The p90 ribosomal S6 kinase (RSK) inhibitor BI-D1870 prevents gamma irradiation-induced apoptosis and mediates senescence via RSK- and p53-independent accumulation of p21WAF1/CIP1

Cell Death and Disease

Volumn 4, Issue 10, 2013, Pages

  Neise, D ^a   Sohn, D ^a   Stefanski, A ^a   Goto, H ^b   Inagaki, M ^b   Wesselborg, S ^a   Budach, W ^a   Stuhler K ^a   Janicke R U ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b AICHI CANCER CENTER HOSPITAL   (Japan)

Author keywords

Apoptosis; BI D1870; Cell cycle; Off target effect; Senescence; SL0101

Indexed keywords

AURORA B KINASE; BID 1870; CYCLIN DEPENDENT KINASE INHIBITOR 1; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHOTRANSFERASE INHIBITOR; POLO LIKE KINASE 1; PROTEIN P53; RAF PROTEIN; S6 KINASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL GROWTH; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GAMMA IRRADIATION; IMMUNOPRECIPITATION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DETERMINATION; RADIATION RESPONSE; RNA INTERFERENCE; SENESCENCE; SIGNAL TRANSDUCTION;

APOPTOSIS; AURORA KINASES; BENZOPYRANS; CELL AGING; CELL CYCLE PROTEINS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GAMMA RAYS; GENE KNOCKDOWN TECHNIQUES; HCT116 CELLS; HUMANS; ISOENZYMES; MONOSACCHARIDES; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PTERIDINES; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; STRESS, PHYSIOLOGICAL; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84887447444     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.386     Document Type: Article

References (52)

1. Anjum R, Blenis J. The RSK family of kinases: Emerging roles in cellular signalling. Nat Rev Mol Cell Biol 2008; 9: 747-758
2. Roberts PJ, Der CJ. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007; 26: 3291-3310
3. Roux PP, Blenis J. ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 2004; 68: 320-344
4. Xing J, Ginty DD, Greenberg ME. Coupling of the Ras-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 1996; 273: 959-963
5. Zhang L, Ma Y, Zhang J, Cheng J, Du J. A new cellular signaling mechanism for angiotensin II activation of NF-kappaB; An IkappaB-independent, RSK-mediated phosphorylation of p65. Arterioscler Thromb Vasc Biol 2005; 25: 1148-1153
6. Shahbazian D, Roux PP, Mieulet V, Cohen MS, Raught B, Taunton J et al. The mTOR/ PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity. EMBO J 2006; 25: 2781-2791
7. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J et al. Ras/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates Cap-dependent translation. J Biol Chem 2007; 282: 14056-14064
8. Fujita N, Sato S, Tsuruo T. Phosphorylation of p27Kip1 at threonine 198 by p90 ribosomal protein S6 kinases promotes its binding to 14-3-3 and cytoplasmic localization. J Biol Chem 2003; 278: 49254-49260
9. Li P, Goto H, Kasahara K, Matsuyama M,Wang Z, Yatabe Y et al. p90 RSK arranges Chk1 in the nucleus for monitoring of genomic integrity during cell proliferation. Mol Biol Cell 2012; 23: 1582-1592
10. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 1999; 286: 1358-1362
11. Dehan E, Bassermann F, Guardavaccaro D, Vasiliver-Shamis G, Cohen M, Lowes KN et al. bTrCP-and RSK1/2-mediated degradation of BimEL inhibits apoptosis. Mol Cell 2009; 33: 109-116
12. Peng C, Cho YY, Zhu F, Zhang J, Wen W, Xu Y et al. Phosphorylation of caspase-8(Thr-263) by ribosomal S6 kinase 2 (RSK2) mediates caspase-8 ubiquitination and stability. J Biol Chem 2011; 286: 6946-6953
13. Cho YY, He Z, Zhang Y, Choi HS, Zhu F, Choi BY et al. The p53 protein is a novel substrate of ribosomal S6 kinase 2 and a critical intermediary for ribosomal S6 kinase 2 and histone H3 interaction. Cancer Res 2005; 65: 3596-3603
14. Clark DE, Errington TM, Smith JA, Frierson HF Jr, Weber MJ, Lannigan DA. The serine/ threonine protein kinase, p90 ribosomal S6 kinase, is an important regulator of prostate cancer cell proliferation. Cancer Res 2005; 65: 3108-3116
15. Smith JA, Poteet-Smith CE, Xu Y, Errington TM, Hecht SM, Lannigan DA. Identification of the first specific inhibitor of p90 ribosomal S6 kinase (RSK) reveals an unexpected role for RSK in cancer cell proliferation. Cancer Res 2005; 65: 1027-1034
16. Cho YY, Yao K, Kim HG, Kang BS, Zhen D, Bode AM et al. Ribosomal S6 kinase 2 is a key regulator in tumor promoter-induced cell transformation. Cancer Res 2007; 67: 8104-8112
17. Shimamura A, Ballif BA, Richards SA, Blenis J. RSK1 mediates a MEK-MAP kinase cell survival signal. Curr Biol 2000; 10: 127-135
18. Abbas T, Dutta A. p21 in cancer: Intricate networks and multiple activities. Nat Rev Cancer 2009; 9: 400-414
19. Jänicke RU, Sohn D, Essmann F, Schulze-Osthoff K. The multiple battles fought by antiapoptotic p21. Cell Cycle 2007; 6: 407-413
20. Child ES, Mann DJ. The intricacies of p21 phosphorylation: Protein/protein interactions, subcellular localization and stability. Cell Cycle 2006; 5: 1313-1319
21. Jung YS, Qian Y, Chen X. Examination of the expanding pathways for the regulation of p21 expression and activity. Cell Signal 2010; 22: 1003-1012
22. Lee YS, Dutta A. MicroRNAs: Small but potent oncogenes or tumor suppressors. Curr Opin Investig Drugs 2006; 7: 560-564
23. Sohn D, Budach W, Jänicke RU. Caspase-2 is required for DNA damage-induced expression of the CDK inhibitor p21(WAF1/CIP1). Cell Death Differ 2011; 18: 1664-1674
24. Zhang J, Chen X. Posttranscriptional regulation of p53 and its targets by RNA-binding proteins. Curr Mol Med 2008; 8: 845-849
25. Neise D, Sohn D, Budach W, Jänicke RU. Evidence for a differential modulation of p53-phosphorylating kinases by the cyclin-dependent kinase inhibitor p21WAF1/CIP1. Cell Cycle 2010; 9: 3575-3583
26. Dent P, Yacoub A, Fisher PB, Hagan MP, Grant S. MAPK pathways in radiation responses. Oncogene 2003; 22: 5885-5896
27. Sebolt-Leopold JS, Herrera R. Targeting the mitogen-activated protein kinase cascade to treat cancer. Nat Rev Cancer 2004; 4: 937-947
28. Sohn D, Essmann F, Schulze-Osthoff K, Jänicke RU. p21 blocks irradiation-induced apoptosis downstream of mitochondria by inhibition of cyclin-dependent kinase-mediated caspase-9 activation. Cancer Res 2006; 66: 11254-11262
29. Sapkota GP, Cummings L, Newell FS, Armstrong C, Bain J, Frodin M. BI-D1870 is a specific inhibitor of the p90 RSK (ribosomal S6 kinase) isoforms in vitro and in vivo. Biochem J 2007; 401: 29-38
30. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H et al. The selectivity of protein kinase inhibitors: A further update. Biochem J 2007; 408: 297-315
31. Lens SMA, Voest EE, Medema RH. Shared and separate functions of polo-like kinases and aurora kinases in cancer. Nat Rev Cancer 2010; 10: 825-841
32. Pearce LR, Komander D, Alessi DR. The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 2010; 11: 9-22
33. Stevenson MA, Pollock SS, Coleman CN, Calderwood SK. X-irradiation, phorbol esters and H2O2 stimulate mitogen-activated protein kinase activity in NIH-3T3 cells through the formation of reactive oxygen intermediates. Cancer Res 1994; 54: 12-15
34. Zhang J, Yang PL, Gray NS. Targeting cancer with small molecule kinase inhibitors. Nature Rev Cancer 2009; 9: 28-39
35. Romeo Y, Roux PP. Paving the way for targeting RSK in cancer. Expert Opin Ther Targets 2011; 15: 5-9
36. David JP, Mehic D, Bakiri L, Schilling AF, Mandic V, Priemel M et al. Essential role of RSK2 in c-Fos-dependent osteosarcoma development. J Clin Invest 2005; 115: 664-672
37. Elf S, Blevins D, Jin L, Chung TW,Williams IR, Lee BH et al. p90RSK2 is essential for FLT3-ITDbut dispensable for BCR-ABL-induced myeloid leukemia. Blood 2011; 117: 6885-6894
38. Kang S, Elf S, Lythgoe K, Hitosugi T, Taunton J, Zhou W et al. p90 ribosomal S6 kinase 2 promotes invasion and metastasis of human head and neck squamous cell carcinoma cells. J Clin Invest 2010; 120: 1165-1177
39. Joel PB, Smith J, Sturgill TW, Fisher TL, Blenis J, Lannigan DA. pp90rsk1 regulates estrogen receptor-mediated transcription through phosphorylation of Ser-167. Mol Cell Biol 1998; 18: 1978-1984
40. Sutherland RL, Musgrove EA. Cyclins and breast cancer. J Mammary Gland Biol Neoplasia 2004; 9: 95-104
41. Stratford AL, Fry CJ, Desilets C, Davies AH, Cho YY, Li Y et al. Y-box binding protein-1 serine 102 is a downstream target of p90 ribosomal S6 kinase in basal-like breast cancer cells. Breast Cancer Res 2008; 10: R99
42. Stratford AL, Reipas K, Hu K, Fotovati A, Brough R, Frankum J et al. Targeting p90 ribosomal S6 kinase eliminates tumor-initiating cells by inactivating Y-box binding protein-1 in triple-negative breast cancers. Stem Cells 2012; 30: 1338-1348
43. Shimura Y, Kuroda J, Ri M, Nagoshi H, Yamamoto-Sugitani M et al. RSK2(Ser227) at N-terminal kinase domain is a potential therapeutic target for multiple myeloma. Mol Cancer Ther 2012; 11: 2600-2609
44. Cohen M, Zhang C, Shokat KM, Taunton J. Structural bioinformatics-based design of selective, irreversible kinase inhibitors. Science 2005; 308: 1318-1321
45. Zaru R, Ronkina N, Gaestel M, Arthur JSC, Watts C. The MAP kinase-activated RSK controls an acute Toll-like receptor signalling response in dendritic cells and is activated via two distinct pathways. Nat. Immunol 2007; 8: 1227-1235
46. Boehm M, Yoshimoto T, Crook MF, Nallamshetty S, True A, Nabel GJ et al. A growth factor-dependent nuclear kinase phosphorylates p27(Kip1) and regulates cell cycle progression. EMBO J 2002; 21: 3390-3401
47. Fujita N, Sato S, Katayama K, Tsuruo T. Akt-dependent phosphorylation of p27Kip1 promotes binding to 14-3-3 and cytoplasmic localization. J Biol Chem 2002; 277: 28706-28713
48. Geraghty KM, Chen S, Harthill JE, Ibrahim AF, Toth R, Morrice NA et al. Regulation of multisite phosphorylation and 14-3-3 binding of AS160 in response to IGF-1, EGF, PMA and AICAR. Biochem J 2007; 407: 231-241
49. Scott MT, Ingram A, Ball KL. PDK1-dependent activation of atypical PKC leads to degradation of the p21 tumour modifier protein. EMBO J 2002; 21: 6771-6780
50. Oh Y-T, Chun KH, Park BD, Choi J-S, Lee SK. Regulation of cyclin-dependent kinase inhibitor p21WAF1/CIP1 by protein kinase Cd-mediated phosphorylation. Apoptosis 2007; 12: 1339-1347
51. Rössig L, Jadidi AS, Urbich C, Gadorff C, Zeiher AM, Dimmeler S. Akt-dependent phosphorylation of p21(CIP1) regulates PCNA binding and proliferation of endothelial cells. Mol Cell Biol 2001; 21: 5644-5657
52. Jänicke RU, Sprengart ML, Wati MR, Porter AG. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 1998; 273: 9357-9360