Blockade of A2A receptors potently suppresses the metastasis of CD73+ tumors

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 36, 2013, Pages 14711-14716

  Beavis, Paul A ^a,b   Divisekera, Upulie ^a,b   Paget, Christophe ^a,b   Chow, Melvyn T ^a,b   John, Liza B ^a,b   Devaud, Christel ^a,b   Dwyer, Karen ^b,c   Stagg, John ^d   Smyth, Mark J ^a,b,e,f   Darcy, Phillip K ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ST VINCENT S HOSPITAL   (Australia)

^d CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^e QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^f UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cancer metastasis; Immunotherapy; Innate immunity; Tumor immunosuppression

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE A2A RECEPTOR; ADENOSINE A2A RECEPTOR ANTAGONIST; ADENOSINE A2B RECEPTOR ANTAGONIST; ADENOSINE RECEPTOR BLOCKING AGENT; GRANZYME B; PERFORIN; UNCLASSIFIED DRUG; 1-PROPYL-8-(4-SULFOPHENYL)XANTHINE; 5-AMINO-7-(2-PHENYLETHYL)-2-(2-FURYL)PYRAZOLO(4,3-E)-1,2,4-TRIAZOLO(1,5-C)PYRIMIDINE; ADENOSINE A2 RECEPTOR ANTAGONIST; ADENOSINE A2B RECEPTOR; GRANZYME; PYRIMIDINE DERIVATIVE; TRIAZOLE DERIVATIVE; XANTHINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST ADENOCARCINOMA; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; CYTOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; METASTASIS; METASTASIS INHIBITION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DRUG EFFECTS; EXPERIMENTAL NEOPLASM; FLOW CYTOMETRY; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

5'-NUCLEOTIDASE; ADENOSINE A2 RECEPTOR ANTAGONISTS; ANIMALS; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; FLOW CYTOMETRY; GRANZYMES; HUMANS; KILLER CELLS, NATURAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASM METASTASIS; NEOPLASMS, EXPERIMENTAL; PYRIMIDINES; RECEPTOR, ADENOSINE A2A; RECEPTOR, ADENOSINE A2B; TRIAZOLES; XANTHINES;

EID: 84883422236     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1308209110     Document Type: Article

References (44)

1. Koebel CM, et al. (2007) Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450(7171):903-907. (Pubitemid 350231320)
2. Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: Integrating immunity's roles in cancer suppression and promotion. Science 331(6024):1565-1570.
3. Ohta A, et al. (2006) A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad Sci USA 103(35):13132-13137. (Pubitemid 44338928)
4. Ohta A, et al. (2009) A2A adenosine receptor may allow expansion of T cells lacking effector functions in extracellular adenosine-rich microenvironments. J Immunol 183(9):5487-5493.
5. Beavis PA, Stagg J, Darcy PK, Smyth MJ (2012) CD73: A potent suppressor of antitumor immune responses. Trends Immunol 33(5):231-237.
6. Loi S, et al. (2013) CD73 promotes anthracycline resistance and poor prognosis in triple negative breast cancer. Proc Natl Acad Sci USA 110(27):11091-11096.
7. Stagg J, et al. (2010) Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci USA 107(4):1547-1552.
8. Stagg J, et al. (2011) CD73-deficient mice have increased antitumor immunity and are resistant to experimental metastasis. Cancer Res 71(8):2892-2900.
9. Stagg J, et al. (2012) CD73-deficient mice are resistant to carcinogenesis. Cancer Res 72(9):2190-2196.
10. Yegutkin GG, et al. (2011) Altered purinergic signaling in CD73-deficient mice inhibits tumor progression. Eur J Immunol 41(5):1231-1241.
11. Wang L, et al. (2011) CD73 has distinct roles in nonhematopoietic and hematopoietic cells to promote tumor growth in mice. J Clin Invest 121(6):2371-2382.
12. Jin D, et al. (2010) CD73 on tumor cells impairs antitumor T-cell responses: A novel mechanism of tumor-induced immune suppression. Cancer Res 70(6):2245-2255.
13. Leth-Larsen R, et al. (2009) Metastasis-related plasma membrane proteins of human breast cancer cells identified by comparative quantitative mass spectrometry. Mol Cell Proteomics 8(6):1436-1449.
14. Lee H, Lin EC, Liu L, Smith JW (2003) Gene expression profiling of tumor xenografts: In vivo analysis of organ-specific metastasis. Int J Cancer 107(4):528-534. (Pubitemid 37296111)
15. Zhang B (2010) CD73: A novel target for cancer immunotherapy. Cancer Res 70(16):6407-6411.
16. Chen JF, Eltzschig HK, Fredholm BB (2013) Adenosine receptors as drug targets - what are the challenges? Nat Rev Drug Discov 12(4):265-286.
17. 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(3):527-535. (Pubitemid 351330458)
18. Cekic C, et al. (2012) Adenosine A2B receptor blockade slows growth of bladder and breast tumors. J Immunol 188(1):198-205.
19. Csóka B, et al. (2012) Adenosine promotes alternative macrophage activation via A2A and A2B receptors. FASEB J 26(1):376-386.
20. Ryzhov S, et al. (2011) Adenosinergic regulation of the expansion and immunosuppressive activity of CD11b+Gr1+ cells. J Immunol 187(11):6120-6129.
21. Wilson JM, et al. (2009) The A2B adenosine receptor impairs the maturation and immunogenicity of dendritic cells. J Immunol 182(8):4616-4623.
22. Wang L, et al. (2008) Ecto-5′-nucleotidase promotes invasion, migration and adhesion of human breast cancer cells. J Cancer Res Clin Oncol 134(3):365-372. (Pubitemid 351170058)
23. Sadej R, Spychala J, Skladanowski AC (2006) Expression of ecto-5′-nucleotidase (eN, CD73) in cell lines from various stages of human melanoma. Melanoma Res 16(3):213-222. (Pubitemid 44085095)
24. Dieckhoff J, et al. (1986) The extracellular matrix proteins laminin and fibronectin modify the AMPase activity of 5′-nucleotidase from chicken gizzard smooth muscle. FEBS Lett 195(1-2):82-86. (Pubitemid 16048981)
25. Kalla RV, Zablocki J (2009) Progress in the discovery of selective, high affinity A(2B) adenosine receptor antagonists as clinical candidates. Purinergic Signal 5(1):21-29.
26. Chow MT, Tschopp J, Möller A, Smyth MJ (2012) NLRP3 promotes inflammation-induced skin cancer but is dispensable for asbestos-induced mesothelioma. Immunol Cell Biol 90(10):983-986.
27. Häusler SF, et al. (2011) Ectonucleotidases CD39 and CD73 on OvCA cells are potent adenosine-generating enzymes responsible for adenosine receptor 2A-dependent suppression of T cell function and NK cell cytotoxicity. Cancer Immunol Immunother 60(10):1405-1418.
28. Harish A, Hohana G, Fishman P, Arnon O, Bar-Yehuda S (2003) A3 adenosine receptor agonist potentiates natural killer cell activity. Int J Oncol 23(4):1245-1249.
29. Morello S, et al. (2011) NK1.1 cells and CD8 T cells mediate the antitumor activity of Cl-IB-MECA in a mouse melanoma model. Neoplasia 13(4):365-373.
30. Wilson JM, et al. (2011) The A2B adenosine receptor promotes Th17 differentiation via stimulation of dendritic cell IL-6. J Immunol 186(12):6746-6752.
31. Panther E, et al. (2003) Adenosine affects expression of membrane molecules, cytokine and chemokine release, and the T-cell stimulatory capacity of human dendritic cells. Blood 101(10):3985-3990. (Pubitemid 36857876)
32. Novitskiy SV, et al. (2008) Adenosine receptors in regulation of dendritic cell differentiation and function. Blood 112(5):1822-1831.
33. Ryzhov S, et al. (2008) Effect of A2B adenosine receptor gene ablation on adenosinedependent regulation of proinflammatory cytokines. J Pharmacol Exp Ther 324(2):694-700. (Pubitemid 351185857)
34. Kreckler LM, Wan TC, Ge ZD, Auchampach JA (2006) Adenosine inhibits tumor necrosis factor-alpha release from mouse peritoneal macrophages via A2A and A2B but not the A3 adenosine receptor. J Pharmacol Exp Ther 317(1):172-180.
35. Desmet CJ, et al. (2013) Identification of a pharmacologically tractable Fra-1/ADORA2B axis promoting breast cancer metastasis. Proc Natl Acad Sci USA 110(13):5139-5144.
36. Cappellari AR, Vasques GJ, Bavaresco L, Braganhol E, Battastini AM (2012) Involvement of ecto-5′-nucleotidase/CD73 in U138MG glioma cell adhesion. Mol Cell Biochem 359(1-2):315-322.
37. Airas L, et al. (1995) CD73 is involved in lymphocyte binding to the endothelium: Characterization of lymphocyte-vascular adhesion protein 2 identifies it as CD73. J Exp Med 182(5):1603-1608.
38. Airas L, Jalkanen S (1996) CD73 mediates adhesion of B cells to follicular dendritic cells. Blood 88(5):1755-1764. (Pubitemid 26307072)
39. Airas L, Niemelä J, Jalkanen S (2000) CD73 engagement promotes lymphocyte binding to endothelial cells via a lymphocyte function-associated antigen-1-dependent mechanism. J Immunol 165(10):5411-5417.
40. Gutensohn W, Resta R, Misumi Y, Ikehara Y, Thompson LF (1995) Ecto-5′-nucleotidase activity is not required for T cell activation through CD73. Cell Immunol 161(2):213-217.
41. Park A, Stacy M (2012) Istradefylline for the treatment of Parkinson's disease. Expert Opin Pharmacother 13(1):111-114.
42. Factor SA, et al. (2013) Long-term safety and efficacy of preladenant in subjects with fluctuating Parkinson's disease. Mov Disord 28(6):817-820.
43. Black KJ, Koller JM, Campbell MC, Gusnard DA, Bandak SI (2010) Quantification of indirect pathway inhibition by the adenosine A2a antagonist SYN115 in Parkinson disease. J Neurosci 30(48):16284-16292.
44. Stewart TJ, Abrams SI (2007) Altered immune function during long-term host-tumor interactions can be modulated to retard autochthonous neoplastic growth. J Immunol 179(5):2851-2859.