Higher ratio immune versus constitutive proteasome level as novel indicator of sensitivity of pediatric acute leukemia cells to proteasome inhibitors

Haematologica

Volumn 98, Issue 12, 2013, Pages 1896-1904

  Niewerth, Denise ^a   Franke, Niels E ^a   Jansen, Gerrit ^a   Assaraf, Yehuda G ^b   van Meerloo, Johan ^a   Kirk, Christopher J ^c   Degenhardt, Jeremiah ^c   Anderl, Janet ^c   Schimmer, Aaron D ^d   Zweegman, Sonja ^a   de Haas, Valerie ^e   Horton, Terzah M ^f   Kaspers, Gertjan J L ^a   Cloos, Jacqueline ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c ONYX PHARMACEUTICALS   (United States)

^d PRINCESS MARGARET HOSPITAL   (Canada)

^e DUTCH CHILDHOOD ONCOLOGY GROUP   (Netherlands)

^f BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; CARFILZOMIB; DEXAMETHASONE; ONX 0914; OPROZOMIB; PROTEASOME; PROTEASOME INHIBITOR; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CANCER GROWTH; CELL COUNT; CELL CULTURE; CELL VIABILITY ASSAY; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG SENSITIVITY; FEMALE; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LC 50; MALE; MTT ASSAY; PRESCHOOL CHILD; PROTEIN EXPRESSION; SCHOOL CHILD; WESTERN BLOTTING;

ADOLESCENT; BORONIC ACIDS; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; INFANT; LEUKEMIA, MYELOID, ACUTE; MALE; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEIN SUBUNITS; PYRAZINES;

EID: 84887608620     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2013.092411     Document Type: Article

References (50)

1. Huber EM, Basler M, Schwab R, Heinemeyer W, Kirk CJ, Groettrup M, et al. Immunoand constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell. 2012;148(4): 727-38.
2. Kuhn DJ, Orlowski RZ. The immunoprotea some as a target in hematologic malignancies. Semin Hematol. 2012;49(3):258-62.
3. Muchamuel T, Basler M, Aujay MA, Suzuki E, Kalim KW, Lauer C, et al. A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat Med. 2009;15(7):781-7.
4. Orlowski RZ, Kuhn DJ. Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin Cancer Res. 2008;14(6): 1649-57.
5. Moreau P, Richardson PG, Cavo M, Orlowski RZ, San Miguel JF, Palumbo A, et al. Proteasome inhibitors in multiple myeloma: 10 years later. Blood. 2012;120(5):947-59.
6. Pui CH, Mullighan CG, Evans WE, Relling M V. Pediatric acute lymphoblastic leukemia: where are we going and how do we get there? Blood. 2012;120(6):1165-74.
7. Kaspers GJ, Veerman AJ, Pieters R, Van Zantwijk CH, Smets LA, Van Wering ER, et al. In vitro cellular drug resistance and prognosis in newly diagnosed childhood acute lymphoblastic leukemia. Blood. 1997;90(7): 2723-9.
8. Cortes J, Thomas D, Koller C, Giles F, Estey E, Faderl S, et al. Phase I study of bortezomib in refractory or relapsed acute leukemias. Clin Cancer Res. 2004;10(10):3371-6.
9. Horton TM, Pati D, Plon SE, Thompson PA, Bomgaars LR, Adamson PC, 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. 2007;13(5):1516-22.
10. Messinger YH, Gaynon PS, Sposto R, Van der GJ, Eckroth E, Malvar J, et al. Bortezomib with chemotherapy is highly active in advanced B-precursor acute lymphoblastic leukemia: Therapeutic Advances in Childhood Leukemia & Lymphoma (TACL) Study. Blood. 2012;120(2):285-90.
11. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol. 2005;6(1):79-87.
12. Vigneron N, Van den Eynde BJ. Proteasome subtypes and the processing of tumor antigens: increasing antigenic diversity. Curr Opin Hematol. 2012;24(1):84-91.
13. Seifert U, Bialy LP, Ebstein F, Bech-Otschir D, Voigt A, Schroter F, et al. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell. 2010;142(4):613-24.
14. Parlati F, Lee SJ, Aujay M, Suzuki E, Levitsky K, Lorens JB, et al. Carfilzomib can induce tumor cell death through selective inhibition of the chymotrypsin-like activity of the proteasome. Blood. 2009;114(16):3439-47.
15. Roccaro AM, Sacco A, Aujay M, Ngo HT, Azab AK, Azab F, et al. Selective inhibition of chymotrypsin-like activity of the immunoproteasome and constitutive proteasome in Waldenstrom macroglobulinemia. Blood. 2010;115(20):4051-60.
16. 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. 2006;58(1):13-23.
17. Houghton PJ, Morton CL, Kolb EA, Lock R, Carol H, Reynolds CP, et al. Initial testing (stage 1) of the proteasome inhibitor bortezomib by the pediatric preclinical testing program. Pediatr Blood Cancer. 2008;50(1): 37-45.
18. Attar EC, De Angelo DJ, Supko JG, D'Amato F, Zahrieh D, Sirulnik A, et al. Phase I and pharmacokinetic study of bortezomib in combination with idarubicin and cytarabine in patients with acute myelogenous leukemia. Clin Cancer Res. 2008;14(5): 1446-54.
19. Niewerth D, Dingjan I, Cloos J, Jansen G, Kaspers G. Proteasome inhibitors in acute leukemia. Expert Rev Anticancer Ther. 2013;13(3):327-37.
20. Franke NE, Niewerth D, Assaraf YG, Van Meerloo J, Vojtekova K, Van Zantwijk CH, et al. Impaired bortezomib binding to mutant beta5 subunit of the proteasome is the underlying basis for bortezomib resistance in leukemia cells. Leukemia. 2012;26 (4):757-68.
21. Kale AJ, Moore BS. Molecular Mechanisms of Acquired Proteasome Inhibitor Resistance. J Med Chem. 2012;55(23):10317-27.
22. Oerlemans R, Franke NE, Assaraf YG, Cloos J, Van Zantwijk I, Berkers CR, et al. Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein. Blood. 2008;112(6):2489-99.
23. Ruschak AM, Slassi M, Kay LE, Schimmer AD. Novel proteasome inhibitors to overcome bortezomib resistance. J Natl Cancer Inst. 2011;103(13):1007-17.
24. Demo SD, Kirk CJ, Aujay MA, Buchholz TJ, Dajee M, Ho MN, et al. Antitumor activity of PR-171, a novel irreversible inhibitor of the proteasome. Cancer Res. 2007;67(13): 6383-91.
25. Chauhan D, Catley L, Li G, Podar K, Hideshima T, Velankar M, et al. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib. Cancer Cell. 2005;8(5):407-19.
26. Li X, Wood TE, Sprangers R, Jansen G, Franke NE, Mao X, et al. Effect of noncompetitive proteasome inhibition on bortezomib resistance. J Natl Cancer Inst. 2010;102(14):1069-82.
27. Van Meerloo J, Kaspers GJ, Cloos J. Cell sensitivity assays: the MTT assay. Methods Mol Biol. 2011;731:237-45.
28. 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.
29. Suzuki E, Demo S, Deu E, Keats J, RastuKapur S, Bergsagel PL, et al. Molecular mechanisms of bortezomib resistant adenocarcinoma cells. PLoS One. 2011;6(12): e27996.
30. Pieters R, Den Boer ML, Durian M, Janka G, Schmiegelow K, Kaspers GJ, et al. Relation between age, immunophenotype and in vitro drug resistance in 395 children with acute lymphoblastic leukemia--implications for treatment of infants. Leukemia. 1998;12 (9):1344-8.
31. Kaspers GJ, Kardos G, Pieters R, Van Zantwijk CH, Klumper E, Hahlen K, et al. Different cellular drug resistance profiles in childhood lymphoblastic and non-lymphoblastic leukemia: a preliminary report. Leukemia. 1994;8(7):1224-9.
32. Balsas P, Galan-Malo P, Marzo I, Naval J. Bortezomib resistance in a myeloma cell line is associated to PSM 5 overexpression and polyploidy. Leuk Res. 2012;36(2):212-8.
33. Ruckrich T, Kraus M, Gogel J, Beck A, Ovaa H, Verdoes M, et al. Characterization of the ubiquitin-proteasome system in bortezomib-adapted cells. Leukemia. 2009;23(6): 1098-105.
34. Ri M, Iida S, Nakashima T, Miyazaki H, Mori F, Ito A, et al. Bortezomib-resistant myeloma cell lines: a role for mutated PSMB5 in preventing the accumulation of unfolded proteins and fatal ER stress. Leukemia. 2010;24(8):1506-12.
35. Lu S, Yang J, Song X, Gong S, Zhou H, Guo L, et al. Point mutation of the proteasome beta5 subunit gene is an important mechanism of bortezomib resistance in bortezomib-selected variants of Jurkat T cell lymphoblastic lymphoma/leukemia line. J Pharmacol Exp Ther. 2008;326(2):423-31.
36. Lichter DI, Danaee H, Pickard MD, Tayber O, Sintchak M, Shi H, et al. Sequence analysis of -subunit genes of the 20S proteasome in patients with relapsed multiple myeloma treated with bortezomib or dexamethasone. Blood. 2012;120(23):4513-6.
37. 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. 2011;39(12):1117-8.
38. Kaspers GJ, Veerman AJ, Pieters R, Van Zantwijk I, Hahlen K, Van Wering ER. Drug combination testing in acute lymphoblastic leukemia using the MTT assay. Leuk Res. 1995;19(3):175-81.
39. Szczepanek J, Pogorzala M, Konatkowska B, Juraszewska E, Badowska W, Olejnik I, et al. Differential ex vivo activity of bortezomib in newly diagnosed paediatric acute lymphoblastic and myeloblastic leukaemia. Anticancer Res. 2010;30(6):2119-24.
40. Kaspers GJ, Pieters R, Klumper E, De Waal FC, Veerman AJ. Glucocorticoid resistance in childhood leukemia. Leuk Lymphoma. 1994;13(3-4):187-201.
41. Ma MH, Yang HH, Parker K, Manyak S, Friedman JM, Altamirano C, et al. The proteasome inhibitor PS-341 markedly enhances sensitivity of multiple myeloma tumor cells to chemotherapeutic agents. Clin Cancer Res. 2003;9(3):1136-44.
42. Guzman ML, Neering SJ, Upchurch D, Grimes B, Howard DS, Rizzieri DA, et al. Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood. 2001;98(8):23017.
43. Bentires-Alj M, Barbu V, Fillet M, Chariot A, Relic B, Jacobs N, et al. NF-kappaB transcription factor induces drug resistance through MDR1 expression in cancer cells. Oncogene. 2003;22(1):90-7.
44. Wood P, Burgess R, MacGregor A, Yin JA. Pglycoprotein expression on acute myeloid leukaemia blast cells at diagnosis predicts response to chemotherapy and survival. Br J Haematol. 1994;87(3):509-14.
45. Verbrugge SE, Assaraf YG, Dijkmans BA, Scheffer GL, Al M, den Uyl D, 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. J Pharmacol Exp Ther. 2012;341(1): 174-82.
46. Chauhan PS, Bhushan B, Singh LC, Mishra AK, Saluja S, Mittal V, et al. Expression of genes related to multiple drug resistance and apoptosis in acute leukemia: response to induction chemotherapy. Exp Mol Pathol. 2012;92(1):44-9.
47. Busse A, Kraus M, Na IK, Rietz A, Scheibenbogen C, Driessen C, et al. Sensitivity of tumor cells to proteasome inhibitors is associated with expression levels and composition of proteasome subunits. Cancer. 2008;112(3):659-70.
48. Matondo M, Bousquet-Dubouch MP, Gallay N, Uttenweiler-Joseph S, Recher C, Payrastre B, et al. Proteasome inhibitorinduced apoptosis in acute myeloid leukemia: a correlation with the proteasome status. Leuk Res. 2010;34(4):498-506.
49. Niewerth D, Franke N, Jansen G, Assaraf Y, Van Meerloo J, Kirk CJ, et al. Interferon-yinduced upregulation of immunoproteasome subunit assembly overcomes bortezomib resistance of leukemia cell lines harbouring bortezomib-induced mutations in constitutive PSMB5. ASH Annual Meeting Abstracts. 2012;120(21):1346.
50. Heink S, Ludwig D, Kloetzel PM, Kruger E. IFN-gamma-induced immune adaptation of the proteasome system is an accelerated and transient response. Proc Natl Acad Sci USA. 2005;102(26):9241-6.