Tuning IL-2 signaling by ADP-ribosylation of CD25

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Teege, Sophie ^a   Hann, Alexander ^a   Miksiewicz, Maria ^a   MacMillan, Cary ^a   Rissiek, Björn ^a   Buck, Friedrich ^a   Menzel, Stephan ^a   Nissen, Marion ^a   Bannas, Peter ^a   Haag, Friedrich ^a   Boyer, Olivier ^b,c,d   Seman, Michel ^b,c   Adriouch, Sahil ^b,c   Koch Nolte, Friedrich ^a,b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF ROUEN   (France)

^c faculté mixte de médecine et de pharmacie de Rouen   (France)

^d ROUEN UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; ADP-RIBOSYLARGININE; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; STAT5 PROTEIN;

ANALOGS AND DERIVATIVES; ANIMAL; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; MOUSE; PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION;

ADENOSINE DIPHOSPHATE RIBOSE; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; HEK293 CELLS; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY;

EID: 84924366068     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08959     Document Type: Article

References (55)

1. Sakaguchi, S. Naturally arising Foxp3-expressing CD251CD41regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 6, 345-352 (2005).
2. Malek, T. R. & Castro, I. Interleukin-2 receptor signaling: at the interface between tolerance and immunity. Immunity 33, 153-165 (2010).
3. Bluestone, J. A. The yin and yang of interleukin-2-mediated immunotherapy. N Engl J Med 365, 2129-2131 (2011).
4. Boyman, O. & Sprent, J. The role of interleukin-2 during homeostasis and activation of the immune system. Nat Rev Immunol 12, 180-190 (2012).
5. Matko, J. et al. GPI-microdomains (membrane rafts) and signaling of the multichain interleukin-2 receptor in human lymphoma/leukemia T cell lines. Eur J Biochem 269, 1199-1208 (2002).
6. Wang, X., Rickert, M. & Garcia, K. C. Structure of the quaternary complex of interleukin-2 with its alpha, beta, and gammac receptors. Science 310, 1159-1163 (2005).
7. Stauber, D. J., Debler, E. W., Horton, P. A., Smith, K. A. & Wilson, I. A. Crystal structure of the IL-2 signaling complex: paradigm for a heterotrimeric cytokine receptor. Proc Natl Acad Sci USA 103, 2788-2793 (2006).
8. Marmor, M. D.&Julius, M. Role for lipid rafts in regulating interleukin-2 receptor signaling. Blood 98, 1489-1497 (2001).
9. Kovanen, P. E. & Leonard, W. J. Cytokines and immunodeficiency diseases: critical roles of the gamma(c)-dependent cytokines interleukins 2, 4, 7, 9, 15, and 21, and their signaling pathways. Immunol Rev 202, 67-83 (2004).
10. Nelson, B. H., Lord, J. D. & Greenberg, P. D. Cytoplasmic domains of the interleukin-2 receptor beta and gamma chains mediate the signal for T-cell proliferation. Nature 369, 333-336 (1994).
11. Bensinger, S. J. et al. Distinct IL-2 receptor signaling pattern in CD41CD251 regulatory T cells. J Immunol 172, 5287-5296 (2004).
12. Burchill, M. A., Yang, J., Vogtenhuber, C., Blazar, B. R. & Farrar, M. A. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp31 regulatory T cells. J Immunol 178, 280-290 (2007).
13. Nouze, C., Pasquet, L. & van Meerwijk, J. P. In vitro expansion of alloantigenspecific regulatory T cells and their use in prevention of allograft rejection. Methods Mol Biol 707, 187-196 (2011).
14. Fontenot, J. D., Rasmussen, J. P., Gavin, M. A. & Rudensky, A. Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol 6, 1142-1151 (2005).
15. Setoguchi, R.,Hori, S., Takahashi, T. & Sakaguchi, S.Homeostatic maintenance of natural Foxp3(1) CD25(1) CD4(1) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 201, 723-735 (2005).
16. Busse, D. et al.Competing feedback loops shape IL-2 signaling between helper and regulatory T lymphocytes in cellularmicroenvironments. Proc Natl Acad SciUS A 107, 3058-3063 (2010).
17. Grinberg-Bleyer, Y. et al. IL-2 reverses established type 1 diabetes inNODmice by a local effect on pancreatic regulatory T cells. J Exp Med 207, 1871-1878 (2011).
18. Tang, Q. et al. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 28, 687-697 (2008).
19. Koreth, J. et al. Interleukin-2 and regulatory T cells in graft-versus-host disease. N Engl J Med 365, 2055-2066 (2011).
20. Saadoun, D. et al. Regulatory T-cell responses to low-dose interleukin-2 in HCVinduced vasculitis. N Engl J Med 365, 2067-2077 (2011).
21. Hartemann, A. et al. Low-dose interleukin 2 in patients with type 1 diabetes: a phase 1/2 randomised, double-blind, placebo-controlled trial. Lancet Diabetes Endocrinol 1, 295-305 (2013).
22. Kim, M. G. et al. IL-2/anti-IL-2 complex attenuates renal ischemia-reperfusion injury through expansion of regulatory T cells. J Am Soc Nephrol 24, 1529-1536 (2013).
23. Letourneau, S. et al. IL-2/anti-IL-2 antibody complexes show strong biological activity by avoiding interaction with IL-2 receptor alpha subunit CD25. Proc Natl Acad Sci USA 107, 2171-2176 (2010).
24. Boyman, O., Kovar, M., Rubinstein, M. P., Surh, C. D. & Sprent, J. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 311, 1924-1927 (2006).
25. Kamimura, D. & Bevan, M. J. Naive CD81 T cells differentiate into protective memory-like cells after IL-2 anti IL-2 complex treatment in vivo. J Exp Med 204, 1803-1812 (2007).
26. Webster, K. E. et al. In vivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of islet allografts without immunosuppression. J Exp Med 206, 751-760 (2009).
27. Krieg, C., Letourneau, S., Pantaleo, G. & Boyman, O. Improved IL-2 immunotherapy by selective stimulation of IL-2 receptors on lymphocytes and endothelial cells. Proc Natl Acad Sci USA 107, 11906-11911 (2010).
28. Boyman, O. et al. Selectively expanding subsets of T cells in mice by injection of interleukin-2/antibody complexes: implications for transplantation tolerance. Transplant Proc 44, 1032-1034 (2012).
29. Hottiger, M. O., Hassa, P. O., Luscher, B., Schuler, H. & Koch-Nolte, F. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 35, 208-219 (2010).
30. Hottiger, M. O. et al. Progress in the function and regulation of ADP-Ribosylation. Sci Signal 4, mr5 (2011).
31. Vitiello, L., Gorini, S., Rosano, G. & la Sala, A. Immunoregulation through extracellular nucleotides. Blood 120, 511-518 (2012).
32. Haag, F. et al. Extracellular NAD and ATP: Partners in immune cell modulation. Purinergic Signal 3, 71-81 (2007).
33. Koch-Nolte, F., Fischer, S., Haag, F. & Ziegler, M. Compartmentation of NAD1-dependent signalling. FEBS Lett 585, 1651-1656 (2011).
34. Deaglio, S. & Robson, S. C. Ectonucleotidases as regulators of purinergic signaling in thrombosis, inflammation, and immunity. Adv Pharmacol 61, 301-332 (2011).
35. Bannas, P. et al. Activity and specificity of toxin-related mouse T cell ecto-ADPribosyltransferase ART2.2 depends on its association with lipid rafts. Blood 105, 3663-3670 (2005).
36. Aswad, F., Kawamura, H. & Dennert, G. High sensitivity of CD41CD251 regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: a role for P2X7 receptors. J Immunol 175, 3075-3083 (2005).
37. Hubert, S. et al. Extracellular NAD1 shapes the Foxp31 regulatory T cell compartment through the ART2-P2X7 pathway. J Exp Med 207, 2561-2568 (2010).
38. Adriouch, S. et al. ADP-ribosylation at R125 gates the P2X7 ion channel by presenting a covalent ligand to its nucleotide binding site. Faseb J 22, 861-869 (2008).
39. Paone, G. et al. ADP-ribosyltransferase-specific modification of human neutrophil peptide-1. J Biol Chem 281, 17054-17060 (2006).
40. Laing, S., Unger, M., Koch-Nolte, F. & Haag, F. ADP-ribosylation of arginine. Amino Acids 41, 257-269 (2011).
41. Koch-Nolte, F. et al. Single domain antibodies from llama effectively and specifically block T cell ecto-ADP-ribosyltransferase ART2.2 in vivo. Faseb J 21, 3490-3498 (2007).
42. Lahl, K. et al. Selective depletion of Foxp31regulatory T cells induces a scurfy-like disease. J Exp Med 204, 57-63 (2007).
43. Robb, R. J., Rusk, C. M. & Neeper, M. P. Structure-function relationships for the interleukin 2 receptor: location of ligand and antibody binding sites on the Tac receptor chain by mutational analysis. Proc Natl Acad Sci USA 85, 5654-5658 (1988).
44. Scheuplein, F. et al. NAD1 and ATP released from injured cells induce P2X7-dependent shedding of CD62L and externalization of phosphatidylserine by murine T cells. J Immunol 182, 2898-2908 (2009).
45. Patton, D. T., Wilson, M. D., Rowan, W. C., Soond, D. R. & Okkenhaug, K. The PI3K p110delta regulates expression of CD38 on regulatory T cells. PLoS One 6, e17359 (2011).
46. Krebs, C. et al. CD38 controls ADP-ribosyltransferase-2-catalyzed ADPribosylation of T cell surface proteins. J Immunol 174, 3298-3305 (2005).
47. Rissiek, B.,Danquah, W.,Haag, F.&Koch-Nolte, F. Technical Advance: a new cell preparation strategy that greatly improves the yield of vital and functional Tregs and NKT cells. J Leukoc Biol 95, 543-549 (2014).
48. Pandiyan, P., Zheng, L., Ishihara, S., Reed, J. & Lenardo, M. J. CD41CD251Foxp31 regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD41 T cells. Nat Immunol 8, 1353-1362 (2007).
49. Churlaud, G. et al. Sustained stimulation and expansion of Tregs by IL2 control autoimmunity without impairing immune responses to infection, vaccination and cancer. Clin Immunol 151, 114-126 (2014).
50. Adriouch, S. et al. NAD1 released during inflammation participates in T cell homeostasis by inducing ART2-mediated death of naive T cells in vivo. J Immunol 179, 186-194 (2007).
51. Uchiyama, T., Broder, S. & Waldmann, T. A. A monoclonal antibody (anti-Tac) reactive with activated and functionally mature human T cells. I. Production of anti-Tac monoclonal antibody and distribution of Tac (1) cells. J Immunol 126, 1393-1397 (1981).
52. Kahl, S. et al. Metalloprotease-mediated shedding of enzymatically active mouse ecto-ADP-ribosyltransferase ART2.2 upon T cell activation. J Immunol 165, 4463-4469 (2000).
53. Ohlrogge, W. et al. Generation and characterization of ecto-ADPribosyltransferase ART2.1/ART2.2-deficient mice. Mol Cell Biol 22, 7535-7542 (2002).
54. Labasi, J. M. et al. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J Immunol 168, 6436-6445 (2002).
55. Koch-Nolte, F. et al. A new monoclonal antibody detects a developmentally regulated mouse ecto ADP-ribosyltransferase on T cells: subset distribution, inbred strain variation, and modulation upon T cell activation. J Immunol 163, 6014-6022 (1999).