EIF2 kinases mediate β-lapachone toxicity in yeast and human cancer cells

Cell Cycle

Volumn 14, Issue 4, 2015, Pages 630-640

  Menacho Márquez, Mauricio ^a   Rodríguez Hernández, Carlos J ^b   Villarong, M Ángeles ^c   Pérez Valle, Jorge ^d   Gadea, José ^e   Belandia, Borja ^f   Murguía, José R ^g  

^a FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

^b HOSPITAL SANT JOAN DE DÉU   (Spain)

^c DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^d INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^e Ciudad Politécnica de la Innovación   (Spain)

^f INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^g UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

Author keywords

Antitumoral drug; DNA damage; Integrated stress response; Reactive oxygen species

Indexed keywords

ANTIFUNGAL AGENT; ANTINEOPLASTIC AGENT; BETA LAPACHONE; COMPLEMENTARY DNA; DICOUMAROL; PROTEIN KINASE R; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; BETA-LAPACHONE; GCN2 PROTEIN, S CEREVISIAE; NAPHTHOQUINONE; NQO1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SACCHAROMYCES CEREVISIAE PROTEIN; SMALL INTERFERING RNA; TETRAZOLIUM; THIAZOLE DERIVATIVE; THIAZOLYL BLUE; TRANSCRIPTOME;

AMINO ACID SYNTHESIS; ANIMAL CELL; ANTIFUNGAL ACTIVITY; ARTICLE; BIOSYNTHESIS; CANCER CELL; CELL SURVIVAL; COMPETITIVE INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA MICROARRAY; DRUG EXPOSURE; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN CELL; MCF 7 CELL LINE; MOUSE; NONHUMAN; OPEN READING FRAME; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; TRANSLATION INITIATION; WESTERN BLOTTING; YEAST; YEAST CELL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYME ACTIVATION; GENETICS; IMMUNOBLOTTING; METABOLISM; SACCHAROMYCETALES;

SACCHAROMYCETALES;

ANTINEOPLASTIC AGENTS; DICUMAROL; EIF-2 KINASE; ENZYME ACTIVATION; HUMANS; IMMUNOBLOTTING; NAD(P)H DEHYDROGENASE (QUINONE); NAPHTHOQUINONES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES; TETRAZOLIUM SALTS; THIAZOLES; TRANSCRIPTOME;

EID: 84923599041     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/15384101.2014.994904     Document Type: Article

References (44)

1. Rajendran JG, Mankoff DA, O'Sullivan F, Peterson LM, Schwartz DL, Conrad EU, Spence AM, Muzi M, Farwell DG, Krohn KA. Hypoxia and glucose metabolism in malignant tumors: evaluation by [18F]fluoromisonidazole and [18F]fluorodeoxyglucose positron emission tomography imaging. Clin Cancer Res 2004; 10:2245-52; PMID:15073099
2. Sivridis E, Giatromanolaki A, Koukourakis MI. The vascular network of tumours-what is it not for? J Pathol 2003; 201:173-80; PMID:14517833; http://dx.doi. org/10.1002/path.1355
3. Brown JM, Wilson WR. Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer 2004; 4:437-47; PMID:15170446; http://dx.doi.org/10.1038/nrc1367
4. Evans SM, Judy KD, Dunphy I, Jenkins WT, Hwang WT, Nelson PT, Lustig RA, Jenkins K, Magarelli DP, Hahn SM, et al. Hypoxia is important in the biology and aggression of human glial brain tumors. Clin Cancer Res 2004; 10:8177-84; PMID:15623592; http:// dx.doi.org/10.1158/1078-0432.CCR-04-1081
5. Nordsmark M, Bentzen SM, Rudat V, Brizel D, Lartigau E, Stadler P, Becker A, Adam M, Molls M, Dunst J, et al. Prognostic value of tumor oxygenation in 397 head and neck tumors after primary radiation therapy. An international multi-center study. Radiother Oncol 2005; 77:18-24; PMID:16098619; http://dx.doi.org/ 10.1016/j.radonc.2005.06.038
6. Sonenberg N, Hinnebusch AG. New modes of translational control in development, behavior, and disease. Mol Cell 2007; 28:721-9; PMID:18082597; http://dx. doi.org/10.1016/j.molcel.2007.11.018
7. Hinnebusch AG. Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 2005; 59:407-50; PMID:16153175
8. Hinnebusch AG. Translational regulation of yeast GCN4. A window on factors that control initiator-trna binding to the ribosome. J Biol Chem 1997; 272:21661-4; PMID:9268289; http://dx.doi.org/ 10.1074/jbc.272.35.21661
9. Rolfes RJ, Hinnebusch AG. Translation of the yeast transcriptional activator GCN4 is stimulated by purine limitation: implications for activation of the protein kinase GCN2. Mol Cell Biol 1993; 13:5099-111; PMID:8336737
10. Yang R, Wek SA, Wek RC. Glucose limitation induces GCN4 translation by activation of Gcn2 protein kinase. Mol Cell Biol 2000; 20:2706-17; PMID:10733573; http://dx.doi.org/10.1128/ MCB.20.8.2706-2717.2000
11. Goossens A, Dever TE, Pascual-Ahuir A, Serrano R. The protein kinase Gcn2p mediates sodium toxicity in yeast. J Biol Chem 2001; 276:30753-60; PMID:11408481; http://dx.doi.org/10.1074/jbc. M102960200
12. Valenzuela L, Aranda C, Gonzalez A. TOR modulates GCN4-dependent expression of genes turned on by nitrogen limitation. J Bacteriol 2001; 183:2331-4; PMID:11244074; http://dx.doi.org/10.1128/ JB.183.7.2331-2334.2001
13. Palmer LK, Shoemaker JL, Baptiste BA, Wolfe D, Keil RL. Inhibition of translation initiation by volatile anesthetics involves nutrient-sensitive GCN-independent and -dependent processes in yeast. Mol Biol Cell 2005; 16:3727-39; PMID:15930127; http://dx.doi.org/ 10.1091/mbc.E05-02-0127
14. Wek RC, Jiang HY, Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 2006; 34:7-11; PMID:16246168
15. Menacho-Marquez M, Perez-Valle J, Arino J, Gadea J, Murguia JR. Gcn2p regulates a G1/S cell cycle checkpoint in response to DNA damage. Cell Cycle 2007; 6:2302-5; PMID:17890903; http://dx.doi.org/ 10.4161/cc.6.18.4668
16. Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, Hinnebusch AG, Marton MJ. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol Cell Biol 2001; 21:4347-68; PMID:11390663; http://dx.doi.org/10.1128/MCB.21.13.4347-4368.2001
17. Deng J, Harding HP, Raught B, Gingras AC, Berlanga JJ, Scheuner D, Kaufman RJ, Ron D, Sonenberg N. Activation of GCN2 in UV-irradiated cells inhibits translation. Curr Biol 2002; 12:1279-86; PMID:12176355; http://dx.doi.org/10.1016/S0960-9822(02)01037-0
18. Powley IR, Kondrashov A, Young LA, Dobbyn HC, Hill K, Cannell IG, Stoneley M, Kong YW, Cotes JA, Smith GC, et al. Translational reprogramming following UVB irradiation is mediated by DNA-PKcs and allows selective recruitment to the polysomes of mRNAs encoding DNA repair enzymes. Genes Dev 2009; 23:1207-20; PMID:19451221; http://dx.doi. org/10.1101/gad.516509
19. Pardee AB, Li YZ, Li CJ. Cancer therapy with betalapachone. Curr Cancer Drug Targets 2002; 2:227-42; PMID:12188909; http://dx.doi.org/10.2174/ 1568009023333854
20. Li CJ, Li YZ, Pinto AV, Pardee AB. Potent inhibition of tumor survival in vivo by beta-lapachone plus taxol: combining drugs imposes different artificial checkpoints. Proc Natl Acad Sci U S A 1999; 96:13369-74; PMID:10557327; http://dx.doi.org/10.1073/ pnas.96.23.13369
21. Pink JJ, Planchon SM, Tagliarino C, Varnes ME, Siegel D, Boothman DA. NAD(P)H:Quinone oxidoreductase activity is the principal determinant of betalapachone cytotoxicity. J Biol Chem 2000; 275:5416-24; PMID:10681517; http://dx.doi.org/10.1074/ jbc.275.8.5416
22. Menacho-Marquez M, Murguia JR. Beta-lapachone activates a Mre11p-Tel1p G1/S checkpoint in budding yeast. Cell Cycle 2006; 5:2509-16; PMID:17106258; http://dx.doi.org/10.4161/cc.5.21.3394
23. Sun X, Li Y, Li W, Zhang B, Wang AJ, Sun J, Mikule K, Jiang Z, Li CJ. Selective induction of necrotic cell death in cancer cells by beta-lapachone through activation of DNA damage response pathway. Cell Cycle 2006; 5:2029-35; PMID:16969131; http://dx.doi.org/ 10.4161/cc.5.17.3312
24. Dev K, Qiu H, Dong J, Zhang F, Barthlme D, Hinnebusch AG. The beta/Gcd7 subunit of eukaryotic translation initiation factor 2B (eIF2B), a guanine nucleotide exchange factor, is crucial for binding eIF2 in vivo. Mol Cell Biol 2010; 30(21):5218-33; PMID:20805354; http://dx.doi.org/10.1128/ MCB.00265-10
25. Yang W, Hinnebusch AG. Identification of a regulatory subcomplex in the guanine nucleotide exchange factor eIF2B that mediates inhibition by phosphorylated eIF2. Mol Cell Biol 1996; 16(11):6603-16; PMID:8887689
26. Bentle MS, Reinicke KE, Dong Y, Bey EA, Boothman DA. Nonhomologous end joining is essential for cellular resistance to the novel antitumor agent, beta-lapachone. Cancer Res 2007; 67:6936-45; PMID:17638905; http://dx.doi.org/10.1158/0008-5472.CAN-07-0935
27. Bey EA, Bentle MS, Reinicke KE, Dong Y, Yang CR, Girard L, Minna JD, Bornmann WG, Gao J, Boothman DA. An NQO1- and PARP-1-mediated cell death pathway induced in non-small-cell lung cancer cells by beta-lapachone. Proc Natl Acad Sci U S A 2007; 104:11832-7; PMID:17609380; http://dx.doi.org/ 10.1073/pnas.0702176104
28. Kubata BK, Kabututu Z, Nozaki T, Munday CJ, Fukuzumi S, Ohkubo K, Lazarus M, Maruyama T, Martin SK, Duszenko M, et al. A key role for old yellow enzyme in the metabolism of drugs by Trypanosoma cruzi. J Eep Med 2002; 196:1241-51; PMID:12417633; http://dx.doi.org/10.1084/jem. 20020885
29. Rouse J, Jackson SP. Interfaces between the detection, signaling, and repair of DNA damage. Science 2002; 297:547-51; PMID:12142523; http://dx.doi.org/ 10.1126/science.1074740
30. Asher G, Lotem J, Sachs L, Kahana C, Shaul Y. Mdm-2 and ubiquitin-independent p53 proteasomal degradation regulated by NQO1. Proc Natl Acad Sci U S A 2002; 99:13125-30; PMID:12232053; http://dx.doi. org/10.1073/pnas.202480499
31. Lee H, Park MT, Choi BH, Oh ET, Song MJ, Lee J, Kim C, Lim BU, Park HJ. Endoplasmic reticulum stress-induced JNK activation is a critical event leading to mitochondria-mediated cell death caused by b-lapachone treatment. PLoS One. 2011; 6(6):e21533; PMID:21738692; http://dx.doi.org/10.1371/journal. pone.0021533
32. Malzer E, Daly ML, Moloney A, Sendall TJ, Thomas SE, Ryder E, Ryoo HD, Crowther DC, Lomas DA, Marciniak SJ. Impaired tissue growth is mediated by checkpoint kinase 1 (CHK1) in the integrated stress response. J Cell Sci. 2010; 123(Pt 17):2892-900; PMID:20682638; http://dx.doi.org/10.1242/jcs. 070078
33. Yuzefovych LV, LeDoux SP, Wilson GL, Rachek LI. Mitochondrial DNA damage via augmented oxidative stress regulates endoplasmic reticulum stress and autophagy: crosstalk, links and signaling. PLoS One. 2013; 8(12):e83349; PMID:24349491; http://dx.doi. org/10.1371/journal.pone.0083349
34. van Galen P, Kreso A, Mbong N, Kent DG, Fitzmaurice T, Chambers JE, Xie S, Laurenti E, Hermans K, Eppert K, Marciniak SJ, Goodall JC, Green AR, Wouters BG, Wienholds E, Dick JE. The unfolded protein response governs integrity of the haematopoietic stem-cell pool during stress. Nature 2014; 510 (7504):268-72; PMID:24776803; http://dx.doi.org/ 10.1038/nature13228
35. Jiang HY, Wek RC. GCN2 phosphorylation of eIF2alpha activates NF-kappaB in response to UV irradiation. Biochem J 2005; 385, 371-380; PMID:15355306; http://dx.doi.org/10.1042/BJ20041348
36. Wu S, Hu Y, Wang JL, Chatterjee M, Shi Y, Kaufman RJ. Ultraviolet light inhibits translation through activation of the unfolded protein response kinase PERK in the lumen of the endoplasmic reticulum. J Biol Chem 2002; 277:18077-18083; PMID:11877419; http://dx. doi.org/10.1074/jbc.M110164200
37. Prinz W. Guide to yeast genetics and molecular cell biology. In: Guthrie CF, GR, ed. Guide to Yeast Genetics and Molecular Cell Biology, Part B, Volume 350 (Methods in Enzymology). New York: Academic Press, 2003.
38. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001; 98:5116-21; PMID:11309499; http://dx.doi.org/10.1073/pnas .091062498
39. Al-Shahrour F, Minguez P, Tarraga J, Montaner D, Alloza E, Vaquerizas JM, Conde L, Blaschke C, Vera J, Dopazo J. BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments. Nucleic Acids Res 2006; 34:W472-6; PMID:16845052; http://dx.doi.org/10.1093/nar/ gkl172
40. Teixeira MC, Monteiro P, Jain P, Tenreiro S, Fernandes AR, Mira NP, Alenquer M, Freitas AT, Oliveira AL, Sa-Correia I. The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 2006; 34:D446-51; PMID:16381908; http://dx.doi.org/ 10.1093/nar/gkj013
41. Jiang HY, Wek RC. Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem 2005; 280:14189-202; PMID:15684420; http://dx.doi.org/ 10.1074/jbc.M413660200
42. Madeo F, Frohlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Frohlich KU. Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 1999; 145:757-67; PMID:10330404; http://dx.doi.org/10.1083/jcb.145. 4.757
43. de la Torre-Ruiz MA, Green CM, Lowndes NF. RAD9 and RAD24 define two additive, interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation. EMBO J 1998; 17: 2687-98; PMID:9564050; http://dx.doi.org/ 10.1093/emboj/17.9.2687
44. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65:55-63; PMID:6606682; http://dx.doi.org/10.1016/0022-1759(83)90303-4