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Review

Ferroptosis: a new unexpected chance to treat metastatic melanoma?

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 2411-2425 | Received 10 Jun 2020, Accepted 28 Jul 2020, Published online: 20 Aug 2020

References

  • Tsao H, Atkins MB, Sober Arthur J. Management of cutaneous melanoma. N Engl J Med. 2004;351:998-1012.
  • Markovic SN, Erickson LA, Rao RD, et al. Malignant melanoma in the 21st century, part 1: epidemiology, risk factors, screening, prevention, and diagnosis. Proceed Mayo Clin Proceed. Elsevier Ltd. 2007;82:364–380.
  • All cancers; 2018. Available from: https://gco.iarc.fr/today/data/factsheets/cancers/16-Melanoma-of-skin-fact-sheet.pdf
  • Table S. Tobacco use 44 sources of statistics 68 American cancer society recommendations for the early detection of cancer in average-risk asymptomatic people 71. Atlanta: American Cancer Society; 2020.
  • Rigel DS. Rigel epidemiology of melanoma. Semin Cutan Med Surg. 2010 Dec;29(4):204–209. .
  • Lasithiotakis KG, Petrakis IE, Garbe C. Cutaneous melanoma in the elderly: epidemiology, prognosis and treatment. Melanoma Res. 2010;20:163–170.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7–30.
  • Cho E, BA R, GA. C. Risk factors for melanoma by body site. Cancer Epidemiol Biomarkers Prev. 2005;14:1241–1244.
  • Kraemer KH, Greene MH. Dysplastic nevus syndrome. Familial and sporadic precursors of cutaneous melanoma. Dermatol Clin. 1985;3:225–237.
  • Corazzari M, PE. L. Harnessing autophagy for melanoma benefit. Cell Biol Res Ther. 2013;2:1.
  • DE B, JA R, JA S, et al. J., P. A role for sunlight in skin cancer: uVinduced p53 mutations in squamous cell carcinoma. PNAS. 1991;88:10124–10128.
  • Kamb A, Gruis NA, Weaver-Feldhaus J, et al. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 1994;264:436–440.
  • Potrony M, Badenas C, Aguilera P, et al. Update in genetic susceptibility in melanoma. Ann Transl Med. 2015;3:210.
  • Tagliabue E, Gandini S, Bellocco R, et al. MC1R variants as melanoma risk factors independent of at-risk phenotypic characteristics: a pooled analysis from the M-SKIP project. Cancer Manag Res. 2018;10:1143–1154.
  • Flaherty KT, Infante JR, Daud A, et al. Combined BRAF and MEK Inhibition in Melanoma with BRAF V600 Mutations. N Engl J Med. 2012;367:1694–1703.
  • Gray-Schopfer V, Wellbrock C, Marais R. R., M. Melanoma biology and new targeted therapy. Nature. 2007;445:851–857.
  • ER C-D, JJ O, OM. S. BRAFV600E: implications for carcinogenesis and molecular therapy. Mol Cancer Ther. 2011;10:385–394.
  • Dhomen N, Marais R, Signaling BRAF. Targeted Therapies in Melanoma. Hematol Oncol Clin North Am. 2009;23:529–545.
  • AH A-T, Li G. G., L. Genetic alterations of PTEN in human melanoma. Cell Mol Life Sci. 2012;69:1475–1491.
  • Giglio P, Fimia GM, Lovat PE, et al. Fateful music from a talented orchestra with a wicked conductor: connection between oncogenic BRAF, ER stress, and autophagy in human melanoma. Mol Cell Oncol. 2015;2:e995016.
  • White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer. 2012;12:401–410.
  • Hersey P, Zhang XD. Adaptation to ER stress as a driver of malignancy and resistance to therapy in human melanoma. Pigment Cell Melanoma Res. 2008;21:358–367.
  • Corazzari M, Lovat PE, Armstrong JL, et al. Targeting homeostatic mechanisms of endoplasmic reticulum stress to increase susceptibility of cancer cells to fenretinide-induced apoptosis: the role of stress proteins ERdj5 and ERp57. Br J Cancer. 2007;96:1062–71.
  • Corazzari M, Fimia GM, Lovat P, et al. Why is autophagy important for melanoma? Molecular mechanisms and therapeutic implications. Semin Cancer Biol. 2013;23:337–43.
  • JL A, Corazzari M, Martin S, et al. Oncogenic B-RAF signaling in melanoma impairs the therapeutic advantage of autophagy inhibition. Clin Cancer Res. 2011;17:2216–2226.
  • DT R, SM A, Miller CN, et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 2006;4:e374.
  • Corazzari M, Gagliardi M, Fimia GM, et al. Endoplasmic reticulum stress, unfolded protein response, and cancer cell fate. Front Oncol. 2017;7:78.
  • Corazzari M, Rapino F, Ciccosanti F, et al. Oncogenic BRAF induces chronic ER stress condition resulting in increased basal autophagy and apoptotic resistance of cutaneous melanoma. Cell Death Differ. 2015;22:946–958.
  • Lovat PE, Corazzari M, Armstrong JL, et al. Increasing melanoma cell death using inhibitors of protein disulfide isomerases to abrogate survival responses to endoplasmic reticulum stress. Cancer Res. 2008;68:5363–9.
  • Niezgoda A, Niezgoda P, Czajkowski R. R., C. Novel approaches to treatment of advanced melanoma: a review on targeted therapy and immunotherapy. Biomed Res Int. 2015;2015:851387.
  • TR W, Fridlyand J, Yan Y, et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature. 2012;487:505–509.
  • Long GV, Stroyakovskiy D, Gogas H, et al. Combined BRAF and MEK inhibition versus BRAF inhibition alone in melanoma. N Engl J Med. 2014;371:1877–1888.
  • Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39:1–10.
  • Li X, Lu W, Zheng X, et al. Emerging immune checkpoints for cancer therapy. Acta Oncol. 2015;54:1706–1713.
  • Weber J. Overcoming immunologic tolerance to melanoma: targeting CTLA-4 with ipilimumab (MDX-010). Oncol. 2008;13:16–25.
  • Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–264.
  • Schadendorf D, Hodi FS, Robert C, et al. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma. J Clin Oncol. 2015;33:1889–1894.
  • Hodi FS, O’Day SJ, McDermott DF, et al. Improved Survival with Ipilimumab in Patients with Metastatic Melanoma. N Engl J Med. 2010;363:711–723.
  • Dong H, SE S, DR S, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8:793–800.
  • Schachter J, Ribas A, Long GV, et al. Pembrolizumab versus ipilimumab for advanced melanoma: final overall survival results of a multicentre, randomised, open-label phase 3 study (KEYNOTE-006). Lancet. 2017;390:1853–1862.
  • Ribas A. Tumor immunotherapy directed at PD-1. N Engl J Med. 2012;366:2517–2519.
  • Galluzzi L, Vitale I, JM A, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012;19:107–120.
  • DR G, Ferguson T, Zitvogel L. G., K. Immunogenic and tolerogenic cell death. Nat Rev Immunol. 2009;9:353–363.
  • AM D, Martin S, AD G. P., A. Immature, semi‐mature, and fully mature dendritic cells: toward a DC‐cancer cells interface that augments anticancer immunity.. Front Immunol. 2013;4:438.
  • AD G, Galluzzi L, Apetoh L, et al. Molecular and translational Classifications of DaMPs in immunogenic cell death. Front Immunol. 2015;6:588.
  • Bezu L, LC G-S, Ewitte HBK, et al. G., K. Combinatorial strategies for the induction of immunogenic cell death. Front Immunol. 2015;6:187.
  • Fucikova J, Kralikova P, Fialova A, et al. R., S. Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res. 2011;71:4821–4833.
  • Tesniere A, Schlemmer F, Boige V, et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene. 2010;29:482–491.
  • Schiavoni G, Sistigu A, Valentini M, et al. Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res. 2011;71:768–778.
  • Spisek R, Charalambous A, Mazumder A, et al. Bortezomib enhances dendritic cell (DC)-mediated induction of immunity to human myeloma via exposure of cell surface heat shock protein 90 on dying tumor cells: therapeutic implications. Blood. 2007;109:4839–4845.
  • Giglio P, Gagliardi M, Tumino N, et al. PKR and GCN2 stress kinases promote an ER stress-independent eIF2α phosphorylation responsible for calreticulin exposure in melanoma cells. Oncoimmunology. 2018. DOI:10.1080/2162402X.2018.1466765.
  • Giglio P, Gagliardi M, Bernardini R, et al. Ecto-Calreticulin is essential for an efficient immunogenic cell death stimulation in mouse melanoma. Genes Immun 2019;20:509–513.
  • Dolma S, SL L, WC H, et al. Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell. 2003;3:285–296.
  • WS Y, BR S. Synthetic lethal screening identifies compounds activating iron-dependent, nonapoptotic cell death in oncogenic-RAS-harboring cancer cells. Chem Biol. 2008;15:234–245.
  • Kroemer G, Galluzzi L, Vandenabeele P, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16:3–11.
  • Galluzzi L, Vitale I, Aaronson SA, et al.. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ. 2018;25:486–541.
  • Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an Iron-Dependent Form of Nonapoptotic Cell Death. Cell. 2012;149:1060–1072.
  • Shah R, Shchepinov MS, Pratt DA. Resolving the Role of Lipoxygenases in the Initiation and Execution of Ferroptosis. ACS Cent Sci. 2018;4:387–396.
  • DM W. J., and K. Ferroportin-mediated iron transport: expression and regulation. Biochim Biophys Acta. 2012;1823:1426–1433.
  • Gao M, Monian P, Qudri N, et al. Glutaminolysis and Transferrin Regulate Ferroptosis. Mol Cell. 2015;59:298–308.
  • JD M, Wang X, Steven PG, et al. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy.. Nature. 2014;509:105–109.
  • JD M, VL. P, Nissim S, et al. Ferritinophagy via NCOA4 is required for erythropoiesis and is regulated by iron dependent HERC2-mediated proteolysis. Elife. 2015;4:e10308.
  • Song X, Zhu S, Chen P, et al. AMPK-Mediated BECN1 Phosphorylation Promotes Ferroptosis by Directly Blocking System Xc– activity. Curr Biol. 2018;28:2388–2399.e5.
  • WS Y, KJ K, Gaschler MM, et al. Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc Natl Acad Sci U S A. 2016;113:E4966–75.
  • JZ H, CD. F. Lipoxygenase and leukotriene pathways: biochemistry, biology, and roles in disease. Chem Rev. 2011;111:5866–5898.
  • Yan S, XF Y, Liu HL, et al. Longchain acyl-CoA synthetase in fatty acid metabolism involved in liver and other diseases: an update. World J Gastroenterol. 2015;21:3492–3498.
  • Xie Y, Hou W, Song X, et al. Ferroptosis: process and function. Cell Death Differ. 2016;23:369–379.
  • Birben E, UM S, Sackesen C, et al., O., K. Oxidative Stress and Antioxidant Defense. World Allergy Organ J. 2012;5:9–19.
  • Gagliardi M, Cotella D, Santoro C, et al. M., C. Aldo-keto reductases protect metastatic melanoma from ER stress-independent ferroptosis. Cell Death Dis. 2019;10:902.
  • SJ D, GE W, LS M, et al. Human Haploid Cell Genetics Reveals Roles for Lipid Metabolism Genes in Nonapoptotic Cell Death. ACS Chem Biol. 2015;10:1604–1609.
  • Yuan H, Li X, Zhang X, et al. Identification of ACSL4 as a biomarker and contributor of ferroptosis. Biochem Biophys Res Commun. 2016;478:1338–1343.
  • Burton GW, KU I. Vitamin E: application of the principles of physical organic chemistry to the exploration of its structure and function. Acc Chem Res. 1986;19:194–201.
  • Lucarini M, Pedrielli P, Pedulli GF, et al. Bond Dissociation Energies of O−H Bonds in Substituted Phenols from Equilibration Studies. J Org Chem. 1996;61:9259–9263.
  • Feng H, Stockwell BR. Unsolved mysteries: how does lipid peroxidation cause ferroptosis? PLOS Biol. 2018;16:e2006203.
  • Doll S, Freitas FP, Shah R, et al. FSP1 is a glutathione-independent ferroptosis suppressor. Nature. 2019;575:693–698.
  • Bersuker K, Hendricks JM, Li Z, et al. The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis. Nature. 2019;575:688–692.
  • Kagan VE, Mao G, Qu F, et al. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat Chem Biol. 2017;13:81–90.
  • QZ T, Lei P, Jackman KA, et al. Tau-mediated iron export prevents ferroptotic damage after ischemic stroke.. Mol Psychiatry. 2017;22:1520–1530.
  • Perez MA, Magtanong L, Dixon SJ, et al. Dietary Lipids Induce Ferroptosis in Caenorhabditis elegans and Human Cancer Cells. Dev Cell. 2020;S1534-5807(20)30498-6.
  • Sato H, Tamba M, Ishii T. S., B.Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem. 1999;274:11455–11458.
  • MC J, DD. Z. The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev. 2013;27:2179–2191.
  • Jiang L, Kon N, Li T, et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature. 2015;520:57–62.
  • Had-Aissouni L. Toward a new role for plasma membrane sodium-dependent glutamate transporters of astrocytes: maintenance of antioxidant defenses beyond extracellular glutamate clearance. Amin Acids. 2012;42:181–197.
  • Okuno S, Sato H, Kuriyama-Matsumura K, et al. Role of cystine transport in intracellular glutathione level and cisplatin resistance in human ovarian cancer cell lines. Br J Cancer. 2003;88:951–956.
  • SC B, SL C, BR H, et al. H., S. Glutamate release by primary brain tumors induces epileptic activity. Nat Med. 2011;17:1269–1274.
  • Coriat R, Nicco C, Chéreau C, et al. Sorafenib-induced hepatocellular carcinoma cell death depends on reactive oxygen species production in vitro and in vivo. Mol Cancer Ther. 2012;11:2284–2293.
  • Xu X, Zhang X, Wei C, et al. Targeting SLC7A11 specifically suppresses the progression of colorectal cancer stem cells via inducing ferroptosis. Eur J Pharm Sci. 2020;152:105450.
  • Hayano M, WS Y, CK C, et al. Loss of cysteinyl-tRNA synthetase (CARS) induces the transsulfuration pathway and inhibits ferroptosis induced by cystine deprivation. Cell Death Differ. 2016;23:270–278.
  • LJ Y, Ran Q, Rao L, et al. The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic Biol Med. 2003;34:496–502.
  • Brigelius-Flohé R. M., M. Glutathione Peroxidases. Biochim Biophys Acta. 2013;1830:3289–3303.
  • Sui X, Zhang R, Liu S, et al. RSL3 Drives Ferroptosis Through GPX4 Inactivation and ROS Production in Colorectal Cancer. Front Pharmacol. 2018;9:1371.
  • Yang WS, SriRamaratnam R, Welsch ME, et al. Regulation of Ferroptotic Cancer Cell Death by GPX4. Cell. 2014;156:317–331.
  • 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;98:609–619.
  • Shimada K, Hayano M, NC P, et al. Cell-Line Selectivity Improves the Predictive Power of Pharmacogenomic Analyses and Helps Identify NADPH as Biomarker for Ferroptosis Sensitivity. Cell Chem Biol. 2016;23:225–235.
  • Krajka-Kuźniak V, Paluszczak J. W., B.-D. The Nrf2-ARE signaling pathway: an update on its regulation and possible role in cancer prevention and treatment. Pharmacol Rep. 2017;69:393–402.
  • Nguyen T, Nioi P, Pickett CB. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem. 2009;284:13291–13295.
  • Ma Q. Role of Nrf2 in Oxidative Stress and Toxicity. Annu Rev Pharmacol Toxicol. 2013;53:401–426.
  • MB S, KT L. NRF2 and cancer: the good, the bad and the importance of context. Nat Rev Cancer. 2012;12:564–571.
  • Wu X, Liu C, Li Z, et al. Regulation of GSK3β/Nrf2 signaling pathway modulated erastin-induced ferroptosis in breast cancer. Mol Cell Biochem. 2020;10.1007/s11010-020-03821-8.
  • Lu B, Chen XB, Ying MD, et al. The Role of Ferroptosis in Cancer Development and Treatment Response. Front Pharmacol. 2018;8:992.
  • Pollak N, Dölle C, Ziegler M. M., Z. The power to reduce: pyridine nucleotides–small molecules with a multitude of functions. Biochem J. 2007;402:205–218.
  • TM P, JE D. Human Aldo-Keto Reductases: function, Gene Regulation, and Single Nucleotide Polymorphisms. Arch Biochem Biophys. 2007;464:241–250.
  • Barski OA, Bhatnagar A, Bhatnagar A. T.S.M. The Aldo-Keto Reductase Superfamily and its Role in Drug Metabolism and Detoxification. Drug Metab Rev. 2008;40:553–624.
  • TM D, DW B, FL A, et al. PTHrP stimulates prostate cancer cell growth and upregulates aldo–keto reductase 1C3. Cancer Lett. 2011;306:52–59.
  • HK L, Steckelbroeck S, Fung KM, et al. Characterization of a monoclonal antibody for human aldo-keto reductase AKR1C3 (type 2 3α-hydroxysteroid dehydrogenase/type 5 17β-hydroxysteroid dehydrogenase); immunohistochemical detection in breast and prostate. Steroids. 2004;69:795–801.
  • AK J, Gunnarsson C, Cohen M, et al. O., S. 17β-Hydroxysteroid dehydrogenase 14 affects estradiol levels in breast cancer cells and is a prognostic marker in estrogen receptor positive breast cancer. Canc Res. 2006;66:11471–11477. .
  • Sasano H, Suzuki T, Miki Y. T., M. Intracrinology of estrogens and androgens in breast carcinoma. J Steroid Biochem Mol Biol. 2008;108:181–185. .
  • Tsoi J, Robert L, Paraiso K, et al. Multi-stage Differentiation Defines Melanoma Subtypes with Differential Vulnerability to Drug-Induced Iron-Dependent Oxidative Stress. Cancer Cell. 2018;33(890–904.e5). DOI:10.1016/j.ccell.2018.03.017.
  • DW D, Gout PW, Kurita T, et al. W., P.. Sulfasalazine-Induced Cystine Starvation: potential Use for Prostate CancerTherapy. Prostate. 2007;67:162–171. .
  • VS N, GM P, Gout PW, et al. Sulfasalazine-induced reduction of glutathione levels in breast cancer cells: enhancement of growth-inhibitory activity of Doxorubicin. Chemotherapy. 2007;53:210–217.
  • Lo M, Ling V, YZ W, et al. The xc- cystine/glutamate antiporter: a mediator of pancreatic cancer growth with a role in drug resistance. Br J Cancer. 2008;99:464–472.
  • Huang Y, Dai Z, Barbacioru C. W., S. Cystine-Glutamate Transporter SLC7A11 in Cancer Chemosensitivity and Chemoresistance. Cancer Res. 2005;65:7446–7454.
  • JP FA, DV K, Conrad M. M., C. Ferroptosis at the crossroads of cancer-acquired drug resistance and immune evasion. Nat Rev Cancer. 2019;19:405–414.
  • Wang W, Green M, Choi JE, et al. CD8+ T cells regulate tumour ferroptosis during cancer immunotherapy. Nature. 2019;569:270–274.

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