NPI-0052, a novel proteasome inhibitor, induces caspase-8 and ROS-dependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells

Blood

Volumn 110, Issue 1, 2007, Pages 267-277

  Miller, Claudia P ^a   Ban, Kechen ^a   Dujka, Melanie E ^a   McConkey, David J ^a   Munsell, Mark ^a   Palladino, Michael ^b   Chandra, Joya ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Nereus Pharmaceuticals Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; BORTEZOMIB; CASPASE; CASPASE 8; CASPASE 8 INHIBITOR; CASPASE 9 INHIBITOR; CHYMOTRYPSIN; DNA FRAGMENT; FAS ASSOCIATED DEATH DOMAIN PROTEIN; HISTONE DEACETYLASE INHIBITOR; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; NPI 0052; PROTEASOME; PROTEASOME INHIBITOR; REACTIVE OXYGEN METABOLITE; TRYPSIN; UNCLASSIFIED DRUG; VALPROIC ACID;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER MODEL; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA; LEUKEMIA CELL; LEUKEMIA CELL LINE; LEUKOCYTE COUNT; MALE; MONONUCLEAR CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHILADELPHIA 1 CHROMOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; WILD TYPE;

EID: 34347375499     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-03-013128     Document Type: Article

References (49)

1. Coux O, Tanaka K, Goldberg AL. Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem. 1996;65:801-847.
2. Wolf DH, Hilt W. The proteasome: a proteolytic nanomachine of cell regulation and waste disposal. Biochim Biophys Acta. 2004;1695:19-31.
3. Orlowski M, Wilk S. Catalytic activities of the 20 S proteasome, a multicatalytic proteinase complex. Arch Biochem Biophys. 2000;383:1-16.
4. Kisselev AF, Akopian TN, Castillo V, Goldberg AL. Proteasome active sites allosterically regulate each other, suggesting a cyclical bite-chew mechanism for protein breakdown. Mol Cell. 1999;4:395-402.
5. Adams J. The proteasome: a suitable antineoplastic target. Nat Rev Cancer. 2004;4:349-360.
6. Adams J. The development of proteasome inhibitors as anticancer drugs. Cancer Cell. 2004;5:417-421.
7. Adams J, Kauffman M. Development of the proteasome inhibitor Velcade (Bortezomib). Cancer Invest. 2004;22:304-311.
8. Leonard JP, Furman RR, Coleman M. Proteasome inhibition with bortezomib: a new therapeutic strategy for non-Hodgkin's lymphoma. Int J Cancer. 2006;119:971-979.
9. Williams S, Pettaway C, Song R, Papandreou C, Logothetis C, McConkey DJ. Differential effects of the proteasome inhibitor bortezomib on apoptosis and angiogenesis in human prostate tumor xenografts. Mol Cancer Ther. 2003;2:835-843.
10. Nawrocki ST, Bruns CJ, Harbison MT, et al. Effects of the proteasome inhibitor PS-341 on apoptosis and angiogenesis in orthotopic human pancreatic tumor xenografts. Mol Cancer Ther. 2002;1:1243-1253.
11. Perez-Galan P, Roue G, Villamor N, Montserrat E, Campo E, Colomer D. The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood. 2006;107:257-264.
12. Fribley A, Zeng Q, Wang CY. Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells. Mol Cell Biol. 2004;24:9695-9704.
13. Qin JZ, Ziffra J, Stennett L, et al. Proteasome inhibitors trigger NOXA-mediated apoptosis in melanoma and myeloma cells. Cancer Res. 2005;65:6282-6293.
14. Scagliotti G. Proteasome inhibitors in lung cancer. Crit Rev Oncol Hematol. 2006;58:177-189.
15. Adams J. The proteasome as a novel target for the treatment of breast cancer. Breast Dis. 2002;15:61-70.
16. Yu C, Rahmani M, Dent P, Grant S. The hierarchical relationship between MAPK signaling and ROS generation in human leukemia cells undergoing apoptosis in response to the proteasome inhibitor Bortezomib. Exp Cell Res. 2004;295:555-566.
17. Voorhees PM, Orlowski RZ. The proteasome and proteasome inhibitors in cancer therapy. Annu Rev Pharmacol Toxicol. 2006;46:189-213.
18. Feling RH, Buchanan GO, Mincer TJ, Kauffman CA, Jensen PR, Fenical W. Salinosporamide A: a highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus salinospora. Angew Chem Int Ed Engl. 2003;42:355-357.
19. Macherla VR, Mitchell SS, Manam RR, et al. Structure-activity relationship studies of salino-sporamide A (NPI-0052), a novel marine derived proteasome inhibitor. J Med Chem. 2005;48:3684-3687.
20. Corey EJ, Li WD. Total synthesis and biological activity of lactacystin, omuralide and analogs. Chem Pharm Bull (Tokyo). 1999;47:1-10.
21. Chauhan D, Catley L, Li G, et al. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib. Cancer Cell. 2005;8:407-419.
22. Williamson MJ, Blank JL, Bruzzese FJ, et al. Comparison of biochemical and biological effects of ML858 (salinosporamide A) and bortezomib. Mol Cancer Ther. 2006;5:3052-3061.
23. Rajkumar SV, Richardson PG, Hideshima T, Anderson KC. Proteasome inhibition as a novel therapeutic target in human cancer. J Clin Oncol. 2005;23:630-639.
24. Ling YH, Liebes L, Zou Y, Perez-Soler R. Reactive oxygen species generation and mitochondrial dysfunction in the apoptotic response to Bortezomib, a novel proteasome inhibitor, in human H460 non-small cell lung cancer cells. J Biol Chem. 2003;278:33714-33723.
25. Mitsiades N, Mitsiades CS, Poulaki V, et al. Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proc Natl Acad Sci U S A. 2002;99:14374-14379.
26. Nawrocki ST, Carew JS, Dunner K Jr, et al. Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res. 2005;65:11510-11519.
27. Chandra J, Hackbarth J, Le S, et al. Involvement of reactive oxygen species in adaphostin-induced cytotoxicity in human leukemia cells. Blood. 2003;102:4512-4519.
28. Lightcap ES, McCormack TA, Pien CS, Chau V, Adams J, Elliott PJ. Proteasome inhibition measurements: clinical application. Clin Chem. 2000;46:673-683.
29. Chandra J, Niemer I, Gilbreath J, et al. Proteasome inhibitors induce apoptosis in glucocorticoid-resistant chronic lymphocytic leukemic lymphocytes. Blood. 1998;92:4220-4229.
30. Meng XW, Chandra J, Loegering D, et al. Central role of Fas-associated death domain protein in apoptosis induction by the mitogen-activated protein kinase kinase inhibitor CI-1040 (PD184352) in acute lymphocytic leukemia cells in vitro. J Biol Chem. 2003;278:47326-47339.
31. Chandra J, Tracy J, Loegering D, et al. Adaphostin-induced oxidative stress overcomes BCR/ABL mutation-dependent and -independent imatinib resistance. Blood. 2006;107:2501-2506.
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. Kudo Y, Takata T, Ogawa I, et al. p27Kip1 accumulation by inhibition of proteasome function induces apoptosis in oral squamous cell carcinoma cells. Clin Cancer Res. 2000;6:916-923.
34. An WG, Hwang SG, Trepel JB, Blagosklonny MV. Protease inhibitor-induced apoptosis: accumulation of wt p53, p21WAF1/CIP1, and induction of apoptosis are independent markers of proteasome inhibition. Leukemia. 2000;14:1276-1283.
35. Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407:770-776.
36. Yin XM, Wang K, Gross A, et al. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature. 1999;400:886-891.
37. Armstrong JS. Mitochondrial membrane permeabilization: the sine qua non for cell death. Bioessays. 2006;28:253-260.
38. 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.
39. Yu C, Rahmani M, Conrad D, Subler M, Dent P, Grant S. The proteasome inhibitor bortezomib interacts synergistically with histone deacetylase inhibitors to induce apoptosis in Bcr/Abl+ cells sensitive and resistant to STI571. Blood. 2003;102:3765-3774.
40. Ruiz S, Krupnik Y, Keating M, Chandra J, Palladino M, McConkey D. The proteasome inhibitor NPI-0052 is a more effective inducer of apoptosis than bortezomib in lymphocytes from patients with chronic lymphocytic leukemia. Mol Cancer Ther. 2006;5:1836-1843.
41. Kisselev AF, Callard A, Goldberg AL. Importance of the proteasome's different proteolytic sites and the efficacy of inhibitors varies with the protein substrate. J Biol Chem. 2006;281:8582-8590.
42. Johnson TR, Stone K, Nikrad M, et al. The proteasome inhibitor PS-341 overcomes TRAIL resistance in Bax and caspase 9-negative or Bcl-xL overexpressing cells. Oncogene. 2003;22:4953-4963.
43. Yoshida T, Shiraishi T, Nakata S, et al. Proteasome inhibitor MG132 induces death receptor 5 through CCAAT/enhancer-binding protein homologous protein. Cancer Res. 2005;65:5662-5667.
44. Hougardy BM, Maduro JH, van der Zee AG, et al. Proteasome inhibitor MG132 sensitizes HPV-positive human cervical cancer cells to rhTRAIL-induced apoptosis. Int J Cancer. 2006;118:1892-1900.
45. Sayers TJ, Brooks AD, Koh CY, et al. The proteasome inhibitor PS-341 sensitizes neoplastic cells to TRAIL-mediated apoptosis by reducing levels of c-FLIP. Blood. 2003;102:303-310.
46. Wu HM, Chi KH, Lin WW. Proteasome inhibitors stimulate activator protein-1 pathway via reactive oxygen species production. FEBS Lett. 2002;526:101-105.
47. Pei XY, Dai Y, Grant S. Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitors. Clin Cancer Res. 2004;10:3839-3852.
48. Denlinger CE, Rundall BK, Jones DR. Proteasome inhibition sensitizes non-small cell lung cancer to histone deacetylase inhibitor-induced apoptosis through the generation of reactive oxygen species. J Thorac Cardiovasc Surg. 2004;128:740-748.
49. Ungerstedt JS, Sowa Y, Xu WS, et al. Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proc Natl Acad Sci U S A. 2005;102:673-678.