Proteasome inhibition induces a p38 MAPK pathway-dependent antiapoptotic program via Nrf2 in thyroid cancer cells

Journal of Clinical Endocrinology and Metabolism

Volumn 96, Issue 5, 2011, Pages

  Du, Zhen Xian ^a   Yan, Ying ^a,b   Zhang, Hai Yan ^a   Liu, Bao Qin ^a   Gao, Yan Yan ^a   Niu, Xiao Fang ^a   Meng, Xin ^a   Wang, Hua Qin ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b SHENYANG NORTHERN HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; EPOXOMICIN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; LACTACYSTIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEASOME; PROTEASOME INHIBITOR; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; WORTMANNIN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL FRACTIONATION; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME REPRESSION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; SPECTROFLUOROMETRY; THYROID CANCER; TRANSACTIVATION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; BORONIC ACIDS; CELL DEATH; CELL LINE, TUMOR; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HUMANS; MICROSCOPY, CONFOCAL; NF-E2-RELATED FACTOR 2; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLASMIDS; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THYROID NEOPLASMS; TRANSCRIPTIONAL ACTIVATION; TRANSLOCATION, GENETIC;

EID: 79955647069     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2010-2642     Document Type: Article

References (37)

1. Czaja MJ 2002 Induction and regulation of hepatocyte apoptosis by oxidative stress. Antioxid Redox Signal 4:759-767 (Pubitemid 35246938)
2. Gabbita SP, Robinson KA, Stewart CA, Floyd RA, Hensley K 2000 Redox regulatory mechanisms of cellular signal transduction. Arch Biochem Biophys 376:1-13 (Pubitemid 30205109)
3. Hannun YA 1996 Functions of ceramide in coordinating cellular responses to stress. Science 274:1855-1859 (Pubitemid 26424756)
4. Stennicke HR, Salvesen GS 2000 Caspases - controlling intracellular signals by protease zymogen activation. Biochim Biophys Acta 1477:299-306 (Pubitemid 30119908)
5. Kågedal K, Johansson U, Ollinger K 2001 The lysosomal protease cathepsin D mediates apoptosis induced by oxidative stress. FASEB J 15:1592-1594
6. Haider UG, Sorescu D, Griendling KK, Vollmar AM, Dirsch VM 2003 Resveratrol increases serine15-phosphorylated but transcriptionally impaired p53 and induces a reversible DNA replication block in serum-activated vascular smooth muscle cells. Mol Pharmacol 63:925-932 (Pubitemid 36369000)
7. Pérez-Galán P, Roué G, Villamor N, Montserrat E, Campo E, Colomer D 2006 The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood 107:257-264 (Pubitemid 43053550)
8. Yu C, Rahmani M, Dent P, Grant S 2004 The hierarchical relationship between MAPK signaling and ROS generation in human leukemia cells undergoing apoptosis in response to the proteasome inhibitor Bortezomib. Exp Cell Res 295:555-566 (Pubitemid 38490507)
9. Fribley A, Zeng Q, Wang CY 2004 Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells. Mol Cell Biol 24:9695-9704 (Pubitemid 39458799)
10. Du ZX, Zhang HY, Meng X, Guan Y, Wang HQ 2009 Role of oxidative stress and intracellular glutathione in the sensitivity to apoptosis induced by proteasome inhibitor in thyroid cancer cells. BMC Cancer 9:56
11. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y 1997 An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236:313-322 (Pubitemid 27373291)
12. Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, Yamamoto M 2000 Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 275:16023-16029 (Pubitemid 30366908)
13. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, Yamamoto M 2004 Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 24:7130-7139 (Pubitemid 39014439)
14. Hong F, Sekhar KR, Freeman ML, Liebler DC 2005 Specific patterns of electrophile adduction trigger Keap1 ubiquitination and Nrf2 activation. J Biol Chem 280:31768-31775
15. McMahon M, Itoh K, Yamamoto M, Chanas SA, Henderson CJ, McLellan LI, Wolf CR, Cavin C, Hayes JD 2001 The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res 61:3299-3307 (Pubitemid 32695017)
16. Devling TW, Lindsay CD, McLellan LI, McMahon M, Hayes JD 2005 Utility of siRNA against Keap1 as a strategy to stimulate a cancer chemopreventive phenotype. Proc Natl Acad Sci USA 102:7280-7285A
17. Wang XJ, Hayes JD, Wolf CR 2006 Generation of a stable antioxidant response element-driven reporter gene cell line and its use to show redox-dependent activation of nrf2 by cancer chemotherapeutic agents. Cancer Res 66:10983-10994 (Pubitemid 44876998)
18. Meriin AB, Gabai VL, Yaglom J, Shifrin VI, Sherman MY 1998 Proteasome inhibitors activate stress kinases and induce Hsp72. Diverse effects on apoptosis. J Biol Chem 273:6373-6379 (Pubitemid 28144729)
19. Hideshima T, Podar K, Chauhan D, Ishitsuka K, Mitsiades C, Tai YT, Hamasaki M, Raje N, Hideshima H, Schreiner G, Nguyen AN, Navas T, Munshi NC, Richardson PG, Higgins LS, Anderson KC 2004 p38 MAPK inhibition enhances PS-341 (bortezomib)-induced cytotoxicity against multiple myeloma cells. Oncogene 23:8766-8776 (Pubitemid 39593291)
20. Chauhan D, Li G, Shringarpure R, Podar K, Ohtake Y, Hideshima T, Anderson KC 2003 Blockade of Hsp27 overcomes Bortezomib/proteasome inhibitor PS-341 resistance in lymphoma cells. Cancer Res 63:6174-6177 (Pubitemid 37255160)
21. Yeh CT, Yen GC 2006 Involvement of p38 MAPK and Nrf2 in phenolic acid-induced P-form phenol sulfotransferase expression in human hepatoma HepG2 cells. Carcinogenesis 27:1008-1017
22. Jain AK, Bloom DA, Jaiswal AK 2005 Nuclear import and export signals in control of Nrf2. J Biol Chem 280:29158-29168 (Pubitemid 41161367)
23. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, Fagin JA, Marlow LA, Copland JA, Smallridge RC, Haugen BR 2008 Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 93:4331-4341 (Pubitemid 352789529)
24. Wang HQ, Du ZX, Zhang HY, Gao DX 2007 Different induction of GRP78 and CHOP as a predictor of sensitivity to proteasome inhibitors in thyroid cancer cells. Endocrinology 148:3258-3270
25. Adams J 2004 The proteasome: a suitable antineoplastic target. Nat Rev Cancer 4:349-360 (Pubitemid 38579481)
26. Fleury C, Mignotte B, Vayssière JL 2002 Mitochondrial reactive oxygen species in cell death signaling. Biochimie (Paris) 84:131-141
27. Han YH, Park WH 2010 The effects of MAPK inhibitors on a proteasome inhibitor, MG132-induced HeLa cell death in relation to reactive oxygen species and glutathione. Toxicol Lett 192:134-140
28. Yamamoto N, Sawada H, Izumi Y, Kume T, Katsuki H, Shimohama S, Akaike A 2007 Proteasome inhibition induces glutathione synthesis and protects cells from oxidative stress: relevance to Parkinson disease. J Biol Chem 282:4364-4372 (Pubitemid 47101000)
29. Nguyen T, Sherratt PJ, Huang HC, Yang CS, Pickett CB 2003 Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J Biol Chem 278:4536-4541 (Pubitemid 36800950)
30. Sekhar KR, Yan XX, Freeman ML 2002 Nrf2 degradation by the ubiquitin proteasome pathway is inhibited by KIAA0132, the human homolog to INrf2. Oncogene 21:6829-6834 (Pubitemid 35221925)
31. Dreger H, Westphal K, Weller A, Baumann G, Stangl V, Meiners S, Stangl K 2009 Nrf2-dependent upregulation of antioxidative enzymes: a novel pathway for proteasome inhibitor-mediated cardioprotection. Cardiovasc Res 83:354-361
32. Sahni SK, Rydkina E, Sahni A 2008 The proteasome inhibitor MG132 induces nuclear translocation of erythroid transcription factor Nrf2 and cyclooxygenase-2 expression in human vascular endothelial cells. Thromb Res 122:820-825
33. Buck I, Morceau F, Cristofanon S, Heintz C, Chateauvieux S, Reuter S, Dicato M, Diederich M 2008 Tumor necrosis factor α inhibits erythroid differentiation in human erythropoietin-dependent cells involving p38 MAPK pathway, GATA-1 and FOG-1 downregulation and GATA-2 upregulation. Biochem Pharmacol 76:1229-1239
34. Kocanova S, Buytaert E, Matroule JY, Piette J, Golab J, de Witte P, Agostinis P 2007 Induction of heme-oxygenase 1 requires the p38MAPK and PI3K pathways and suppresses apoptotic cell death following hypericin-mediated photodynamic therapy. Apoptosis 12:731-741 (Pubitemid 46411467)
35. Numazawa S, Ishikawa M, Yoshida A, Tanaka S, Yoshida T 2003 Atypical protein kinase C mediates activation of NF-E2-related factor 2 in response to oxidative stress. Am J Physiol Cell Physiol 285:C334-C342 (Pubitemid 36917848)
36. Lee JM, Hanson JM, Chu WA, Johnson JA 2001 Phosphatidylinositol 3-kinase, not extracellular signal-regulated kinase, regulates activation of the antioxidant-responsive element in IMR-32 human neuroblastoma cells. J Biol Chem 276:20011-20016
37. Shi YY, Small GW, Orlowski RZ 2006 Proteasome inhibitors induce a p38 mitogen-activated protein kinase (MAPK)-dependent antiapoptotic program involving MAPK phosphatase-1 and Akt in models of breast cancer. Breast Cancer Res Treat 100:33-47