Tumour cell generation of inducible regulatory T-cells in multiple myeloma is contact-dependent and antigen-presenting cell-independent

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Feyler, Sylvia ^a,b   Scott, Gina B ^a   Parrish, Christopher ^a   Jarmin, Sarah ^a   Evans, Paul ^c   Short, Mike ^c   McKinley, Katherine ^c   Selby, Peter J ^a   Cook, Gordon ^a,c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b CALDERDALE AND HUDDERSFIELD NHS FOUNDATION TRUST   (United Kingdom)

^c LEEDS TEACHING HOSPITALS NHS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR ALPHA; L SELECTIN; MONOCLONAL ANTIBODY; PROGRAMMED DEATH 1 RECEPTOR; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; GAMMA INTERFERON; ICOS PROTEIN, HUMAN; ICOSLG PROTEIN, HUMAN; INDUCIBLE T CELL COSTIMULATOR; INDUCIBLE T CELL COSTIMULATOR LIGAND;

ANTIGEN PRESENTING CELL; ARTICLE; CANCER CELL CULTURE; CD4+ CD25+ T LYMPHOCYTE; CELL CONTACT; CELL DIFFERENTIATION; CELL EXPANSION; COCULTURE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE EXPANSION; MULTIPLE MYELOMA; MYELOMA CELL; PHENOTYPE; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; BIOSYNTHESIS; CELL COMMUNICATION; CYTOLOGY; IMMUNOLOGY; METABOLISM; PATHOLOGY; PLASMA CELL; TUMOR CELL LINE;

ANTIGEN-PRESENTING CELLS; CELL COMMUNICATION; CELL LINE, TUMOR; HUMANS; INDUCIBLE T-CELL CO-STIMULATOR LIGAND; INDUCIBLE T-CELL CO-STIMULATOR PROTEIN; INTERFERON-GAMMA; MULTIPLE MYELOMA; PHENOTYPE; PLASMA CELLS; T-LYMPHOCYTES, REGULATORY;

EID: 84861538114     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035981     Document Type: Article

References (56)

1. Lizee G, Radvanyi LG, Overwijk WW, Hwu P, (2006) Improving antitumor immune responses by circumventing immunoregulatory cells and mechanisms. Clin Cancer Res 12: 4794-4803.
2. Knutson KL, Disis ML, Salazar LG, (2007) CD4 regulatory T cells in human cancer pathogenesis. Cancer Immunol Immunother 56: 271-285.
3. Filaci G, Fenoglio D, Fravega M, Ansaldo G, Borgonovo G, et al. (2007) CD8+CD28 T Regulatory Lymphocytes Inhibiting T Cell Proliferative and Cytotoxic Functions Infiltrate Human Cancers. J Immunol 179: 4323-4334.
4. Chen W, Jin W, Hardegen N, Lei KJ, Li L, et al. (2003) Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198: 1875-1886.
5. Cobbold SP, Graca L, Lin CY, Adams E, Waldmann H, (2003) Regulatory T cells in the induction and maintenance of peripheral transplantation tolerance. Transpl Int 16: 66-75.
6. Bates GJ, Fox SB, Han C, Leek RD, Garcia JF, et al. (2006) Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol 24: 5373-5380.
7. Miller AM, Lundberg K, Ozenci V, Banham AH, Hellstrom M, et al. (2006) CD4+CD25high T cells are enriched in the tumor and peripheral blood of prostate cancer patients. J Immunol 177: 7398-7405.
8. Gjerdrum LM, Woetmann A, Odum N, Burton CM, Rossen K, et al. (2007) FOXP3+ regulatory T cells in cutaneous T-cell lymphomas: association with disease stage and survival. Leukemia.
9. Prabhala RH, Neri P, Bae JE, Tassone P, Shammas MA, et al. (2006) Dysfunctional T regulatory cells in multiple myeloma. Blood 107: 301-304.
10. Beyer M, Kochanek M, Giese T, Endl E, Weihrauch MR, et al. (2006) In vivo peripheral expansion of naive CD4+CD25high FoxP3+ regulatory T cells in patients with multiple myeloma. Blood 107: 3940-3949.
11. Harrison SJ, Cook G, (2005) Immunotherapy in multiple myeloma-possibility or probability? Br J Haematol 130: 344-362.
12. Cook G, Campbell JD, Carr CE, Boyd KS, Franklin IM, (1999) Transforming growth factor beta from multiple myeloma cells inhibits proliferation and IL-2 responsiveness in T lymphocytes. J Leukoc Biol 66: 981-988.
13. Kim R, Emi M, Tanabe K, (2006) Cancer immunosuppression and autoimmune disease: beyond immunosuppressive networks for tumour immunity. Immunology 119: 254-264.
14. Feyler S, von Lilienfeld-Toal M, Jarmin S, Marles L, Rawstron A, et al. (2009) CD4(+)CD25(+)FoxP3(+) regulatory T cells are increased whilst CD3(+)CD4(-)CD8(-)alphabetaTCR(+) Double Negative T cells are decreased in the peripheral blood of patients with multiple myeloma which correlates with disease burden. Br J Haematol 144: 686-695.
15. Pellat-Deceunynk C, Amiot M, Bataille R, Van Riet I, Van Camp B, et al. (1995) Human myeloma cell lines as a tool for studying the biology of multiple myeloma: a reappraisal 18 years after. Blood 86: 4001-4002.
16. Hamilton MS, Barker HF, Ball J, Drew M, Abbot SD, et al. (1991) Normal and neoplastic human plasma cells express bcl-2 antigen. Leukemia: official journal of the Leukemia Society of America, Leukemia Research Fund, UK 5: 768-771.
17. van Riet I, de Greef C, del Favero H, Demanet C, Van Camp B, (1994) Production of fibronectin and adherence to fibronectin by human myeloma cell lines. British journal of haematology 87: 258-265.
18. Ohtsuki T, Yawata Y, Namba M, (1989) [Establishment and characterization of five human myeloma cell lines]. Human cell: official journal of Human Cell Research Society 2: 297-303.
19. Namba M, Ohtsuki T, Mori M, Togawa A, Wada H, et al. (1989) Establishment of five human myeloma cell lines. In vitro cellular & developmental biology: journal of the Tissue Culture Association 25: 723-729.
20. van Dongen JJ, Langerak AW, Bruggemann M, Evans PA, Hummel M, et al. (2003) Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia 17: 2257-2317.
21. Kmieciak M, Gowda M, Graham L, Godder K, Bear HD, et al. (2009) Human T cells express CD25 and Foxp3 upon activation and exhibit effector/memory phenotypes without any regulatory/suppressor function. J Transl Med 7: 89.
22. Hauben E, Roncarolo MG, (2005) Human CD4+ regulatory T cells and activation-induced tolerance. Microbes Infect 7: 1023-1032.
23. Lutsiak ME, Tagaya Y, Adams AJ, Schlom J, Sabzevari H, (2008) Tumor-induced impairment of TCR signaling results in compromised functionality of tumor-infiltrating regulatory T cells. J Immunol 180: 5871-5881.
24. Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, et al. (2009) IL-17 producing human peripheral regulatory T cells retain suppressive function. Blood.
25. Koenen HJ, Smeets RL, Vink PM, van Rijssen E, Boots AM, et al. (2008) Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 112: 2340-2352.
26. Banerjee DK, Dhodapkar MV, Matayeva E, Steinman RM, Dhodapkar KM, (2006) Expansion of FOXP3high regulatory T cells by human dendritic cells (DCs) in vitro and after injection of cytokine-matured DCs in myeloma patients. Blood 108: 2655-2661.
27. Levings MK, Gregori S, Tresoldi E, Cazzaniga S, Bonini C, et al. (2005) Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood 105: 1162-1169.
28. Ghiringhelli F, Puig PE, Roux S, Parcellier A, Schmitt E, et al. (2005) Tumor cells convert immature myeloid dendritic cells into TGF-beta-secreting cells inducing CD4+CD25+ regulatory T cell proliferation. J Exp Med 202: 919-929.
29. Chatenoud L, Bach JF, (2006) Adaptive human regulatory T cells: myth or reality? J Clin Invest 116: 2325-2327.
30. Mercer F, Unutmaz D, (2009) The biology of FoxP3: a key player in immune suppression during infections, autoimmune diseases and cancer. Adv Exp Med Biol 665: 47-59.
31. Herber DL, Nagaraj S, Djeu JY, Gabrilovich DI, (2007) Mechanism and therapeutic reversal of immune suppression in cancer. Cancer Res 67: 5067-5069.
32. Gabrilovich DI, (2007) Molecular mechanisms and therapeutic reversal of immune suppression in cancer. Curr Cancer Drug Targets 7: 1.
33. Whiteside TL, (2006) Immune suppression in cancer: effects on immune cells, mechanisms and future therapeutic intervention. Semin Cancer Biol 16: 3-15.
34. Wang RF, (2006) Immune suppression by tumor-specific CD4+ regulatory T-cells in cancer. Semin Cancer Biol 16: 73-79.
35. Fiore F, Nuschak B, Peola S, Mariani S, Muraro M, et al. (2005) Exposure to myeloma cell lysates affects the immune competence of dendritic cells and favors the induction of Tr1-like regulatory T cells. Eur J Immunol 35: 1155-1163.
36. Campbell JD, Cook G, Robertson SE, Fraser A, Boyd KS, et al. (2001) Suppression of IL-2-induced T cell proliferation and phosphorylation of STAT3 and STAT5 by tumor-derived TGF beta is reversed by IL-15. J Immunol 167: 553-561.
37. Daniel V, Sadeghi M, Wang H, Opelz G, (2011) CD4+CD25+Foxp3+IFN-gamma+ human induced T regulatory cells are induced by interferon-gamma and suppress alloresponses nonspecifically. Human immunology 72: 699-707.
38. Feng T, Cao AT, Weaver CT, Elson CO, Cong Y, (2011) Interleukin-12 converts Foxp3+ regulatory T cells to interferon-gamma-producing Foxp3+ T cells that inhibit colitis. Gastroenterology 140: 2031-2043.
39. Bruno L, Mazzarella L, Hoogenkamp M, Hertweck A, Cobb BS, et al. (2009) Runx proteins regulate Foxp3 expression. The Journal of experimental medicine 206: 2329-2337.
40. Hadjur S, Bruno L, Hertweck A, Cobb BS, Taylor B, et al. (2009) IL4 blockade of inducible regulatory T cell differentiation: the role of Th2 cells, Gata3 and PU.1. Immunology letters 122: 37-43.
41. Maruyama T, Konkel JE, Zamarron BF, Chen W, (2011) The molecular mechanisms of Foxp3 gene regulation. Seminars in immunology 23: 418-423.
42. Kitani A, Xu L, (2008) Regulatory T cells and the induction of IL-17. Mucosal Immunol 1 (Suppl 1): S43-46.
43. Strauss L, Bergmann C, Szczepanski MJ, Lang S, Kirkwood JM, et al. (2008) Expression of ICOS on human melanoma-infiltrating CD4+CD25highFoxp3+ T regulatory cells: implications and impact on tumor-mediated immune suppression. J Immunol 180: 2967-2980.
44. Ito T, Hanabuchi S, Wang YH, Park WR, Arima K, et al. (2008) Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 28: 870-880.
45. Riley JL, Blair PJ, Musser JT, Abe R, Tezuka K, et al. (2001) ICOS costimulation requires IL-2 and can be prevented by CTLA-4 engagement. J Immunol 166: 4943-4948.
46. Coquerelle C, Oldenhove G, Acolty V, Denoeud J, Vansanten G, et al. (2009) Anti-CTLA-4 treatment induces IL-10-producing ICOS+ regulatory T cells displaying IDO-dependent anti-inflammatory properties in a mouse model of colitis. Gut 58: 1363-1373.
47. de Jong YP, Rietdijk ST, Faubion WA, Abadia-Molina AC, Clarke K, et al. (2004) Blocking inducible co-stimulator in the absence of CD28 impairs Th1 and CD25+ regulatory T cells in murine colitis. Int Immunol 16: 205-213.
48. Zheng SG, Wang J, Wang P, Gray JD, Horwitz DA, (2007) IL-2 is essential for TGF-beta to convert naive CD4+CD25- cells to CD25+Foxp3+ regulatory T cells and for expansion of these cells. J Immunol 178: 2018-2027.
49. Zheng SG, Wang JH, Stohl W, Kim KS, Gray JD, et al. (2006) TGF-beta requires CTLA-4 early after T cell activation to induce FoxP3 and generate adaptive CD4+CD25+ regulatory cells. J Immunol 176: 3321-3329.
50. Oberle N, Eberhardt N, Falk CS, Krammer PH, Suri-Payer E, (2007) Rapid suppression of cytokine transcription in human CD4+CD25 T cells by CD4+Foxp3+ regulatory T cells: independence of IL-2 consumption, TGF-beta, and various inhibitors of TCR signaling. J Immunol 179: 3578-3587.
51. Kullberg MC, Hay V, Cheever AW, Mamura M, Sher A, et al. (2005) TGF-beta1 production by CD4+ CD25+ regulatory T cells is not essential for suppression of intestinal inflammation. Eur J Immunol 35: 2886-2895.
52. Piccirillo CA, Letterio JJ, Thornton AM, McHugh RS, Mamura M, et al. (2002) CD4(+)CD25(+) regulatory T cells can mediate suppressor function in the absence of transforming growth factor beta1 production and responsiveness. J Exp Med 196: 237-246.
53. Ayyoub M, Deknuydt F, Raimbaud I, Dousset C, Leveque L, et al. (2009) Human memory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor RORgamma t. Proceedings of the National Academy of Sciences of the United States of America 106: 8635-8640.
54. Pan F, Fan H, Lu L, Liu Z, Jiang S, (2011) The yin and yang of signaling in Tregs and TH17 cells. Science signaling 4: mr4.
55. Sharma MD, Hou DY, Liu Y, Koni PA, Metz R, et al. (2009) Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes. Blood 113: 6102-6111.
56. Hoechst B, Gamrekelashvili J, Manns MP, Greten TF, Korangy F, (2011) Plasticity of human Th17 cells and iTregs is orchestrated by different subsets of myeloid cells. Blood 117: 6532-6541.