Tumor-derived CD4+CD25+ regulatory T cell suppression of dendritic cell function involves TGF-β and IL-10

Cancer Immunology, Immunotherapy

Volumn 56, Issue 1, 2007, Pages 48-59

  Larmonier, Nicolas ^a   Marron, Marilyn ^a   Zeng, Yi ^a   Cantrell, Jessica ^a   Romanoski, Angela ^a   Sepassi, Marjan ^a   Thompson, Sylvia ^a   Chen, Xinchun ^a   Andreansky, Samita ^a   Katsanis, Emmanuel ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Dendritic cells; Regulatory T cells; Tolerance; Tumor immunity

Indexed keywords

B7 ANTIGEN; BCR ABL PROTEIN; CD40 ANTIGEN; CD86 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; RANTES; STAT3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BONE MARROW; CD4+ CD25+ T LYMPHOCYTE; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; FEMALE; LEUKEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD80; ANTIGENS, CD86; BONE MARROW CELLS; DENDRITIC CELLS; FEMALE; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; FUSION PROTEINS, BCR-ABL; IMMUNOSUPPRESSION; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LEUKEMIA; LYMPHOCYTE ACTIVATION; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-KAPPA B; PHOSPHORYLATION; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 33751371759     PISSN: 03407004     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00262-006-0160-8     Document Type: Article

References (51)

1. Sakaguchi S (2005) Naturally arising Foxp3-expressing CD25(+)CD4(+) regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 6:345-352
2. Shevach EM (2002) CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2:389-400
3. Asano M, Toda M, Sakaguchi N et al (1996) Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med 184:387-396
4. Sakaguchi S, Sakaguchi N, Asano M et al (1995) Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155:1151-1164
5. Belkaid Y, Piccirillo CA, Mendez S et al (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420:502-507
6. Cobbold SP, Nolan KF, Graca L et al (2003) Regulatory T cells and dendritic cells in transplantation tolerance: molecular markers and mechanisms. Immunol Rev 196:109-124
7. Shimizu J, Yamazaki S, Sakaguchi S (1999) Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J Immunol 163:5211-5218
8. Sakaguchi S (2000) Regulatory T cells: key controllers of immunologic self-tolerance. Cell 101:455-458
9. Antony PA, Piccirillo CA, Akpinarli A et al (2005) CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J Immunol 174:2591-2601
10. Woo EY, Yeh H, Chu CS et al (2002) Cutting edge: regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J Immunol 168:4272-4276
11. Liyanage UK, Moore TT, Joo HG et al (2002) Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 169:2756-2761
12. Ormandy LA, Hillemann T, Wedemeyer H et al (2005) Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma. Cancer Res 65:2457-2464
13. Liu JY, Zhang XS, Ding Y et al (2005) The changes of CD4+CD25+/CD4+ proportion in spleen of tumor-bearing BALB/c mice. J Transl Med 3:5
14. Ghiringhelli F, Larmonier N, Schmitt E et al (2004) CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 34:336-344
15. Sutmuller RP, van Duivenvoorde LM, van Elsas A et al (2001) Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 194:823-832
16. Yu P, Lee Y, Liu W et al (2005) Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J Exp Med 201:779-791
17. Prasad SJ, Farrand KJ, Matthews SA et al (2005) Dendritic cells loaded with stressed tumor cells elicit long-lasting protective tumor immunity in mice depleted of CD4+CD25+ regulatory T cells. J Immunol 174:90-98
18. Fontenot JD, Rudensky AY (2005) A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 6:331-337
19. Fontenot JD, Gavin MA, Rudensky AY (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4:330-336
20. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057-1061
21. Fontenot JD, Rasmussen JP, Williams LM et al (2005) Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22:329-341
22. Nakamura K, Kitani A, Fuss I et al (2004) TGF-beta 1 plays an important role in the mechanism of CD4+CD25+ regulatory T cell activity in both humans and mice. J Immunol 172:834-842
23. Nakamura K, Kitani A, Strober W (2001) Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med 194:629-644
24. Piccirillo CA, Letterio JJ, Thornton AM 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
25. Misra N, Bayry J, Lacroix-Desmazes S et al (2004) Cutting edge: human CD4+CD25+ T cells restrain the maturation and antigen-presenting function of dendritic cells. J Immunol 172:4676-4680
26. Sato K, Tateishi S, Kubo K et al (2005) Downregulation of IL-12 and a novel negative feedback system mediated by CD25(+)CD4(+) T cells. Biochem Biophys Res Commun 330:226-232
27. Cederbom L, Hall H, Ivars F (2000) CD4+CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol 30:1538-1543
28. Serra P, Amrani A, Yamanouchi J et al (2003) CD40 ligation releases immature dendritic cells from the control of regulatory CD4+CD25+ T cells. Immunity 19:877-889
29. Chen W, Qin H, Reese VA et al (1998) CTLs specific for bcr-abl joining region segment peptides fail to lyse leukemia cells expressing p210 bcr-abl protein. J Immunother 21:257-268
30. McLaughlin J, Chianese E, Witte ON (1987) In vitro transformation of immature hematopoietic cells by the P210 BCR/ ABL oncogene product of the Philadelphia chromosome. Proc Natl Acad Sci USA 84:6558-6562
31. He L, Feng H, Raymond A et al (2001) Dendritic-cell-peptide immunization provides immunoprotection against bcr-abl-positive leukemia in mice. Cancer Immunol Immunother 50:31-40
32. Feng H, Zeng Y, Whitesell L et al (2001) Stressed apoptotic tumor cells express heat shock proteins and elicit tumor-specific immunity. Blood 97:3505-3512
33. Nishikawa H, Jager E, Ritter G et al (2005) CD4+ CD25+ regulatory T cells control the induction of antigen-specific CD4+ helper T cell responses in cancer patients. Blood 106:1008-1011
34. Somasundaram R, Jacob L, Swoboda R et al (2002) Inhibition of cytolytic T lymphocyte proliferation by autologous CD4+/ CD25+ regulatory T cells in a colorectal carcinoma patient is mediated by transforming growth factor-beta. Cancer Res 62:5267-5272
35. Onishi H, Kuroki H, Matsumoto K et al (2004) Monocyte-derived dendritic cells that capture dead tumor cells secrete IL-12 and TNF-alpha through IL-12/TNF-alpha/NF-kappaB autocrine loop. Cancer Immunol Immunother 53:1093-1100
36. Sakaguchi S (2004) Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22:531-562
37. Thornton AM, Shevach EM (1998) CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 188:287-296
38. Chen W, Wahl SM (2003) TGF-beta: the missing link in CD4+CD25+ regulatory T cell-mediated immunosuppression. Cytokine Growth Factor Rev 14:85-89
39. Moore KW, de Waal Malefyt R, Coffman RL et al (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683-765
40. Williams LM, Ricchetti G, Sarma U et al (2004) Interleukin-10 suppression of myeloid cell activation - a continuing puzzle. Immunology 113:281-292
41. Hoentjen F, Sartor RB, Ozaki M et al (2005) STAT3 regulates NF-kappaB recruitment to the IL-12p40 promoter in dendritic cells. Blood 105:689-696
42. Taams LS, van Amelsfort JM, Tiemessen MM et al (2005) Modulation of monocyte/macrophage function by human CD4+CD25+ regulatory T cells. Hum Immunol 66:222-230
43. Almand B, Clark JI, Nikitina E et al (2001) Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 166:678-689
44. Almand B, Resser JR, Lindman B et al (2000) Clinical significance of defective dendritic cell differentiation in cancer. Clin Cancer Res 6:1755-1766
45. Chaux P, Favre N, Martin M et al (1997) Tumor-infiltrating dendritic cells are defective in their antigen-presenting function and inducible B7 expression in rats. Int J Cancer 72:619-624
46. Gabrilovich D (2004) Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol 4:941-952
47. Monti P, Leone BE, Zerbi A et al (2004) Tumor-derived MUC1 mucins interact with differentiating monocytes and induce IL-10 high IL-12 low regulatory dendritic cell. J Immunol 172:7341-7349
48. Steinbrink K, Jonuleit H, Muller G et al (1999) Interleukin-10-treated human dendritic cells induce a melanoma-antigen-specific anergy in CD8(+) T cells resulting in a failure to lyse tumor cells. Blood 93:1634-1642
49. Kuwana M (2002) Induction of anergic and regulatory T cells by plasmacytoid dendritic cells and other dendritic cell subsets. Hum Immunol 63:1156-1163
50. Verginis P, Li HS, Carayanniotis G (2005) Tolerogenic semimature dendritic cells suppress experimental autoimmune thyroiditis by activation of thyroglobulin-specific CD4+CD25+ T Cells. J Immunol 174:7433-7439
51. Mahnke K, Qian Y, Knop J et al (2003) Induction of CD4+/CD25+ regulatory T cells by targeting of antigens to immature dendritic cells. Blood 101:4862-4869