CD73 and CD39 ectonucleotidases in T cell differentiation: Beyond immunosuppression

FEBS Letters

Volumn 589, Issue 22, 2015, Pages 3454-3460

  Bono, María Rosa ^a   Fernández, Dominique ^a   Flores Santibáñez, Felipe ^a   Rosemblatt, Mario ^a,b,c   Sauma, Daniela ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b Fundacion Ciencia para la Vida   (Chile)

^c UNIVERSIDAD ANDRÉS BELLO   (Chile)

Author keywords

Adenosine; CD39; CD73; Differentiation; Ectonucleotidase; T cell

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE A2A RECEPTOR AGONIST; ADENOSINE A2B RECEPTOR; ADENOSINE A3 RECEPTOR; ADENOSINE TRIPHOSPHATE; CD39 ANTIGEN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ECTONUCLEOTIDASE; UNCLASSIFIED DRUG; APYRASE; LEUKOCYTE ANTIGEN;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL SURVIVAL; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; ENZYME INHIBITION; HOMEOSTASIS; HUMAN; HYDROLYSIS; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MEMORY CELL; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TUMOR ESCAPE; TUMOR MICROENVIRONMENT; CELL DIFFERENTIATION; CYTOLOGY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM;

5'-NUCLEOTIDASE; ADENOSINE; ANTIGENS, CD; APYRASE; CELL DIFFERENTIATION; HUMANS; IMMUNE TOLERANCE; T-LYMPHOCYTES;

EID: 84946488586     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.07.027     Document Type: Review

References (90)

1. G.G. Yegutkin Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade Biochim. Biophys. Acta 1783 2008 673 694
2. M.R. Elliott, F.B. Chekeni, P.C. Trampont, E.R. Lazarowski, A. Kadl, S.F. Walk, D. Park, R.I. Woodson, M. Ostankovich, P. Sharma, J.J. Lysiak, T.K. Harden, N. Leitinger, and K.S. Ravichandran Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance Nature 461 2009 282 286
3. A. Trautmann Extracellular ATP in the immune system: more than just a "danger signal" Sci. Signal. 2 2009 pe6
4. M.V. Sitkovsky, D. Lukashev, S. Apasov, H. Kojima, M. Koshiba, C. Caldwell, A. Ohta, and M. Thiel Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors Annu. Rev. Immunol. 22 2004 657 682
5. G. Burnstock Physiology and pathophysiology of purinergic neurotransmission Physiol. Rev. 87 2007 659 797
6. P. Pellegatti, L. Raffaghello, G. Bianchi, F. Piccardi, V. Pistoia, and F. Di Virgilio Increased level of extracellular ATP at tumor sites: in vivo imaging with plasma membrane luciferase PLoS ONE 3 2008 e2599
7. Y. Chen, R. Corriden, Y. Inoue, L. Yip, N. Hashiguchi, A. Zinkernagel, V. Nizet, P.A. Insel, and W.G. Junger ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors Science 314 2006 1792 1795
8. U. Schenk, A.M. Westendorf, E. Radaelli, A. Casati, M. Ferro, M. Fumagalli, C. Verderio, J. Buer, E. Scanziani, and F. Grassi Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels Sci. Signal. 1 2008 ra6
9. F. Di Virgilio, and M. Vuerich Purinergic signaling in the immune system Auton Neurosci. 2015
10. C. Cekic, D. Sag, Y.J. Day, and J. Linden Extracellular adenosine regulates naive T cell development and peripheral maintenance J. Exp. Med. 210 2013 2693 2706
11. C. Cekic, and J. Linden Adenosine A2A receptors intrinsically regulate CD8+ T cells in the tumor microenvironment Cancer Res. 74 2014 7239 7249
12. M. Sakowicz-Burkiewicz, and T. Pawelczyk Recent advances in understanding the relationship between adenosine metabolism and the function of T and B lymphocytes in diabetes J. Physiol. Pharmacol. 62 2011 505 512
13. P.A. Beavis, J. Stagg, P.K. Darcy, and M.J. Smyth CD73: a potent suppressor of antitumor immune responses Trends Immunol. 33 2012 231 237
14. S.C. Robson, J. Sevigny, and H. Zimmermann The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance Purinergic Signal. 2 2006 409 430
15. F.S. Regateiro, S.P. Cobbold, and H. Waldmann CD73 and adenosine generation in the creation of regulatory microenvironments Clin. Exp. Immunol. 171 2013 1 7
16. J. Park, and R.S. Gupta Adenosine kinase and ribokinase-the RK family of proteins Cell. Mol. Life Sci. 65 2008 2875 2896
17. L. Antonioli, P. Pacher, E.S. Vizi, and G. Hasko CD39 and CD73 in immunity and inflammation Trends Mol. Med. 19 2013 355 367
18. B.P. Chadwick, and A.M. Frischauf The CD39-like gene family: identification of three new human members (CD39L2, CD39L3, and CD39L4), their murine homologues, and a member of the gene family from Drosophila melanogaster Genomics 50 1998 357 367
19. E. Kaczmarek, K. Koziak, J. Sevigny, J.B. Siegel, J. Anrather, A.R. Beaudoin, F.H. Bach, and S.C. Robson Identification and characterization of CD39/vascular ATP diphosphohydrolase J. Biol. Chem. 271 1996 33116 33122
20. L.F. Thompson, H.K. Eltzschig, J.C. Ibla, C.J. Van De Wiele, R. Resta, J.C. Morote-Garcia, and S.P. Colgan Crucial role for ecto-5'-nucleotidase (CD73) in vascular leakage during hypoxia J. Exp. Med. 200 2004 1395 1405
21. J. Bastid, A. Cottalorda-Regairaz, G. Alberici, N. Bonnefoy, J.F. Eliaou, and A. Bensussan ENTPD1/CD39 is a promising therapeutic target in oncology Oncogene 32 2013 1743 1751
22. L. Airas, and S. Jalkanen CD73 mediates adhesion of B cells to follicular dendritic cells Blood 88 1996 1755 1764
23. S. Deaglio, K.M. Dwyer, W. Gao, D. Friedman, A. Usheva, A. Erat, J.F. Chen, K. Enjyoji, J. Linden, M. Oukka, V.K. Kuchroo, T.B. Strom, and S.C. Robson Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression J. Exp. Med. 204 2007 1257 1265
24. G.S. Kansas, G.S. Wood, and T.F. Tedder Expression, distribution, and biochemistry of human CD39. Role in activation-associated homotypic adhesion of lymphocytes J. Immunol. 146 1991 2235 2244
25. E.D. Pulte, M.J. Broekman, K.E. Olson, J.H. Drosopoulos, J.R. Kizer, N. Islam, and A.J. Marcus CD39/NTPDase-1 activity and expression in normal leukocytes Thromb. Res. 121 2007 309 317
26. S. Ryzhov, S.V. Novitskiy, A.E. Goldstein, A. Biktasova, M.R. Blackburn, I. Biaggioni, M.M. Dikov, and I. Feoktistov Adenosinergic regulation of the expansion and immunosuppressive activity of CD11b+Gr1+ cells J. Immunol. 187 2011 6120 6129
27. L.F. Thomson, J.M. Ruedi, A. Glass, G. Moldenhauer, P. Moller, M.G. Low, M.R. Klemens, M. Massaia, and A.H. Lucas Production and characterization of monoclonal antibodies to the glycosyl phosphatidylinositol-anchored lymphocyte differentiation antigen ecto-5'-nucleotidase (CD73) Tissue Antigens 35 1990 9 19
28. J.J. Kobie, P.R. Shah, L. Yang, J.A. Rebhahn, D.J. Fowell, and T.R. Mosmann 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. 177 2006 6780 6786
29. S. Sad, and T.R. Mosmann Single IL-2-secreting precursor CD4 T cell can develop into either Th1 or Th2 cytokine secretion phenotype J. Immunol. 153 1994 3514 3522
30. L. Yang, J.J. Kobie, and T.R. Mosmann CD73 and Ly-6A/E distinguish in vivo primed but uncommitted mouse CD4 T cells from type 1 or type 2 effector cells J. Immunol. 175 2005 6458 6464
31. F. Chalmin, G. Mignot, M. Bruchard, A. Chevriaux, F. Vegran, A. Hichami, S. Ladoire, V. Derangere, J. Vincent, D. Masson, S.C. Robson, G. Eberl, J.R. Pallandre, C. Borg, B. Ryffel, L. Apetoh, C. Rebe, and F. Ghiringhelli Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression Immunity 36 2012 362 373
32. I. Kryczek, E. Zhao, Y. Liu, Y. Wang, L. Vatan, W. Szeliga, J. Moyer, A. Klimczak, A. Lange, and W. Zou Human TH17 cells are long-lived effector memory cells Sci. Transl. Med. 3 2011 104ra100
33. N. Martin-Orozco, P. Muranski, Y. Chung, X.O. Yang, T. Yamazaki, S. Lu, P. Hwu, N.P. Restifo, W.W. Overwijk, and C. Dong T helper 17 cells promote cytotoxic T cell activation in tumor immunity Immunity 31 2009 787 798
34. P. Muranski, A. Boni, P.A. Antony, L. Cassard, K.R. Irvine, A. Kaiser, C.M. Paulos, D.C. Palmer, C.E. Touloukian, K. Ptak, L. Gattinoni, C. Wrzesinski, C.S. Hinrichs, K.W. Kerstann, L. Feigenbaum, C.C. Chan, and N.P. Restifo Tumor-specific Th17-polarized cells eradicate large established melanoma Blood 112 2008 362 373
35. P. Muranski, Z.A. Borman, S.P. Kerkar, C.A. Klebanoff, Y. Ji, L. Sanchez-Perez, M. Sukumar, R.N. Reger, Z. Yu, S.J. Kern, R. Roychoudhuri, G.A. Ferreyra, W. Shen, S.K. Durum, L. Feigenbaum, D.C. Palmer, P.A. Antony, C.C. Chan, A. Laurence, R.L. Danner, L. Gattinoni, and N.P. Restifo Th17 cells are long lived and retain a stem cell-like molecular signature Immunity 35 2011 972 985
36. S. Nunez, J.J. Saez, D. Fernandez, F. Flores-Santibanez, K. Alvarez, G. Tejon, P. Ruiz, P. Maldonado, Y. Hidalgo, V. Manriquez, M.R. Bono, M. Rosemblatt, and D. Sauma T helper type 17 cells contribute to anti-tumour immunity and promote the recruitment of T helper type 1 cells to the tumour Immunology 139 2013 61 71
37. S. Wei, E. Zhao, I. Kryczek, and W. Zou Th17 cells have stem cell-like features and promote long-term immunity Oncoimmunology 1 2012 516 519
38. S. Chatterjee, K. Thyagarajan, P. Kesarwani, J.H. Song, M. Soloshchenko, J. Fu, S.R. Bailey, C. Vasu, A.S. Kraft, C.M. Paulos, X.Z. Yu, and S. Mehrotra Reducing CD73 expression by IL1beta-Programmed Th17 cells improves immunotherapeutic control of tumors Cancer Res. 74 2014 6048 6059
39. H. Moncrieffe, K. Nistala, Y. Kamhieh, J. Evans, A. Eddaoudi, S. Eaton, and L.R. Wedderburn 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. 185 2010 134 143
40. Q. Zhou, J. Yan, P. Putheti, Y. Wu, X. Sun, V. Toxavidis, J. Tigges, N. Kassam, K. Enjyoji, S.C. Robson, T.B. Strom, and W. Gao Isolated CD39 expression on CD4+ T cells denotes both regulatory and memory populations Am. J. Transplant. 9 2009 2303 2311
41. C.R. Maliszewski, G.J. Delespesse, M.A. Schoenborn, R.J. Armitage, W.C. Fanslow, T. Nakajima, E. Baker, G.R. Sutherland, K. Poindexter, C. Birks, and et al. The CD39 lymphoid cell activation antigen. Molecular cloning and structural characterization J. Immunol. 153 1994 3574 3583
42. R. Corriden, Y. Chen, Y. Inoue, G. Beldi, S.C. Robson, P.A. Insel, and W.G. Junger Ecto-nucleoside triphosphate diphosphohydrolase 1 (E-NTPDase1/CD39) regulates neutrophil chemotaxis by hydrolyzing released ATP to adenosine J. Biol. Chem. 283 2008 28480 28486
43. F. Schena, S. Volpi, C.E. Faliti, F. Penco, S. Santi, M. Proietti, U. Schenk, G. Damonte, A. Salis, M. Bellotti, F. Fais, C. Tenca, M. Gattorno, H. Eibel, M. Rizzi, K. Warnatz, M. Idzko, C.K. Ayata, M. Rakhmanov, T. Galli, A. Martini, M. Canossa, F. Grassi, and E. Traggiai Dependence of immunoglobulin class switch recombination in B cells on vesicular release of ATP and CD73 ectonucleotidase activity Cell Rep. 3 2013 1824 1831
44. H.K. Eltzschig, D. Kohler, T. Eckle, T. Kong, S.C. Robson, and S.P. Colgan Central role of Sp1-regulated CD39 in hypoxia/ischemia protection Blood 113 2009 224 232
45. K. Synnestvedt, G.T. Furuta, K.M. Comerford, N. Louis, J. Karhausen, H.K. Eltzschig, K.R. Hansen, L.F. Thompson, and S.P. Colgan Ecto-5'-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia J. Clin. Invest. 110 2002 993 1002
46. F.S. Regateiro, D. Howie, K.F. Nolan, E.I. Agorogiannis, D.R. Greaves, S.P. Cobbold, and H. Waldmann Generation of anti-inflammatory adenosine by leukocytes is regulated by TGF-beta Eur. J. Immunol. 41 2011 2955 2965
47. J. Niemela, T. Henttinen, G.G. Yegutkin, L. Airas, A.M. Kujari, P. Rajala, and S. Jalkanen IFN-alpha induced adenosine production on the endothelium: a mechanism mediated by CD73 (ecto-5'-nucleotidase) up-regulation J. Immunol. 172 2004 1646 1653
48. J. Spychala, and J. Kitajewski Wnt and beta-catenin signaling target the expression of ecto-5'-nucleotidase and increase extracellular adenosine generation Exp. Cell Res. 296 2004 99 108
49. B. Allard, M. Turcotte, and J. Stagg CD73-generated adenosine: orchestrating the tumor-stroma interplay to promote cancer growth J. Biomed. Biotechnol. 2012 2012 485156
50. V. Ralevic, and G. Burnstock Receptors for purines and pyrimidines Pharmacol. Rev. 50 1998 413 492
51. J. Stagg, and M.J. Smyth Extracellular adenosine triphosphate and adenosine in cancer Oncogene 29 2010 5346 5358
52. G.C. Parry, and N. Mackman Role of cyclic AMP response element-binding protein in cyclic AMP inhibition of NF-kappaB-mediated transcription J. Immunol. 159 1997 5450 5456
53. C. Ramstad, V. Sundvold, H.K. Johansen, and T. Lea CAMP-dependent protein kinase (PKA) inhibits T cell activation by phosphorylating ser-43 of raf-1 in the MAPK/ERK pathway Cell. Signal. 12 2000 557 563
54. D.R. DeSilva, E.A. Jones, M.F. Favata, B.D. Jaffee, R.L. Magolda, J.M. Trzaskos, and P.A. Scherle Inhibition of mitogen-activated protein kinase kinase blocks T cell proliferation but does not induce or prevent anergy J. Immunol. 160 1998 4175 4181
55. S. Huang, S. Apasov, M. Koshiba, and M. Sitkovsky Role of A2a extracellular adenosine receptor-mediated signaling in adenosine-mediated inhibition of T-cell activation and expansion Blood 90 1997 1600 1610
56. A. Ohta, A. Ohta, M. Madasu, R. Kini, M. Subramanian, N. Goel, and M. Sitkovsky A2A adenosine receptor may allow expansion of T cells lacking effector functions in extracellular adenosine-rich microenvironments J. Immunol. 183 2009 5487 5493
57. B. Csoka, L. Himer, Z. Selmeczy, E.S. Vizi, P. Pacher, C. Ledent, E.A. Deitch, Z. Spolarics, Z.H. Nemeth, and G. Hasko Adenosine A2A receptor activation inhibits T helper 1 and T helper 2 cell development and effector function FASEB J. 22 2008 3491 3499
58. P.E. Zarek, C.T. Huang, E.R. Lutz, J. Kowalski, M.R. Horton, J. Linden, C.G. Drake, and J.D. Powell A2A receptor signaling promotes peripheral tolerance by inducing T-cell anergy and the generation of adaptive regulatory T cells Blood 111 2008 251 259
59. K. Wing, and S. Sakaguchi Regulatory T cells exert checks and balances on self tolerance and autoimmunity Nat. Immunol. 11 2010 7 13
60. G. Borsellino, M. Kleinewietfeld, D. Di Mitri, A. Sternjak, A. Diamantini, R. Giometto, S. Hopner, D. Centonze, G. Bernardi, M.L. Dell'Acqua, P.M. Rossini, L. Battistini, O. Rotzschke, and K. Falk Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression Blood 110 2007 1225 1232
61. F. Salcido-Ochoa, J. Tsang, P. Tam, K. Falk, and O. Rotzschke Regulatory T cells in transplantation: does extracellular adenosine triphosphate metabolism through CD39 play a crucial role? Trans. Rev. (Orlando). 24 2010 52 66
62. C. Linnemann, F.A. Schildberg, A. Schurich, L. Diehl, S.I. Hegenbarth, E. Endl, S. Lacher, C.E. Muller, J. Frey, L. Simeoni, B. Schraven, D. Stabenow, and P.A. Knolle Adenosine regulates CD8 T-cell priming by inhibition of membrane-proximal T-cell receptor signalling Immunology 128 2009 e728 e737
63. T. Vang, K.M. Torgersen, V. Sundvold, M. Saxena, F.O. Levy, B.S. Skalhegg, V. Hansson, T. Mustelin, and K. Tasken Activation of the COOH-terminal Src kinase (Csk) by cAMP-dependent protein kinase inhibits signaling through the T cell receptor J. Exp. Med. 193 2001 497 507
64. A. Ohta, R. Kini, A. Ohta, M. Subramanian, M. Madasu, and M. Sitkovsky The development and immunosuppressive functions of CD4(+) CD25(+) FoxP3(+) regulatory T cells are under influence of the adenosine-A2A adenosine receptor pathway Front. Immunol. 3 2012 190
65. D. Jin, J. Fan, L. Wang, L.F. Thompson, A. Liu, B.J. Daniel, T. Shin, T.J. Curiel, and B. Zhang CD73 on tumor cells impairs antitumor T-cell responses: a novel mechanism of tumor-induced immune suppression Cancer Res. 70 2010 2245 2255
66. A. Ohta, E. Gorelik, S.J. Prasad, F. Ronchese, D. Lukashev, M.K. Wong, X. Huang, S. Caldwell, K. Liu, P. Smith, J.F. Chen, E.K. Jackson, S. Apasov, S. Abrams, and M. Sitkovsky A2A adenosine receptor protects tumors from antitumor T cells Proc. Natl. Acad. Sci. U.S.A. 103 2006 13132 13137
67. S.F. Hausler, I. Montalban del Barrio, J. Strohschein, P. Anoop Chandran, J.B. Engel, A. Honig, M. Ossadnik, E. Horn, B. Fischer, M. Krockenberger, S. Heuer, A.A. Seida, M. Junker, H. Kneitz, D. Kloor, K.N. Klotz, J. Dietl, and J. Wischhusen 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 2011 1405 1418
68. J.M. Wilson, W.G. Ross, O.N. Agbai, R. Frazier, R.A. Figler, J. Rieger, J. Linden, and P.B. Ernst The A2B adenosine receptor impairs the maturation and immunogenicity of dendritic cells J. Immunol. 182 2009 4616 4623
69. B. Csoka, Z. Selmeczy, B. Koscso, Z.H. Nemeth, P. Pacher, P.J. Murray, D. Kepka-Lenhart, S.M. Morris Jr., W.C. Gause, S.J. Leibovich, and G. Hasko Adenosine promotes alternative macrophage activation via A2A and A2B receptors FASEB J. 26 2012 376 386
70. L. Antonioli, C. Blandizzi, P. Pacher, and G. Hasko Immunity, inflammation and cancer: a leading role for adenosine Nat. Rev. Cancer 13 2013 842 857
71. F. Di Virgilio, P. Chiozzi, D. Ferrari, S. Falzoni, J.M. Sanz, A. Morelli, M. Torboli, G. Bolognesi, and O.R. Baricordi Nucleotide receptors: an emerging family of regulatory molecules in blood cells Blood 97 2001 587 600
72. F. Aswad, H. Kawamura, and G. Dennert High sensitivity of CD4+CD25+ regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: a role for P2X7 receptors J. Immunol. 175 2005 3075 3083
73. M. Massaia, L. Perrin, A. Bianchi, J. Ruedi, C. Attisano, D. Altieri, G.T. Rijkers, and L.F. Thompson Human T cell activation. Synergy between CD73 (ecto-5'-nucleotidase) and signals delivered through CD3 and CD2 molecules J. Immunol. 145 1990 1664 1674
74. L.F. Thompson, J.M. Ruedi, A. Glass, M.G. Low, and A.H. Lucas Antibodies to 5'-nucleotidase (CD73), a glycosyl-phosphatidylinositol-anchored protein, cause human peripheral blood T cells to proliferate J. Immunol. 143 1989 1815 1821
75. R. Loertscher, and P. Lavery The role of glycosyl phosphatidyl inositol (GPI)-anchored cell surface proteins in T-cell activation Transpl. Immunol. 9 2002 93 96
76. U. Dianzani, V. Redoglia, M. Bragardo, C. Attisano, A. Bianchi, D. Di Franco, U. Ramenghi, H. Wolff, L.F. Thompson, A. Pileri, and et al. Co-stimulatory signal delivered by CD73 molecule to human CD45RAhiCD45ROlo (naive) CD8+ T lymphocytes J. Immunol. 151 1993 3961 3970
77. R. Resta, Y. Yamashita, and L.F. Thompson Ecto-enzyme and signaling functions of lymphocyte CD73 Immunol. Rev. 161 1998 95 109
78. L. Airas, J. Hellman, M. Salmi, P. Bono, T. Puurunen, D.J. Smith, and S. Jalkanen CD73 is involved in lymphocyte binding to the endothelium: characterization of lymphocyte-vascular adhesion protein 2 identifies it as CD73 J. Exp. Med. 182 1995 1603 1608
79. L. Airas, J. Niemela, and S. Jalkanen CD73 engagement promotes lymphocyte binding to endothelial cells via a lymphocyte function-associated antigen-1-dependent mechanism J. Immunol. 165 2000 5411 5417
80. S.E. Hamilton, and S.C. Jameson CD8 T cell quiescence revisited Trends Immunol. 33 2012 224 230
81. K.M. Knudson, S.E. Hamilton, M.A. Daniels, S.C. Jameson, and E. Teixeiro Cutting edge: The signals for the generation of T cell memory are qualitatively different depending on TCR ligand strength J. Immunol. 191 2013 5797 5801
82. E.H. Kim, and M. Suresh Role of PI3K/Akt signaling in memory CD8 T cell differentiation Front. Immunol. 4 2013 20
83. S. Kim, K. Jee, D. Kim, H. Koh, and J. Chung Cyclic AMP inhibits Akt activity by blocking the membrane localization of PDK1 J. Biol. Chem. 276 2001 12864 12870
84. J.G. Crompton, M. Sukumar, R. Roychoudhuri, D. Clever, A. Gros, R.L. Eil, E. Tran, K. Hanada, Z. Yu, D.C. Palmer, S.P. Kerkar, R.D. Michalek, T. Upham, A. Leonardi, N. Acquavella, E. Wang, F.M. Marincola, L. Gattinoni, P. Muranski, M.S. Sundrud, C.A. Klebanoff, S.A. Rosenberg, D.T. Fearon, and N.P. Restifo Akt inhibition enhances expansion of potent tumor-specific lymphocytes with memory cell characteristics Cancer Res. 75 2015 296 305
85. A.N. Macintyre, D. Finlay, G. Preston, L.V. Sinclair, C.M. Waugh, P. Tamas, C. Feijoo, K. Okkenhaug, and D.A. Cantrell Protein kinase B controls transcriptional programs that direct cytotoxic T cell fate but is dispensable for T cell metabolism Immunity 34 2011 224 236
86. T.W. Hand, W. Cui, Y.W. Jung, E. Sefik, N.S. Joshi, A. Chandele, Y. Liu, and S.M. Kaech Differential effects of STAT5 and PI3K/AKT signaling on effector and memory CD8 T-cell survival Proc. Natl. Acad. Sci. U.S.A. 107 2010 16601 16606
87. E.H. Kim, J.A. Sullivan, E.H. Plisch, M.M. Tejera, A. Jatzek, K.Y. Choi, and M. Suresh Signal integration by Akt regulates CD8 T cell effector and memory differentiation J. Immunol. 188 2012 4305 4314
88. C. Cekic, D. Sag, Y. Li, D. Theodorescu, R.M. Strieter, and J. Linden Adenosine A2B receptor blockade slows growth of bladder and breast tumors J. Immunol. 188 2012 198 205
89. C. Gouttefangeas, I. Mansur, M. Schmid, H. Dastot, C. Gelin, G. Mahouy, L. Boumsell, and A. Bensussan The CD39 molecule defines distinct cytotoxic subsets within alloactivated human CD8-positive cells Eur. J. Immunol. 22 1992 2681 2685
90. I. Toth, A.Q. Le, P. Hartjen, A. Thomssen, V. Matzat, C. Lehmann, C. Scheurich, C. Beisel, P. Busch, O. Degen, A.W. Lohse, T. Eiermann, G. Fatkenheuer, D. Meyer-Olson, M. Bockhorn, J. Hauber, J. van Lunzen, and J. Schulze Zur Wiesch Decreased frequency of CD73+CD8+ T cells of HIV-infected patients correlates with immune activation and T cell exhaustion J. Leukoc. Biol. 94 2013 551 561