Targeting human inducible regulatory T cells (Tr1) in patients with cancer: Blocking of adenosineprostaglandin E2 cooperation

Expert Opinion on Biological Therapy

Volumn 11, Issue 9, 2011, Pages 1203-1214

  Mandapathil, Magis ^a   Whiteside, Theresa L ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Adenosine; Cancer; CD39; CD73; PGE2; Treg

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE A2A RECEPTOR; ADENOSINE TRIPHOSPHATE; BETA ACTIN; CD39 ANTIGEN; CD4 ANTIGEN; CELECOXIB; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE 1; CYCLOOXYGENASE 2; CYCLOPHOSPHAMIDE; DACLIZUMAB; DENILEUKIN DIFTITOX; DICLOFENAC; DIPEPTIDYL PEPTIDASE IV; IBUPROFEN; INDOMETACIN; INTERLEUKIN 10; NUCLEOTIDASE; PROSTAGLANDIN E RECEPTOR; PROSTAGLANDIN E2; ROLIPRAM; SUNITINIB; TRANSFORMING GROWTH FACTOR BETA1;

ADVANCED CANCER; ANTIGEN EXPRESSION; CANCER IMMUNOLOGY; CANCER PATIENT; CD4+ T LYMPHOCYTE; CYTOSOL; EFFECTOR CELL; ENZYME ACTIVATION; HUMAN; IMMUNE DEFICIENCY; LOW DRUG DOSE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TUMOR MICROENVIRONMENT; UPREGULATION;

ADENOSINE; DINOPROSTONE; HUMANS; NEOPLASMS; T-LYMPHOCYTES, REGULATORY;

ERAGROSTIS TEF;

EID: 80051508106     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.2011.581225     Document Type: Review

References (80)

1. Hoskin DW, Mader JS, Furlong SJ, et al. Inhibition of T cell and natural killer cell function by adenosine and its contribution to immune evasion by tumor cells (Review). Int J Oncol 2008;32:527-35 (Pubitemid 351330458)
2. Blay J, White TD, Hoskin DW. The extracellular fluid of solid carcinomas contains immunosuppressive concentrations of adenosine. Cancer Res 1997;57:2602-5 (Pubitemid 27283766)
3. Sitarz R, Leguit RJ, de Leng WW, et al. Cyclooxygenase-2 mediated regulation of E-cadherin occurs in conventional but not early-onset gastric cancer cell lines. Cell Oncol 2009;31:475-85
4. Wang D, Dubois RN. Eicosanoids and cancer. Nat Rev Cancer 2010;10:181-93
5. Zhang Y, Liu Q, Zhang M, et al. Fas signal promotes lung cancer growth by recruiting myeloid-derived suppressor cells via cancer cell-derived PGE2. J Immunol 2009;182:3801-8
6. Toutirais O, Chartier P, Dubois D, et al. Constitutive expression of TGF-beta1, interleukin-6 and interleukin-8 by tumor cells as a major component of immune escape in human ovarian carcinoma. Eur Cytokine Netw 2003;14:246-55 (Pubitemid 38122233)
7. Sa G, Das T, Moon C, et al. GD3, an overexpressed tumor-derived ganglioside, mediates the apoptosis of activated but not resting T cells. Cancer Res 2009;69:3095-104
8. Gabrilovich D, Ishida T, Oyama T, et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood 1998;92:4150-66 (Pubitemid 28544331)
9. Doubrovina ES, Doubrovin MM, Vider E, et al. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J Immunol 2003;171:6891-9 (Pubitemid 37532125)
10. Kim R, Emi M, Tanabe K, Arihiro K. Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res 2006;66:5527-36 (Pubitemid 43927099)
11. Whiteside TL. Immune responses to malignancies. J Allergy Clin Immunol 2010;125:S272-83
12. Whiteside TL. The role of immune cells in the tumor microenvironment. Cancer Treat Res 2006;130:103-24
13. Reichert TE, Strauss L, Wagner EM, et al. Signaling abnormalities and reduced proliferation of circulating and tumor-infiltrating lymphocytes in patients with oral carcinoma. Clin Cancer Res 2002;8:3137-45 (Pubitemid 35155023)
14. Ferrone S, Whiteside TL. Tumor microenvironment and immune escape. Surg Oncol Clin North AM 2007;16:755-74 (Pubitemid 350101281)
15. Oble DA, Loewe R, Yu P, Mihm MC Jr. Focus on TILs: prognostic significance of tumor infiltrating lymphocytes in human melanoma. Cancer Immun 2009;9:3
16. Fakhry C, Westra WH, Li S, et al. Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst 2008;100:261-9 (Pubitemid 351480538)
17. Whiteside TL. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008;27:5904-12
18. Uppaluri R, Dunn GP, Lewis JS Jr. Focus on TILs: prognostic significance of tumor infiltrating lymphocytes in head and neck cancers. Cancer Immun 2008;8:16
19. Imai N, Ikeda H, Tawara I, Shiku H. Tumor progression inhibits the induction of multifunctionality in adoptively transferred tumor-specific CD8+ T cells. Eur J Immunol 2009;39:241-53
20. Bergmann C, Strauss L, Wang Y, et al. T regulatory type 1 cells (Tr1) in squamous cell carcinoma of the head and neck: mechanisms of suppression and expansion in advanced disease. Clin Cancer Res 2008;14:3706-15
21. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10:942-9 (Pubitemid 39273735)
22. Strauss L, Bergmann C, Gooding W, et al. The frequency and suppressor function of CD4+CD25highFoxp3+ T cells in the circulation of patients with squamous cell carcinoma of the head and neck. Clin Cancer Res 2007;13:6301-11 (Pubitemid 350075018)
23. Mandapathil M, Szczepanski MJ, Szajnik M, et al. Increased ectonucleotidase expression and activity in regulatory T cells of patients with head and neck cancer. Clin Cancer Res 2009;15:6348-57
24. Salama P, Phillips M, Grieu F, et al. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 2009;27:186-92
25. Correale P, Rotundo MS, DelVecchio MT, et al. Regulatory (FOXP3+) T-cell tumor infiltration is a favorable prognostic factor in advanced colon cancer patients undergoing chemo or chemoimmunotherapy. J Immunother 2010;33:435-41
26. Sitkovsky MV, Kjaergaard J, Lukashev D, Ohta A. Hypoxia-adenosinergic immunosuppression: tumor protection by T regulatory cells and cancerous tissue hypoxia. Clin Cancer Res 2008;14:5947-52
27. Czystowska M, Strauss L, Bergmann C, et al. Reciprocal granzyme/perforin-mediated death of human regulatory and responder T cells is regulated by interleukin-2 (IL-2). J Mol Med 2010;88:577-88
28. Nishikawa H, Sakaguchi S. Regulatory T cells in tumor immunity. Int J Cancer 2010;127:759-67
29. Sakaguchi S, Wing K, Yamaguchi T. Dynamics of peripheral tolerance and immune regulation mediated by Treg. Eur J Immunol 2009;39:2331-6
30. Strauss L, Bergmann C, Whiteside TL. Human circulating CD4+ CD25highFoxp3+ Treg kill autologous CD8+ but not CD4+ responder cells by Fas-mediated apoptosis. J Immunology 2009;182:1469-80
31. Shevach EM. Mechanisms of Foxp3+ T regulatory cell-mediated suppression. Immunity 2009;30:636-45
32. Raimondi G, Turner MS, Thomson AW, Morel PA. Naturally occurring regulatory T cells: recent insights in health and disease. Crit Rev Immunol 2007;27:61-95 (Pubitemid 46659048)
33. Jonuleit H, Schmitt E, Stassen M, et al. Identification and functional characterization of human CD4+CD25+ T cells with regulatory properties isolated from peripheral blood. J Exp Med 2001;193:1285-94 (Pubitemid 32524778)
34. Roncarolo MG, Gregori S, Battaglia M, et al. Interleukin-10 secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006;212:28-50 (Pubitemid 44116698)
35. Bergmann C, Strauss L, Zeidler R, et al. Expansion of human T regulatory type 1 cells in the microenvironment of cyclooxygenase 2 overexpressing head and neck squamous cell carcinoma. Cancer Res 2007;67:8865-73 (Pubitemid 47437463)
36. Roncarolo MG, Bacchetta R, Bordignon C, et al. Type 1 T regulatory cells. Immunol Rev 2001;182:68-79 (Pubitemid 33070208)
37. Mougiakakos D, Choudhury A, Lladsev A, et al. Regulatory T cells in cancer. Adv Cancer Res 2010;107:57-117
38. Szczepanski MJ, Szajnik M, Czystowska M, et al. Increased frequency and suppression by regulatory T cells in patients with acute myelogenous leukemia. Clin Cancer Res 2009;15:3325-32
39. Suchard MS, Mayne E, Green VA, et al. FOXP3 expression is upregulated in CD4+ T cells in progressive HIV-1 infection and is a marker of disease severity. PLoS One 2010;5:e11762
40. Bettini M, Vignali DA. Regulatory T cells and inhibitory cytokines in autoimmunity. Curr Opin Immunol 2009;21:612-18
41. Strauss L, Bergmann C, Szczepanski M, et al. A unique subset of CD4+CD25highFoxp3+ T cells secreting IL-10 and TGF-beta1 mediates suppression in the tumor microenvironment. Clin Cancer Res 2007;13:4345-54
42. Sitkovsky MV, Lukashev D, Apasov S, et al. Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu Rev Immunol 2004;22:657-82 (Pubitemid 38680437)
43. Dannenberg AJ, Altorki NK, Boyle JO, et al. Cyclo-oxygenase 2: a pharmacological target for the prevention of cancer. Lancet Oncol 2001;2:544-51 (Pubitemid 33586867)
44. Dzhandzhugazyan KN, Kirkin AF, thor Straten P, Zeuthen J. Ecto-ATP diphosphohydrolase/CD39 is overexpressed in differentiated human melanomas. FEBS Lett 1998;430:227-30 (Pubitemid 28337918)
45. Mandapathil M, Lang S, Jackson EK, Gorelik E. Tumor-derived adenosine enhances generation and suppressive functions of human adaptive regulatory T cells. (abstract). ISBTC Ann Meeting, Washington DC, Oct 28-29, 2009
46. Zhang X, Meng L, He B, et al. The role of P2X7 receptor in ATP-mediated human leukemia cell death: calcium influx-independent. Acta Biochim Biophys Sin (Shanghai) 2009;41:362-9
47. Sitkovsky M, Lukashev D, Deaglio S, et al. Adenosine A2A receptor antagonists: blockade of adenosinergic effects and T regulatory cells. Br J Pharma 2008;153:S457-64 (Pubitemid 351341019)
48. Stagg J, Smyth MJ. Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 2010;29:5346-58
49. Zhang B. CD73: a novel target for cancer immunotherapy. Cancer Res 2010;70:6407-11
50. Mandapathil M, Hilldorfer B, Szczepanski MJ, et al. Generation and accumulation of immunosuppressive adenosine by human CD4+ CD25highFOXP3+ regulatory T cells. J Biol Chem 2010;285:7176-86
51. Borsellino G, Kleinewietfeld M, Di Mitri D, et al. Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 2007;110:1225-32 (Pubitemid 47281420)
52. Deaglio S, Dwyer KM, Gao W, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007;204:1257-65 (Pubitemid 46919862)
53. Mandapathil M, Szczepanski MJ, Szajnik M, et al. Adenosine and prostaglandin E2 cooperate in the suppression of immune responses mediated by adaptive regulatory T cells. J Biol Chem 2010;285:27571-80
54. Schuler P, Harasymczuk M, Schilling B, et al. The identification of two phenotypically and functionally distinct subsets within the human CD4+CD39+ T cell population. J Immunol Meth 2011;369:59-68
55. Mandapathil M, Lang S, Gorelik E, Whiteside TL. Isolation of functional human regulatory T cells (Treg) from the peripheral blood based on the CD39 expression. J Immunol Meth 2009;346:55-63
56. Zhou L, Chong MW, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity 2009;30:646-55
57. Zhang H, Conrad DM, Butler JJ, et al. Adenosine acts through A2 receptors to inhibit IL-2-induced tyrosine phosphorylation of STAT5 in T lymphocytes: role of cyclic adenosine 3¢,5¢-monophosphate and phosphatises. J Immunol 2004;173:932-44 (Pubitemid 38924266)
58. Raskovalova T, Lokshin A, Huang X, et al. Inhibition of cytokine production and cytotoxic activity of human anti melanoma specific CD8+ and CD4+ T lymphocytes by adenosine-protein kinase A type I signalling. Cancer Res 2007;67:5949-56 (Pubitemid 46985031)
59. Kameoka J, Tanaka T, Nojima Y, et al. Direct association of adenosine deaminase with a T cell activation antigen, CD26. Science 1993;261:466-9 (Pubitemid 23276554)
60. Schrader WP, West CA. Localization of adenosine deaminase and adenosine deaminase complexing protein in rabbit heart. Implications for adenosine metabolism. Circ Res 1990;66:754-62 (Pubitemid 20086913)
61. Dong RP, Kameoka J, Hegen M, et al. Characterization of adenosine deaminase binding to human CD26 on T cells and its biologic role in immune response. J Immunol 1996;156:1349-55 (Pubitemid 26065841)
62. Havre PA, Abe M, Urasaki Y, et al. The role of CD26/dipeptidyl peptidase IV in cancer. Front Biosci 2008;13:1634-45 (Pubitemid 351599721)
63. Bergmann C, Strauss L, Zeidler R, et al. Expansion and characteristics of human T regulatory type 1 cells in co-cultures simulating tumor microenvironment. Cancer Immunol Immunother 2007;56:1429-42 (Pubitemid 47024702)
64. Wang D, Dubois RN. Prostaglandins and cancer. Gut 2006;55:115-22 (Pubitemid 41820645)
65. Singh B, Cook KR, Vincent L, et al. Cyclooxygenase-2 induces genomic instability, BCL2 expression, doxorubicin resistance, and altered cancer-initiating cell phenotype in MCF7 breast cancer cells. J Surg Res 2008;147:240-6
66. Yaqub S, Tasken K. Role for the cAMP-protein kinase A signaling pathway in suppression of antitumor immune responses by regulatory T cells. Crit Rev Oncog 2008;14:57-77
67. Su Y, Huang X, Raskovalova T, et al. Cooperation of adenosine and prostaglandin E2 (PGE2) in amplification of cAMP-PKA signaling and immunosuppression. Cancer Immunol Immunother 2008;57:1611-23
68. Sugimoto Y, Narumiya S. Prostaglandin E receptors. J Biol Chem 2007;282:11613-17 (Pubitemid 47100657)
69. Su Y, Jackson EK, Gorelik E. Receptor desensitization and blockade of the suppressive effects of prostaglandin E2 and adenosine on the cytotoxic activity of human melanoma-infiltrating T lymphocytes. Cancer Immunol Immunother 2011;60:111-22
70. Whiteside TL. Inhibiting the inhibitors: evaluating agents targeting cancer immunosuppression. Exp Opin Biol Ther 2010;10:1019-35
71. Hasko G, Linden J, Cronstein B, et al. Adenosine receptors: therapeutic aspects for inflammatory and immune disease. Nat Rev Drug Discov 2008;7:759-70
72. Ghiringhelli F, Menard C, Puig PE, et al. Metronomic cyclophosphamide regimen selectively depicts CD4+CD25+ regulatory T cells and restores T and NK effector functions in early stage cancer patients. Cancer Immunol Immunother 2007;56:641-8 (Pubitemid 46348738)
73. Morse MA, Hobeika AC, Osada T, et al. Depletion of human regulatory T cells specifically enhances antigen specific immune responses to cancer vaccines. Blood 2008;112:610-18
74. Finke JH, Rini B, Ireland J, et al. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clin Cancer Res 2008;14:6674-82
75. DeVries IJM, Castelli C, Huygens C, et al. Frequency of circulating Tregs with demethylated FOXP3 intron 1 in melanoma patients receiving tumor vaccines and potentially Treg-depleting agents. Clin Cancer Res 2010;17:1-8
76. Ernst PB, Garrison JC, Thompson LF. Much ado about adenosine: adenosine synthesis and function in regulatory T cell biology. J Immunol 2010;185:1993-8
77. Greenhough A, Smartt HJM, Moore AE, et al. The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis 2009;30:377-86
78. Iwatsubo K, Okumura S, Ishikawa Y. Drug therapy aimed at adenylyl cyclase to regulate cyclic nucleotide signaling. Endocr Metab Immune Disord Drug Targets 2006;6:239-47 (Pubitemid 44383207)
79. Pavan B, Biondi C, Dalpiaz A. Adenylyl cyclases as innovative therapeutic goals. Drug Discov Today 2009;14:982-91
80. Duan B, Davis R, Sadat EL, et al. Distinct roles of adenylyl cyclase VII in regulating the immune responses in mice. J Immunol 2010;185:335-44