The proteasome inhibitor bortezomib interacts synergistically with histone deacetylase inhibitors to induce apoptosis in Bcr/Abl+ cells sensitive and resistant to STI571

Blood

Volumn 102, Issue 10, 2003, Pages 3765-3774

  Yu, Chunrong ^b   Rahmani, Mohamed ^b   Conrad, Daniel ^b   Subler, Mark ^b   Dent, Paul ^b   Grant, Steven ^a  

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

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; BCR ABL PROTEIN; BORTEZOMIB; BUTYRIC ACID; CASPASE 3; CASPASE 8; CYCLIN D1; HISTONE DEACETYLASE INHIBITOR; IMATINIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEASOME INHIBITOR; PROTEIN P21; RAF PROTEIN; REACTIVE OXYGEN METABOLITE; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG; VORINOSTAT;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME DEGRADATION; HEMATOLOGIC MALIGNANCY; HUMAN; HUMAN CELL; LEUKEMIA CELL; MITOCHONDRION; MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION;

EID: 0242493856     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2003-03-0737     Document Type: Article

References (54)

1. Sawyers CL. Chronic myeloid leukemia. N Engl J Med. 1999;340:1330-1340.
2. McLaughlin J, Chianese E, Witte ON. In vitro transformation of immature hematopoietic cells by the P210 BCR/ABL oncogene product of the Philadelphia chromosome. Proc Natl Acad Sci U S A. 1987;84:6558-6562.
3. McGahon A, Bissonnette R, Schmitt M, Cotter KM, Green DR, Cotter TG. BCR-ABL maintains resistance of chronic myelogenous leukemia cells to apoptotic cell death. Blood. 1994;83:1179-1187.
4. Bedi A, Barber JP, Bedi GC, et al. BCR-ABL-mediated inhibition of apoptosis with delay of G2/M transition after DNA damage: a mechanism of resistance to multiple anticancer agents. Blood. 1995;86:1148-1158.
5. Amarante-Mendes GP, McGahon AJ, Nishioka WK, Afar DE, Witte ON, Green DR. Bcl-2-independent Bcr-Abl-mediated resistance to apoptosis: protectionis correlated with up regulation of Bcl-xL. Oncogene. 1998;16:1383-1390.
6. Gesbert F, Sellers WR, Signoretti S, Loda M, Griffin JD. BCR/ABL regulates expression of the cyclin-dependent kinase inhibitor p27Kip1 through the phosphatidylinositol 3-Kinase/AKT pathway. J Biol Chem. 2000; 275:39223-39230.
7. Kang CD, Yoo SD, Hwang BW, et al. The inhibition of ERK/MAPK not the activation of JNK/ SAPK is primarily required to induce apoptosis in chronic myelogenous leukemic K562 cells. Leuk Res. 2000;24:527-534.
8. Sonoyama J, Matsumura I, Ezoe S, et al. Functional cooperation among Ras, STAT5, and phosphatidylinositol 3-kinase is required for full oncogenic activities of BCR/ABL in K562 cells. J Biol Chem. 2002;277:8076-8082.
9. Rhodes J, York RD, Tara D, Tajinda K, Druker BJ. CrkL functions as a nuclear adaptor and transcriptional activator in Bcr-Abl-expressing cells. Exp Hematol. 2000;28:305-310.
10. Druker BJ, Perspectives on the development of a molecularly targeted agent. Cancer Cell. 2002;1: 31-36.
11. Mow BM, Chandra J, Svingen PA, et al. Effects of the Bcr/abl kinase inhibitors STI571 and adaphostin (NSC 680410) on chronic myelogenous leukemia cells in vitro. Blood. 2002;99:664-671.
12. Kawaguchi Y, Jinnai I, Nagai K, et al. Effect of a selective Abl tyrosine kinase inhibitor, STI571, on in vitro growth of BCR-ABL-positive acute lymphoblastic leukemia cells. Leukemia 2001;15: 590-594.
13. Druker BJ, Talpaz M, Resta DJ, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001;344:1031-1037.
14. Gorre ME, Sawyers CL. Molecular mechanisms of resistance to STI571 in chronic myeloid leukemia. Curr Opin Hematol. 2002;9:303-307.
15. Almond JB, Cohen GM. The proteasome: a novel target for cancer chemotherapy. Leukemia. 2002; 16:433-443.
16. Lin ZP, Boller YC, Amer SM, et al. Prevention of brefeldin A-induced resistance to teniposide by the proteasome inhibitor MG-132: involvement of NF-kappaB activation in drug resistance. Cancer Res. 1998;58:3059-3065.
17. Adams J, Palombella VJ, Sausville EA, et al. Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res. 1999;59: 2615-2622.
18. An B, Goldfarb RH, Siman R, Dou QP. Novel dipeptidyl proteasome inhibitors overcome Bcl-2 protective function and selectively accumulate the cyclin-dependent kinase inhibitor p27 and induce apoptosis in transformed, but not normal, human fibroblasts. Cell Death Differ. 1998;5: 1062-1075.
19. Cusack JC Jr, Liu R, Houston M, et al. Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-kappaB inhibition. Cancer Res. 2001;61: 3535-3540.
20. Orlowski RZ, Stinchcombe TE, Mitchell BS, et al. Phase I trial of the proteasome inhibitor PS-341 in patients with refractory hematologic malignancies. J Clin Oncol. 2002;20:4420-4427.
21. Marks P, Rifkind RA, Richon VM, Breslow R, Miller T, Kelly WK. Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer. 2001 1:194-202.
22. Rosato RR, Wang Z, Gopalkrishnan RV, Fisher PB, Grant S. Evidence of a functional role for the cyclin-dependent kinase-inhibitor p21WAF1/CIP1/MDA6 in promoting differentiation and preventing mitochondrial dysfunction and apoptosis induced by sodium butyrate in human myelomonocytic leukemia cells (U937). Int J Oncol. 2001;19:181-191.
23. Ruefli AA, Ausserlechner MJ, Bernhard D, et al. The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc Natl Acad Sci U S A. 2001; 98:10833-10838.
24. Witt O, Sand K, Pekrun A. Butyrate-induced erythroid differentiation of human K562 leukemia cells involves inhibition of ERK and activation of p38 MAP kinase pathways. Blood. 2000;95:2391-2396.
25. O'Connor O, Kelly W, Wang ES, et al. Clinical development of the histone deacetylase inhibitor suberoylanalide hyroxamic acid (SAHA) in aggressive non-Hodgkin's lymphoma (NHL) and Hodgkin's disease (HD) [abstract]. Blood. 2001; 98:611a.
26. Sandor V, Bakke S, Robey RW, et al. Phase I trial of the histone deacetylase inhibitor, depsipeptide (FR901228, NSC 630176), in patients with refractory neoplasms. Clin Cancer Res. 2002;8:718-728.
27. Gore SD, Weng LJ, Figg WD, et al. Impact of prolonged infusions of the putative differentiating agent sodium phenylbutyrate on myelodysplastic syndromes and acute myeloid leukemia. Clin Cancer Res. 2002;8:963-970.
28. Yin L, Laevsky G, Giardina C. Butyrate suppression of colonocyte NF-kappa B activation and cellular proteasome activity. J Biol Chem. 2001;276: 44641-44646.
29. Yu C, Krystal G, Varticovksi L, et al. Pharmacologic mitogen-activated protein/extracellular signal-regulated kinase kinase/mitogen-activated protein kinase inhibitors interact synergistically with ST1571 to induce apoptosis in Bcr/Abl-expressing human leukemia cells. Cancer Res. 2002;62:188-199.
30. Yu C, Krystal G, Dent P, Grant S. Flavopiridol potentiates STI571-induced mitochondrial damage and apoptosis in BCR-ABL-positive human leukemia cells. Clin Cancer Res. 2002;8:2976-2984.
31. Rahmani M, Peron P, Weitzman J, Bakiri L, Lardeux B, Bernuau D. Functional cooperation between JunD and NF-kappaB in rat hepatocytes. Oncogene. 2001;20:5132-5142.
32. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 1984;22:27-55.
33. Ghezzi P, Bianchi M, Gianera L, Landolfo S, Salmona M. Role of reactive oxygen intermediates in the interferon-mediated depression of hepatic drug metabolism and protective effect of N-acetylcysteine in mice. Cancer Res. 1985; 45:3444-3447.
34. Giuliano M, Lauricella M, Calvaruso G, et al. The apoptotic effects and synergistic interaction of sodium butyrate and MG132 in human retinoblastoma Y79 cells. Cancer Res. 1999;59:5586-5595.
35. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 1995;270: 1326-1331.
36. Tournier C, Hess P, Yang DD, et al. The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase. Mol Cell Biol. 2002; 22:4929-4942.
37. Tacchini L, Dansi P, Matteucci E, Bernelli-Zazzera A, Desiderio MA. Influence of proteasome and redox state on heat shock-induced activation of stress kinases, AP-1 and HSF. Biochim Biophys Acta. 2001; 1538:76-89.
38. Orlowski RZ, Small GW, Shi YY. Evidence that inhibition of p44/42 mitogen-activated protein kinase signaling is a factor in proteasome inhibitormediated apoptosis. J Biol Chem. 2002;277: 27864-27871.
39. Yu X, Guo ZS, Marcu MG, et al. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J Natl Cancer Inst. 2002;94:504-513.
40. + human leukemia cells sensitive and resistant to STI571. Cancer Res. 2003; 63:2118-2126.
41. Nimmanapalli R, Fuino L, Stobaugh C, Richon V, Bhalla K. Cotreatment with the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) enhances imatinib-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Blood. 2003;101:3236-3239.
42. Asada M, Yamada T, Ichijo H, et al. Apoptosis inhibitory activity of cytoplasmic p21(Cip1/WAF1) in monocytic differentiation. EMBO J. 1999; 18: 1223-1234.
43. Vrana JA, Decker RH, Johnson CR, et al. Induction of apoptosis in U937 human leukemia cells by suberoylanilide hydroxamic acid (SAHA) proceeds through pathways that are regulated by Bcl-2/Bcl-XL, c-Jun, and p21CIP1, but independent of p53. Oncogene. 1999; 18:7016-7025.
44. Di Cunto F, Topley G, Calautti E, et al. Inhibitory function of p21Cip1/WAF1 in differentiation of primary mouse keratinocytes independent of cell cycle control. Science. 1998;280:1069-1072.
45. Chinery R, Brockman JA, Peeler MO, Shyr Y, Beauchamp RD, Coffey RJ. Antioxidants enhance the cytotoxicity of chemotherapeutic agents in colorectal cancer: a p53-independent induction of p21WAF1/CIP1 via C/EBPbeta. Nat Med. 1997;3:1233-1241.
46. Levkau B, Koyama H, Raines EW, et al. Cleavage of p21Cip1/Waf1 and p27Kip1 mediates apoptosis in endothelial cells through activation of Cdk2: role of a caspase cascade. Mol Cell. 1998; 1:553-563.
47. Nahta R, Iglehart JD, Kempkes B, Schmidt EV. Rate-limiting effects of cyclin D1 in transformation by ErbB2 predicts synergy between herceptin and flavopiridol. Cancer Res. 2002;62:2267-2271.
48. Chau BN, Wang JY. Coordinated regulation of life and death by RB. Nat Rev Cancer. 2003;3:130-138.
49. Chai J, Du C, Wu JW, Kyin S, Wang X, Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature. 2000;406:855-862.
50. Zhang B, Gojo I, Fenton RG. Myeloid cell factor-1 is a critical survival factor for multiple myeloma. Blood. 2002;99:1885-1893.
51. Schreck R, Albermann K, Baeuerle PA. Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells. Free Radic Res Commun. 1992;17:221-237.
52. Macip S, Igarashi M, Fang L, et al. Inhibition of p21-mediated ROS accumulation can rescue p21-induced senescence. EMBO J. 2002;21: 2180-2188.
53. Shah NP, Nicoll JM, Nagar B, et al. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell. 2002;2:117-125.
54. La Rosee P, Corbin AS, Stoffregen EP, Deininger MW, Druker BJ. Activity of the Bcr-Abl kinase inhibitor PD180970 against clinically relevant Bcr-Abl isoforms that cause resistance to imatinib mesylate (Gleevec, STI571). Cancer Res. 2002; 62:7149-7153.