Pim kinase inhibitor, SGI-1776, induces apoptosis in chronic lymphocytic leukemia cells

Blood

Volumn 114, Issue 19, 2009, Pages 4150-4157

  Chen, Lisa S ^a   Redkar, Sanjeev ^b   Bearss, David ^b   Wierda, William G ^a   Gandhi, Varsha ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b SuperGen Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CELL CYCLE PROTEIN; HISTONE H3; MYC PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE INHIBITOR; PROTEIN KINASE PIM 1; PROTEIN KINASE PIM 2; PROTEIN KINASE PIM 3; PROTEIN MCL 1; SERINE; SGI 1776; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

APOPTOSIS; ARTICLE; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; RNA SYNTHESIS;

EID: 77950538522     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-03-212852     Document Type: Article

References (52)

1. Shah N, Pang B, Yeoh KG, et al. Potential roles for the PIM1 kinase in human cancer - a molecular and therapeutic appraisal. Eur J Cancer. 2008; 44(15):2144-2151.
2. 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.
3. 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.
4. Wingett D, Long A, Kelleher D, Magnuson NS. pim-1 proto-oncogene expression in anti-CD3-mediated T-cell activation is associated with protein kinase C activation and is independent of Raf-1. J Immunol. 1996;156(2):549-557.
5. Cibull TL, Jones TD, Li L, et al. Overexpression of Pim-1 during progression of prostatic adenocarcinoma. J Clin Pathol. 2006;59(3):285-288.
6. Amaravadi R, Thompson CB. The survival kinases Akt and Pim as potential pharmacological targets. J Clin Invest. 2005;115(10):2618-2624.
7. Fox CJ, Hammerman PS, Thompson CB. The Pim kinases control rapamycin-resistant T-cell survival and activation. J Exp Med. 2005;201(2): 259-266.
8. 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(8):932-944.
9. Macdonald A, Campbell DG, Toth R, McLauchlan H, Hastie CJ, Arthur JS. Pim kinases phosphorylate multiple sites on Bad and promote 14-3-3 binding and dissociation from Bcl-XL. BMC Cell Biol. 2006;7:1.
10. Li YY, Popivanova BK, Nagai Y, Ishikura H, Fujii C, Mukaida N. Pim-3, a proto-oncogene with serine/threonine kinase activity, is aberrantly expressed in human pancreatic cancer and phosphorylates bad to block bad-mediated apoptosis in human pancreatic cancer cell lines. Cancer Res. 2006;66(13):6741-6747.
11. Roh M, Gary B, Song C, et al. Overexpression of the oncogenic kinase Pim-1 leads to genomic instability. Cancer Res. 2003;63(23):8079-8084.
12. Möröy T, Grzeschiczek A, Petzold S, Hartmann KU. Expression of a Pim-1 transgene accelerates lymphoproliferation and inhibits apoptosis in lpr/ lpr mice. Proc Natl Acad Sci U S A. 1993;90(22): 10734-10738.
13. Pircher TJ, Zhao S, Geiger JN, Joneja B, Wojchowski DM. Pim-1 kinase protects hematopoietic FDC cells from genotoxin-induced death. Oncogene. 2000;19(32):3684-3692.
14. Lilly M, Kraft A. Enforced expression of the Mr 33,000 Pim-1 kinase enhances factor-independent survival and inhibits apoptosis in murine myeloid cells. Cancer Res. 1997;57(23): 5348-5355.
15. 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.
16. Wang Z, Bhattacharya N, Weaver M, et al. Pim-1: a serine/threonine kinase with a role in cell survival, proliferation, differentiation and tumorigenesis. J Vet Sci. 2001;2(3):167-179.
17. 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.
18. Hammerman PS, Fox CJ, Birnbaum MJ, Thompson CB. Pim and Akt oncogenes are independent regulators of hematopoietic cell growth and survival. Blood. 2005;105(11):4477-4483.
19. Chen JL, Limnander A, Rothman PB. Pim-1 and Pim-2 kinases are required for efficient pre-B-cell transformation by v-Abl oncogene. Blood. 2008; 111(3):1677-1685.
20. 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 Bad-mediated apoptosis. Cancer Sci. 2007;98(3):321-328.
21. Giles F. A Pim kinase inhibitor, please. Blood. 2005;105(11):4158-4159.
22. Balakrishnan K, Wierda WG, Keating MJ, Gandhi V. Mechanisms of cell death of chronic lymphocytic leukemia lymphocytes by RNA-directed agent, 8-NH2-adenosine. Clin Cancer Res. 2005; 11(18):6745-6752.
23. Gandhi V, Balakrishnan K, Chen LS. Mcl-1: the 1 in CLL. Blood. 2008;112(9):3538-3540.
24. Rassenti LZ, Huynh L, Toy TL, et al. ZAP-70 compared with immunoglobulin heavy-chain gene mutation status as a predictor of disease progression in chronic lymphocytic leukemia. N Engl J Med. 2004;351(9):893-901.
25. Glassman AB, Hayes KJ. The value of fluorescence in situ hybridization in the diagnosis and prognosis of chronic lymphocytic leukemia. Cancer Genet Cytogenet. 2005;158(1):88-91.
26. Plunkett W, Hug V, Keating MJ, Chubb S. Quantitation of 1-beta-D-arabinofuranosylcytosine 5′-triphosphate in the leukemic cells from bone marrow and peripheral blood of patients receiving 1-beta-D- arabinofuranosylcytosine therapy. Cancer Res. 1980;40(3):588-591.
27. Millipore. KinaseProfiler. http://www.millipore. com/drugdiscovery/dd3/ KinaseProfiler. Accessed September 15, 2009.
28. Huttmann A, Klein-Hitpass L, Thomale J, et al. Gene expression signatures separate B-cell chronic lymphocytic leukaemia prognostic subgroups defined by ZAP-70 and CD38 expression status. Leukemia. 2006;20(10):1774-1782.
29. 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.
30. 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- 41682.
31. Kumar A, Mandiyan V, Suzuki Y, et al. Crystal structures of proto-oncogene kinase Pim1: a target of aberrant somatic hypermutations in diffuse large cell lymphoma. J Mol Biol. 2005;348(1):183-193.
32. Bullock AN, Debreczeni JE, Fedorov OY, Nelson A, Marsden BD, Knapp S. Structural basis of inhibitor specificity of the human protooncogene proviral insertion site in moloney murine leukemia virus (PIM-1) kinase. J Med Chem. 2005;48(24): 7604-7614.
33. Pogacic V, Bullock AN, Fedorov O, et al. Structural analysis identifies imidazo[1,2-b]pyridazines as PIM kinase inhibitors with in vitro antileukemic activity. Cancer Res. 2007;67(14):6916-6924.
34. 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(3):655-664.
35. Xie Y, Xu K, Linn DE, et al. The 44-kDa Pim-1 kinase phosphorylates BCRP/ABCG2 and thereby promotes its multimerization and drug-resistant activity in human prostate cancer cells. J Biol Chem. 2008;283(6):3349-3356.
36. Adam M, Pogacic V, Bendit M, et al. Targeting PIM kinases impairs survival of hematopoietic cells transformed by kinase inhibitor-sensitive and kinase inhibitor-resistant forms of Fms-like tyrosine kinase 3 and BCR/ABL. Cancer Res. 2006;66(7):3828-3835.
37. Small D. Targeting FLT3 for the treatment of leukemia. Semin Hematol. 2008;45(3 suppl 2): S17-21.
38. Reuther GW, Lambert QT, Caligiuri MA, Der CJ. Identification and characterization of an activating TrkA deletion mutation in acute myeloid leukemia. Mol Cell Biol. 2000;20(23):8655-8666.
39. Meyer J, Rhein M, Schiedlmeier B, et al. Remarkable leukemogenic potency and quality of a constitutively active neurotrophin receptor, deltaTrkA. Leukemia. 2007;21(10):2171-2180.
40. Dai J, Sullivan BA, Higgins JM. Regulation of mitotic chromosome cohesion by Haspin and Aurora B. Dev Cell. 2006;11(5):741-750.
41. Dai J, Sultan S, Taylor SS, Higgins JM. The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev. 2005;19(4):472-488.
42. Zhang Y, Wang Z, Li X, Magnuson NS. Pim kinase-dependent inhibition of c-Myc degradation. Oncogene. 2008;27(35):4809-4819.
43. Thompson CB, Challoner PB, Neiman PE, Groudine M. Levels of c-myc oncogene mRNA are invariant throughout the cell cycle. Nature. 1985;314(6009):363-366.
44. Patel JH, Loboda AP, Showe MK, Showe LC, McMahon SB. Analysis of genomic targets reveals complex functions of MYC. Nat Rev Cancer. 2004;4(7):562-568.
45. Johns Hopkins University School of Medicine & Johns Hopkins Health System. Myc cancer gene. http://www.myccancergene.org/. Accessed September 15, 2009.
46. Merino R, Ding L, Veis DJ, Korsmeyer SJ, Nunez G. Developmental regulation of the Bcl-2 protein and susceptibility to cell death in B lymphocytes. EMBO J. 1994;13(3):683-691.
47. Xin M, Deng X. Nicotine inactivation of the proapoptotic function of Bax through phosphorylation. J Biol Chem. 2005;280(11):10781-10789.
48. Yang T, Kozopas KM, Craig RW. The intracellular distribution and pattern of expression of Mcl-1 overlap with, but are not identical to, those of Bcl-2. J Cell Biol. 1995;128(6):1173-1184.
49. Dessauge F, Hilaly S, Baumgartner M, Blumen B, Werling D, Langsley G. c-Myc activation by Theileria parasites promotes survival of infected B-lymphocytes. Oncogene. 2005;24(6):1075-1083.
50. Kitada S, Andersen J, Akar S, et al. Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlations with In vitro and In vivo chemoresponses. Blood. 1998;91(9):3379-3389.
51. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood. 2006;107(5):1761-1767.
52. 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(3):170-181.