The multikinase inhibitor sorafenib induces apoptosis in highly imatinib mesylate-resistant Bcr/Abl+ human leukemia cells in association with signal transducer and activator of transcription 5 inhibition and myeloid cell leukemia-1 down-regulation

Molecular Pharmacology

Volumn 72, Issue 3, 2007, Pages 788-795

  Rahmani, Mohamed ^a   Nguyen, Tri K ^a   Dent, Paul ^b   Grant, Steven ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CRK LIKE PROTEIN; DASATINIB; IMATINIB; INITIATION FACTOR 4E; NILOTINIB; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE LYN; PROTEIN MCL 1; SHORT HAIRPIN RNA; SORAFENIB; STAT5 PROTEIN;

APOPTOSIS; ARTICLE; BONE MARROW CELL; CD34 SELECTION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG INHIBITION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LEUKEMIA CELL; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZENESULFONATES; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; K562 CELLS; LEUKEMIA, MYELOID, CHRONIC; PIPERAZINES; PROTEIN KINASE INHIBITORS; PYRIDINES; PYRIMIDINES; STAT5 TRANSCRIPTION FACTOR;

EID: 34548412863     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.106.033308     Document Type: Article

References (40)

1. Aichberger KJ, Mayerhofer M, Krauth MT, Skvara H, Florian S, Sonneck K, Akgul C, Derdak S, Pickl WF, Wacheck V, et al. (2005) Identification of mcl-1 as a BCR/ABL-dependent target in chronic myeloid leukemia (CML): evidence for cooperative antileukemic effects of imatinib and mcl-1 antisense oligonucleotides. Blood 105:3303-3311.
2. Ariyoshi K, Nosaka T, Yamada K, Onishi M, Oka Y, Miyajima A, and Kitamura T (2000) Constitutive activation of STAT5 by a point mutation in the SH2 domain. J Biol Chem 275:24407-24413.
3. Awada A, Hendlisz A, Gil T, Bartholomeus S, Mano M, de Valeriola D, Strumberg D, Brendel E, Haase CG, Schwartz B, et al. (2005) Phase I safety and pharmacokinetics of BAY 43-9006 administered for 21 days on/7 days off in patients with advanced, refractory solid tumours. Br J Cancer 92:1855-1861.
4. Buchdunger E, Cioffi CL, Law N, Stover D, Ohno-Jones S, Druker BJ, and Lydon NB (2000) Abl protein-tyrosine kinase inhibitor STI571 inhibits in vitro signal transduction mediated by C-Kit and platelet-derived growth factor receptors. J Pharmacol Exp Ther 295:139-145.
5. Chandra J, Tracy J, Loegering D, Flatten K, Verstovsek S, Beran M, Gorre M, Estrov Z, Donato N, Talpaz M, et al. (2006) Adaphostin-induced oxidative stress overcomes BCR/ABL mutation-dependent and -independent imatinib resistance. Blood 107:2501-2506.
6. Copland M, Hamilton A, Elrick LJ, Baird JW, Allan EK, Jordanides N, Barow M, Mountford JC, and Holyoake TL (2006) Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood 107:4532-4539.
7. Dai Y, Rahmani M, Corey SJ, Dent P, and Grant S (2004) A Bcr/Abl-independent, Lyn-dependent form of imatinib mesylate (STI-571) resistance is associated with altered expression of Bcl-2. J Biol Chem 279:34227-34239.
8. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, et al. (2002) Mutations of the BRAF gene in human cancer. Nature 417:949-954.
9. de Groot RP, Raaijmakers JA, Lammers JW, Jove R, and Koenderman L (1999) STAT5 activation by BCR-Abl contributes to transformation of K562 leukemia cells. Blood 94:1108-1112.
10. Derenne S, Monia B, Dean NM, Taylor JK, Rapp MJ, Harousseau JL, Bataille R, and Amiot M (2002) Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-xL is an essential survival protein of human myeloma cells. Blood 100:194-199.
11. Donato NJ, Wu JY, Stapley J, Gallick G, Lin H, Arlinghaus R, and Talpaz M (2003) BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to STI571. Blood 101:690-698.
12. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, Lydon NB, Kantarjian H, Capdeville R, Ohno-Jones S, et al. (2001) Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 344:1031-1037.
13. Fiskus W, Pranpat M, Bali P, Balasis M, Kumaraswamy S, Boyapalle S, Rocha K, Wu J, Giles F, Manley PW, et al. (2006) Combined effects of novel tyrosine kinase inhibitor AMN107 and histone deacetylase inhibitor LBH589 against Bcr-Abl-expressing human leukemia cells. Blood 108:645-652.
14. Gomez-Bougie P, Bataille R, and Amiot M (2005) Endogenous association of Bim BH3-only protein with Mcl-1, Bcl-xL and Bcl-2 on mitochondria in human B cells. Eur J Immunol 35:971-976.
15. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN, and Sawyers CL (2001) Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293:876-880.
16. Graham SM, Jorgensen HG, Allan E, Pearson C, Alcorn MJ, Richmond L, and Holyoake TL (2002) Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 99:319-325.
17. Huang M, Dorsey JF, Epling-Burnette PK, Nimmanapalli R, Landowski TH, Mora LB, Niu G, Sinibaldi D, Bai F, Kraker A, et al. (2002) Inhibition of Bcr-Abl kinase activity by PD180970 blocks constitutive activation of Stat5 and growth of CML cells. Oncogene 21:8804-8816.
18. La Rosée P, Corbin AS, Stoffregen EP, Deininger MW, and Druker BJ (2002) Activity of the Bcr-Abl kinase inhibitor PD180970 against clinically relevant Bcr-Abl isoforms that cause resistance to imatinib mesylate (Gleevec, STI571). Cancer Res 62:7149-7153.
19. Lierman E, Folens C, Stover EH, Mentens N, Van Miegroet H, Scheers W, Boogaerts M, Vandenberghe P, Marynen P, and Cools J (2006) Sorafenib (BAY43-9006) is a potent inhibitor of FIP1L1-PDGFRα and the imatinib resistant FIP1L1-PDGFRα T674I Mutant. Blood 108:1374-1376.
20. Lyons JF, Wilhelm S, Hibner B, and Bollag G (2001) Discovery of a novel raf kinase inhibitor. Endocr Relat Cancer 8:219-225.
21. Malhi H, Bronk SF, Werneburg NW, and Gores GJ (2006) Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J Biol Chem 281:12093-12101.
22. Mazurkiewicz-Munoz AM, Argetsinger LS, Kouadio JL, Stensballe A, Jensen ON, Cline JM, and Carter-Su C (2006) Phosphorylation of JAK2 at serine 523: a negative regulator of JAK2 that is stimulated by growth hormone and epidermal growth factor. Mol Cell Biol 26:4052-4062.
23. Moulding DA, Giles RV, Spiller DG, White MR, Tidd DM, and Edwards SW (2000) Apoptosis is rapidly triggered by antisense depletion of MCL-1 in differentiating U937 Cells. Blood 96:1756-1763.
24. O'Hare T, Walters DK, Stoffregen EP, Jia T, Manley PW, Mestan J, Cowan-Jacob SW, Lee FY, Heinrich MC, Deininger MW, et al. (2005) In vitro activity of Bcr-Abl inhibitors AMN107 and BMS-354825 against clinically relevant imatinib-resistant Abl kinase domain mutants. Cancer Res 65:4500-4505.
25. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K, and Korsmeyer SJ (2005) Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307:1101-1104.
26. Rahmani M, Dai Y, and Grant S (2002) The histone deacetylase inhibitor sodium butyrate interacts synergistically with phorbol myristate acetate (PMA) to induce mitochondrial damage and apoptosis in human myeloid leukemia cells through a tumor necrosis factor-alpha-mediated process. Exp Cell Res 277:31-47.
27. Rahmani M, Davis EM, Bauer C, Dent P, and Grant S (2005a) Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves downregulation of Mcl-1 through inhibition of translation. J Biol Chem 280:35217-35227.
28. Rahmani M, Reese E, Dai Y, Bauer C, Kramer LB, Huang M, Jove R, Dent P, and Grant S (2005b) Cotreatment with suberanoylanilide hydroxamic acid and 17-allylamino 17-demethoxygeldanamycin synergistically induces apoptosis in Bcr-Abl+ cells sensitive and resistant to STI571 (imatinib mesylate) in association with down-regulation of Bcr-Abl, abrogation of signal transducer and activator of transcription 5 activity, and Bax conformational change. Mol Pharmacol 67:1166-1176.
29. Rajagopalan H, Bardelli A, Lengauer C, Kinzler KW, Vogelstein B, and Velculescu VE (2002) Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature 418:934.
30. Strumberg D, Richly H, Hilger RA, Schleucher N, Korfee S, Tewes M, Faghih M, Brendel E, Voliotis D, Haase CG, et al. (2005) Phase I clinical and pharmacokinetic study of the novel Raf kinase and vascular endothelial growth factor receptor inhibitor BAY 43-9006 in patients with advanced refractory solid tumors. J Clin Oncol 23:965-972.
31. Talpaz M, Shah NP, Kantarjian H, Donato N, Nicoll J, Paquette R, Cortes J, O'Brien S, Nicaise C, Bleickardt E, et al. (2006) Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 354:2531-2541.
32. ten Hoeve J, Arlinghaus RB, Guo JQ, Heisterkamp N, and Groffen J (1994) Tyrosine phosphorylation of CRKL in Philadelphia+ leukemia. Blood 84:1731-1736.
33. Van Etten RA (2004) Mechanisms of transformation by the BCR-ABL oncogene: new perspectives in the post-imatinib era. Leuk Res 28 (Suppl 1):S21-S28.
34. von Bubnoff N, Manley PW, Mestan J, Sanger J, Peschel C, and Duyster J (2006) Bcr-Abl resistance screening predicts a limited spectrum of point mutations to be associated with clinical resistance to the Abl kinase inhibitor nilotinib (AMN107). Blood 108:1328-1333.
35. Walz C and Sattler M (2006) Novel targeted therapies to overcome imatinib mesylate resistance in chronic myeloid leukemia (CML). Crit Rev Oncol Hematol 57:145-164.
36. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, Chen C, Zhang X, Vincent P, McHugh M, et al. (2004) BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 64:7099-7109.
37. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams JM, and Huang DC (2005) Proapoptotic Bak is sequestered by Mcl-1 and Bcl-XL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19:1294-1305.
38. Young MA, Shah NP, Chao LH, Seeliger M, Milanov ZV, Biggs WH III, Treiber DK, Patel HK, Zarrinkar PP, Lockhart DJ, et al. (2006) Structure of the kinase domain of an imatinib-resistant Abl mutant in complex with the aurora kinase inhibitor VX-680. Cancer Res 66:1007-1014.
39. Yu C, Bruzek LM, Meng XW, Gores GJ, Carter CA, Kaufmann SH, and Adjei AA (2005) The role of Mcl-1 downregulation in the proapoptotic activity of the multikinase inhibitor BAY 43-9006. Oncogene 24:6861-6869.
40. Yu C, Krystal G, Varticovksi L, McKinstry R, Rahmani M, Dent P, and Grant S (2002) Pharmacologic mitogen-activated protein/extracellular signal-regulated kinase kinase/mitogen-activated protein kinase inhibitors interact synergistically with STI571 to induce apoptosis in Bcr/Abl-expressing human leukemia cells. Cancer Res 62:188-199.