Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: Hydrolysis of extracellular ATP and immune suppression

Blood

Volumn 110, Issue 4, 2007, Pages 1225-1232

  Borsellino, Giovanna ^a   Kleinewietfeld, Markus ^b   Di Mitri, Diletta ^a   Sternjak, Alexander ^b   Diamantini, Adamo ^a   Giometto, Raffaella ^a   Höpner, Sabine ^b   Centonze, Diego ^c   Bernardi, Giorgio ^c   Dell'Acqua, Maria Luisa ^d   Rossini, Paolo Maria ^d   Battistini, Luca ^a   Rötzschke, Olaf ^b   Falk, Kirsten ^b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d UNIVERSITY CAMPUS BIO MEDICO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD39 ANTIGEN; PURINE P2 RECEPTOR; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ADULT; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL MATURATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DENDRITIC CELL; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOSUPPRESSIVE TREATMENT; MALE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

EID: 34547098277     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-12-064527     Document Type: Article

References (47)

1. Burnstock G. Overview: purinergic mechanisms. Ann N Y Acad Sci. 1990;603:1-17.
2. Burnstock G. Introduction: P2 receptors. Curr Top Med Chem. 2004;4:793-803.
3. Volonte C, Amadio S, Cavaliere F, D'Ambrosi N, Vacca F, Bernardi G. Extracellular ATP and neurodegeneration. Curr Drug Targets CNS Neurol Disord. 2003;2:403-412.
4. la Sala A, Ferrari D, Corinti S, Cavani A, Di Virgilio F, Girolomoni G. Extracellular ATP induces a distorted maturation of dendritic cells and inhibits their capacity to initiate Th1 responses. J Immunol. 2001;166:1611-1617.
5. Khakh BS, North RA. P2X receptors as cell-surface ATP sensors in health and disease. Nature. 2006;442:527-532.
6. Di Virgilio F, Chiozzi P, Ferrari D, et al. Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood. 2001;97:587-600.
7. Ferrari D, Chiozzi P, Falzoni S, Hanau S, Di Virgilio F. Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J Exp Med. 1997;185:579-582.
8. MacKenzie A, Wilson HL, Kiss-Toth E, Dower SK, North RA, Surprenant A. Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity. 2001;15:825-835.
9. Idzko M, Dichmann S, Ferrari D, et al. Nucleotides induce chemotaxis and actin polymerization in immature but not mature human dendritic cells via activation of pertussis toxin-sensitive P2y receptors. Blood. 2002;100:925-932.
10. Gallucci S, Lolkema M, Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat Med. 1999;5:1249-1255.
11. Matzinger P. The danger model: a renewed sense of self. Science. 2002;296:301-305.
12. Beigi RD, Kertesy SB, Aquilina G, Dubyak GR. Oxidized ATP (oATP) attenuates proinflammatory signaling via P2 receptor-independent mechanisms. Br J Pharmacol. 2003;140:507-519.
13. Canaday DH, Beigi R, Silver RF, Harding CV, Boom WH, Dubyak GR. ATP and control of intracellular growth of mycobacteria by T cells. Infect Immun. 2002;70:6456-6459.
14. Wilkin F, Duhant X, Bruyns C, Suarez-Huerta N, Boeynaems JM, Robaye B. The P2Y11 receptor mediates the ATP-induced maturation of human monocyte-derived dendritic cells. J Immunol. 2001;166:7172-7177.
15. Hanley PJ, Musset B, Renigunta V, et al. Extracellular ATP induces oscillations of intracellular Ca2+ and membrane potential and promotes transcription of IL-6 in macrophages. Proc Natl Acad Sci U S A. 2004;101:9479-9484.
16. Zimmermann H. Biochemistry, localization and functional roles of ecto-nucleotidases in the nervous system. Prog Neurobiol. 1996;49:589-618.
17. Robson SC, Sevigny J, Zimmermann H. The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance. Purinergic Signal. 2006;2:409-430.
18. Mizumoto N, Kumamoto T, Robson SC, et al. CD39 is the dominant Langerhans cell-associated ecto-NTPDase: modulatory roles in inflammation and immune responsiveness. Nat Med. 2002;8:358-365.
19. 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.
20. Airas L, Hellman J, Salmi M, et al. CD73 is involved in lymphocyte binding to the endothelium: characterization of lymphocyte-vascular adhesion protein 2 identifies it as CD73. J Exp Med. 1995;182:1603-1608.
21. Thiel M, Caldwell CC, Sitkovsky MV. The critical role of adenosine A2A receptors in downregulation of inflammation and immunity in the pathogenesis of infectious diseases. Microbes Infect. 2003;5:515-526.
22. Maliszewski CR, Delespesse GJ, Schoenborn MA, et al. The CD39 lymphoid cell activation antigen. Molecular cloning and structural characterization. J Immunol. 1994;153:3574-3583.
23. O'Garra A, Vieira P. Regulatory T cells and mechanisms of immune system control. Nat Med. 2004;10:801-805.
24. Enjyoji K, Sevigny J, Lin Y, et al. Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat Med. 1999;5:1010-1017.
25. Sevigny J, Sundberg C, Braun N, et al. Differential catalytic properties and vascular topography of murine nucleoside triphosphate diphosphohydrolase 1 (NTPDase1) and NTPDase2 have implications for thromboregulation. Blood. 2002;99:2801-2809.
26. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299:1057-1061.
27. Crack BE, Pollard CE, Beukers MW, et al. Pharmacological and biochemical analysis of FPL 67156, a novel, selective inhibitor of ecto-ATPase. Br J Pharmacol. 1995;114:475-481.
28. Iqbal J, Vollmayer P, Braun N, Zimmermann H, Müller CE. A capillary electrophoresis method for the characterization of ecto-nucleoside triphosphate diphosphohydrolases (NTPDases) and the analysis of inhibitors by in-capillary enzymatic microreaction. Purinergic Signal. 2005;1:349-358.
29. Chow SC, Kass GE, Orrenius S. Purines and their roles in apoptosis. Neuropharmacology. 1997;36:1149-1156.
30. Aswad F, Kawamura H, Dennert G. High sensitivity of CD4+CD25+ regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: a role for P2X7 receptors. J Immunol. 2005;175:3075-3083.
31. Viglietta V, Baecher-Allan C, Weiner HL, Hafler DA. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis. J Exp Med. 2004;199:971-979.
32. Kleinewietfeld M, Puentes F, Borsellino G, Battistini L, Rotzschke O, Falk K. CCR6 expression defines regulatory effector/memory-like cells within the CD25(+)CD4+ T-cell subset. Blood. 2005;105:2877-2886.
33. Lim HW, Broxmeyer HE, Kim CH. Regulation of trafficking receptor expression in human forkhead box P3+ regulatory T cells. J Immunol. 2006;177:840-851.
34. Varona R, Cadenas V, Lozano M, et al. CCR6 regulates the function of alloreactive and regulatory CD4+ T cells during acute graft-versus-host disease. Leuk Lymphoma. 2006;47:1469-1476.
35. Baecher-Allan C, Wolf E, Hafler DA. MHC class II expression identifies functionally distinct human regulatory T cells. J Immunol. 2006;176:4622-4631.
36. Khoury SJ, Guttmann CR, Orav EJ, Kikinis R, Jolesz FA, Weiner HL. Changes in activated T cells in the blood correlate with disease activity in multiple sclerosis. Arch Neurol. 2000;57:1183-1189.
37. Putheti P, Pettersson A, Soderstrom M, Link H, Huang YM. Circulating CD4+CD25+ T regulatory cells are not altered in multiple sclerosis and unaffected by disease-modulating drugs. J Clin Immunol. 2004;24:155-161.
38. Koziak K, Kaczmarek E, Kittel A, et al. Palmitoylation targets CD39/endothelial ATP diphosphohydrolase to caveolae. J Biol Chem. 2000;275:2057-2062.
39. Papanikolaou A, Papafotika A, Murphy C, et al. Cholesterol-dependent lipid assemblies regulate the activity of the ecto-nucleotidase CD39. J Biol Chem. 2005;280:26406-26414.
40. Wu Y, Sun X, Kaczmarek E, et al. RanBPM associates with CD39 and modulates ecto-nucleotidase activity. Biochem J. 2006;396:23-30.
41. Dieckmann D, Bruett CH, Ploettner H, Lutz MB, Schuler G. Human CD4(+)CD25(+) regulatory, contact-dependent T cells induce interleukin 10-producing, contact-independent type 1-like regulatory T cells [corrected]. J Exp Med. 2002;196:247-253.
42. Imai M, Goepfert C, Kaczmarek E, Robson SC. CD39 modulates IL-1 release from activated endothelial cells. Biochem Biophys Res Commun. 2000;270:272-278.
43. 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;177:2765-2769.
44. 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;177:6780-6786.
45. Huan J, Culbertson N, Spencer L, et al. Decreased FOXP3 levels in multiple sclerosis patients. J Neurosci Res. 2005;81:45-52.
46. Venken K, Hellings N, Hensen K, et al. Secondary progressive in contrast to relapsing-remitting multiple sclerosis patients show a normal CD4+CD25+ regulatory T-cell function and FOXP3 expression. J Neurosci Res. 2006;83:1432-1446.
47. Valencia X, Yarboro C, Illei G, Lipsky PE. Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J Immunol. 2007;178:2579-2588.