Towards graft-specific immune suppression: Gene therapy of the transplanted kidney

Advanced Drug Delivery Reviews

Volumn 62, Issue 14, 2010, Pages 1358-1368

  Sandovici, Maria ^a,b   Deelman, Leo E ^a   Benigni, Ariela ^c   Henning, Robert H ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b MEDICAL CENTER LEEUWARDEN   (Netherlands)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

Gene delivery; Kidney transplantation; Liposome; Plasmid; Rejection; Small interfering RNA; Tolerance; Virus

Indexed keywords

GENE DELIVERY; KIDNEY TRANSPLANTATION; PLASMID; REJECTION; SMALL INTERFERING RNA; TOLERANCE;

GENE TRANSFER; GRAFTING (CHEMICAL); GRAFTS; MICROBIOLOGY; RNA; VIRUSES;

GENE THERAPY;

ABATACEPT; ADENOVIRUS VECTOR; CYCLOSPORIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; GAMMA INTERFERON; HISTONE DEACETYLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 4; LIPOSOME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OLIGODEOXYNUCLEOTIDE; PARVOVIRUS VECTOR; PLASMID DNA; RETROVIRUS VECTOR; SCATTER FACTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR SHARP 2; TRANSFORMING GROWTH FACTOR BETA3; TRYPTOPHAN; TUMOR NECROSIS FACTOR RECEPTOR P55 IMMUNOGLOBULIN; UNCLASSIFIED DRUG; VIRUS VECTOR;

ADD ON THERAPY; ALLOTRANSPLANTATION; ANTIGEN PRESENTING CELL; CELL BASED GENE THERAPY; CHRONIC GRAFT REJECTION; DENDRITIC CELL; ELECTROPORATION; FIBROSING ALVEOLITIS; GENE DELIVERY SYSTEM; GENE OVEREXPRESSION; GENE TARGETING; GENE THERAPY; GENE TRANSFER; GENETIC TRANSFECTION; GLOMERULOSCLEROSIS; HUMAN; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY FAILURE; KIDNEY FIBROSIS; KIDNEY GRAFT; KIDNEY GRAFT REJECTION; KIDNEY TRANSPLANTATION; LIPOSOMAL GENE DELIVERY SYSTEM; MICROBUBBLE; NEPHROTOXICITY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; PROMOTER REGION; QUALITY OF LIFE; REGULATORY T LYMPHOCYTE; REVIEW; SURVIVAL RATE; T LYMPHOCYTE; TH1 CELL; TH2 CELL; TRANSGENE;

DRUG DELIVERY SYSTEMS; GENE THERAPY; GENETIC VECTORS; GRAFT REJECTION; GRAFT SURVIVAL; HUMANS; IMMUNOSUPPRESSION; IMMUNOSUPPRESSIVE AGENTS; KIDNEY; KIDNEY FAILURE, CHRONIC; KIDNEY TRANSPLANTATION; PROMOTER REGIONS, GENETIC; TRANSPLANTATION TOLERANCE;

EID: 78649445784     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.addr.2010.07.010     Document Type: Review

References (129)

1. Laupacis A., Keown P., Pus N., Krueger H., Ferguson B., Wong C., Muirhead N. A study of the quality of life and cost-utility of renal transplantation. Kidney Int. 1996, 50:235-242.
2. Wolfe R.A., Ashby V.B., Milford E.L., Ojo A.O., Ettenger R.E., Agodoa L.Y., Held P.J., Port F.K. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N Engl J. Med. 1999, 341:1725-1730.
3. Halloran P.F. Immunosuppressive drugs for kidney transplantation. N Engl J. Med. 2004, 351:2715-2729.
4. Kotton C.N., Fishman J.A. Viral infection in the renal transplant recipient. J. Am. Soc. Nephrol. 2005, 16:1758-1774.
5. Patel R. Infections in recipients of kidney transplants. Infect. Dis. Clin. North Am. 2001, 15:901-952. xi.
6. Buell J.F., Gross T.G., Woodle E.S. Malignancy after transplantation. Transplantation 2005, 80:S254-S264.
7. Marcen R. Immunosuppressive drugs in kidney transplantation: impact on patient survival, and incidence of cardiovascular disease, malignancy and infection. Drugs 2009, 69:2227-2243.
8. Luan F.L., Steffick D.E., Ojo A.O. Steroid-free maintenance immunosuppression in kidney transplantation: is it time to consider it as a standard therapy?. Kidney Int. 2009, 76:825-830.
9. Vincenti F., Friman S., Scheuermann E., Rostaing L., Jenssen T., Campistol J.M., Uchida K., Pescovitz M.D., Marchetti P., Tuncer M., Citterio F., Wiecek A., Chadban S., El Shahawy M., Budde K., Goto N. Results of an international, randomized trial comparing glucose metabolism disorders and outcome with cyclosporine versus tacrolimus. Am. J. Transplant. 2007, 7:1506-1514.
10. Ekberg H., Tedesco-Silva H., Demirbas A., Vitko S., Nashan B., Gurkan A., Margreiter R., Hugo C., Grinyo J.M., Frei U., Vanrenterghem Y., Daloze P., Halloran P.F. Reduced exposure to calcineurin inhibitors in renal transplantation. N Engl J. Med. 2007, 357:2562-2575.
11. Ekberg H., Grinyo J., Nashan B., Vanrenterghem Y., Vincenti F., Voulgari A., Truman M., Nasmyth-Miller C., Rashford M. Cyclosporine sparing with mycophenolate mofetil, daclizumab and corticosteroids in renal allograft recipients: the CAESAR Study. Am. J. Transplant. 2007, 7:560-570.
12. Yates P.J., Nicholson M.L. The aetiology and pathogenesis of chronic allograft nephropathy. Transpl. Immunol. 2006, 16:148-157.
13. Hanss B., Bruggeman L.A. Applications of gene therapy to kidney disease. Curr. Opin. Nephrol. Hypertens. 2003, 12:439-445.
14. Phillips B., Giannoukakis N., Trucco M. Renal diseases as targets of gene therapy. Contrib. Nephrol. 2008, 159:1-12.
15. Al Awqati Q., Oliver J.A. Stem cells in the kidney. Kidney Int. 2002, 61:387-395.
16. Fechner H., Haack A., Wang H., Wang X., Eizema K., Pauschinger M., Schoemaker R., Veghel R., Houtsmuller A., Schultheiss H.P., Lamers J., Poller W. Expression of coxsackie adenovirus receptor and alphav-integrin does not correlate with adenovector targeting in vivo indicating anatomical vector barriers. Gene Ther. 1999, 6:1520-1535.
17. Somiari S., Glasspool-Malone J., Drabick J.J., Gilbert R.A., Heller R., Jaroszeski M.J., Malone R.W. Theory and in vivo application of electroporative gene delivery. Mol. Ther. 2000, 2:178-187.
18. Taniyama Y., Tachibana K., Hiraoka K., Aoki M., Yamamoto S., Matsumoto K., Nakamura T., Ogihara T., Kaneda Y., Morishita R. Development of safe and efficient novel nonviral gene transfer using ultrasound: enhancement of transfection efficiency of naked plasmid DNA in skeletal muscle. Gene Ther. 2002, 9:372-380.
19. Ferrara K.W. Driving delivery vehicles with ultrasound. Adv. Drug Deliv. Rev. 2008, 60:1097-1102.
20. Schmidt-Wolf G.D., Schmidt-Wolf I.G. Non-viral and hybrid vectors in human gene therapy: an update. Trends Mol. Med. 2003, 9:67-72.
21. Tomasoni S., Azzollini N., Casiraghi F., Capogrossi M.C., Remuzzi G., Benigni A. CTLA4Ig gene transfer prolongs survival and induces donor-specific tolerance in a rat renal allograft. J. Am. Soc. Nephrol. 2000, 11:747-752.
22. Liu F., Song Y., Liu D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 1999, 6:1258-1266.
23. Maruyama H., Higuchi N., Nishikawa Y., Hirahara H., Iino N., Kameda S., Kawachi H., Yaoita E., Gejyo F., Miyazaki J. Kidney-targeted naked DNA transfer by retrograde renal vein injection in rats. Hum. Gene Ther. 2002, 13:455-468.
24. Wu X., Gao H., Pasupathy S., Tan P.H., Ooi L.L., Hui K.M. Systemic administration of naked DNA with targeting specificity to mammalian kidneys. Gene Ther. 2005, 12:477-486.
25. Isaka Y., Yamada K., Takabatake Y., Mizui M., Miura-Tsujie M., Ichimaru N., Yazawa K., Utsugi R., Okuyama A., Hori M., Imai E., Takahara S. Electroporation-mediated HGF gene transfection protected the kidney against graft injury. Gene Ther. 2005, 12:815-820.
26. Franquesa M., Alperovich G., Herrero-Fresneda I., Lloberas N., Bolanos N., Fillat C., Rama I., Cruzado J.M., Grinyo J.M., Torras J. Direct electrotransfer of hHGF gene into kidney ameliorates ischemic acute renal failure. Gene Ther. 2005, 12:1551-1558.
27. Azuma H., Tomita N., Kaneda Y., Koike H., Ogihara T., Katsuoka Y., Morishita R. Transfection of NFkappaB-decoy oligodeoxynucleotides using efficient ultrasound-mediated gene transfer into donor kidneys prolonged survival of rat renal allografts. Gene Ther. 2003, 10:415-425.
28. Benigni A., Tomasoni S., Lutz J., Amuchastegui S., Capogrossi M.C., Remuzzi G. Nonviral and viral gene transfer to the kidney in the context of transplantation. Nephron 2000, 85:307-316.
29. Vos I.H., Govers R., Grone H.J., Kleij L., Schurink M., De Weger R.A., Goldschmeding R., Rabelink T.J. NFkappaB decoy oligodeoxynucleotides reduce monocyte infiltration in renal allografts. FASEB J. 2000, 14:815-822.
30. Dragun D., Tullius S.G., Park J.K., Maasch C., Lukitsch I., Lippoldt A., Gross V., Luft F.C., Haller H. ICAM-1 antisense oligodesoxynucleotides prevent reperfusion injury and enhance immediate graft function in renal transplantation. Kidney Int. 1998, 54:590-602.
31. Imai E., Isaka Y. Strategies of gene transfer to the kidney. Kidney Int. 1998, 53:264-272.
32. Kita J., Kobayashi E., Hishinuma A., Kaneda Y. Genetic modification of cold-preserved renal grafts using HSP70 or bcl-2 HVJ-liposome method. Transpl. Immunol. 2003, 11:7-14.
33. Hamilton A.J., Baulcombe D.C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 1999, 286:950-952.
34. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411:494-498.
35. Tijsterman M., Plasterk R.H. Dicers at RISC; the mechanism of RNAi. Cell 2004, 117:1-3.
36. Hamar P., Song E., Kokeny G., Chen A., Ouyang N., Lieberman J. Small interfering RNA targeting Fas protects mice against renal ischemia-reperfusion injury. Proc. Natl Acad. Sci. USA 2004, 101:14883-14888.
37. Zheng X., Zhang X., Sun H., Feng B., Li M., Chen G., Vladau C., Chen D., Suzuki M., Min L., Liu W., Zhong R., Garcia B., Jevnikar A., Min W.P. Protection of renal ischemia injury using combination gene silencing of complement 3 and caspase 3 genes. Transplantation 2006, 82:1781-1786.
38. Zheng X., Feng B., Chen G., Zhang X., Li M., Sun H., Liu W., Vladau C., Liu R., Jevnikar A.M., Garcia B., Zhong R., Min W.P. Preventing renal ischemia-reperfusion injury using small interfering RNA by targeting complement 3 gene. Am. J. Transplant. 2006, 6:2099-2108.
39. Zheng X., Zhang X., Feng B., Sun H., Suzuki M., Ichim T., Kubo N., Wong A., Min L.R., Budohn M.E., Garcia B., Jevnikar A.M., Min W.P. Gene silencing of complement C5a receptor using siRNA for preventing ischemia/reperfusion injury. Am. J. Pathol. 2008, 173:973-980.
40. Feng B., Chen G., Zheng X., Sun H., Zhang X., Zhang Z.X., Xiang Y., Ichim T.E., Garcia B., Luke P., Jevnikar A.M., Min W.P. Small interfering RNA targeting RelB protects against renal ischemia-reperfusion injury. Transplantation 2009, 87:1283-1289.
41. Zheng X., Lian D., Wong A., Bygrave M., Ichim T.E., Khoshniat M., Zhang X., Sun H., De Zordo T., Lacefield J.C., Garcia B., Jevnikar A.M., Min W.P. Novel small interfering RNA-containing solution protecting donor organs in heart transplantation. Circulation 2009, 120:1099-1107. 1.
42. Luo G.H., Lu Y.P., Song J., Yang L., Shi Y.J., Li Y.P. Inhibition of connective tissue growth factor by small interfering RNA prevents renal fibrosis in rats undergoing chronic allograft nephropathy. Transplant. Proc. 2008, 40:2365-2369.
43. Molitoris B.A., Dagher P.C., Sandoval R.M., Campos S.B., Ashush H., Fridman E., Brafman A., Faerman A., Atkinson S.J., Thompson J.D., Kalinski H., Skaliter R., Erlich S., Feinstein E. siRNA targeted to p53 attenuates ischemic and cisplatin-induced acute kidney injury. J. Am. Soc. Nephrol. 2009, 20:1754-1764.
44. Du C., Wang S., Diao H., Guan Q., Zhong R., Jevnikar A.M. Increasing resistance of tubular epithelial cells to apoptosis by shRNA therapy ameliorates renal ischemia-reperfusion injury. Am. J. Transplant. 2006, 6:2256-2267.
45. Schiedner G., Morral N., Parks R.J., Wu Y., Koopmans S.C., Langston C., Graham F.L., Beaudet A.L., Kochanek S. Genomic DNA transfer with a high-capacity adenovirus vector results in improved in vivo gene expression and decreased toxicity. Nat. Genet. 1998, 18:180-183.
46. Alba R., Bosch A., Chillon M. Gutless adenovirus: last-generation adenovirus for gene therapy. Gene Ther. 2005, 12(Suppl 1):S18-S27.
47. Dmitriev I., Krasnykh V., Miller C.R., Wang M., Kashentseva E., Mikheeva G., Belousova N., Curiel D.T. An adenovirus vector with genetically modified fibers demonstrates expanded tropism via utilization of a coxsackievirus and adenovirus receptor-independent cell entry mechanism. J. Virol. 1998, 72:9706-9713.
48. McDonald G.A., Zhu G., Li Y., Kovesdi I., Wickham T.J., Sukhatme V.P. Efficient adenoviral gene transfer to kidney cortical vasculature utilizing a fiber modified vector. J. Gene Med. 1999, 1:103-110.
49. Barnett B.G., Crews C.J., Douglas J.T. Targeted adenoviral vectors. Biochim. Biophys. Acta 2002, 1575:1-14.
50. Pellegrini C., O'Brien T., Jeppsson A., Fitzpatrick L.A., Yap J., Tazelaar H.D., McGregor C.G. Influence of temperature on adenovirus-mediated gene transfer. Eur. J. Cardiothorac. Surg. 1998, 13:599-603.
51. Heikkila P., Parpala T., Lukkarinen O., Weber M., Tryggvason K. Adenovirus-mediated gene transfer into kidney glomeruli using an ex vivo and in vivo kidney perfusion system - first steps towards gene therapy of Alport syndrome. Gene Ther. 1996, 3:21-27.
52. Moullier P., Friedlander G., Calise D., Ronco P., Perricaudet M., Ferry N. Adenoviral-mediated gene transfer to renal tubular cells in vivo. Kidney Int. 1994, 45:1220-1225.
53. Reddy P.S., Sakhuja K., Ganesh S., Yang L., Kayda D., Brann T., Pattison S., Golightly D., Idamakanti N., Pinkstaff A., Kaloss M., Barjot C., Chamberlain J.S., Kaleko M., Connelly S. Sustained human factor VIII expression in hemophilia A mice following systemic delivery of a gutless adenoviral vector. Mol. Ther. 2002, 5:63-73.
54. Zou L., Zhou H., Pastore L., Yang K. Prolonged transgene expression mediated by a helper-dependent adenoviral vector (hdAd) in the central nervous system. Mol. Ther. 2000, 2:105-113.
55. Cassivi S.D., Liu M., Boehler A., Pierre A., Tanswell A.K., O'Brodovich H., Mullen J.B., Slutsky A.S., Keshavjee S.H. Transplant immunosuppression increases and prolongs transgene expression following adenoviral-mediated transfection of rat lungs. J. Heart Lung Transplant. 2000, 19:984-994.
56. Zeigler S.T., Kerby J.D., Curiel D.T., Diethelm A.G., Thompson J.A. Molecular conjugate-mediated gene transfer into isolated human kidneys. Transplantation 1996, 61:812-817.
57. Parpala-Sparman T., Lukkarinen O., Heikkila P., Tryggvason K. A novel surgical organ perfusion method for effective ex vivo and in vivo gene transfer into renal glomerular cells. Urol. Res. 1999, 27:97-102.
58. Brasile L., Stubenitsky B.M., Booster M.H., Arenada D., Haisch C., Kootstra G. Transfection and transgene expression in a human kidney during ex vivo warm perfusion. Transplant. Proc. 2002, 34:2624.
59. Blydt-Hansen T.D., Katori M., Lassman C., Ke B., Coito A.J., Iyer S., Buelow R., Ettenger R., Busuttil R.W., Kupiec-Weglinski J.W. Gene transfer-induced local heme oxygenase-1 overexpression protects rat kidney transplants from ischemia/reperfusion injury. J. Am. Soc. Nephrol. 2003, 14:745-754.
60. Sandovici M., Deelman L.E., van Goor H., Helfrich W., de Zeeuw D., Henning R.H. Adenovirus-mediated interleukin-13 gene therapy attenuates acute kidney allograft injury. J. Gene Med. 2007, 9:1024-1032.
61. Sandovici M., Henning R.H., van Goor H., Helfrich W., de Zeeuw D., Deelman L.E. Systemic gene therapy with interleukin-13 attenuates renal ischemia-reperfusion injury. Kidney Int. 2008, 73:1364-1373.
62. van Goor H., Coers W., van der Horst M.L., Huitema S., Suurmeijer A.J. Distribution of cytoskeletal proteins, integrins, leukocyte adhesion molecules and extracellular matrix proteins in plastic-embedded human and rat kidneys. Anal. Quant. Cytol. Histol. 2001, 23:345-354.
63. Belousova N., Krendelchtchikova V., Curiel D.T., Krasnykh V. Modulation of adenovirus vector tropism via incorporation of polypeptide ligands into the fiber protein. J. Virol. 2002, 76:8621-8631.
64. Sandovici M., Deelman L.E., Smit-van Oosten A., van Goor H., Rots M.G., de Zeeuw D., Henning R.H. Enhanced transduction of fibroblasts in transplanted kidney with an adenovirus having an RGD motif in the HI loop. Kidney Int. 2006, 69:45-52.
65. Chen W.Y., Bailey E.C., McCune S.L., Dong J.Y., Townes T.M. Reactivation of silenced, virally transduced genes by inhibitors of histone deacetylase. Proc. Natl Acad. Sci. USA 1997, 94:5798-5803.
66. Woolf A.S., Palmer S.J., Snow M.L., Fine L.G. Creation of a functioning chimeric mammalian kidney. Kidney Int. 1990, 38:991-997.
67. Mah C., Byrne B.J., Flotte T.R. Virus-based gene delivery systems. Clin. Pharmacokinet. 2002, 41:901-911.
68. Gusella G.L., Fedorova E., Hanss B., Marras D., Klotman M.E., Klotman P.E. Lentiviral gene transduction of kidney. Hum. Gene Ther. 2002, 13:407-414.
69. Shou Z., Xiao H., Xu Y., Wang Y., Yang Y., Jiang H., Chen J., Yamada K., Miyamoto K. SHARP-2 gene silencing by lentiviral-based short hairpin RNA interference prolonged rat kidney transplant recipients' survival time. J. Int. Med. Res. 2009, 37:766-778.
70. Benigni A., Tomasoni S., Turka L.A., Longaretti L., Zentilin L., Mister M., Pezzotta A., Azzollini N., Noris M., Conti S., Abbate M., Giacca M., Remuzzi G. Adeno-associated virus-mediated CTLA4Ig gene transfer protects MHC-mismatched renal allografts from chronic rejection. J. Am. Soc. Nephrol. 2006, 17:1665-1672.
71. Sonntag K.C., Emery D.W., Yasumoto A., Haller G., Germana S., Sablinski T., Shimizu A., Yamada K., Shimada H., Arn S., Sachs D.H., LeGuern C. Tolerance to solid organ transplants through transfer of MHC class II genes. J. Clin. Invest. 2001, 107:65-71.
72. Morelli A.E., Thomson A.W. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat. Rev. Immunol. 2007, 7:610-621.
73. Lee W.C., Zhong C., Qian S., Wan Y., Gauldie J., Mi Z., Robbins P.D., Thomson A.W., Lu L. Phenotype, function, and in vivo migration and survival of allogeneic dendritic cell progenitors genetically engineered to express TGF-beta. Transplantation 1998, 66:1810-1817.
74. Zhang H.G., Su X., Liu D., Liu W., Yang P., Wang Z., Edwards C.K., Bluethmann H., Mountz J.D., Zhou T. Induction of specific T cell tolerance by Fas ligand-expressing antigen-presenting cells. J. Immunol. 1999, 162:1423-1430.
75. Porgador A., Irvine K.R., Iwasaki A., Barber B.H., Restifo N.P., Germain R.N. Predominant role for directly transfected dendritic cells in antigen presentation to CD8+ T cells after gene gun immunization. J. Exp. Med. 1998, 188:1075-1082.
76. Min W.P., Gorczynski R., Huang X.Y., Kushida M., Kim P., Obataki M., Lei J., Suri R.M., Cattral M.S. Dendritic cells genetically engineered to express Fas ligand induce donor-specific hyporesponsiveness and prolong allograft survival. J. Immunol. 2000, 164:161-167.
77. Hammer M.H., Schroder G., Risch K., Flugel A., Volk H.D., Lehmann M., Ritter T. Antigen-dependent transgene expression in kidney transplantation: a novel approach using gene-engineered T lymphocytes. J. Am. Soc. Nephrol. 2002, 13:511-518.
78. Chai J.G., Xue S.A., Coe D., Addey C., Bartok I., Scott D., Simpson E., Stauss H.J., Hori S., Sakaguchi S., Dyson J. Regulatory T cells, derived from naive CD4+. Transplantation 2005, 79:1310-1316.
79. Tsujie M., Isaka Y., Nakamura H., Imai E., Hori M. Electroporation-mediated gene transfer that targets glomeruli. J. Am. Soc. Nephrol. 2001, 12:949-954.
80. Tomita N., Higaki J., Morishita R., Kato K., Mikami H., Kaneda Y., Ogihara T. Direct in vivo gene introduction into rat kidney. Biochem. Biophys. Res. Commun. 1992, 186:129-134.
81. Tsujie M., Isaka Y., Ando Y., Akagi Y., Kaneda Y., Ueda N., Imai E., Hori M. Gene transfer targeting interstitial fibroblasts by the artificial viral envelope-type hemagglutinating virus of Japan liposome method. Kidney Int. 2000, 57:1973-1980.
82. Cornell L.D., Smith R.N., Colvin R.B. Kidney transplantation: mechanisms of rejection and acceptance. Annu. Rev. Pathol. 2008, 3:189-220.
83. Sharpe A.H., Freeman G.J. The B7-CD28 superfamily. Nat. Rev. Immunol. 2002, 2:116-126.
84. Atalar K., Afzali B., Lord G., Lombardi G. Relative roles of Th1 and Th17 effector cells in allograft rejection. Curr. Opin. Organ Transplant. 2009, 14:23-29.
85. Gorczynski R.M. Role of cytokines in allograft rejection. Curr. Pharm. Des. 2001, 7:1039-1057.
86. Nagano H., Nadeau K.C., Takada M., Kusaka M., Tilney N.L. Sequential cellular and molecular kinetics in acutely rejecting renal allografts in rats. Transplantation 1997, 63:1101-1108.
87. Muthukumar T., Dadhania D., Ding R., Snopkowski C., Naqvi R., Lee J.B., Hartono C., Li B., Sharma V.K., Seshan S.V., Kapur S., Hancock W.W., Schwartz J.E., Suthanthiran M. Messenger RNA for FOXP3 in the urine of renal-allograft recipients. N Engl J. Med. 2005, 353:2342-2351.
88. Vincenti F., Larsen C., Durrbach A., Wekerle T., Nashan B., Blancho G., Lang P., Grinyo J., Halloran P.F., Solez K., Hagerty D., Levy E., Zhou W., Natarajan K., Charpentier B. Costimulation blockade with belatacept in renal transplantation. N Engl J. Med. 2005, 353:770-781.
89. Tomasoni S., Azzollini N., Casiraghi F., Capogrossi M.C., Remuzzi G., Benigni A. CTLA4Ig gene transfer prolongs survival and induces donor-specific tolerance in a rat renal allograft. J. Am. Soc. Nephrol. 2000, 11:747-752.
90. Tomasoni S., Longaretti L., Azzollini N., Gagliardini E., Mister M., Buehler T., Remuzzi G., Benigni A. Favorable effect of cotransfection with TGF-beta and CTLA4Ig of the donor kidney on allograft survival. Am. J. Nephrol. 2004, 24:275-283.
91. Arai H., Gordon D., Nabel E.G., Nabel G.J. Gene transfer of Fas ligand induces tumor regression in vivo. Proc. Natl Acad. Sci. USA 1997, 94:13862-13867.
92. Martinez O.M., Krams S.M. Involvement of Fas-Fas ligand interactions in graft rejection. Int. Rev. Immunol. 1999, 18:527-546.
93. Swenson K.M., Ke B., Wang T., Markowitz J.S., Maggard M.A., Spear G.S., Imagawa D.K., Goss J.A., Busuttil R.W., Seu P. Fas ligand gene transfer to renal allografts in rats: effects on allograft survival. Transplantation 1998, 65:155-160.
94. Ke B., Coito A.J., Kato H., Zhai Y., Wang T., Sawitzki B., Seu P., Busuttil R.W., Kupiec-Weglinski J.W. Fas ligand gene transfer prolongs rat renal allograft survival and down-regulates anti-apoptotic Bag-1 in parallel with enhanced Th2-type cytokine expression. Transplantation 2000, 69:1690-1694.
95. Mellor A.L., Munn D.H. Tryptophan catabolism and regulation of adaptive immunity. J. Immunol. 2003, 170:5809-5813.
96. Fallarino F., Grohmann U., You S., McGrath B.C., Cavener D.R., Vacca C., Orabona C., Bianchi R., Belladonna M.L., Volpi C., Santamaria P., Fioretti M.C., Puccetti P. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J. Immunol. 2006, 176:6752-6761.
97. Munn D.H., Zhou M., Attwood J.T., Bondarev I., Conway S.J., Marshall B., Brown C., Mellor A.L. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998, 281:1191-1193.
98. Uyttenhove C., Pilotte L., Theate I., Stroobant V., Colau D., Parmentier N., Boon T., Van den Eynde B.J. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2, 3-dioxygenase. Nat. Med. 2003, 9:1269-1274.
99. Alexander A.M., Crawford M., Bertera S., Rudert W.A., Takikawa O., Robbins P.D., Trucco M. Indoleamine 2, 3-dioxygenase expression in transplanted NOD Islets prolongs graft survival after adoptive transfer of diabetogenic splenocytes. Diabetes 2002, 51:356-365.
100. Swanson K.A., Zheng Y., Heidler K.M., Mizobuchi T., Wilkes D.S. CDllc+ cells modulate pulmonary immune responses by production of indoleamine 2, 3-dioxygenase. Am. J. Respir. Cell Mol. Biol. 2004, 30:311-318.
101. Li J., Meinhardt A., Roehrich M.E., Golshayan D., Dudler J., Pagnotta M., Trucco M., Vassalli G. Indoleamine 2, 3-dioxygenase gene transfer prolongs cardiac allograft survival. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H3415-H3423.
102. Haniffa M.A., Wang X.N., Holtick U., Rae M., Isaacs J.D., Dickinson A.M., Hilkens C.M., Collin M.P. Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J. Immunol. 2007, 179:1595-1604.
103. Jalili R.B., Rayat G.R., Rajotte R.V., Ghahary A. Suppression of islet allogeneic immune response by indoleamine 2, 3 dioxygenase-expressing fibroblasts. J. Cell. Physiol. 2007, 213:137-143.
104. Kato H., Ritter T., Ke B., Murakami M., Kusano M., Busuttil R.W., Kupiec-Weglinski J.W. Adenovirus-mediated gene transfer of IL-4 prolongs rat renal allograft survival and inhibits the p21(ras)-activation pathway. Transplant. Proc. 2000, 32:245-246.
105. Yang J., Reutzel-Selke A., Steier C., Jurisch A., Tullius S.G., Sawitzki B., Kolls J., Volk H.D., Ritter T. Targeting of macrophage activity by adenovirus-mediated intragraft overexpression of TNFRp55-Ig, IL-12p40, and vIL-10 ameliorates adenovirus-mediated chronic graft injury, whereas stimulation of macrophages by overexpression of IFN-gamma accelerates chronic graft injury in a rat renal allograft model. J. Am. Soc. Nephrol. 2003, 14:214-225.
106. Gong N., Dong C., Chen Z., Chen X., Guo H., Zeng Z., Ming C., Klaus C.Z. Adenovirus-mediated antisense-ERK2 gene therapy attenuates chronic allograft nephropathy. Transplant. Proc. 2006, 38:3228-3230.
107. Kingsley C.I., Nadig S.N., Wood K.J. Transplantation tolerance: lessons from experimental rodent models. Transpl. Int. 2007, 20:828-841.
108. Kawai T., Cosimi A.B., Spitzer T.R., Tolkoff-Rubin N., Suthanthiran M., Saidman S.L., Shaffer J., Preffer F.I., Ding R., Sharma V., Fishman J.A., Dey B., Ko D.S., Hertl M., Goes N.B., Wong W., Williams W.W., Colvin R.B., Sykes M., Sachs D.H. HLA-mismatched renal transplantation without maintenance immunosuppression. N Engl J. Med. 2008, 358:353-361.
109. Scandling J.D., Busque S., Dejbakhsh-Jones S., Benike C., Millan M.T., Shizuru J.A., Hoppe R.T., Lowsky R., Engleman E.G., Strober S. Tolerance and chimerism after renal and hematopoietic-cell transplantation. N Engl J. Med. 2008, 358:362-368.
110. Girlanda R., Kirk A.D. Frontiers in nephrology: immune tolerance to allografts in humans. J. Am. Soc. Nephrol. 2007, 18:2242-2251.
111. Newell K.A., Larsen C.P. Tolerance assays: measuring the unknown. Transplantation 2006, 81:1503-1509.
112. Gorczynski R.M., Bransom J., Cattral M., Huang X., Lei J., Xiaorong L., Min W.P., Wan Y., Gauldie J. Synergy in induction of increased renal allograft survival after portal vein infusion of dendritic cells transduced to express TGFbeta and IL-10, along with administration of CHO cells expressing the regulatory molecule OX-2. Clin. Immunol. 2000, 95:182-189.
113. Tomasoni S., Aiello S., Cassis L., Noris M., Longaretti L., Cavinato R.A., Azzollini N., Pezzotta A., Remuzzi G., Benigni A. Dendritic cells genetically engineered with adenoviral vector encoding dnIKK2 induce the formation of potent CD4+ T-regulatory cells. Transplantation 2005, 79:1056-1061.
114. Aiello S., Cassis P., Cassis L., Tomasoni S., Benigni A., Pezzotta A., Cavinato R.A., Cugini D., Azzollini N., Mister M., Longaretti L., Thomson A.W., Remuzzi G., Noris M. DnIKK2-transfected dendritic cells induce a novel population of inducible nitric oxide synthase-expressing CD4+. Transplantation 2007, 83:474-484.
115. Yu G., Fang M., Gong M., Liu L., Zhong J., Feng W., Xiong P., Wang C.Y., Gong F. Steady state dendritic cells with forced IDO expression induce skin allograft tolerance by upregulation of regulatory T cells. Transpl. Immunol. 2008, 18:208-219.
116. Cook C.H., Bickerstaff A.A., Wang J.J., Nadasdy T., Della P.P., Colvin R.B., Orosz C.G. Spontaneous renal allograft acceptance associated with "regulatory" dendritic cells and IDO. J. Immunol. 2008, 180:3103-3112.
117. Grohmann U., Orabona C., Fallarino F., Vacca C., Calcinaro F., Falorni A., Candeloro P., Belladonna M.L., Bianchi R., Fioretti M.C., Puccetti P. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 2002, 3:1097-1101.
118. Stallone G., Infante B., Schena A., Battaglia M., Ditonno P., Loverre A., Gesualdo L., Schena F.P., Grandaliano G. Rapamycin for treatment of chronic allograft nephropathy in renal transplant patients. J. Am. Soc. Nephrol. 2005, 16:3755-3762.
119. Montanaro D., Gropuzzo M., Tulissi P., Vallone C., Boscutti G., Mioni R., Risaliti A., Baccarani U., Adani G.L., Sainz M., Bresadola F., Mioni G. Renoprotective effect of early inhibition of the renin-angiotensin system in renal transplant recipients. Transplant. Proc. 2005, 37:991-993.
120. Nankivell B.J., Borrows R.J., Fung C.L., O'Connell P.J., Allen R.D., Chapman J.R. The natural history of chronic allograft nephropathy. N Engl J. Med. 2003, 349:2326-2333.
121. Ritter T., Kupiec-Weglinski J.W. Gene therapy for the prevention of ischemia/reperfusion injury in organ transplantation. Curr. Gene Ther. 2005, 5:101-109.
122. Sandovici M., Deelman L.E., de Zeeuw D., van Goor H., Henning R.H. Immune modulation and graft protection by gene therapy in kidney transplantation. Eur. J. Pharmacol. 2008, 585:261-269.
123. Bottinger E.P. TGF-beta in renal injury and disease. Semin. Nephrol. 2007, 27:309-320.
124. Djamali A., Samaniego M. Fibrogenesis in kidney transplantation: potential targets for prevention and therapy. Transplantation 2009, 88:1149-1156.
125. Hwang M., Kim H.J., Noh H.J., Chang Y.C., Chae Y.M., Kim K.H., Jeon J.P., Lee T.S., Oh H.K., Lee Y.S., Park K.K. TGF-beta1 siRNA suppresses the tubulointerstitial fibrosis in the kidney of ureteral obstruction. Exp. Mol. Pathol. 2006, 81:48-54.
126. Lan H.Y., Mu W., Tomita N., Huang X.R., Li J.H., Zhu H.J., Morishita R., Johnson R.J. Inhibition of renal fibrosis by gene transfer of inducible Smad7 using ultrasound-microbubble system in rat UUO model. J. Am. Soc. Nephrol. 2003, 14:1535-1548.
127. Noh H., Oh E.Y., Seo J.Y., Yu M.R., Kim Y.O., Ha H., Lee H.B. Histone deacetylase-2 is a key regulator of diabetes- and transforming growth factor-beta1-induced renal injury. Am. J. Physiol. Renal Physiol. 2009, 297:F729-F739.
128. Herrero-Fresneda I., Torras J., Franquesa M., Vidal A., Cruzado J.M., Lloberas N., Fillat C., Grinyo J.M. HGF gene therapy attenuates renal allograft scarring by preventing the profibrotic inflammatory-induced mechanisms. Kidney Int. 2006, 70:265-274.
129. Mizui M., Isaka Y., Takabatake Y., Mizuno S., Nakamura T., Ito T., Imai E., Hori M. Electroporation-mediated HGF gene transfer ameliorated cyclosporine nephrotoxicity. Kidney Int. 2004, 65:2041-2053.