Targeting Btk/Etk of prostate cancer cells by a novel dual inhibitor

Cell Death and Disease

Volumn 5, Issue 9, 2014, Pages

  Guo, W ^a   Liu, R ^a   Bhardwaj, G ^a   Yang, J C ^b   Changou, C ^a   Ma, A H ^a   Mazloom, A ^a   Chintapalli, S ^a   Xiao, K ^a   Xiao, W ^a   Kumaresan, P ^a   Sanchez, E ^a   Yeh, C T ^c   Evans, C P ^b   Patterson, R ^a   Lam, K S ^a   Kung, H J ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d National Health Research Institutes NHRI   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

3ATA; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; ANTINEOPLASTIC AGENT; BRUTON TYROSINE KINASE; BRUTON TYROSINE KINASE INHIBITOR; CTN 06; DOCETAXEL; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; LMF A 13; MICRORNA; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; RAF PROTEIN; SARACATINIB; SORAFENIB; TYROSINE KINASE ETK; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR; AGAMMAGLOBULINAEMIA TYROSINE KINASE; BMX PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; N-(7-ISOBUTYL-6-OXO-1-(3-(PIPERIDIN-1-YL)PROPYL)-5,6-DIHYDRO-1H-IMIDAZO(4,5-G)QUINOXALIN-2-YL)-4-(PYRIDIN-4-YL)BENZAMIDE; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE B; PROTEIN KINASE INHIBITOR; QUINOXALINE DERIVATIVE; SMALL INTERFERING RNA; STAT3 PROTEIN; TAXOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER GRADING; CANCER INHIBITION; CANCER TISSUE; CELL KILLING; CELL MIGRATION; CONTROLLED STUDY; DRUG POTENCY; DRUG STRUCTURE; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; IC50; IMMORTALIZED CELL LINE; IN VIVO STUDY; MALE; MOUSE; MOUSE MODEL; NONHUMAN; PATIENT CARE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROSTATE EPITHELIUM CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; WOUND HEALING; ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MOLECULAR DOCKING; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; BINDING SITES; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; IMIDAZOLES; MALE; MICE; MICE, NUDE; MOLECULAR DOCKING SIMULATION; PHOSPHOLIPASE C GAMMA; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; QUINOXALINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; STAT3 TRANSCRIPTION FACTOR; TAXOIDS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84927737139     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.343     Document Type: Article

References (61)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T et al. Cancer statistics 2008. CA Cancer J Clin 2008; 58: 71-96.
2. Stommel JM, Kimmelman AC, Ying H, Nabioullin R, Ponugoti AH, Wiedemeyer R et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 2007; 318: 287-290.
3. Honda F, Kano H, Kanegane H, Nonoyama S, Kim ES, Lee SK et al. The kinase Btk negatively regulates the production of reactive oxygen species and stimulation-induced apoptosis in human neutrophils. Nat Immunol 2012; 13: 369-378.
4. Conley ME, Dobbs AK, Farmer DM, Kilic S, Paris K, Grigoriadou S et al. Primary B cell immunodeficiencies: comparisons and contrasts. Annu Rev Immunol 2009; 27: 199-227.
5. Gray P, Dunne A, Brikos C, Jefferies CA, Doyle SL, O'Neill LA. MyD88 adapter-like (Mal) is phosphorylated by Bruton's tyrosine kinase during TLR2 and TLR4 signal transduction. J Biol Chem 2006; 281: 10489-10495.
6. Khare A, Viswanathan B, Gund R, Jain N, Ravindran B, George A et al. Role of Bruton's tyrosine kinase in macrophage apoptosis. Apoptosis 2011; 16: 334-346.
7. Herman SE, Gordon AL, Hertlein E, Ramanunni A, Zhang X, Jaglowski S et al. Bruton tyrosine kinase represents a promising therapeutic target for treatment of chronic lymphocytic leukemia and is effectively targeted by PCI-32765. Blood 2011; 117: 6287-6296.
8. Rushworth SA, Bowles KM, Barrera LN, Murray MY, Zaitseva L, MacEwan DJ. BTK inhibitor ibrutinib is cytotoxic to myeloma and potently enhances bortezomib and lenalidomide activities through NF-kB. Cell Signal 2013; 25: 106-112.
9. Mahajan S, Ghosh S, Sudbeck EA, Zheng Y, Downs S, Hupke M et al. Rational design and synthesis of a novel anti-leukemic agent targeting Bruton's tyrosine kinase (BTK), LFM-A13 [alpha-cyano-beta-hydroxy-beta-methyl-N-(2, 5-dibromophenyl)propenamide]. J Biol Chem 1999; 274: 9587-9599.
10. de Rooij MF, Kuil A, Geest CR, Eldering E, Chang BY, Buggy JJ et al. The clinically active BTK inhibitor PCI-32765 targets B-cell receptor-and chemokine-controlled adhesion and migration in chronic lymphocytic leukemia. Blood 2012; 119: 2590-2594.
11. Winer ES, Ingham RR, Castillo JJ. PCI-32765: a novel Bruton's tyrosine kinase inhibitor for the treatment of lymphoid malignancies. Expert Opin Investig Drugs 2012; 21: 355-361.
12. Chang BY, Huang MM, Francesco M, Chen J, Sokolove J, Magadala P et al. The Bruton tyrosine kinase inhibitor PCI-32765 ameliorates autoimmune arthritis by inhibition of multiple effector cells. Arthritis Res Ther 2011; 13: R115.
13. Tai YT, Chang BY, Kong SY, Fulciniti M, Yang G, Calle Y et al. Bruton tyrosine kinase inhibition is a novel therapeutic strategy targeting tumor in the bone marrow microenvironment in multiple myeloma. Blood 2012; 120: 1877-1887.
14. Guo S, Sun F, Guo Z, Li W, Alfano A, Chen H, Magyar CE et al. Tyrosine kinase ETK/BMX is up-regulated in bladder cancer and predicts poor prognosis in patients with cystectomy. PLoS One 2011; 6: e17778.
15. Zhang Z, Zhu W, Zhang J, Guo L. Tyrosine kinase Etk/BMX protects nasopharyngeal carcinoma cells from apoptosis induced by radiation. Cancer Biol Ther 2011; 11: 690-698.
16. Guo L, Guo Y, Xiao S. Expression of tyrosine kinase Etk/Bmx and its relationship with AP-1-and NF-kappaB-associated proteins in hepatocellular carcinoma. Oncology 2007; 72: 410-416.
17. Xue LY, Qiu Y, He J, Kung HJ, Oleinick NL. Etk/Bmx, a PH-domain containing tyrosine kinase, protects prostate cancer cells from apoptosis induced by photodynamic therapy or thapsigargin. Oncogene 1999; 18: 3391-3398.
18. Chang YM, Kung HJ, Evans CP. Nonreceptor tyrosine kinases in prostate cancer. Neoplasia 2007; 9: 90-100.
19. Dai B, Kim O, Xie Y, Guo Z, Xu K, Wang B et al. Tyrosine kinase Etk/BMX is up-regulated in human prostate cancer and its overexpression induces prostate intraepithelial neoplasia in mouse. Cancer Res 2006; 66: 8058-8064.
20. Holopainen T, López-Alpuche V, Zheng W, Heljasvaara R, Jones D, He Y et al. Deletion of the endothelial Bmx tyrosine kinase decreases tumor angiogenesis and growth. Cancer Res 2012; 72: 3512-3521.
21. Lee LF, Guan J, Qiu Y, Kung HJ. Neuropeptide-induced androgen independence in prostate cancer cells: roles of nonreceptor tyrosine kinases Etk/Bmx, Src, and focal adhesion kinase. Mol Cell Biol 2001; 21: 8385-8397.
22. Chen R, Kim O, Li M, Xiong X, Guan JL, Kung HJ et al. Regulation of the PH-domaincontaining tyrosine kinase Etk by focal adhesion kinase through the FERM domain. Nat Cell Biol 2001; 3: 439-444.
23. Jiang X, Borgesi RA, McKnight NC, Kaur R, Carpenter CL, Balk SP. Activation of nonreceptor tyrosine kinase Bmx/Etk mediated by phosphoinositide 3-kinase, epidermal growth factor receptor, and ErbB3 in prostate cancer cells. J Biol Chem 2007; 282: 32689-32698.
24. Qiu Y, Robinson D, Pretlow TG, Kung HJ. Etk/Bmx, a tyrosine kinase with a pleckstrinhomology domain, is an effector of phosphatidylinositol 3'-kinase and is involved in interleukin 6-induced neuroendocrine differentiation of prostate cancer cells. Proc Natl Acad Sci USA 1998; 95: 3644-3649.
25. Jiang T, Guo Z, Dai B, Kang M, Ann DK, Kung HJ et al. Bi-directional regulation between tyrosine kinase Etk/BMX and tumor suppressor p53 in response to DNA damage. J Biol Chem 2004; 279: 50181-50189.
26. Guryanova OA, Wu Q, Cheng L, Lathia JD, Huang Z, Yang J et al. Nonreceptor tyrosine kinase BMX maintains self-renewal and tumorigenic potential of glioblastoma stem cells by activating STAT3. Cancer Cell 2011; 19: 498-511.
27. Chau CH, Chen KY, Deng HT, Kim KJ, Hosoya K, Terasaki T et al. Coordinating Etk/Bmx activation and VEGF upregulation to promote cell survival and proliferation. Oncogene 2002; 21: 8817-8829.
28. Lou Y, Owens TD, Kuglstatter A, Kondru RK, Goldstein DM. Bruton's tyrosine kinase inhibitors: approaches to potent and selective inhibition, preclinical and clinical evaluation for inflammatory diseases and B cell malignancies. J Med Chem 2012; 55: 4539-4550.
29. Kuglstatter A, Wong A, Tsing S, Lee SW, Lou Y, Villasenõr AG et al. Insights into the conformational flexibility of Bruton's tyrosine kinase from multiple ligand complex structures. Protein Sci 2011; 20: 428-436.
30. Wu Z, Chang PC, Yang JC, Chu CY, Wang LY, Chen NT et al. Autophagy blockade sensitizes prostate cancer cells towards Src family kinase inhibitors. Genes Cancer 2010; 1: 40-49.
31. Tsai YT, Su YH, Fang SS, Huang TN, Qiu Y, Jou YS et al. Etk, a Btk family tyrosine kinase, mediates cellular transformation by linking Src to STAT3 activation. Mol Cell Biol 2000; 20: 2043-2054.
32. Wang XY, Wu MH, Liu F, Li Y, Li N, Li GY et al. Differential miRNA expression and their target genes between NGX6-positive and negative colon cancer cells. Mol Cell Biochem 2010; 345: 283-290.
33. Gattolliat CH, Thomas L, Ciafrè SA, Meurice G, Le Teuff G, Job B et al. Expression of miR-487b and miR-410 encoded by 14q32.31 locus is a prognostic marker in neuroblastoma. Br J Cancer 2011; 105: 1352-1361.
34. Zhang S, Hao J, Xie F, Hu X, Liu C, Tong J et al. Downregulation of miR-132 by promoter methylation contributes to pancreatic cancer development. Carcinogenesis 2011; 32: 1183-1189.
35. Formosa A, Lena AM, Markert EK, Cortelli S, Miano R, Mauriello A et al. DNA methylation silences miR-132 in prostate cancer. Oncogene 2013; 32: 127-134.
36. Navarro A, Diaz T, Martinez A, Gaya A, Pons A, Gel B et al. Regulation of JAK2 by miR-135a: prognostic impact in classic Hodgkin lymphoma. Blood 2009; 114: 2945-2951.
37. Wang WL, Chatterjee N, Chittur SV, Welsh J, Tenniswood MP. Effects of 1a,25 dihydroxyvitamin D3 and testosterone on miRNA and mRNA expression in LNCaP cells. Mol Cancer 2011; 10: 58.
38. Zhang Y, Liao JM, Zeng SX, Lu H. p53 downregulates Down syndrome-associated DYRK1A through miR-1246. EMBO Rep 2011; 12: 811-817.
39. Kim WK, Park M, Kim YK, Tae YK, Yang HK, Lee JM et al. MicroRNA-494 downregulates KIT and inhibits gastrointestinal stromal tumor cell proliferation. Clin Cancer Res 2011; 17: 7584-7594.
40. Ghisi M, Corradin A, Basso K, Frasson C, Serafin V, Mukherjee S et al. Modulation of microRNA expression in human T-cell development: targeting of NOTCH3 by miR-150. Blood 2011; 117: 7053-7062.
41. Wang B, Li W, Guo K, Xiao Y, Wang Y, Fan J. miR-181b promotes hepatic stellate cells proliferation by targeting p27 and is elevated in the serum of cirrhosis patients. Biochem Biophys Res Commun 2012; 421: 4-8.
42. Hu H, Du L, Nagabayashi G, Seeger RC, Gatti RA. ATM is down-regulated by N-Myc-regulated microRNA-421. Proc Natl Acad Sci USA 2010; 107: 1506-1511.
43. Zhang Y, Gong W, Dai S, Huang G, Shen X, Gao M et al. Downregulation of human farnesoid X receptor by miR-421 promotes proliferation and migration of hepatocellular carcinoma cells. Mol Cancer Res 2012; 10: 516-522.
44. Dai Y, Siemann DW. Constitutively active c-Met kinase in PC-3 cells is autocrineindependent and can be blocked by the Met kinase inhibitor BMS-777607. BMC Cancer 2012; 12: 1-98.
45. Xiong J, Du Q, Liang Z. Tumor-suppressive microRNA-22 inhibits the transcription of E-box-containing c-Myc target genes by silencing c-Myc binding protein. Oncogene 2010; 29: 4980-4988.
46. Lam KS, Salmon SE, Hersh EM, Hruby VJ, Kazmierski WM, Knapp RJ. A new type of synthetic peptide library for identifying ligand-binding activity. Nature 1991; 354: 82-84.
47. McDonald OB, Chen WJ, Ellis B, Hoffman C, Overton L, Rink M et al. A scintillation proximity assay for the Raf/MEK/ERK kinase cascade: high-throughput screening and identification of selective enzyme inhibitors. Anal Biochem 1999; 268: 318-329.
48. Wilhelm S, Carter C, Lynch M, Lowinger T, Dumas J, Smith RA et al. Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat Rev Drug Discov 2006; 5: 835-844.
49. Dai B, Chen H, Guo S, Yang X, Linn DE, Sun F et al. Compensatory upregulation of tyrosine kinase Etk/BMX in response to androgen deprivation promotes castration-resistant growth of prostate cancer cells. Cancer Res 2010; 70: 5587-5596.
50. Bagheri-Yarmand R, Mandal M, Taludker AH, Wang RA, Vadlamudi RK, Kung HJ et al. Etk/Bmx tyrosine kinase activates Pak1 and regulates tumorigenicity of breast cancer cells. J Biol Chem 2001; 276: 29403-29409.
51. Hur W, Velentza A, Kim S, Flatauer L, Jiang X, Valente D et al. Clinical stage EGFR inhibitors irreversibly alkylate Bmx kinase. Bioorg Med Chem Lett 2008; 18: 5916-5919.
52. Campos S, Hamid O, Seiden MV, Oza A, Plante M, Potkul RK et al. Multicenter, randomized phase II trial of oral CI-1033 for previously treated advanced ovarian cancer. J Clin Oncol 2005; 23: 5597-5604.
53. Yang JC, Bai L, Yap S, Gao AC, Kung HJ, Evans CP. Effect of the specific Src family kinase inhibitor saracatinib on osteolytic lesions using the PC-3 bone model. Mol Cancer Ther 2010; 9: 1629-1637.
54. van Bokhoven A, Varella-Garcia M, Korch C, Johannes WU, Smith EE, Miller HL et al. Molecular characterization of human prostate carcinoma cell lines. Prostate 2003; 57: 205-225.
55. Lou Q, Wu J, Lam KS. A protein kinase assay system for both acidic and basic peptides. Anal Biochem 1996; 235: 107-109.
56. Grosdidier A, Zoete V, Michielin O, Swiss Dock. a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Res 2011; 39: W270-W277.
57. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS et al. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 2009; 30: 2785-2791.
58. Solis FJ, Wets RJB. Minimization by random search techniques. Math Oper Res 1981; 6: 19-30.
59. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E et al. Scalable molecular dynamics with NAMD. J Comput Chem 2005; 26: 1781-1802.
60. Zoete V, Cuendet MA, Grosdidier A, Michielin O. SwissParam: a fast force field generation tool for small organic molecules. J Comput Chem 2011; 32: 2359-2368.
61. Grasso AW, Wen D, Miller CM, Rhim JS, Pretlow TG, Kung HJ. ErbB kinases and NDF signaling in human prostate cancer cells. Oncogene 1997; 15: 2705-2716.