The Pim kinase inhibitor SGI-1776 decreases cell surface expression of P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and drug transport by Pim-1-dependent and -independent mechanisms

Biochemical Pharmacology

Volumn 85, Issue 4, 2013, Pages 514-524

  Natarajan, Karthika ^a   Bhullar, Jasjeet ^a   Shukla, Suneet ^b   Burcu, Mehmet ^a   Chen, Zhe Sheng ^c   Ambudkar, Suresh V ^b   Baer, Maria R ^a,d  

^a UNIVERSITY OF MARYLAND   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c ST JOHN'S UNIVERSITY   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

ABCB1; ABCG2; Leukemia; Multidrug resistance; Pim 1 kinase; SGI 1776

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BREAST CANCER RESISTANCE PROTEIN; ENZYME INHIBITOR; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN KINASE PIM 1; SGI 1776; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL SURFACE; CELL SURVIVAL; CHEMOSENSITIVITY; CHEMOSENSITIZATION; COLONY FORMATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG BINDING; DRUG RESISTANCE; DRUG STRUCTURE; DRUG TRANSPORT; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IC 50; PHOTOAFFINITY LABELING; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; IMIDAZOLES; MOLECULAR STRUCTURE; NEOPLASM PROTEINS; P-GLYCOPROTEIN; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-PIM-1; PYRIDAZINES;

EID: 84872675468     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2012.12.006     Document Type: Article

References (63)

1. G. Szakács, J.K. Paterson, J.A. Ludwig, C. Booth-Genthe, and M.M. Gottesman Targeting multidrug resistance in cancer Nat Rev Drug Discov 5 2006 219 234
2. Z. Benderra, A.M. Faussat, L. Sayada, J.Y. Perrot, D. Chaoui, and J.P. Marie Breast cancer resistance protein and P-glycoprotein in 149 adult acute myeloid leukemias Clin Cancer Res 10 2004 7896 7902
3. D. Damiani, M. Tiribelli, E. Calistri, A. Geromin, A. Chiarvesio, and A. Michelutti The prognostic value of P-glycoprotein (ABCB) and breast cancer resistance protein (ABCG2) in adults with de novo acute myeloid leukemia with normal karyotype Haematologica 91 2006 825 828
4. M.R. Baer, S.L. George, R.K. Dodge, K.L. O'Loughlin, H. Minderman, and M.A. Caligiuri Phase 3 study of the multidrug resistance modulator PSC-833 in previously untreated patients 60 years of age and older with acute myeloid leukemia: Cancer and Leukemia Group B Study 9720 Blood 100 2002 1224 1232
5. P.L. Greenberg, S.J. Lee, R. Advani, M.S. Tallman, B.I. Sikic, and L. Letendre Mitoxantrone, etoposide, and cytarabine with or without valspodar in patients with relapsed or refractory acute myeloid leukemia and high-risk myelodysplastic syndrome: a phase III trial (E2995) J Clin Oncol 22 2004 1078 1086
6. B. van der Holt, B. Löwenberg, A.K. Burnett, W.U. Knauf, J. Shepherd, and P.P. Piccaluga The value of the MDR1 reversal agent PSC-833 in addition to daunorubicin and cytarabine in the treatment of elderly patients with previously untreated acute myeloid leukemia (AML), in relation to MDR1 status at diagnosis Blood 106 2005 2646 2654
7. J.E. Kolitz, S.L. George, G. Marcucci, R. Vij, B.L. Powell, and S.L. Allen P-glycoprotein inhibition using valspodar (PSC-833) does not improve outcomes for patients younger than age 60 years with newly diagnosed acute myeloid leukemia: Cancer and Leukemia Group B study 19808 Blood 116 2010 1413 1421
8. L.D. Cripe, H. Uno, E.M. Paietta, M.R. Litzow, R.P. Ketterling, and J.M. Bennett Zosuquidar, a novel modulator of P-glycoprotein, does not improve the outcome of older patients with newly diagnosed acute myeloid leukemia: a randomized, placebo-controlled trial of the Eastern Cooperative Oncology Group 3999 Blood 116 2010 4077 4085
9. M. Raaijmakers, E. de Grouw, L. Heuver, B. van der Reijden, J. Jansen, and R. Scheper Breast cancer resistance protein in drug resistance of primitive CD34 + 38- cells in acute myeloid leukemia Clin Cancer Res 11 2005 2436 2444
10. M.H. Raaijmakers, E.P. de Grouw, B.A. van der Reijden, T.J. de Witte, J.H. Jansen, and R.A. Raymakers ABCB1 modulation does not circumvent drug extrusion from primitive leukemic progenitor cells and may preferentially target residual normal cells in acute myelogenous leukemia Clin Cancer Res 12 2006 3452 3458
11. M. Qadir, K.L. O'Loughlin, S.M. Fricke, N.A. Williamson, W.R. Greco, and H. Minderman Cyclosporin A is a broad-spectrum multidrug resistance modulator Clin Cancer Res 11 2005 2320 2326
12. A.F. List, K.J. Kopecky, C.L. Willman, D.R. Head, D.L. Persons, and M.L. Slovak Benefit of cyclosporine modulation of drug resistance in patients with poor-risk acute myeloid leukemia: a Southwest Oncology Group study Blood 98 2001 3212 3220
13. P. Matsouka, M. Pagoni, P. Zikos, N. Giannakoulas, I. Apostolidis, and T. Asprogeraka Addition of cyclosporin-A to chemotherapy in secondary (post-MDS) AML in the elderly. A multicenter randomized trial of the Leukemia Working Group of the Hellenic Society of Hematology Ann Hematol 85 2006 250 256
14. T.R. Chauncey, H. Gundacker, M. Shadman, A.F. List, S.R. Dakhil, and H.P. Erba Sequential phase II Southwest Oncology Group studies (S0112 and S0301) of daunorubicin and cytarabine by continuous infusion, without and with ciclosporin, in older patients with previously untreated acute myeloid leukaemia Br J Haematol 148 2010 48 58
15. D. Becton, G.V. Dahl, Y. Ravindranath, M.N. Chang, F.G. Behm, and S.C. Raimondi Randomized use of cyclosporin A (CsA) to modulate P-glycoprotein in children with AML in remission: Pediatric Oncology Group Study 9421 Blood 107 2006 1315 1324
16. L. Brault, C. Gasser, F. Bracher, K. Huber, S. Knapp, and J. Schwaller PIM serine/threonine kinases in the pathogenesis and therapy of hematologic malignancies and solid cancers Haematologica 95 2010 1004 1015
17. Y. Xie, M. Burcu, D.E. Linn, Y. Qiu, and Baer MR Pim-1 kinase protects P-glycoprotein from degradation and enables its glycosylation and cell surface expression. Mol Pharmacol 78 2010 310 318
18. Y. Xie, K. Xu, D.E. Linn, X. Yang, Z. Guo, and H. Shimelis 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 283 2008 3349 3356
19. R. Amson, F. Sigaux, S. Przedborski, G. Flandrin, D. Givol, and A. Telerman The human protooncogene product p33pim is expressed during fetal hematopoiesis and in diverse leukemias Proc Natl Acad Sci USA 86 1989 8857 8861
20. S.M. Mumenthaler, P.Y. Ng, A. Hodge, D. Bearss, G. Berk, and S. Kanekal Pharmacologic inhibition of Pim kinases alters prostate cancer cell growth and resensitizes chemoresistant cells to taxanes Mol Cancer Ther 8 2009 2882 2893
21. L.S. Chen, S. Redkar, D. Bearss, W.G. Wierda, and V. Gandhi Pim kinase inhibitor, SGI-1776, induces apoptosis in chronic lymphocytic leukemia cells Blood 114 2009 4150 4157
22. L.S. Chen, S. Redkar, P. Taverna, J.E. Cortes, and V. Gandhi Mechanisms of cytotoxicity to Pim kinase inhibitor, SGI-1776, in acute myeloid leukemia Blood 118 2011 693 702
23. B. Ogretmen, and A.R. Safa Identification and characterization of the MDR1 promoter-enhancing factor 1 (MEF1) in the multidrug resistant HL60/VCR human acute myeloid leukemia cell line Biochemistry 39 2000 194 204
24. L.A. Hazlehurst, N.E. Foley, M.C. Gleason-Guzman, M.P. Hacker, A.E. Cress, and L.W. Greenberger Multiple mechanisms confer drug resistance to mitoxantrone in the human 8226 myeloma cell line Cancer Res 59 1999 1021 1028
25. P. Hafkemeyer, T. Licht, I. Pastan, and M.M. Gottesman Chemoprotection of hematopoietic cells by a mutant P-glycoprotein resistant to a potent chemosensitizer of multidrug-resistant cancers Hum Gene Ther 11 2000 555 565
26. K. Yanase, S. Tsukahara, S. Asada, E. Ishikawa, Y. Imai, and Y. Sugimoto Gefitinib reverses breast cancer resistance protein-mediated drug resistance Mol Cancer Ther 3 2004 1119 1125
27. R.W. Robey, W.Y. Medina-Perez, K. Nishiyama, T. Lahusen, K. Miyake, and T. Litman Overexpression of the ATP-binding cassette half-transporter, ABCG2 (Mxr/BCrp/ABCP1), in flavopiridol-resistant human breast cancer cells Clin Cancer Res 7 2001 145 152
28. R. Sen, K. Natarajan, J. Bhullar, S. Shukla, H.B. Fang, and L. Cai The novel BCR-ABL and FLT3 inhibitor ponatinib is a potent inhibitor of the multidrug resistance-associated ATP-binding cassette transporter ABCG2 Mol Cancer Ther 11 2012 2033 2044
29. H. Minderman, A. Suvannasankha, K.L. O'Loughlin, G.L. Scheffer, R.J. Scheper, and R.W. Robey Flow cytometric analysis of breast cancer resistance protein expression and function Cytometry 48 2002 59 65
30. R.W. Robey, K. Steadman, O. Polgar, K. Morisaki, M. Blayney, and P. Mistry Pheophorbide a is a specific probe for ABCG2 function and inhibition Cancer Res 64 2004 1242 1246
31. K. Horikawa, and K. Takatsu Interleukin-5 regulates genes involved in B-cell terminal maturation Immunology 118 2006 497 508
32. K.T. Kim, M. Levis, and D. Small Constitutively activated FLT3 phosphorylates BAD partially through pim-1 Br J Haematol 134 2006 500 509
33. I.T. Young Proof without prejudice: use of the Kolmogorov-Smirnov test for the analysis of histograms from flow systems and other sources J Histochem Cytochem 25 1977 935 941
34. H. Minderman, K.L. O'Loughlin, L. Pendyala, and M.R. Baer VX-710 (biricodar) increases drug retention and enhances chemosensitivity in resistant cells overexpressing P-glycoprotein, multidrug resistance protein, and breast cancer resistance protein Clin Cancer Res 10 2004 1826 1834
35. Z.E. Sauna, and S.V. Ambudkar Evidence for a requirement for ATP hydrolysis at two distinct steps during a single turnover of the catalytic cycle of human P-glycoprotein Proc Natl Acad Sci USA 97 2000 2515 2520
36. S. Shukla, R.W. Robey, S.E. Bates, and S.V. Ambudkar The calcium channel blockers, 1,4-dihydropyridines, are substrates of the multidrug resistance-linked ABC drug transporter, ABCG2 Biochemistry 45 2006 8940 8951
37. S.V. Ambudkar Drug-stimulatable ATPase activity in crude membranes of human MDR1-transfected mammalian cells Methods Enzymol 292 1998 504 514
38. R.G. Miller Jr. Simultaneous Statistical Inference 1991 Springer-Verlag New York
39. C.J. Saris, J. Domen, and A. Berns The pim-1 oncogene encodes two related protein-serine/threonine kinases by alternative initiation at AUG and CUG EMBO J 10 1991 655 664
40. Y. Xie, K. Xu, B. Dai, Z. Guo, T. Jiang, and H. Chen The 44 kDa Pim-1 kinase directly interacts with tyrosine kinase Etk/BMX and protects human prostate cancer cells from apoptosis induced by chemotherapeutic drugs Oncogene 25 2006 70 78
41. M.W. Nasser, J. Datta, G. Nuovo, H. Kutay, T. Motiwala, and S. Majumder Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1 J Biol Chem 283 2008 33394 33405
42. J. Chen, H. Yin, Y. Jiang, S.K. Radhakrishnan, Z.P. Huang, and J. Li Induction of microRNA-1 by myocardin in smooth muscle cells inhibits cell proliferation Arterioscler Thromb Vasc Biol 31 2011 368 375
43. R. Katare, A. Caporali, L. Zentilin, E. Avolio, G. Sala-Newby, and A. Oikawa Intravenous gene therapy with PIM-1 via a cardiotropic viral vector halts the progression of diabetic cardiomyopathy through promotion of prosurvival signaling Circ Res 108 2011 1238 1251
44. K.T. Kim, A.P. Carroll, B. Mashkani, M.J. Cairns, D. Small, and R.J. Scott MicroRNA-16 is down-regulated in mutated FLT3 expressing murine myeloid FDC-P1 cells and interacts with Pim-1 PLoS ONE 7 2012 e44546
45. A.F. Ibrahim, U. Weirauch, M. Thomas, A. Grünweller, R.K. Hartmann, and A. Aigner MicroRNA replacement therapy for miR-145 and miR-33a is efficacious in a model of colon carcinoma Cancer Res 71 2011 5214 5224
46. M. Thomas, K. Lange-Grünweller, U. Weirauch, D. Gutsch, A. Aigner, and A. Grünweller The proto-oncogene Pim-1 is a target of miR-33a Oncogene 31 2012 918 928
47. A.M. Eiring, J.G. Harb, P. Neviani, C. Garton, J.J. Oaks, and R. Spizzo miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts Cell 140 2010 652 665
48. D.A. Gutmann, A. Ward, I.L. Urbatsch, G. Chang, and H.W. van Veen Understanding polyspecificity of multidrug ABC transporters: closing in on the gaps in ABCB1 Trends Biochem Sci 35 2010 36 42
49. T. Illmer, M. Schaich, U. Platzbecker, J. Freiberg-Richter, U. Oelschlägel, and M. von Bonin P-glycoprotein-mediated drug efflux is a resistance mechanism of chronic myelogenous leukemia cells to treatment with imatinib mesylate Leukemia 18 2004 401 408
50. H. Burger, H. van Tol, A.W. Boersma, M. Brok, E.A. Wiemer, and G. Stoter Imatinib mesylate (STI571) is a substrate for the breast cancer resistance protein (BCRP)/ABCG2 drug pump Blood 104 2004 2940 2942
51. P.J. Houghton, G.S. Germain, F.C. Harwood, J.D. Schuetz, C.F. Stewart, and E. Buchdunger Imatinib mesylate is a potent inhibitor of the ABCG2 (BCRP) transporter and reverses resistance to topotecan and SN-38 in vitro Cancer Res 64 2004 2333 2337
52. S. Shukla, Z. Sauna, and S. Ambudkar Evidence for the interaction of imatinib at the transport-substrate site(s) of the multidrug-resistance-linked ABC drug transporters ABCB1 (P-glycoprotein) and ABCG2 Leukemia 22 2008 445 447
53. A.K. Tiwari, K. Sodani, S.R. Wang, Y.H. Kuang, C.R. Ashby Jr., and X. Chen Nilotinib (AMN107, Tasigna) reverses multidrug resistance by inhibiting the activity of the ABCB1/Pgp and ABCG2/BCRP/MXR transporters Biochem Pharmacol 78 2009 153 161
54. J.S. Lagas, R.A. van Waterschoot, V.A. van Tilburg, M.J. Hillebrand, N. Lankheet, and H. Rosing Brain accumulation of dasatinib is restricted by P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and can be enhanced by elacridar treatment Clin Cancer Res 15 2009 2344 2351
55. M. Dohse, C. Scharenberg, S. Shukla, R.W. Robey, T. Volkmann, and J.F. Deeken Comparison of ATP-binding cassette transporter interactions with the tyrosine kinase inhibitors imatinib, nilotinib, and dasatinib Drug Metab Dispos 38 2010 1371 1380
56. H.M. Hunter, M. Pallis, C.H. Seedhouse, M. Grundy, C. Gray, and N.H. Russell The expression of P-glycoprotein in AML cells with FLT3 internal tandem duplications is associated with reduced apoptosis in response to FLT3 inhibitors Br J Haematol 127 2004 26 33
57. J.J. Yang, M.N. Milton, S. Yu, M. Liao, N. Liu, and J.T. Wu P-glycoprotein and breast cancer resistance protein affect disposition of tandutinib, a tyrosine kinase inhibitor Drug Metab Lett 4 2010 201 212
58. J.S. Lagas, R.A. van Waterschoot, R.W. Sparidans, E. Wagenaar, J.H. Beijnen, and A.H. Schinkel Breast cancer resistance protein and P-glycoprotein limit sorafenib brain accumulation Mol Cancer Ther 9 2010 319 326
59. S. Shukla, R.W. Robey, S.E. Bates, and Ambudkar S.V. Sunitinib (Sutent, SU11248), a small-molecule receptor tyrosine kinase inhibitor, blocks function of the ATP-binding cassette (ABC) transporters P-glycoprotein (ABCB1) and ABCG2 Drug Metab Dispos 37 2009 359 365
60. W.S. Huang, C.A. Metcalf, R. Sundaramoorthi, Y. Wang, D. Zou, and R.M. Thomas Discovery of 3-[2-(imidazo[1,2-b]pyridazin-3-yl)ethynyl]-4-methyl-N-{4- [(4-methylpiperazin-1-yl)methyl]-3-(trifluoromethyl)phenyl}benzamide (AP24534), a potent, orally active pan-inhibitor of breakpoint cluster region-abelson (BCR-ABL) kinase including the T315I gatekeeper mutant J Med Chem 53 2010 4701 4719
61. K.F. Byth, N. Cooper, J.D. Culshaw, D.W. Heaton, S.E. Oakes, and C.A. Minshull Imidazo[1,2-b]pyridazines: a potent and selective class of cyclin-dependent kinase inhibitors Bioorg Med Chem Lett 14 2004 2249 2252
62. H. Shimizu, S. Tanaka, T. Toki, I. Yasumatsu, T. Akimoto, and K. Morishita Discovery of imidazo[1,2-b]pyridazine derivatives as IKKbeta inhibitors. Part 1: hit-to-lead study and structure-activity relationship Bioorg Med Chem Lett 20 2010 5113 5118
63. H. Iwata, S. Imamura, A. Hori, M.S. Hixon, H. Kimura, and H. Miki Biochemical characterization of TAK-593, a novel VEGFR/PDGFR inhibitor with a two-step slow binding mechanism Biochemistry 50 2011 738 751