Activation of the MAPK11/12/13/14 (p38 MAPK) pathway regulates the transcription of autophagy genes in response to oxidative stress induced by a novel copper complex in HeLa cells

Autophagy

Volumn 10, Issue 7, 2014, Pages 1285-1300

  Zhong, Wu ^a   Zhu, Haichuan ^a,b   Sheng, Fugeng ^c   Tian, Yonglu ^d   Zhou, Jun ^a   Chen, Yingyu ^d   Li, Song ^a   Lin, Jian ^b  

^a BEIJING INSTITUTE OF PHARMACOLOGY AND TOXICOLOGY   (China)

^b PEKING UNIVERSITY   (China)

^c BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^d PEKING UNIVERSITY   (China)

Author keywords

Autophagy; cHYF127c Cu; Copper; MAPK11; MAPK12; MAPK13; MAPK14; Oxidative stress; p38 mitogen activated protein kinase; Transcription

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTINEOPLASTIC AGENT; BAG3 PROTEIN; CELL PROTEIN; COPPER COMPLEX; DI 2 PYRIDYL KETONE 4 ALLYL 3 SELENOSEMICARBAZIDE; HSPA1A PROTEIN; MAP1LC3B PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 11; MITOGEN ACTIVATED PROTEIN KINASE 12; MITOGEN ACTIVATED PROTEIN KINASE 13; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE P38; SEMICARBAZIDE DERIVATIVE; UNCLASSIFIED DRUG; COPPER; IMIDAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGY; CANCER CELL; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; GENE EXPRESSION; GROWTH INHIBITION; HELA CELL LINE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT; UTERINE CERVIX CANCER; APOPTOSIS; CELL PROLIFERATION; CELL VACUOLE; CHEMISTRY; DOWN REGULATION; DRUG EFFECTS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGICAL STRESS; SEQUENCE ANALYSIS; ULTRASTRUCTURE;

APOPTOSIS; AUTOPHAGY; CELL PROLIFERATION; COPPER; DOWN-REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HUMANS; IMIDAZOLES; MAP KINASE SIGNALING SYSTEM; NEOPLASM PROTEINS; NEOPLASMS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; SEQUENCE ANALYSIS, RNA; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC; VACUOLES;

EID: 84903833678     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.28789     Document Type: Article

References (46)

1. Skrott Z, Cvek B. Diethyldithiocarbamate complex with copper: the mechanism of action in cancer cells. Mini Rev Med Chem 2012; 12:1184-92; PMID:22931589; http://dx.doi.org/10.2174/138955712802762068
2. Loganathan R, Ramakrishnan S, Suresh E, Riyasdeen A, Akbarsha MA, Palaniandavar M. Mixed ligand copper(II) complexes of N,N-bis(benzimidazol-2- ylmethyl)amine (BBA) with diimine co-ligands: efficient chemical nuclease and protease activities and cytotoxicity. Inorg Chem 2012; 51:5512-32; PMID:22559171; http://dx.doi.org/10.1021/ic2017177
3. Gandin V, Pellei M, Tisato F, Porchia M, Santini C, Marzano C. A novel copper complex induces paraptosis in colon cancer cells via the activation of ER stress signalling. J Cell Mol Med 2012; 16:142-51; PMID:21388518; http://dx.doi.org/10.1111/j.1582-4934.2011.01292.x
4. Duff B, Thangella VR, Creaven BS, Walsh M, Egan DA. Anti-cancer activity and mutagenic potential of novel copper(II) quinolinone Schiff base complexes in hepatocarcinoma cells. Eur J Pharmacol 2012; 689:45-55; PMID:22705894; http://dx.doi.org/10.1016/j.ejphar.2012.06.004
5. Frezza M, Hindo S, Chen D, Davenport A, Schmitt S, Tomco D, Dou QP. Novel metals and metal complexes as platforms for cancer therapy. Curr Pharm Des 2010; 16:1813-25; PMID:20337575; http://dx.doi.org/10.2174/138161210791209009
6. Chen D, Dou QP. New uses for old copper-binding drugs: converting the pro-angiogenic copper to a specific cancer cell death inducer. Expert Opin Ther Targets 2008; 12:739-48; PMID:18479220; http://dx.doi.org/10.1517/14728222.12.6. 739
7. Chen D, Milacic V, Frezza M, Dou QP. Metal complexes, their cellular targets and potential for cancer therapy. Curr Pharm Des 2009; 15:777-91; PMID:19275642; http://dx.doi.org/10.2174/138161209787582183
8. Kelland L. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 2007; 7:573-84; PMID:17625587; http://dx.doi.org/10.1038/nrc2167
9. Tardito S, Marchiò L. Copper compounds in anticancer strategies. Curr Med Chem 2009; 16:1325-48; PMID:19355889; http://dx.doi.org/10.2174/ 092986709787846532
10. Jungwirth U, Kowol CR, Keppler BK, Hartinger CG, Berger W, Heffeter P. Anticancer activity of metal complexes: involvement of redox processes. Antioxid Redox Signal 2011; 15:1085-127; PMID:21275772; http://dx.doi.org/10.1089/ars. 2010.3663
11. Duncan C, White AR. Copper complexes as therapeutic agents. Metallomics 2012; 4:127-38; PMID:22187112; http://dx.doi.org/10.1039/c2mt00174h
12. Chen D, Cui QC, Yang H, Dou QP. Disulfiram, a clinically used anti-alcoholism drug and copperbinding agent, induces apoptotic cell death in breast cancer cultures and xenografts via inhibition of the proteasome activity. Cancer Res 2006; 66:10425-33; PMID:17079463; http://dx.doi.org/10.1158/0008- 5472.CAN-06-2126
13. Lovejoy DB, Jansson PJ, Brunk UT, Wong J, Ponka P, Richardson DR. Antitumor activity of metal-chelating compound Dp44mT is mediated by formation of a redox-active copper complex that accumulates in lysosomes. Cancer Res 2011; 71:5871-80; PMID:21750178; http://dx.doi.org/10.1158/0008-5472.CAN-11-1218
14. Tardito S, Bassanetti I, Bignardi C, Elviri L, Tegoni M, Mucchino C, Bussolati O, Franchi-Gazzola R, Marchiò L. Copper binding agents acting as copper ionophores lead to caspase inhibition and paraptotic cell death in human cancer cells. J Am Chem Soc 2011; 133:6235-42; PMID:21452832; http://dx.doi.org/10.1021/ja109413c
15. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
16. Sun Y, Zou M, Hu C, Qin Y, Song X, Lu N, et al. Wogonoside induces autophagy in MDA-MB-231 cells by regulating MAPK-mTOR pathway. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association 2013; 51:53-60.
17. Zhou Z, Zhang D, Yang L, Ma P, Si Y, Kortz U, Niu J, Wang J. Nona-copper(II)-containing 18-tungsto-8-arsenate(III) exhibits antitumor activity. Chem Commun (Camb) 2013; 49:5189-91; PMID:23628910; http://dx.doi.org/10.1039/c3cc41628c
18. Trejo-Solís C, Jimenez-Farfan D, Rodriguez-Enriquez S, Fernandez-Valverde F, Cruz-Salgado A, Ruiz-Azuara L, Sotelo J. Copper compound induces autophagy and apoptosis of glioma cells by reactive oxygen species and JNK activation. BMC Cancer 2012; 12:156; PMID:22540380; http://dx.doi.org/10. 1186/1471-2407-12-156
19. Sun T, Yan Y, Zhao Y, Guo F, Jiang C. Copper oxide nanoparticles induce autophagic cell death in A549 cells. PLoS One 2012; 7:e43442; PMID:22916263; http://dx.doi.org/10.1371/journal.pone.0043442
20. Hancock CN, Stockwin LH, Han B, Divelbiss RD, Jun JH, Malhotra SV, Hollingshead MG, Newton DL. A copper chelate of thiosemicarbazone NSC 689534 induces oxidative/ER stress and inhibits tumor growth in vitro and in vivo. Free Radic Biol Med 2011; 50:110-21; PMID:20971185; http://dx.doi.org/10.1016/j. freeradbiomed.2010.10.696
21. Guo WJ, Ye SS, Cao N, Huang J, Gao J, Chen QY. ROS-mediated autophagy was involved in cancer cell death induced by novel copper(II) complex. Experimental and toxicologic pathology: official journal of the Gesellschaft fur Toxikologische Pathologie 2010; 62:577-82.
22. Paris I, Perez-Pastene C, Couve E, Caviedes P, Ledoux S, Segura-Aguilar J. Copper dopamine complex induces mitochondrial autophagy preceding caspase-independent apoptotic cell death. J Biol Chem 2009; 284:13306-15; PMID:19265190; http://dx.doi.org/10.1074/jbc.M900323200
23. Myhre O, Andersen JM, Aarnes H, Fonnum F. Evaluation of the probes 2′,7′-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation. Biochem Pharmacol 2003; 65:1575-82; PMID:12754093; http://dx.doi.org/10.1016/S0006-2952(03)00083-2
24. Meister A, Anderson ME. Glutathione. Annu Rev Biochem 1983; 52:711-60; PMID:6137189; http://dx.doi.org/10.1146/annurev.bi.52.070183.003431
25. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009; 10:57-63; PMID:19015660; http://dx.doi.org/10.1038/nrg2484
26. Ozsolak F, Milos PM. RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 2011; 12:87-98; PMID:21191423; http://dx.doi.org/ 10.1038/nrg2934
27. Wacker SA, Houghtaling BR, Elemento O, Kapoor TM. Using transcriptome sequencing to identify mechanisms of drug action and resistance. Nat Chem Biol 2012; 8:235-7; PMID:22327403; http://dx.doi.org/10.1038/nchembio.779
28. Rouschop KM, van den Beucken T, Dubois L, Niessen H, Bussink J, Savelkouls K, Keulers T, Mujcic H, Landuyt W, Voncken JW, et al. The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J Clin Invest 2010; 120:127-41; PMID:20038797; http://dx.doi.org/10.1172/JCI40027
29. Zhang XY, Wu XQ, Deng R, Sun T, Feng GK, Zhu XF. Upregulation of sestrin 2 expression via JNK pathway activation contributes to autophagy induction in cancer cells. Cell Signal 2013; 25:150-8; PMID:22982090; http://dx.doi.org/10. 1016/j.cellsig.2012.09.004
30. Carra S, Seguin SJ, Landry J. HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 2008; 4:237-9; PMID:18094623
31. Behl C. BAG3 and friends: co-chaperones in selective autophagy during aging and disease. Autophagy 2011; 7:795-8; PMID:21681022; http://dx.doi.org/10. 4161/auto.7.7.15844
32. Yang Y, Fiskus W, Yong B, Atadja P, Takahashi Y, Pandita TK, Wang HG, Bhalla KN. Acetylated hsp70 and KAP1-mediated Vps34 SUMOylation is required for autophagosome creation in autophagy. Proc Natl Acad Sci U S A 2013; 110:6841-6; PMID:23569248; http://dx.doi.org/10.1073/pnas.1217692110
33. Lin J, Zheng Z, Li Y, Yu W, Zhong W, Tian S, Zhao F, Ren X, Xiao J, Wang N, et al. A novel Bcl-XL inhibitor Z36 that induces autophagic cell death in Hela cells. Autophagy 2009; 5:314-20; PMID:19242113; http://dx.doi.org/10.4161/ auto.5.3.7888
34. Malik SA, Shen S, Mariño G, BenYounès A, Maiuri MC, Kroemer G. BH3 mimetics reveal the network properties of autophagy-regulatory signaling cascades. Autophagy 2011; 7:914-6; PMID:21508685; http://dx.doi.org/10.4161/ auto.7.8.15785
35. Zhou F, Yang Y, Xing D. Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J 2011; 278:403-13; PMID:21182587; http://dx.doi.org/10.1111/j.1742-4658.2010.07965.x
36. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75; PMID:18188003
37. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell.2011.02.013
38. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5:726-34; PMID:16148885; http://dx.doi.org/10.1038/nrc1692
39. Tian S, Lin J, Jun Zhou J, Wang X, Li Y, Ren X, Yu W, Zhong W, Xiao J, Sheng F, et al. Beclin 1-independent autophagy induced by a Bcl-XL/Bcl-2 targeting compound, Z18. Autophagy 2010; 6:1032-41; PMID:20818185; http://dx.doi.org/10.4161/auto.6.8.13336
40. Whitmarsh AJ. A central role for p38 MAPK in the early transcriptional response to stress. BMC Biol 2010; 8:47; PMID:20515460; http://dx.doi.org/10. 1186/1741-7007-8-47
41. Bazuine M, Carlotti F, Rabelink MJ, Vellinga J, Hoeben RC, Maassen JA. The p38 mitogen-activated protein kinase inhibitor SB203580 reduces glucose turnover by the glucose transporter-4 of 3T3-L1 adipocytes in the insulin-stimulated state. Endocrinology 2005; 146:1818-24; PMID:15665038; http://dx.doi.org/10.1210/en.2004-1347
42. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh Y, et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 2001; 98:13681-6; PMID:11717429; http://dx.doi.org/10.1073/pnas.251194298
43. Hancock CN, Stockwin LH, Han B, Divelbiss RD, Jun JH, Malhotra SV, Hollingshead MG, Newton DL. A copper chelate of thiosemicarbazone NSC 689534 induces oxidative/ER stress and inhibits tumor growth in vitro and in vivo. Free Radic Biol Med 2011; 50:110-21; PMID:20971185; http://dx.doi.org/10.1016/j. freeradbiomed.2010.10.696
44. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12:401-10; PMID:22534666; http://dx.doi.org/10. 1038/nrc3262
45. He H, Zang LH, Feng YS, Chen LX, Kang N, Tashiro S, Onodera S, Qiu F, Ikejima T. Physalin A induces apoptosis via p53-Noxa-mediated ROS generation, and autophagy plays a protective role against apoptosis through p38-NF-κB survival pathway in A375-S2 cells. J Ethnopharmacol 2013; 148:544-55; PMID:23684722; http://dx.doi.org/10.1016/j.jep.2013.04.051
46. McClung JM, Judge AR, Powers SK, Yan Z. p38 MAPK links oxidative stress to autophagy-related gene expression in cachectic muscle wasting. Am J Physiol Cell Physiol 2010; 298:C542-9; PMID:19955483; http://dx.doi.org/10.1152/ajpcell. 00192.2009