Anergic bone marrow Vγ9Vδ2 T cells as early and long-lasting markers of PD-1-targetable microenvironment-induced immune suppression in human myeloma

OncoImmunology

Volumn 4, Issue 11, 2015, Pages

  Castella, Barbara ^a,b   Foglietta, Myriam ^a,b   Sciancalepore, Patrizia ^a,b   Rigoni, Micol ^a,b   Coscia, Marta ^a,b   Griggio, Valentina ^a,b   Vitale, Candida ^a,b   Ferracini, Riccardo ^c   Saraci, Elona ^b   Omedé, Paola ^b   Riganti, Chiara ^b   Palumbo, Antonio ^b   Boccadoro, Mario ^b   Massaia, Massimo ^a,b  

^a Centro di Ricerca in Medicina Sperimentale   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c CITTÀ DELLA SALUTE E DELLA SCIENZA HOSPITAL   (Italy)

Author keywords

MDSC; multiple myeloma; PD 1 PDL 1 pathway; V 9V 2 T cells

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; N METHYLTRYPTOPHAN; PHOSPHODIESTERASE V; PROGRAMMED DEATH 1 RECEPTOR; REACTIVE OXYGEN METABOLITE; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; ZOLEDRONIC ACID;

ARTICLE; B LYMPHOCYTE; BONE MARROW DERIVED MONONUCLEAR CELL; BONE MARROW T LYMPHOCYTE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNOCOMPETENCE; IMMUNOPATHOLOGY; IMMUNOPHENOTYPING; IMMUNOSUPPRESSIVE TREATMENT; MAJOR CLINICAL STUDY; MEMORY T LYMPHOCYTE; MONOCLONAL IMMUNOGLOBULINEMIA; MULTIPLE MYELOMA; MYELOMA CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMACYTOMA; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SUPPRESSOR CELL; T CELL DEPLETION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR MICROENVIRONMENT;

EID: 84941771207     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1047580     Document Type: Article

References (36)

1. M.S.Raab, K.Podar, I.Breitkreutz, P.G.Richardson, K.C.Anderson. Multiple myeloma. Lancet. 2009; 374:324-39; PMID:19541364; http://dx.doi.org/10.1016/S0140-6736(09)60221-X
2. B.Castella, C.Vitale, M.Coscia, M.Massaia. Vγ9Vδ2 T cell-based immunotherapy in hematological malignancies: from bench to bedside. Cell Mol Life Sci. 2011; 68(14):2419-32; PMID:21584812; http://dx.doi.org/10.1007/s00018-011-0704-8
3. H.J.Gober, M.Kistowska, L.Angman, P.Jeno, L.Mori, G.De Libero. Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 2003; 197:163-168; PMID:12538656; http://dx.doi.org/10.1084/jem.20021500
4. A.J.Roelofs, K.Thompson, S.Gordon, M.J.Rogers. Molecular mechanisms of action of bisphosphonates: current status. Clin. Cancer Res. 2006; 12:6222s-6230s; PMID:17062705; http://dx.doi.org/10.1158/1078-0432.CCR-06-0843
5. H.Monkkonen, P.D.Ottewell, J.Kuokkanen, J.Monkkonen, S.Auriola, I.Holen. Zoledronic acid-induced IPP/ApppI production in vivo. Life Sci. 2007; 81:1066-1070; PMID:17850825; http://dx.doi.org/10.1016/j.lfs.2007.08.007
6. S.Mariani, M.Muraro, F.Pantaleoni, F.Fiore, B.Nuschak, S.Peola, M.Foglietta, A.Palumbo, M.Coscia, B.Castella et al. Effector gammadelta T cells and tumor cells as immune targets of zoledronic acid in multiple myeloma. Leukemia. 2005; 19: 664-670; PMID:15744346; http://dx.doi.org/10.1038/sj.leu.2403693
7. F.Fiore, B.Castella, B.Nuschak, R.Bertieri, S.Mariani, B.Bruno, F.Pantaleoni, M.Foglietta, M.Boccadoro, M.Massaia. Enhanced ability of dendritic cells to stimulate innate and adaptive immunity upon short-term incubation with zoledronic acid. Blood. 2007; 110:921-927; PMID:17403919; http://dx.doi.org/10.1182/blood-2006-09-044321
8. E.Aktas, U.C.Kucuksezer, S.Bilgic, G.Erten, G.Deniz. Relationship between CD107a expression and cytotoxic activity. Cell Immunol. 2009; 254(2):149-54; PMID:18835598; http://dx.doi.org/10.1016/j.cellimm.2008.08.007
9. B.Castella, C.Riganti, F.Fiore, F.Pantaleoni, M.E.Canepari, S.Peola, M.Foglietta, A.Palumbo, A.Bosia, M.Coscia et al. Immune Modulation by Zoledronic Acid in Human Myeloma: An Advantageous Cross Talk between V{gamma}9V{delta}2 T Cells, {alpha}{beta} CD8+ T Cells, Regulatory T Cells, and Dendritic Cells. J Immunol. 2011; 187:1578-90; PMID:21753152; http://dx.doi.org/10.4049/jimmunol.1002514
10. G.T.Görgün, G.Whitehill, J.L.Anderson, T.Hideshima, C.Maguire, J.Laubach, N.Raje, N.C.Munshi, P.G.Richardson, K.C.Anderson. Tumor-promoting immune-suppressive myeloid-derived suppressor cells in the multiple myeloma microenvironment in humans. Blood. 2013; 121:2975-2987; PMID:23321256; http://dx.doi.org/10.1182/blood-2012-08-448548
11. I.R.Ramachandran, A.Martner, A.Pisklakova, T.Condamine, T.Chase, T.Vogl, J.Roth, D.Gabrilovich, Y.Nefedova. Myeloid-derived suppressor cells regulate growth of multiple myeloma by inhibiting T cells in bone marrow. J Immunol. 2013; 190(7):3815-23; PMID:23460744; http://dx.doi.org/10.4049/jimmunol.1203373
12. E.Espinosa, C.Belmant, F.Pont, B.Luciani, R.Poupot, F.Romagné, H.Brailly, M.Bonneville, J.J.Fournié. Chemical synthesis and biological activity of bromohydrin pyrophosphate, a potent stimulator of human gamma delta T cells. J Biol Biochem 2001; 276(21):18337-44; PMID:11279081; http://dx.doi.org/10.1074/jbc.M100495200
13. M.Foglietta, B.Castella, S.Mariani, M.Coscia, L.Godio, R.Ferracini, M.Ruggeri, V.Muccio, P.Omedé, A.Palumbo et al. The bone marrow of myeloma patients is steadily inhabited by a normal-sized pool of functional regulatory T cells irrespective of the disease status. Haematologica. 2014; 99(10):1605-10; PMID:24972771; http://dx.doi.org/10.3324/haematol.2014.105866
14. V.Kunzmann, B.Kimmel, T.Herrmann, H.Einsele, M.Wilhelm. Inhibition of phosphoantigen-mediated gammadelta T-cell proliferation by CD4+ CD25+ FoxP3+ regulatory T cells. Immunology. 2009; 126(2):256-67; PMID:18775028; http://dx.doi.org/10.1111/j.1365-2567.2008.02894.x
15. T.Ito, Y.H.Wang, O.Duramad, S.Hanabuchi, O.A.Perng, M.Gilliet, F.X.Qin, Y.J.Liu. OX40 ligand shuts down IL-10-producing regulatory T cells. Proc Natl Acad Sci. 2006; 103:13138-43; PMID:16924108; http://dx.doi.org/10.1073/pnas.0603107103
16. J.Liu, A.Hamrouni, D.Wolowiec, V.Coiteux, K.Kuliczkowski, D.Hetuin, A.Saudemont, B.Quesnel. Plasma cells from multiple myeloma patients express B7-H1 (PD-L1) and increase expression after stimulation with IFN-{gamma} and TLR ligands via a MyD88, TRAF6-, and MEK-dependent pathway. Blood. 2007; 110:296-304; PMID:17363736; http://dx.doi.org/10.1182/blood-2006-10-051482
17. D.M.BensonJr, C.E.Bakan, A.Mishra, C.C.Hofmeister, Y.Efebera, B.Becknell, R.A.Baiocchi, J.Zhang, J.Yu, M.K.Smith et al. The PD-1/PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody. Blood. 2010; 116(13):2286-94; PMID:20460501; http://dx.doi.org/10.1182/blood-2010-02-271874
18. J.Rosenblatt, B.Glotzbecker, H.Mills, B.Vasir, D.Tzachanis, J.D.Levine, R.M.Joyce, K.Wellenstein, W.Keefe, M.Schickler et al. PD-1 blockade by CT-011, anti-PD-1 antibody, enhances ex vivo T-cell responses to autologous dendritic cell/myeloma fusion vaccine. J Immunother. 2011; 34(5):409-18; PMID:21577144; http://dx.doi.org/10.1097/CJI.0b013e31821ca6ce
19. K.Luptakova, J.Rosenblatt, B.Glotzbecker, H.Mills, D.Stroopinsky, T.Kufe, B.Vasir, J.Arnason, D.Tzachanis, J.I.Zwicker et al. Lenalidomide enhances anti-myeloma cellular immunity. Cancer Immunol Immunother. 2013; 62(1):39-49; PMID:22733396; http://dx.doi.org/10.1007/s00262-012-1308-3
20. W.H.Hallett, W.Jing, W.R.Drobyski, B.D.Johnson. Immunosuppressive effects of multiple myeloma are overcome by PD-L1 blockade. Biol Blood Marrow Transplant. 2011; 17(8):1133-45; PMID:21536144; http://dx.doi.org/10.1016/j.bbmt.2011.03.011
21. T.J.Kearl, W.Jing, J.A.Gershan, B.D.Johnson. Programmed death receptor-1/programmed death receptor ligand-1 blockade after transient lymphodepletion to treat myeloma. J Immunol. 2013; 190(11):5620-8; PMID:23616570; http://dx.doi.org/10.4049/jimmunol.1202005
22. F.Dieli, F.Poccia, M.Lipp, G.Sireci, N.Caccamo, C.Di Sano, A.Salerno. Differentiation of effector/memory Vdelta2 T cells and migratory routes in lymph nodes or inflammatory sites. J Exp Med. 2003; 198(3):391-7; PMID:12900516; http://dx.doi.org/10.1084/jem.20030235
23. M.Iwasaki, Y.Tanaka, H.Kobayashi, K.Murata-Hirai, H.Miyabe, T.Sugie, M.Toi, N.Minato. Expression and function of PD-1 in human γδ T cells that recognize phosphoantigens. Eur J Immunol. 2011; 41(2):345-55; PMID:21268005; http://dx.doi.org/10.1002/eji.201040959
24. J.Favaloro, T.Liyadipitiya, R.Brown, S.Yang, H.Suen, N.Woodland, N.Nassif, D.Hart, P.Fromm, C.Weatherburn et al. Myeloid derived suppressor cells are numerically, functionally and phenotypically different in patients with multiple myeloma. Leuk Lymphoma. 2014; 12:1–8; PMID:4625328; http://dx.doi.org/10.3109/10428194.2014.904511
25. S.K.Martin, P.Diamond, S.Gronthos, D.J.Peet, A.C.Zannettino. The emerging role of hypoxia, HIF-1 and HIF-2 in multiple myeloma. Leukemia. 2011; 25(10):1533-42; PMID:21637285; http://dx.doi.org/10.1038/leu.2011.122
26. M.Z.Noman, G.Desantis, B.Janji, M.Hasmim, S.Karray, P.Dessen, V.Bronte, S.Chouaib. PD-L1 is a novel direct target of HIF-1α, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med. 2014; 211(5):781-90; PMID:24778419; http://dx.doi.org/10.1084/jem.20131916
27. J.H.Myklebust, J.M.Irish, J.Brody, D.K.Czerwinski, R.Houot, H.E.Kohrt, J.Timmerman, J.Said, M.R.Green, J.Delabie et al. High PD-1 expression and suppressed cytokine signaling distinguish T cells infiltrating follicular lymphoma tumor from peripheral T cells. Blood. 2013; 121(8):1367-76; PMID:23297127; http://dx.doi.org/10.1182/blood-2012-04-421826
28. H.Tamura, M.Ishibashi, T.Yamashita, S.Tanosaki, N.Okuyama, A.Kondo, H.Hyodo, E.Shinya, H.Takahashi, H.Dong et al. Marrow stromal cells induce B7-H1 expression on myeloma cells, generating aggressive characteristics in multiple myeloma. Leukemia. 2013; 27(2):464-72; PMID:22828443; http://dx.doi.org/10.1038/leu.2012.213
29. S.F.Wang, S.Fouquet, M.Chapon, H.Salmon, F.Regnier, K.Labroquère, C.Badoual, D.Damotte, P.Validire, E.Maubec et al. Early T Cell Signalling Is Reversibly Altered in PD-1+ T Lymphocytes Infiltrating Human Tumors. PloS ONE. 2011; 6(3):e17621; PMID:21408177; http://dx.doi.org/10.1371/journal.pone.0017621
30. B.Youngblood, K.J.Oestreich, S.J.Ha, J.Duraiswamy, R.S.Akondy, E.E.West, Z.Wei, P.Lu, J.W.Austin, J.L.Riley et al. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity. 2011; 35(3):400-12; PMID:21943489; http://dx.doi.org/10.1016/j.immuni.2011.06.015
31. Q.Yi, A.Osterborg, S.Bergenbrant, H.Mellstedt, G.Holm, A.K.Lefvert. Idiotype-reactive T-cell subsets and tumor load in monoclonal gammopathies. Blood. 1995; 86(8):3043-9; PMID:7579398
32. J.Richter, N.Neparidze, L.Zhang, S.Nair, T.Monesmith, R.Sundaram, F.Miesowicz, K.M.Dhodapkar, M.V.Dhodapkar. Clinical regressions and broad immune activation following combination therapy targeting human NKT cells in myeloma. Blood. 2013; 121(3):423-30; PMID:23100308; http://dx.doi.org/10.1182/blood-2012-06-435503
33. M.M.Zheng, Z.Zhang, K.Bemis, A.R.Belch, L.M.Pilarski, J.E.Shively, J.Kirshner. The systemic cytokine environment is permanently altered in multiple myeloma. PloS One. 2013; 8(3):e58504; PMID:23544044; http://dx.doi.org/10.1371/journal.pone.0058504
34. P.Musto, M.T.Petrucci, S.Bringhen, T.Guglielmelli, T.Caravita, V.Bongarzoni, A.Andriani, G.D'Arena, E.Balleari, G.Pietrantuono et al. GIMEMA (Italian Group for Adult Hematologic Diseases)/Multiple Myeloma Working Party and the Italian Myeloma Network. A multicenter, randomized clinical trial comparing zoledronic acid versus observation in patients with asymptomatic myeloma. Cancer. 2008; 113(7):1588-95; PMID:18683218; http://dx.doi.org/10.1002/cncr.23783
35. M.Wilhelm, V.Kunzmann, S.Eckstein, P.Reimer, F.Weissinger, T.Ruediger, H.P.Tony. Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood. 2003; 102(1):200-6; PMID:12623838; http://dx.doi.org/10.1182/blood-2002-12-3665
36. Y.Abe, M.Muto, M.Nieda, Y.Nakagawa, A.Nicol, T.Kaneko, S.Goto, K.Yokokawa, K.Suzuki. Clinical and immunological evaluation of zoledronate-activated Vgamma9gammadelta T-cell-based immunotherapy for patients with multiple myeloma. Exp Hematol. 2009; 37(8):956-68; PMID:19409955; http://dx.doi.org/10.1016/j.exphem.2009.04.008