Role of IDO in Organ Transplantation: Promises and Difficulties

REFERENCES

• Lopez M. M., Valenzuela J. E., Alvarez F. C., Lopez-Alvarez M. R., Cecilia G. S., Paricio P. P. Long-term problems related to immunosuppression. Transpl Immunol 2006; 17: 31–35
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Thackray S. J., Mowat C. G., Chapman S. K. Exploring the mechanism of tryptophan 2,3-dioxygenase. Biochem Soc Trans 2008; 36: 1120–1123
   PubMed Web of Science ®Google Scholar
• Taylor M. W., Feng G. S. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. Faseb J 1991; 5: 2516–2522
   PubMed Web of Science ®Google Scholar
• Werner-Felmayer G., Werner E. R., Fuchs D., Hausen A., Reibnegger G., Wachter H. Characteristics of interferon induced tryptophan metabolism in human cells in vitro. Biochim Biophys Acta 1989; 1012: 140–147
   PubMed Web of Science ®Google Scholar
• Mahanonda R., Sa-Ard-Iam N., Montreekachon P., Pimkhaokham A., Yongvanichit K., Fukuda M. M., Pichyangkul S. IL-8 and IDO expression by human gingival fibroblasts via TLRs. J Immunol 2007; 178: 1151–1157
   PubMed Web of Science ®Google Scholar
• Furset G., Floisand Y., Sioud M. Impaired expression of indoleamine 2, 3-dioxygenase in monocyte-derived dendritic cells in response to Toll-like receptor-7/8 ligands. Immunology 2008; 123: 263–271
   PubMed Web of Science ®Google Scholar
• Grohmann U., Volpi C., Fallarino F., Bozza S., Bianchi R., Vacca C., Orabona C., Belladonna M. L., Ayroldi E., Nocentini G., Boon L., Bistoni F., Fioretti M. C., Romani L., Riccardi C., Puccetti P. Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat Med 2007; 13: 579–586
   PubMed Web of Science ®Google Scholar
• Reddy P., Sun Y., Toubai T., Duran-Struuck R., Clouthier S. G., Weisiger E., Maeda Y., Tawara I., Krijanovski O., Gatza E., Liu C., Malter C., Mascagni P., Dinarello C. A., Ferrara J. L. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J Clin Invest 2008; 118: 2562–2573
   PubMed Web of Science ®Google Scholar
• Beutelspacher S. C., Tan P. H., McClure M. O., Larkin D. F., Lechler R. I., George A. J. Expression of indoleamine 2,3-dioxygenase (IDO) by endothelial cells: Implications for the control of alloresponses. Am J Transplant 2006; 6: 1320–1330
   PubMed Web of Science ®Google Scholar
• Pantoja L. G., Miller R. D., Ramirez J. A., Molestina R. E., Summersgill J. T. Inhibition of Chlamydia pneumoniae replication in human aortic smooth muscle cells by gamma interferon-induced indoleamine 2, 3-dioxygenase activity. Infect Immun 2000; 68: 6478–6481
   PubMed Web of Science ®Google Scholar
• Pfefferkorn E. R. Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc Natl Acad Sci USA 1984; 81: 908–912
   PubMed Web of Science ®Google Scholar
• Oberdorfer C., Adams O., MacKenzie C. R., De Groot C. J., Daubener W. Role of IDO activation in anti-microbial defense in human native astrocytes. Adv Exp Med Biol 2003; 527: 15–26
   PubMedGoogle Scholar
• Munn D. H., Shafizadeh E., Attwood J. T., Bondarev I., Pashine A., Mellor A. L. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med 1999; 189: 1363–1372
   PubMed Web of Science ®Google Scholar
• Mellor A. L., Baban B., Chandler P., Marshall B., Jhaver K., Hansen A., Koni P. A., Iwashima M., Munn D. H. Cutting edge: Induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J Immunol 2003; 171: 1652–1655
   PubMed Web of Science ®Google Scholar
• Mellor A. L., Chandler P., Baban B., Hansen A. M., Marshall B., Pihkala J., Waldmann H., Cobbold S., Adams E., Munn D. H. Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2,3 dioxygenase. Int Immunol 2004; 16: 1391–1401
   PubMed Web of Science ®Google Scholar
• Munn D. H., Sharma M. D., Lee J. R., Jhaver K. G., Johnson T. S., Keskin D. B., Marshall B., Chandler P., Antonia S. J., Burgess R., Slingluff C. L., Jr., Mellor A. L. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 2002; 297: 1867–1870
   PubMed Web of Science ®Google Scholar
• Hirata F., Hayaishi O. Studies on indoleamine 2,3-dioxygenase. I. Superoxide anion as substrate. J Biol Chem 1975; 250: 5960–5966
   PubMed Web of Science ®Google Scholar
• Moffett J. R., Namboodiri M. A. Tryptophan and the immune response. Immunol Cell Biol 2003; 81: 247–265
   PubMed Web of Science ®Google Scholar
• Robinson C. M., Shirey K. A., Carlin J. M. Synergistic transcriptional activation of indoleamine dioxygenase by IFN-gamma and tumor necrosis factor-alpha. J Interferon Cytokine Res 2003; 23: 413–421
   PubMed Web of Science ®Google Scholar
• Puccetti P., Grohmann U. IDO and regulatory T cells: A role for reverse signalling and non-canonical NF-kappaB activation. Nat Rev Immunol 2007; 7: 817–823
   PubMed Web of Science ®Google Scholar
• Farrar M. A., Schreiber R. D. The molecular cell biology of interferon-gamma and its receptor. Annu Rev Immunol 1993; 11: 571–611
   PubMed Web of Science ®Google Scholar
• Braun D., Longman R. S., Albert M. L. A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood 2005; 106: 2375–2381
   PubMed Web of Science ®Google Scholar
• Hayaishi O. Utilization of superoxide anion by indoleamine oxygenase-catalyzed tryptophan and indoleamine oxidation. Adv Exp Med Biol 1996; 398: 285–289
   PubMedGoogle Scholar
• Thomas S. R., Stocker R. Redox reactions related to indoleamine 2,3-dioxygenase and tryptophan metabolism along the kynurenine pathway. Redox Rep 1999; 4: 199–220
   PubMed Web of Science ®Google Scholar
• Ball H. J., Sanchez-Perez A., Weiser S., Austin C. J., Astelbauer F., Miu J., McQuillan J. A., Stocker R., Jermiin L. S., Hunt N. H. Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene 2007; 396: 203–213
   PubMed Web of Science ®Google Scholar
• Metz R., Duhadaway J. B., Kamasani U., Laury-Kleintop L., Muller A. J., Prendergast G. C. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2,3-dioxygenase inhibitory compound D-1-methyl-tryptophan. Cancer Res 2007; 67: 7082–7087
   PubMed Web of Science ®Google Scholar
• Lob S., Konigsrainer A., Schafer R., Rammensee H. G., Opelz G., Terness P. Levo- but not dextro-1-methyl tryptophan abrogates the IDO activity of human dendritic cells. Blood 2008; 111: 2152–2154
   PubMed Web of Science ®Google Scholar
• Lob S., Konigsrainer A., Zieker D., Brucher B. L., Rammensee H. G., Opelz G., Terness P. IDO1 and IDO2 are expressed in human tumors: Levo- but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol Immunother 2009; 58: 153–157
   PubMed Web of Science ®Google Scholar
• Lee G. K., Park H. J., Macleod M., Chandler P., Munn D. H., Mellor A. L. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology 2002; 107: 452–460
   PubMed Web of Science ®Google Scholar
• Munn D. H., Sharma M. D., Baban B., Harding H. P., Zhang Y., Ron D., Mellor A. L. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 2005; 22: 633–642
   PubMed Web of Science ®Google Scholar
• Frumento G., Rotondo R., Tonetti M., Damonte G., Benatti U., Ferrara G. B. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med 2002; 196: 459–468
   PubMed Web of Science ®Google Scholar
• Terness P., Bauer T. M., Rose L., Dufter C., Watzlik A., Simon H., Opelz G. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: Mediation of suppression by tryptophan metabolites. J Exp Med 2002; 196: 447–457
   PubMed Web of Science ®Google Scholar
• Fallarino F., Grohmann U., Vacca C., Orabona C., Spreca A., Fioretti M. C., Puccetti P. T cell apoptosis by kynurenines. Adv Exp Med Biol 2003; 527: 183–190
   PubMed Web of Science ®Google Scholar
• Chen W., Liang X., Peterson A. J., Munn D. H., Blazar B. R. The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol 2008; 181: 5396–5404
   PubMed Web of Science ®Google Scholar
• Belladonna M. L., Grohmann U., Guidetti P., Volpi C., Bianchi R., Fioretti M. C., Schwarcz R., Fallarino F., Puccetti P. Kynurenine pathway enzymes in dendritic cells initiate tolerogenesis in the absence of functional IDO. J Immunol 2006; 177: 130–137
   PubMed Web of Science ®Google Scholar
• Hayashi T., Mo J. H., Gong X., Rossetto C., Jang A., Beck L., Elliott G. I., Kufareva I., Abagyan R., Broide D. H., Lee J., Raz E. 3-Hydroxyanthranilic acid inhibits PDK1 activation and suppresses experimental asthma by inducing T cell apoptosis. Proc Natl Acad Sci USA 2007; 104: 18619–18624
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Baban B., Chandler P., McCool D., Marshall B., Munn D. H., Mellor A. L. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J Reprod Immunol 2004; 61: 67–77
   PubMed Web of Science ®Google Scholar
• Sawitzki B., Kingsley C. I., Oliveira V., Karim M., Herber M., Wood K. J. IFN-gamma production by alloantigen-reactive regulatory T cells is important for their regulatory function in vivo. J Exp Med 2005; 201: 1925–1935
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Blair P. J., Riley J. L., Levine B. L., Lee K. P., Craighead N., Francomano T., Perfetto S. J., Gray G. S., Carreno B. M., June C. H. CTLA-4 ligation delivers a unique signal to resting human CD4 T cells that inhibits interleukin-2 secretion but allows Bcl-X(L) induction. J Immunol 1998; 160: 12–15
   PubMed Web of Science ®Google Scholar
• Collins A. V., Brodie D. W., Gilbert R. J., Iaboni A., Manso-Sancho R., Walse B., Stuart D. I., van der Merwe P. A., Davis S. J. The interaction properties of costimulatory molecules revisited. Immunity 2002; 17: 201–210
   PubMed Web of Science ®Google Scholar
• Fallarino F., Grohmann U., Hwang K. W., Orabona C., Vacca C., Bianchi R., Belladonna M. L., Fioretti M. C., Alegre M. L., Puccetti P. Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol 2003; 4: 1206–1212
   PubMed Web of Science ®Google Scholar
• Pree I., Bigenzahn S., Fuchs D., Koporc Z., Nierlich P., Winkler C., Brandacher G., Sykes M., Muehlbacher F., Langer F., Wekerle T. CTLA4Ig promotes the induction of hematopoietic chimerism and tolerance independently of indoleamine-2,3-dioxygenase. Transplantation 2007; 83: 663–667
   PubMed Web of Science ®Google Scholar
• Tan P. H., Yates J. B., Xue S. A., Chan C., Jordan W. J., Harper J. E., Watson M. P., Dong R., Ritter M. A., Lechler R. I., Lombardi G., George A. J. Creation of tolerogenic human dendritic cells via intracellular CTLA4: a novel strategy with potential in clinical immunosuppression. Blood 2005; 106: 2936–2943
   PubMed Web of Science ®Google Scholar
• Moreland L., Bate G., Kirkpatrick P. Abatacept. Nat Rev Drug Discov 2006; 5: 185–186
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Lee R. S., Rusche J. R., Maloney M. E., Sachs D. H., Sayegh M. H., Madsen J. C. CTLA4Ig-induced linked regulation of allogeneic T cell responses. J Immunol 2001; 166: 1572–1582
   Google Scholar
• Roy-Chaudhury P., Nickerson P. W., Manfro R. C., Zheng X. X., Steiger J., Li Y. S., Strom T. B. CTLA4Ig attenuates accelerated rejection (presensitization) in the mouse islet allograft model. Transplantation 1997; 64: 172–175
   Google Scholar
• Davis P. M., Abraham R., Xu L., Nadler S. G., Suchard S. J. Abatacept binds to the Fc receptor CD64 but does not mediate complement-dependent cytotoxicity or antibody-dependent cellular cytotoxicity. J Rheumatol 2007; 34: 2204–2210
   PubMed Web of Science ®Google Scholar
• Davis P. M., Nadler S. G., Stetsko D. K., Suchard S. J. Abatacept modulates human dendritic cell-stimulated T-cell proliferation and effector function independent of IDO induction. Clin Immunol 2008; 126: 38–47
   PubMed Web of Science ®Google Scholar
• Scheipers P., Reiser H. Fas-independent death of activated CD4(+) T lymphocytes induced by CTLA-4 crosslinking. Proc Natl Acad Sci USA 1998; 95: 10083–10088
   PubMed Web of Science ®Google Scholar
• Haspot F., Seveno C., Dugast A. S., Coulon F., Renaudin K., Usal C., Hill M., Anegon I., Heslan M., Josien R., Brouard S., Soulillou J. P., Vanhove B. Anti-CD28 antibody-induced kidney allograft tolerance related to tryptophan degradation and TCR class II B7 regulatory cells. Am J Transplant 2005; 5: 2339–2348
   PubMed Web of Science ®Google Scholar
• Stoiber D., Kovarik P., Cohney S., Johnston J. A., Steinlein P., Decker T. Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-gamma. J Immunol 1999; 163: 2640–2647
   PubMedGoogle Scholar
• Logue E. C., Sha W. C. CD28-B7 bidirectional signaling: A two-way street to activation. Nat Immunol 2004; 5: 1103–1105
   PubMedGoogle Scholar
• Orabona C., Grohmann U., Belladonna M. L., Fallarino F., Vacca C., Bianchi R., Bozza S., Volpi C., Salomon B. L., Fioretti M. C., Romani L., Puccetti P. CD28 induces immunostimulatory signals in dendritic cells via CD80 and CD86. Nat Immunol 2004; 5: 1134–1142
   PubMed Web of Science ®Google Scholar
• Orabona C., Belladonna M. L., Vacca C., Bianchi R., Fallarino F., Volpi C., Gizzi S., Fioretti M. C., Grohmann U., Puccetti P. Cutting edge: Silencing suppressor of cytokine signaling 3 expression in dendritic cells turns CD28-Ig from immune adjuvant to suppressant. J Immunol 2005; 174: 6582–6586
   PubMed Web of Science ®Google Scholar
• Orabona C., Pallotta M. T., Volpi C., Fallarino F., Vacca C., Bianchi R., Belladonna M. L., Fioretti M. C., Grohmann U., Puccetti P. SOCS3 drives proteasomal degradation of indoleamine 2,3-dioxygenase (IDO) and antagonizes IDO-dependent tolerogenesis. Proc Natl Acad Sci U S A 2008; 105: 20828–20833
   PubMed Web of Science ®Google Scholar
• Larsen C. P., Elwood E. T., Alexander D. Z., Ritchie S. C., Hendrix R., Tucker-Burden C., Cho H. R., Aruffo A., Hollenbaugh D., Linsley P. S., Winn K. J., Pearson T. C. Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 1996; 381: 434–438
   PubMed Web of Science ®Google Scholar
• Adams A. B., Shirasugi N., Jones T. R., Durham M. M., Strobert E. A., Cowan S., Rees P., Hendrix R., Price K., Kenyon N. S., Hagerty D., Townsend R., Hollenbaugh D., Pearson T. C., Larsen C. P. Development of a chimeric anti-CD40 monoclonal antibody that synergizes with LEA29Y to prolong islet allograft survival. J Immunol 2005; 174: 542–550
   PubMed Web of Science ®Google Scholar
• Guillot C., Guillonneau C., Mathieu P., Gerdes C. A., Menoret S., Braudeau C., Tesson L., Renaudin K., Castro M. G., Lowenstein P. R., Anegon I. Prolonged blockade of CD40-CD40 ligand interactions by gene transfer of CD40Ig results in long-term heart allograft survival and donor-specific hyporesponsiveness, but does not prevent chronic rejection. J Immunol 2002; 168: 1600–1609
   Google Scholar
• Quezada S. A., Jarvinen L. Z., Lind E. F., Noelle R. J. CD40/CD154 interactions at the interface of tolerance and immunity. Annu Rev Immunol 2004; 22: 307–328
   PubMed Web of Science ®Google Scholar
• Honey K., Cobbold S. P., Waldmann H. CD40 ligand blockade induces CD4+ T cell tolerance and linked suppression. J Immunol 1999; 163: 4805–4810
   PubMedGoogle Scholar
• Monk N. J., Hargreaves R. E., Marsh J. E., Farrar C. A., Sacks S. H., Millrain M., Simpson E., Dyson J., Jurcevic S. Fc-dependent depletion of activated T cells occurs through CD40L-specific antibody rather than costimulation blockade. Nat Med 2003; 9: 1275–1280
   PubMedGoogle Scholar
• Blair P. J., Riley J. L., Harlan D. M., Abe R., Tadaki D. K., Hoffmann S. C., White L., Francomano T., Perfetto S. J., Kirk A. D., June C. H. CD40 ligand (CD154) triggers a short-term CD4(+) T cell activation response that results in secretion of immunomodulatory cytokines and apoptosis. J Exp Med 2000; 191: 651–660
   PubMedGoogle Scholar
• Albert M. L., Jegathesan M., Darnell R. B. Dendritic cell maturation is required for the cross-tolerization of CD8+ T cells. Nat Immunol 2001; 2: 1010–1017
   PubMed Web of Science ®Google Scholar
• Grohmann U., Fallarino F., Silla S., Bianchi R., Belladonna M. L., Vacca C., Micheletti A., Fioretti M. C., Puccetti P. CD40 ligation ablates the tolerogenic potential of lymphoid dendritic cells. J Immunol 2001; 166: 277–283
   PubMed Web of Science ®Google Scholar
• Martin E., O'Sullivan B., Low P., Thomas R. Antigen-specific suppression of a primed immune response by dendritic cells mediated by regulatory T cells secreting interleukin-10. Immunity 2003; 18: 155–167
   PubMed Web of Science ®Google Scholar
• Hancock W. W., Sayegh M. H., Zheng X. G., Peach R., Linsley P. S., Turka L. A. Costimulatory function and expression of CD40 ligand, CD80, and CD86 in vascularized murine cardiac allograft rejection. Proc Natl Acad Sci U S A 1996; 93: 13967–13972
   PubMed Web of Science ®Google Scholar
• Jones N. D., Van Maurik A., Hara M., Spriewald B. M., Witzke O., Morris P. J., Wood K. J. CD40-CD40 ligand-independent activation of CD8+ T cells can trigger allograft rejection. J Immunol 2000; 165: 1111–1118
   PubMed Web of Science ®Google Scholar
• Kirk A. D., Burkly L. C., Batty D. S., Baumgartner R. E., Berning J. D., Buchanan K., Fechner J. H., Jr., Germond R. L., Kampen R. L., Patterson N. B., Swanson S. J., Tadaki D. K., TenHoor C. N., White L., Knechtle S. J., Harlan D. M. Treatment with humanized monoclonal antibody against CD154 prevents acute renal allograft rejection in nonhuman primates. Nat Med 1999; 5: 686–693
   PubMed Web of Science ®Google Scholar
• Guillonneau C., Hill M., Hubert F. X., Chiffoleau E., Herve C., Li X. L., Heslan M., Usal C., Tesson L., Menoret S., Saoudi A., Le Mauff B., Josien R., Cuturi M. C., Anegon I. CD40Ig treatment results in allograft acceptance mediated by CD8CD45RC T cells, IFN-gamma, and indoleamine 2,3-dioxygenase. J Clin Invest 2007; 117: 1096–1106
   PubMed Web of Science ®Google Scholar
• von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol 2005; 6: 338–344
   PubMed Web of Science ®Google Scholar
• Sharma M. D., Baban B., Chandler P., Hou D. Y., Singh N., Yagita H., Azuma M., Blazar B. R., Mellor A. L., Munn D. H. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest 2007; 117: 2570–2582
   PubMed Web of Science ®Google Scholar
• Thebault P., Condamine T., Heslan M., Hill M., Bernard I., Saoudi A., Josien R., Anegon I., Cuturi M. C., Chiffoleau E. Role of IFNgamma in allograft tolerance mediated by CD4+CD25+ regulatory T cells by induction of IDO in endothelial cells. Am J Transplant 2007; 7: 2472–2482
   PubMed Web of Science ®Google Scholar
• Fallarino F., Asselin-Paturel C., Vacca C., Bianchi R., Gizzi S., Fioretti M. C., Trinchieri G., Grohmann U., Puccetti P. Murine plasmacytoid dendritic cells initiate the immunosuppressive pathway of tryptophan catabolism in response to CD200 receptor engagement. J Immunol 2004; 173: 3748–3754
   PubMed Web of Science ®Google Scholar
• Colvin B. L., Sumpter T. L., Tokita D., Salati J., Mellor A. L., Thomson A. W. Allostimulatory activity of bone marrow-derived plasmacytoid dendritic cells is independent of indoleamine dioxygenase but regulated by inducible costimulator ligand expression. Hum Immunol 2009; 70: 313–320
   Google Scholar
• Colonna M., Trinchieri G., Liu Y. J. Plasmacytoid dendritic cells in immunity. Nat Immunol 2004; 5: 1219–1226
   PubMed Web of Science ®Google Scholar
• Terness P., Chuang J. J., Bauer T., Jiga L., Opelz G. Regulation of human auto- and alloreactive T cells by indoleamine 2,3-dioxygenase (IDO)-producing dendritic cells: too much ado about IDO?. Blood 2005; 105: 2480–2486
   PubMed Web of Science ®Google Scholar
• Terness P., Chuang J. J., Opelz G. The immunoregulatory role of IDO-producing human dendritic cells revisited. Trends Immunol 2006; 27: 68–73
   PubMed Web of Science ®Google Scholar
• Lob S., Ebner S., Wagner S., Weinreich J., Schafer R., Konigsrainer A. Are indoleamine-2,3-dioxygenase producing human dendritic cells a tool for suppression of allogeneic t-cell responses?. Transplantation 2007; 83: 468–473
   Google Scholar
• de Faudeur G., de Trez C., Muraille E., Leo O. Normal development and function of dendritic cells in mice lacking IDO-1 expression. Immunol Lett 2008; 118: 21–29
   PubMed Web of Science ®Google Scholar
• Munn D. H., Sharma M. D., Hou D., Baban B., Lee J. R., Antonia S. J., Messina J. L., Chandler P., Koni P. A., Mellor A. L. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J Clin Invest 2004; 114: 280–290
   PubMed Web of Science ®Google Scholar
• Muller A. J., Malachowski W. P., Prendergast G. C. Indoleamine 2,3-dioxygenase in cancer: Targeting pathological immune tolerance with small-molecule inhibitors. Expert Opin Ther Targets 2005; 9: 831–849
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Beutelspacher S. C., Pillai R., Watson M. P., Tan P. H., Tsang J., McClure M. O., George A. J., Larkin D. F. Function of indoleamine 2,3-dioxygenase in corneal allograft rejection and prolongation of allograft survival by over-expression. Eur J Immunol 2006; 36: 690–700
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Li Y., Tredget E. E., Ghaffari A., Lin X., Kilani R. T., Ghahary A. Local expression of indoleamine 2,3-dioxygenase protects engraftment of xenogeneic skin substitute. J Invest Dermatol 2006; 126: 128–136
   PubMed Web of Science ®Google Scholar
• Liu H., Liu L., Fletcher B. S., Visner G. A. Sleeping Beauty-based gene therapy with indoleamine 2,3-dioxygenase inhibits lung allograft fibrosis. Faseb J 2006; 20: 2384–2386
   PubMed Web of Science ®Google Scholar
• Liu H., Liu L., Fletcher B. S., Visner G. A. Novel action of indoleamine 2,3-dioxygenase attenuating acute lung allograft injury. Am J Respir Crit Care Med 2006; 173: 566–572
   PubMed Web of Science ®Google Scholar
• Liu H., Liu L., Visner G. A. Nonviral gene delivery with indoleamine 2,3-dioxygenase targeting pulmonary endothelium protects against ischemia-reperfusion injury. Am J Transplant 2007; 7: 2291–2300
   PubMed Web of Science ®Google Scholar
• Wee J. L., Christiansen D., Li Y. Q., Boyle W., Sandrin M. S. Suppression of cytotoxic and proliferative xenogeneic T-cell responses by transgenic expression of indoleamine 2,3-dioxygenase. Immunol Cell Biol 2008; 86: 460–465
   PubMed Web of Science ®Google Scholar
• Yu G., Dai H., Chen J., Duan L., Gong M., Liu L., Xiong P., Wang C. Y., Fang M., Gong F. Gene delivery of indoleamine 2,3-dioxygenase prolongs cardiac allograft survival by shaping the types of T-cell responses. J Gene Med 2008; 10: 754–761
   PubMed Web of Science ®Google Scholar
• Tan P. H., Tan P. L., George A. J., Chan C. L. Gene therapy for transplantation with viral vectors—how much of the promise has been realised?. Expert Opin Biol Ther 2006; 6: 759–772
   PubMed Web of Science ®Google Scholar
• Tan P. H., Chan C. L., George A. J. Strategies to improve non-viral vectors—potential applications in clinical transplantation. Expert Opin Biol Ther 2006; 6: 619–630
   PubMed Web of Science ®Google Scholar
• Laurence J. M., Wang C., Park E. T., Buchanan A., Clouston A., Allen R. D., McCaughan G. W., Bishop G. A., Sharland A. F. Blocking indoleamine dioxygenase activity early after rat liver transplantation prevents long-term survival but does not cause acute rejection. Transplantation 2008; 85: 1357–1361
   PubMed Web of Science ®Google Scholar
• Bauer T. M., Jiga L. P., Chuang J. J., Randazzo M., Opelz G., Terness P. Studying the immunosuppressive role of indoleamine 2,3-dioxygenase: Tryptophan metabolites suppress rat allogeneic T-cell responses in vitro and in vivo. Transpl Int 2005; 18: 95–100
   PubMed Web of Science ®Google Scholar
• Cook C. H., Bickerstaff A. A., Wang J. J., Nadasdy T., Della Pelle P., Colvin R. B., Orosz C. G. Spontaneous renal allograft acceptance associated with “regulatory” dendritic cells and IDO. J Immunol 2008; 180: 3103–3112
   PubMed Web of Science ®Google Scholar
• Lin Y. C., Chen C. L., Nakano T., Goto S., Kao Y. H., Hsu L. W., Lai C. Y., Jawan B., Cheng Y. F., Tateno C., Yoshizato K. Immunological role of indoleamine 2,3-dioxygenase in rat liver allograft rejection and tolerance. J Gastroenterol Hepatol 2008; 23: e243–e250
   Google Scholar
• Lin Y. C., Goto S., Tateno C., Nakano T., Cheng Y. F., Jawan B., Kao Y. H., Hsu L. W., Lai C. Y., Yoshizato K., Chen C. L. Induction of indoleamine 2,3-dioxygenase in livers following hepatectomy prolongs survival of allogeneic hepatocytes after transplantation. Transplant Proc 2008; 40: 2706–2708
   Google Scholar
• Barnes R. M., Alexander L. C. Beta-2-microglobulin. Quantitation by rocket immunoelectrophoresis and evaluation of serum levels in renal transplant patients. Transplantation 1983; 35: 552–555
   Google Scholar
• Claesson K., Ronnblom L., Alm G., Tufveson G. Antiviral activity appearing in serum of renal transplant recipients. Its possible relation to immunological rejection. Transplantation 1984; 38: 32–34
   PubMedGoogle Scholar
• Schafer A. J., Daniel V., Dreikorn K., Opelz G. Assessment of plasma neopterin in clinical kidney transplantation. Transplantation 1986; 41: 454–459
   PubMed Web of Science ®Google Scholar
• Backman L., Ringden O., Bjorkhem I. Monitoring of serum beta 2 microglobulin and neopterin levels in renal transplant recipients: increased values during impaired renal function and cytomegalovirus infection. Transplant Proc 1988; 20: 410–412
   Google Scholar
• Didlake R. H., Kim E. K., Sheehan K., Schreiber R. D., Kahan B. D. Effect of combined anti-gamma interferon antibody and cyclosporine therapy on cardiac allograft survival in the rat. Transplantation 1988; 45: 222–223
   Google Scholar
• Landolfo S., Cofano F., Giovarelli M., Prat M., Cavallo G., Forni G. Inhibition of interferon-gamma may suppress allograft reactivity by T lymphocytes in vitro and in vivo. Science 1985; 229: 176–179
   PubMedGoogle Scholar
• Holmes E. W., Russell P. M., Kinzler G. J., Reckard C. R., Flanigan R. C., Thompson K. D., Bermes E. W. Jr., Oxidative tryptophan metabolism in renal allograft recipients: Increased kynurenine synthesis is associated with inflammation and OKT3 therapy. Cytokine 1992; 4: 205–213
   Google Scholar
• Brandacher G., Cakar F., Winkler C., Schneeberger S., Obrist P., Bosmuller C., Werner-Felmayer G., Werner E. R., Bonatti H., Margreiter R., Fuchs D. Non-invasive monitoring of kidney allograft rejection through IDO metabolism evaluation. Kidney Int 2007; 71: 60–67
   PubMed Web of Science ®Google Scholar
• Hwang S. L., Chung N. P., Chan J. K., Lin C. L. Indoleamine 2, 3-dioxygenase (IDO) is essential for dendritic cell activation and chemotactic responsiveness to chemokines. Cell Res 2005; 15: 167–175
   PubMed Web of Science ®Google Scholar
• Tan P. H., Beutelspacher S. C., Xue S. A., Wang Y. H., Mitchell P., McAlister J. C., Larkin D. F., McClure M. O., Stauss H. J., Ritter M. A., Lombardi G., George A. J. Modulation of human dendritic-cell function following transduction with viral vectors: Implications for gene therapy. Blood 2005; 105: 3824–3832
   PubMed Web of Science ®Google Scholar
• Hacein-Bey-Abina S., von Kalle C., Schmidt M., Le Deist F., Wulffraat N., McIntyre E., Radford I., Villeval J. L., Fraser C. C., Cavazzana-Calvo M., Fischer A. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2003; 348: 255–256
   PubMed Web of Science ®Google Scholar
• Couzin J., Kaiser J. Gene therapy. As Gelsinger case ends, gene therapy suffers another blow. Science 2005; 307: 1028
   PubMed Web of Science ®Google Scholar
• Mailankot M., Smith D., Howell S., Wang B., Jacobberger J. W., Stefan T., Nagaraj R. H. Cell cycle arrest by kynurenine in lens epithelial cells. Invest Ophthalmol Vis Sci 2008; 49: 5466–5475
   PubMed Web of Science ®Google Scholar