The nuclear factor (erythroid-derived 2)-like 2 and proteasome maturation protein axis mediate bortezomib resistance in multiple myeloma

Journal of Biological Chemistry

Volumn 290, Issue 50, 2015, Pages 29854-29868

  Li, Bingzong ^a,b   Fu, Jinxiang ^a   Chen, Ping ^a   Ge, Xueping ^a   Li, Yali ^a   Kuiatse, Isere ^b   Wang, Hua ^b   Wang, Huihan ^b   Zhang, Xingding ^b   Orlowski, Robert Z ^b  

^a THE SECOND AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

BORTEZOMIB; CHEMO SENSITIZATIONS; MULTIPLE MYELOMA; NUCLEAR FACTORS; PROTEASOME INHIBITORS; PROTEASOMES;

BIOLOGY;

BORTEZOMIB; KELCH LIKE ECH ASSOCIATED PROTEIN 1; RETINOIC ACID; TRANSCRIPTION FACTOR NRF2; CHAPERONE; NFE2L2 PROTEIN, HUMAN; PROTEASSEMBLIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CANCER RESISTANCE; CARCINOGENESIS; CELL PROLIFERATION; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME ACTIVITY; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE REPRESSION; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MULTIPLE MYELOMA; NONHUMAN; NRF2 GENE; POMP GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VERY ELDERLY; DRUG RESISTANCE; PHYSIOLOGY; TUMOR CELL LINE;

BORTEZOMIB; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; HUMANS; MOLECULAR CHAPERONES; MULTIPLE MYELOMA; NF-E2-RELATED FACTOR 2; TRETINOIN;

EID: 84949643262     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.664953     Document Type: Article

References (57)

1. Richardson, P. G., Barlogie, B., Berenson, J., Singhal, S., Jagannath, S., Irwin, D., Rajkumar, S. V., Srkalovic, G., Alsina, M., Alexanian, R., Siegel, D., Orlowski, R. Z., Kuter, D., Limentani, S. A., Lee, S., et al. (2003)Aphase 2 study of bortezomib in relapsed, refractory myeloma. N. Engl. J. Med. 348, 2609-2617
2. Richardson, P. G., Sonneveld, P., Schuster, M. W., Irwin, D., Stadtmauer, E. A., Facon, T., Harousseau, J. L., Ben-Yehuda, D., Lonial, S., Goldschmidt, H., Reece, D., San-Miguel, J. F., Bladé, J., Boccadoro, M., Cavenagh, J., et al. (2005) Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N. Engl. J. Med. 352, 2487-2498
3. Orlowski, R. Z., Nagler, A., Sonneveld, P., Bladé, J., Hajek, R., Spencer, A., San Miguel, J., Robak, T., Dmoszynska, A., Horvath, N., Spicka, I., Sutherland, H. J., Suvorov, A. N., Zhuang, S. H., Parekh, T., et al. (2007) Randomized phase III study of pegylated liposomal doxorubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: combination therapy improves time to progression. J. Clin. Oncol. 25, 3892-3901
4. San Miguel, J. F., Schlag, R., Khuageva, N. K., Dimopoulos, M. A., Shpilberg, O., Kropff, M., Spicka, I., Petrucci, M. T., Palumbo, A., Samoilova, O. S., Dmoszynska, A., Abdulkadyrov, K. M., Schots, R., Jiang, B., Mateos, M. V., et al. (2008) Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma. N. Engl. J. Med. 359, 906-917
5. Harousseau, J. L., Attal, M., Avet-Loiseau, H., Marit, G., Caillot, D., Mohty, M., Lenain, P., Hulin, C., Facon, T., Casassus, P., Michallet, M., Maisonneuve, H., Benboubker, L., Maloisel, F., Petillon, M. O., et al. (2010) Bortezomib plus dexamethasone is superior to vincristine plus doxorubicin plus dexamethasone as induction treatment prior to autologous stem-cell transplantation in newly diagnosed multiple myeloma: results of the IFM 2005-01 phase III trial. J. Clin. Oncol. 28, 4621-4629
6. Cavo, M., Tacchetti, P., Patriarca, F., Petrucci, M. T., Pantani, L., Galli, M., Di Raimondo, F., Crippa, C., Zamagni, E., Palumbo, A., Offidani, M., Corradini, P., Narni, F., Spadano, A., Pescosta, N., et al. (2010) 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, 2075-2085
7. Sonneveld, P., Schmidt-Wolf, I. G., van der Holt, B., El Jarari, L., Bertsch, U., Salwender, H., Zweegman, S., Vellenga, E., Broyl, A., Blau, I. W., Weisel, K. C., Wittebol, S., Bos, G. M., Stevens-Kroef, M., Scheid, C., et al. (2012) Bortezomib induction and maintenance treatment in patients with newly diagnosed multiple myeloma: results of the randomized phase III HOVON-65/GMMG-HD4 trial. J. Clin. Oncol. 30, 2946-2955
8. Anderson, K. C., Alsina, M., Bensinger, W., Biermann, J. S., Cohen, A. D., Devine, S., Djulbegovic, B., Faber, E. A., Jr., Gasparetto, C., Hernandez-Illizaliturri, F., Huff, C. A., Kassim, A., Krishnan, A. Y., Liedtke, M., Meredith, R., et al. (2013) Multiple myeloma, version 1.2013. J. Natl. Compr. Canc. Netw. 11, 11-17
9. Mahindra, A., Laubach, J., Raje, N., Munshi, N., Richardson, P. G., and Anderson, K. (2012) Latest advances and current challenges in the treatment of multiple myeloma. Nat. Rev. Clin. Oncol. 9, 135-143
10. Pozzi, S., Marcheselli, L., Bari, A., Liardo, E. V., Marcheselli, R., Luminari, S., Quaresima, M., Cirilli, C., Ferri, P., Federico, M., and Sacchi, S. (2013) Survival of multiple myeloma patients in the era of novel therapies confirms the improvement in patients younger than 75 years: a populationbased analysis. Br. J. Haematol. 163, 40-46
11. Kumar, S. K., Dispenzieri, A., Lacy, M. Q., Gertz, M. A., Buadi, F. K., Pandey, S., Kapoor, P., Dingli, D., Hayman, S. R., Leung, N., Lust, J., Mc-Curdy, A., Russell, S. J., Zeldenrust, S. R., Kyle, R. A., and Rajkumar, S. V. (2014) Continued improvement in survival in multiple myeloma: changes in early mortality and outcomes in older patients. Leukemia 28, 1122-1128
12. Ozaki, S., Harada, T., Saitoh, T., Shimazaki, C., Itagaki, M., Asaoku, H., Kuroda, Y., Chou, T., Yoshiki, Y., Suzuki, K., Murakami, H., Hayashi, K., Mina, R., Palumbo, A., and Shimizu, K. (2014) Survival of multiple myeloma patients aged 65-70 years in the era of novel agents and autologous stem cell transplantation. A multicenter retrospective collaborative study of the Japanese Society of Myeloma and the European Myeloma Network. Acta Haematol. 132, 211-219
13. Cenci, S., Mezghrani, A., Cascio, P., Bianchi, G., Cerruti, F., Fra, A., Lelouard, H., Masciarelli, S., Mattioli, L., Oliva, L., Orsi, A., Pasqualetto, E., Pierre, P., Ruffato, E., Tagliavacca, L., and Sitia, R. (2006) Progressively impaired proteasomal capacity during terminal plasma cell differentiation. EMBO J. 25, 1104-1113
14. Bianchi, G., Oliva, L., Cascio, P., Pengo, N., Fontana, F., Cerruti, F., Orsi, A., Pasqualetto, E., Mezghrani, A., Calbi, V., Palladini, G., Giuliani, N., Anderson, K. C., Sitia, R., and Cenci, S. (2009) The proteasome load versus capacity balance determines apoptotic sensitivity of multiple myeloma cells to proteasome inhibition. Blood 113, 3040-3049
15. Chen, D., Frezza, M., Schmitt, S., Kanwar, J., and Dou, Q. P. (2011) Bortezomib as the first proteasome inhibitor anticancer drug: current status and future perspectives. Curr. Cancer Drug Targets 11, 239-253
16. Laubach, J. P., Mitsiades, C. S., Roccaro, A. M., Ghobrial, I. M., Anderson, K. C., and Richardson, P. G. (2009) Clinical challenges associated with bortezomib therapy in multiple myeloma and Waldenstroms macroglobulinemia. Leukemia Lymphoma 50, 694-702
17. Orlowski, R. Z., and Kuhn, D. J. (2008) Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin. Cancer Res. 14, 1649-1657
18. Lü, S., Yang, J., Song, X., Gong, S., Zhou, H., Guo, L., Song, N., Bao, X., Chen, P., and Wang, J. (2008) Point mutation of the proteasome β5 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. 326, 423-431
19. Lü, S., Chen, Z., Yang, J., Chen, L., Zhou, H., Xu, X., Li, J., Han, F., and Wang, J. (2010) The effects of proteasome inhibitor bortezomib on a P-gp positive leukemia cell line K562/A02. Int. J. Lab. Hematol. 32, e123-31
20. Oerlemans, R., Franke, N. E., Assaraf, Y. G., Cloos, J., van Zantwijk, I., Berkers, C. R., Scheffer, G. L., Debipersad, K., Vojtekova, K., Lemos, C., van der Heijden, J. W., Ylstra, B., Peters, G. J., Kaspers, G. L., Dijkmans, B. A., et al. (2008) Molecular basis of bortezomib resistance: proteasome subunit β5 (PSMB5) gene mutation and overexpression of PSMB5 protein. Blood 112, 2489-2499
21. Marques, A. J., Palanimurugan, R., Matias, A. C., Ramos, P. C., and Dohmen, R. J. (2009) Catalytic mechanism and assembly of the proteasome. Chem. Rev. 109, 1509-1536
22. Murata, S., Yashiroda, H., and Tanaka, K. (2009) Molecular mechanisms of proteasome assembly. Nat. Rev. Mol. Cell Biol. 10, 104-115
23. Politou, M., Karadimitris, A., Terpos, E., Kotsianidis, I., Apperley, J. F., and Rahemtulla, A. (2006) No evidence of mutations of the PSMB5 (β-5 subunit of proteasome) in a case of myeloma with clinical resistance to bortezomib. Leuk. Res. 30, 240-241
24. Lichter, D. I., Danaee, H., Pickard, M. D., Tayber, O., Sintchak, M., Shi, H., Richardson, P. G., Cavenagh, J., Bladé, J., Façon, T., Niesvizky, R., Alsina, M., Dalton, W., Sonneveld, P., Lonial, S., et al. (2012) Sequence analysis of β-subunit genes of the 20S proteasome in patients with relapsed multiple myeloma treated with bortezomib or dexamethasone. Blood 120, 4513-4516
25. Leung-Hagesteijn, C., Erdmann, N., Cheung, G., Keats, J. J., Stewart, A. K., Reece, D. E., Chung, K. C., and Tiedemann, R. E. (2013) Xbp1s-negative tumor B cells and pre-plasmablasts mediate therapeutic proteasome inhibitor resistance in multiple myeloma. Cancer Cell 24, 289-304
26. Orlowski, R. Z. (2013) Why proteasome inhibitors cannot ERADicate multiple myeloma. Cancer Cell 24, 275-277
27. Kuhn, D. J., Berkova, Z., Jones, R. J., Woessner, R., Bjorklund, C. C., Ma, W., Davis, R. E., Lin, P., Wang, H., Madden, T. L., Wei, C., Baladandayuthapani, V., Wang, M., Thomas, S. K., Shah, J. J., Weber, D. M., and Orlowski, R. Z. (2012) Targeting the insulin-like growth factor-1 receptor to overcome bortezomib resistance in preclinical models of multiple myeloma. Blood 120, 3260-3270
28. Bjorklund, C. C., Baladandayuthapani, V., Lin, H. Y., Jones, R. J., Kuiatse, I., Wang, H., Yang, J., Shah, J. J., Thomas, S. K., Wang, M., Weber, D. M., and Orlowski, R. Z. (2014) Evidence of a role for CD44 and cell adhesion in mediating resistance to lenalidomide in multiple myeloma: therapeutic implications. Leukemia 28, 373-383
29. Chorley, B. N., Campbell, M. R., Wang, X., Karaca, M., Sambandan, D., Bangura, F., Xue, P., Pi, J., Kleeberger, S. R., and Bell, D. A. (2012) Identification of novel NRF2-regulated genes by ChIP-Seq: influence on retinoid X receptor α. Nucleic Acids Res. 40, 7416-7429
30. Jaramillo, M. C., and Zhang, D. D. (2013) The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev. 27, 2179-2191
31. Chondrogianni, N., and Gonos, E. S. (2007) Overexpression of hUMP1/ POMPproteasome accessory protein enhances proteasome-mediated antioxidant defence. Exp. Gerontol. 42, 899-903
32. Wang, X. J., Hayes, J. D., Henderson, C. J., and Wolf, C. R. (2007) Identification of retinoic acid as an inhibitor of transcription factor Nrf2 through activation of retinoic acid receptor α. Proc. Natl. Acad. Sci. U.S.A. 104, 19589-19594
33. De Braekeleer, E., Douet-Guilbert, N., and De Braekeleer, M. (2014)RARA fusion genes in acute promyelocytic leukemia: a review. Expert Rev. Hematol. 7, 347-357
34. Kobayashi, A., Kang, M. I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K., and Yamamoto, M. (2004) Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24, 7130-7139
35. Siegel, D. S., Martin, T., Wang, M., Vij, R., Jakubowiak, A. J., Lonial, S., Trudel, S., Kukreti, V., Bahlis, N., Alsina, M., Chanan-Khan, A., Buadi, F., Reu, F. J., Somlo, G., Zonder, J., et al. (2012)Aphase 2 study of single-agent carfilzomib (PX-171-003-A1) in patients with relapsed and refractory multiple myeloma. Blood 120, 2817-2825
36. Niesvizky, R., Martin, T. G., 3rd, Bensinger, W. I., Alsina, M., Siegel, D. S., Kunkel, L. A., Wong, A. F., Lee, S., Orlowski, R. Z., and Wang, M. (2013) Phase Ib dose-escalation study (PX-171-006) of carfilzomib, lenalidomide, and low-dose dexamethasone in relapsed or progressive multiple myeloma. Clin. Cancer Res. 19, 2248-2256
37. Wang, M., Martin, T., Bensinger, W., Alsina, M., Siegel, D. S., Kavalerchik, E., Huang, M., Orlowski, R. Z., and Niesvizky, R. (2013) Phase 2 doseexpansion study (PX-171-006) of carfilzomib, lenalidomide, and lowdose dexamethasone in relapsed or progressive multiple myeloma. Blood 122, 3122-3128
38. Jakubowiak, A. J., Dytfeld, D., Griffith, K. A., Lebovic, D., Vesole, D. H., Jagannath, S., Al-Zoubi, A., Anderson, T., Nordgren, B., Detweiler-Short, K., Stockerl-Goldstein, K., Ahmed, A., Jobkar, T., Durecki, D. E., McDonnell, K., et al. (2012) A phase 1/2 study of carfilzomib in combination with lenalidomide and low-dose dexamethasone as a frontline treatment for multiple myeloma. Blood 120, 1801-1809
39. Lawasut, P., Chauhan, D., Laubach, J., Hayes, C., Fabre, C., Maglio, M., Mitsiades, C., Hideshima, T., Anderson, K. C., and Richardson, P. G. (2012) New proteasome inhibitors in myeloma. Curr. Hematol. Malig. Rep. 7, 258-266
40. Kumar, S. K., Lee, J. H., Lahuerta, J. J., Morgan, G., Richardson, P. G., Crowley, J., Haessler, J., Feather, J., Hoering, A., Moreau, P., LeLeu, X., Hulin, C., Klein, S. K., Sonneveld, P., Siegel, D., et al. (2012) Risk of progression and survival in multiple myeloma relapsing after therapy with IMiDs and bortezomib: a multicenter international myeloma working group study. Leukemia 26, 149-157
41. Jang, J., Wang, Y., Kim, H. S., Lalli, M. A., and Kosik, K. S. (2014) Nrf2, a regulator of the proteasome, controls self-renewal and pluripotency in human embryonic stem cells. Stem Cells 32, 2616-2625
42. Kwak, M. K., Wakabayashi, N., Greenlaw, J. L., Yamamoto, M., and Kensler, T. W. (2003) Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol. Cell. Biol. 23, 8786-8794
43. Pickering, A. M., Linder, R. A., Zhang, H., Forman, H. J., and Davies, K. J. (2012) Nrf2-dependent induction of proteasome and Pa28αβ regulator are required for adaptation to oxidative stress. J. Biol. Chem. 287, 10021-10031
44. Radhakrishnan, S. K., Lee, C. S., Young, P., Beskow, A., Chan, J. Y., and Deshaies, R. J. (2010) Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 38, 17-28
45. Stessman, H. A., Baughn, L. B., Sarver, A., Xia, T., Deshpande, R., Mansoor, A., Walsh, S. A., Sunderland, J. J., Dolloff, N. G., Linden, M. A., Zhan, F., Janz, S., Myers, C. L., and Van Ness, B. G. (2013) Profiling bortezomib resistance identifies secondary therapies in a mouse myeloma model. Mol. Cancer Ther. 12, 1140-1150
46. Biran, N., Jagannath, S., and Chari, A. (2013) Risk stratification in multiple myeloma, part 1: characterization of high-risk disease. Clin. Adv. Hematol. Oncol. 11, 489-503
47. Moriuchi, M., Ohmachi, K., Kojima, M., Tsuboi, K., Ogawa, Y., Nakamura, N., and Ando, K. (2010) Three cases of bortezomib-resistant multiple myeloma with extramedullary masses. Tokai J. Exp. Clin. Med. 35, 17-20
48. Paton-Hough, J., Chantry, A. D., and Lawson, M. A. (2015) A review of current murine models of multiple myeloma used to assess the efficacy of therapeutic agents on tumour growth and bone disease. Bone 77, 57-68
49. Zhang, N., Liang, J., Tian, Y., Yuan, L., Wu, L., Miao, S., Zong, S., and Wang, L. (2010) A novel testis-specific GTPase serves as a link to proteasome biogenesis: functional characterization of RhoS/RSA-14-44 in spermatogenesis. Mol. Biol. Cell 21, 4312-4324
50. Witt, E., Zantopf, D., Schmidt, M., Kraft, R., Kloetzel, P. M., and Krüger, E. (2000) Characterisation of the newly identified human Ump1 homologue POMP and analysis of LMP7(β5i) incorporation into 20 S proteasomes. J. Mol. Biol. 301, 1-9
51. Fricke, B., Heink, S., Steffen, J., Kloetzel, P. M., and Krüger, E. (2007) The proteasome maturation protein POMP facilitates major steps of 20S proteasome formation at the endoplasmic reticulum. EMBO Rep. 8, 1170-1175
52. Meiners, S., Heyken, D., Weller, A., Ludwig, A., Stangl, K., Kloetzel, P. M., and Krüger, E. (2003) Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of mammalian proteasomes. J. Biol. Chem. 278, 21517-21525
53. Fuchs, D., Berges, C., Opelz, G., Daniel, V., and Naujokat, C. (2008) Increased expression and altered subunit composition of proteasomes induced by continuous proteasome inhibition establish apoptosis resistance and hyperproliferation of Burkitt lymphoma cells. J. Cell Biochem. 103, 270-283
54. Wolf, J., Richardson, P. G., Schuster, M., LeBlanc, A., Walters, I. B., and Battleman, D. S. (2008) Utility of bortezomib retreatment in relapsed or refractory multiple myeloma patients: a multicenter case series. Clin. Adv. Hematol. Oncol. 6, 755-760
55. Hrusovsky, I., Emmerich, B., von Rohr, A., Voegeli, J., Taverna, C., Olie, R. A., Pliskat, H., Frohn, C., and Hess, G. (2010) Bortezomib retreatment in relapsed multiple myeloma-results from a retrospective multicentre survey in Germany and Switzerland. Oncology 79, 247-254
56. Namani, A., Li, Y., Wang, X. J., and Tang, X. (2014) Modulation of NRF2 signaling pathway by nuclear receptors: implications for cancer. Biochim. Biophys. Acta 1843, 1875-1885
57. Magesh, S., Chen, Y., and Hu, L. (2012) Small molecule modulators of Keap1-Nrf2-ARE pathway as potential preventive and therapeutic agents. Med. Res. Rev. 32, 687-726