Ectonucleotidase CD38 Demarcates Regulatory, Memory-Like CD8+ T Cells with IFN-γ-Mediated Suppressor Activities

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Bahri, Rajia ^a   Bollinger, Annalena ^a   Bollinger, Thomas ^b   Orinska, Zane ^a   Bulfone Paus, Silvia ^a,c  

^a RESEARCH CENTER BORSTEL   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD38 ANTIGEN; ECTONUCLEOTIDASE; GAMMA INTERFERON; GRANZYME B; HERMES ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 2 RECEPTOR BETA; L SELECTIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL CONTACT; CELL EXPANSION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME RELEASE; FEMALE; IMMUNE RESPONSE; IMMUNOPHENOTYPING; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; MEMORY T LYMPHOCYTE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; REGULATORY T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD38; CD8-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FLOW CYTOMETRY; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; INTERFERON-GAMMA; INTERLEUKIN-15; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; NUCLEOTIDASES; T-LYMPHOCYTES, REGULATORY;

MURINAE; MUS;

EID: 84866463384     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045234     Document Type: Article

References (53)

1. Wei S, Kryczek I, Zou L, Daniel B, Cheng P, et al. (2005) Plasmacytoid dendritic cells induce CD8+ regulatory T cells in human ovarian carcinoma. Cancer Res 65: 5020-5026.
2. Najafian N, Chitnis T, Salama AD, Zhu B, Benou C, et al. (2003) Regulatory functions of CD8+CD28- T cells in an autoimmune disease model. J Clin Invest 112: 1037-1048.
3. Garba ML, Pilcher CD, Bingham AL, Eron J, Frelinger JA, (2002) HIV antigens can induce TGF-beta(1)-producing immunoregulatory CD8+ T cells. J Immunol 168: 2247-2254.
4. Smith TR, Kumar V, (2008) Revival of CD8+ Treg-mediated suppression. Trends Immunol 29: 337-342.
5. Chang CC, Ciubotariu R, Manavalan JS, Yuan J, Colovai AI, et al. (2002) Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 3: 237-243.
6. Mahic M, Henjum K, Yaqub S, Bjornbeth BA, Torgersen KM, et al. (2008) Generation of highly suppressive adaptive CD8(+)CD25(+)FOXP3(+) regulatory T cells by continuous antigen stimulation. Eur J Immunol 38: 640-646.
7. Endharti AT, Rifa IM, Shi Z, Fukuoka Y, Nakahara Y, et al. (2005) Cutting edge: CD8+CD122+ regulatory T cells produce IL-10 to suppress IFN-gamma production and proliferation of CD8+ T cells. J Immunol 175: 7093-7097.
8. Scotto L, Naiyer AJ, Galluzzo S, Rossi P, Manavalan JS, et al. (2004) Overlap between molecular markers expressed by naturally occurring CD4+CD25+ regulatory T cells and antigen specific CD4+CD25+ and CD8+CD28- T suppressor cells. Hum Immunol 65: 1297-1306.
9. Ben-David H, Sharabi A, Dayan M, Sela M, Mozes E, (2007) The role of CD8+CD28 regulatory cells in suppressing myasthenia gravis-associated responses by a dual altered peptide ligand. Proc Natl Acad Sci U S A 104: 17459-17464.
10. Hadley GA, Bartlett ST, Via CS, Rostapshova EA, Moainie S, (1997) The epithelial cell-specific integrin, CD103 (alpha E integrin), defines a novel subset of alloreactive CD8+ CTL. J Immunol 159: 3748-3756.
11. Koch SD, Uss E, van Lier RA, ten Berge IJ, (2008) Alloantigen-induced regulatory CD8+CD103+ T cells. Hum Immunol 69: 737-744.
12. Myers L, Croft M, Kwon BS, Mittler RS, Vella AT, (2005) Peptide-specific CD8 T regulatory cells use IFN-gamma to elaborate TGF-beta-based suppression. J Immunol 174: 7625-7632.
13. Kim HJ, Verbinnen B, Tang X, Lu L, Cantor H, (2010) Inhibition of follicular T-helper cells by CD8(+) regulatory T cells is essential for self tolerance. Nature 467: 328-332.
14. Tennakoon DK, Mehta RS, Ortega SB, Bhoj V, Racke MK, et al. (2006) Therapeutic induction of regulatory, cytotoxic CD8+ T cells in multiple sclerosis. J Immunol 176: 7119-7129.
15. Kim HJ, Wang X, Radfar S, Sproule TJ, Roopenian DC, et al. (2011) CD8+ T regulatory cells express the Ly49 Class I MHC receptor and are defective in autoimmune prone B6-Yaa mice. Proc Natl Acad Sci U S A 108: 2010-2015.
16. Bienvenu B, Martin B, Auffray C, Cordier C, Becourt C, et al. (2005) Peripheral CD8+CD25+ T lymphocytes from MHC class II-deficient mice exhibit regulatory activity. J Immunol 175: 246-253.
17. Beeston T, Smith TR, Maricic I, Tang X, Kumar V, (2010) Involvement of IFN-gamma and perforin, but not Fas/FasL interactions in regulatory T cell-mediated suppression of experimental autoimmune encephalomyelitis. J Neuroimmunol 229: 91-97.
18. Shi Z, Okuno Y, Rifa'i M, Endharti AT, Akane K, et al. (2009) Human CD8+CXCR3+ T cells have the same function as murine CD8+CD122+ Treg. Eur J Immunol 39: 2106-2119.
19. Lee YH, Ishida Y, Rifa'i M, Shi Z, Isobe K, et al. (2008) Essential role of CD8+CD122+ regulatory T cells in the recovery from experimental autoimmune encephalomyelitis. J Immunol 180: 825-832.
20. Endharti AT, Okuno Y, Shi Z, Misawa N, Toyokuni S, et al. (2011) CD8+CD122+ regulatory T cells (Tregs) and CD4+ Tregs cooperatively prevent and cure CD4+ cell-induced colitis. J Immunol 186: 41-52.
21. Deaglio S, Robson SC, (2011) Ectonucleotidases as regulators of purinergic signaling in thrombosis, inflammation, and immunity. Adv Pharmacol 61: 301-332.
22. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, et al. (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 204: 1257-1265.
23. Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos-Argumedo L, et al. (1993) Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262: 1056-1059.
24. Schuber F, Lund FE, (2004) Structure and enzymology of ADP-ribosyl cyclases: conserved enzymes that produce multiple calcium mobilizing metabolites. Curr Mol Med 4: 249-261.
25. Malavasi F, Deaglio S, Funaro A, Ferrero E, Horenstein AL, et al. (2008) Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol Rev 88: 841-886.
26. Read S, Mauze S, Asseman C, Bean A, Coffman R, et al. (1998) CD38+ CD45RB(low) CD4+ T cells: a population of T cells with immune regulatory activities in vitro. Eur J Immunol 28: 3435-3447.
27. Chen J, Chen YG, Reifsnyder PC, Schott WH, Lee CH, et al. (2006) Targeted disruption of CD38 accelerates autoimmune diabetes in NOD/Lt mice by enhancing autoimmunity in an ADP-ribosyltransferase 2-dependent fashion. J Immunol 176: 4590-4599.
28. Krebs C, Adriouch S, Braasch F, Koestner W, Leiter EH, et al. (2005) CD38 controls ADP-ribosyltransferase-2-catalyzed ADP-ribosylation of T cell surface proteins. J Immunol 174: 3298-3305.
29. Patton DT, Wilson MD, Rowan WC, Soond DR, Okkenhaug K, (2011) The PI3K p110delta regulates expression of CD38 on regulatory T cells. PLoS One 6: e17359.
30. Antonelli A, Fallahi P, Nesti C, Pupilli C, Marchetti P, et al. (2001) Anti-CD38 autoimmunity in patients with chronic autoimmune thyroiditis or Graves' disease. Clin Exp Immunol 126: 426-431.
31. Pupilli C, Antonelli A, Iughetti L, D'Annunzio G, Cotellessa M, et al. (2005) Anti-CD38 autoimmunity in children with newly diagnosed type 1 diabetes mellitus. J Pediatr Endocrinol Metab 18: 1417-1423.
32. Mehta K, Shahid U, Malavasi F, (1996) Human CD38, a cell-surface protein with multiple functions. FASEB J 10: 1408-1417.
33. Bean AG, Godfrey DI, Ferlin WG, Santos-Argumedo L, Parkhouse ME, et al. (1995) CD38 expression on mouse T cells: CD38 defines functionally distinct subsets of alpha beta TCR+CD4-CD8- thymocytes. Int Immunol 7: 213-221.
34. Sandoval-Montes C, Santos-Argumedo L, (2005) CD38 is expressed selectively during the activation of a subset of mature T cells with reduced proliferation but improved potential to produce cytokines. J Leukoc Biol 77: 513-521.
35. Blair PA, Norena LY, Flores-Borja F, Rawlings DJ, Isenberg DA, et al. (2010) CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 32: 129-140.
36. Yu A, Zhu L, Altman NH, Malek TR, (2009) A low interleukin-2 receptor signaling threshold supports the development and homeostasis of T regulatory cells. Immunity 30: 204-217.
37. Rifa'i M, Kawamoto Y, Nakashima I, Suzuki H, (2004) Essential roles of CD8+CD122+ regulatory T cells in the maintenance of T cell homeostasis. J Exp Med 200: 1123-1134.
38. Tsai S, Shameli A, Yamanouchi J, Clemente-Casares X, Wang J, et al. (2010) Reversal of autoimmunity by boosting memory-like autoregulatory T cells. Immunity 32: 568-580.
39. Haag F, Adriouch S, Brass A, Jung C, Moller S, et al. (2007) Extracellular NAD and ATP: Partners in immune cell modulation. Purinergic Signal 3: 71-81.
40. Jiang H, Curran S, Ruiz-Vazquez E, Liang B, Winchester R, et al. (2003) Regulatory CD8+ T cells fine-tune the myelin basic protein-reactive T cell receptor V beta repertoire during experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 100: 8378-8383.
41. Hu D, Ikizawa K, Lu L, Sanchirico ME, Shinohara ML, et al. (2004) Analysis of regulatory CD8 T cells in Qa-1-deficient mice. Nat Immunol 5: 516-523.
42. Sprent J, Surh CD, (2011) Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat Immunol 12: 478-484.
43. Osborne LC, Abraham N, (2009) Regulation of memory T cells by gammac cytokines. Cytokine 50: 105-113.
44. Funaro A, De Monte LB, Dianzani U, Forni M, Malavasi F, (1993) Human CD38 is associated to distinct molecules which mediate transmembrane signaling in different lineages. Eur J Immunol 23: 2407-2411.
45. Munoz P, Navarro MD, Pavon EJ, Salmeron J, Malavasi F, et al. (2003) CD38 signaling in T cells is initiated within a subset of membrane rafts containing Lck and the CD3-zeta subunit of the T cell antigen receptor. J Biol Chem 278: 50791-50802.
46. Dinesh RK, Skaggs BJ, La Cava A, Hahn BH, Singh RP, (2010) CD8+ Tregs in lupus, autoimmunity, and beyond. Autoimmun Rev 9: 560-568.
47. Molloy MJ, Zhang W, Usherwood EJ, (2011) Suppressive CD8+ T cells arise in the absence of CD4 help and compromise control of persistent virus. J Immunol 186: 6218-6226.
48. Suzuki H, Shi Z, Okuno Y, Isobe K, (2008) Are CD8+CD122+ cells regulatory T cells or memory T cells? Hum Immunol 69: 751-754.
49. Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, et al. (2000) Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 191: 771-780.
50. Yamada H, Matsuzaki G, Iwamoto Y, Nomoto K, (2000) Unusual cytotoxic activities of thymus-independent, self-antigen-specific CD8(+) T cells. Int Immunol 12: 1677-1683.
51. Yamada H, Matsuzaki G, Chen Q, Iwamoto Y, Nomoto K, (2001) Reevaluation of the origin of CD44(high) "memory phenotype" CD8 T cells: comparison between memory CD8 T cells and thymus-independent CD8 T cells. Eur J Immunol 31: 1917-1926.
52. Tsai S, Clemente-Casares X, Santamaria P (2011) CD8(+) Tregs in autoimmunity: learning "self"-control from experience. Cell Mol Life Sci.
53. Marks-Konczalik J, Dubois S, Losi JM, Sabzevari H, Yamada N, et al. (2000) IL-2-induced activation-induced cell death is inhibited in IL-15 transgenic mice. Proc Natl Acad Sci U S A 97: 11445-11450.