Metallothionein-1G facilitates sorafenib resistance through inhibition of ferroptosis

Hepatology

Volumn 64, Issue 2, 2016, Pages 488-500

  Sun, Xiaofang ^a   Niu, Xiaohua ^a   Chen, Ruochan ^b   He, Wenyin ^a   Chen, De ^a   Kang, Rui ^b   Tang, Daolin ^a,b  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERLOTINIB; GEFITINIB; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMATINIB; MASITINIB; MESSENGER RNA; METALLOPROTEIN; METALLOTHIONEIN 1G; PONATINIB; PROPARGYLGLYCINE; RETINOIC ACID; SELUMETINIB; SORAFENIB; TIVANTINIB; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; VEMURAFENIB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL DEATH; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TREATMENT DURATION; TUMOR XENOGRAFT;

EID: 84978997718     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.28574     Document Type: Article

References (46)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin 2016;66:7-30.
2. El-Serag HB. Hepatocellular carcinoma. N Engl J Med 2011;365:1118-1127.
3. Siegel AB, Olsen SK, Magun A, Brown RS Jr. Sorafenib: where do we go from here? Hepatology 2010;52:360-369.
4. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008;359:378-390.
5. Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 2009;10:25-34.
6. Coyle P, Philcox JC, Carey LC, Rofe AM. Metallothionein: the multipurpose protein. Cell Mol Life Sci 2002;59:627-647.
7. Chun JH, Kim HK, Kim E, Kim IH, Kim JH, Chang HJ, et al. Increased expression of metallothionein is associated with irinotecan resistance in gastric cancer. Cancer Res 2004;64:4703-4706.
8. Gumulec J, Raudenska M, Adam V, Kizek R, Masarik M. Metallothionein—immunohistochemical cancer biomarker: a meta-analysis. PloS One 2014;9:e85346.
9. Eckschlager T, Adam V, Hrabeta J, Figova K, Kizek R. Metallothioneins and cancer. Curr Protein Pept Sci 2009;10:360-375.
10. Yang WS, Stockwell BR. Ferroptosis: death by lipid peroxidation. Trends Cell Biol 2016;26:165-176.
11. Xie Y, Hou W, Song X, Yu Y, Huang J, Sun X, et al. Ferroptosis: process and function. Cell Death Differ 2016;23:369-379.
12. Yan W, Chang Y, Liang X, Cardinal JS, Huang H, Thorne SH, et al. High-mobility group box 1 activates caspase-1 and promotes hepatocellular carcinoma invasiveness and metastases. Hepatology 2012;55:1863-1875.
13. Berry MN, Friend DS. High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study. J Cell Biol 1969;43:506-520.
14. Lecluyse EL, Alexandre E. Isolation and culture of primary hepatocytes from resected human liver tissue. Methods Mol Biol 2010;640:57-82.
15. Wang P, Yu J, Zhang L. The nuclear function of p53 is required for PUMA-mediated apoptosis induced by DNA damage. Proc Natl Acad Sci USA 2007;104:4054-4059.
16. Tang D, Kang R, Livesey KM, Kroemer G, Billiar TR, Van Houten B, et al. High-mobility group box 1 is essential for mitochondrial quality control. Cell Metab 2011;13:701-711.
17. Yang L, Xie M, Yang M, Yu Y, Zhu S, Hou W, et al. PKM2 regulates the Warburg effect and promotes HMGB1 release in sepsis. Nat Commun 2014;5:4436.
18. Wei JC, Meng FD, Qu K, Wang ZX, Wu QF, Zhang LQ, et al. Sorafenib inhibits proliferation and invasion of human hepatocellular carcinoma cells via up-regulation of p53 and suppressing FoxM1. Acta Pharmacol Sin 2015;36:241-251.
19. Liang Y, Zheng T, Song R, Wang J, Yin D, Wang L, et al. Hypoxia-mediated sorafenib resistance can be overcome by EF24 through Von Hippel-Lindau tumor suppressor-dependent HIF-1alpha inhibition in hepatocellular carcinoma. Hepatology 2013;57:1847-1857.
20. Sun X, Ou Z, Chen R, Niu X, Chen D, Kang R, et al. Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology 2016;63:173-184.
21. Wang XJ, Hayes JD, Henderson CJ, Wolf CR. Identification of retinoic acid as an inhibitor of transcription factor Nrf2 through activation of retinoic acid receptor alpha. Proc Natl Acad Sci USA 2007;104:19589-19594.
22. Arlt A, Sebens S, Krebs S, Geismann C, Grossmann M, Kruse ML, et al. Inhibition of the Nrf2 transcription factor by the alkaloid trigonelline renders pancreatic cancer cells more susceptible to apoptosis through decreased proteasomal gene expression and proteasome activity. Oncogene 2013;32:4825-4835.
23. Ren D, Villeneuve NF, Jiang T, Wu T, Lau A, Toppin HA, et al. Brusatol enhances the efficacy of chemotherapy by inhibiting the Nrf2-mediated defense mechanism. Proc Natl Acad Sci USA 2011;108:1433-1438.
24. Lertratanangkoon K, Scimeca JM, Wei JN. Inhibition of glutathione synthesis with propargylglycine enhances N-acetylmethionine protection and methylation in bromobenzene-treated Syrian hamsters. J Nutr 1999;129:649-656.
25. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 2012;149:1060-1072.
26. Friedmann Angeli JP, Schneider M, Proneth B, Tyurina YY, Tyurin VA, Hammond VJ, et al. Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat Cell Biol 2014;16:1180-1191.
27. Dixon SJ, Stockwell BR. The role of iron and reactive oxygen species in cell death. Nat Chem Biol 2014;10:9-17.
28. Yang WS, SriRamaratnam R, Welsch ME, Shimada K, Skouta R, Viswanathan VS, et al. Regulation of ferroptotic cancer cell death by GPX4. Cell 2014;156:317-331.
29. Kanda M, Nomoto S, Okamura Y, Nishikawa Y, Sugimoto H, Kanazumi N, et al. Detection of metallothionein 1G as a methylated tumor suppressor gene in human hepatocellular carcinoma using a novel method of double combination array analysis. Int J Oncol 2009;35:477-483.
30. Datta J, Majumder S, Kutay H, Motiwala T, Frankel W, Costa R, et al. Metallothionein expression is suppressed in primary human hepatocellular carcinomas and is mediated through inactivation of CCAAT/enhancer binding protein alpha by phosphatidylinositol 3-kinase signaling cascade. Cancer Res 2007;67:2736-2746.
31. Majumder S, Roy S, Kaffenberger T, Wang B, Costinean S, Frankel W, et al. Loss of metallothionein predisposes mice to diethylnitrosamine-induced hepatocarcinogenesis by activating NF-kappaB target genes. Cancer Res 2010;70:10265-10276.
32. Bahnson RR, Basu A, Lazo JS. The role of metallothioneins in anticancer drug resistance. Cancer Treat Res 1991;57:251-260.
33. Ma Q. Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 2013;53:401-426.
34. Suzuki T, Motohashi H, Yamamoto M. Toward clinical application of the Keap1-Nrf2 pathway. Trends Pharmacol Sci 2013;34:340-346.
35. Linkermann A, Skouta R, Himmerkus N, Mulay SR, Dewitz C, De Zen F, et al. Synchronized renal tubular cell death involves ferroptosis. Proc Natl Acad Sci USA 2014;111:16836-16841.
36. 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;212:555-568.
37. Gascon S, Murenu E, Masserdotti G, Ortega F, Russo GL, Petrik D, et al. Identification and successful negotiation of a metabolic checkpoint in direct neuronal reprogramming. Cell Stem Cell 2016;18:396-409.
38. Louandre C, Ezzoukhry Z, Godin C, Barbare JC, Maziere JC, Chauffert B, et al. Iron-dependent cell death of hepatocellular carcinoma cells exposed to sorafenib. Int J Cancer 2013;133:1732-1742.
39. Galmiche A, Chauffert B, Barbare JC. New biological perspectives for the improvement of the efficacy of sorafenib in hepatocellular carcinoma. Cancer Lett 2014;346:159-162.
40. Lachaier E, Louandre C, Godin C, Saidak Z, Baert M, Diouf M, et al. Sorafenib induces ferroptosis in human cancer cell lines originating from different solid tumors. Anticancer Res 2014;34:6417-6422.
41. Dixon SJ, Patel DN, Welsch M, Skouta R, Lee ED, Hayano M, et al. Pharmacological inhibition of cystine-glutamate exchange induces endoplasmic reticulum stress and ferroptosis. eLife 2014;3:e02523.
42. Sun X, Ou Z, Xie M, Kang R, Fan Y, Niu X, et al. HSPB1 as a novel regulator of ferroptotic cancer cell death. Oncogene 2015;34:5617-5625.
43. Jiang L, Kon N, Li T, Wang SJ, Su T, Hibshoosh H, et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature 2015;520:57-62.
44. Hayano M, Yang WS, Corn CK, Pagano NC, Stockwell BR. Loss of cysteinyl-tRNA synthetase (CARS) induces the transsulfuration pathway and inhibits ferroptosis induced by cystine deprivation. Cell Death Differ 2016;23:270-278.
45. Ruttkay-Nedecky B, Nejdl L, Gumulec J, Zitka O, Masarik M, Eckschlager T, et al. The role of metallothionein in oxidative stress. Int J Mol Sci 2013;14:6044-6066.
46. Conrad M, Angeli JP, Vandenabeele P, Stockwell BR. Regulated necrosis: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 2016; doi: 10.1038/nrd.2015.6.