B and T lymphocyte attenuator mediates inhibition of tumor-reactive CD8 + T cells in patients after allogeneic stem cell transplantation

Journal of Immunology

Volumn 189, Issue 1, 2012, Pages 39-49

  Hobo, Willemijn ^a   Norde, Wieger J ^a   Schaap, Nicolaas ^b   Fredrix, Hanny ^a   Maas, Frans ^a   Schellens, Karen ^a   Falkenburg, J H Frederik ^c   Korman, Alan J ^d   Olive, Daniel ^e   Van Der Voort, Robbert ^a   Dolstra, Harry ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d BRISTOL MYERS SQUIBB   (United States)

^e INSTITUT PAOLI CALMETTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

B AND T LYMPHOCYTE ATTENUATOR; CYTOKINE; HERPESVIRUS ENTRY MEDIATOR LIGAND; LYMPHOCYTE RECEPTOR; MINOR HISTOCOMPATIBILITY ANTIGEN; PROGRAMMED DEATH 1 RECEPTOR; RECEPTOR ANTIBODY; UNCLASSIFIED DRUG;

ALLOGENEIC STEM CELL TRANSPLANTATION; ARTICLE; B CELL LYMPHOMA; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DEGRANULATION; DENDRITIC CELL; EFFECTOR CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; LEUKEMIA CELL; LYMPHOCYTE PROLIFERATION; LYMPHOMA CELL; MEMORY T LYMPHOCYTE; MULTIPLE MYELOMA; MYELOID LEUKEMIA; MYELOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TUMOR ESCAPE; UPREGULATION;

ANTIBODIES, BLOCKING; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; EPITOPES, T-LYMPHOCYTE; GENE TARGETING; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOLOGIC MEMORY; MINOR HISTOCOMPATIBILITY ANTIGENS; NEOPLASM RECURRENCE, LOCAL; RECEPTORS, IMMUNOLOGIC; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 14; TUMOR CELLS, CULTURED;

EID: 84862841841     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102807     Document Type: Article

References (45)

1. Kolb, H. J. 2008. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 112: 4371-4383.
2. Goulmy, E. 2004. Minor histocompatibility antigens: allo target molecules for tumor-specific immunotherapy. Cancer J. 10: 1-7. (Pubitemid 44313565)
3. Bleakley, M., and S. R. Riddell. 2004. Molecules and mechanisms of the graft-versus- leukaemia effect. Nat. Rev. Cancer 4: 371-380. (Pubitemid 38579483)
4. D'Cruz, L. M., M. P. Rubinstein, and A. W. Goldrath. 2009. Surviving the crash: transitioning from effector to memory CD8+ T cell. Semin. Immunol. 21: 92-98.
5. de Rijke, B., A. van Horssen-Zoetbrood, J. M. Beekman, B. Otterud, F. Maas, R. Woestenenk, M. Kester, M. Leppert, A. V. Schattenberg, T. de Witte, et al. 2005. A frameshift polymorphism in P2X5 elicits an allogeneic cytotoxic T lymphocyte response associated with remission of chronic myeloid leukemia. J. Clin. Invest. 115: 3506-3516. (Pubitemid 43121838)
6. Norde, W. J., I. M. Overes, F. Maas, H. Fredrix, J. C. Vos, M. G. Kester, R. van der Voort, I. Jedema, J. H. Falkenburg, A. V. Schattenberg, et al. 2009. Myeloid leukemic progenitor cells can be specifically targeted by minor histocompatibility antigen LRH-1-reactive cytotoxic T cells. Blood 113: 2312-2323.
7. Croci, D. O., M. F. Zacarías Fluck, M. J. Rico, P. Matar, G. A. Rabinovich, and O. G. Scharovsky. 2007. Dynamic cross-talk between tumor and immune cells in orchestrating the immunosuppressive network at the tumor microenvironment. Cancer Immunol. Immunother. 56: 1687-1700. (Pubitemid 47313090)
8. Cox, M. A., L. E. Harrington, and A. J. Zajac. 2011. Cytokines and the inception of CD8 T cell responses. Trends Immunol. 32: 180-186.
9. Chen, L. 2004. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat. Rev. Immunol. 4: 336-347. (Pubitemid 38649276)
10. Zang, X., and J. P. Allison. 2007. The B7 family and cancer therapy: costimulation and coinhibition. Clin. Cancer Res. 13: 5271-5279. (Pubitemid 47510350)
11. Kaufmann, D. E., and B. D. Walker. 2009. PD-1 and CTLA-4 inhibitory cosignaling pathways in HIV infection and the potential for therapeutic intervention. J. Immunol. 182: 5891-5897.
12. Watanabe, T., A. Bertoletti, and T. A. Tanoto. 2010. PD-1/PD-L1 pathway and T-cell exhaustion in chronic hepatitis virus infection. J. Viral Hepat. 17: 453-458.
13. Kaehler, K. C., S. Piel, E. Livingstone, B. Schilling, A. Hauschild, and D. Schadendorf. 2010. Update on immunologic therapy with anti-CTLA-4 antibodies in melanoma: identification of clinical and biological response patterns, immune-related adverse events, and their management. Semin. Oncol. 37: 485-498.
14. Malaspina, T. S., T. H. Gasparoto, M. R. Costa, E. F. de Melo, Jr., M. R. Ikoma, J. H. Damante, K. A. Cavassani, G. P. Garlet, J. S. da Silva, and A. P. Campanelli. 2011. Enhanced programmed death 1 (PD-1) and PD-1 ligand (PD-L1) expression in patients with actinic cheilitis and oral squamous cell carcinoma. Cancer Immunol. Immunother. 60: 965-974.
15. Zhang, J., X. Xiao, W. Liu, G. Demirci, and X. C. Li. 2009. Inhibitory receptors of the immune system: functions and therapeutic implications. Cell. Mol. Immunol. 6: 407-414.
16. Norde, W. J., F. Maas, W. Hobo, A. Korman, M. Quigley, M. G. Kester, K. Hebeda, J. H. Falkenburg, N. Schaap, T. M. deWitte, et al. 2011. PD-1/PD-L1 interactions contribute to functional T-cell impairment in patients who relapse with cancer after allogeneic stem cell transplantation. Cancer Res. 71: 5111-5122.
17. Riley, J. L. 2009. PD-1 signaling in primary T cells. Immunol. Rev. 229: 114-125.
18. Blackburn, S. D., H. Shin, W. N. Haining, T. Zou, C. J. Workman, A. Polley, M. R. Betts, G. J. Freeman, D. A. Vignali, and E. J. Wherry. 2009. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10: 29-37.
19. Watanabe, N., M. Gavrieli, J. R. Sedy, J. Yang, F. Fallarino, S. K. Loftin, M. A. Hurchla, N. Zimmerman, J. Sim, X. Zang, et al. 2003. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat. Immunol. 4: 670-679. (Pubitemid 36874444)
20. Sedy, J. R., M. Gavrieli, K. G. Potter, M. A. Hurchla, R. C. Lindsley, K. Hildner, S. Scheu, K. Pfeffer, C. F. Ware, T. L. Murphy, and K. M. Murphy. 2005. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat. Immunol. 6: 90-98. (Pubitemid 40136700)
21. Cai, G., and G. J. Freeman. 2009. The CD160, BTLA, LIGHT/HVEM pathway: a bidirectional switch regulating T-cell activation. Immunol. Rev. 229: 244-258.
22. del Rio, M. L., C. L. Lucas, L. Buhler, G. Rayat, and J. I. Rodriguez-Barbosa. 2010. HVEM/LIGHT/BTLA/CD160 cosignaling pathways as targets for immune regulation. J. Leukoc. Biol. 87: 223-235.
23. Derré, L., J. P. Rivals, C. Jandus, S. Pastor, D. Rimoldi, P. Romero, O. Michielin, D. Olive, and D. E. Speiser. 2010. BTLA mediates inhibition of human tumor-specific CD8+ T cells that can be partially reversed by vaccination. J. Clin. Invest. 120: 157-167.
24. Hobo, W., F. Maas, N. Adisty, T. de Witte, N. Schaap, R. van der Voort, and H. Dolstra. 2010. siRNA silencing of PD-L1 and PD-L2 on dendritic cells augments expansion and function of minor histocompatibility antigen-specific CD8+ T cells. Blood 116: 4501-4511.
25. Feng, X., K. M. Hui, H. M. Younes, and A. G. Brickner. 2008. Targeting minor histocompatibility antigens in graft versus tumor or graft versus leukemia responses. Trends Immunol. 29: 624-632.
26. Dazzi, F., R. M. Szydlo, and J. M. Goldman. 1999. Donor lymphocyte infusions for relapse of chronic myeloid leukemia after allogeneic stem cell transplant: where we now stand. Exp. Hematol. 27: 1477-1486. (Pubitemid 29458421)
27. Flies, D. B., and L. Chen. 2006. Modulation of immune response by B7 family molecules in tumor microenvironments. Immunol. Invest. 35: 395-418. (Pubitemid 44266781)
28. Duraiswamy, J., C. C. Ibegbu, D. Masopust, J. D. Miller, K. Araki, G. H. Doho, P. Tata, S. Gupta, M. J. Zilliox, H. I. Nakaya, et al. 2011. Phenotype, function, and gene expression profiles of programmed death-1(hi) CD8 T cells in healthy human adults. J. Immunol. 186: 4200-4212.
29. van der Velden, W. J., A. H. Herbers, T. Feuth, N. P. Schaap, J. P. Donnelly, and N. M. Blijlevens. 2010. Intestinal damage determines the inflammatory response and early complications in patients receiving conditioning for a stem cell transplantation. PLoS ONE 5: e15156.
30. Grogan, B. M., L. Tabellini, B. Storer, T. E. Bumgarner, C. C. Astigarraga, M. E. Flowers, S. J. Lee, P. J. Martin, E. H. Warren, and J. A. Hansen. 2011. Activation and expansion of CD8(+) T effector cells in patients with chronic graft-versus-host disease. Biol. Blood Marrow Transplant. 17: 1121-1132.
31. Chidrawar, S., N. Khan, W. Wei, A. McLarnon, N. Smith, L. Nayak, and P. Moss. 2009. Cytomegalovirus-seropositivity has a profound influence on the magnitude of major lymphoid subsets within healthy individuals. Clin. Exp. Immunol. 155: 423-432.
32. Peric, Z., X. Cahu, P. Chevallier, E. Brissot, F. Malard, T. Guillaume, J. Delaunay, S. Ayari, V. Dubruille, S. Le Gouill, et al. 2011. Features of Epstein-Barr virus (EBV) reactivation after reduced intensity conditioning allogeneic hematopoietic stem cell transplantation. Leukemia 25: 932-938.
33. Serriari, N. E., F. Gondois-Rey, Y. Guillaume, E. B. Remmerswaal, S. Pastor, N. Messal, A. Truneh, I. Hirsch, R. A. van Lier, and D. Olive. 2010. B and T lymphocyte attenuator is highly expressed on CMV-specific T cells during infection and regulates their function. J. Immunol. 185: 3140-3148.
34. Costello, R. T., F. Mallet, B. Barbarat, J. M. Schiano De Colella, D. Sainty, R. W. Sweet, A. Truneh, and D. Olive. 2003. Stimulation of non-Hodgkin's lymphoma via HVEM: an alternate and safe way to increase Fas-induced apoptosis and improve tumor immunogenicity. Leukemia 17: 2500-2507. (Pubitemid 38072590)
35. Pasero, C., B. Barbarat, S. Just-Landi, A. Bernard, T. Aurran-Schleinitz, J. Rey, E. Eldering, A. Truneh, R. T. Costello, and D. Olive. 2009. A role for HVEM, but not lymphotoxin-beta receptor, in LIGHT-induced tumor cell death and chemokine production. Eur. J. Immunol. 39: 2502-2514.
36. Cheung, T. C., M. W. Steinberg, L. M. Oborne, M. G. Macauley, S. Fukuyama, H. Sanjo, C. D'Souza, P. S. Norris, K. Pfeffer, K. M. Murphy, et al. 2009. Unconventional ligand activation of herpesvirus entry mediator signals cell survival. Proc. Natl. Acad. Sci. USA 106: 6244-6249.
37. Murphy, T. L., and K. M. Murphy. 2010. Slow down and survive: enigmatic immunoregulation by BTLA and HVEM. Annu. Rev. Immunol. 28: 389-411.
38. Levenga, H., N. Schaap, F. Maas, B. Esendam, H. Fredrix, A. Greupink-Draaisma, T. de Witte, H. Dolstra, and R. Raymakers. 2010. Partial T celldepleted allogeneic stem cell transplantation following reduced-intensity conditioning creates a platform for immunotherapy with donor lymphocyte infusion and recipient dendritic cell vaccination in multiple myeloma. Biol. Blood Marrow Transplant. 16: 320-332.
39. Brahmer, J. R., C. G. Drake, I. Wollner, J. D. Powderly, J. Picus, W. H. Sharfman, E. Stankevich, A. Pons, T. M. Salay, T. L. McMiller, et al. 2010. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J. Clin. Oncol. 28: 3167-3175.
40. Albring, J. C., M. M. Sandau, A. S. Rapaport, B. T. Edelson, A. Satpathy, M. Mashayekhi, S. K. Lathrop, C. S. Hsieh, M. Stelljes, M. Colonna, et al. 2010. Targeting of B and T lymphocyte associated (BTLA) prevents graft-versus-host disease without global immunosuppression. J. Exp. Med. 207: 2551-2559.
41. Sakoda, Y., J. J. Park, Y. Zhao, A. Kuramasu, D. Geng, Y. Liu, E. Davila, and K. Tamada. 2011. Dichotomous regulation of GVHD through bidirectional functions of the BTLA-HVEM pathway. Blood 117: 2506-2514.
42. Quigley, M., F. Pereyra, B. Nilsson, F. Porichis, C. Fonseca, Q. Eichbaum, B. Julg, J. L. Jesneck, K. Brosnahan, S. Imam, et al. 2010. Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat. Med. 16: 1147-1151.
43. Chemnitz, J. M., R. V. Parry, K. E. Nichols, C. H. June, and J. L. Riley. 2004. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J. Immunol. 173: 945-954. (Pubitemid 38924267)
44. Gavrieli, M., N. Watanabe, S. K. Loftin, T. L. Murphy, and K. M. Murphy. 2003. Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of B and T lymphocyte attenuator required for association with protein tyrosine phosphatases SHP-1 and SHP-2. Biochem. Biophys. Res. Commun. 312: 1236-1243. (Pubitemid 37490949)
45. Gavrieli, M., and K. M. Murphy. 2006. Association of Grb-2 and PI3K p85 with phosphotyrosile peptides derived from BTLA. Biochem. Biophys. Res. Commun. 345: 1440-1445. (Pubitemid 43817892)