Targeting p53 via JNK pathway: A novel role of RITA for apoptotic signaling in multiple myeloma

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Saha, Manujendra N ^a,b   Jiang, Hua ^c   Yang, Yijun ^a,b   Zhu, Xiaoyun ^a,b   Wang, Xiaoming ^d   Schimmer, Aaron D ^d   Qiu, Lugui ^e   Chang, Hong ^a,b,f  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

^d PRINCESS MARGARET HOSPITAL   (Canada)

^e INSTITUTE OF HEMATOLOGY AND BLOOD DISEASES HOSPITAL   (China)

^f UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ASK 1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; PROTEIN P53; REACTIVATION OF P53 AND INDUCTION OF TUMOR CELL APOPTOSIS; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; FURAN DERIVATIVE; NSC 652287;

APOPTOSIS; ARTICLE; BINDING SITE; CANCER CELL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME BINDING; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MULTIPLE MYELOMA; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STRESS; UPREGULATION; WILD TYPE; CELL LINE; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; DRUG EFFECT; IMMUNOBLOTTING; IN VITRO STUDY; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

APOPTOSIS; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; FURANS; HUMANS; IMMUNOBLOTTING; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MULTIPLE MYELOMA; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84856041539     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030215     Document Type: Article

References (42)

1. Avet-Loiseau H, Li JY, Godon C, Morineau N, Daviet A, et al. (1999) p53 deletion is not a frequent event in multiple myeloma. Br J Haematol 106: 717-719.
2. Chng WJ, Price-Troska T, Gonzalea-Paz N, Van Wier S, Jacobus S, et al. (2007) Clinical significance of TP53 mutation in myeloma. Leukemia 21: 582-584.
3. Chang H, Qi C, Yi Q, Reece D, Stewart AK, (2005) p53 gene deletion detected by fluorescence in situ hybridization is an adverse prognostic factor for patients with multiple myeloma following autologous stem cell transplantation. Blood 105: 358-360.
4. Vassilev LT, (2007) MDM2 inhibitors for cancer therapy. Trends Mol Med 13: 23-31.
5. Saha MN, Micallef J, Qiu L, Chang H, (2010) Pharmacological activation of the p53 pathway in haematological malignancies. J Clin Pathol 63: 204-209.
6. Saha MN, Jiang H, Chang H, (2010) Molecular mechanisms of nutlin-induced apoptosis in multiple myeloma: evidence for p53-transcription-dependent and-independent pathways. Cancer Biol Ther 10: 567-578.
7. Saha MN, Jiang H, Jayakar J, Reece D, Branch DR, et al. (2010) MDM2 antagonist nutlin plus proteasome inhibitor velcade combination displays a synergistic anti-myeloma activity. Cancer Biol Ther 9: 936-944.
8. Issaeva N, Bozko P, Enge M, Protopopova M, Verhoef LG, et al. (2004) Small molecule RITA binds to p53, blocks p53-HDM-2 interaction and activates p53 function in tumors. Nat Med 10: 1321-1328.
9. Saha MN, Jiang H, Muaki A, Chang H, (2010) RITA inhibits multiple myeloma cell growth through induction of p53-mediated caspase-dependent apoptosis and synergistically enhances nutlin-induced cytotoxic responses. Mol Cancer Ther 9: 3041-3051.
10. Rinaldo C, Prodosmo A, Siepi F, Moncada A, Sacchi A, et al. (2009) HIPK2 regulation by MDM2 determines tumor cell response to the p53-reactivating drugs nutlin-3 and RITA. Cancer Res 69: 6241-6248.
11. Enge M, Bao W, Hedström E, Jackson SP, Moumen A, et al. (2009) MDM2-dependent downregulation of p21 and hnRNP K provides a switch between apoptosis and growth arrest induced by pharmacologically activated p53. Cancer Cell 15: 171-183.
12. Grinkevich VV, Nikulenkov F, Shi Y, Enge M, Bao W, et al. (2009) Ablation of Key oncogenic pathways by RITA-reactivated p53 is required for efficient apoptosis. Cancer Cell 15: 441-453.
13. Krajewski M, Ozdowy P, D'Silva L, Rothweiler U, Holak TA, (2005) NMR indicates that the small molecule RITA does not block p53-MDM2 binding in vitro. Nat Med 11: 1135-1136.
14. Fuchs SY, Adler V, Buschmann T, Yin Z, Wu X, et al. (1998) JNK targets p53 ubiquitination and degradation in nonstressed cells. Genes Dev 12: 2658-2663.
15. Fuchs SY, Adler V, Pincus MR, Ronai Z, (1998) MEKK1/JNK signaling stabilizes and activates p53. Proc Natl Acad Sci USA 95: 10541-10546.
16. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, et al. (1994) The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369: 156-160.
17. Shaulian E, Karin M, (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4: E131-E136.
18. Fan M, Goodwin ME, Birrer MJ, Chambers TC, (2001) The c-Jun NH(2)-terminal protein kinase/AP-1 pathway is required for efficient apoptosis induced by vinblastine. Cancer Res 61: 4450-4458.
19. Schroeter H, Boyd CS, Ahmed R, Spencer JP, Duncan RF, et al. (2003) c-Jun N-terminal kinase (JNK)-mediated modulation of brain mitochondria function: new target proteins for JNK signalling in mitochondrion-dependent apoptosis. Biochem J 372: 359-369.
20. Adler V, Pincus MR, Minamoto T, Fuchs SY, Bluth MJ, et al. (1997) Conformation-dependent phosphorylation of p53. Proc Natl Acad Sci USA 94: 1686-1691.
21. Hideshima T, Mitsiades C, Akiyama M, Hayashi T, Chauhan D, et al. (2003) Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood 101: 1530-1534.
22. Anderson KC, (2005) Lenalidmide and thalidomide: mechanisms of action: similarities and differences. Semin Hematol 42: S3-S8.
23. Hideshima T, Catley L, Yasui H, Ishitsuka K, Raje N, et al. (2006) Perifosine, an oral bioactive novel alkylphospholipid, inhibits Akt and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells. Blood 107: 4053-4062.
24. Kobayashi T, Kuroda J, Ashihara E, Oomizu S, Terui Y, et al. (2010) Galectin-9 exhibits anti-myeloma activity through JNK and p38 MAP kinase pathways. Leukemia 24: 843-850.
25. Carew JS, Nawrocki ST, Reddy VK, Bush D, Rehg JE, et al. (2008) The novel polyamine analogue CGC-11093 enhanced the anti-myeloma activity of bortezomib. Cancer Res 68: 4783-4790.
26. Chen L, Wang S, Zhou Y, Wu X, Entin I, et al. (2010) Identification of early growth response protein 1 (EGR-1) as a novel target for JUN-induced apoptosis in multiple myeloma. Blood 115: 61-70.
27. Schreiber M, Kolbus A, Piu F, Szabowski A, Möhle-Steinlein U, et al. (1999) Control of cell cycle progression by c-JUN is p53 dependent. Genes Dev 13: 607-619.
28. Zhao CY, Szekely L, Bao W, Selivanova G, (2010) Rescue of p53 function by small-molecule RITA in cervical carcinoma by blocking E6-mediated degradation. Cancer Res 70: 3372-3381.
29. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, et al. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 98: 13681-13686.
30. Ginsberg D, Oren M, Yaniv M, Piette J, (1990) Protein binding elements in the promoter region of the mouse p53 gene. Oncogene 5: 1285-1290.
31. Zhang JP, Wong CK, Lam CW, (2000) Role of caspases in dexamethasone-induced apoptosis and activation of c-Jun NH2-terminal kinase and p38 mitogen-activated protein kinase in human eosinophils. Clin Exp Immunol 122: 20-27.
32. Zou W, Yue P, Khuri FR, Sun SY, (2008) Coupling of endoplasmic reticulum stress to CDDO-Me-induced up-regulation of death receptor 5 via a CHOP-dependent mechanism involving JNK activation. Cancer Res 68: 7484-7492.
33. Singh AV, Bandi M, Raje N, Richardson P, Palladino MA, et al. (2011) A novel vascular disrupting agent plinabulin triggers JNK-mediated apoptosis and inhibits angiogenesis in multiple myeloma cells. 117: 5692-5700.
34. Behrens A, Sibilia M, Wagner EF, (1999) Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet 21: 326-329.
35. Raab MS, Breitkreutz I, Tonon G, Zhang J, Hayden PJ, et al. (2009) Targeting PKC: a novel role for beta-catenin in ER stress and apoptotic signaling. Blood 113: 1513-1521.
36. Zhang H, Shi X, Zhang QJ, Hampong M, Paddon H, et al. (2002) Nocodazole-induced p53-dependent c-Jun N-terminal kinase activation reduces apoptosis in human colon carcinoma HCT116 cells. J Biol Chem 277: 43648-43658.
37. Milne DM, Campbell LE DG, Meek DW, (1995) p53 phosphorylated in vitro and in vivo by an ultraviolet radiation-induced protein kinase characteristic of the c-Jun kinase, JNK1. J Biol Chem 270: 5511-5518.
38. Buschmann T, Potapova O, Bar-Shira A, Ivanov VN, Fuchs SY, et al. (2001) JUN NH2-terminal kinase phosphorylation of p53 on Thr-81 is important for p53 stabilization and transcriptional activities in response to stress. Mol Cell Biol 21: 2743-2754.
39. Shimada K, Nakamura M, Ishida E, Kishi M, Konishi N, (2003) Roles of p38- and c-jun NH2-terminal-kinase-mediated pathways in 2-methoxyestradiol-induced p53 induction and apoptosis. Carcinogenesis 24: 1067-1075.
40. Nahi H, Selivanova G, Lehmann S, Möllgård L, Bengtzen S, et al. (2008) Mutated and non-mutated TP53 as targets in the treatment of leukaemia. Br J Haematol 141: 445-453.
41. Barré B, Vigneron A, Coqueret O, (2005) The STAT3 transcription factor is a target for the Myc and riboblastoma proteins on the Cdc25A promoter. J Biol Chem 280: 15673-15681.
42. She QB, Ma WY, Dong Z, (2002) Role of MAP kinases in UVB-induced phosphorylation of p53 at serine 20. Oncogene 21: 1580-1589.