Human regulatory T cells do not suppress the antitumor immunity in the bone marrow: A role for bone marrow stromal cells in neutralizing regulatory T cells

Clinical Cancer Research

Volumn 19, Issue 6, 2013, Pages 1467-1475

  Guichelaar, Teun ^a,c   Emmelot, Maarten E ^a   Rozemuller, Henk ^a   Martini, Bianka ^a   Groen, Richard W J ^a   Storm, Gert ^b   Lokhorst, Henk M ^a   Martens, Anton C ^a   Mutis, Tuna ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c Netherlands Institute for Health and the Environment   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW; BONE MARROW CELL; BONE MARROW STROMAL CELL; CANCER GROWTH; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENGRAFTMENT; GRAFT VERSUS HOST REACTION; GRAFT VERSUS LEUKEMIA EFFECT; HUMAN; HUMAN CELL; IMMUNOGENICITY; IN VITRO STUDY; LYMPHOCYTE HOMING; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TUMOR IMMUNITY;

ANIMALS; BONE MARROW CELLS; FEMALE; GRAFT VS HOST DISEASE; GRAFT VS TUMOR EFFECT; HUMANS; INTERLEUKIN-17; INTERLEUKIN-6; LEUKOCYTES, MONONUCLEAR; MICE; MULTIPLE MYELOMA; STROMAL CELLS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HOMOLOGOUS;

EID: 84875160155     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-2177     Document Type: Article

References (40)

1. Mutis T, van Rijn RS, Simonetti ER, arts-Riemens T, Emmelot ME, van BL, et al. Human regulatory T cells control xenogeneic graft-versushost disease induced by autologous T cells in RAG2-/-gammac-/- immunodeficient mice. Clin Cancer Res 2006;12:5520-5.
2. Soiffer R. Immune modulation and chronic graft-versus-host disease. Bone Marrow Transplant 2008;42 Suppl 1:S66-69.
3. Lokhorst HM, Schattenberg A, Cornelissen JJ, Thomas LL, Verdonck LF. Donor leukocyte infusions are effective in relapsed multiple myeloma after allogeneic bone marrow transplantation. Blood 1997;90:4206-11.
4. Lokhorst HM, Wu K, Verdonck LF, Laterveer LL, van de Donk NW, van Oers MH, et al. The occurrence of graft-versus-host disease is the major predictive factor for response to donor lymphocyte infusions in multiple myeloma. Blood 2004;103:4362-4.
5. Tricot G, Vesole DH, Jagannath S, Hilton J, Munshi N, Barlogie B. Graft-versus-MM effect: proof of principle. Blood 1996;87:1196-8.
6. Brunstein CG, Miller JS, Cao Q,McKenna DH, Hippen KL, Curtsinger J, et al. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: safety profile and detection kinetics. Blood 2011;117:1061-70.
7. Edinger M, Hoffmann P, Ermann J, Drago K, Fathman CG, Strober S, et al. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med 2003;9:1144-50.
8. Trenado A, Charlotte F, Fisson S, Yagello M, Klatzmann D, Salomon BL, et al. Recipient-type specific CD4+CD25+ regulatory T cells favor immune reconstitution and control graft-versus-host disease while maintaining graft-versus-leukemia. J Clin Invest 2003;112:1688-96.
9. Curiel TJ. Tregs and rethinking cancer immunotherapy. J Clin Invest 2007;117:1167-74.
10. Baecher-Allan C, Anderson DE. Immune regulation in tumor-bearing hosts. Curr Opin Immunol 2006;18:214-9.
11. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10: 942-9.
12. Heier I, Hofgaard PO, Brandtzaeg P, Jahnsen FL, Karlsson M. Depletion of CD4+CD25+regulatory T cells inhibits local tumour growth in a mouse model of B cell lymphoma. Clin Exp Immunol 2008;152:381-7.
13. Jacob JB, Kong YC, Nalbantoglu I, Snower DP, Wei WZ. Tumor regression following DNA vaccination and regulatory T cell depletion in neu transgenic mice leads to an increased risk for autoimmunity. J Immunol 2009;182:5873-81.
14. Maury S, Lemoine FM, Hicheri Y, Rosenzwajg M, Badoual C, Cherai M, et al. CD4+CD25+ regulatory T cell depletion improves the graftversus-tumor effect of donor lymphocytes after allogeneic hematopoietic stem cell transplantation. Sci Transl Med 2010;2:41ra52.
15. Wang HY, Lee DA, Peng G, Guo Z, Li Y, Kiniwa Y, et al. Tumor-specific human CD4+ regulatory T cells and their ligands: implications for immunotherapy. Immunity 2004;20:107-18.
16. Rozemuller H, van der Spek E, Bogers-Boer LH, Zwart MC, Verweij V, Emmelot M, et al. A bioluminescence imaging based in vivo model for preclinical testing of novel cellular immunotherapy strategies to improve the graft-versus-MM effect. Haematologica 2008;93: 1049-57.
17. van Rijn RS, Simonetti ER, Hagenbeek A, Hogenes MC, de Weger RA, Canninga-van Dijk MR, et al. A new xenograft model for graft-versushost disease by intravenous transfer of human peripheral blood mononuclear cells in RAG2-/- gammac-/- double-mutant mice. Blood 2003;102:2522-31.
18. Bluestone JA. Regulatory T-cell therapy: is it ready for the clinic? Nat Rev Immunol 2005;5:343-9.
19. Yamagiwa S, Gray JD, Hashimoto S, Horwitz DA. A role for TGF-beta in the generation and expansion of CD4+CD25+ regulatory T cells from human peripheral blood. J Immunol 2001;166:7282-9.
20. Vercoulen Y, Guichelaar T, Meerding J, Emmelot M, Pingen M, Storm G, et al. Application of cultured human regulatory T cells requires preclinical in vivo evaluation. J Allergy Clin Immunol 2012;129:852-5.
21. Koenen HJ, Smeets RL, Vink PM, van Rijssen E, Boots AM, Joosten I. Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 2008;112:2340-52.
22. Aarts-Riemens T, Emmelot ME, Verdonck LF, Mutis T. Forced overexpression of either of the two common human Foxp3 isoforms can induce regulatory T cells from CD4(+)CD25(-) cells. Eur J Immunol 2008;38:1381-90.
23. Spaapen RM, Groen RW, van den OK, Guichelaar T, van EM, arts-Riemens T, et al. Eradication of medullary multiple myeloma by CD4+cytotoxic human T lymphocytes directed at a single minor histocompatibility antigen. Clin Cancer Res 2010;16:5481-8.
24. Baecher-Allan C, Viglietta V, Hafler DA. Inhibition of human CD4(+) CD25(+high) regulatory T cell function. J Immunol 2002;169:6210-7.
25. Derksen PW, Keehnen RM, Evers LM, van Oers MH, Spaargaren M, Pals ST. Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood 2002;99:1405-10.
26. Nishikawa H, Tsuji T, Jager E, Briones G, Ritter G, Old LJ, et al. Induction of regulatory T cell-resistant helper CD4+T cells by bacterial vector. Blood 2008;111:1404-12.
27. O'Sullivan BJ, ThomasHE, Pai S, Santamaria P, Iwakura Y, Steptoe RJ, et al. IL-1 beta breaks tolerance through expansion of CD25+ effector T cells. J Immunol 2006;176:7278-87.
28. Afzali B, Mitchell P, Lechler RI, John S, Lombardi G. Translational minireview series on Th17 cells: induction of interleukin-17 production by regulatory T cells. Clin Exp Immunol 2010;159:120-30.
29. Xu L, Kitani A, Fuss I, Strober W. Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol 2007;178:6725-9.
30. Hombach AA, Kofler D, Rappl G, Abken H. Redirecting human CD4+CD25+ regulatory T cells from the peripheral blood with predefined target specificity. Gene Ther 2009;16:1088-96.
31. Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 2007;37:129-38.
32. Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 2007;110:2983-90.
33. Sundrud MS, NolanMA. Synergistic and combinatorial control of T cell activation and differentiation by transcription factors. Curr Opin Immunol 2010;22:286-92.
34. Bettelli E, Dastrange M, Oukka M. Foxp3 interacts with nuclear factor of activated T cells and NF-kappa B to repress cytokine gene expression and effector functions of T helper cells. Proc Natl Acad Sci U S A 2005;102:5138-43.
35. Kerdiles YM, Stone EL, Beisner DL, McGargill MA, Ch'en IL, Stockmann C, et al. Foxo transcription factors control regulatory T cell development and function. Immunity 2010;33:890-904.
36. Hideshima T, Mitsiades C, Tonon G, Richardson PG, Anderson KC. Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets. Nat Rev Cancer 2007;7:585-98.
37. Prabhala RH, Pelluru D, Fulciniti M, Prabhala HK, Nanjappa P, Song W, et al. Elevated IL-17 produced by TH17 cells promotes MM cell growth and inhibits immune function in multiple myeloma. Blood 2010; 115:5385-92.
38. Minnema MC, van de Donk NW, Zweegman S, Hegenbart U, Schonland S, Raymakers R, et al. Extramedullary relapses after allogeneic non-myeloablative stem cell transplantation in multiple myeloma patients do not negatively affect treatment outcome. Bone Marrow Transplant 2008;41:779-84.
39. Niu Q, Cai B, Huang ZC, Shi YY,Wang LL. Disturbed Th17/Treg balance in patients with rheumatoid arthritis. Rheumatol Int 2012;32:2731-6.
40. Bertin-Maghit S, Pang D, O'Sullivan B, Best S, Duggan E, Paul S, et al. Interleukin-1beta produced in response to islet autoantigen presentation differentiates T-helper 17 cells at the expense of regulatory Tcells: implications for the timing of tolerizing immunotherapy. Diabetes 2011;60:248-57.