Computational prediction and experimental validation of a novel synthesized pan-PIM inhibitor PI003 and its apoptosis-inducing mechanisms in cervical cancer

Oncotarget

Volumn 6, Issue 10, 2015, Pages 8019-8035

  Liu, Zhongyu ^a   He, Weihua ^a   Gao, Jianglin ^a   Luo, Junhua ^a   Huang, Xian ^a   Gao, Chunfang ^a  

^a Institute of Anal Colorectal Surgery   (China)

Author keywords

Apoptosis; HeLa cell; MicroRNA; Pan PIM inhibitor (PI003); PIM kinase family

Indexed keywords

ANTINEOPLASTIC AGENT; BETA ACTIN; CASPASE 3; CASPASE 8; CASPASE 9; HEAT SHOCK PROTEIN 90; MICRORNA; PI 003; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN KINASE; PROTEIN KINASE PIM 1; PROTEIN KINASE PIM 2; PROTEIN KINASE PIM 3; UNCLASSIFIED DRUG; MOLECULAR LIBRARY; PROTEIN KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CELL MIGRATION; CONTROLLED STUDY; DIMERIZATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG PROTEIN BINDING; DRUG STRUCTURE; DRUG SYNTHESIS; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYDROGEN BOND; IN VIVO STUDY; LOW DRUG DOSE; MATHEMATICAL COMPUTING; MICROARRAY ANALYSIS; MITOCHONDRION; MOLECULAR DOCKING; MOUSE; NONHUMAN; PREDICTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIMULATION; UTERINE CERVIX CANCER; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BAYES THEOREM; DRUG EFFECTS; DRUG SCREENING; ENZYMOLOGY; HELA CELL LINE; MOLECULAR LIBRARY; MOLECULAR MODEL; NUDE MOUSE; PATHOLOGY; PHARMACOLOGY; PHOSPHORYLATION; TUMOR CELL LINE; UTERINE CERVICAL NEOPLASMS;

ANIMALS; APOPTOSIS; BAYES THEOREM; CELL LINE, TUMOR; FEMALE; HELA CELLS; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-PIM-1; SMALL MOLECULE LIBRARIES; UTERINE CERVICAL NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84928381869     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3139     Document Type: Article

References (53)

1. Brault L, Gasser C, Bracher F, Huber K, Knapp S, Schwaller J. PIM serine/threonine kinases in the pathogenesis and therapy of hematologic malignancies and solid cancers. Haematologica. 2010; 95:1004-1015.
2. Eichmann A, Yuan L, Breant C, Alitalo K, Koskinen PJ. Developmental expression of pim kinases suggests functions also outside of the hematopoietic system. Oncogene. 2000; 19:1215-1224.
3. Bachmann M, Moroy T. The serine/threonine kinase Pim-1. Int J Biochem Cell Biol. 2005; 37:726-730.
4. Amaravadi R, Thompson CB. The survival kinases Akt and Pim as potential pharmacological targets. J Clin Invest. 2005; 115:2618-2624.
5. Nawijn MC, Alendar A, Berns A. For better or for worse: The role of Pim oncogenes in tumorigenesis. Nat Rev Cancer. 2011; 11:23-34.
6. Wang Z, Bhattacharya N, Weaver M, Petersen K, Meyer M, Gapter L, Magnuson NS. Pim-1: A serine/threonine kinase with a role in cell survival, proliferation, differentiation and tumorigenesis. J Vet Sci. 2001; 2:167-179.
7. Chen J, Kobayashi M, Darmanin S, Qiao Y, Gully C, Zhao R, et al. Hypoxia mediated up-regulation of Pim-1 contributes to solid tumor formation. Am J Pathol. 2009; 175:400-11.
8. Narlik-Grassow M, Blanco-Aparicio C, Cecilia Y, Peregrina S, Serelde BG, Munoz-Galvan S, et al. Essential role of PIM kinases in sarcoma growth and bone invasion. Carcinogenesis. 2012; 33:1479-86.
9. Wen X, Wu JM, Wang FT, Liu B, Huang CH. Free Radical Bio Med!. 2013; 65:402-410.
10. Reiser-Erkan C, Erkan M, Pan Z, Bekasi S, Giese NA, Streit S, et al. Hypoxiainducible proto-oncogene Pim-1 is a prognostic marker in pancreatic ductal adenocarcinoma. Cancer Biol Ther. 2008; 7:1352-9.
11. Morwick T. a survey of the patent literature. Expert Opin Ther Pat. 2010; 20:193-212.
12. Pogacic V, Bullock AN, Fedorov O, Filippakopoulos P, Gasser C, Biondi A, et al. Structural analysis identifies imidazo[1,2-b]pyridazines as PIM kinase inhibitors with in vitro antileukemic activity. Cancer Res. 2007; 67:6916-24.
13. Blanco-Aparicio C, Collazo AM, Oyarzabal J, Leal JF, Albaran MI, Lima FR, et al. Pim 1 kinase inhibitor ETP-45299 suppresses cellular proliferation and synergizes with PI3K inhibition. Cancer Lett. 2011; 300:145-53.
14. Carmen BA, Amancio C. Pim kinases in cancer: Diagnostic, prognostic and treatment opportunities. Biochemical Pharmacology. 2013; 85:629-643.
15. Popivanova BK, Li YY, Zheng H, et al. Protooncogene, Pim-3 with serine/threonine kinase activity, is aberrantly expressed in human colon cancer cells and can prevent Badmediated apoptosis. Cancer Sci. 2007; 98:321-328.
16. Pierre F, Stefan E, Nédellec AS, Chevrel MC, Collin F, Regan, et al. 7-(4H-1,4-Triazol-3-yl)benzoc.2,6.naphthyridines: A novel class of Pim kinase inhibitors with potent cell antiproliferative activity. Bioorganic and Medicinal Chemistry Letters. 2011; 21:6687-6692.
17. Michael P, Dwyera, Kartik K, Kamil P, Carmen A, Marc L, et al. Discovery of pyrazolo1,5-a.pyrimidine-based Pim inhibitors: A template-based approach. Bioorganic and Medicinal Chemistry Letters. 2013; 23:6178-6182.
18. Dakin LA, Block MH, Chen HW, Code E, Dowling JE, Feng XM, et al. Discovery of novel benzylidene-1, 3-thiazolidine-2,4-diones as potent and selective inhibitors of the PIM-1, PIM-2, and PIM-3 protein kinases. Bioorganic and Medicinal Chemistry Letters. 2012; 22:4599-4604.
19. Haddach M, Michaux J, Schwaebe MK, Pierre F, O'Brien SE, Borsan C. Discovery of CX-6258. A potent, selective, and orally efficacious pan-Pim kinases inhibitor. ACS Med Chem Lett. 2012; 3:135-139.
20. Garcia PD, Langowski JL, Wang YY, Chen M, Castillo J, Fanton C. Pan-PIM kinase inhibition provides a novel therapy for treating hematologic cancers. Clin Cancer Res. 2014; 20:1834-1845.
21. Lisa SC, Sanjeev R, David B, William G, Wierda G. Pim kinase inhibitor, SGI-1776, induces apoptosis in chronic lymphocytic leukemia cells. Blood. 2009; 114:4150-4157.
22. Erika KK, Kristen M, Keith SD, Sangeetha P, Cao YC, et al. AZD1208, a potent and selective pan-Pim kinase inhibitor, demonstrates efficacy in preclinical models of acute myeloid leukemia. Blood. 2014; 123:905-913.
23. Mishra GR, Suresh M, Kumaran K, Kannabiran N, Suresh S, Bala P, et al. Human protein reference database-2006 update. Nucleic Acids Research. 2006; 34:411-414.
24. Alfarano C, Andrade CE, Anthony K, Bahroos N, Bajec M, Bantoft K, et al. The Biomolecular Interaction Network Database and related tools 2005 update. Nucleic Acids Research. 2005; 33:418-424.
25. Xenarios I, Salwinski L, Duan XJ, Higney P, Kim SM, Eisenberg D. DIP, the Database of Interacting Proteins: a research tool for studying cellular networks of protein interactions. Nucleic Acids Research. 2002; 30:303-305.
26. Mewes HW, Frishman D, Güldener U, Mannhaupt G, Mayer K, Mokrejs M, Morgenstern B, Münsterkötter M, Rudd S, Weil B. MIPS: a database for genomes and protein sequences. Nucleic Acids Research. 2002; 30:31-4.
27. Kerrien S, Alam-Faruque Y, Aranda B, Bancarz I, Bridge A, Derow C, et al. IntAct-open source resource for molecular interaction data. Nucleic Acids Research. 2007; 35:D561-D565.
28. Zhang QC, Petrey D, Garzón JI, Deng L, Honig B. PrePPI: a structure-informed database of protein-protein interactions. Nature. 2012; 490:556-560.
29. Wang N, Xu HL, Zhao X, Wen X, Wang FT, Wang SY, et al. Network-based identification of novel connections among apoptotic signaling pathways in cancer. Applied Biochemistry and Biotechnology. 2012; 167:621-631.
30. Baldi P, Brunak S, Chauvin Y, et al. Assessing the accuracy of prediction algorithms for classification: an overview, Bioinformatics. 2000; 16:412-424.
31. Liu B, Cheng Y, Zhang B, Bian HJ, Bao JK. Polygonatum cyrtonema lectin induces apoptosis and autophagy in human melanoma A375 cells through a mitochondriamediated ROS-p38-p53 pathway. Cancer Lett. 2009; 275:54-60.
32. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983; 65:55-63.
33. Wei J, Shi J, Zhang J, He G, Pan J, He J, et al. Ouyang, Design, synthesis and biological evaluation of enzymatically cleavable NSAIDs prodrugs derived from self-immolative dendritic scaffolds for the treatment of inflammatory diseases. Bioorg Med Chem. 2013; 21:192-200.
34. Ouyang L, Huang Y, Zhao Y, He G, Xie Y, Liu J, et al. Preparation, antibacterial evaluation and preliminary structure-activity relationship (SAR) study of benzothiazol-and benzoxazol-2-amine derivatives. Bioorg Med Chem Lett. 2012; 22:3044-3049.
35. Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, et al. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics. 2013; 29:845-854.
36. Zhang T, Xie N, He WF, Liu R, Lei YL, Tan H, et al. An integrated proteomics and bioinformatics analyses of Hepatitis B Virus X protein and identification of a novel interactor apoA-I. Journal of Proteomics. 2013; 84:92-105.
37. Schüttelkopf AW, Van Aalten DM. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes, ActaCrystallogr. D Biol. Crystallogr. 2004; 60:1355-1363.
38. Ouyang L, Chen Y, Wang XY, Lu RF, Zhang SY, Tian M, et al. Polygonatum odoratum lectin induces apoptosis and autophagy via targeting EGFR-mediated Ras-Raf-MEK-ERK pathway in human MCF-7 breast cells. Phytomedicine. 2014; 21:1658-1665.
39. May MJ, Madge LA. Caspase inhibition sensitizes inhibitor of NFkappaB kinase beta-deficient fibroblasts to caspaseindependent cell death via the generation of reactive oxygen species. J Biol Chem. 2007; 282:16105-16116.
40. Liu B, Wu JM, Li J, Li WW, Liu JJ, Li CY, et al. Polygonatum cyrtonema lectin induces murine fibrosarcoma L9 cell apoptosis and autophagy via blocking Ras-Raf and PI3K-Akt signaling pathways. Biochimie. 2010; 92:1934-1938.
41. Chen JS, Lin SC, Chen CY, Hsieh YT, Pai PH, Chen LK, et al. Development of a microarray for two rice subspecies: characterization and validation of gene expression in rice tissues. BMC Res. 2014; 8:7-15.
42. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to transcriptional responses to ionizing radiation. Proc Natl Acad Sci. 2001; 98:5116-5121.
43. Tan AC, Naiman DQ, Xu L, et al. Simple decision rules for classifying human cancers from gene expression profiles. Bioinformatics. 2005; 21:3896-3904.
44. Dweep H, Sticht C, Pandey P, Gretz N. miRWalk-database: prediction of possible miRNA binding sites by "walking" the genes of 3 genomes. Journal of Biomedical Informatics. 2011; 44:839-837.
45. Kiriakidou M, Nelson PT, Kouranov A, Fitziev P, Bouyioukos C, Mourelatos Z, et al. A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 2004; 18:1165-1178.
46. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human microRNA targets. PLoS Biol. 2004; 2:e363.
47. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al. Combinatorial microRNA target predictions. Nat Genet. 2005; 37:495-500.
48. Wang X. MiRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA. 2008; 14:1012-1017.
49. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. The role of site accessibility in microRNA target recognition. Nat Genet. 2007; 39:1278-1284.
50. Dweep H, Sticht C, Pandey P, Gretz N. miRWalk-database: prediction of possible miRNA binding sites by "walking" the genes of 3 genomes. Journal of Biomedical Informatics. 2011; 44:839-837.
51. Miranda KC, et al. A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell. 2006; 126:1203-1217.
52. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA. 2014; 10:1507-1517.
53. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005; 120:5-20.