PIM2 inhibition as a rational therapeutic approach in B-cell lymphoma

Blood

Volumn 118, Issue 20, 2011, Pages 5517-5527

  Gómez Abad, Cristina ^a   Pisonero, Helena ^a,b   Blanco Aparicio, Carmen ^a   Roncador, Giovanna ^a   González Menchén, Alberto ^c   Martinez Climent, Jose A ^d   Mata, Eva ^a   Rodríguez, María Elena ^a   Muñoz González, Guillermo ^a   Sánchez Beato, Margarita ^a   Leal, Juan F ^a   Bischoff, James R ^a   Piris, Miguel A ^a,b  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^c HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

^d UNIVERSITY OF NAVARRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MOLECULAR MARKER; PROTEIN PIM2; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; B CELL LYMPHOMA; CANCER INHIBITION; CELL VIABILITY; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; ENZYME INHIBITION; FOLLICULAR LYMPHOMA; GENE AMPLIFICATION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; LARGE CELL LYMPHOMA; MANTLE CELL LYMPHOMA; MARGINAL ZONE LYMPHOMA; NODAL MARGINAL ZONE LYMPHOMA; NONHUMAN; PHARMACODYNAMICS; PRIORITY JOURNAL; PROTEIN TRANSPORT;

EID: 81555196341     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-03-344374     Document Type: Article

References (51)

1. Swerdlow SH, Campo E, Harris NL, et al. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Vol. 2(2). Lyon, France: IARC Press; 2008.
2. Rimsza LM, Wright GW, Schwartz M, et al. Accurate classification of diffuse large b cell lymphoma into germinal center and activated b cell subtypes using a nuclease protection assay on paraffin embedded tissues. Clin Cancer Res. 2011; 17(11):3727-3732.
3. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000; 403(6769):503-511. (Pubitemid 30082188)
4. Meyer PN, Fu K, Greiner T, et al. The stromal cell marker SPARC predicts for survival in patients with diffuse large B-cell lymphoma treated with rituximab. Am J Clin Pathol. 2011;135(1):54-61.
5. Choi WW, Weisenburger DD, Greiner TC, et al. A new immunostain algorithm classifies diffuse large B-cell lymphoma into molecular subtypes with high accuracy. Clin Cancer Res. 2009; 15(17):5494-5502.
6. Hutchinson CB, Wang E. Primary mediastinal (thymic) large B-cell lymphoma: a short review with brief discussion of mediastinal gray zone lymphoma. Arch Pathol Lab Med. 2011;135(3): 394-398.
7. Coiffier B. State-of-the-art therapeutics: diffuse large B-cell lymphoma. J Clin Oncol. 2005; 23(26):6387-6393. (Pubitemid 46218851)
8. Vose JM, Link BK, Grossbard ML, et al. Phase II study of rituximab in combination with chop chemotherapy in patients with previously untreated, aggressive non-Hodgkin's lymphoma. J Clin Oncol. 2001;19(2):389-397. (Pubitemid 32112850)
9. Lenz G, Staudt LM. Aggressive lymphomas. N Engl J Med. 2010;362(15):1417-29.
10. Yan B, Zemskova M, Holder S, et al. The PIM-2 kinase phosphorylates BAD on serine 112 and reverses BAD-induced cell death. J Biol Chem. 2003;278(46):45358-45367. (Pubitemid 37432672)
11. Aho TL, Sandholm J, Peltola KJ, Mankonen HP, Lilly M, Koskinen PJ. Pim-1 kinase promotes inactivation of the pro-apoptotic Bad protein by phosphorylating it on the Ser112 gatekeeper site. FEBS Lett. 2004;571(1-3):43-49. (Pubitemid 38992921)
12. Wang Z, Bhattacharya N, Mixter PF, Wei W, Sedivy J, Magnuson NS. Phosphorylation of the cell cycle inhibitor p21Cip1/WAF1 by Pim-1 kinase. Biochim Biophys Acta. 2002;1593(1):45-55. (Pubitemid 35335911)
13. Morishita D, Katayama R, Sekimizu K, Tsuruo T, Fujita N. Pim kinases promote cell cycle progression by phosphorylating and down-regulating p27Kip1 at the transcriptional and posttranscriptional levels. Cancer Res. 2008;68(13):5076- 5085.
14. Krishnan N, Pan H, Buckley DJ, Buckley A. Prolactin- regulated pim-1 transcription: identification of critical promoter elements and Akt signaling. Endocrine. 2003;20(1-2):123-30.
15. Lin YW, Beharry ZM, Hill EG, et al. A small molecule inhibitor of Pim protein kinases blocks the growth of precursor T-cell lymphoblastic leukemia/ lymphoma. Blood. 2010;115(4):824-833.
16. Hogan C, Hutchison C, Marcar L, et al. Elevated levels of oncogenic protein kinase Pim-1 induce the p53 pathway in cultured cells and correlate with increased Mdm2 in mantle cell lymphoma. J Biol Chem. 2008;283(26):18012-18023.
17. Shirogane T, Fukada T, Muller JM, Shima DT, Hibi M, Hirano T. Synergistic roles for Pim-1 and c-Myc in STAT3-mediated cell cycle progression and antiapoptosis. Immunity. 1999;11(6):709-719. (Pubitemid 30030710)
18. 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(6):1004-1015.
19. van Lohuizen M, Verbeek S, Krimpenfort P, et al. Predisposition to lymphomagenesis in pim-1 transgenic mice: cooperation with c-myc and Nmyc in murine leukemia virus-induced tumors. Cell. 1989;56(4):673-682. (Pubitemid 19065532)
20. van der Lugt NM, Domen J, Verhoeven E, et al. Proviral tagging in E mu-myc transgenic mice lacking the Pim-1 proto-oncogene leads to compensatory activation of Pim-2. EMBO J. 1995; 14(11):2536-2544.
21. Hsi ED, Jung SH, Lai R, et al. Ki67 and PIM1 expression predict outcome in mantle cell lymphoma treated with high dose therapy, stem cell transplantation and rituximab: a Cancer and Leukemia Group B 59909 correlative science study. Leuk Lymphoma. 2008;49(11):2081-2090.
22. Cohen AM, Grinblat B, Bessler H, et al. Increased expression of the hPim-2 gene in human chronic lymphocytic leukemia and non-Hodgkin lymphoma. Leuk Lymphoma. 2004;45(5):951-955. (Pubitemid 38444671)
23. Pasqualucci L, Neumeister P, Goossens T, et al. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature. 2001;412(6844):341-346. (Pubitemid 32691848)
24. Amson R, Sigaux F, Przedborski S, Flandrin G, Givol D, Telerman A. The human protooncogene product p33pim is expressed during fetal hematopoiesis and in diverse leukemias. Proc Natl Acad Sci U S A. 1989;86(22):8857-8861. (Pubitemid 20010324)
25. Claudio JO, Masih-Khan E, Tang H, et al. A molecular compendium of genes expressed in multiple myeloma. Blood. 2002;100(6):2175-2186. (Pubitemid 35001254)
26. Chen WW, Chan DC, Donald C, Lilly MB, Kraft AS. Pim family kinases enhance tumor growth of prostate cancer cells. Mol Cancer Res. 2005;3(8): 443-451. (Pubitemid 41232606)
27. Reiser-Erkan C, Erkan M, Pan Z, et al. Hypoxiainducible proto-oncogene Pim-1 is a prognostic marker in pancreatic ductal adenocarcinoma. Cancer Biol Ther. 2008;7(9):1352-1359.
28. Rossi D, Berra E, Cerri M, et al. Aberrant somatic hypermutation in transformation of follicular lymphoma and chronic lymphocytic leukemia to diffuse large B-cell lymphoma. Haematologica. 2006;91(10):1405-1409. (Pubitemid 44569818)
29. Akué-Gédu R, Rossignol E, Azzaro S, et al. Synthesis, kinase inhibitory potencies, and in vitro antiproliferative evaluation of new Pim kinase inhibitors. J Med Chem. 2009;52(20):6369-6381.
30. Beharry Z, Zemskova M, Mahajan S, et al. 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(6):1473-1483.
31. Grey R, Pierce AC, Bemis GW, et al. Structurebased design of 3-aryl-6-amino-triazolo[4,3-b]pyridazine inhibitors of Pim-1 kinase. Bioorg Med Chem Lett. 2009;19(11):3019-3022.
32. Hu XF, Li J, Vandervalk S, Wang Z, Magnuson NS, Xing PX. PIM-1-specific mAb suppresses human and mouse tumor growth by decreasing PIM-1 levels, reducing Akt phosphorylation, and activating apoptosis. J Clin Invest. 2009; 119(2):362-375.
33. Xia Z, Knaak C, Ma J, et al. Synthesis and evaluation of novel inhibitors of Pim-1 and Pim-2 protein kinases. J Med Chem. 2009;52(1):74-86.
34. Morwick T. Pim kinase inhibitors: a survey of the patent literature. Expert Opin Ther Pat. 2010; 20(2):193-212.
35. Aggarwal M, Sanchez-Beato M, Gomez-Lopez G, et al. Functional signatures identified in B-cell non-Hodgkin lymphoma profiles. Leuk Lymphoma. 2009;50(10):1699-1708.
36. Kaplan E MP. Nonparametric estimation from incomplete observations. Am Stat Assoc J. 1958; 53:457-481.
37. Cheson BD, Pfistner B, Juweid ME, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007;25(5):579-586. (Pubitemid 350002966)
38. Peto R, Pike MC, Armitage P, et al. Design and analysis of randomized clinical trials requiring prolonged observation of each patient. II. analysis and examples. Br J Cancer. 1977;35(1):1-39. (Pubitemid 8018922)
39. 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(15): 1841-1854. (Pubitemid 36944562)
40. Wozniak MB, Villuendas R, Bischoff JR, et al. Vorinostat interferes with the signaling transduction pathway of T-cell receptor and synergizes with phosphoinositide-3 kinase inhibitors in cutaneous T-cell lymphoma. Haematologica. 2010; 95(4):613-621.
41. Bullock AN, Debreczeni J, Amos AL, Knapp S, Turk BE. Structure and substrate specificity of the Pim-1 kinase. J Biol Chem. 2005;280(50):41675- 82.
42. Amaravadi R, Thompson CB. The survival kinases Akt and Pim as potential pharmacological targets. J Clin Invest. 2005;115(10):2618-2624. (Pubitemid 41434384)
43. Mikkers H, Allen J, Knipscheer P, et al. Highthroughput retroviral tagging to identify components of specific signaling pathways in cancer. Nat Genet. 2002;32(1):153-159. (Pubitemid 34977211)
44. Muraski JA, Rota M, Misao Y, et al. Pim-1 regulates cardiomyocyte survival downstream of Akt. Nat Med. 2007;13(12):1467-1475. (Pubitemid 350224243)
45. Bachmann M, Moroy T. The serine/threonine kinase Pim-1. Int J Biochem Cell Biol. 2005;37(4): 726-730. (Pubitemid 40202995)
46. Mikkers H, Nawijn M, Allen J, et al. Mice deficient for all PIM kinases display reduced body size and impaired responses to hematopoietic growth factors. Mol Cell Biol. 2004;24(13):6104-6115. (Pubitemid 38787993)
47. Bachmann M, Kosan C, Xing PX, Montenarh M, Hoffmann I, Moroy T. The oncogenic serine/threonine kinase Pim-1 directly phosphorylates and activates the G2/M specific phosphatase Cdc25C. Int J Biochem Cell Biol. 2006;38(3):430- 443.
48. Bachmann M, Hennemann H, Xing PX, Hoffmann I, Moroy T. The oncogenic serine/threonine kinase Pim-1 phosphorylates and inhibits the activity of Cdc25C-associated kinase 1 (C-TAK1): a novel role for Pim-1 at the G2/M cell cycle checkpoint. J Biol Chem. 2004;279(46):48319-48328. (Pubitemid 39540988)
49. Hammerman PS, Fox CJ, Cinalli RM, et al. Lymphocyte transformation by Pim-2 is dependent on nuclear factor-kappaB activation. Cancer Res. 2004;64(22):8341-8348. (Pubitemid 39491773)
50. Blanco-Aparicio C, Collazo AM, Oyarzabal J, et al. Pim 1 kinase inhibitor ETP-45299 suppresses cellular proliferation and synergizes with PI3K inhibition. Cancer Lett. 2011;300(2):145-153.
51. Lam LT, Wright G, Davis RE, et al. Cooperative signaling through the signal transducer and activator of transcription 3 and nuclear factor- {kappa}B pathways in subtypes of diffuse large B-cell lymphoma. Blood. 2008;111(7):3701- 3713.