CTLA4Ig adenoviral gene transfer induces long-term islet rat allograft survival, without tolerance, after systemic but not local intragraft expression

Human Gene Therapy

Volumn 14, Issue 6, 2003, Pages 561-575

  Laumonier, Thomas ^a   Potiron, Nicolas ^a   Boeffard, Françoise ^a   Chagneau, Carine ^a   Brouard, Sophie ^a   Guillot, Cécile ^a   Soulillou, Jean Paul ^a   Anegon, Ignacio ^a   Le Mauff, Brigitte ^a,b  

^a Inst Transplant/Rech Transplant   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOMODULATING AGENT;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; GENE TRANSFER; GENETIC ENGINEERING; GRAFT REJECTION; GRAFT SURVIVAL; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; INCUBATION TIME; MALE; NONHUMAN; PANCREAS ISLET CELL; PANCREAS ISLET TRANSPLANTATION; PLAQUE FORMING CELL; RAT; STATISTICAL ANALYSIS; SURVIVAL TIME; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT;

ADENOVIRIDAE; ANIMALS; GENETIC VECTORS; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOCOMPROMISED HOST; IMMUNOCONJUGATES; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; ISOANTIBODIES; MALE; MICE; RATS; RATS, INBRED BN; RATS, INBRED LEW; RATS, INBRED WF; SPLEEN; TRANSDUCTION, GENETIC; TRANSPLANTATION TOLERANCE;

ADENOVIRIDAE; ANIMALIA;

EID: 0037431319     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/104303403764539341     Document Type: Article

References (57)

1. AKALIN, E., CHANDRAKER, A., RUSSEL, M., TURKA, L., HANCOCK, W., and SAYEGH, M. (1996). CD28-B7 T cell costimulation blockade by CTLA4Ig in the rat renal allograft model. Inhibition of cell-mediated and humoral responses in vivo. Transplantation 62, 1942-1945.
2. BALIGA, P., CHAVIN, K., QIN, L., WOODWARD, J., LIN, J., LINSLEY, P., and BROMBERG, J. (1994). CTLA4Ig prolongs allograft survival while suppressing cell-mediated immunity. Transplantation 58, 1082-1090.
3. BARROU, B., BERTRY-COUSSOT, L., MORIN, S., SAINZ, J., LUCAS, B., BITKER, M.O., DEBRE, P., and LEMARCHAND, P. (2002). Prolonged islet allograft survival by adenovirus-mediated transfer of sICAM-1/Ig immunoadhesin gene. Hum. Gene Ther. 13, 1441-1450.
4. BRADY, J.L., and LEW, A.M. (2000). Additive efficacy of CTLA4Ig and OX40Ig secreted by genetically modified grafts. Transplantation 69, 724-730.
5. CHAHINE, A., YU, M., MCKERNAN, M., STOECKERT, C., and LAU, H. (1995). Immunomodulation of pancreatic islet allografts in mice with CTLA4Ig secreting muscle cells. Transplantation 59, 1313-1318.
6. COULOMBE, M., and GILL, R.G. (1994). Tolerance induction to cultured islet allografts. I. Characterization of the tolerant state. Transplantation 57, 1195-1200.
7. CROXFORD, J.L., O'NEILL, J.K., ALI, R.R., BROWNE, K., BYRNES, A.P., DALLMAN, M.J., WOOD, M.J., FEDLMANN, M., and BAKER, D. (1998). Local gene therapy with CTLA4-immunoglobulin fusion protein in experimental allergic encephalomyelitis. Eur. J. Immunol. 28, 3904-3916.
8. CSETE, M., BENHAMOU, P., DRAZAN, K., WU, L., MCINTEE, D., AFRA, R., MULLEN, Y., BUSUTTIL, R., and SHAKED, A. (1995). Efficient gene transfer to pancreatic islets mediated by adenovirat vectors. Transplantation 59, 263-268.
9. DAI, Y., SCHWARZ, E., GU, D., ZHANG, W., SARVETNICK, N., and VERMA, I. (1995). Cellular and humorat immune responses to adenoviral vectors containing factor IX gene: tolerization of factor IX and vector antigens for long-term expression. Proc. Natl. Acad. Sci. U.S.A. 92, 1401-1405.
10. DAVID, A., COUPEL-CLAUCE, H., CHETRITT, J., TESSON, L., CASSARD, A., CHARREAU, B., SOULILLOU, J.P., and ANEGON, I. (1998). Anti-adenovirus immune responses in rats are enhanced by interteukin 4 but not interleukin 10 produced by recombinant adenovirus. Hum. Gene Ther. 9, 1755-1768.
11. DEWEY, R.A., MORRISSEY, G., COWSILL, C.M., STONE, D., BOLOGNANI, F., DODD, N.J., SOUTHGATE, T.D., KLATZMANN, D., LASSMANN, H., CASTRO, M.G., and LOWENSTEIN, P.R. (1999). Chronic brain inflammation and persistent herpes simplex virus 1 thymidine kinase expression in survivors of syngeneic glioma treated by adenovirus-mediated gene therapy: implications for clinical trials. Nat. Med. 5, 1256-1263.
12. EIZIRIK, D.L., DELANEY, C.A., GREEN, M.H., CUNNINGHAM, J.M., THORPE, J.R., PIPELEERS, D.G., HELLERSTROM, C., and GREEN, I.C. (1996). Nitric oxide donors decrease the function and survival of human pancreatic islets. Mol. Cell. Endocrinol. 118, 71-83.
13. FENG, S., QUICKEL, R.R., HOLLISTER-LOCK, J., MCLEOD, M., BONNER-WEIR, S., MULLIGAN, R.C., and WEIR, G.C. (1999). Prolonged xenograft survival of islets infected with small doses of adenovirus expressing CTLA4Ig. Transplantation 67, 1607-1613.
14. GAINER, A., KORBUTT, G., RAJOTTE, R., WARNOCK, G., and ELLIOT, J. (1997). Expression of CTLA4-Ig by biolistically transfected mouse islets promotes islet allograft survival. Transplantation 63, 1017-1021.
15. GAINER, A., SUAREZ-PINZON, W., MIN, W., SWISTON, J., HANCOCK-FRIESEN, C., KORBUTT, G., RAJOTTE, R., WARNOCK, G., and ELLIOT, J. (1998). Improved survival of biolistically transfected mouse islet allografts expressing CTLA4-Ig or soluble Fas ligand. Transplantation 66, 194-199.
16. GIANNOUKAKIS, N., RUDERT, W., GHIVIZZANI, S., GAMBOTO, A., RICORDI, C., TRUCCO, M., and ROBBINS, P. (1999). Adenoviral gene transfer of the interleukin-1 receptor antagonist protein to human islets prevents IL1b-induced b-cell impairment and activation of islet cell apoptosis in vitro. Diabetes 48, 1730-1736.
17. GREY, S., ARVELO, M., HASENKAMP, W., BACH, F., and FERRAN, C. (1999). A20 inhibits cytokine-apoptosis and nuclear factor kB-dependent gene activation in islets. J. Exp. Med. 190, 1135-1145.
18. GUILLOT, C., LE MAUFF, B., CUTURI, M.C., and ANEGON, I. (2000a). Gene therapy in transplantation in the year 2000: Moving towards clinical applications? Gene Ther. 7, 14-19.
19. GUILLOT, C., MATHIEU, P., COATHALEM, H., LE MAUFF, B., CASTRO, M.G., TESSON, L., USAL, C., LAUMONIER, T., BROUARD, S., SOULILLOU, J.P., LOWENSTEIN, P.R., CUTURI, M.C., and ANEGON, I. (2000b). Tolerance to cardiac allografts via local and systemic mechanisms after adenovirus-mediated CTLA4Ig expression. J. Immunol. 164, 5258-5268.
20. HADJIVASSILIOU, V., GREEN, M.H., JAMES, R.F., SWIFT, S.M., CLAYTON, H.A., and GREEN, I.C. (1998). Insulin secretion, DNA damage, and apoptosis in human and rat islets of Langerhans following exposure to nitric oxide, peroxynitrite, and cytokines. Nitric Oxide 2, 429-441.
21. JIANG, Z., FEINGOLD, E., KOCHANEK, S., and CLEMENS, P.R. (2002). Systemic delivery of a high-capacity adenoviral vector expressing mouse CTLA4Ig improves skeletal muscle gene therapy. Mol. Ther. 6, 369-376.
22. JOOSS, K., TURKA, L.A., and WILSON, J.M. (1998). Blunting of immune responses to adenoviral vectors in mouse liver and lung with CTLA4Ig. Gene Ther. 5, 309-319.
23. JUDGE, T.A., WU, Z., ZHENG, X.G., SHARPE, A.H., SAYEGH, M.H., and TURKA, L.A. (1999). The role of CD80, CD86, and CTLA4 in alloimmune responses and the induction of long-term allograft survival. J. Immunol. 162, 1947-1951.
24. KAY, M.A., HOLTERMAN, A.X., MEUSE, L., GOWN, A., OCHS, H.D., LINSLEY, P.S., and WILSON, C.B. (1995). Long-term hepatic adenovirus-mediated gene expression in mice following CTLA4Ig administration. Nat. Genet. 11, 191-197.
25. KITA, Y., LI, X.K., OHBA, M., FUNESHIMA, N., ENOSAWA, S., TAMURA, A., SUZUKI, K, AMEMIYA, H., HAYASHI, S., KAZUI, T., and SUZUKI, S. (1999). Prolonged cardiac allograft survival in rats systemically injected adenoviral vectors containing CTLA4Ig-gene. Transplantation 68, 758-766.
26. KRONCKE, K.D., RODRIGUEZ, M.L., KOLB, H., and KOLB-BACHOFEN, V. (1993). Cytotoxicity of activated rat macrophages against syngeneic islet cells is arginine-dependent, correlates with citrulline and nitrite concentrations and is identical to lysis by the nitric oxide donor nitroprusside. Diabetologia 36, 17-24.
27. LACY, P., and KOSTIANOVSKY, M. (1967). A method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes 16, 35-39.
28. LACY, P.E., DAVIE, J.M., and FINKE, E.H. (1979). Prolongation of islet allograft survival following in vitro culture (24 degrees C) and a single injection of ALS. Science 204, 312-313.
29. LARSEN, C., ELWOOD, E., ALEXANDER, D., RITCJIE, S., HENDRIX, R., TUCKER-BUREDEN, C., CHO, H., ARUFFO, A., HOLLENBAUGH, D., LINSLEY, P., WINN, K., and PEARSON, T. (1996). Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 381, 434-438.
30. LENSCHOW, D., ZENG, Y., THISTLETHWAITE, J., MONTAG, A., BRADY, W., GIBSON, M., LINSLEY, P., and BLUESTONE, J. (1992). Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4Ig. Science 257, 789-792.
31. LENSCHOW, D.J., WALUNAS, T.L., and BLUESTONE, J.A. (1996). CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 14, 233-258.
32. LEVISETTI, M., PADRID, P., SZOT, G., MITTAL, N., MEEHAN, S., WARDRIP, C., GRAY, G., BRUCE, D., THISTLETHWAITE, J.J., and BLUESTONE, J. (1997). Immunosuppressive effects of human CTLA4-Ig in a non human primate model of allogeneic pancreatic islet transplantation. J. Immunol. 159, 5187-5191.
33. LEW, A., BRADY, J., SILVA, A., COLIGAN, J., and GEORGIOU, H. (1996). Secretion of CTLA4Ig by an SV40 T antigen-transformed islet cell line inhibits graft rejection against the neoantigen. Transplantation 62, 83-89.
34. LIN, H., BOLLING, S., LINSLEY, P., WEI, R., GORDON, D., THOMPSON, C., and TURKA, L. (1993). Long-term acceptance of major histocompatibility complex mismatched cardiac allografts induced by CTLA4Ig plus donor-specific transfusion. J. Exp. Med. 178, 1801-1806.
35. MANDELBROT, D.A., FURUKAWA, Y., MCADAM, A.J., ALEXANDER, S.I., LIBBY, P., MITCHELL, R.N., and SHARPE, A.H. (1999). Expression of B7 molecules in recipient, not donor, mice determines the survival of cardiac allografts. J. Immunol. 163, 3753-3757.
36. MATSUMURA, Y., ZUO, X., PREHN, J., LINSLEY, P., MARCHEVSKY, A., KASS, R., MATLOFF, J., and JORDAN, S. (1995). Soluble CTLA4Ig modifies parameters of acute inflammation in rat lung allograft rejection without altering lymphocytes infiltration or transcription of key cytokines. Transplantation 59, 551-558.
37. NAKAGAWA, I., MURAKAMI, M., IJIMA, K, CHIKUMA, S., SAITO, I., KANEGAE, Y., ISIHKURA, H., YOSHIKI, T., OKAMOTO, H., KITABATAKE, A., and UEDE, T. (1998). Persistent and secondary adenovirus-mediated hepatic gene expression using adenovirus vector containing CTLA4IgG. Hum. Gene Ther. 9, 1739-1745.
38. OLTHOFF, K.M., JUDGE, T.A., GELMAN, A.E., DA SHEN, X., HANCOCK, W.W., TURKA, L.A., and SHAKED, A. (1998). Adenovirus-mediated gene transfer into cold-preserved liver allografts: Survival pattern and unresponsiveness following transduction with CTLA4Ig. Nat. Med. 4, 194-200.
39. PEARSON, T., ALEXANDER, D., WINN, K., LINSLEY, P., LOWRY, R., and LARSEN, C. (1994). Transplantation tolerance induced by CTLA4-Ig. Transplantation 57, 1701-1706.
40. PEREZ, V.L., VAN PARIJS, L., BIUCKIANS, A., ZHENG, X.X., STROM, T.B., and ABBAS, A.K. (1997). Induction of peripheral T cell tolerance in vivo requires CTLA-4 engagement. Immunity 6, 411-417.
41. SAADI, S., and PLATT, J.L. (1995). Transient perturbation of endothelial integrity induced by natural antibodies and complement. J. Exp. Med. 181, 21-31.
42. SARUKHAN, A., CAMUGLI, S., GJATA, B., VON BOEHMER, H., DANOS, O., and JOOSS, K. (2001). Successful interference with cellular immune responses to immunogenic proteins encoded by recombinant viral vectors. J. Virol. 75, 269-277.
43. SAYEGH, M., AKALIN, E., HANCOCK, W., RUSSELL, M., CARPENTER, C., LINSLEY, P., and TURKA, L. (1995). CD28-B7 blockade after alloantigenic challenge in vivo inhibits Th1 cytokines but spares Th2. J. Exp. Med. 1869-1874.
44. SCHAUB, M., STADLBAUER, T.H., CHANDRAKER, A., VELLA, J.P., TURKA, L.A., and SAYEGH, M.H. (1998). Comparative strategies to induce long-term graft acceptance in fully allogeneic renal versus cardiac allograft models by CD28-B7 T cell costimulatory blockade: role of thymus and spleen. J. Am. Soc. Nephrol. 9, 891-898.
45. SCHOWALTER, D.B., MEUSE, L., WILSON, C.B., LINSLEY, P.S., and KAY, M.A. (1997). Constitutive expression of murine CTLA4Ig from a recombinant adenovirus vector results in prolonged transgene expression. Gene Ther. 4, 853-860.
46. SHAPIRO, A.M., LAKEY, J.R., RYAN, E.A., KORBUTT, G.S., TOTH, E., WARNOCK, G.L., KNETEMAN, N.M., and RAJOTTE, R.V. (2000). Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen [see comments]. N. Engl. J. Med. 343, 230-238.
47. SIGALLA, J., DAVID, A., ANEGON, I., FICHE, M., HUVELIN, J., BOEFFARD, F., CASSARD, A., SOULILLOU, J., and LE MAUFF, B. (1997). Adenovirus-mediated gene transfer into isolated mouse adult pancreatic islets: Normal b-cell function despite induction of an anti-adenovirus immune response. Hum. Gene Ther. 8, 1625-1634.
48. STEURER, W., NICKERSON, P.W., STEELE, A.W., STEIGER, J., ZHENG, X.X., and STROM, T.B. (1995). Ex vivo coating of islet cell allografts with murine CTLA4/Fc promotes graft tolerance. J. Immunol. 155, 1165-1174.
49. SUTHERLAND, R.M., BRADY, J.L., GEORGIOU, H.M., THOMAS, H.E., and LEW, A.M. (2000). Protective effect of CTLA4Ig secreted by transgenic fetal pancreas allografts. Transplantation 69, 1806-1812.
50. SZOT, G.L., ZHOU, P., SHARPE, A.H., HE, G., KIM, O., NEWELL, K.A., BLUESTONE, J.A., and THISTLETHWAITE, J.R., Jr. (2000). Absence of host B7 expression is sufficient for long-term murine vascularized heart allograft survival. Transplantation 69, 904-909.
51. TOMASONI, S., AZZOLLINI, N., CASIRAGHI, F., CAPOGROSSI, M.C., REMUZZI, G., and BENIGNI, A. (2000). CTLA4Ig gene transfer prolongs survival and induces donor-specific tolerance in a rat renal allograft. J. Am. Soc. Nephrol. 11, 747-752.
52. TRAN, H., NICKERSON, P., RESTIFO, A., IVIS-WOODWARD, M., PATEL, A., ALLEN, R., STROM, T., and O'CONNELL, P. (1997). Distinct mechanisms for the induction and maintenance of allograft tolerance with CTLA4-Fc treatment. J. Immunol. 159, 2232-2239.
53. TURKA, L., LINSLEY, P., LIN, H., BRADY, W., LEIDEN, J., WEI, R., GIBSON, M., ZHENG, X., MYRDAL, S., GORDON, D., BAILEY, T., BOLLING, S., and THOMPSON, C. (1992). T-cell activation by the CD28 ligand B7 is required for cardiac allograft rejection in vivo. Proc. Natl. Acad. Sci. U.S.A. 89, 11102-11105.
54. WALLACE, P., RODGERS, J., LEYTZE, G., JOHNSON, J., and LINSLEY, P. (1995). Induction and reversal of long-lived specific unresponsiveness to a T-dependent antigen following CTLA4Ig treatment. J. Immunol. 154, 5885-5895.
55. WILLIAMS, M.A., TRAMBLEY, J., HA, J., ADAMS, A.B., DURHAM, M.M., REES, P., COWAN, S.R., PEARSON, T.C., and LARSEN, C.P. (2000). Genetic characterization of strain differences in the ability to mediate CD40/CD28-independent rejection of skin allografts. J. Immunol. 165, 6849-6857.
56. YANG, Z., ROSTAMI, S., KOEBERLEIN, B., BARKER, C., and NAJI, A. (1999). Cardiac allograft tolerance induced by intra-arterial infusion of recombinant adenoviral CTLA41g. Transplantation 67, 1517-1523.
57. YIN, D., and FATHMAN, C. (1995). Induction of tolerance to heart allografts in high responder rats by combining anti-CD4 with CTLA4Ig. J. Immunol. 155, 1655-1659.