Induction of regulatory T cells and indefinite survival of fully allogeneic cardiac grafts by ursodeoxycholic acid in mice

Transplantation

Volumn 88, Issue 12, 2009, Pages 1360-1370

  Zhang, Qi ^a   Nakaki, Toshio ^a   Iwami, Daiki ^a   Niimi, Masanori ^a   Shirasugi, Nozomu ^a,b  

^a TEIKYO UNIVERSITY   (Japan)

^b Aisei Hospital   (Japan)

Author keywords

Cardiac transplantation; Mouse; Regulatory T cells; Ursodeoxycholic acid

Indexed keywords

CYCLOSPORIN A; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 6; TACROLIMUS; URSODEOXYCHOLIC ACID; CHOLAGOGUE;

ADOPTIVE TRANSFER; ALLOGRAFT; ALLOIMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIAC GRAFT REJECTION; CD4+ CD25+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG ANTAGONISM; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; GRAFT SURVIVAL; HEART TRANSPLANTATION; IMMUNOMODULATION; LOW DRUG DOSE; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SINGLE DRUG DOSE; SPLEEN CELL; ALLOTRANSPLANTATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CBA MOUSE; COMPARATIVE STUDY; GRAFT REJECTION; IMMUNOLOGY; PATHOLOGY; SKIN TRANSPLANTATION;

ANIMALS; CHOLAGOGUES AND CHOLERETICS; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED CBA; SKIN TRANSPLANTATION; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HOMOLOGOUS; URSODEOXYCHOLIC ACID;

EID: 74049133584     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0b013e3181bc2f4f     Document Type: Article

References (43)

1. Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003; 3: 199.
2. + regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005; 6: 345.
3. Lazaridis KN, Gores GJ, Lindor KD. Ursodeoxycholic acid 'mechanisms of action and clinical use in hepatobiliary disorders.' J Hepatol 2001; 35: 134.
4. Rust C, Beuers U. Medical treatment of primary biliary cirrhosis and primary sclerosing cholangitis. Clin Rev Allergy Immunol 2005; 28:135.
5. Lacaille F, Paradis K. The immunosuppressive effect of ursodeoxycholic acid: A comparative in vitro study on human peripheral blood mononuclear cells. Hepatology 1993; 18: 165.
6. Calmus Y, Weill B, Ozier Y, et al. Immunosuppressive properties of chenodeoxycholic and ursodeoxycholic acids in the mouse. Gastroenterology 1992; 103: 617.
7. +-T cell line. Int Hepatol Comm 1996; 4: 268.
8. Persson H, Friman S, Schersten T, et al. Ursodeoxycholic acid for prevention of acute rejection in liver transplant recipients. Lancet 1990; 336: 52.
9. Olausson M, Mjornstedt L, Wramner L, et al. Adjuvant treatment with ursodeoxycholic acid prevents acute rejection in rats receiving heart allografts. TransplInt 1992; 5(suppl 1): S539.
10. Fleckenstein JF, Paredes M, Thuluvath PJ. A prospective, randomized, double-blind trial evaluating the efficacy of ursodeoxycholic acid in prevention of liver transplant rejection. Liver Transpl Surg 1998; 4:276.
11. Keiding S, Hockerstedt K, Bjoro K, et al. The Nordic multicenter double-blind randomized controlled trial of prophylactic ursodeoxycholic acid in liver transplant patients. Transplantation 1997; 63: 1591.
12. Barnes D, Talenti D, Cammell G, et al. A randomized clinical trial of ursodeoxycholic acid as adjuvant treatment to prevent liver transplant rejection. Hepatology 1997; 26: 853.
13. Bahrle S, Szabo G, Stiehl A, et al. Adjuvant treatment with ursodeoxycholic acid may reduce the incidence of acute cardiac allograft rejection. J Heart Lung Transplant 1998; 17: 592.
14. AssyN, Adams PC, Myers P, et al. Randomized controlled trial of total immunosuppression withdrawal in liver transplant recipients: Role of ursodeoxycholic acid. Transplantation 2007; 83: 1571.
15. Niimi M. The technique for heterotopic cardiac transplantation in mice: Experience of 3000 operations by one surgeon. J Heart Lung Transplant 2001; 20: 1123.
16. Shirasugi N, Adams AB, Durham MM, et al. Prevention of chronic rejection in murine cardiac allografts: A comparison of chimerism-and nonchimerism- inducing costimulation blockade-based tolerance induction regimens. J Immunol 2002; 169: 2677.
17. Perros P, Weightman DR. Measurement of cell proliferation by enzyme-linked immunosorbent assay (ELISA) using a monoclonal antibody to bromodeoxyuridine. CellProlif 1991; 24: 517.
18. Inoue F, Zhang Q, Akiyoshi T, et al. Prolongation of survival of fully allogeneic cardiac grafts and generation of regulatory cells by a histamine receptor 2 antagonist. Transplantation 2007; 84: 1288.
19. Shibutani S, Inoue F, Aramaki O, et al. Effects of immunosuppressants on induction of regulatory cells after intratracheal delivery of alloanti-gen. Transplantation 2005; 79: 904.
20. Aramaki O, Takayama T, Yokoyama T, et al. High dose of antithrom-bin III induces indefinite survival of fully allogeneic cardiac grafts and generates regulatory cells. Transplantation 2003; 75: 217.
21. + regulatory cells. J Thorac Cardiovasc Surg 2005; 130: 1167.
22. Lee WY, Han SH, Cho TS, et al. Effect of ursodeoxycholic acid on ischemia/reperfusion injury in isolated rat heart. Arch Pharm Res 1999; 22: 479.
23. Rodrigues CM, Fan G, Ma X, et al. A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J Clin Invest 1998; 101: 2790.
24. Ikegami T, Matsuzaki Y, Fukushima S, et al. Suppressive effect of ursodeoxycholic acid on type IIA phospholipase A2 expression in HepG2 cells. Hepatology 2005; 41: 896.
25. Shah SA, Volkov Y, Arfin Q, et al. Ursodeoxycholic acid inhibits inter-leukin 1 beta [corrected] and deoxycholic acid-induced activation of NF-kappaB and AP1 in human colon cancer cells. Int J Cancer 2006; 118: 532.
26. Yokomori H, Oda M, Wakabayashi G, et al. Ursodeoxycholic acid therapy attenuated expression of adhesion molecule in primary biliary cirrhosis. Intern Med 2003; 42: 1259.
27. Moore KW, de Waal Malefyt R, Coffman RL, et al. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001; 19: 683.
28. + naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J Immunol 1999; 162: 5317.
29. Wan YY, Flavell RA. The roles for cytokines in the generation and maintenance of regulatory T cells. Immunol Rev 2006; 212: 114.
30. Aramaki O, Inoue F, Takayama T, et al. Interleukin-10 but not transforming growth factor-beta is essential for generation and suppressor function of regulatory cells induced by intratracheal delivery of alloan-tigen. Transplantation 2005; 79: 568.
31. Gonzalez-Rey E, Chorny A, Fernandez-Martin A, et al. Vasoactive intestinal peptide generates human tolerogenic dendritic cells that induce CD4 and CD8 regulatory T cells. Blood 2006; 107: 3632.
32. Barrat FJ, Cua DJ, Boonstra A, et al. In vitro generation of interleukin 10-producing regulatory CD4( + ) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)-and Th2-inducing cytokines. J Exp Med 2002; 195: 603.
33. + regulatory T cells. J Immunol 2007; 179: 3724.
34. Miura T, Ouchida R, Yoshikawa N, et al. Functional modulation of the glucocorticoid receptor and suppression of NF-kappaB-dependent transcription by ursodeoxycholic acid. J Biol Chem 2001; 276: 47371.
35. Fitzer CJ, O'Brian CA, Guillem JG, et al. The regulation of protein kinase C by chenodeoxycholate, deoxycholate and several structurally related bile acids. Carcinogenesis 1987; 8: 217.
36. Ishizaki K, Iwaki T, Kinoshita S, et al. Ursodeoxycholic acid protects concanavalin A-induced mouse liver injury through inhibition of intrahepatic tumor necrosis factor-alpha and macrophage inflammatory protein-2 production. Eur J Pharmacol 2008; 578: 57.
37. Tanaka H, Makino Y, Miura T, et al. Ligand-independent activation of the glucocorticoid receptor by ursodeoxycholic acid. Repression of IFN-gamma-induced MHC class II gene expression via a glucocorticoid receptor-dependent pathway. J Immunol 1996; 156: 1601.
38. Richards DF, Fernandez M, Caulfield J, et al. Glucocorticoids drive human CD8( + ) T cell differentiation towards a phenotype with high IL-10 and reduced IL-4, IL-5 and IL-13 production. Eur J Immunol 2000; 30: 2344.
39. + regulatory T cells. J Immunol 2004; 172: 5986.
40. Denton MD, Magee CC, Sayegh MH. Immunosuppressive strategies in transplantation. Lancet 1999; 353: 1083.
41. Vincenti F, Jensik SC, Filo RS, et al. A long-term comparison of tacrolimus (FK506) and cyclosporine in kidney transplantation: Evidence for improved allograft survival at five years. Transplantation 2002; 73:775.
42. Auchincloss H Jr. In search of the elusive Holy Grail: The mechanisms and prospects for achieving clinical transplantation tolerance. Am J Transplant 2001; 1: 6.
43. Wang H, Zhao L, Sun Z, et al. A potential side effect of cyclosporin A: Inhibition of CD4(+)CD25( + ) regulatory T cells in mice. Transplantation 2006; 82: 1484.