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Review Article

The crosstalk between ferroptosis and autophagy in cancer

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Article: 2289362 | Received 26 May 2023, Accepted 26 Nov 2023, Published online: 08 Dec 2023

References

  • 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(3):1–19.
  • Christgen S, Tweedell RE, Kanneganti T-D. Programming inflammatory cell death for therapy. Pharmacol Ther. 2021;232:108010.
  • Galluzzi L, Pedro B-S, Manuel J, et al. Regulated cell death and adaptive stress responses. Cell Mol Life Sci. 2016;73(11–12):2405–2410.
  • Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell. 2011;147(4):742–758.
  • Conradt B. Genetic control of programmed cell death during animal development. Annu Rev Genet. 2009;43(1):493–523.
  • Dolma S, Lessnick SL, Hahn WC, et al. Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell. 2003;3(3):285–296.
  • Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149(5):1060–1072.
  • Ursini F, Maiorino M. Lipid peroxidation and ferroptosis: the role of GSH and GPx4. Free Radic Biol Med. 2020;152:175–185.
  • Doll S, Freitas FP, Shah R, et al. FSP1 is a glutathione-independent ferroptosis suppressor. Nature. 2019;575(7784):693–698.
  • Mao C, Liu X, Zhang Y, et al. DHODH-mediated ferroptosis defence is a targetable vulnerability in cancer. Nature. 2021;593(7860):586–590.
  • Dai E, Meng L, Kang R, et al. ESCRT-III–dependent membrane repair blocks ferroptosis. Biochem Biophys Res Commun. 2020;522(2):415–421.
  • Kraft VA, Bezjian CT, Pfeiffer S, et al. GTP cyclohydrolase 1/tetrahydrobiopterin counteract ferroptosis through lipid remodeling. ACS Cent Sci. 2019;6(1):41–53.
  • Mizushima N, Levine B. Autophagy in human diseases. N Engl J Med. 2020;383(16):1564–1576.
  • Hara T, Takamura A, Kishi C, et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol. 2008;181(3):497–510.
  • Backer JM. The intricate regulation and complex functions of the class III phosphoinositide 3-kinase Vps34. Biochem J. 2016;473(15):2251–2271.
  • Ohashi Y, Tremel S, Williams RL. VPS34 complexes from a structural perspective. J Lipid Res. 2019;60(2):229–241.
  • Yang WS, SriRamaratnam R, Welsch ME, et al. Regulation of ferroptotic cancer cell death by GPX4. Cell. 2014;156(1–2):317–331.
  • Dixon SJ. Ferroptosis: bug or feature? Immunol Rev. 2017;277(1):150–157.
  • Thomasova D, Bruns HA, Kretschmer V, et al. Murine double minute-2 prevents p53-overactivation-related cell death (podoptosis) of podocytes. J Am Soc Nephrol. 2015;26(7):1513–1523.
  • Yoshida GJ. Therapeutic strategies of drug repositioning targeting autophagy to induce cancer cell death: from pathophysiology to treatment. J Hematol Oncol. 2017;10(1):67.
  • Chen X, Li J, Kang R, et al. Ferroptosis: machinery and regulation. Autophagy. 2021;17(9):2054–2081.
  • Hou W, Xie Y, Song X, et al. Autophagy promotes ferroptosis by degradation of ferritin. Autophagy. 2016;12(8):1425–1428.
  • Gao M, Monian P, Pan Q, et al. Ferroptosis is an autophagic cell death process. Cell Res. 2016;26(9):1021–1032.
  • Park E, Chung SW. ROS-mediated autophagy increases intracellular iron levels and ferroptosis by ferritin and transferrin receptor regulation. Cell Death Dis. 2019;10(11):822.
  • Zhang Z, Yao Z, Wang L, et al. Activation of ferritinophagy is required for the RNA-binding protein ELAVL1/HuR to regulate ferroptosis in hepatic stellate cells. Autophagy. 2018;14(12):2083–2103.
  • Bailey AP, Koster G, Guillermier C, et al. Antioxidant role for lipid droplets in a stem cell niche of drosophila. Cell. 2015;163(2):340–353.
  • Bai Y, Meng L, Han L, et al. Lipid storage and lipophagy regulates ferroptosis. Biochem Biophys Res Commun. 2019;508(4):997–1003.
  • Yang M, Chen P, Liu J, et al. Clockophagy is a novel selective autophagy process favoring ferroptosis. Sci Adv. 2019;5(7):eaaw2238.
  • Narendra DP, Jin SM, Tanaka A, et al. PINK1 is selectively stabilized on impaired mitochondria to activate parkin. PLOS Biol. 2010;8(1):e1000298.
  • Li C, Zhang Y, Cheng X, et al. PINK1 and PARK2 suppress pancreatic tumorigenesis through control of mitochondrial iron-mediated immunometabolism. Dev Cell. 2018;46(4):441–455. e8.
  • Basit F, Van Oppen LM, Schöckel L, et al. Mitochondrial complex I inhibition triggers a mitophagy-dependent ROS increase leading to necroptosis and ferroptosis in melanoma cells. Cell Death Dis. 2017;8(3):e2716-e–e2716.
  • Chang L-C, Chiang S-K, Chen S-E, et al. Heme oxygenase-1 mediates Bay 11–7085 induced ferroptosis. Cancer Lett. 2018;416:124–137.
  • Gao M, Yi J, Zhu J, et al. Role of mitochondria in ferroptosis. Mol Cell. 2019;73(2):354–363. e3.
  • Dice JF. Chaperone-mediated autophagy. Autophagy. 2007;3(4):295–299.
  • Wu Z, Geng Y, Lu X, et al. Chaperone-mediated autophagy is involved in the execution of ferroptosis. Proc Natl Acad Sci U S A. 2019;116(8):2996–3005.
  • Tang D, Chen X, Kang R, et al. Ferroptosis: molecular mechanisms and health implications. Cell Res. 2021;31(2):107–125.
  • Yu Y, Xie Y, Cao L, et al. The ferroptosis inducer erastin enhances sensitivity of acute myeloid leukemia cells to chemotherapeutic agents. Mol Cell Oncol. 2015;2(4):e1054549.
  • Cao JY, Dixon SJ. Mechanisms of ferroptosis. Cell Mol Life Sci. 2016;73(11-12):2195–2209.
  • Kahlson MA, Dixon SJ. Copper-induced cell death. Science. 2022;375(6586):1231–1232.
  • Li Z, Ferguson L, Deol KK, et al. Ribosome stalling during selenoprotein translation exposes a ferroptosis vulnerability. Nat Chem Biol. 2022;18(7):751–761.
  • Poltorack CD, Dixon SJ. Understanding the role of cysteine in ferroptosis: progress & paradoxes. Febs J. 2022;289(2):374–385.
  • Peng Q, Liu H, Luo Z, et al. Effect of autophagy on ferroptosis in foam cells via Nrf2. Mol Cell Biochem. 2022;477(5):1597–1606.
  • Wang J, Deng B, Liu Q, et al. Pyroptosis and ferroptosis induced by mixed lineage kinase 3 (MLK3) signaling in cardiomyocytes are essential for myocardial fibrosis in response to pressure overload. Cell Death Dis. 2020;11(7):574.
  • Jiang L, Kon N, Li T, et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature. 2015;520(7545):57–62.
  • Tarangelo A, Magtanong L, Bieging-Rolett KT, et al. p53 suppresses metabolic stress-induced ferroptosis in cancer cells. Cell Rep. 2018;22(3):569–575.
  • Gao M, Monian P, Quadri N, et al. Glutaminolysis and transferrin regulate ferroptosis. Mol Cell. 2015;59(2):298–308.
  • Ou Y, Wang S-J, Li D, et al. Activation of SAT1 engages polyamine metabolism with p53-mediated ferroptotic responses. Proc Natl Acad Sci U S A. 2016;113(44):E6806–E6812.
  • Yu H, Guo P, Xie X, et al. Ferroptosis, a new form of cell death, and its relationships with tumourous diseases. J Cell Mol Med. 2017;21(4):648–657.
  • Li W, Luo L-X, Zhou Q-Q, et al. Phospholipid peroxidation inhibits autophagy via stimulating the delipidation of oxidized LC3-PE. Redox Biol. 2022;55:102421.
  • Lee Y-S, Lee D-H, Choudry HA, et al. Ferroptosis-induced endoplasmic reticulum stress: cross-talk between ferroptosis and apoptosis. Mol Cancer Res. 2018;16(7):1073–1076.
  • Sumpter R, Jr, Levine B. Autophagy and innate immunity: triggering, targeting and tuning. Semin Cell Dev Biol. 2010;21(7):699–711. editors Elsevier.
  • Wen Q, Liu J, Kang R, et al. The release and activity of HMGB1 in ferroptosis. Biochem Biophys Res Commun. 2019;510(2):278–283.
  • Xu T, Jiang L, Wang Z. The progression of HMGB1-induced autophagy in cancer biology. Onco Targets Ther. 2019;12:365–377.
  • Lv X, Dong M, Tang W, et al. Ferroptosis, novel therapeutics in asthma. Biomed Pharmacother. 2022;153:113516.
  • Lee HK, Lund JM, Ramanathan B, et al. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science. 2007;315(5817):1398–1401.
  • Tal MC, Sasai M, Lee HK, et al. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci U S A. 2009;106(8):2770–2775.
  • Jounai N, Takeshita F, Kobiyama K, et al. The Atg5–Atg12 conjugate associates with innate antiviral immune responses. Proc Natl Acad Sci U S A. 2007;104(35):14050–14055.
  • Saitoh T, Fujita N, Hayashi T, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci U S A. 2009;106(49):20842–20846.
  • Biswas D, Qureshi OS, Lee W-Y, et al. ATP-induced autophagy is associated with rapid killing of intracellular mycobacteria within human monocytes/macrophages. BMC Immunol. 2008;9(1):35.
  • Scherz-Shouval R, Shvets E, Fass E, et al. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. Embo J. 2007;26(7):1749–1760.
  • Chen X, Xu S, Zhao C, et al. Role of TLR4/NADPH oxidase 4 pathway in promoting cell death through autophagy and ferroptosis during heart failure. Biochem Biophys Res Commun. 2019;516(1):37–43.
  • Jonckheere N, Van Seuningen I. Fine-tuning autophagy in pancreatic adenocarcinoma: full blockage is required. Ann Transl Med. 2019;7(Suppl 1):S43–S43.
  • Akalay I, Janji B, Hasmim M, et al. Epithelial-to-mesenchymal transition and autophagy induction in breast carcinoma promote escape from T-cell–mediated lysis. Cancer Res. 2013;73(8):2418–2427.
  • Viswanathan VS, Ryan MJ, Dhruv HD, et al. Dependency of a therapy-resistant state of cancer cells on a lipid peroxidase pathway. Nature. 2017;547(7664):453–457.
  • Brown CW, Amante JJ, Goel HL, et al. The α6β4 integrin promotes resistance to ferroptosis. J Cell Biol. 2017;216(12):4287–4297.
  • Yang W-H, Huang Z, Wu J, et al. A TAZ–ANGPTL4–NOX2 axis regulates ferroptotic cell death and chemoresistance in epithelial ovarian CancerTAZ promotes ferroptosis in OvCa. Mol Cancer Res. 2020;18(1):79–90.
  • Li J, Liu J, Xu Y, et al. Tumor heterogeneity in autophagy-dependent ferroptosis. Autophagy. 2021;17(11):3361–3374.
  • Sharma P, Hu-Lieskovan S, Wargo JA, et al. Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell. 2017;168(4):707–723.
  • Efimova I, Catanzaro E, Van der Meeren L, et al. Vaccination with early ferroptotic cancer cells induces efficient antitumor immunity. J Immunother Cancer. 2020;8(2):e001369.
  • Tang D, Kepp O, Kroemer G. Ferroptosis becomes immunogenic: implications for anticancer treatments. Oncoimmunology. 2021;10(1):1862949.
  • Galluzzi L, Vitale I, Warren S, et al. Consensus guidelines for the definition, detection and interpretation of immunogenic cell death. J Immunother Cancer. 2020;8(1):e000337.
  • Luo X, Gong H-B, Gao H-Y, et al. Oxygenated phosphatidylethanolamine navigates phagocytosis of ferroptotic cells by interacting with TLR2. Cell Death Differ. 2021;28(6):1971–1989.
  • White E, Lattime EC, Guo JY. Autophagy regulates stress responses, metabolism, and anticancer immunity. Trends Cancer. 2021;7(8):778–789.
  • Abudu YP, Pankiv S, Mathai BJ, et al. NIPSNAP1 and NIPSNAP2 act as “eat me” signals to allow sustained recruitment of autophagy receptors during mitophagy. Autophagy. 2019;15(10):1845–1847.
  • Quezada SA, Peggs KS, Curran MA, et al. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J Clin Invest. 2006;116(7):1935–1945.
  • Alissafi T, Banos A, Boon L, et al. Tregs restrain dendritic cell autophagy to ameliorate autoimmunity. J Clin Invest. 2017;127(7):2789–2804.
  • Bai D, Feng H, Yang J, et al. Genomic analysis uncovers prognostic and immunogenic characteristics of ferroptosis for clear cell renal cell carcinoma. Mol Ther Nucleic Acids. 2021;25:186–197.
  • Liu J, Zhang Z, Zhang W, et al. Ferroptosis mediation patterns reveal novel tool to implicate immunotherapy and multi-omics characteristics in bladder cancer. Front Cell Dev Biol. 2022;10:791630.
  • Kato H, Perl A. Blockade of treg cell differentiation and function by the interleukin-21–mechanistic target of rapamycin axis via suppression of autophagy in patients with systemic lupus erythematosus. Arthritis Rheumatol. 2018;70(3):427–438.
  • Oweida A, Hararah MK, Phan A, et al. Resistance to radiotherapy and PD-L1 blockade is mediated by TIM-3 upregulation and regulatory T-cell infiltration. Clin Cancer Res. 2018;24(21):5368–5380.
  • Mahmutovic Persson I, Menzel M, Ramu S, et al. IL-1β mediates lung neutrophilia and IL-33 expression in a mouse model of viral-induced asthma exacerbation. Respir Res. 2018;19(1):16.
  • Xu C, Sun S, Johnson T, et al. The glutathione peroxidase Gpx4 prevents lipid peroxidation and ferroptosis to sustain Treg cell activation and suppression of antitumor immunity. Cell Rep. 2021;35(11):109235.
  • Li C-W, Lim S-O, Chung EM, et al. Eradication of triple-negative breast cancer cells by targeting glycosylated PD-L1. Cancer Cell. 2018;33(2):187–201. e10.
  • Yao H, Lan J, Li C, et al. Inhibiting PD-L1 palmitoylation enhances T-cell immune responses against tumours. Nat Biomed Eng. 2019;3(4):306–317.
  • Wang H, Yao H, Li C, et al. HIP1R targets PD-L1 to lysosomal degradation to alter T cell–mediated cytotoxicity. Nat Chem Biol. 2019;15(1):42–50.
  • Zhou X, Zou L, Liao H, et al. Abrogation of HnRNP L enhances anti-PD-1 therapy efficacy via diminishing PD-L1 and promoting CD8+ T cell-mediated ferroptosis in castration-resistant prostate cancer. Acta Pharm Sin B. 2022;12(2):692–707.
  • Zhou X, Li Q, He J, et al. HnRNP-L promotes prostate cancer progression by enhancing cell cycling and inhibiting apoptosis. Oncotarget. 2017;8(12):19342–19353.
  • Abusamra AJ, Zhong Z, Zheng X, et al. Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol Dis. 2005;35(2):169–173.
  • Ning Y, Shen K, Wu Q, et al. Tumor exosomes block dendritic cells maturation to decrease the T cell immune response. Immunol Lett. 2018;199:36–43.
  • Zhao X, Yuan C, Wangmo D, et al. Tumor-secreted extracellular vesicles regulate T-cell costimulation and can be manipulated to induce tumor-specific T-cell responses. Gastroenterology. 2021;161(2):560–574. e11.
  • Jaiswal S, Jamieson CH, Pang WW, et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell. 2009;138(2):271–285.
  • Casey SC, Tong L, Li Y, et al. MYC regulates the antitumor immune response through CD47 and PD-L1. Science. 2016;352(6282):227–231.
  • Kamerkar S, LeBleu VS, Sugimoto H, et al. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature. 2017;546(7659):498–503.
  • Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30(1):255–289.
  • Bhattacharya S, Pal K, Sharma AK, et al. GAIP interacting protein C-terminus regulates autophagy and exosome biogenesis of pancreatic cancer through metabolic pathways. PLOS One. 2014;9(12):e114409.
  • Guo H, Chitiprolu M, Roncevic L, et al. Atg5 disassociates the V1V0-ATPase to promote exosome production and tumor metastasis independent of canonical macroautophagy. Dev Cell. 2017;43(6):716–730. e7.
  • Xie L, Li J, Wang G, et al. Phototheranostic metal-phenolic networks with antiexosomal PD-L1 enhanced ferroptosis for synergistic immunotherapy. J Am Chem Soc. 2022;144(2):787–797.
  • Xiong A, Duan L, Chen J, et al. Flt3L combined with rapamycin promotes cardiac allograft tolerance by inducing regulatory dendritic cells and allograft autophagy in mice. 2012;7(10):e46230.
  • Zhu Y, Knolhoff BL, Meyer MA, et al. CSF1/CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer ModelsCSF1R blockade improves checkpoint immunotherapy. Cancer Res. 2014;74(18):5057–5069.
  • 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):2069–2083.
  • Jiang Z, Lim S-O, Yan M, et al. TYRO3 induces anti–PD-1/PD-L1 therapy resistance by limiting innate immunity and tumoral ferroptosis. J Clin Invest. 2021;131(8):e139434.
  • Sena LA, Li S, Jairaman A, et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity. 2013;38(2):225–236.
  • Wang Y, Tian Q, Hao Y, et al. The kinase complex mTORC2 promotes the longevity of virus-specific memory CD4+ T cells by preventing ferroptosis. Nat Immunol. 2022;23(2):303–317.
  • Xia H, Wang W, Crespo J, et al. Suppression of FIP200 and autophagy by tumor-derived lactate promotes naive T cell apoptosis and affects tumor immunity. Sci Immunol. 2017;2(17):eaan4631.
  • Hubbard VM, Valdor R, Patel B, et al. Macroautophagy regulates energy metabolism during effector T cell activation. J Immunol. 2010;185(12):7349–7357.
  • Botbol Y, Patel B, Macian F. Common γ-chain cytokine signaling is required for macroautophagy induction during CD4+ T-cell activation. Autophagy. 2015;11(10):1864–1877.
  • Garg SK, Yan Z, Vitvitsky V, et al. Differential dependence on cysteine from transsulfuration versus transport during T cell activation. Antioxid Redox Signal. 2011;15(1):39–47.
  • Levring TB, Hansen AK, Nielsen BL, et al. Activated human CD4+ T cells express transporters for both cysteine and cystine. Sci Rep. 2012;2(1):266.
  • Michalek RD, Gerriets VA, Jacobs SR, et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol. 2011;186(6):3299–3303.
  • Pua HH, Guo J, Komatsu M, et al. Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J Immunol. 2009;182(7):4046–4055.
  • Singh R, Kaushik S, Wang Y, et al. Autophagy regulates lipid metabolism. Nature. 2009;458(7242):1131–1135.
  • Xu X, Araki K, Li S, et al. Autophagy is essential for effector CD8+ T cell survival and memory formation. Nat Immunol. 2014;15(12):1152–1161.
  • Carleton G, Lum JJ. Autophagy metabolically suppresses CD8+ T cell antitumor immunity. Autophagy. 2019;15(9):1648–1649.
  • Wang W, Green M, Choi JE, et al. CD8+ T cells regulate tumour ferroptosis during cancer immunotherapy. Nature. 2019;569(7755):270–274.
  • Miller BC, Zhao Z, Stephenson LM, et al. The autophagy gene ATG5 plays an essential role in B lymphocyte development. Autophagy. 2008;4(3):309–314.
  • Muri J, Thut H, Bornkamm GW, et al. 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.
  • Pengo N, Scolari M, Oliva L, et al. Plasma cells require autophagy for sustainable immunoglobulin production. Nat Immunol. 2013;14(3):298–305.
  • Yao Y, Chen Z, Zhang H, et al. Selenium–GPX4 axis protects follicular helper T cells from ferroptosis. Nat Immunol. 2021;22(9):1127–1139.
  • Zhang Y, Morgan MJ, Chen K, et al. Induction of autophagy is essential for monocyte-macrophage differentiation. Blood, JAm Soc Hemato. 2012;119(12):2895–2905.
  • Handa P, Thomas S, Morgan-Stevenson V, et al. Iron alters macrophage polarization status and leads to steatohepatitis and fibrogenesis. J Leukoc Biol. 2019;105(5):1015–1026.
  • Zhou Y, Que KT, Zhang Z, et al. Iron overloaded polarizes macrophage to proinflammation phenotype through ROS/acetyl-p53 pathway. Cancer Med. 2018;7(8):4012–4022.
  • Chen W, Ma T, Shen X-N, et al. Macrophage-induced tumor angiogenesis is regulated by the TSC2–mTOR pathwaytsc2–mTOR regulates macrophage-induced tumor angiogenesis. Cancer Res. 2012;72(6):1363–1372.
  • Chang C-P, Su Y-C, Lee P-H, et al. Targeting NFKB by autophagy to polarize hepatoma-associated macrophage differentiation. Autophagy. 2013;9(4):619–621.
  • Chang C, Su Y, Hu C, et al. TLR2-dependent selective autophagy regulates NF-κB lysosomal degradation in hepatoma-derived M2 macrophage differentiation. Cell Death Differ. 2013;20(3):515–523.
  • Roca H, Varsos ZS, Sud S, et al. CCL2 and interleukin-6 promote survival of human CD11b + peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem. 2009;284(49):34342–34354.
  • Jiang G-M, Tan Y, Wang H, et al. The relationship between autophagy and the immune system and its applications for tumor immunotherapy. Mol Cancer. 2019;18(1):17.
  • Folgiero V, Miele E, Carai A, et al. IDO1 involvement in mTOR pathway: a molecular mechanism of resistance to mTOR targeting in medulloblastoma. Oncotarget. 2016;7(33):52900–52911.