Evaluation of the expression and function of the P2X7 receptor and ART1 in human regulatory T-cell subsets

Immunobiology

Volumn 221, Issue 1, 2016, Pages 84-93

  Cortés Garcia, Juan D ^a   López López, Cintya ^b   Cortez Espinosa, Nancy ^a   García Hernández, Mariana H ^c   Guzmán Flores, Juan M ^a   Layseca Espinosa, Esther ^a   Portales Cervantes, Liliana ^a   Portales Pérez, Diana P ^a  

^a UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^b INSTITUTO POTOSINO DE INVESTIGACIÓN CIENTÍFICA Y TECNOLÓGICA   (Mexico)

^c Unit of Medicine Investigation IMSS   (Mexico)

Author keywords

ART1; ATP; CD39; Immune regulation; NAD; P2X7 receptor

Indexed keywords

ADENOSINE A2A RECEPTOR AGONIST; ADENOSINE A2A RECEPTOR ANTAGONIST; ADENOSINE TRIPHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PURINERGIC P2X7 RECEPTOR; 2-(4-(2-CARBOXYETHYL)PHENETHYLAMINO)-5'-N-ETHYLCARBOXAMIDOADENOSINE; 4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; ADENOSINE; ADENOSINE A2 RECEPTOR; ADENOSINE A2 RECEPTOR AGONIST; ADENOSINE A2 RECEPTOR ANTAGONIST; APYRASE; ART1 PROTEIN, HUMAN; CD39 ANTIGEN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; L SELECTIN; LEUKOCYTE ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; P2XR RECEPTOR, HUMAN; PHENETHYLAMINE DERIVATIVE; TRIAZINE DERIVATIVE; TRIAZOLE DERIVATIVE;

ANIMAL CELL; ARTICLE; CD39+ REGULATORY T LYMPHOCYTE; CD39- REGULATORY T LYMPHOCYTE; CD4+ CD25+ CD39+ T LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOMODULATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; T LYMPHOCYTE; ADOLESCENT; ADULT; ANALOGS AND DERIVATIVES; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; MALE; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION;

ADENOSINE; ADENOSINE A2 RECEPTOR AGONISTS; ADENOSINE A2 RECEPTOR ANTAGONISTS; ADENOSINE TRIPHOSPHATE; ADOLESCENT; ADP RIBOSE TRANSFERASES; ADULT; ANTIGENS, CD; APYRASE; CELL DEATH; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION; GPI-LINKED PROTEINS; HUMANS; IMMUNOPHENOTYPING; L-SELECTIN; MALE; NAD; PHENETHYLAMINES; PRIMARY CELL CULTURE; RECEPTORS, ADENOSINE A2; RECEPTORS, PURINERGIC P2X7; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TRIAZINES; TRIAZOLES;

EID: 84946493315     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2015.07.018     Document Type: Article

References (54)

1. Adriouch S., Ohlrogge W., Haag F., Koch-Nolte F., Seman M. Rapid induction of naive T cell apoptosis by ecto-nicotinamide adenine dinucleotide: requirement for mono(ADP-ribosyl) transferase 2 and a downstream effector. J. Immunol. 2001, 167:196-203.
2. Allport J.R., Donnelly L.E., Kefalas P., Lo G., Nunn A., Yadollahi-Farsani M., Rendell N.B., Murray S., Taylor G.W., MacDermot J. A possible role for mono (ADP-ribosyl) transferase in the signalling pathway mediating neutrophil chemotaxis. Br. J. Clin. Pharmacol. 1996, 42:99-106.
3. Aswad F., Dennert G. P2X7 receptor expression levels determine lethal effects of a purine based danger signal in T lymphocytes. Cell Immunol. 2006, 243:58-65.
4. 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.
5. Bartlett R., Stokes L., Sluyter R. The P2X7 receptor channel: recent developments and the use of P2X7 antagonists in models of disease. Pharmacol. Rev. 2014, 66:638-675.
6. Bavec A. Mono-ADP-ribosyltransferase as a potential pharmacological drug target in the GLP-1 based therapy of obesity and diabetes mellitus type 2. Acta Chim. Slov. 2013, 60:237-242.
7. Bortell R., Moss J., McKenna R.C., Rigby M.R., Niedzwiecki D., Stevens L.A., Patton W.A., Mordes J.P., Greiner D.L., Rossini A.A. Nicotinamide adenine dinucleotide (NAD) and its metabolites inhibit T lymphocyte proliferation: role of cell surface NAD glycohydrolase and pyrophosphatase activities. J. Immunol. 2001, 167:2049-2059.
8. Bourgeois C., Okazaki I., Cavanaugh E., Nightingale M., Moss J. Identification of regulatory domains in ADP-ribosyltransferase-1 that determine transferase and NAD glycohydrolase activities. J. Biol. Chem. 2003, 278:26351-26355.
9. Buckner J.H. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat. Rev. Immunol. 2010, 10:849-859.
10. Buckner J.H., Ziegler S.F. Regulating the immune system: the induction of regulatory T cells in the periphery. Arthritis Res. Ther. 2004, 6:215-222.
11. Bulanova E., Budagian V., Orinska Z., Koch-Nolte F., Haag F., Bulfone-Paus S. ATP induces P2X7 receptor-independent cytokine and chemokine expression through P2X1 and P2X3 receptors in murine mast cells. J. Leukoc. Biol. 2009, 85:692-702.
12. Caragnano M., Tortorella P., Bergami A., Ruggieri M., Livrea P., Specchio L.M., Martino G., Trojano M., Furlan R., Avolio C. Monocytes P2X7 purinergic receptor is modulated by glatiramer acetate in multiple sclerosis. J. Neuroimmunol. 2012, 245:93-97.
13. Clifford E.E., Parker K., Humphreys B.D., Kertesy S.B., Dubyak G.R. The P2X1 receptor, an adenosine triphosphate-gated cation channel, is expressed in human platelets but not in human blood leukocytes. Blood 1998, 91:3172-3181.
14. Corda D., Di G.M. Functional aspects of protein mono-ADP-ribosylation. EMBO J. 2003, 22:1953-1958.
15. Dalla L.D., Di M.D., Bergami A., Centonze D., Gasperini C., Grasso M.G., Galgani S., Martinelli V., Comi G., Avolio C., Martino G., Borsellino G., Sallusto F., Battistini L., Furlan R. T regulatory cells are markers of disease activity in multiple sclerosis patients. PLoS One 2011, 6:e21386.
16. Del V.M., Balducci E. Mono ADP-ribosylation inhibitors prevent inflammatory cytokine release in alveolar epithelial cells. Mol. Cell Biochem. 2008, 310:77-83.
17. Dwyer K.M., Hanidziar D., Putheti P., Hill P.A., Pommey S., McRae J.L., Winterhalter A., Doherty G., Deaglio S., Koulmanda M., Gao W., Robson S.C., Strom T.B. Expression of CD39 by human peripheral blood CD4+ CD25+ T cells denotes a regulatory memory phenotype. Am. J. Transplant. 2010, 10:2410-2420.
18. Fletcher J.M., Lonergan R., Costelloe L., Kinsella K., Moran B., O'Farrelly C., Tubridy N., Mills K.H. CD39+Foxp3+ regulatory T Cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J. Immunol. 2009, 183:7602-7610.
19. Garavaglia S., Bruzzone S., Cassani C., Canella L., Allegrone G., Sturla L., Mannino E., Millo E., De F.A., Rizzi M. The high-resolution crystal structure of periplasmic Haemophilus influenzae NAD nucleotidase reveals a novel enzymatic function of human CD73 related to NAD metabolism. Biochem. J. 2012, 441:131-141.
20. Garcia-Hernandez M.H., Portales-Cervantes L., Cortez-Espinosa N., Vargas-Morales J.M., Fritche Salazar J.F., Rivera-Lopez E., Rodriguez-Rivera J.G., Quezada-Calvillo R., Portales-Perez D.P. Expression and function of P2X(7) receptor and CD39/Entpd1 in patients with type 2 diabetes and their association with biochemical parameters. Cell Immunol. 2011, 269:135-143.
21. Glowacki G., Braren R., Firner K., Nissen M., Kuhl M., Reche P., Bazan F., Cetkovic-Cvrlje M., Leiter E., Haag F., Koch-Nolte F. The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Sci. 2002, 11:1657-1670.
22. Gotoh K., Nemoto E., Kanaya S., Shimauchi H. Extracellular beta-NAD(+) inhibits interleukin-1-induced matrix metalloproteinase-1 and -3 expression on human gingival fibroblasts. Connect. Tissue Res. 2013, 54:204-209.
23. Grahnert A., Friedrich M., Pfister M., Haag F., Koch-Nolte F., Hauschildt S. Mono-ADP-ribosyltransferases in human monocytes: regulation by lipopolysaccharide. Biochem. J. 2002, 362:717-723.
24. Haag F., Adriouch S., Brass A., Jung C., Moller S., Scheuplein F., Bannas P., Seman M., Koch-Nolte F. Extracellular NAD and ATP: partners in immune cell modulation. Purinergic Signal. 2007, 3:71-81.
25. Hong S., Schwarz N., Brass A., Seman M., Haag F., Koch-Nolte F., Schilling W.P., Dubyak G.R. Differential regulation of P2X7 receptor activation by extracellular nicotinamide adenine dinucleotide and ecto-ADP-ribosyltransferases in murine macrophages and T cells. J. Immunol. 2009, 183:578-592.
26. Hubert S., Rissiek B., Klages K., Huehn J., Sparwasser T., Haag F., Koch-Nolte F., Boyer O., Seman M., Adriouch S. Extracellular NAD+ shapes the Foxp3+ regulatory T cell compartment through the ART2-P2X7 pathway. J. Exp. Med. 2010, 207:2561-2568.
27. Jacob F., Perez N.C., Bachert C., Van C.K. Purinergic signaling in inflammatory cells: P2 receptor expression, functional effects, and modulation of inflammatory responses. Purinergic Signal. 2013, 9:285-306.
28. Keystone E.C., Wang M.M., Layton M., Hollis S., McInnes I.B. Clinical evaluation of the efficacy of the P2X7 purinergic receptor antagonist AZD9056 on the signs and symptoms of rheumatoid arthritis in patients with active disease despite treatment with methotrexate or sulphasalazine. Ann. Rheum. Dis. 2012, 71:1630-1635.
29. Klein C., Grahnert A., Abdelrahman A., Muller C.E., Hauschildt S. Extracellular NAD(+) induces a rise in [Ca(2+)](i) in activated human monocytes via engagement of P2Y(1) and P2Y(11) receptors. Cell Calcium 2009, 46:263-272.
30. Krebs C., Adriouch S., Braasch F., Koestner W., Leiter E.H., Seman M., Lund F.E., Oppenheimer N., Haag F., Koch-Nolte F. CD38 controls ADP-ribosyltransferase-2-catalyzed ADP-ribosylation of T cell surface proteins. J. Immunol. 2005, 174:3298-3305.
31. Laing S., Unger M., Koch-Nolte F., Haag F. ADP-ribosylation of arginine. Amino Acids 2011, 41:257-269.
32. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
33. Manohar M., Hirsh M.I., Chen Y., Woehrle T., Karande A.A., Junger W.G. ATP release and autocrine signaling through P2X4 receptors regulate gammadelta T cell activation. J. Leukoc. Biol. 2012, 92:787-794.
34. Nikolova M., Carriere M., Jenabian M.A., Limou S., Younas M., Kok A., Hue S., Seddiki N., Hulin A., Delaneau O., Schuitemaker H., Herbeck J.T., Mullins J.I., Muhtarova M., Bensussan A., Zagury J.F., Lelievre J.D., Levy Y. CD39/adenosine pathway is involved in AIDS progression. PLoS Pathog. 2011, 7:e1002110.
35. Ohkura N., Kitagawa Y., Sakaguchi S. Development and maintenance of regulatory T cells. Immunity 2013, 38:414-423.
36. Okamoto S., Azhipa O., Yu Y., Russo E., Dennert G. Expression of ADP-ribosyltransferase on normal T lymphocytes and effects of nicotinamide adenine dinucleotide on their function. J. Immunol. 1998, 160:4190-4198.
37. Paone G., Stevens L.A., Levine R.L., Bourgeois C., Steagall W.K., Gochuico B.R., Moss J. ADP-ribosyltransferase-specific modification of human neutrophil peptide-1. J. Biol. Chem. 2006, 281:17054-17060.
38. Portales-Cervantes L., Nino-Moreno P., Salgado-Bustamante M., Garcia-Hernandez M.H., Baranda-Candido L., Reynaga-Hernandez E., Barajas-Lopez C., Gonzalez-Amaro R., Portales-Perez D.P. The His155Tyr (489C>T) single nucleotide polymorphism of P2RX7 gene confers an enhanced function of P2X7 receptor in immune cells from patients with rheumatoid arthritis. Cell Immunol. 2012, 276:168-175.
39. Rizzo R., Ferrari D., Melchiorri L., Stignani M., Gulinelli S., Baricordi O.R., Di V.F. Extracellular ATP acting at the P2X7 receptor inhibits secretion of soluble HLA-G from human monocytes. J. Immunol. 2009, 183:4302-4311.
40. Sakaguchi S., Vignali D.A., Rudensky A.Y., Niec R.E., Waldmann H. The plasticity and stability of regulatory T cells. Nat. Rev. Immunol. 2013, 13:461-467.
41. Schenk U., Frascoli M., Proietti M., Geffers R., Traggiai E., Buer J., Ricordi C., Westendorf A.M., Grassi F. ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Sci. Signal. 2011, 4:ra12.
42. Scheuplein F., Adriouch S., Glowacki G., Haag F., Seman M., Koch-Nolte F. Triggering of T-cell apoptosis by toxin-related ecto-ADP-ribosyltransferase ART2. Ann. N. Y. Acad. Sci. 2003, 1010:296-299. 296-9.
43. Scheuplein F., Schwarz N., Adriouch S., Krebs C., Bannas P., Rissiek B., Seman M., Haag F., Koch-Nolte F. NAD+ and ATP released from injured cells induce P2X7-dependent shedding of CD62L and externalization of phosphatidylserine by murine T cells. J. Immunol. 2009, 182:2898-2908.
44. Schilling E., Hauschildt S. Extracellular ATP induces P2X7-dependent nicotinamide phosphoribosyltransferase release in LPS-activated human monocytes. Innate Immun. 2012, 18:738-744.
45. Schuler P.J., Schilling B., Harasymczuk M., Hoffmann T., Johnson J., Lang S., Whiteside T.L. Phenotypic and functional characteristics of ATP-hydrolysing CD4(+) CD39(+) FOXP3(+) and CD4(+) CD39(+) FOXP3(neg) T-cell subsets in patients with cancer. Eur. J. Immunol. 2012, 42:1876-1885.
46. Seman M., Adriouch S., Scheuplein F., Krebs C., Freese D., Glowacki G., Deterre P., Haag F., Koch-Nolte F. NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 2003, 19:571-582.
47. Stock T.C., Bloom B.J., Wei N., Ishaq S., Park W., Wang X., Gupta P., Mebus C.A. Efficacy and safety of CE-224,535, an antagonist of P2X7 receptor, in treatment of patients with rheumatoid arthritis inadequately controlled by methotrexate. J. Rheumatol. 2012, 39:720-727.
48. Tang Y., Jiang L., Zheng Y., Ni B., Wu Y. Expression of CD39 on FoxP3+ T regulatory cells correlates with progression of HBV infection. BMC Immunol. 2012, 13:17.
49. Trabanelli S., Ocadlikova D., Gulinelli S., Curti A., Salvestrini V., Vieira R.P., Idzko M., Di V.F., Ferrari D., Lemoli R.M. Extracellular ATP exerts opposite effects on activated and regulatory CD4+ T cells via purinergic P2 receptor activation. J. Immunol. 2012, 189:1303-1310.
50. Wang J., Nemoto E., Kots A.Y., Kaslow H.R., Dennert G. Regulation of cytotoxic T cells by ecto-nicotinamide adenine dinucleotide (NAD) correlates with cell surface GPI-anchored/arginine ADP-ribosyltransferase. J. Immunol. 1994, 153:4048-4058.
51. Weng B., Thompson W.C., Kim H.J., Levine R.L., Moss J. Modification of the ADP-ribosyltransferase and NAD glycohydrolase activities of a mammalian transferase (ADP-ribosyltransferase 5) by auto-ADP-ribosylation. J. Biol. Chem. 1999, 274:31797-31803.
52. Woehrle T., Yip L., Elkhal A., Sumi Y., Chen Y., Yao Y., Insel P.A., Junger W.G. Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood. 2010, 116:3475-3484.
53. Xu, H., Liang, SD., 2013. [Effect of P2X7 receptor on inflammatory diseases and its mechanism]. Sheng Li Xue Bao. 65, 244-252.
54. Xu X.J., Boumechache M., Robinson L.E., Marschall V., Gorecki D.C., Masin M., Murrell-Lagnado R.D. Splice variants of the P2X7 receptor reveal differential agonist dependence and functional coupling with pannexin-1. J. Cell Sci. 2012, 125:3776-3789.