Intestinal immunopathology is associated with decreased CD73-generated adenosine during lethal infection

Mucosal Immunology

Volumn 8, Issue 4, 2015, Pages 773-784

  Francois, V ^a   Shehade, H ^a   Acolty, V ^a   Preyat, N ^a   Delree P ^b   Moser, M ^a   Oldenhove, G ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b Institute of Pathology and Genetics Gosselies   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE A2A RECEPTOR; ADENOSINE A2B RECEPTOR; ADENOSINE RECEPTOR; CD39 ANTIGEN; RETINOIC ACID; TRANSFORMING GROWTH FACTOR BETA; APYRASE; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL POLARITY; CONTROLLED STUDY; DISEASE ASSOCIATION; DYSBIOSIS; ENTERITIS; FEMALE; IMMUNOPATHOLOGY; INTESTINE EPITHELIUM; INTESTINE INFECTION; LAMINA PROPRIA; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; SPLEEN; STEADY STATE; TH1 CELL; TOXOPLASMOSIS; ANIMAL; DISEASE MODEL; DRUG EFFECTS; ENTEROPATHY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PARASITOLOGY; T LYMPHOCYTE SUBPOPULATION; TOXOPLASMA;

5'-NUCLEOTIDASE; ADENOSINE; ANIMALS; ANTIGENS, CD; APYRASE; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENE EXPRESSION REGULATION; INTESTINAL DISEASES; MICE; MICE, KNOCKOUT; RECEPTOR, ADENOSINE A2A; RECEPTOR, ADENOSINE A2B; T-LYMPHOCYTE SUBSETS; TOXOPLASMA; TRANSFORMING GROWTH FACTOR BETA; TRETINOIN;

EID: 84932623761     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.108     Document Type: Article

References (52)

1. Friedman D.J., et al. From the Cover: CD39 deletion exacerbates experimental murine colitis and human polymorphisms increase susceptibility to inflammatory bowel disease. Proc. Natl. Acad. Sci. USA 106, 16788-16793 (2009
2. Haskó, G., et al. Ecto-50-nucleotidase (CD73) decreases mortality and organ injury in sepsis. J. Immunol. 187, 4256-4267 (2011
3. Bynoe M.S., et al. CD73 is critical for the resolution of murine colonic inflammation. J. Biomed. Biotechnol. 2012, 260983 (2012
4. Wang L., et al. Graft-versus-host disease is enhanced by selective CD73 blockade in mice. PLoS One 8, e58397 (2013
5. Antonioli L., Pacher P., Vizi E.S. & Haskó, G. CD39 and CD73 in immunity and inflammation. Trends Mol. Med. 19, 355-367 (2013
6. Sprague R.S., Ellsworth M.L., Stephenson A.H. & Lonigro A.J. ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am. J. Physiol. 271, H2717-H2722 (1996
7. Ayna G., et al. ATP release from dying autophagic cells and their phagocytosis are crucial for inflammasome activation in macrophages. PLoS One 7, e40069 (2012
8. Martins I., et al. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ. 21, 79-91 (2014
9. Beigi R., Kobatake E., Aizawa M. & Dubyak G.R. Detection of local ATP release from activated platelets using cell surface-attached firefly luciferase. Am. J. Physiol. 276, C267-C278 (1999
10. Ivanova E.P., Alexeeva Y.V., Pham D.K., Wright J.P. & Nicolau D. V ATP level variations in heterotrophic bacteria during attachment on hydrophilic and hydrophobic surfaces. Int. Microbiol. 9, 37-46 (2006
11. Atarashi K., et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 455, 808-812 (2008
12. Gombault A., Baron L. & Couillin I. ATP release and purinergic signaling in NLRP3 inflammasome activation. Front. Immunol. 3, 414 (2012
13. Chen Y., et al. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science 314, 1792-1795 (2006
14. Ma Y., et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 38, 729-741 (2013
15. Ma Y., et al. ATP-dependent recruitment, survival and differentiation of dendritic cell precursors in the tumor bed after anticancer chemotherapy. Oncoimmunology 2, e24568 (2013
16. Kurashima Y., et al. Extracellular ATPmediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nat. Commun. 3, 1034 (2012
17. Schenk U., et al. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 1, ra6 (2008
18. Woehrle T., et al. Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 116, 3475-3484 (2010
19. Schenk U., et al. ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Sci. Signal. 4, ra12 (2011
20. Haskó, G. & Cronstein B.N. Adenosine: an endogenous regulator of innate immunity. Trends Immunol. 25, 33-39 (2004
21. Panther E., et al. Adenosine affects expression of membrane molecules, cytokine and chemokine release, and the T-cell stimulatory capacity of human dendritic cells. Blood 101, 3985-3990 (2003
22. Schnurr M., et al. Role of adenosine receptors in regulating chemotaxis and cytokine production of plasmacytoid dendritic cells. Blood 103, 1391-1397 (2004
23. Li L., et al. Dendritic cells tolerized with adenosine A2AR agonist attenuate acute kidney injury. J. Clin. Invest. 122, 3931-3942 (2012
24. Linden J. & Cekic C. Regulation of lymphocyte function by adenosine. Arterioscler. Thromb. Vasc. Biol. 32, 2097-2103 (2012
25. Csóka B., et al. Adenosine A2A receptor activation inhibits T helper 1 and T helper 2 cell development and effector function. FASEBJ. 22, 3491-3499 (2008
26. Ohta A., et al. A2A adenosine receptor protects tumors from antitumor T cells. Proc. Natl. Acad. Sci. USA 103, 13132-13137 (2006
27. Ernst P.B., Garrison J.C. & Thompson L.F. Much ado about adenosine: adenosine synthesis and function in regulatory T cell biology. J. Immunol. 185, 1993-1998 (2010
28. Deaglio S., et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204, 1257-1265 (2007
29. Borsellino G., et al. Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 110, 1225-1232 (2007
30. Alam M.S., et al.CD73 is expressed by human regulatory T helper cells and suppresses proinflammatory cytokine production and Helicobacter felisinduced gastritis in mice. J. Infect. Dis. 199, 494-504 (2009
31. Chalmin F., et al. Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression. Immunity 36, 362-373 (2012
32. Iyer S.S., et al. Identification of novel markers for mouse CD4(+) T follicular helper cells. Eur. J. Immunol. 43, 3219-3232 (2013
33. Regateiro F.S., et al. Generation of anti-inflammatory adenosine by leukocytes is regulated by TGF-b. Eur. J. Immunol. 41, 2955-2965 (2011
34. Iwata M., et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538 (2004
35. Gazzinelli R.T., et al. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J. Immunol. 157, 798-805 (1996
36. Oldenhove G., et al. Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 31, 772-786 (2009
37. Louis N.A., et al. Control of IFN-alphaA by CD73: implications for mucosal inflammation. J. Immunol. 180, 4246-4255 (2008
38. Sun C.-M., et al. Small intestine lamina propria dendritic cells promote De novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007
39. Coombes J.L., et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764 (2007
40. Molenaar R., et al. Expression of retinaldehyde dehydrogenase enzymes in mucosal dendritic cells and gut-draining lymph node stromal cells is controlled by dietary vitamin A. J. Immunol. 186, 1934-1942 (2011
41. Mucida D., et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317, 256-260 (2007
42. Odashima M., et al. Activation of A2A adenosine receptor attenuates intestinal inflammation in animal models of inflammatory bowel disease. Gastroenterology 129, 26-33 (2005
43. Li Y., et al. Adenosine A2A receptor activation reduces recurrence and mortality from Clostridium difficile infection in mice following vancomycin treatment. BMC Infect. Dis. 12, 342 (2012
44. Yegutkin G.G., et al. Disordered lymphoid purine metabolism contributes to the pathogenesis of persistent Borrelia garinii infection in mice. J. Immunol. 184, 5112-5120 (2010
45. Morello S., Sorrentino R. & Pinto A. Adenosine A2a receptor agonists as regulators of inflammation: pharmacology and therapeutic opportunities. J Recept. Ligand Channel Res., 11-17 (2009
46. Ohta A., et al. 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, 190 (2012
47. Hart M.L., Jacobi B., Schittenhelm J., Henn M. & Eltzschig H.K. Cutting edge: A2B adenosine receptor signaling provides potent protection during intestinal ischemia/reperfusion injury. J. Immunol. 182, 3965-3968 (2009
48. Madara J.L., et al. 50-adenosine monophosphate is the neutrophil-derived paracrine factor that elicits chloride secretion from T84 intestinal epithelial cell monolayers. J. Clin. Invest. 91, 2320-2325 (1993
49. Mahamed D.A., Mills J.H., Egan C.E., Denkers E.Y. & Bynoe M.S. CD73-generated adenosine facilitates Toxoplasma gondii differentiation to long-lived tissue cysts in the central nervous system. Proc. Natl. Acad. Sci. USA 109, 16312-16317 (2012
50. Raetz M., et al. Parasite-induced TH1 cells and intestinal dysbiosis cooperate in IFN-g-dependent elimination of Paneth cells. Nat. Immunol. 14, 136-142 (2013
51. Hand T.W., et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337, 1553-1556 (2012
52. Burg J.L., Grover C.M., Pouletty P. & Boothroyd J.C. Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J. Clin. Microbiol. 27, 1787-1792 (1989