2,762
Views
21
CrossRef citations to date
0
Altmetric
Original Research

Bortezomib sensitizes multiple myeloma to NK cells via ER-stress-induced suppression of HLA-E and upregulation of DR5

ORCID Icon, , , , , ORCID Icon & show all
Article: e1534664 | Received 30 Apr 2018, Accepted 05 Oct 2018, Published online: 02 Nov 2018

References

  • Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9(5):503–510. doi:10.1038/ni1582.
  • Anfossi N, Andre P, Guia S, Falk CS, Roetynck S, Stewart CA, Breso V, Frassati C, Reviron D, Middleton D, et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity. 2006;25(2):331–342. doi:10.1016/j.immuni.2006.06.013.
  • Brodin P, Karre K, Hoglund P. NK cell education: not an on-off switch but a tunable rheostat. Trends Immunol. 2009;30(4):143–149. doi:10.1016/j.it.2009.01.006.
  • Shah JJ, Orlowski RZ. Proteasome inhibitors in the treatment of multiple myeloma. Leukemia. 2009;23(11):1964–1979. doi:10.1038/leu.2009.173.
  • Obeng EA, Carlson LM, Gutman DM, Harrington WJ Jr., Lee KP, Boise LH. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood. 2006;107(12):4907–4916. doi:10.1182/blood-2005-08-3531.
  • Rutkowski DT, Kaufman RJ. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci. 2007;32(10):469–476. doi:10.1016/j.tibs.2007.09.003.
  • Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 2007;14(9):1576–1582. doi:10.1038/sj.cdd.4402200.
  • Marino G, Niso-Santano M, Baehrecke EH, Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol. 2014;15(2):81–94. doi:10.1038/nrm3735.
  • Chauhan D, Hideshima T, Mitsiades C, Richardson P, Anderson KC. Proteasome inhibitor therapy in multiple myeloma. Mol Cancer Ther. 2005;4(4):686–692. doi:10.1158/1535-7163.MCT-04-0338.
  • Mateos MV, Oriol A, Martinez-Lopez J, Gutierrez N, Teruel AI, de Paz R, García-Laraña J, Bengoechea E, Martín A, Mediavilla JD, et al. Bortezomib, melphalan, and prednisone versus bortezomib, thalidomide, and prednisone as induction therapy followed by maintenance treatment with bortezomib and thalidomide versus bortezomib and prednisone in elderly patients with untreated multiple myeloma: a randomised trial. Lancet Oncol. 2010;11(10):934–941. doi:10.1016/S1470-2045(10)70187-X.
  • Gutman D, Morales AA, Boise LH. Acquisition of a multidrug-resistant phenotype with a proteasome inhibitor in multiple myeloma. Leukemia. 2009;23(11):2181–2183. doi:10.1038/leu.2009.123.
  • Chauhan D, Li G, Shringarpure R, Podar K, Ohtake Y, Hideshima T, Anderson KC. Blockade of Hsp27 overcomes Bortezomib/proteasome inhibitor PS-341 resistance in lymphoma cells. Cancer Research. 2003;63(19):6174–6177.
  • Oerlemans R, Franke NE, Assaraf YG, Cloos J, van Zantwijk I, Berkers CR, Scheffer GL, Debipersad K, Vojtekova K, Lemos C, et al. Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein. Blood. 2008;112(6):2489–2499. doi:10.1182/blood-2007-08-104950.
  • Ri M, Iida S, Nakashima T, Miyazaki H, Mori F, Ito A, Inagaki A, Kusumoto S, Ishida T, Komatsu H, 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):1506–1512. doi:10.1038/leu.2010.137.
  • Schewe DM, Aguirre-Ghiso JA. Inhibition of eIF2alpha dephosphorylation maximizes bortezomib efficiency and eliminates quiescent multiple myeloma cells surviving proteasome inhibitor therapy. Cancer Research. 2009;69(4):1545–1552. doi:10.1158/0008-5472.CAN-08-3858.
  • de Wilt LH, Kroon J, Jansen G, de Jong S, Peters GJ, Kruyt FA. Bortezomib and TRAIL: a perfect match for apoptotic elimination of tumour cells? Crit Rev Oncol Hematol. 2013;85(3):363–372. doi:10.1016/j.critrevonc.2012.08.001.
  • Lundqvist A, Abrams SI, Schrump DS, Alvarez G, Suffredini D, Berg M, Childs R. Bortezomib and depsipeptide sensitize tumors to tumor necrosis factor-related apoptosis-inducing ligand: a novel method to potentiate natural killer cell tumor cytotoxicity. Cancer Research. 2006;66(14):7317–7325. doi:10.1158/0008-5472.CAN-06-0680.
  • Ames E, Hallett WH, Murphy WJ. Sensitization of human breast cancer cells to natural killer cell-mediated cytotoxicity by proteasome inhibition. Clin Exp Immunol. 2009;155(3):504–513. doi:10.1111/j.1365-2249.2008.03818.x.
  • Hallett WH, Ames E, Motarjemi M, Barao I, Shanker A, Tamang DL, Sayers TJ, Hudig D, Murphy WJ. Sensitization of tumor cells to NK cell-mediated killing by proteasome inhibition. J Immunology. 2008;180(1):163–170. doi:10.4049/jimmunol.180.1.163.
  • Moreau P, Coiteux V, Hulin C, Leleu X, van de Velde H, Acharya M, Harousseau J-L. Prospective comparison of subcutaneous versus intravenous administration of bortezomib in patients with multiple myeloma. Haematologica. 2008;93(12):1908–1911. doi:10.3324/haematol.13285.
  • Braud VM, Allan DS, O’Callaghan CA, Soderstrom K, D’Andrea A, Ogg GS, Lazetic S, Young NT, Bell JI, Phillips JH, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998;391(6669):795–799. doi:10.1038/35869.
  • Shi J, Tricot GJ, Garg TK, Malaviarachchi PA, Szmania SM, Kellum RE, Storrie B, Mulder A, Shaughnessy JD, Barlogie B, et al. Bortezomib down-regulates the cell-surface expression of HLA class I and enhances natural killer cell-mediated lysis of myeloma. Blood. 2008;111(3):1309–1317. doi:10.1182/blood-2007-03-078535.
  • Reger R, Berg M, Lundqvist A, Donohue T, Carlsten M, Betters D, Cook L, Ramos C, Grasmeder S, Su S, et al. A Phase I trial of adoptively transferred Ex-vivo expanded autologous natural killer (NK) cells following treatment with bortezomib to sensitize tumors to NK cell cytotoxicity. American Society of Hematology. Volume 118: Blood; 2011. p Abstract 1001.
  • Xu L, Su L, Liu X. PKCdelta regulates death receptor 5 expression induced by PS-341 through ATF4-ATF3/CHOP axis in human lung cancer cells. Mol Cancer Ther. 2012;11(10):2174–2182. doi:10.1158/1535-7163.MCT-12-0602.
  • Ulbrecht M, Kellermann J, Johnson JP, Weiss EH. Impaired intracellular transport and cell surface expression of nonpolymorphic HLA-E: evidence for inefficient peptide binding. J Exp Med. 1992;176(4):1083–1090.
  • Ulbrecht M, Modrow S, Srivastava R, Peterson PA, Weiss EH. Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J Immunology. 1998;160(9):4375–4385.
  • Bland FA, Lemberg MK, McMichael AJ, Martoglio B, Braud VM. Requirement of the proteasome for the trimming of signal peptide-derived epitopes presented by the nonclassical major histocompatibility complex class I molecule HLA-E. J Biol Chem. 2003;278(36):33747–33752. doi:10.1074/jbc.M305593200.
  • Enqvist M, Nilsonne G, Hammarfjord O, Wallin RP, Bjorkstrom NK, Bjornstedt M, Hjerpe A, Ljunggren H-G, Dobra K, Malmberg K-J, et al. Selenite induces posttranscriptional blockade of HLA-E expression and sensitizes tumor cells to CD94/NKG2A-positive NK cells. J Immunology. 2011;187(7):3546–3554. doi:10.4049/jimmunol.1100610.
  • Godal R, Bachanova V, Gleason M, McCullar V, Yun GH, Cooley S, Verneris MR, McGlave PB, Miller JS. Natural killer cell killing of acute myelogenous leukemia and acute lymphoblastic leukemia blasts by killer cell immunoglobulin-like receptor-negative natural killer cells after NKG2A and LIR-1 blockade. Biol Blood Marrow Transplant. 2010;16(5):612–621. doi:10.1016/j.bbmt.2010.01.019.
  • Nguyen S, Beziat V, Dhedin N, Kuentz M, Vernant JP, Debre P, Vieillard V. HLA-E upregulation on IFN-gamma-activated AML blasts impairs CD94/NKG2A-dependent NK cytolysis after haplo-mismatched hematopoietic SCT. Bone Marrow Transplant. 2009;43(9):693–699. doi:10.1038/bmt.2008.380.
  • Carlsten M, Korde N, Kotecha R, Reger R, Bor S, Kazandjian D, Landgren O, Childs RW. Checkpoint inhibition of KIR2D with the monoclonal antibody IPH2101 induces contraction and hyporesponsiveness of NK cells in patients with myeloma. Clin Cancer Res. 2016;22(21):5211–5222. doi:10.1158/1078-0432.CCR-16-1108.
  • Dosani T, Carlsten M, Maric I, Landgren O. The cellular immune system in myelomagenesis: NK cells and T cells in the development of myeloma [corrected] and their uses in immunotherapies. Blood Cancer J. 2015;5:e306. doi:10.1038/bcj.2015.32.
  • Carlsten M, Norell H, Bryceson YT, Poschke I, Schedvins K, Ljunggren HG, Kiessling R, Malmberg K-J. Primary human tumor cells expressing CD155 impair tumor targeting by down-regulating DNAM-1 on NK cells. J Immunology. 2009;183(8):4921–4930. doi:10.4049/jimmunol.0901226.
  • Carlsten M, Baumann BC, Simonsson M, Jadersten M, Forsblom AM, Hammarstedt C, Bryceson YT, Ljunggren H-G, Hellström-Lindberg E, Malmberg K-J. Reduced DNAM-1 expression on bone marrow NK cells associated with impaired killing of CD34+ blasts in myelodysplastic syndrome. Leukemia. 2010;24(9):1607–1616. doi:10.1038/leu.2010.149.
  • Fauriat C, Just-Landi S, Mallet F, Arnoulet C, Sainty D, Olive D, Costello RT. Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood. 2007;109(1):323–330. doi:10.1182/blood-2005-08-027979.
  • Childs RW, Berg M. Bringing natural killer cells to the clinic: ex vivo manipulation. Hematology Am Soc Hematol Educ Program. 2013;2013:234–246. doi:10.1182/asheducation-2013.1.234.
  • Carlsten M, Childs RW. Genetic manipulation of NK cells for cancer immunotherapy: techniques and clinical implications. Front Immunol. 2015;6:266. doi:10.3389/fimmu.2015.00266.
  • de Kruijf EM, Sajet A, van Nes JG, Natanov R, Putter H, Smit VT, Liefers GJ, van Den Elsen PJ, van de Velde CJH, Kuppen PJK. HLA-E and HLA-G expression in classical HLA class I-negative tumors is of prognostic value for clinical outcome of early breast cancer patients. J Immunology. 2010;185(12):7452–7459. doi:10.4049/jimmunol.1002629.
  • Malmberg K-J, Levitsky V, Norell H, de Matos CT, Carlsten M, Schedvins K, Rabbani H, Moretta A, Söderström K, Levitskaya J, et al. IFN-gamma protects short-term ovarian carcinoma cell lines from CTL lysis via a CD94/NKG2A-dependent mechanism. J Clin Invest. 2002;110(10):1515–1523. doi:10.1172/JCI15564.
  • Levy EM, Bianchini M, Von Euw EM, Barrio MM, Bravo AI, Furman D, Domenichini E, Macagno C, Pinsky V, Zucchini C, et al. Human leukocyte antigen-E protein is overexpressed in primary human colorectal cancer. Int J Oncol. 2008;32(3):633–641.
  • Goncalves MA, Le Discorde M, Simoes RT, Rabreau M, Soares EG, Donadi EA, Carosella ED. Classical and non-classical HLA molecules and p16(INK4a) expression in precursors lesions and invasive cervical cancer. Eur J Obstet Gynecol Reprod Biol. 2008;141(1):70–74. doi:10.1016/j.ejogrb.2008.06.010.
  • Derre L, Corvaisier M, Charreau B, Moreau A, Godefroy E, Moreau-Aubry A, Jotereau F, Gervois N. Expression and release of HLA-E by melanoma cells and melanocytes: potential impact on the response of cytotoxic effector cells. J Immunology. 2006;177(5):3100–3107. doi:10.4049/jimmunol.177.5.3100.
  • Wischhusen J, Friese MA, Mittelbronn M, Meyermann R, Weller MHLA-E. protects glioma cells from NKG2D-mediated immune responses in vitro: implications for immune escape in vivo. J Neuropathol Exp Neurol. 2005;64(6):523–528.
  • Dutta N, Majumder D, Gupta A, Mazumder DN, Banerjee S. Analysis of human lymphocyte antigen class I expression in gastric cancer by reverse transcriptase-polymerase chain reaction. Hum Immunol. 2005;66(2):164–169. doi:10.1016/j.humimm.2004.10.010.
  • Seliger B, Jasinski-Bergner S, Quandt D, Stoehr C, Bukur J, Wach S, Legal W, Taubert H, Wullich B, Hartmann A. HLA-E expression and its clinical relevance in human renal cell carcinoma. Oncotarget. 2016;7(41):67360–67372. doi:10.18632/oncotarget.11744.
  • Liu BQ, Gao YY, Niu XF, Xie JS, Meng X, Guan Y, Wang H-Q. Implication of unfolded protein response in resveratrol-induced inhibition of K562 cell proliferation. Biochem Biophys Res Commun. 2010;391(1):778–782. doi:10.1016/j.bbrc.2009.11.137.
  • Segar KP, Chandrawanshi V, Mehra S. Activation of unfolded protein response pathway is important for valproic acid mediated increase in immunoglobulin G productivity in recombinant Chinese hamster ovary cells. J Biosci Bioeng. 2017. doi:10.1016/j.jbiosc.2017.05.005.
  • Haefliger S, Klebig C, Schaubitzer K, Schardt J, Timchenko N, Mueller BU, Pabst T. Protein disulfide isomerase blocks CEBPA translation and is up-regulated during the unfolded protein response in AML. Blood. 2011;117(22):5931–5940. doi:10.1182/blood-2010-08-304485.
  • Brodin O, Eksborg S, Wallenberg M, Asker-Hagelberg C, Larsen EH, Mohlkert D, Lenneby-Helleday C, Jacobsson H, Linder S, Misra S, et al. Pharmacokinetics and toxicity of sodium selenite in the treatment of patients with carcinoma in a Phase I clinical trial: the SECAR study. Nutrients. 2015;7(6):4978–4994. doi:10.3390/nu7064978.
  • Shigemi Z, Manabe K, Hara N, Baba Y, Hosokawa K, Kagawa H, Watanabe T, Fujimuro M. Methylseleninic acid and sodium selenite induce severe ER stress and subsequent apoptosis through UPR activation in PEL cells. Chem Biol Interact. 2017;266:28–37. doi:10.1016/j.cbi.2017.01.027.