Identification of a new class of MDM2 inhibitor that inhibits growth of orthotopic pancreatic tumors in mice

Gastroenterology

Volumn 147, Issue 4, 2014, Pages 893-902.e2

  Wang, Wei ^a   Qin, Jiang Jiang ^a   Voruganti, Sukesh ^a   Wang, Ming Hai ^a   Sharma, Horrick ^b   Patil, Shivaputra ^b   Zhou, Jianwei ^c   Wang, Hui ^d   Mukhopadhyay, Debabrata ^e   Buolamwini, John K ^b   Zhang, Ruiwen ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c NANJING MEDICAL UNIVERSITY   (China)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^e MAYO GRADUATE SCHOOL   (United States)

Author keywords

BCL2; Chemotherapy; P21; P53 Independent

Indexed keywords

CASPASE 3; CYCLIN E; CYTOTOXIC AGENT; LIGASE INHIBITOR; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN MDM2; PROTEIN P53; SP 141; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; 6-METHOXY-1-(NAPHTHALEN-1-YL)-9H-PYRIDO(3,4-B)INDOLE; ANTINEOPLASTIC AGENT; ENZYME INHIBITOR; INDOLE DERIVATIVE; MDM2 PROTEIN, HUMAN; PROTEASOME; PYRIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER REGRESSION; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL VIABILITY; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; ENZYME ACTIVITY; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; INHIBITION KINETICS; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; ORTHOTOPIC PANCREATIC TUMOR; PANCREAS TUMOR; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UBIQUITINATION; UPREGULATION; WILD TYPE; ADENOCARCINOMA; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; CHEMISTRY; DOSE RESPONSE; DRUG DESIGN; DRUG EFFECTS; DRUG SCREENING; ENZYMOLOGY; FEMALE; GENETIC TRANSFECTION; GENETICS; IC50; METABOLISM; MOLECULARLY TARGETED THERAPY; NUDE MOUSE; PANCREATIC NEOPLASMS; PATHOLOGY; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; TIME; TUMOR CELL LINE; TUMOR VOLUME;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DESIGN; ENZYME INHIBITORS; FEMALE; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; INDOLES; INHIBITORY CONCENTRATION 50; MICE; MICE, NUDE; MOLECULAR TARGETED THERAPY; PANCREATIC NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-MDM2; PYRIDINES; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TIME FACTORS; TRANSFECTION; TUMOR BURDEN; UBIQUITINATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84917680263     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.07.001     Document Type: Article

References (46)

1. R. Siegel, D. Naishadham, and A. Jemal Cancer statistics, 2013 CA Cancer J Clin 63 2013 11 30
2. A.S. Paulson, H.S. Tran Cao, and M.A. Tempero Therapeutic advances in pancreatic cancer Gastroenterology 144 2013 1316 1326
3. A.N. Shah, J.M. Summy, and J. Zhang Development and characterization of gemcitabine-resistant pancreatic tumor cells Ann Surg Oncol 14 2007 3629 3637
4. M. Hidalgo Pancreatic cancer N Engl J Med 362 2010 1605 1617
5. Z. Wang, Y. Li, and A. Ahmad Pancreatic cancer: understanding and overcoming chemoresistance Nat Rev Gastroenterol Hepatol 8 2011 27 33
6. J.D. Oliner, J.A. Pietenpol, and S. Thiagalinggam Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53 Nature 362 1993 857 860
7. M.H. Kubbutat, S.N. Jones, and K.H. Vousden Regulation of p53 stability by Mdm2 Nature 387 1997 299 303
8. R. Honda, H. Tanaka, and H. Yasuda Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53 FEBS Lett 420 1997 25 27
9. Y. Haupt, R. Maya, and A. Kazaz Mdm2 promotes the rapid degradation of p53 Nature 387 1997 296 299
10. E.R. Rayburn, S.J. Ezell, and R. Zhang Recent advances in validating MDM2 as a cancer target Anticancer Agents Med Chem 9 2009 882 903
11. R. Zhang, and H. Wang MDM2 Oncogene as a novel target for human cancer therapy Curr Pharm Des 6 2000 393 416
12. E. Rayburn, R. Zhang, and J. He MDM2 and human malignancies: expression, clinical pathology, prognostic markers, and implications for chemotherapy Curr Cancer Drug Targets 5 2005 27 42
13. W. Wang, and Y. Hu Small molecule agents targeting the p53-MDM2 pathway for cancer therapy Med Res Rev 32 2012 1159 1196
14. S. Shangary, and S. Wang Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: a novel approach for cancer therapy Annu Rev Pharmacol Toxicol 49 2009 223 241
15. Q. Li, and G. Lozano Molecular pathways: targeting Mdm2 and Mdm4 in cancer therapy Clin Cancer Res 19 2013 34 41
16. L.T. Vassilev, B.T. Vu, and B. Graves In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 303 2004 844 848
17. N. Issaeva, P. Bozko, and M. Enge Small molecule RITA binds to p53, blocks p53-HDM-2 interaction and activates p53 function in tumors Nat Med 10 2004 1321 1328
18. S. Shangary, D. Qin, and D. McEachern Temporal activation of p53 by a specific MDM2 inhibitor is selectively toxic to tumors and leads to complete tumor growth inhibition Proc Natl Acad Sci U S A 105 2008 3933 3938
19. A. Scarpa, P. Capelli, and K. Mukai Pancreatic adenocarcinomas frequently show p53 gene mutations Am J Pathol 142 1993 1534 1543
20. Z. Zhang, and R. Zhang p53-independent activities of MDM2 and their relevance to cancer therapy Curr Cancer Drug Targets 5 2005 9 20
21. J.J. Qin, S. Nag, and S. Voruganti Natural product MDM2 inhibitors: anticancer activity and mechanisms of action Curr Med Chem 19 2012 5705 5725
22. D.A. Vargas, S. Takahashi, and Z. Ronai Mdm2: a regulator of cell growth and death Adv Cancer Res 89 2003 1 34
23. A. Bouska, T. Lushnikova, and S. Plaza Mdm2 promotes genetic instability and transformation independent of p53 Mol Cell Biol 28 2008 4862 4874
24. L. Gu, N. Zhu, and H. Zhang Regulation of XIAP translation and induction by MDM2 following irradiation Cancer Cell 15 2009 363 375
25. W. Fu, Q. Ma, and L. Chen MDM2 acts downstream of p53 as an E3 ligase to promote FOXO ubiquitination and degradation J Biol Chem 284 2009 13987 14000
26. N. Vlatkovic, S. Guerrera, and Y. Li MDM2 interacts with the C-terminus of the catalytic subunit of DNA polymerase epsilon Nucleic Acids Res 28 2000 3581 3586
27. H. Asahara, Y. Li, and J. Fuss Stimulation of human DNA polymerase epsilon by MDM2 Nucleic Acids Res 31 2003 2451 2459
28. M. Burmakin, Y. Shi, and E. Hedström Dual targeting of wild-type and mutant p53 by small molecule RITA results in the inhibition of N-Myc and key survival oncogenes and kills neuroblastoma cells in vivo and in vitro Clin Cancer Res 19 2013 5092 5103
29. S. Nag, J. Qin, and K. Srivenugopal The MDM2-p53 pathway revisited J Biomed Res 27 2013 254 271
30. W. Wang, E.R. Rayburn, and Y. Zhao Novel ginsenosides 25-OH-PPD and 25-OCH3-PPD as experimental therapy for pancreatic cancer: anticancer activity and mechanisms of action Cancer Lett 278 2009 241 248
31. X.R. Zhang, H. Xu, and X. Zhang Preclinical evaluation of anticancer efficacy and pharmacological properties of FBA-TPQ, a novel synthetic makaluvamine analog Marine Drugs 10 2012 1138 1155
32. W. Wang, L. Ao, and E.R. Rayburn KCN1, a novel synthetic sulfonamide anticancer agent: in vitro and in vivo anti-pancreatic cancer activities and preclinical pharmacology PLoS ONE 7 2012 e44883
33. S.S. Padhye, S. Guin, and H.P. Yao Sustained expression of the RON receptor tyrosine kinase by pancreatic cancer stem cells as a potential targeting moiety for antibody-directed chemotherapeutics Mol Pharm 8 2011 2310 2319
34. M.H. Muders, P.K. Vohra, and S.K. Dutta Targeting GIPC/synectin in pancreatic cancer inhibits tumor growth Clin Cancer Res 15 2009 4095 4103
35. L. Chen, S. Agrawal, and W. Zhou Synergistic activation of p53 by inhibition of MDM2 expression and DNA damage Proc Natl Acad Sci U S A 95 1998 195 200
36. Z. Zhang, M. Li, and H. Wang Antisense therapy targeting MDM2 oncogene in prostate cancer: Effects on proliferation, apoptosis, multiple gene expression, and chemotherapy Proc Natl Acad Sci U S A 100 2003 11636 11641
37. R. Zhang, H. Wang, and S. Agrawal Novel antisense anti-MDM2 mixed-backbone oligonucleotides: proof of principle, in vitro and in vivo activities, and mechanisms Curr Cancer Drug Targets 5 2005 43 50
38. Z. Zhang, H. Wang, and M. Li Novel MDM2 p53-independent functions identified through RNA silencing technologies Ann NY Acad Sci 1058 2005 205 214
39. M. Li, Z. Zhang, and D.L. Hill Genistein, a dietary isoflavone, down-regulates the MDM2 oncogene at both transcriptional and posttranslational levels Cancer Res 65 2005 8200 8208
40. M. Li, Z. Zhang, and D.L. Hill Curcumin, a dietary component, has anticancer, chemosensitization, and radiosensitization effects by down-regulating the MDM2 oncogene through the PI3K/mTOR/ETS2 pathway Cancer Res 67 2007 1988 1996
41. W. Wang, E.R. Rayburn, and S.E. Velu In vitro and in vivo anti-cancer activity of novel synthetic makaluvamine analogs Clin Cancer Res 15 2009 3511 3518
42. 3-PPD inhibits breast cancer growth and metastasis through down-regulating MDM2 PLoS One 7 2012 e41586
43. X. Zhang, W. Wang, and H. Wang Identification of ribosomal protein S25 (RPS25)-MDM2-p53 regulatory feedback loop Oncogene 32 2013 2782 2791
44. D. Menendez, A. Inga, and M.A. Resnick The expanding universe of p53 targets Nat Rev Cancer 9 2009 724 737
45. K.H. Vousden, and C. Prives Blinded by the light: the growing complexity of p53 Cell 137 2009 413 431
46. J. Momand, D. Jung, and S. Wilczynski The MDM2 gene amplification database Nucleic Acids Res 26 1998 3453 3459