A Small-Molecule Inhibitor of PIM Kinases as a Potential Treatment for Urothelial Carcinomas

Neoplasia (United States)

Volumn 16, Issue 5, 2014, Pages 403-412

  Foulks, Jason M ^a   Carpenter, Kent J ^b   Luo, Bai ^a   Xu, Yong ^a   Senina, Anna ^a   Nix, Rebecca ^a   Chan, Ashley ^a   Clifford, Adrianne ^a   Wilkes, Marcus ^a   Vollmer, David ^a   Brenning, Benjamin ^a   Merx, Shannon ^a   Lai, Shuping ^a   McCullar, Michael V ^a   Ho, Koc Kan ^a   Albertson, Daniel J ^c   Call, Lee T ^b   Bearss, Jared J ^d   Tripp, Sheryl ^e   Liu, Ting ^c   Stephens, Bret J ^b   Mollard, Alexis ^b   Warner, Steven L ^b   Bearss, David J ^b   Kanner, Steven B ^a   more..

^a ASTEX PHARMACEUTICALS   (United Kingdom)

^b Tolero Pharmaceuticals Inc   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF UTAH   (United States)

^e ARUP LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; POTASSIUM CHANNEL HERG; PROTEIN BAD; PROTEIN KINASE PIM 1; PROTEIN SERINE THREONINE KINASE INHIBITOR; TP 3654; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOMATED PATCH CLAMP; BLADDER CARCINOMA; CANCER CHEMOTHERAPY; CANCER GROWTH; CARCINOGENICITY; CARCINOMA CELL; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; CYTOLYSIS; DRUG BIOAVAILABILITY; DRUG HALF LIFE; DRUG MECHANISM; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; RETROSPECTIVE STUDY; SIGNAL TRANSDUCTION; TIME TO MAXIMUM PLASMA CONCENTRATION; TRANSITIONAL CELL CARCINOMA; TUMOR XENOGRAFT;

EID: 84920733820     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2014.05.004     Document Type: Article

References (61)

1. Cuypers HT, Selten G, Quint W, Zijlstra M, Maandag ER, Boelens W, van Wezenbeek P, Melief C, Berns A Murine leukemia virus-induced T-cell lymphomagenesis: integration of proviruses in a distinct chromosomal region. Cell 1984, 37:141-150.
2. Meeker TC, Nagarajan L, ar-Rushdi A, Rovera G, Huebner K, Croce CM Characterization of the human PIM-1 gene: a putative proto-oncogene coding for a tissue specific member of the protein kinase family. Oncogene Res 1987, 1:87-101.
3. Breuer ML, Cuypers HT, Berns A Evidence for the involvement of pim-2, a new common proviral insertion site, in progression of lymphomas. EMBO J 1989, 8:743-748.
4. Saris CJ, Domen J, Berns A The pim-1 oncogene encodes two related protein-serine/threonine kinases by alternative initiation at AUG and CUG. EMBO J 1991, 10:655-664.
5. Ragoussis J, Senger G, Mockridge I, Sanseau P, Ruddy S, Dudley K, Sheer D, Trowsdale J A testis-expressed Zn finger gene (ZNF76) in human 6p21.3 centromeric to the MHC is closely linked to the human homolog of the t-complex gene tcp-11. Genomics 1992, 14:673-679.
6. Feldman JD, Vician L, Crispino M, Tocco G, Marcheselli VL, Bazan NG, Baudry M, Herschman HR KID-1, a protein kinase induced by depolarization in brain. J Biol Chem 1998, 273:16535-16543.
7. Matikainen S, Sareneva T, Ronni T, Lehtonen A, Koskinen PJ, Julkunen I Interferon-alpha activates multiple STAT proteins and upregulates proliferation-associated IL-2Rα, c-myc, and pim-1 genes in human T cells. Blood 1999, 93:1980-1991.
8. Kottaridis PD, Gale RE, Frew ME, Harrison G, Langabeer SE, Belton AA, Walker H, Wheatley K, Bowen DT, Burnett AK, et al. The presence of a FLT3 internal tandem duplication in patients with acute myeloid leukemia (AML) adds important prognostic information to cytogenetic risk group and response to the first cycle of chemotherapy: analysis of 854 patients from the United Kingdom Medical Research Council AML 10 and 12 trials. Blood 2001, 98:1752-1759.
9. Mizuno K, Shirogane T, Shinohara A, Iwamatsu A, Hibi M, Hirano T Regulation of Pim-1 by Hsp90. Biochem Biophys Res Commun 2001, 281:663-669.
10. Pasqualucci L, Neumeister P, Goossens T, Nanjangud G, Chaganti RS, Küppers R, Dalla-Favera R Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 2001, 412:341-346.
11. 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.
12. Mikkers H, Allen J, Knipscheer P, Romeijn L, Hart A, Vink E, Berns A High-throughput retroviral tagging to identify components of specific signaling pathways in cancer. Nat Genet 2002, 32:153-159.
13. Zhu N, Ramirez LM, Lee RL, Magnuson NS, Bishop GA, Gold MR CD40 signaling in B cells regulates the expression of the Pim-1 kinase via the NF-κB pathway. J Immunol 2002, 168:744-754.
14. Fox CJ, Hammerman PS, Cinalli RM, Master SR, Chodosh LA, Thompson CB The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor. Genes Dev 2003, 17:1841-1854.
15. Gaidano G, Pasqualucci L, Capello D, Berra E, Deambrogi C, Rossi D, Maria Larocca L, Gloghini A, Carbone A, Dalla-Favera R Aberrant somatic hypermutation in multiple subtypes of AIDS-associated non-Hodgkin lymphoma. Blood 2003, 102:1833-1841.
16. Fathi AT, Arowojolu O, Swinnen I, Sato T, Rajkhowa T, Small D, Marmsater F, Robinson JE, Gross SD, Martinson M, et al. A potential therapeutic target for FLT3-ITD AML: PIM1 kinase. Leuk Res 2012, 36:224-231.
17. Guo S, Mao X, Chen J, Huang B, Jin C, Xu Z, Qiu S Overexpression of Pim-1 in bladder cancer. J Exp Clin Cancer Res 2010, 29:161.
18. Wang J, Anderson PD, Luo W, Gius D, Roh M, Abdulkadir SA Pim1 kinase is required to maintain tumorigenicity in MYC-expressing prostate cancer cells. Oncogene 2012, 31:1794-1803.
19. Beier UH, Weise JB, Laudien M, Sauerwein H, Görögh T Overexpression of Pim-1 in head and neck squamous cell carcinomas. Int J Oncol 2007, 30:1381-1387.
20. Decker S, Finter J, Forde A, Kissel S, Schwaller J, Mack TS, Kuhn A, Gray NS, Follo M, Jumaa H, et al. PIM kinases are essential for chronic lymphocytic leukemia cell survival (PIM2/3) and CXCR4 mediated microenvironmental interactions (PIM1). Mol Cancer Ther 2014, 13:1231-1245.
21. Lu J, Zavorotinskaya T, Dai Y, Niu XH, Castillo J, Sim J, Yu J, Wang Y, Langowski JL, Holash J, et al. Pim2 is required for maintaining multiple myeloma cell growth through modulating TSC2 phosphorylation. Blood 2013, 122:1610-1620.
22. Gómez-Abad C, Pisonero H, Blanco-Aparicio C, Roncador G, González-Menchén A, Martinez-Climent JA, Mata E, Rodríguez ME, Muñoz-González G, Sánchez-Beato M, et al. PIM2 inhibition as a rational therapeutic approach in B-cell lymphoma. Blood 2011, 118:5517-5527.
23. Cibull TL, Jones TD, Li L, Eble JN, Ann Baldridge L, Malott SR, Luo Y, Cheng L Overexpression of Pim-1 during progression of prostatic adenocarcinoma. J Clin Pathol 2006, 59:285-288.
24. Liu HT, Wang N, Wang X, Li SL Overexpression of Pim-1 is associated with poor prognosis in patients with esophageal squamous cell carcinoma. J Surg Oncol 2010, 102:683-688.
25. Warnecke-Eberz U, Bollschweiler E, Drebber U, Metzger R, Baldus SE, Hölscher AH, Mönig S Prognostic impact of protein overexpression of the proto-oncogene PIM-1 in gastric cancer. Anticancer Res 2009, 29:4451-4455.
26. Yang Q, Chen LS, Neelapu SS, Miranda RN, Medeiros LJ, Gandhi V Transcription and translation are primary targets of Pim kinase inhibitor SGI-1776 in mantle cell lymphoma. Blood 2012, 120:3491-3500.
27. Zippo A, De Robertis A, Serafini R, Oliviero S PIM1-dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation. Nat Cell Biol 2007, 9:932-944.
28. Zhang Y, Wang Z, Li X, Magnuson NS Pim kinase-dependent inhibition of c-Myc degradation. Oncogene 2008, 27:4809-4819.
29. Wang J, Kim J, Roh M, Franco OE, Hayward SW, Wills ML, Abdulkadir SA Pim1 kinase synergizes with c-MYC to induce advanced prostate carcinoma. Oncogene 2010, 29:2477-2487.
30. Magnuson NS, Wang Z, Ding G, Reeves R Why target PIM1 for cancer diagnosis and treatment?. Future Oncol 2010, 6:1461-1478.
31. Wierenga AT, Vellenga E, Schuringa JJ Maximal STAT5-induced proliferation and self-renewal at intermediate STAT5 activity levels. Mol Cell Biol 2008, 28:6668-6680.
32. Beharry Z, Zemskova M, Mahajan S, Zhang F, Ma J, Xia Z, Lilly M, Smith CD, Kraft AS Novel benzylidene-thiazolidine-2,4-diones inhibit Pim protein kinase activity and induce cell cycle arrest in leukemia and prostate cancer cells. Mol Cancer Ther 2009, 8:1473-1483.
33. Bullock AN, Russo S, Amos A, Pagano N, Bregman H, Debreczeni JE, Lee WH, von Delft F, Meggers E, Knapp S Crystal structure of the PIM2 kinase in complex with an organoruthenium inhibitor. PLoS One 2009, 4:e7112.
34. Chen LS, Redkar S, Bearss D, Wierda WG, Gandhi V Pim kinase inhibitor, SGI-1776, induces apoptosis in chronic lymphocytic leukemia cells. Blood 2009, 114:4150-4157.
35. Xia Z, Knaak C, Ma J, Beharry ZM, McInnes C, Wang W, Kraft AS, Smith CD Synthesis and evaluation of novel inhibitors of Pim-1 and Pim-2 protein kinases. J Med Chem 2009, 52:74-86.
36. Anizon F, Shtil AA, Danilenko VN, Moreau P Fighting tumor cell survival: advances in the design and evaluation of Pim inhibitors. Curr Med Chem 2010, 17:4114-4133.
37. 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.
38. Tyr705 phosphorylation. Mol Cancer Ther 2010, 9:2478-2487.
39. Santio NM, Vahakoski RL, Rainio EM, Sandholm JA, Virtanen SS, Prudhomme M, Anizon F, Moreau P, Koskinen PJ Pim-selective inhibitor DHPCC-9 reveals Pim kinases as potent stimulators of cancer cell migration and invasion. Mol Cancer 2010, 9:279.
40. Kelly KR, Espitia CM, Taverna P, Choy G, Padmanabhan S, Nawrocki ST, Giles FJ, Carew JS Targeting PIM kinase activity significantly augments the efficacy of cytarabine. Br J Haematol 2012, 156:129-132.
41. Hospital MA, Green AS, Lacombe C, Mayeux P, Bouscary D, Tamburini J The FLT3 and Pim kinases inhibitor SGI-1776 preferentially target FLT3-ITD AML cells. Blood 2012, 119:1791-1792.
42. Chen LS, Redkar S, Taverna P, Cortes JE, Gandhi V Mechanisms of cytotoxicity to Pim kinase inhibitor, SGI-1776, in acute myeloid leukemia. Blood 2011, 118:693-702.
43. Isaac M, Siu A, Jongstra J The oncogenic PIM kinase family regulates drug resistance through multiple mechanisms. Drug Resist Updat 2011, 14:203-211.
44. Mahalingam D, Espitia CM, Medina EC, Esquivel JA, Kelly KR, Bearss D, Choy G, Taverna P, Carew JS, Giles FJ, et al. Targeting PIM kinase enhances the activity of sunitinib in renal cell carcinoma. Br J Cancer 2011, 105:1563-1573.
45. 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.
46. Nishiguchi GA, Atallah G, Bellamacina C, Burger MT, Ding Y, Feucht PH, Garcia PD, Han W, Klivansky L, Lindvall M Discovery of novel 3,5-disubstituted indole derivatives as potent inhibitors of Pim-1, Pim-2, and Pim-3 protein kinases. Bioorg Med Chem Lett 2011, 21:6366-6369.
47. Siu A, Virtanen C, Jongstra J PIM kinase isoform specific regulation of MIG6 expression and EGFR signaling in prostate cancer cells. Oncotarget 2011, 2:1134-1144.
48. Mumenthaler SM, Ng PY, Hodge A, Bearss D, Berk G, Kanekal S, Redkar S, Taverna P, Agus DB, Jain A Pharmacologic inhibition of Pim kinases alters prostate cancer cell growth and resensitizes chemoresistant cells to taxanes. Mol Cancer Ther 2009, 8:2882-2893.
49. Alvarado Y, Giles FJ, Swords RT The PIM kinases in hematological cancers. Expert Rev Hematol 2012, 5:81-96.
50. Jöhrer K, Obkircher M, Neureiter D, Parteli J, Zelle-Rieser C, Maizner E, Kern J, Hermann M, Hamacher F, Merkel O, et al. Antimyeloma activity of the sesquiterpene lactone cnicin: impact on Pim-2 kinase as a novel therapeutic target. J Mol Med 2012, 90:681-693.
51. Song JH, Kraft AS Pim kinase inhibitors sensitize prostate cancer cells to apoptosis triggered by Bcl-2 family inhibitor ABT-737. Cancer Res 2012, 72:294-303.
52. Tsuganezawa K, Watanabe H, Parker L, Yuki H, Taruya S, Nakagawa Y, Kamei D, Mori M, Ogawa N, Tomabechi Y, et al. A novel Pim-1 kinase inhibitor targeting residues that bind the substrate peptide. J Mol Biol 2012, 417:240-252.
53. Tsuhako AL, Brown DS, Koltun ES, Aay N, Arcalas A, Chan V, Du H, Engst S, Franzini M, Galan A, et al. The design, synthesis, and biological evaluation of PIM kinase inhibitors. Bioorg Med Chem Lett 2012, 22:3732-3738.
54. Bullock AN, Debreczeni J, Amos AL, Knapp S, Turk BE Structure and substrate specificity of the Pim-1 kinase. J Biol Chem 2005, 280:41675-41682.
55. Jacobs MD, Black J, Futer O, Swenson L, Hare B, Fleming M, Saxena K Pim-1 ligand-bound structures reveal the mechanism of serine/threonine kinase inhibition by LY294002. J Biol Chem 2005, 280:13728-13734.
56. Shay KP, Wang Z, Xing PX, McKenzie IF, Magnuson NS Pim-1 kinase stability is regulated by heat shock proteins and the ubiquitin-proteasome pathway. Mol Cancer Res 2005, 3:170-181.
57. Holder S, Zemskova M, Zhang C, Tabrizizad M, Bremer R, Neidigh JW, Lilly MB Characterization of a potent and selective small-molecule inhibitor of the PIM1 kinase. Mol Cancer Ther 2007, 6:163-172.
58. Pierre F, Regan CF, Chevrel MC, Siddiqui-Jain A, Macalino D, Streiner N, Drygin D, Haddach M, O'Brien SE, Rice WG, et al. Novel potent dual inhibitors of CK2 and Pim kinases with antiproliferative activity against cancer cells. Bioorg Med Chem Lett 2012, 22:3327-3331.
59. Garcia PD, Langowski JL, Wang Y, Chen M, Castillo J, Fanton C, Ison M, Zavorotinskaya T, Dai Y, Lu J, et al. Pan-PIM kinase inhibition provides a novel therapy for treating hematologic cancers. Clin Cancer Res 2014, 20:1834-1845.
60. Molecular pathogenesis of urothelial carcinoma and the development of novel therapeutic strategies 2010, Y. Christopher, D.T. Thomas (Eds.).
61. White E The pims and outs of survival signaling: role for the Pim-2 protein kinase in the suppression of apoptosis by cytokines. Genes Dev 2003, 17:1813-1816.