Response of myeloma to the proteasome inhibitor bortezomib is correlated with the unfolded protein response regulator XBP-1

Haematologica

Volumn 97, Issue 1, 2012, Pages 64-72

  Ling, Silvia C W ^a,f   Lau, Edwin K K ^a   Al Shabeeb, Ammira ^a   Nikolic, Angela ^a   Catalano, Albert ^b   Iland, Harry ^b   Horvath, Noemi ^c   Ho, P Joy ^b   Harrison, Simon ^d,e   Fleming, Shaun ^d   Joshua, Douglas E ^a,b   Allen, John D ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^c INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^d PETER MACCALLUM CANCER CENTRE   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f LIVERPOOL HOSPITAL   (Australia)

Author keywords

Bortezomib; Myeloma; Unfolded protein response; XBP 1

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; BORTEZOMIB; CYTOTOXIC AGENT; DEXAMETHASONE; IMMUNOGLOBULIN; MELPHALAN; PREDNISONE; PROTEASOME; REGULATOR PROTEIN; TUNICAMYCIN; X BOX BINDING PROTEIN 1;

ADULT; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CANCER CELL CULTURE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; CROSS RESISTANCE; DOWN REGULATION; DRUG MEGADOSE; DRUG RESISTANCE; DRUG RESPONSE; DRUG SENSITIVITY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGLOBULIN PRODUCTION; IN VITRO STUDY; MALE; MULTIPLE CYCLE TREATMENT; MYELOMA; PREDICTION; PROTEIN EXPRESSION; UNFOLDED PROTEIN RESPONSE;

ACTIVATING TRANSCRIPTION FACTOR 6; ADULT; AGED; ANTINEOPLASTIC AGENTS; BORONIC ACIDS; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; FEMALE; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOGLOBULINS; JURKAT CELLS; MALE; MIDDLE AGED; MULTIPLE MYELOMA; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES; RNA SPLICING; RNA, MESSENGER; TRANSCRIPTION FACTORS; TREATMENT OUTCOME; UNFOLDED PROTEIN RESPONSE;

EID: 84855224484     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2011.043331     Document Type: Article

References (41)

1. Attal M, Moreau P, Avet-Loiseau H, Harousseau JL 2007. Stem cell transplantation in multiple myeloma. Hematology Hematology Am Soc Hematol Educ Program. 2007:311-6.
2. Child JA, Morgan GJ, Davies FE, Owen RG, Bell SE, Hawkins K, et al. High-dose chemotherapy with hematopoietic stem-cell rescue for multiple myeloma. N Engl J Med. 2003;348(19):1875-83.
3. Fermand JP, Katsahian S, Divine M, Leblond V, Dreyfus F, Macro M, et al. High-dose therapy and autologous blood stem-cell transplantation compared with conventional treatment in myeloma patients aged 55 to 65 years: long-term results of a randomized control trial from the Group Myelome-Autogreffe. J Clin Oncol. 2005;23(36):9227-33.
4. Lenhoff S, Hjorth M, Turesson I, Westin J, Gimsing P, Wisloff F, et al. Intensive therapy for multiple myeloma in patients younger than 60 years. Long-term results focusing on the effect of the degree of response on survival and relapse pattern after transplantation. Haematologica 2006; 91(9):1228-33.
5. Jagannath S, Barlogie B, Berenson J, Siegel D, Irwin D, Richardson PG, et al. A phase 2 study of two doses of bortezomib in relapsed or refractory myeloma. Br J Haematol. 2004;127(2):165-72.
6. Richardson PG, Barlogie B, Berenson J, Singhal S, Jagannath S, Irwin D, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma.[see comment]. N Engl J Med. 2003;348(26):2609-17.
7. Richardson PG, Barlogie B, Berenson J, Singhal S, Jagannath S, Irwin D, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med. 2003; 348(26):2609-17.
8. Richardson PG, Sonneveld P, Schuster MW, Irwin D, Stadtmauer EA, Facon T, et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 2005;352(24):2487-98.
9. Meister S, Schubert U, Neubert K, Herrmann K, Burger R, Gramatzki M, et al. Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Res. 2007;67(4):1783-92.
10. 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(7):1276-83.
11. 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 (19):16639-47.
12. 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(4):1530-4.
13. 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(7):3071-6.
14. 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(22):14374-9.
15. Fagioli C, Mezghrani A, Sitia R. Reduction of interchain disulfide bonds precedes the dislocation of Ig-mu chains from the endo-plasmic reticulum to the cytosol for protea-somal degradation. J Biol Chem. 2001;276(44):40962-7.
16. Lee YK, Brewer JW, Hellman R, Hendershot LM. BiP and immunoglobulin light chain cooperate to control the folding of heavy chain and ensure the fidelity of immunoglobulin assembly. Mol Biol Cell. 1999;10(7):2209-19.
17. O'Hare T, Wiens GD, Whitcomb EA, Enns CA, Rittenberg MB. Cutting edge: protea-some involvement in the degradation of unassembled Ig light chains. J Immunol 1999;163(1):11-4.
18. Imai J, Yashiroda H, Maruya M, Yahara I, Tanaka K. Proteasomes and molecular chaperones: cellular machinery responsible for folding and destruction of unfolded proteins. Cell Cycle. 2003;2(6):585-90.
19. Iwakoshi NN, Lee AH, Glimcher LH. The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response. Immunol Rev. 2003;194:29-38.
20. Iwakoshi NN, Lee AH, Vallabhajosyula P, Otipoby KL, Rajewsky K, Glimcher LH. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1.[see comment]. Nat Immunol. 2003;4(4):321-9.
21. Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, Gravallese EM, et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature. 2001;412(6844):300-7.
22. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee AH, Qian SB, Zhao H, et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 2004;21(1):81-93.
23. Lee AH, Iwakoshi NN, Anderson KC, Glimcher LH. Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc Natl Acad Sci USA. 2003;100(17):9946-51.
24. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticu-lum resident chaperone genes in the unfolded protein response. Mol Cell Biol. 2003;23(21):7448-59.
25. Shen Y, Hendershot LM. Identification of ERdj3 and OBF-1/BOB-1/OCA-B as direct targets of XBP-1 during plasma cell differentiation. J Immunol. 2007;179(5):2969-78.
26. Warburton P, Joshua DE, Ioannidis R, Brown R, Yuen E, Gibson J. Characterisation of a t(14;18) germinal centre cell line. Proceedings of the Haematology Society of Australia 1990:60.
27. Allen JD, Jackson SC, Schinkel AH. A mutation hot spot in the Bcrp1 (Abcg2) mul-tidrug transporter in mouse cell lines selected for Doxorubicin resistance. Cancer Res. 2002;62(8):2294-9.
28. Avery DT, Bryant VL, Ma CS, de Waal Malefyt R, Tangye SG. IL-21-induced iso-type switching to IgG and IgA by human naive B cells is differentially regulated by IL-4. J Immunol. 2008;181(3):1767-79.
29. Blade J, Samson D, Reece D, Apperley J, Bjorkstrand B, Gahrton G, et al. Criteria for evaluating disease response and progression in patients with multiple myeloma treated by high-dose therapy and haemopoietic stem cell transplantation. Myeloma Subcommittee of the EBMT. European Group for Blood and Marrow Transplant. Br J Haematol. 1998;102(5): 1115-23.
30. Bagratuni T, Wu P, Gonzalez de Castro D, Davenport EL, Dickens NJ, Walker BA, et al. XBP1s levels are implicated in the biology and outcome of myeloma mediating different clinical outcomes to thalidomide-based treatments. Blood. 116(2):250-3.
31. Mulligan G, Mitsiades C, Bryant B, Zhan F, Chng WJ, Roels S, et al. Gene expression profiling and correlation with outcome in clinical trials of the proteasome inhibitor bortezomib. Blood. 2007;109(8):3177-88.
32. Shringarpure R, Catley L, Bhole D, Burger R, Podar K, Tai YT, et al. Gene expression analysis of B-lymphoma cells resistant and sensitive to bortezomib. Br J Haematol. 2006;134(2):145-56.
33. Zhan F, Barlogie B, Mulligan G, Shaughnessy JD, Bryant B. High-risk myeloma: a gene expression based risk-stratification model for newly diagnosed multiple myeloma treated with high-dose therapy is predictive of outcome in relapsed disease treated with single-agent bortezomib or high-dose dexamethasone. Blood. 2008;111(2):968-9.
34. Oakervee HE, Popat R, Curry N, Smith P, Morris C, Drake M, et al. PAD combination therapy (PS-341/bortezomib, doxorubicin and dexamethasone) for previously untreated patients with multiple myeloma. Br J Haematol. 2005;129(6):755-62.
35. Jagannath S, Durie BG, Wolf J, Camacho E, Irwin D, Lutzky J, et al. Bortezomib therapy alone and in combination with dexam-ethasone for previously untreated symptomatic multiple myeloma. Br J Haematol. 2005;129(6):776-83.
36. Jagannath S, Richardson PG, Barlogie B, Berenson JR, Singhal S, Irwin D, et al. Bortezomib in combination with dexam-ethasone for the treatment of patients with relapsed and/or refractory multiple myeloma with less than optimal response to bortezomib alone. Haematologica. 2006;91 (7):929-34.
37. Orlowski RZ, Nagler A, Sonneveld P, Blade J, Hajek R, Spencer A, et al. Randomized phase III study of pegylated liposomal dox-orubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: combination therapy improves time to progression. J Clin Oncol. 2007;25(25):3892-901.
38. Palumbo A, Ambrosini MT, Benevolo G, Pregno P, Pescosta N, Callea V, et al. Bortezomib, melphalan, prednisone, and thalidomide for relapsed multiple myeloma. Blood. 2007;109(7):2767-72.
39. Adams J, Palombella VJ, Sausville EA, Johnson J, Destree A, Lazarus DD, et al. Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res. 1999;59(11):2615-22.
40. Fisher RI, Bernstein SH, Kahl BS, Djulbegovic B, Robertson MJ, de Vos S, et al. Multicenter phase II study of borte-zomib in patients with relapsed or refractory mantle cell lymphoma.[see comment]. J Clin Oncol. 2006;24(30):4867-74.
41. Treon SP, Ioakimidis L, Soumerai JD, Patterson CJ, Sheehy P, Nelson M, et al. Primary therapy of Waldenstrom macroglobulinemia with bortezomib, dex-amethasone, and rituximab: WMCTG clinical trial 05-180. J Clin Oncol. 2009;27(23): 3830-5.