Regulatory T cell subsets in human cancer: Are they regulating for or against tumor progression?

Cancer Immunology, Immunotherapy

Volumn 63, Issue 1, 2014, Pages 67-72

  Whiteside, Theresa L ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Adenosine; CITIM 2013; Immune regulation; Inducible Treg; PGE2; Tumor microenvironment

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE TRIPHOSPHATE; CD39 ANTIGEN; INTERLEUKIN 10; PROSTAGLANDIN E2; TRANSFORMING GROWTH FACTOR BETA; TUMOR ANTIGEN;

CANCER IMMUNOTHERAPY; CANCER PATIENT; CHEMORADIOTHERAPY; HUMAN; INFLAMMATORY INFILTRATE; LUNG NON SMALL CELL CANCER; MOLECULAR INTERACTION; NEOPLASM; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE SUBPOPULATION; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

EID: 84891876304     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1490-y     Document Type: Review

References (45)

1. Duhen T, Duhen R, Lanzavecchia A, Sallusto F, Campbell DJ (2012) Functionally distinct subsets of human FOXP3+ Treg cells that phenotypically mirror effector Th cells. Blood 119:4430-4440. doi: 10.1182/blood-2011-11-392324
2. Asano M, Toda M, Sakaguchi N, Sakaguchi S (1996) Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med 184:387-396 (Pubitemid 26324092)
3. Mougiakakos D, Choudhury A, Lladser A, Kiessling R, Johansson CC (2010) Regulatory T cells in cancer. Adv Cancer Res 107:57-117. doi: 10.1016/S0065-230X(10)07003-X
4. Jenabian MA, Seddiki N, Yatim A et al (2013) Regulatory T cells negatively affect IL-2 production of effector T cells through CD39/adenosine pathway in HIV infection. PLoS Pathog 9:e1003319. doi: 10.1371/journal.ppat. 1003319
5. Nishikawa H, Sakaguchi S (2010) Regulatory T cells in tumor immunity. Int J Cancer 127:759-767. doi: 10.1002/ijc.25429
6. highFoxp3+ T cells in the circulation of patients with squamous cell carcinoma of the head and neck. Clin Cancer Res 13:6301-6311. doi: 10.1158/1078-0432.CCR-07-1403 (Pubitemid 350075018)
7. deLeeuw RJ, Kost SE, Kakal JA, Nelson BH (2012) The prognostic value of FoxP3+ tumor-infiltrating lymphocytes in cancer: a critical review of the literature. Clin Cancer Res 18:3022-3029. doi: 10.1158/1078-0432.CCR-11-3216
8. Curiel TJ, Coukos G, Zou L et al (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10:942-949. doi: 10.1038/nm1093 (Pubitemid 39273735)
9. Salama P, Phillips M, Grieu F, Morris M, Zeps N, Joseph D, Platell C, Iacopetta B (2009) Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Ooncol 27:186-192. doi: 10.1200/JCO.2008.18.7229
10. Whiteside TL (2008) The tumor microenvironment and its role in promoting tumor growth. Oncogene 27:5904-5912. doi: 10.1038/onc.2008.271
11. Kelley TW, Parker CJ (2010) CD4 (+)CD25 (+)Foxp3 (+) regulatory T cells and hematologic malignancies. Front Biosci 2:980-992
12. Bates GJ, Fox SB, Han C, Leek RD, Garcia JF, Harris AL, Banham AH (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. doi: 10.1200/JCO.2006.05.9584 (Pubitemid 46623168)
13. Fridman WH, Galon J, Pages F, Tartour E, Sautes-Fridman C, Kroemer G (2011) Prognostic and predictive impact of intra- and peritumoral immune infiltrates. Cancer Res 71:5601-5605. doi: 10.1158/0008-5472
14. Tosolini M, Kirilovsky A, Mlecnik B et al (2011) Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, Th2, Treg, Th17) in patients with colorectal cancer. Cancer Res 71:1263-1271. doi: 10.1158/0008-5472.CAN-10-2907
15. Delgoffe GM, Woo SR, Turnis ME et al (2013) Stability and function of regulatory T cells is maintained by a neuropilin-1-semaphorin-4a axis. Nature 501:252-256. doi: 10.1038/nature12428
16. Tel J, Smits EL, Anguille S, Joshi RN, Figdor CG, de Vries IJ (2012) Human plasmacytoid dendritic cells are equipped with antigen-presenting and tumoricidal capacities. Blood 120:3936-3944. doi: 10.1182/blood-2012-06-435941
17. Borsellino G, Kleinewietfeld M, Di Mitri D et al (2007) Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 110:1225-1232. doi: 10.1182/blood-2006-12-064527 (Pubitemid 47281420)
18. Deaglio S, Dwyer KM, Gao W et al (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 204:1257-1265. doi: 10.1084/jem.20062512 (Pubitemid 46919862)
19. highFOXP3+ regulatory T cells. J Biol Chem 285:7176-7186. doi: 10.1074/jbc.M109.047423
20. Bergmann C, Strauss L, Zeidler R, Lang S, Whiteside TL (2007) Expansion and characteristics of human T regulatory type 1 cells in co-cultures simulating tumor microenvironment. Cancer Immunol Immunother 56:1429-1442. doi: 10.1007/s00262-007-0280-9 (Pubitemid 47024702)
21. Roncarolo MG, Bacchetta R, Bordignon C, Narula S, Levings MK (2001) Type 1 T regulatory cells. Immunol Rev 182:68-79 (Pubitemid 33070208)
22. Saze Z, Schuler PJ, Hong CS, Cheng D, Jackson EK, Whiteside TL (2013) Adenosine production by human B cells and B cell-mediated suppression of activated T cells. Blood 122:9-18. doi: 10.1182/blood-2013-02-482406
23. Curotto de Lafaille MA, Lafaille JJ (2009) Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 30:626-635. doi: 10.1016/j.immuni.2009.05.002
24. Campbell DJ, Koch MA (2011) Phenotypical and functional specialization of FOXP3+ regulatory T cells. Nat Rev Immunol 11:119-130. doi: 10.1038/nri2916
25. Hall BM, Verma ND, Tran GT, Hodgkinson SJ (2011) Distinct regulatory CD4+ T cell subsets; differences between naive and antigen specific T regulatory cells. Curr Opin Immunol 23:641-647. doi: 10.1016/j.coi.2011.07.012
26. Vignali DA, Collison LW, Workman CJ (2008) How regulatory T cells work. Nat Rev Immunol 8:523-532. doi: 10.1038/nri2343
27. Whiteside TL, Schuler P, Schilling B (2012) Induced and natural regulatory T cells in human cancer. Expert Opin Biol Ther 12:1383-1397. doi: 10.1517/14712598.2012.707184
28. Bergmann C, Strauss L, Wang Y, Szczepanski MJ, Lang S, Johnson JT, Whiteside TL (2008) T regulatory type 1 cells in squamous cell carcinoma of the head and neck: mechanisms of suppression and expansion in advanced disease. Clin Cancer Res 14:3706-3715. doi: 10.1158/1078-0432.CCR-07-5126
29. Rittiner JE, Korboukh I, Hull-Ryde EA, Jin J, Janzen WP, Frye SV, Zylka MJ (2012) AMP is an adenosine A1 receptor agonist. J Biol Chem 287:5301-5309. doi: 10.1074/jbc.M111.291666
30. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM (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. doi: 10.1084/jem.20030152 (Pubitemid 38032120)
31. Zou W (2005) Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5:263-274. doi: 10.1038/nrc1586 (Pubitemid 40488632)
32. Whiteside TL (2013) Immune modulation of T-cell and NK (natural killer) cell activities by TEXs (tumour-derived exosomes). Biochem Soc Trans 41:245-251. doi: 10.1042/BST20120265
33. Yan M, Jene N, Byrne D et al (2011) Recruitment of regulatory T cells is correlated with hypoxia-induced CXCR4 expression, and is associated with poor prognosis in basal-like breast cancers. Breast Cancer Res 13:R47. doi: 10.1186/bcr2869
34. Popple A, Durrant LG, Spendlove I, Rolland P, Scott IV, Deen S, Ramage JM (2012) The chemokine, CXCL12, is an independent predictor of poor survival in ovarian cancer. Br J Cancer 106:1306-1313. doi: 10.1038/bjc.2012.49
35. Chung DJ, Rossi M, Romano E, Ghith J, Yuan J, Munn DH, Young JW (2009) Indoleamine 2,3-dioxygenase-expressing mature human monocyte-derived dendritic cells expand potent autologous regulatory T cells. Blood 114:555-563. doi: 10.1182/blood-2008-11-191197
36. Fallarino F, Grohmann U, Hwang KW et al (2003) Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol 4:1206-1212. doi: 10.1038/ni1003 (Pubitemid 37547898)
37. Munn DH, Sharma MD, Baban B, Harding HP, Zhang Y, Ron D, Mellor AL (2005) GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 22:633-642. doi: 10.1016/j.immuni.2005.03.013 (Pubitemid 40719198)
38. Wang D, DuBois RN (2013) The role of anti-inflammatory drugs in colorectal cancer. Ann Rev Med 64:131-144. doi: 10.1146/annurev-med-112211- 154330
39. Mandapathil M, Szczepanski MJ, Szajnik M, Ren J, Jackson EK, Johnson JT, Gorelik E, Lang S, Whiteside TL (2010) Adenosine and prostaglandin E2 cooperate in the suppression of immune responses mediated by adaptive regulatory T cells. J Biol Chem 285:27571-27580. doi: 10.1074/jbc.M110.127100
40. Su Y, Jackson EK, Gorelik E (2011) Receptor desensitization and blockade of the suppressive effects of prostaglandin E(2) and adenosine on the cytotoxic activity of human melanoma-infiltrating T lymphocytes. Cancer Immunol Immunother 60:111-122. doi: 10.1007/s00262-010-0924-z
41. Stagg J, Smyth MJ (2010) Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 29:5346-5358. doi: 10.1038/onc.2010.292
42. Bergmann C, Strauss L, Zeidler R, Lang S, Whiteside TL (2007) Expansion of human T regulatory type 1 cells in the microenvironment of cyclooxygenase 2 overexpressing head and neck squamous cell carcinoma. Cancer Res 67:8865-8873. doi: 10.1158/0008-5472.CAN-07-0767 (Pubitemid 47437463)
43. Whiteside TL, Jackson EK (2013) Adenosine and prostaglandin e2 production by human inducible regulatory T cells in health and disease. Front Immunol 4:212. doi: 10.3389/fimmu.2013.00212
44. Hoskin DW, Mader JS, Furlong SJ, Conrad DM, Blay J (2008) Inhibition of T cell and natural killer cell function by adenosine and its contribution to immune evasion by tumor cells (Review). Int J Oncol 32:527-535 (Pubitemid 351330458)
45. Schuler PJ, Harasymczuk M, Schilling B, Saze Z, Strauss L, Lang S, Johnson JT, Whiteside TL (2013) Effects of adjuvant and chemoradiotherapy on the frequency and function of regulatory T cells in patients with head and neck cancer. Clin Cancer Res. [Epub ahead of print]