186(15), 3148-3165.e20. doi: 10.1016/j.cell.2023.06.002 PMID: 37413990
  113. Feng, Y.; Dai, Y. APOL3-LDHA axis related immunity activation and cancer ferroptosis induction. Int. J. Biol. Sci., 2023, 19(5), 1401-1402. doi: 10.7150/ijbs.83342 PMID: 37056935
  114. Dai, E.; Han, L.; Liu, J.; Xie, Y.; Kroemer, G.; Klionsky, D.J.; Zeh, H.J.; Kang, R.; Wang, J.; Tang, D. Autophagy-dependent ferroptosis drives tumor-associated macrophage polarization via release and uptake of oncogenic KRAS protein. Autophagy, 2020, 16(11), 2069-2083. doi: 10.1080/15548627.2020.1714209 PMID: 31920150

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