The proteasome inhibitor bortezomib promotes mitochondrial injury and apoptosis induced by the small molecule Bcl-2 inhibitor HA14-1 in multiple myeloma cells

Leukemia

Volumn 17, Issue 10, 2003, Pages 2036-2045

  Pei, X Y ^a   Dai, Y ^a   Grant, S ^a  

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

Author keywords

Apoptosis; Bcl 2; HA14 1; Mitochondrial injury; Myeloma; ROS

Indexed keywords

2 AMINO 6 BROMO 4 (1 CYANO 2 ETHOXY 2 OXOETHYL) 4H CHROMENE 3 CARBOXYLIC ACID ETHYL ESTER; ACETYLCYSTEINE; ANTISENSE OLIGONUCLEOTIDE; APOPTOSIS INDUCING FACTOR; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; CASPASE 3; CASPASE 8; CASPASE 9; CYTOCHROME C; CYTOTOXIC AGENT; DEXAMETHASONE; ENZYME PRECURSOR; INTERLEUKIN 6; JANUS KINASE; MITOCHONDRIAL PROTEIN; OBLIMERSEN; PROTEASOME INHIBITOR; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN INHIBITOR; PROTEIN MCL 1; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SCAVENGER; UNCLASSIFIED DRUG; UNINDEXED DRUG; ANTINEOPLASTIC AGENT; BORONIC ACID DERIVATIVE; CYSTEINE PROTEINASE; MULTIENZYME COMPLEX; PROTEASOME; PROTEINASE INHIBITOR; PYRAZINE DERIVATIVE;

APOPTOSIS; ARTICLE; BIOACCUMULATION; CANCER CELL CULTURE; CANCER RESISTANCE; CELL DAMAGE; CELL MEMBRANE POTENTIAL; CELL SECRETION; CLONOGENESIS; CONTROLLED STUDY; DRUG EXPOSURE; ENZYME ACTIVATION; ENZYME INDUCTION; HUMAN; HUMAN CELL; MITOCHONDRION; MOLECULAR SIZE; MULTIPLE MYELOMA; MYELOMA CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN INDUCTION; PROTEIN SECRETION; PROTEIN TRANSPORT; TIME; TREATMENT PLANNING; UPREGULATION; CELL CULTURE; CELL DIVISION; DRUG ANTAGONISM; DRUG EFFECT; PHYSIOLOGY;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BORONIC ACIDS; CELL DIVISION; CYSTEINE ENDOPEPTIDASES; CYTOCHROME C GROUP; DEXAMETHASONE; HUMANS; MEMBRANE POTENTIALS; MITOCHONDRIA; MULTIENZYME COMPLEXES; MULTIPLE MYELOMA; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES; TUMOR CELLS, CULTURED;

EID: 0142244338     PISSN: 08876924     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.leu.2403109     Document Type: Article

References (57)

1. Johnstone RW, Ruefli AA, Lowe SW. Apoptosis: a link between cancer genetics and chemotherapy. Cell 2002; 108: 153-164.
2. Schimmer AD, Hedley DW, Penn LZ, Minden MD. Receptor- and mitochondrial-mediated apoptosis in acute leukemia: a translational view. Blood 2001; 98: 3541-3553.
3. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001; 15: 2922-2933.
4. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000; 102: 33-42.
5. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000; 102: 45-53.
6. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397: 441-446.
7. Igney FH, Krammer PH. Death and anti-death: tumor resistance to apoptosis. Nat Rev Cancer 2002; 2: 277-288.
8. Cory S, Adams JM. The Bcl-2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002; 2: 647-656.
9. L sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell 2001; 8: 705-711.
10. Gutierrez-Puente Y, Zapata-Benavides P, Tari AM, Lopez-Berestein C. Bcl-2-related antisense therapy. Semin Oncol 2002; 29: 71-76.
11. Wang JL, Liu D, Zhang ZJ, Shan S, Han X, Srinivasula SM et al. Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc Natl Acad Sci USA 2000; 97: 7124-7129.
12. Dalton WS, Bergsagel PL, Kuehl WM, Anderson KC, Harousseau JL. Multiple myeloma. Hematology 2001, 157-177.
13. Strasser K, Ludwig H. Thalidomide treatment in multiple myeloma. Blood Rev 2002; 16: 207-215.
14. Anderson KC, Boise LH, Louie R, Waxman S. Arsenic trioxide in multiple myeloma: rationale and future directions. Cancer J 2002; 8: 12-25.
15. Hideshima T, Richardson P, Chauhan D, Palombella VJ, Elliott PJ, Adams J et al. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res 2001; 61: 3071-3076.
16. Hideshima T, Mitsiades C, Akiyama M, Hayashi T, Chauhan D, Richardson P et al. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood 2003; 101: 1530-1534.
17. Mitsiades N, Mitsiades CS, Poulaki V, Chauhan D, Fanourakis G, Gu X et al. Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proc Natl Acad Sci USA 2002; 99: 14374-14379.
18. Adams J. Proteasome inhibition: a novel approach to cancer therapy. Trends Mol Med 2002; 8: S49-S54.
19. LeBlanc R, Catley LP, Hideshima T, Lentzsch S, Mitsiades CS, Mitsiades N et al. Proteasome inhibitor PS-341 inhibits human myeloma cell growth in vivo and prolongs survival in a murine model. Cancer Res 2002; 62: 4996-5000.
20. Orlowski RZ, Stinchcombe TE, Mitchell BS, Shea TC, Baldwin AS, Stahl S 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. 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.
22. Mitsiades N, Mitsiades CS, Richardson PC, Poulaki V, Tai YT, Chauhan D et al. The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications. Blood 2003; 101: 2377-2380.
23. Moalli PA, Pillay S, Weiner D, Leikin R, Rosen ST. A mechanism of resistance to glucocorticoids in multiple myeloma: transient expression of a truncated glucocorticoid receptor mRNA. Blood 1992; 79: 213-222.
24. Dai Y, Yu C, Singh V, Tang L, Wang Z, McInistry R et al. Pharmacological inhibitors of the mitogen-activated protein kinase (MAPK) kinase/MAPK cascade interact synergistically with UCN-01 to induce mitochondrial dysfunction and apoptosis in human leukemia cells. Cancer Res 2001; 61: 5106-5115.
25. Dai Y, Landowski TH, Rosen ST, Dent P, Grant S. Combined treatment with the checkpoint abrogator UCN-01 and MEK1/2 inhibitors potently induces apoptosis in drug-sensitive and -resistant myeloma cells through an IL-6-independent mechanism. Blood 2002; 100: 3333-3343.
26. Leach JK, Tuyle GV, Lin PS, Schmidt-Ullrich R, Mikkelsen RB. Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res 2001; 61: 3894-3901.
27. 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.
28. Ao Y, Rohde LH, Naumovski L. p53-interacting protein 53BP2 inhibits clonogenic survival and sensitizes cells to doxorubicin but not paclitaxel-induced apoptosis. Oncogene 2001; 20: 2720-2725.
29. Kirsch DG, Doseff A, Chau BN, Lim DS, de Souza-Pinto NC, Hansford R et al. Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochrome c. J Biol Chem 1999; 274: 21155-21161.
30. 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.
31. Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis. Genes Dev 1999; 13: 1899-1911.
32. Grad JM, Bahlis NJ, Reis I, Oshiro MM, Dalton WS, Boise LH. Ascorbic acid enhances arsenic trioxide-induced cytotoxicity in multiple myeloma cells. Blood 2001; 98: 805-813.
33. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 2001; 98: 13681-13686.
34. Frassanito MA, Cusmai A, Iodice G, Dammacco F. Autocrine interleukin-6 production and highly malignant multiple myeloma: relation with resistance to drug-induced apoptosis. Blood 2001; 97: 483-489.
35. Hideshima T, Chauhan D, Podar K, Schlossman RL, Richardson P, Anderson KC. Novel therapies targeting the myeloma cell and its bone marrow microenvironment. Semin Oncol 2001; 28: 607-612.
36. Chen J, Freeman A, Liu J, Dai Q, Lee RM. The apoptotic effect of HA14-1, a Bcl-2-molecular compound, requires Bax translocation and is enhanced by PK11195. Mol Cancer Ther 2002; 1: 961-967.
37. McEnery MW, Snowman AM, Trifiletti RR, Snyder SH. Isolation of the mitochondrial benzodiazepine receptor: association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc Natl Acad Sci USA 1992; 89: 3170-3174.
38. Breitschopf K, Zeiher AM, Dimmeler S. Ubiquitin-mediated degradation of the proapoptotic active form of bid. A functional consequence on apoptosis induction. J Biol Chem 2000; 275: 21648-21652.
39. Li B, Dou QP. Bax degradation by the ubiquitin/proteasome-dependent pathway: involvement in tumor survival and progression. Proc Natl Acad Sci USA 2000; 97: 3850-3855.
40. Chadebech P, Brichese L, Baldin V, Vidal S, Valette A. Phosphorylation and proteasome-dependent degradation of Bcl-2 in mitotic-arrested cells after microtubule damage. Biochem Biophys Res Commun 1999; 262: 823-827.
41. Mahyar-Roemer M, Roemer K. p21 Waf1/Cip1 can protect human colon carcinoma cells against p53-dependent and p53-independent apoptosis induced by natural chemopreventive and therapeutic agents. Oncogene 2001; 20: 3387-3398.
42. Xiang H, Fox JA, Totpal K, Aikawa M, Dupree K, Sinicropi D et al. Enhanced tumor killing by Apo2L/TRAIL and CPT-11 co-treatment is associated with p21 cleavage and differential regulation of Apo2L/TRAIL ligand and its receptors. Oncogene 2002; 21: 3611-3619.
43. Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol 2000; 20: 7311-7318.
44. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 2000; 288: 870-874.
45. Chauhan D, Li G, Hideshima T, Podar K, Mitsiades C, Mitsiades N et al. JNK-dependent release of mitochondrial protein, SMAC during apoptosis in multiple myeloma (MM) cells. J Biol Chem 2003; 278: 17593-17596.
46. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 3: 577-590.
47. Amstad PA, Liu H, Ichimiya M, Berezesky IK, Trump BF, Buhimschi IA et al. BCL-2 is involved in preventing oxidant-induced cell death and in decreasing oxygen radical production. Redox Rep 2001; 6: 351-362.
48. Lezoualc'h F, Sagara Y, Holsboer F, Behl C. High constitutive NF-kappaB activity mediates resistance to oxidative stress in neuronal cells. J Neurosci 1998; 18: 3224-3232.
49. Hideshima T, Chauhan D, Richardson P, Mitsiades C, Mitsiades N, Hayashi T et al. NF-kappa B as a therapeutic target in multiple myeloma. J Biol Chem 2002; 277: 16639-16647.
50. Konopleva M, Tari AM, Estrov Z, Harris D, Xie Z, Zhao S et al. Liposomal Bcl-2 antisense oligonucleotides enhance proliferation, sensitize acute myeloid leukemia to cytosine-arabinoside, and induce apoptosis independent of other antiapoptotic proteins. Blood 2000; 95: 3929-3938.
51. van de Donk NW, Kamphuis MM, van Dijk M, Borst HP, Bloem AC, Lokhorst HM. Chemosensitization of myeloma plasma cells by an antisense-mediated downregulation of Bcl-2 protein. Leukemia 2003; 17: 211-219.
52. Marcucci G, Byrd JC, Dai G, Klisovic MI, Kourlas PJ, Young DC et al. Phase 1 and pharmacodynamic studies of G3139, a Bcl-2 antisense oligonucleotide, in combination with chemotherapy in refractory or relapsed acute leukemia. Blood 2003; 101: 425-432.
53. Morris MJ, Tong WP, Cordon-Cardo C, Drobnjak M, Kelly WK, Slovin SF et al. Phase I trial of BCL-2 antisense oligonucleotide (C3139) administered by continuous intravenous infusion in patients with advanced cancer. Clin Cancer Res 2002; 8: 679-683.
54. Liu Q, Gazitt Y. Potentiation of dexamethasone, taxel, and Ad-p53-induced apoptosis by Bcl-2 anti-sense oligodeoxynucleotides in drug-resistant multiple myeloma cells. Blood 2003; 101: 4105-4114.
55. Degterev A, Lugovskoy A, Cardone M, Mulley B, Wagner G, Mitchison T et al. Identification of small-molecule inhibitors of interaction between the BH3 domain and Bcl-xL. Nat Cell Biol 2001; 3: 173-182.
56. Milella M, Estrov Z, Kornblau SM, Carter BZ, Konopleva M, Tari A et al. Synergistic induction of apoptosis by simultaneous disruption of the Bcl-2 and MEK/MAPK pathways in acute myelogenous leukemia. Blood 2002; 99: 3461-3464.
57. Nimmanapalli R, O'Bryan E, Kuhn D, Yamaguchi H, Wang HG, Bhalla KN. Regulation of 17-AAG-induced apoptosis: role of Bcl-2, Bcl-xL, and Bax downstream of 17-AAG-mediated downregulation of Akt, Raf-1 and Src kinases. Blood 2003; 102: 269-275.