Graft-versus-Host Disease Is Enhanced by Selective CD73 Blockade in Mice

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Wang, Long ^a   Fan, Jie ^b   Chen, Siqi ^b   Zhang, Yi ^c   Curiel, Tyler J ^a   Zhang, Bin ^a,b,c  

^a University of Texas Health Science Center at San Antonio   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE A2A RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ALLOIMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL DEATH; CYTOKINE PRODUCTION; DISEASE EXACERBATION; ENZYME ACTIVITY; GRAFT VERSUS HOST REACTION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; RECEPTOR BLOCKING; REGULATORY T LYMPHOCYTE; SPLEEN CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

5'-NUCLEOTIDASE; ADENOSINE A2 RECEPTOR ANTAGONISTS; ANIMALS; BONE MARROW TRANSPLANTATION; GRAFT VS HOST DISEASE; GRAFT VS LEUKEMIA EFFECT; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; RECEPTOR, ADENOSINE A2A; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HOMOLOGOUS;

EID: 84874784746     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058397     Document Type: Article

References (53)

1. Shlomchik WD, (2007) Graft-versus-host disease. Nat Rev Immunol 7: 340-352.
2. Ferrara JL, Levy R, Chao NJ, (1999) Pathophysiologic mechanisms of acute graft-vs.-host disease. Biol Blood Marrow Transplant 5: 347-356.
3. Welniak LA, Blazar BR, Murphy WJ, (2007) Immunobiology of allogeneic hematopoietic stem cell transplantation. Annu Rev Immunol 25: 139-170.
4. Holler E, (2002) Cytokines, viruses, and graft-versus-host disease. Curr Opin Hematol 9: 479-484.
5. van den Brink MR, Burakoff SJ, (2002) Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol 2: 273-281.
6. Resta R, Yamashita Y, Thompson LF, (1998) Ecto-enzyme and signaling functions of lymphocyte CD73. Immunol Rev 161: 95-109.
7. Colgan SP, Eltzschig HK, Eckle T, Thompson LF, (2006) Physiological roles for ecto-5′-nucleotidase (CD73). Purinergic Signal 2: 351-360.
8. Yegutkin GG, (2008) Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783: 673-694.
9. Jalkanen S, Salmi M, (2008) VAP-1 and CD73, endothelial cell surface enzymes in leukocyte extravasation. Arterioscler Thromb Vasc Biol 28: 18-26.
10. Algars A, Karikoski M, Yegutkin GG, Stoitzner P, Niemela J, et al. (2011) Different role of CD73 in leukocyte trafficking via blood and lymph vessels. Blood 117: 4387-4393.
11. 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.
12. Zhang B, (2010) CD73: A Novel Target for Cancer Immunotherapy. Cancer Res 70: 6407-6411.
13. Ernst PB, Garrison JC, Thompson LF, (2010) Much ado about adenosine: adenosine synthesis and function in regulatory T cell biology. J Immunol 185: 1993-1998.
14. Eckle T, Krahn T, Grenz A, Kohler D, Mittelbronn M, et al. (2007) Cardioprotection by ecto-5′-nucleotidase (CD73) and A2B adenosine receptors. Circulation 115: 1581-1590.
15. Mills JH, Thompson LF, Mueller C, Waickman AT, Jalkanen S, et al. (2008) CD73 is required for efficient entry of lymphocytes into the central nervous system during experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 105: 9325-9330.
16. Louis NA, Robinson AM, MacManus CF, Karhausen J, Scully M, et al. (2008) Control of IFN-alphaA by CD73: implications for mucosal inflammation. J Immunol 180: 4246-4255.
17. Antonioli L, Fornai M, Colucci R, Awwad O, Ghisu N, et al. (2011) Differential recruitment of high affinity A1 and A2A adenosine receptors in the control of colonic neuromuscular function in experimental colitis. Eur J Pharmacol 650: 639-649.
18. Alam MS, Kurtz CC, Rowlett RM, Reuter BK, Wiznerowicz E, et al. (2009) CD73 is expressed by human regulatory T helper cells and suppresses proinflammatory cytokine production and Helicobacter felis-induced gastritis in mice. J Infect Dis 199: 494-504.
19. Jin D, Fan J, Wang L, Thompson LF, Liu A, et al. (2010) CD73 on tumor cells impairs antitumor T-cell responses: a novel mechanism of tumor-induced immune suppression. Cancer Res 70: 2245-2255.
20. Wang L, Fan J, Thompson LF, Zhang Y, Shin T, et al. (2011) CD73 has distinct roles in nonhematopoietic and hematopoietic cells to promote tumor growth in mice. J Clin Invest 121: 2371-2382.
21. Stagg J, Divisekera U, McLaughlin N, Sharkey J, Pommey S, et al. (2010) Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci U S A 107: 1547-1552.
22. Stagg J, Divisekera U, Duret H, Sparwasser T, Teng MW, et al. (2011) CD73-deficient mice have increased antitumor immunity and are resistant to experimental metastasis. Cancer Res 71: 2892-2900.
23. Yegutkin GG, Marttila-Ichihara F, Karikoski M, Niemela J, Laurila JP, et al. (2011) Altered purinergic signaling in CD73-deficient mice inhibits tumor progression. Eur J Immunol 41: 1231-1241.
24. Robson SC, Wu Y, Sun X, Knosalla C, Dwyer K, et al. (2005) Ectonucleotidases of CD39 family modulate vascular inflammation and thrombosis in transplantation. Semin Thromb Hemost 31: 217-233.
25. Enjyoji K, Sevigny J, Lin Y, Frenette PS, Christie PD, et al. (1999) Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat Med 5: 1010-1017.
26. Wilhelm K, Ganesan J, Muller T, Durr C, Grimm M, et al. (2010) Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nat Med 16: 1434-1438.
27. Hasegawa T, Bouis D, Liao H, Visovatti SH, Pinsky DJ, (2008) Ecto-5′ nucleotidase (CD73)-mediated adenosine generation and signaling in murine cardiac allograft vasculopathy. Circ Res 103: 1410-1421.
28. Ohtsuka T, Changelian PS, Bouis D, Noon K, Harada H, et al. (2010) Ecto-5′-nucleotidase (CD73) attenuates allograft airway rejection through adenosine 2A receptor stimulation. J Immunol 185: 1321-1329.
29. Thompson LF, Eltzschig HK, Ibla JC, Van De Wiele CJ, Resta R, et al. (2004) Crucial role for ecto-5′-nucleotidase (CD73) in vascular leakage during hypoxia. J Exp Med 200: 1395-1405.
30. Eltzschig HK, Thompson LF, Karhausen J, Cotta RJ, Ibla JC, et al. (2004) Endogenous adenosine produced during hypoxia attenuates neutrophil accumulation: coordination by extracellular nucleotide metabolism. Blood 104: 3986-3992.
31. Koszalka P, Ozuyaman B, Huo Y, Zernecke A, Flogel U, et al. (2004) Targeted disruption of cd73/ecto-5′-nucleotidase alters thromboregulation and augments vascular inflammatory response. Circ Res 95: 814-821.
32. Hart ML, Grenz A, Gorzolla IC, Schittenhelm J, Dalton JH, et al. (2011) Hypoxia-inducible factor-1alpha-dependent protection from intestinal ischemia/reperfusion injury involves ecto-5′-nucleotidase (CD73) and the A2B adenosine receptor. J Immunol 186: 4367-4374.
33. Chen BJ, Cui X, Sempowski GD, Liu C, Chao NJ, (2004) Transfer of allogeneic CD62L- memory T cells without graft-versus-host disease. Blood 103: 1534-1541.
34. Edinger M, Hoffmann P, Ermann J, Drago K, Fathman CG, et al. (2003) CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med 9: 1144-1150.
35. Trenado A, Charlotte F, Fisson S, Yagello M, Klatzmann D, et al. (2003) Recipient-type specific CD4+CD25+ regulatory T cells favor immune reconstitution and control graft-versus-host disease while maintaining graft-versus-leukemia. J Clin Invest 112: 1688-1696.
36. Strohmeier GR, Lencer WI, Patapoff TW, Thompson LF, Carlson SL, et al. (1997) Surface expression, polarization, and functional significance of CD73 in human intestinal epithelia. J Clin Invest 99: 2588-2601.
37. Shlomchik WD, Couzens MS, Tang CB, McNiff J, Robert ME, et al. (1999) Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science 285: 412-415.
38. Duffner UA, Maeda Y, Cooke KR, Reddy P, Ordemann R, et al. (2004) Host dendritic cells alone are sufficient to initiate acute graft-versus-host disease. J Immunol 172: 7393-7398.
39. Teshima T, Ordemann R, Reddy P, Gagin S, Liu C, et al. (2002) Acute graft-versus-host disease does not require alloantigen expression on host epithelium. Nat Med 8: 575-581.
40. Tsukamoto H, Chernogorova P, Ayata K, Gerlach UV, Rughani A, et al. (2012) Deficiency of CD73/ecto-5′-nucleotidase in mice enhances acute graft-versus-host disease. Blood 119: 4554-4564.
41. Mikhailov A, Sokolovskaya A, Yegutkin GG, Amdahl H, West A, et al. (2008) CD73 participates in cellular multiresistance program and protects against TRAIL-induced apoptosis. J Immunol 181: 464-475.
42. Airas L, Niemela J, Jalkanen S, (2000) CD73 engagement promotes lymphocyte binding to endothelial cells via a lymphocyte function-associated antigen-1-dependent mechanism. J Immunol 165: 5411-5417.
43. Airas L, Niemela J, Salmi M, Puurunen T, Smith DJ, et al. (1997) Differential regulation and function of CD73, a glycosyl-phosphatidylinositol-linked 70-kD adhesion molecule, on lymphocytes and endothelial cells. J Cell Biol 136: 421-431.
44. Romio M, Reinbeck B, Bongardt S, Huls S, Burghoff S, et al. (2011) Extracellular purine metabolism and signaling of CD73-derived adenosine in murine Treg and Teff cells. Am J Physiol Cell Physiol 301: C530-539.
45. Wood KJ, Sakaguchi S, (2003) Regulatory T cells in transplantation tolerance. Nat Rev Immunol 3: 199-210.
46. Salcido-Ochoa F, Tsang J, Tam P, Falk K, Rotzschke O, (2010) Regulatory T cells in transplantation: does extracellular adenosine triphosphate metabolism through CD39 play a crucial role? Transplant Rev (Orlando) 24: 52-66.
47. Thomson LF, Ruedi JM, Glass A, Moldenhauer G, Moller P, et al. (1990) Production and characterization of monoclonal antibodies to the glycosyl phosphatidylinositol-anchored lymphocyte differentiation antigen ecto-5′-nucleotidase (CD73). Tissue Antigens 35: 9-19.
48. Yamashita Y, Hooker SW, Jiang H, Laurent AB, Resta R, et al. (1998) CD73 expression and fyn-dependent signaling on murine lymphocytes. Eur J Immunol 28: 2981-2990.
49. Airas L, Jalkanen S, (1996) CD73 mediates adhesion of B cells to follicular dendritic cells. Blood 88: 1755-1764.
50. Regateiro FS, Howie D, Nolan KF, Agorogiannis EI, Greaves DR, et al. (2011) Generation of anti-inflammatory adenosine by leukocytes is regulated by TGF-beta. Eur J Immunol.
51. Liang Y, Liu C, Djeu JY, Zhong B, Peters T, et al. (2008) Beta2 integrins separate graft-versus-host disease and graft-versus-leukemia effects. Blood 111: 954-962.
52. Lappas CM, Liu PC, Linden J, Kang EM, Malech HL, (2010) Adenosine A2A receptor activation limits graft-versus-host disease after allogenic hematopoietic stem cell transplantation. J Leukoc Biol 87: 345-354.
53. Kaplan DH, Anderson BE, McNiff JM, Jain D, Shlomchik MJ, et al. (2004) Target antigens determine graft-versus-host disease phenotype. J Immunol 173: 5467-5475.