Proteasome inhibitors in acute leukemia

Expert Review of Anticancer Therapy

Volumn 13, Issue 3, 2013, Pages 327-337

  Niewerth, Denise ^a   Dingjan, Ilse ^a   Cloos, Jacqueline ^a   Jansen, Gerrit ^a   Kaspers, Gertjan ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

(immuno) proteasome inhibitor; acute leukemia; bortezomib; carfilzomib; CEP 18770; marizomib; MLN9708; multiple myeloma; ONX 0914; PR 924

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ANTINEOPLASTIC AGENT; BELINOSTAT; BORTEZOMIB; CARFILZOMIB; CYCLOPHOSPHAMIDE; CYTARABINE; DELANZOMIB; DEXAMETHASONE; DOXORUBICIN; ETOPOSIDE; GLUCOCORTICOID; IDARUBICIN; IXAZOMIB CITRATE; LENALIDOMIDE; METHOTREXATE; MIDOSTAURIN; MITOXANTRONE; NELFINAVIR; ONX 0914; OPROZOMIB; PLACEBO; PR 924; PROTEASOME INHIBITOR; SALINOSPORAMIDE A; SORAFENIB; THALIDOMIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VINCRISTINE; VORINOSTAT;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; CHRONIC LYMPHATIC LEUKEMIA; COMBINATION CHEMOTHERAPY; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG PROTEIN BINDING; DRUG SELECTIVITY; DRUG STRUCTURE; DRUG TARGETING; DRUG TOLERABILITY; HEMATOLOGIC MALIGNANCY; HUMAN; IC 50; LYMPHOMA; MONOTHERAPY; MULTIPLE MYELOMA; NEUROTOXICITY; NONHUMAN; PERIPHERAL NEUROPATHY; RECOMMENDED DRUG DOSE; REVIEW; SOLID TUMOR;

ANIMALS; ANTINEOPLASTIC AGENTS; CLINICAL TRIALS AS TOPIC; DRUG EVALUATION, PRECLINICAL; HUMANS; LEUKEMIA; PROTEASOME INHIBITORS; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 84874854942     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/era.13.4     Document Type: Review

References (77)

1. Pui CH, Mullighan CG, Evans WE, Relling MV. Pediatric acute lymphoblastic leukemia: where are we going and how do we get there? Blood 120(6), 1165-1174 (2012).
2. Kaspers GJ. Pediatric acute myeloid leukemia. Expert Rev. Anticancer Ther. 12(3), 405-413 (2012).
3. Pulte D, Redaniel MT, Jansen L, Brenner H, Jeffreys M. Recent trends in survival of adult patients with acute leukemia: overall improvements, but persistent and partly increasing disparity in survival of minority patients. Haematologica doi:10.3324/ haematol.2012.063602 (2012) (Epub ahead of print).
4. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat. Rev. Mol. Cell Biol. 6(1), 79-87 (2005).
5. Groettrup M, Kirk CJ, Basler M. Proteasomes in immune cells: more than peptide producers? Nat. Rev. Immunol. 10(1), 73-78 (2010).
6. Parlati F, Lee SJ, Aujay M et al. Carfilzomib can induce tumor cell death through selective inhibition of the chymotrypsinlike activity of the proteasome. Blood 114(16), 3439-3447 (2009).
7. Roccaro AM, Sacco A, Aujay M et al. Selective inhibition of chymotrypsin-like activity of the immunoproteasome and constitutive proteasome in Waldenstrom macroglobulinemia. Blood 115(20), 4051-4060 (2010).
8. Seifert U, Bialy LP, Ebstein F et al. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 142(4), 613-624 (2010).
9. Bianchi G, Oliva L, Cascio P et al. The proteasome load versus capacity balance determines apoptotic sensitivity of multiple myeloma cells to proteasome inhibition. Blood 113(13), 3040-3049 (2009).
10. Kumatori A, Tanaka K, Inamura N et al. Abnormally high expression of proteasomes in human leukemic cells. Proc. Natl Acad. Sci. USA 87(18), 7071-7075 (1990).
11. Orlowski RZ, Kuhn DJ. Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin. Cancer Res. 14(6), 1649-1657 (2008).
12. Kisselev AF, van der Linden WA, Overkleeft HS. Proteasome inhibitors: an expanding army attacking a unique target. Chem. Biol. 19(1), 99-115 (2012).
13. Kupperman E, Lee EC, Cao Y et al. Evaluation of the proteasome inhibitor MLN9708 in preclinical models of human cancer. Cancer Res. 70(5), 1970-1980 (2010).
14. Siegel DS, Martin T, Wang M et al. A Phase 2 study of single-agent carfilzomib (PX-171-003-A1) in patients with relapsed and refractory multiple myeloma. Blood 120(14), 2817-2825 (2012).
15. Chauhan D, Singh AV, Aujay M et al. A novel orally active proteasome inhibitor ONX 0912 triggers in vitro and in vivo cytotoxicity in multiple myeloma. Blood 116(23), 4906-4915 (2010).
16. Miller CP, Ban K, Dujka ME et al. NPI-0052, a novel proteasome inhibitor, induces caspase-8 and ROS-dependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells. Blood 110(1), 267-277 (2007).
17. Kuhn DJ, Orlowski RZ. The immunoproteasome as a target in hematologic malignancies. Semin. Hematol. 49(3), 258-262 (2012).
18. Huber EM, Groll M. Inhibitors for the immuno- and constitutive proteasome: current and future trends in drug development. Angew. Chem. Int. Ed. Engl. 51(35), 8708-8720 (2012).
19. Li X, Wood TE, Sprangers R et al. Effect of noncompetitive proteasome inhibition on bortezomib resistance. J. Natl Cancer Inst. 102(14), 1069-1082 (2010).
20. Ruschak AM, Slassi M, Kay LE, Schimmer AD. Novel proteasome inhibitors to overcome bortezomib resistance. J. Natl Cancer Inst. 103(13), 1007-1017 (2011).
21. Laubach JP, Schlossman RL, Mitsiades CS, Anderson KC, Richardson PG. Thalidomide, lenalidomide and bortezomib in the management of newly diagnosed multiple myeloma. Expert Rev. Hematol. 4(1), 51-60 (2011).
22. Cavo M, Tacchetti P, Patriarca F et al.; GIMEMA Italian Myeloma Network. Bortezomib with thalidomide plus dexamethasone compared with thalidomide plus dexamethasone as induction therapy before, and consolidation therapy after, double autologous stem-cell transplantation in newly diagnosed multiple myeloma: a randomised Phase 3 study. Lancet 376(9758), 2075-2085 (2010).
23. Richardson PG, Weller E, Lonial S et al. Lenalidomide, bortezomib, and dexamethasone combination therapy in patients with newly diagnosed multiple myeloma. Blood 116(5), 679-686 (2010).
24. Richardson PG, Xie W, Mitsiades C et al. Single-agent bortezomib in previously untreated multiple myeloma: efficacy, characterization of peripheral neuropathy, and molecular correlations with response and neuropathy. J. Clin. Oncol. 27(21), 3518-3525 (2009).
25. Arastu-Kapur S, Anderl JL, Kraus M et al. Nonproteasomal targets of the proteasome inhibitors bortezomib and carfilzomib: a link to clinical adverse events. Clin. Cancer Res. 17(9), 2734-2743 (2011).
26. Moreau P, Pylypenko H, Grosicki S et al. Subcutaneous versus intravenous administration of bortezomib in patients with relapsed multiple myeloma: a randomised, Phase 3, non-inferiority study. Lancet Oncol. 12(5), 431-440 (2011).
27. Assouline S, Chang JE, Cheson BD et al. Results of a Phase 1 dose-escalation study of once-weekly MLN9708, an investigational proteasome inhibitor, in patients with relapsed/refractory lymphoma. Presented at: ASH Annual Meeting. Atlanta, GA, USA, 8-11 December 2012.
28. Kumar S, Bensinger WI, Reeder CB et al. Weekly dosing of the investigational oral proteasome inhibitor MLN9708 in patients with relapsed and/or refractory multiple myeloma: results from a Phase 1 doseescalation study. Presented at: ASH Annual Meeting. San Diego, CA, USA, 10-13 December 2011.
29. Richardson PG, Baz R, Wang L et al. Investigational agent MLN9708, an oral proteasome inhibitor, in patients (Pts) with relapsed and/or refractory multiple myeloma (MM): results from the expansion cohorts of a Phase 1 dose-escalation study. Presented at: ASH Annual Meeting. San Diego, CA, USA, 10-13 December 2011.
30. Kumar SK, Berdeja JG, Niesvizky R et al. A Phase 1/2 study of weekly MLN9708, an investigational oral proteasome inhibitor, in combination with lenalidomide and dexamethasone in patients with previously untreated multiple myeloma (MM). Presented at: ASH Annual Meeting. Atlanta, GA, USA, 8-11 December 2012.
31. Gallerani E, Zucchetti M, Brunelli D et al. A first in human Phase I study of the proteasome inhibitor CEP-18770 in patients with advanced solid tumours and multiple myeloma. Eur. J. Cancer 49(2), 290-296 (2013).
32. Moreau P, Richardson PG, Cavo M et al. Proteasome inhibitors in multiple myeloma: 10 years later. Blood 120(5), 947-959 (2012).
33. Korde N, Zingone A, Kwok M et al. Phase II clinical and correlative study of carfilzomib, lenalidomide, and dexamethasone (CRd) in newly diagnosed multiple myeloma (MM) patients. Presented at: ASH Annual Meeting. Atlanta, GA, USA, 8-2 December 2012.
34. Mikhael JR, Reeder CB, Libby EN III et al. Results from the Phase II dose expansion of cyclophosphamide, carfilzomib, thalidomide and dexamethasone (CYCLONE) in patients with newly diagnosed multiple myeloma. Presented at: ASH Annual Meeting. Atlanta, GA, USA, 8-11 December 2012.
35. Sonneveld P, Asselbergs E, Zweegman S et al. Carfilzomib combined with thalidomide and dexamethasone (CTD) is an highly effective induction and consolidation treatment in newly diagnosed patients with multiple myeloma (MM) who are transplant candidate. Presented at: ASH Annual Meeting. Atlanta, GA, USA, 8-11 December 2012.
36. Savona MR, Berdeja JG, Lee SJ et al. A Phase 1b dose-escalation study of split-dose oprozomib (ONX0912) in patients with hematologic malignancies. Presented at: ASH Annual Meeting. Atlanta, GA, USA, 8-11 December 2012.
37. Richardson PG, Spencer A, Cannell P et al. Phase 1 clinical evaluation of twice-weekly marizomib (NPI-0052), a novel proteasome inhibitor, in patients with relapsed/ refractory multiple myeloma (MM). Presented at: ASH Annual Meeting. San Diego, CA, USA, 10-13 December 2011.
38. Muchamuel T, Basler M, Aujay MA et al. A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat. Med. 15(7), 781-787 (2009).
39. Franke NE, Niewerth D, Assaraf YG et al. Impaired bortezomib binding to mutant b5 subunit of the proteasome is the underlying basis for bortezomib resistance in leukemia cells. Leukemia 26(4), 757-768 (2012).
40. Singh AV, Bandi M, Aujay MA et al. PR-924, a selective inhibitor of the immunoproteasome subunit LMP-7, blocks multiple myeloma cell growth both in vitro and in vivo. Br. J. Haematol. 152(2), 155-163 (2011).
41. Horton TM, Pati D, Plon SE et al. A Phase 1 study of the proteasome inhibitor bortezomib in pediatric patients with refractory leukemia: a Children's Oncology Group study. Clin. Cancer Res. 13(5), 1516-1522 (2007).
42. Cortes J, Thomas D, Koller C et al. Phase I study of bortezomib in refractory or relapsed acute leukemias. Clin. Cancer Res. 10(10), 3371-3376 (2004).
43. Faderl S, Rai K, Gribben J et al. Phase II study of single-agent bortezomib for the treatment of patients with fludarabinerefractory B-cell chronic lymphocytic leukemia. Cancer 107(5), 916-924 (2006).
44. Santos FP, Kantarjian H, McConkey D et al. Pilot study of bortezomib for patients with imatinib-refractory chronic myeloid leukemia in chronic or accelerated Phase. Clin. Lymphoma. Myeloma Leuk. 11(4), 355-360 (2011).
45. Attar EC, De Angelo DJ, Supko JG et al. Phase I and pharmacokinetic study of bortezomib in combination with idarubicin and cytarabine in patients with acute myelogenous leukemia. Clin. Cancer Res. 14(5), 1446-1454 (2008).
46. Blum W, Schwind S, Tarighat SS et al. Clinical and pharmacodynamic activity of bortezomib and decitabine in acute myeloid leukemia. Blood 119(25), 6025-6031 (2012).
47. Orlowski RZ, Voorhees PM, Garcia RA et al. Phase 1 trial of the proteasome inhibitor bortezomib and pegylated liposomal doxorubicin in patients with advanced hematologic malignancies. Blood 105(8), 3058-3065 (2005).
48. Brown RE, Bostrom B, Zhang PL. Morphoproteomics and bortezomib/ dexamethasone-induced response in relapsed acute lymphoblastic leukemia. Ann. Clin. Lab. Sci. 34(2), 203-205 (2004).
49. Messinger YH, Gaynon PS, Sposto R et al.; Therapeutic Advances in Childhood Leukemia & Lymphoma (TACL) Consortium. Bortezomib with chemotherapy is highly active in advanced B-precursor acute lymphoblastic leukemia: Therapeutic Advances in Childhood Leukemia & Lymphoma (TACL) Study. Blood 120(2), 285-290 (2012).
50. Horton TM, Perentesis J, Gamis AS et al. A Phase 2 study of bortezomib combined with reinduction chemotherapy in children and young adults with recurrent, refractory or secondary acute myeloid leukemia: a Children's Oncology Group (COG) study. Presented at: ASH Annual Meeting. Atlanta, GA, USA, 8-11 December 2012.
51. Franke NE, van Zantwijk I, Kaspers GJ et al. Ex vivo activity of bortezomib and dexamethasone combinations against childhood acute leukemia cells. Presented at: ASH Annual Meeting. Atlanta, GA, USA, 8-11 December 2007.
52. Szczepanek J, Pogorzala M, Konatkowska B et al. Differential ex vivo activity of bortezomib in newly diagnosed paediatric acute lymphoblastic and myeloblastic leukaemia. Anticancer Res. 30(6), 2119-2124 (2010).
53. Stapnes C, Døskeland AP, Hatfield K et al. The proteasome inhibitors bortezomib and PR-171 have antiproliferative and proapoptotic effects on primary human acute myeloid leukaemia cells. Br. J. Haematol. 136(6), 814-828 (2007).
54. Niewerth D, Franke N, Jansen G et al. Sensitivity of pediatric acute leukemia cells to bortezomib and epoxyketone-based proteasome inhibitors: correlations with proteasome subunit expression. Presented at: ASH Annual Meeting. San Diego, CA, USA, 10-13 December 2011.
55. Wright JJ. Combination therapy of bortezomib with novel targeted agents: an emerging treatment strategy. Clin. Cancer Res. 16(16), 4094-4104 (2010).
56. Sanchez E, Li M, Steinberg JA et al. The proteasome inhibitor CEP-18770 enhances the anti-myeloma activity of bortezomib and melphalan. Br. J. Haematol. 148(4), 569-581 (2010).
57. Sanchez E, Li M, Li J et al. CEP-18770 (delanzomib) in combination with dexamethasone and lenalidomide inhibits the growth of multiple myeloma. Leuk. Res. 36(11), 1422-1427 (2012).
58. Chauhan D, Tian Z, Zhou B et al. In vitro and in vivo selective antitumor activity of a novel orally bioavailable proteasome inhibitor MLN9708 against multiple myeloma cells. Clin. Cancer Res. 17(16), 5311-5321 (2011).
59. Chauhan D, Singh AV, Ciccarelli B, Richardson PG, Palladino MA, Anderson KC. Combination of novel proteasome inhibitor NPI-0052 and lenalidomide trigger in vitro and in vivo synergistic cytotoxicity in multiple myeloma. Blood 115(4), 834-845 (2010).
60. Horton TM, Gannavarapu A, Blaney SM, D'Argenio DZ, Plon SE, Berg SL. Bortezomib interactions with chemotherapy agents in acute leukemia in vitro. Cancer Chemother. Pharmacol. 58(1), 13-23 (2006).
61. Chauhan D, Singh A, Brahmandam M et al. Combination of proteasome inhibitors bortezomib and NPI-0052 trigger in vivo synergistic cytotoxicity in multiple myeloma. Blood 111(3), 1654-1664 (2008).
62. Hideshima T, Richardson PG, Anderson KC. Mechanism of action of proteasome inhibitors and deacetylase inhibitors and the biological basis of synergy in multiple myeloma. Mol. Cancer Ther. 10(11), 2034-2042 (2011).
63. Nie D, Huang K, Yin S et al. Synergistic/ additive interaction of valproic acid with bortezomib on proliferation and apoptosis of acute myeloid leukemia cells. Leuk. Lymphoma 53(12), 2487-2495 (2012).
64. Kumar SK, Lee JH, Lahuerta JJ et al.; International Myeloma Working Group. Risk of progression and survival in multiple myeloma relapsing after therapy with IMiDs and bortezomib: a multicenter international myeloma working group study. Leukemia 26(1), 149-157 (2012).
65. Markovina S, Callander NS, O'Connor SL et al. Bortezomib-resistant nuclear factor-kappaB activity in multiple myeloma cells. Mol. Cancer Res. 6(8), 1356-1364 (2008).
66. Keats JJ, Fonseca R, Chesi M et al. Promiscuous mutations activate the noncanonical NF-κB pathway in multiple myeloma. Cancer Cell 12(2), 131-144 (2007).
67. Markovina S, Callander NS, O'Connor SL et al. Bone marrow stromal cells from multiple myeloma patients uniquely induce bortezomib resistant NF-κB activity in myeloma cells. Mol. Cancer 9, 176 (2010).
68. Shuqing L, Jianmin Y, Chongmei H, Hui C, Wang J. Upregulated expression of the PSMB5 gene may contribute to drug resistance in patient with multiple myeloma when treated with bortezomib-based regimen. Exp. Hematol. 39(12), 1117-1118 (2011).
69. McConkey DJ, Zhu K. Mechanisms of proteasome inhibitor action and resistance in cancer. Drug Resist. Updat. 11(4-5), 164-179 (2008).
70. Kale AJ, Moore BS. Molecular mechanisms of acquired proteasome inhibitor resistance. J. Med. Chem. 55(23), 10317-10327 (2012). • Excellent summary of mechanisms of acquired proteasome inhibitor resistance.
71. Kuhn DJ, Chen Q, Voorhees PM et al. Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood 110(9), 3281-3290 (2007).
72. Verbrugge SE, Assaraf YG, Dijkmans BA et al. Inactivating PSMB5 mutations and P-glycoprotein (multidrug resistance-associated protein/ATP-binding cassette B1) mediate resistance to proteasome inhibitors: ex vivo efficacy of (immuno) proteasome inhibitors in mononuclear blood cells from patients with rheumatoid arthritis. J. Pharmacol. Exp. Ther. 341(1), 174-182 (2012).
73. Ao L, Wu Y, Kim D et al. Development of peptide-based reversing agents for P-glycoprotein-mediated resistance to carfilzomib. Mol. Pharm. doi:10.1021/ mp300044b (2012) (Epub ahead of print).
74. 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 8(5), 407-419 (2005).
75. Kale AJ, McGlinchey RP, Lechner A, Moore BS. Bacterial self-resistance to the natural proteasome inhibitor salinosporamide A. ACS Chem. Biol. 6(11), 1257-1264 (2011).
76. ClinicalTrials.gov. www.clinicaltrials.gov (Accessed 12 December 2012
77. The Netherlands trial registery. www.trialregister.nl (Accessed 12 December 2012