CD28-mediated pro-survival signaling induces chemotherapeutic resistance in multiple myeloma

Blood

Volumn 123, Issue 24, 2014, Pages 3770-3779

  Murray, Megan E ^a   Gavile, Catherine M ^b   Nair, Jayakumar R ^a   Koorella, Chandana ^a   Carlson, Louise M ^a   Buac, Daniela ^a   Utley, Adam ^a   Chesi, Marta ^c   Bergsagel, P Leif ^c   Boise, Lawrence H ^b   Lee, Kelvin P ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABATACEPT; CD28 ANTIGEN; IMMUNOGLOBULIN G; MELPHALAN; PHOSPHATIDYLINOSITOL 3 KINASE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RESISTANCE; CANCER SURVIVAL; CELL ISOLATION; CELL SURVIVAL; CONTROLLED STUDY; CROSS LINKING; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IN VITRO STUDY; MOUSE; MULTIPLE MYELOMA; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; WESTERN BLOTTING;

ANIMALS; ANTIBODIES; ANTIGENS, CD28; ANTINEOPLASTIC AGENTS; CELL SURVIVAL; CELLS, CULTURED; DENDRITIC CELLS; DRUG RESISTANCE, NEOPLASM; HUMANS; MICE; MICE, TRANSGENIC; MULTIPLE MYELOMA; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84902602754     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-10-530964     Document Type: Article

References (58)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010;60(5):277-300.
2. Attal M, Harousseau JL, Leyvraz S, et al Inter-Groupe Francophone du Myélome (IFM). Maintenance therapy with thalidomide improves survival in patients with multiple myeloma. Blood. 2006;108(10):3289-3294.
3. Kumar SK, Rajkumar SV, Dispenzieri A, et al. Improved survival in multiple myeloma and the impact of novel therapies. Blood. 2008;111(5):2516- 2520.
4. Richardson PG, Barlogie B, Berenson J, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med. 2003;348(26):2609- 2617. (Pubitemid 36741588)
5. Spanswick VJ, Craddock C, Sekhar M, et al. Repair of DNA interstrand crosslinks as a mechanism of clinical resistance to melphalan in multiple myeloma. Blood. 2002;100(1):224-229. (Pubitemid 35177451)
6. 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. 2011;10(11):2034-2042.
7. Hideshima T, Chauhan D, Shima Y, et al. Thalidomide and its analogs overcome drug resistance of human multiple myeloma cells to conventional therapy. Blood. 2000;96(9):2943-2950.
8. Mitsiades CS, Mitsiades NS, Munshi NC, Richardson PG, Anderson KC. The role of the bone microenvironment in the pathophysiology and therapeutic management of multiple myeloma: interplay of growth factors, their receptors and stromal interactions. Eur J Cancer. 2006;42(11):1564-1573. (Pubitemid 44118771)
9. Degrassi A, Hilbert DM, Rudikoff S, Anderson AO, Potter M, Coon HG. In vitro culture of primary plasmacytomas requires stromal cell feeder layers. Proc Natl Acad Sci USA. 1993;90(5):2060-2064. (Pubitemid 23069997)
10. Zhang XG, Gaillard JP, Robillard N, et al. Reproducible obtaining of human myeloma cell lines as a model for tumor stem cell study in human multiple myeloma. Blood. 1994;83(12):3654-3663. (Pubitemid 24175556)
11. Caligaris-Cappio F, Gregoretti MG, Ghia P, Bergui L. In vitro growth of human multiple myeloma: implications for biology and therapy. Hematol Oncol Clin North Am. 1992;6(2):257-271.
12. Hideshima T, Nakamura N, Chauhan D, Anderson KC. Biologic sequelae of interleukin-6 induced PI3-K/Akt signaling in multiple myeloma. Oncogene. 2001;20(42):5991-6000. (Pubitemid 32955041)
13. Hirano T, Ishihara K, Hibi M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene. 2000;19(21):2548-2556. (Pubitemid 30339210)
14. Nair JR, Carlson LM, Koorella C, et al. CD28 expressed on malignant plasma cells induces a prosurvival and immunosuppressive microenvironment. J Immunol. 2011;187(3):1243-1253.
15. Moreaux J, Legouffe E, Jourdan E, et al. BAFF and APRIL protect myeloma cells from apoptosis induced by interleukin 6 deprivation and dexamethasone. Blood. 2004;103(8):3148-3157. (Pubitemid 38451693)
16. Tai YT, Li XF, Breitkreutz I, et al. Role of B-cell-activating factor in adhesion and growth of human multiple myeloma cells in the bone marrow microenvironment. Cancer Res. 2006;66(13):6675-6682. (Pubitemid 44085624)
17. Damiano JS, Cress AE, Hazlehurst LA, Shtil AA, Dalton WS. Cell adhesion mediated drug resistance (CAM-DR): role of integrins and resistance to apoptosis in human myeloma cell lines. Blood. 1999;93(5):1658-1667. (Pubitemid 29102494)
18. Damiano JS, Dalton WS. Integrin-mediated drug resistance in multiple myeloma. Leuk Lymphoma. 2000;38(1-2):71-81. (Pubitemid 30224324)
19. Zheng Y, Cai Z, Wang S, et al. Macrophages are an abundant component of myeloma microenvironment and protect myeloma cells from chemotherapy drug-induced apoptosis. Blood. 2009;114(17):3625-3628.
20. Bahlis NJ, King AM, Kolonias D, et al. CD28-mediated regulation of multiple myeloma cell proliferation and survival. Blood. 2007;109(11):5002-5010. (Pubitemid 46827800)
21. Hazlehurst LA, Enkemann SA, Beam CA, et al. Genotypic and phenotypic comparisons of de novo and acquired melphalan resistance in an isogenic multiple myeloma cell line model. Cancer Res. 2003;63(22):7900-7906. (Pubitemid 37466725)
22. Nefedova Y, Cheng P, Alsina M, Dalton WS, Gabrilovich DI. Involvement of Notch-1 signaling in bone marrow stroma-mediated de novo drug resistance of myeloma and other malignant lymphoid cell lines. Blood. 2004;103(9):3503-3510. (Pubitemid 38525684)
23. Rudd CE, Taylor A, Schneider H. CD28 and CTLA-4 coreceptor expression and signal transduction. Immunol Rev. 2009;229(1):12-26.
24. Sharpe AH, Freeman GJ. The B7-CD28 superfamily. Nat Rev Immunol. 2002;2(2):116-126. (Pubitemid 37323235)
25. Kozbor D, Moretta A, Messner HA, Moretta L, Croce CM. Tp44 molecules involved in antigen-independent T cell activation are expressed on human plasma cells. J Immunol. 1987;138(12):4128-4132. (Pubitemid 17090376)
26. Rozanski CH, Arens R, Carlson LM, et al. Sustained antibody responses depend on CD28 function in bone marrow-resident plasma cells. J Exp Med. 2011;208(7):1435-1446.
27. Robillard N, Jego G, Pellat-Deceunynck C, et al. CD28, a marker associated with tumoral expansion in multiple myeloma. Clin Cancer Res. 1998;4(6):1521-1526. (Pubitemid 28265238)
28. Almeida J, Orfao A, Ocqueteau M, et al. High-sensitive immunophenotyping and DNA ploidy studies for the investigation of minimal residual disease in multiple myeloma. Br J Haematol. 1999;107(1):121-131. (Pubitemid 29500817)
29. Paiva B, Vidriales MB, Cerveró J, et al GEM (Grupo Español de MM)/PETHEMA (Programa para el Estudio de la Terapéutica en Hemopatías Malignas) Cooperative Study Groups. Multiparameter flow cytometric remission is the most relevant prognostic factor for multiple myeloma patients who undergo autologous stem cell transplantation. Blood. 2008;112(10):4017-4023.
30. Mateo G, Castellanos M, Rasillo A, et al. Genetic abnormalities and patterns of antigenic expression in multiple myeloma. Clin Cancer Res. 2005;11(10):3661-3667. (Pubitemid 40685582)
31. Pope B, Brown RD, Gibson J, Yuen E, Joshua D. B7-2-positive myeloma: incidence, clinical characteristics, prognostic significance, and implications for tumor immunotherapy. Blood. 2000;96(4):1274-1279. (Pubitemid 30658455)
32. Friend LD, Shah DD, Deppong C, et al. A dose-dependent requirement for the proline motif of CD28 in cellular and humoral immunity revealed by a targeted knockin mutant. J Exp Med. 2006;203(9):2121-2133. (Pubitemid 44352233)
33. Burr JS, Savage ND, Messah GE, et al. Cutting edge: distinct motifs within CD28 regulate T cell proliferation and induction of Bcl-XL. J Immunol. 2001;166(9):5331-5335. (Pubitemid 32374151)
34. Pene F, Claessens YE, Muller O, et al. Role of the phosphatidylinositol 3-kinase/Akt and mTOR/P70S6-kinase pathways in the proliferation and apoptosis in multiple myeloma. Oncogene. 2002;21(43):6587-6597. (Pubitemid 35177037)
35. Hideshima T, Catley L, Yasui H, et al. Perifosine, an oral bioactive novel alkylphospholipid, inhibits Akt and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells. Blood. 2006;107(10):4053-4062. (Pubitemid 43726814)
36. Marani M, Tenev T, Hancock D, Downward J, Lemoine NR. Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol Cell Biol. 2002;22(11):3577-3589. (Pubitemid 34527138)
37. Chesi M, Robbiani DF, Sebag M, et al. AID-dependent activation of a MYC transgene induces multiple myeloma in a conditional mouse model of post-germinal center malignancies. Cancer Cell. 2008;13(2):167-180. (Pubitemid 351163163)
38. Vieira P, Rajewsky K. The half-lives of serum immunoglobulins in adult mice. Eur J Immunol. 1988;18(2):313-316. (Pubitemid 18078861)
39. Peterson TR, Laplante M, Thoreen CC, et al. DEPTOR is an mTOR inhibitor frequently overexpressed in multiple myeloma cells and required for their survival. Cell. 2009;137(5):873-886.
40. Menu E, Kooijman R, Van Valckenborgh E, et al. Specific roles for the PI3K and the MEK-ERK pathway in IGF-1-stimulated chemotaxis, VEGF secretion and proliferation of multiple myeloma cells: study in the 5T33MM model. Br J Cancer. 2004;90(5):1076-1083. (Pubitemid 38495831)
41. Zhu S, Evans S, Yan B, et al. Transcriptional regulation of Bim by FOXO3a and Akt mediates scleroderma serum-induced apoptosis in endothelial progenitor cells. Circulation. 2008;118(21):2156-2165.
42. Skurk C, Maatz H, Kim HS, et al. The Akt-regulated forkhead transcription factor FOXO3a controls endothelial cell viability through modulation of the caspase-8 inhibitor FLIP. J Biol Chem. 2004;279(2):1513-1525. (Pubitemid 38082681)
43. Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene. 2005;24(50):7410-7425. (Pubitemid 41637981)
44. Van Der Heide LP, Hoekman MF, Smidt MP. The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J. 2004;380(Pt 2):297-309. (Pubitemid 38788101)
45. Gilley J, Coffer PJ, Ham J. FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol. 2003;162(4):613-622. (Pubitemid 37022939)
46. Sunters A, Fernández de Mattos S, Stahl M, et al. FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem. 2003;278(50):49795-49805.
47. Urbich C, Knau A, Fichtlscherer S, et al. FOXO-dependent expression of the proapoptotic protein Bim: pivotal role for apoptosis signaling in endothelial progenitor cells. FASEB J. 2005;19(8):974-976. (Pubitemid 40827722)
48. Guan H, Song L, Cai J, et al. Sphingosine kinase 1 regulates the Akt/FOXO3a/Bim pathway and contributes to apoptosis resistance in glioma cells. PLoS ONE. 2011;6(5):e19946.
49. Gomez-Bougie P, Bataille R, Amiot M. The imbalance between Bim and Mcl-1 expression controls the survival of human myeloma cells. Eur J Immunol. 2004;34(11):3156-3164. (Pubitemid 39549394)
50. Morales AA, Kurtoglu M, Matulis SM, et al. Distribution of Bim determines Mcl-1 dependence or codependence with Bcl-xL/Bcl-2 in Mcl-1-expressing myeloma cells. Blood. 2011;118(5):1329-1339.
51. Munugalavadla V, Mariathasan S, Slaga D, et al. The PI3K inhibitor GDC-0941 combines with existing clinical regimens for superior activity in multiple myeloma. Oncogene. 2014;33(3):316-325.
52. Wong TW, Kita H, Hanson CA, Walters DK, Arendt BK, Jelinek DF. Induction of malignant plasma cell proliferation by eosinophils. PLoS ONE. 2013;8(7):e70554.
53. Davis TA, Craighead N, Williams AJ, Scadron A, June CH, Lee KP. Primary porcine endothelial cells express membrane-bound B7-2 (CD86) and a soluble factor that co-stimulate cyclosporin A-resistant and CD28-dependent human T cell proliferation. Int Immunol. 1996;8(7):1099-1111. (Pubitemid 26235713)
54. Stagg J, Pommey S, Eliopoulos N, Galipeau J. Interferon-gamma-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood. 2006;107(6):2570-2577. (Pubitemid 43348704)
55. Abe M, Shintani Y, Eto Y, Harada K, Kosaka M, Matsumoto T. Potent induction of activin A secretion from monocytes and bone marrow stromal fibroblasts by cognate interaction with activated T cells. J Leukoc Biol. 2002;72(2):347-352.
56. Alexanian R, Bergsagel DE, Migliore PJ, Vaughn WK, Howe CD. Melphalan therapy for plasma cell myeloma. Blood. 1968;31(1):1-10.
57. Ruderman EM, Pope RM. The evolving clinical profile of abatacept (CTLA4-Ig): a novel co-stimulatory modulator for the treatment of rheumatoid arthritis. Arthritis Res Ther. 2005;7(Suppl 2):S21-S25. (Pubitemid 40936617)
58. You H, Pellegrini M, Tsuchihara K, et al. FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J Exp Med. 2006;203(7):1657-1663. (Pubitemid 44036270)