Protein biosynthesis, a target of sorafenib, interferes with the unfolded protein response (UPR) and ferroptosis in hepatocellular carcinoma cells

Oncotarget

Volumn 9, Issue 9, 2018, Pages 8400-8414

  Sauzay, Chloé ^a,b   Louandre, Christophe ^a   Bodeau, Sandra ^a   Anglade, Frédéric ^a   Godin, Corinne ^a,b   Saidak, Zuzana ^a   Fontaine, Jean Xavier ^c   Usureau, Cédric ^a   Martin, Nathalie ^d   Molinie, Roland ^c   Pascal, Julie ^c   Mesnard, François ^c   Pluquet, Olivier ^d   Galmiche, Antoine ^a,b  

^a AMIENS UNIVERSITY HOSPITAL   (France)

^b Unité de Traitement de l'image Médicale   (France)

^c Université de Picardie Jules Verne   (France)

^d UNIV LILLE   (France)

Author keywords

Ferroptosis; Hepatocellular carcinoma; Sorafenib; Translation; Unfolded protein response (UPR)

Indexed keywords

ALPHA FETOPROTEIN; AMINO ACID DERIVATIVE; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; SORAFENIB; TRAMETINIB; TUNICAMYCIN;

AMINO ACID TRANSPORT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CARCINOMA CELL; CELL DEATH; CELL MEMBRANE TRANSPORT; CELL PROTECTION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; DRUG TARGETING; FERROPTOSIS; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MTOR SIGNALING; OXIDATIVE STRESS; PROTEIN HOMEOSTASIS; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; PROTEIN SYNTHESIS REGULATION; TRANSLATION INITIATION; TRANSLATION REGULATION; UNFOLDED PROTEIN RESPONSE;

EID: 85041463791     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.23843     Document Type: Article

References (50)

1. Villanueva A, Hernandez-Gea V, Llovet JM. Medical therapies for hepatocellular carcinoma: a critical view of the evidence. Nat Rev Gastroenterol Hepatol. 2013; 10:34-42. https://doi.org/10.1038/nrgastro.2012.199..
2. Davis MI, Hunt JP, Herrgard S, Ciceri P, Wodicka LM, Pallares G, Hocker M, Treiber DK, Zarrinkar PP. Comprehensive analysis of kinase inhibitor selectivity. Nat Biotechnol. 2011; 29:1046-51. https://doi.org/10.1038/nbt.1990..
3. Llovet JM, Hernandez-Gea V. Hepatocellular carcinoma: reasons for phase III failure and novel perspectives on trial design. Clin Cancer Res. 2014; 20:2072-9. https://doi.org/10.1158/1078-0432.CCR-13-0547..
4. Galmiche A, Chauffert B, Barbare JC. New biological perspectives for the improvement of the efficacy of sorafenib in hepatocellular carcinoma. Cancer Lett. 2014; 346:159-62. https://doi.org/10.1016/j.canlet.2013.12.028..
5. Labbadia J, Morimoto RI. The biology of proteostasis in aging and disease. Annu Rev Biochem. 2015; 84:435-64. https://doi.org/10.1146/annurev-biochem-060614-033955..
6. Shimizu S, Takehara T, Hikita H, Kodama T, Tsunematsu H, Miyagi T, Hosui A, Ishida H, Tatsumi T, Kanto T, Hiramatsu N, Fujita N, Yoshimori T, et al. Inhibition of autophagy potentiates the antitumor effect of the multikinase inhibitor sorafenib in hepatocellular carcinoma. Int J Cancer. 2012; 131:548-57. https://doi.org/10.1002/ijc.26374..
7. Shi YH, Ding ZB, Zhou J, Hui B, Shi GM, Ke AW, Wang XY, Dai Z, Peng YF, Gu CY, Qiu SJ, Fan J. Targeting autophagy enhances sorafenib lethality for hepatocellular carcinoma via ER stress-related apoptosis. Autophagy. 2011; 7:1159-72. https://doi.org/10.4161/auto.7.10.16818..
8. Honma Y, Harada M. Sorafenib enhances proteasome inhibitor-mediated cytotoxicity via inhibition of unfolded protein response and keratin phosphorylation. Exp Cell Res. 2013; 319:2166-78. https://doi.org/10.1016/j.yexcr.2013.05.023..
9. Dixon SJ, Patel DN, Welsch M, Skouta R, Lee ED, Hayano M, Thomas AG, Gleason CE, Tatonetti NP, Slusher BS, Stockwell BR. Pharmacological inhibition of cystine-glutamate exchange induces endoplasmic reticulum stress and ferroptosis. eLife. 2014; 3:e02523. https://doi.org/10.7554/eLife.02523..
10. Booth L, Shuch B, Albers T, Roberts JL, Tavallai M, Proniuk S, Zukiwski A, Wang D, Chen CS, Bottaro D, Ecroyd H, Lebedyeva IO, Dent P. Multi-kinase inhibitors can associate with heat shock proteins through their NH2-termini by which they suppress chaperone function. Oncotarget. 2016; 7:12975-96. https://doi.org/10.18632/oncotarget.7349..
11. Adjibade P, St-Sauveur VG, Quevillon Huberdeau M, Fournier MJ, Savard A, Coudert L, Khandjian EW, Mazroui R. Sorafenib, a multikinase inhibitor, induces formation of stress granules in hepatocarcinoma cells. Oncotarget. 2015; 6:43927-43. https://doi.org/10.18632/oncotarget.5980..
12. Buszczak M, Signer RA, Morrison SJ. Cellular differences in protein synthesis regulate tissue homeostasis. Cell. 2014; 159:242-51. https://doi.org/10.1016/j.cell.2014.09.016..
13. Truitt ML, Ruggero D. New frontiers in translational control of the cancer genome. Nat Rev Cancer. 2016; 16:288-304. https://doi.org/10.1038/nrc.2016.27..
14. Boussemart L, Malka-Mahieu H, Girault I, Allard D, Hemmingsson O, Tomasic G, Thomas M, Basmadjian C, Ribeiro N, Thuaud F, Mateus C, Routier E, Kamsu-Kom N, et al. eIF4F is a nexus of resistance to anti-BRAF and anti-MEK cancer therapies. Nature. 2014; 513:105-9. https://doi.org/10.1038/nature13572..
15. Bruno PM, Liu Y, Park GY, Murai J, Koch CE, Eisen TJ, Pritchard JR, Pommier Y, Lippard SJ, Hemann MT. A subset of platinum-containing chemotherapeutic agents kills cells by inducing ribosome biogenesis stress. Nat Med. 2017; 23: 461-471. https://doi.org/10.1038/nm.4291..
16. Li J, Shi L, Zhang X, Sun B, Yang Y, Ge N, Liu H, Yang X, Chen L, Qian H, Wu M, Yin Z. pERK/pAkt phenotyping in circulating tumor cells as a biomarker for sorafenib efficacy in patients with advanced hepatocellular carcinoma. Oncotarget. 2016; 7:2646-59. https://doi.org/10.18632/oncotarget.6104..
17. Hetz C, Chevet E, Oakes SA. Proteostasis control by the unfolded protein response. Nat Cell Biol. 2015; 17:829-38. https://doi.org/10.1038/ncb3184..
18. Wang M, Kaufman RJ. Protein misfolding in the endoplasmic reticulum as a conduit to human disease. Nature. 2016; 529:326-35. https://doi.org/10.1038/nature17041..
19. Yi P, Higa A, Taouji S, Bexiga MG, Marza E, Arma D, Castain C, Le Bail B, Simpson JC, Rosenbaum J, Balabaud C, Bioulac-Sage P, Blanc JF, et al. Sorafenib-mediated targeting of the AAA+ ATPase p97/VCP leads to disruption of the secretory pathway, endoplasmic reticulum stress, and hepatocellular cancer cell death. Mol Cancer Ther. 2012; 11:2610-20. https://doi.org/10.1158/1535-7163.MCT-12-0516..
20. Houessinon A, Gicquel A, Bochereau F, Louandre C, Nyga R, Godin C, Degonville J, Fournier E, Saidak Z, Drullion C, Barbare JC, Chauffert B, François C, et al. Alpha-fetoprotein is a biomarker of unfolded protein response and altered proteostasis in hepatocellular carcinoma cells exposed to sorafenib. Cancer Lett. 2016; 370:242-9. https://doi.org/10.1016/j.canlet.2015.10.032..
21. Urra H, Dufey E, Avril T, Chevet E, Hetz C. Endoplasmic Reticulum Stress and the Hallmarks of Cancer. Trends Cancer. 2016; 2:252-62.
22. Galmiche A, Sauzay C, Chevet E, Pluquet O. Role of the unfolded protein response in tumor cell characteristics and cancer outcome. Curr Opin Oncol. 2017; 29:41-7. https://doi.org/10.1097/CCO.0000000000000339..
23. Yu X, Long YC. Crosstalk between cystine and glutathione is critical for the regulation of amino acid signaling pathways and ferroptosis. Sci Rep. 2016; 6:30033. https://doi.org/10.1038/srep30033..
24. Louandre C, Ezzoukhry Z, Godin C, Barbare JC, Mazière JC, Chauffert B, Galmiche A. Iron-dependent cell death of hepatocellular carcinoma cells exposed to sorafenib. Int J Cancer. 2013; 133:1732-42. https://doi.org/10.1002/ijc.28159..
25. Lachaier E, Louandre C, Godin C, Saidak Z, Baert M, Diouf M, Chauffert B, Galmiche A. Sorafenib induces ferroptosis in human cancer cell lines originating from different solid tumors. Anticancer Res. 2014; 34:6417-22.
26. Houessinon A, François C, Sauzay C, Louandre C, Mongelard G, Godin C, Bodeau S, Takahashi S, Saidak Z, Gutierrez L, Régimbeau JM, Barget N, Barbare JC, et al. Metallothionein-1 as a biomarker of altered redox metabolism in hepatocellular carcinoma cells exposed to sorafenib. Mol Cancer. 2016; 15:38. https://doi.org/10.1186/s12943-016-0526-2..
27. Cao JY, Dixon SJ. Mechanisms of ferroptosis. Cell Mol Life Sci. 2016; 73:2195-209. https://doi.org/10.1007/s00018-016-2194-1..
28. Gaschler MM, Stockwell BR. Lipid peroxidation in cell death. Biochem Biophys Res Commun. 2017; 482:419-25. https://doi.org/10.1016/j.bbrc.2016.10.086..
29. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, Morrison B, Stockwell BR. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012; 149:1060-72. https://doi.org/10.1016/j.cell.2012.03.042..
30. Sauzay C, Petit A, Bourgeois AM, Barbare JC, Chauffert B, Galmiche A, Houessinon A. Alpha-foetoprotein (AFP): A multi-purpose marker in hepatocellular carcinoma. Clin Chim Acta. 2016; 463:39-44. https://doi.org/10.1016/j.cca.2016.10.006..
31. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, Antipin Y, Reva B, Goldberg AP, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012; 2:401-4. https://doi.org/10.1158/2159-8290.CD-12-0095..
32. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, Cerami E, Sander C, Schultz N. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013; 6:pl1. https://doi.org/10.1126/scisignal.2004088..
33. Ezzoukhry Z, Louandre C, Trécherel E, Godin C, Chauffert B, Dupont S, Diouf M, Barbare JC, Mazière JC, Galmiche A. EGFR activation is a potential determinant of primary resistance of hepatocellular carcinoma cells to sorafenib. Int J Cancer. 2012; 131:2961-9. https://doi.org/10.1002/ijc.27604..
34. Schmidt EK, Clavarino G, Ceppi M, Pierre P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods. 2009; 6:275-7. https://doi.org/10.1038/nmeth.1314..
35. Abou-Alfa GK, Schwartz L, Ricci S, Amadori D, Santoro A, Figer A, De Greve J, Douillard JY, Lathia C, Schwartz B, Taylor I, Moscovici M, Saltz LB. Phase II Study of Sorafenib in Patients With Advanced Hepatocellular Carcinoma. J Clin Oncol. 2006; 24:4293-300. https://doi.org/10.1200/JCO.2005.01.3441..
36. Cross BC, Bond PJ, Sadowski PG, Jha BK, Zak J, Goodman JM, Silverman RH, Neubert TA, Baxendale IR, Ron D, Harding HP. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule. Proc Natl Acad Sci U S A. 2012; 109:E869-878. https://doi.org/10.1073/pnas.1115623109..
37. Axten JM, Medina JR, Feng Y, Shu A, Romeril SP, Grant SW, Li WHH, Heerding DA, Minthorn E, Mencken T, Atkins C, Liu Q, Rabindran S, et al. Discovery of 7-methyl-5-(1-[[3-(trifluoromethyl)phenyl]acetyl]-2,3-dihydro-1H-indol-5-yl)-7H-pyrrolo[2,3-d]pyrimidin-4-amine (GSK2606414), a potent and selective first-in-class inhibitor of protein kinase R (PKR)-like endoplasmic reticulum kinase (PERK). J Med Chem. 2012; 55:7193-207. https://doi.org/10.1021/jm300713s..
38. Foucquier J, Guedj M. Analysis of drug combinations: current methodological landscape. Pharmacol Res Perspect. 2015; 3:e00149. https://doi.org/10.1002/prp2.149..
39. Saxton RA, Sabatini DM. mTOR Signaling in Growth, Metabolism, and Disease. Cell. 2017; 168:960-76. https://doi.org/10.1016/j.cell.2017.02.004..
40. Ilagan E, Manning BD. Emerging role of mTOR in the response to cancer therapeutics. Trends Cancer. 2016; 2:241-51. https://doi.org/10.1016/j.trecan.2016.03.008..
41. Vandewynckel YP, Laukens D, Bogaerts E, Paridaens A, Van den Bussche A, Verhelst X, Van Steenkiste C, Descamps B, Vanhove C, Libbrecht L, De Rycke R, Lambrecht BN, Geerts A, et al. Modulation of the unfolded protein response impedes tumor cell adaptation to proteotoxic stress: a PERK for hepatocellular carcinoma therapy. Hepatol Int. 2015; 9:93-104. https://doi.org/10.1007/s12072-014-9582-0..
42. Yamasaki S, Anderson P. Reprogramming mRNA translation during stress. Curr Opin Cell Biol. 2008; 20:222-6. https://doi.org/10.1016/j.ceb.2008.01.013..
43. Robichaud N, Sonenberg N. Translational control and the cancer cell response to stress. Curr Opin Cell Biol. 2017; 45:102-9. https://doi.org/10.1016/j.ceb.2017.05.007..
44. Senft D, Ronai ZE. Adaptive Stress Responses During Tumor Metastasis and Dormancy. Trends Cancer. 2016; 2:429-42. https://doi.org/10.1016/j.trecan.2016.06.004..
45. Leprivier G, Remke M, Rotblat B, Dubuc A, Mateo AR, Kool M, Agnihotri S, El-Naggar A, Yu B, Somasekharan SP, Faubert B, Bridon G, Tognon CE, et al. The eEF2 kinase confers resistance to nutrient deprivation by blocking translation elongation. Cell. 2013; 153:1064-79. https://doi.org/10.1016/j.cell.2013.04.055..
46. 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; 23:270-8. https://doi.org/10.1038/cdd.2015.93..
47. Sun SY, Rosenberg LM, Wang X, Zhou Z, Yue P, Fu H, Khuri FR. Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res. 2005; 65:7052-8. https://doi.org/10.1158/0008-5472.CAN-05-0917..
48. Tsukumo Y, Alain T, Fonseca BD, Nadon R, Sonenberg N. Translation control during prolonged mTORC1 inhibition mediated by 4E-BP3. Nat Commun. 2016; 7:11776. https://doi.org/10.1038/ncomms11776..
49. Galmiche A, Ezzoukhry Z, François C, Louandre C, Sabbagh C, Nguyen-Khac E, Descamps V, Trouillet N, Godin C, Regimbeau JM, Joly JP, Barbare JC, Duverlie G, et al. BAD, a proapoptotic member of the BCL2 family, is a potential therapeutic target in hepatocellular carcinoma. Mol Cancer Res. 2010; 8:1116-25. https://doi.org/10.1158/1541-7786.MCR-10-0029..
50. Morita M, Gravel SP, Chénard V, Sikström K, Zheng L, Alain T, Gandin V, Avizonis D, Arguello M, Zakaria C, McLaughlan S, Nouet Y, Pause A, et al. mTORC1 Controls Mitochondrial Activity and Biogenesis through 4E-BP-Dependent Translational Regulation. Cell Metab. 2013; 18:698-711. https://doi.org/10.1016/j.cmet.2013.10.001..