CD39 deficiency in murine liver allografts promotes inflammatory injury and immune-mediated rejection

Transplant Immunology

Volumn 32, Issue 2, 2015, Pages 76-83

  Yoshida, Osamu ^a   Dou, Lei ^a   Kimura, Shoko ^a   Yokota, Shinichiro ^a   Isse, Kumiko ^a,b   Robson, Simon C ^c   Geller, David A ^a   Thomson, Angus W ^a,b  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Adenosine triphosphate; CD39; Liver allograft; T cell

Indexed keywords

ALANINE AMINOTRANSFERASE; CD39 ANTIGEN; GAMMA INTERFERON; APYRASE; LEUKOCYTE ANTIGEN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; COLD ISCHEMIA; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNE MEDIATED REJECTION; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; KNOCKOUT MOUSE; LIVER TRANSPLANTATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REGULATORY T LYMPHOCYTE; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE INJURY; WILD TYPE; ALLOGRAFT; ANIMAL; DEFICIENCY; GENETICS; HEPATITIS; IMMUNOLOGY; PATHOLOGY;

ALLOGRAFTS; ANIMALS; ANTIGENS, CD; APYRASE; GRAFT REJECTION; GRAFT SURVIVAL; HEPATITIS; LIVER TRANSPLANTATION; MALE; MICE; MICE, KNOCKOUT;

EID: 84926422212     PISSN: 09663274     EISSN: 18785492     Source Type: Journal    
DOI: 10.1016/j.trim.2015.01.003     Document Type: Article

References (52)

1. Crispe I.N. The liver as a lymphoid organ. Annu Rev Immunol 2009, 27:147-163.
2. Adams D.H., Eksteen B., Curbishley S.M. Immunology of the gut and liver: a love/hate relationship. Gut 2008, 57:838-848.
3. Thomson A.W., Knolle P.A. Antigen-presenting cell function in the tolerogenic liver environment. Nat Rev Immunol 2010, 10:753-766.
4. Crispe I.N., Hepatic T. Cells and liver tolerance. Nat Rev Immunol 2003, 3:51-62.
5. Bishop A.G., Bertolino P.D., Bowen D.G., McCaughan G.W. Tolerance in liver transplantation. Best Pract Res Clin Gastroenterol 2012, 26:73-84.
6. Calne R.Y., Sells R.A., Pena J.R., Davis D.R., Millard P.R., Herbertson B.M., et al. Induction of immunological tolerance by porcine liver allografts. Nature 1969, 223:472-476.
7. Qian S., Demetris A.J., Murase N., Rao A.S., Fung J.J., Starzl T.E. Murine liver allograft transplantation: tolerance and donor cell chimerism. Hepatology 1994, 19:916-924.
8. Pons J.A., Revilla Nuin B., Ramirez P., Baroja Mazo A., Martinez Alarcon L., Robles R., et al. What do we know about the clinical impact of complete withdrawal of immunosuppression in liver transplantation?. Transplant Proc 2012, 44:1530-1532.
9. Sanchez-Fueyo A., Strom T.B. Immunological tolerance and liver transplantation. J Hepatol 2004, 41:698-705.
10. Bishop G.A., Wang C., Sharland A.F., McCaughan G. Spontaneous acceptance of liver transplants in rodents: evidence that liver leucocytes induce recipient T-cell death by neglect. Immunol Cell Biol 2002, 80:93-100.
11. Sharland A., Yan Y., Wang C., Bowen D.G., Sun J., Sheil A.G., et al. Evidence that apoptosis of activated T cells occurs in spontaneous tolerance of liver allografts and is blocked by manipulations which break tolerance. Transplantation 1999, 68:1736-1745.
12. Thomson A.W., Lu L., Murase N., Demetris A.J., Rao A.S., Starzl T.E. Microchimerism, dendritic cell progenitors and transplantation tolerance. Stem Cells 1995, 13:622-639.
13. Lu L., Rudert W.A., Qian S., McCaslin D., Fu F., Rao A.S., et al. Growth of donor-derived dendritic cells from the bone marrow of murine liver allograft recipients in response to granulocyte/macrophage colony stimulating factor. J Exp Med 1995, 182:379-387.
14. Shalev I., Selzner N., Shyu W., Grant D., Levy G. Role of regulatory T cells in the promotion of transplant tolerance. Liver Transpl 2012, 18:761-770.
15. Li W., Kuhr C.S., Zheng X.X., Carper K., Thomson A.W., Reyes J.D., et al. New insights into mechanisms of spontaneous liver transplant tolerance: the role of Foxp3-expressing CD25+ CD4+ regulatory T cells. Am J Transplant 2008, 8:1639-1651.
16. Morita M., Fujino M., Jiang G., Kitazawa Y., Xie L., Azuma M., et al. PD-1/B7-H1 interaction contribute to the spontaneous acceptance of mouse liver allograft. Am J Transplant 2010, 10:40-46.
17. Yoshida O., Kimura S., Dou L., Matta B.M., Yokota S., Ross M.A., et al. DAP12 deficiency in liver allografts results in enhanced donor DC migration, augmented effector T cell responses and abrogation of transplant tolerance. Am J Transplant 2014, 14:1791-1805.
18. Trautmann A. Extracellular ATP in the immune system: more than just a "danger signal". Sci Signal 2009, 2. [pe6].
19. Eltzschig H.K., Sitkovsky M.V., Robson S.C. Purinergic signaling during inflammation. N Engl J Med 2012, 367:2322-2333.
20. Elliott M.R., Chekeni F.B., Trampont P.C., Lazarowski E.R., Kadl A., Walk S.F., et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009, 461:282-286.
21. Weber F.C., Esser P.R., Muller T., Ganesan J., Pellegatti P., Simon M.M., et al. Lack of the purinergic receptor P2X(7) results in resistance to contact hypersensitivity. J Exp Med 2010, 207:2609-2619.
22. Pellegatti P., Raffaghello L., Bianchi G., Piccardi F., Pistoia V., Di Virgilio F. Increased level of extracellular ATP at tumor sites: in vivo imaging with plasma membrane luciferase. PLoS One 2008, 3:e2599.
23. Ayata C.K., Ganal S.C., Hockenjos B., Willim K., Vieira R.P., Grimm M., et al. Purinergic P2Y(2) receptors promote neutrophil infiltration and hepatocyte death in mice with acute liver injury. Gastroenterology 2012, 143:1620-1629.
24. Wilhelm K., Ganesan J., Muller T., Durr C., Grimm M., Beilhack A., et al. Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nat Med 2010, 16:1434-1438.
25. Vergani A., Tezza S., Fotino C., Visner G., Pileggi A., Chandraker A., et al. The purinergic system in allotransplantation. Am J Transplant 2014, 14:507-514.
26. Vergani A., Tezza S., D'Addio F., Fotino C., Liu K., Niewczas M., et al. Long-term heart transplant survival by targeting the ionotropic purinergic receptor P2X7. Circulation 2013, 127:463-475.
27. Antonioli L., Pacher P., Vizi E.S., Hasko G. CD39 and CD73 in immunity and inflammation. Trends Mol Med 2013, 19:355-367.
28. Schulze Zur Wiesch J., Thomssen A., Hartjen P., Toth I., Lehmann C., Meyer-Olson D., et al. Comprehensive analysis of frequency and phenotype of T regulatory cells in HIV infection: CD39 expression of FoxP3+ T regulatory cells correlates with progressive disease. J Virol 2011, 85:1287-1297.
29. Hilchey S.P., Kobie J.J., Cochran M.R., Secor-Socha S., Wang J.C., Hyrien O., et al. Human follicular lymphoma CD39+-infiltrating T cells contribute to adenosine-mediated T cell hyporesponsiveness. J Immunol 2009, 183:6157-6166.
30. Mandapathil M., Szczepanski M.J., Szajnik M., Ren J., Lenzner D.E., Jackson E.K., et al. Increased ectonucleotidase expression and activity in regulatory T cells of patients with head and neck cancer. Clin Cancer Res 2009, 15:6348-6357.
31. Sun X., Han L., Seth P., Bian S., Li L., Csizmadia E., et al. Disordered purinergic signaling and abnormal cellular metabolism are associated with development of liver cancer in Cd39/ENTPD1 null mice. Hepatology 2013, 57:205-216.
32. Fletcher J.M., Lonergan R., Costelloe L., Kinsella K., Moran B., O'Farrelly C., et al. CD39+ Foxp3+ regulatory T Cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J Immunol 2009, 183:7602-7610.
33. Moncrieffe H., Nistala K., Kamhieh Y., Evans J., Eddaoudi A., Eaton S., et al. High expression of the ectonucleotidase CD39 on T cells from the inflamed site identifies two distinct populations, one regulatory and one memory T cell population. J Immunol 2010, 185:134-143.
34. Grant C.R., Liberal R., Holder B.S., Cardone J., Ma Y., Robson S.C., et al. Dysfunctional CD39(POS) regulatory T cells and aberrant control of T-helper type 17 cells in autoimmune hepatitis. Hepatology 2014, 59:1007-1015.
35. Bonner F., Borg N., Burghoff S., Schrader J. Resident cardiac immune cells and expression of the ectonucleotidase enzymes CD39 and CD73 after ischemic injury. PLoS One 2012, 7:e34730.
36. Grenz A., Zhang H., Hermes M., Eckle T., Klingel K., Huang D.Y., et al. Contribution of E-NTPDase1 (CD39) to renal protection from ischemia-reperfusion injury. FASEB J 2007, 21:2863-2873.
37. Guckelberger O., Sun X.F., Sevigny J., Imai M., Kaczmarek E., Enjyoji K., et al. Beneficial effects of CD39/ecto-nucleoside triphosphate diphosphohydrolase-1 in murine intestinal ischemia-reperfusion injury. Thromb Haemost 2004, 91:576-586.
38. Beldi G., Banz Y., Kroemer A., Sun X., Wu Y., Graubardt N., et al. Deletion of CD39 on natural killer cells attenuates hepatic ischemia/reperfusion injury in mice. Hepatology 2010, 51:1702-1711.
39. Pommey S., Lu B., McRae J., Stagg J., Hill P., Salvaris E., et al. Liver grafts from CD39-overexpressing rodents are protected from ischemia reperfusion injury due to reduced numbers of resident CD4(+) T cells. Hepatology 2013, 57:1597-1606.
40. Yoshida O., Kimura S., Jackson E.K., Robson S.C., Geller D.A., Murase N., et al. CD39 expression by hepatic myeloid dendritic cells attenuates inflammation in liver transplant ischemia-reperfusion injury in mice. Hepatology 2013, 58:2163-2175.
41. Lechler R.I., Ng W.F., Steinman R.M. Dendritic cells in transplantation - friend or foe?. Immunity 2001, 14:357-368.
42. Morelli A.E., Thomson A.W. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 2007, 7:610-621.
43. Ueki S., Castellaneta A., Yoshida O., Ozaki K., Zhang M., Kimura S., et al. Hepatic B7 homolog 1 expression is essential for controlling cold ischemia/reperfusion injury after mouse liver transplantation. Hepatology 2011, 54:216-228.
44. Castellaneta A., Yoshida O., Kimura S., Yokota S., Geller D.A., Murase N., et al. Plasmacytoid dendritic cell-derived IFN-alpha promotes murine liver ischemia/reperfusion injury by induction of hepatocyte IRF-1. Hepatology 2014, 60:267-277.
45. Demetris A., Batts K.P., Dhillon A.P., Ferrell L., Fung J.J., Geller D.A., et al. Banff schema for grading liver allograft rejection: an international consensus document. Hepatology 1997, 25:658-663.
46. Wood K.J., Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003, 3:199-210.
47. Londono M.C., Rimola A., O'Grady J., Sanchez-Fueyo A. Immunosuppression minimization vs. complete drug withdrawal in liver transplantation. J Hepatol 2013, 59:872-879.
48. Feng S. Long-term management of immunosuppression after pediatric liver transplantation: is minimization or withdrawal desirable or possible or both?. Curr Opin Organ Transplant 2008, 13:506-512.
49. Junger W.G. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 2011, 11:201-212.
50. Ernst P.B., Garrison J.C., Thompson L.F. Much ado about adenosine: adenosine synthesis and function in regulatory T cell biology. J Immunol 2010, 185:1993-1998.
51. Hyman M.C., Petrovic-Djergovic D., Visovatti S.H., Liao H., Yanamadala S., Bouis D., et al. Self-regulation of inflammatory cell trafficking in mice by the leukocyte surface apyrase CD39. J Clin Invest 2009, 119:1136-1149.
52. Shen K., Zheng S.S., Park O., Wang H., Sun Z., Gao B. Activation of innate immunity (NK/IFN-gamma) in rat allogeneic liver transplantation: contribution to liver injury and suppression of hepatocyte proliferation. Am J Physiol Gastrointest Liver Physiol 2008, 294:G1070-G1077.