CD73 and adenosine generation in the creation of regulatory microenvironments

Clinical and Experimental Immunology

Volumn 171, Issue 1, 2013, Pages 1-7

  Regateiro, F S ^a,b   Cobbold, S P ^a   Waldmann, H ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Adenosine; CD73; Immune regulation; Lymphocytes; TGF

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE TRIPHOSPHATE; CD39 ANTIGEN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CANCER INVASION; DEPHOSPHORYLATION; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; UPREGULATION;

5'-NUCLEOTIDASE; ADENOSINE; ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIGENS, CD; APYRASE; CYTOKINES; HUMANS; INFLAMMATION MEDIATORS; MICE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; TUMOR ESCAPE;

EID: 84870465551     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2012.04623.x     Document Type: Article

References (70)

1. Waldmann H, Graca L, Cobbold S, Adams E, Tone M, Tone Y. Regulatory T cells and organ transplantation. Semin Immunol 2004; 16:119-26.
2. Waldmann H, Chen TC, Graca L etal. Regulatory T cells in transplantation. Semin Immunol 2006; 18:111-9.
3. Waldmann H, Adams E, Fairchild P, Cobbold S. Infectious tolerance and the long-term acceptance of transplanted tissue. Immunol Rev 2006; 212:301-13.
4. Waldmann H, Adams E, Cobbold S. Reprogramming the immune system: co-receptor blockade as a paradigm for harnessing tolerance mechanisms. Immunol Rev 2008; 223:361-70.
5. Mellor AL, Munn DH. Creating immune privilege: active local suppression that benefits friends, but protects foes. Nat Rev Immunol 2008; 8:74-80.
6. Cobbold SP, Nolan KF, Graca L etal. Regulatory T cells and dendritic cells in transplantation tolerance: molecular markers and mechanisms. Immunol Rev 2003; 196:109-24.
7. Sanjabi S, Zenewicz LA, Kamanaka M, Flavell RA. Anti-inflammatory and pro-inflammatory roles of TGF-beta, IL-10, and IL-22 in immunity and autoimmunity. Curr Opin Pharmacol 2009; 9:447-53.
8. Soares MP, Lin Y, Anrather J etal. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 1998; 4:1073-7.
9. Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 2003; 24:449-55.
10. McDaid J, Yamashita K, Chora A etal. Heme oxygenase-1 modulates the allo-immune response by promoting activation-induced cell death of T cells. FASEB J 2005; 19:458-60.
11. Munder M, Schneider H, Luckner C etal. Suppression of T-cell functions by human granulocyte arginase. Blood 2006; 108:1627-34.
12. Munn DH, Zhou M, Attwood JT etal. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998; 281:1191-3.
13. Fallarino F, Grohmann U, Hwang KW etal. Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol 2003; 4:1206-12.
14. Mellor AL, Chandler P, Baban B etal. Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2, 3 dioxygenase. Int Immunol 2004; 16:1391-401.
15. Cobbold SP, Adams E, Farquhar CA etal. Infectious tolerance via the consumption of essential amino acids and mTOR signaling. Proc Natl Acad Sci USA 2009; 106:12055-60.
16. Peter C, Waldmann H, Cobbold SP. mTOR signalling and metabolic regulation of T cell differentiation. Curr Opin Immunol 2010; 22:655-61.
17. Jacobson KA, Gao ZG. Adenosine receptors as therapeutic targets. Nat Rev Drug Discov 2006; 5:247-64.
18. Hasko G, Linden J, Cronstein B, Pacher P. Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov 2008; 7:759-70.
19. Sakowicz-Burkiewicz M, Pawelczyk T. Recent advances in understanding the relationship between adenosine metabolism and the function of T and B lymphocytes in diabetes. J Physiol Pharmacol 2011; 62:505-12.
20. Sitkovsky MV, Lukashev D, Apasov S etal. Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu Rev Immunol 2004; 22:657-82.
21. Ohta A, Sitkovsky M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 2001; 414:916-20.
22. Huang S, Apasov S, Koshiba M, Sitkovsky M. Role of A2a extracellular adenosine receptor-mediated signaling in adenosine-mediated inhibition of T-cell activation and expansion. Blood 1997; 90:1600-10.
23. Lappas CM, Rieger JM, Linden J. A2A adenosine receptor induction inhibits IFN-gamma production in murine CD4+ T cells. J Immunol 2005; 174:1073-80.
24. Zarek PE, Huang CT, Lutz ER etal. A2A receptor signaling promotes peripheral tolerance by inducing T-cell anergy and the generation of adaptive regulatory T cells. Blood 2008; 111:251-9.
25. Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC. Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther 2006; 112:358-404.
26. Kumar V, Sharma A. Adenosine: an endogenous modulator of innate immune system with therapeutic potential. Eur J Pharmacol 2009; 616:7-15.
27. Franco R, Valenzuela A, Lluis C, Blanco J. Enzymatic and extraenzymatic role of ecto-adenosine deaminase in lymphocytes. Immunol Rev 1998; 161:27-42.
28. Blackburn MR, Kellems RE. Adenosine deaminase deficiency: metabolic basis of immune deficiency and pulmonary inflammation. Adv Immunol 2005; 86:1-41.
29. Novak I. ATP as a signaling molecule: the exocrine focus. News Physiol Sci 2003; 18:12-7.
30. Resta R, Yamashita Y, Thompson LF. Ecto-enzyme and signaling functions of lymphocyte CD73. Immunol Rev 1998; 161:95-109.
31. Schenk U, Westendorf AM, Radaelli E etal. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci Signal 2008; 1:ra6.
32. Schenk U, Frascoli M, Proietti M etal. ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Sci Signal 2011; 4:ra12.
33. Atarashi K, Nishimura J, Shima T etal. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008; 455:808-12.
34. Junger WG. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 2011; 11:201-12.
35. Colgan SP, Eltzschig HK, Eckle T, Thompson LF. Physiological roles for ecto-5′-nucleotidase (CD73). Purinergic Signal 2006; 2:351-60.
36. Koziak K, Sevigny J, Robson SC, Siegel JB, Kaczmarek E. Analysis of CD39/ATP diphosphohydrolase (ATPDase) expression in endothelial cells, platelets and leukocytes. Thromb Haemost 1999; 82:1538-44.
37. Dwyer KM, Deaglio S, Gao W, Friedman D, Strom TB, Robson SC. CD39 and control of cellular immune responses. Purinergic Signal 2007; 3:171-80.
38. Pulte ED, Broekman MJ, Olson KE etal. CD39/NTPDase-1 activity and expression in normal leukocytes. Thromb Res 2007; 121:309-17.
39. Thompson LF, Eltzschig HK, Ibla JC etal. Crucial role for ecto-5′-nucleotidase (CD73) in vascular leakage during hypoxia. J Exp Med 2004; 200:1395-405.
40. Gavin MA, Rasmussen JP, Fontenot JD etal. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 2007; 445:771-5.
41. Kobie JJ, Shah PR, Yang L, Rebhahn JA, Fowell DJ, Mosmann TR. T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5′-adenosine monophosphate to adenosine. J Immunol 2006; 177:6780-6.
42. Borsellino G, Kleinewietfeld M, Di Mitri D etal. Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 2007; 110:1225-32.
43. Deaglio S, Dwyer KM, Gao W etal. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007; 204:1257-65.
44. Zhou Q, Yan J, Putheti P etal. Isolated CD39 expression on CD4+ T cells denotes both regulatory and memory populations. Am J Transplant 2009; 9:2303-11.
45. Regateiro FS, Howie D, Nolan KF etal. Generation of anti-inflammatory adenosine by leukocytes is regulated by TGF-beta. Eur J Immunol 2011; 41:2955-65.
46. Mandapathil M, Hilldorfer B, Szczepanski MJ etal. Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells. J Biol Chem 2010; 285:7176-86.
47. Fletcher JM, Lonergan R, Costelloe L etal. CD39+Foxp3+ regulatory T cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J Immunol 2009; 183:7602-10.
48. Moncrieffe H, Nistala K, Kamhieh Y etal. High expression of the ectonucleotidase CD39 on T cells from the inflamed site identifies two distinct populations, one regulatory and one memory T cell population. J Immunol 2010; 185:134-43.
49. Burton CT, Westrop SJ, Eccles-James I etal. Altered phenotype of regulatory T cells associated with lack of human immunodeficiency virus (HIV)-1-specific suppressive function. Clin Exp Immunol 2011; 166:191-200.
50. Peola S, Borrione P, Matera L, Malavasi F, Pileri A, Massaia M. Selective induction of CD73 expression in human lymphocytes by CD38 ligation: a novel pathway linking signal transducers with ecto-enzyme activities. J Immunol 1996; 157:4354-62.
51. Chen W, Jin W, Hardegen N etal. 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 2003; 198:1875-86.
52. Cobbold SP, Castejon R, Adams E etal. Induction of FoxP3+ regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J Immunol 2004; 172:6003-10.
53. D'Alise AM, Ergun A, Hill JA, Mathis D, Benoist C. A cluster of coregulated genes determines TGF-beta-induced regulatory T-cell (Treg) dysfunction in NOD mice. Proc Natl Acad Sci USA 2011; 108:8737-42.
54. Wang L, Zhou X, Zhou T etal. Ecto-5′-nucleotidase promotes invasion, migration and adhesion of human breast cancer cells. J Cancer Res Clin Oncol 2008; 134:365-72.
55. 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.
56. Ohta A, Gorelik E, Prasad SJ etal. A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad Sci USA 2006; 103:13132-7.
57. Jin D, Fan J, Wang L etal. CD73 on tumor cells impairs antitumor T-cell responses: a novel mechanism of tumor-induced immune suppression. Cancer Res 2010; 70:2245-55.
58. Stagg J, Divisekera U, McLaughlin N etal. Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci USA 2010; 107:1547-52.
59. Yegutkin GG, Marttila-Ichihara F, Karikoski M etal. Altered purinergic signaling in CD73-deficient mice inhibits tumor progression. Eur J Immunol 2011; 41:1231-41.
60. Serra S, Horenstein AL, Vaisitti T etal. CD73-generated extracellular adenosine in chronic lymphocytic leukemia creates local conditions counteracting drug-induced cell death. Blood 2011; 118:6141-52.
61. Sun X, Wu Y, Gao W etal. CD39/ENTPD1 expression by CD4+Foxp3+ regulatory T cells promotes hepatic metastatic tumor growth in mice. Gastroenterology 2010; 139:1030-40.
62. Wang L, Fan J, Thompson LF etal. CD73 has distinct roles in nonhematopoietic and hematopoietic cells to promote tumor growth in mice. J Clin Invest 2011; 121:2371-82.
63. Yang C, Robbins PD. The roles of tumor-derived exosomes in cancer pathogenesis. Clin Dev Immunol 2011; 2011:842-849.
64. Zhang HG, Grizzle WE. Exosomes and cancer: a newly described pathway of immune suppression. Clin Cancer Res 2011; 17:959-64.
65. Clayton A, Al-Taei S, Webber J, Mason MD, Tabi Z. Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J Immunol 2011; 187:676-83.
66. Wrzesinski SH, Wan YY, Flavell RA. Transforming growth factor-beta and the immune response: implications for anticancer therapy. Clin Cancer Res 2007; 13 (18 Pt 1):5262-70.
67. Gorelik L, Flavell RA. Immune-mediated eradication of tumors through the blockade of transforming growth factor-beta signaling in T cells. Nat Med 2001; 7:1118-22.
68. Naganuma M, Wiznerowicz EB, Lappas CM, Linden J, Worthington MT, Ernst PB. Cutting edge: critical role for A2A adenosine receptors in the T cell-mediated regulation of colitis. J Immunol 2006; 177:2765-9.
69. Sitkovsky M, Lukashev D, Deaglio S, Dwyer K, Robson SC, Ohta A. Adenosine A2A receptor antagonists: blockade of adenosinergic effects and T regulatory cells. Br J Pharmacol 2008; 153 (Suppl. 1):S457-64.
70. Hashikawa T, Hooker SW, Maj JG etal. Regulation of adenosine receptor engagement by ecto-adenosine deaminase. FASEB J 2004; 18:131-3.