Glucocorticoid-induced TNFR-related (GITR) protein and its ligand in antitumor immunity: Functional role and therapeutic modulation

Clinical and Developmental Immunology

Volumn 2010, Issue , 2010, Pages

  Placke, Theresa ^a   Kopp, Hans Georg ^a   Salih, Helmut Rainer ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; GAMMA INTERFERON; GELATINASE B; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; NERVE GROWTH FACTOR RECEPTOR; TNFRSF18 PROTEIN, HUMAN; TNFSF18 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RECEPTOR;

B LYMPHOCYTE; CANCER IMMUNOTHERAPY; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CYTOKINE PRODUCTION; CYTOTOXICITY; GENETIC TRANSFECTION; GRANULOCYTE; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREACTIVITY; IMMUNOSTIMULATION; MACROPHAGE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; TUMOR IMMUNITY; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; IMMUNITY; IMMUNOLOGY; METABOLISM; MOUSE; NEOPLASM; T LYMPHOCYTE;

ANIMALS; HUMANS; IMMUNITY; KILLER CELLS, NATURAL; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASMS; RECEPTORS, NERVE GROWTH FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUMOR NECROSIS FACTORS;

EID: 78349278492     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2010/239083     Document Type: Review

References (89)

1. Gurney A. L., Marsters S. A., Huang A., Pitti R. M., Mark M., Baldwin D. T., Gray A. M., Dowd P., Brush J., Heldens S., Schow P., Goddard A. D., Wood W. I., Baker K. P., Godowski P. J., Ashkenazi A., Identification of a new member of the tumor necrosis factor family and its receptor, a human ortholog of mouse GITR Current Biology 1999 9 4 215 218
2. Kwon B., Yu K.-Y., Ni J., Yu G.-L., Jang I.-K., Kim Y.-J., Xing L., Liu D., Wang S.-X., Kwon B. S., Identification of a novel activation-inducible protein of the tumor necrosis factor receptor superfamily and its ligand The Journal of Biological Chemistry 1999 274 10 6056 6061
3. Nocentini G., Giunchi L., Ronchetti S., Krausz L. T., Bartoli A., Moraca R., Migliorati G., Riccardi C., A new member of the tumor necrosis factor/nerve growth factor receptor family inhibits T cell receptor-induced apoptosis Proceedings of the National Academy of Sciences of the United States of America 1997 94 12 6216 6221
4. Nocentini G., Ronchetti S., Bartoli A., Spinicelli S., Delfino D., Brunetti L., Migliorati G., Riccardi C., Identification of three novel mRNA splice variants of GITR Cell Death and Differentiation 2000 7 4 408 410
5. Kim J. D., Choi B. K., Bae J. S., Lee U. H., Han I. S., Lee H. W., Youn B. S., Vinay D. S., Kwon B. S., Cloning and characterization of GITR ligand Genes and Immunity 2003 4 8 564 569
6. Tone M., Tone Y., Adams E., Yates S. F., Frewin M. R., Cobbold S. P., Waldmann H., Mouse glucocorticoid-induced tumor necrosis factor receptor ligand is costimulatory for T cells Proceedings of the National Academy of Sciences of the United States of America 2003 100 25 15059 15064
7. Chattopadhyay K., Ramagopal U. A., Mukhopadhaya A., Malashkevich V. N., DiLorenzo T. P., Brenowitz M., Nathenson S. G., Almo S. C., Assembly and structural properties of glucocorticoid-induced TNF receptor ligand: implications for function Proceedings of the National Academy of Sciences of the United States of America 2007 104 49 19452 19457
8. Chattopadhyay K., Ramagopal U. A., Brenowitz M., Nathenson S. G., Almo S. C., Evolution of GITRL immune function: murine GITRL exhibits unique structural and biochemical properties within the TNF superfamily Proceedings of the National Academy of Sciences of the United States of America 2008 105 2 635 640
9. Zhou Z., Song X., Berezov A., Zhang G., Li Y., Zhang H., Murali R., Li B., Greene M. I., Human glucocorticoid-induced TNF receptor ligand regulates its signaling activity through multiple oligomerization states Proceedings of the National Academy of Sciences of the United States of America 2008 105 14 5465 5470
10. Zhou Z., Tone Y., Song X., Furuuchi K., Lear J. D., Waldmann H., Tone M., Greene M. I., Murali R., Structural basis for ligand-mediated mouse GITR activation Proceedings of the National Academy of Sciences of the United States of America 2008 105 2 641 645
11. Baltz K. M., Krusch M., Baessler T., Schmiedel B. J., Bringmann A., Brossart P., Salih H. R., Neutralization of tumor-derived soluble Glucocorticoid-Induced TNFR-related protein ligand increases NK cell anti-tumor reactivity Blood 2008 112 9 3735 3743
12. Baumgartner-Nielsen J., Vestergaard C., Thestrup-Pedersen K., Deleuran M., Deleuran B., Glucocorticoid-induced tumour necrosis factor receptor (GITR) and its ligand (GITRL) in atopic dermatitis Acta Dermato-Venereologica 2006 86 5 393 398
13. Mahesh S. P., Li Z., Liu B., Fariss R. N., Nussenblat R. B., Expression of GITR ligand abrogates immunosuppressive function of ocular tissue and differentially modulates inflammatory cytokines and chemokines European Journal of Immunology 2006 36 8 2128 2138
14. McHugh R. S., Whitters M. J., Piccirillo C. A., Young D. A., Shevach E. M., Collins M., Byrne M. C., CD4+ CD25+ Immunoregulatory T Cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor Immunity 2002 16 2 311 323
15. Shimizu J., Yamazaki S., Takahashi T., Ishida Y., Sakaguchi S., Stimulation of CD25+ CD4+ regulatory T cells through GITR breaks immunological self-tolerance Nature Immunology 2002 3 2 135 142
16. Stephens G. L., McHugh R. S., Whitters M. J., Young D. A., Luxenberg D., Carreno B. M., Collins M., Shevach E. M., Engagement of glucocorticoid-induced TNFR family-related receptor on effector T cells by its ligand mediates resistance to suppression by CD4+ CD25+ T cells Journal of Immunology 2004 173 8 5008 5020
17. Ikeda M., Takeshima F., Ohba K., Ohnita K., Isomoto H., Yamakawa M., Omagari K., Mizuta Y., Kohno S., Flow cytometric analysis of expression of transforming growth factor- and glucocorticoid-induced tumor necrosis factor receptor on CD4+ CD25+ T cells of patients with inflammatory bowel disease Digestive Diseases and Sciences 2006 51 1 178 184
18. Li Z., Mahesh S. P., Kim B. J., Buggage R. R., Nussenblatt R. B., Expression of Glucocorticoid Induced TNF Receptor Family Related Protein (GITR) on peripheral T cells from normal human donors and patients with non-infectious uveitis Journal of Autoimmunity 2003 21 1 83 92
19. Kanamaru F., Youngnak P., Hashiguchi M., Nishioka T., Takahashi T., Sakaguchi S., Ishikawa I., Azuma M., Costimulation via glucocorticoid-induced TNF receptor in both conventional and CD25+ regulatory CD4+ T cells Journal of Immunology 2004 172 12 7306 7314
20. Kim J., Choi W. S., Kang H., Kim H. J., Suh J.-H., Sakaguchi S., Kwon B., Conversion of alloantigen-specific CD8+ T cell anergy to CD8+ T cell priming through in vivo ligation of glucocorticoid- induced TNF receptor Journal of Immunology 2006 176 9 5223 5231
21. Nishioka T., Nishida E., Iida R., Morita A., Shimizu J., In vivo expansion of CD4+ Foxp3+ regulatory T cells mediated by GITR molecules Immunology Letters 2008 121 2 97 104
22. Ronchetti S., Nocentini G., Bianchini R., Krausz L. T., Migliorati G., Riccardi C., Glucocorticoid-induced TNFR-related protein lowers the threshold of CD28 costimulation in CD8+ T cells Journal of Immunology 2007 179 9 5916 5926
23. Suvas S., Kim B., Sarangi P. P., Tone M., Waldmann H., Rouse B. T., In vivo kinetics of GITR and GITR ligand expression and their functional significance in regulating viral immunopathology Journal of Virology 2005 79 18 11935 11942
24. Kohm A. P., Williams J. S., Miller S. D., Cutting edge: ligation of the glucocorticoid-Induced TNF receptor enhances autoreactive CD4+ T cell activation and experimental autoimmune encephalomyelitis Journal of Immunology 2004 172 8 4686 4690
25. Ramirez-Montagut T., Chow A., Hirschhorn-Cymerman D., Terwey T. H., Kochman A. A., Lu S., Miles R. C., Sakaguchi S., Houghton A. N., Van Den Brink M. R. M., Glucocorticoid-induced TNF receptor family related gene activation overcomes tolerance/ignorance to melanoma differentiation antigens and enhances antitumor immunity Journal of Immunology 2006 176 11 6434 6442
26. Chen S., Ndhlovu L. C., Takahashi T., Takeda K., Ikarashi Y., Kikuchi T., Murata K., Pandolfi P. P., Riccardi C., Ono M., Sugamura K., Ishii N., Co-inhibitory roles for glucocorticoid-induced TNF receptor in CD1d-dependent natural killer T cells European Journal of Immunology 2008 38 8 2229 2240
27. Kim W.-J., Bae E.-M., Kang Y.-J., Bae H.-U., Hong S. H., Lee J. Y., Park J.-E., Kwon B. S., Suk K., Lee W.-H., Glucocorticoid-induced tumour necrosis factor receptor family related protein (GITR) mediates inflammatory activation of macrophages that can destabilize atherosclerotic plaques Immunology 2006 119 3 421 429
28. Zhou P., L'Italien L., Hodges D., Schebye X. M., Pivotal roles of CD4+ effector T cells in mediating agonistic anti-GITR mAb-induced-immune activation and tumor immunity in CT26 tumors Journal of Immunology 2007 179 11 7365 7375
29. Bae E., Kim W.-J., Kang Y.-M., Suk K., Koh E.-M., Cha H.-S., Ahn K.-S., Huh T.-L., Lee W.-H., Glucocorticoid-induced tumour necrosis factor receptor-related protein-mediated macrophage stimulation may induce cellular adhesion and cytokine expression in rheumatoid arthritis Clinical and Experimental Immunology 2007 148 3 410 418
30. Bae E. M., Kim W.-J., Suk K., Kang Y.-M., Park J.-E., Kim W. Y., Choi E. M., Choi B. K., Kwon B. S., Lee W.-H., Reverse signaling initiated from GITRL induces NF- B activation through ERK in the inflammatory activation of macrophages Molecular Immunology 2008 45 2 523 533
31. Baltz K. M., Krusch M., Bringmann A., Brossart P., Mayer F., Kloss M., Baessler T., Kumbier I., Peterfi A., Kupka S., Kroeber S., Menzel D., Radsak M. P., Rammensee H.-G., Salih H. R., Cancer immunoediting by GITR (glucocorticoid-induced TNF-related protein) ligand in humans: NK cell/tumor cell interactions The FASEB Journal 2007 21 10 2442 2454
32. Hanabuchi S., Watanabe N., Wang Y.-H., Wang Y.-H., Ito T., Shaw J., Cao W., Xiao-Feng Qin F., Liu Y.-J., Human plasmacytoid predendritic cells activate NK cells through glucocorticoid-induced tumor necrosis factor receptor-ligand (GITRL) Blood 2006 107 9 3617 3623
33. Liu B., Li Z., Mahesh S. P., Pantanelli S., Hwang F. S., Siu W. O., Nussenblatt R. B., Glucocorticoid-induced tumor necrosis factor receptor negatively regulates activation of human primary natural killer (NK) cells by blocking proliferative signals and increasing NK cell apoptosis The Journal of Biological Chemistry 2008 283 13 8202 8210
34. Wang J., Devgan V., Corrado M., Prabhu N. S., El-Deiry W. S., Riccardi C., Pandolfi P. P., Missero C., Dotto G. P., Glucocorticoid-induced tumor necrosis factor receptor is a p21 Cip1/WAF1 transcriptional target conferring resistance of keratinocytes to UV light-induced apoptosis The Journal of Biological Chemistry 2005 280 45 37725 37731
35. Lahey T. P., Loisel S. D., Wieland-Alter W., Glucocorticoid-induced tumor necrosis factor receptor family-related protein triggering enhances HIV-specific CD4+ T cell cytokine secretion and protects HIV-specific CD4+ T cells from apoptosis Journal of Infectious Diseases 2007 196 1 43 49
36. Wilde B., Dolff S., Cai X., Specker C., Becker J., Ttsch M., Costabel U., Drig J., Kribben A., Tervaert J. W. C., Schmid K. W., Witzke O., CD4+ CD25+ T-cell populations expressing CD134 and GITR are associated with disease activity in patients with Wegener's granulomatosis Nephrology Dialysis Transplantation 2009 24 1 161 171
37. Lee J.-H., Wang L.-C., Lin Y.-T., Yang Y.-H., Lin D.-T., Chiang B.-L., Inverse correlation between CD4+ regulatory T-cell population and autoantibody levels in paediatric patients with systemic lupus erythematosus Immunology 2006 117 2 280 286
38. uczyski W., Wawrusiewicz-Kurylonek N., Stasiak-Barmuta A., Urban R., Iendo E., Urban M., Hryszko M., Kretowski A., Grska M., Diminished expression of ICOS, GITR and CTLA-4 at the mRNA level in T regulatory cells of children with newly diagnosed type 1 diabetes Acta Biochimica Polonica 2009 56 2 361 370
39. Kim B. J., Li Z., Fariss R. N., Shen D. F., Mahesh S. P., Egwuagu C., Yu C.-R., Nagineni C. N., Chan C.-C., Nussenblatt R. B., Constitutive and cytokine-induced GITR ligand expression on human retinal pigment epithelium and photoreceptors Investigative Ophthalmology and Visual Science 2004 45 9 3170 3176
40. Cardona I. D., Goleva E., Ou L.-S., Leung D. Y. M., Staphylococcal enterotoxin B inhibits regulatory T cells by inducing glucocorticoid-induced TNF receptor-related protein ligand on monocytes Journal of Allergy and Clinical Immunology 2006 117 3 688 695
41. Hwang H., Lee S., Lee W.-H., Lee H.-J., Suk K., Stimulation of glucocorticoid-induced tumor necrosis factor receptor family-related protein ligand (GITRL) induces inflammatory activation of microglia in culture Journal of Neuroscience Research 2010 88 10 2188 2196
42. Piao J., Kamimura Y., Iwai H., Cao Y., Kikuchi K., Hashiguchi M., Masunaga T., Jiang H., Tamura K., Sakaguchi S., Azuma M., Enhancement of T-cell-mediated anti-tumour immunity via the ectopically expressed glucocorticoid-induced tumour necrosis factor receptor-related receptor ligand (GITRL) on tumours Immunology 2009 127 4 489 499
43. Baessler T., Krusch M., Schmiedel B. J., Kloss M., Baltz K. M., Wacker A., Schmetzer H. M., Salih H. R., Glucocorticoid-induced tumor necrosis factor receptor-related protein ligand subverts immunosurveillance of acute myeloid leukemia in humans Cancer Research 2009 69 3 1037 1045
44. Placke T., Kopp H. G., Kanz L., Coating of tumor cells by platelets confers expression of immunoregulatory molecules which impair NK cell anti-tumor reactivity Blood 2009 114 22 1168 1168
45. Ji H.-B., Liao G., Faubion W. A., Abada-Molina A. C., Cozzo C., Laroux F. S., Caton A., Terhorst C., Cutting edge: the natural ligand for glucocorticoid-induced TNF receptor-related protein abrogates regulatory T cell suppression Journal of Immunology 2004 172 10 5823 5827
46. Ronchetti S., Zollo O., Bruscoli S., Agostini M., Bianchini R., Nocentini G., Ayroldi E., Riccardi C., GITR, a member of the TNF receptor superfamily, is costimulatory to mouse T lymphocyte subpopulations European Journal of Immunology 2004 34 3 613 622
47. Levings M. K., Sangregorio R., Sartirana C., Moschin A. L., Battaglia M., Orban P. C., Roncarolo M.-G., Human CD25+ CD4+ T suppressor cell clones produce transforming growth factor, but not interleukin 10, and are distinct from type 1 T regulatory cells Journal of Experimental Medicine 2002 196 10 1335 1346
48. Tuyaerts S., Van Meirvenne S., Bonehill A., Heirman C., Corthals J., Waldmann H., Breckpot K., Thielemans K., Aerts J. L., Expression of human GITRL on myeloid dendritic cells enhances their immunostimulatory function but does not abrogate the suppressive effect of CD4+ CD25+ regulatory T cells Journal of Leukocyte Biology 2007 82 1 93 105
49. Calmels B., Paul S., Futin N., Ledoux C., Stoeckel F., Acres B., Bypassing tumor-associated immune suppression with recombinant adenovirus constructs expressing membrane bound or secreted GITR-L Cancer Gene Therapy 2005 12 2 198 205
50. Cho J. S., Hsu J. V., Morrison S. L., Localized expression of GITR-L in the tumor microenvironment promotes CD8+ T cell dependent anti-tumor immunity Cancer Immunology, Immunotherapy 2009 58 7 1057 1069
51. Esparza E. M., Arch R. H., Glucocorticoid-induced TNF receptor functions as a costimulatory receptor that promotes survival in early phases of T cell activation Journal of Immunology 2005 174 12 7869 7874
52. Igarashi H., Cao Y., Iwai H., Piao J., Kamimura Y., Hashiguchi M., Amagasa T., Azuma M., GITR ligand-costimulation activates effector and regulatory functions of CD4+ T cells Biochemical and Biophysical Research Communications 2008 369 4 1134 1138
53. Agostini M., Cenci E., Pericolini E., Nocentini G., Bistoni G., Vecchiarelli A., Riccardi C., The glucocorticoid-induced tumor necrosis factor receptor-related gene modulates the response to Candida albicans infection Infection and Immunity 2005 73 11 7502 7508
54. Ronchetti S., Nocentini G., Riccardi C., Pandolfi P. P., Role of GITR in activation response of T lymphocytes Blood 2002 100 1 350 352
55. Cuzzocrea S., Ayroldi E., Di Paola R., Agostini M., Mazzon E., Bruscoli S., Genovese T., Ronchetti S., Caputi A. P., Riccardi C., Role of glucocorticoid-induced TNF receptor family gene (GITR) in collagen-induced arthritis The FASEB Journal 2005 19 10 1253 1265
56. van Olffen R. W., Koning N., van Gisbergen K. P., Wensveen F. M., Hoek R. M., Boon L., Hamann J., van Lier R. A., Nolte M. A., GITR triggering induces expansion of both effector and regulatory CD4+ T cells in vivo Journal of immunology 2009 182 12 7490 7500
57. Cuzzocrea S., Nocentini G., Di Paola R., Agostini M., Mazzon E., Ronchetti S., Crisafulli C., Esposito E., Caputi A. P., Riccardi C., Proinflammatory role of glucocorticoid-induced TNF receptor-related gene in acute lung inflammation Journal of Immunology 2006 177 1 631 641
58. Cuzzocrea S., Ronchetti S., Genovese T., Mazzon E., Agostini M., Di Paola R., Esposito E., Mua C., Nocentini G., Riccardi C., Genetic and pharmacological inhibition of GITR-GITRL interaction reduces chronic lung injury induced by bleomycin instillation The FASEB Journal 2007 21 1 117 129
59. Patel M., Xu D., Kewin P., Choo-Kang B., McSharry C., Thompson N. C., Liew F. Y., Glucocorticoid-induced TNFR family-related protein (GITR) activation exacerbates murine asthma and collagen-induced arthritis European Journal of Immunology 2005 35 12 3581 3590
60. You S., Poulton L., Cobbold S., Liu C.-P., Rosenzweig M., Ringler D., Lee W.-H., Segovia B., Bach J.-F., Waldmann H., Chatenoud L., Key role of the GITR/GITRLigand pathway in the development of murine autoimmune diabetes: a potential therapeutic target PLoS ONE 2009 4 11
61. La S., Kim E., Kwon B., In vivo ligation of glucocorticoid-induced TNF receptor enhances the T-cell immunity to herpes simplex virus type 1 Experimental and Molecular Medicine 2005 37 3 193 198
62. Haque A., Stanley A. C., Amante F. H., Rivera F. D.L., Zhou Y., Kuns R. D., Yardley V., Sakaguchi S., Hill G. R., Engwerda C. R., Therapeutic glucocorticoid-induced TNF receptor-mediated amplification of CD4+ T cell responses enhances antiparasitic immunity Journal of Immunology 2010 184 5 2583 2592
63. Bushell A., Wood K., GITR ligation blocks allograft protection by induced CD25+ CD4+ regulatory T cells without enhancing effector T-cell function American Journal of Transplantation 2007 7 4 759 768
64. Kim J., Woon S. C., Hye J. K., Kwon B., Prevention of chronic graft-versus-host disease by stimulation with glucocorticoid-induced TNF receptor Experimental and Molecular Medicine 2006 38 1 94 99
65. Muriglan S. J., Ramirez-Montagut T., Alpdogan O., Van Huystee T. W., Eng J. M., Hubbard V. M., Kochman A. A., Tjoe K. H., Riccardi C., Pandolfi P. P., Sakaguchi S., Houghton A. N., Van Den Brink M. R. M., GITR activation induces an opposite effect on alloreactive CD4+ and CD8+ T cells in graft-versus-host disease Journal of Experimental Medicine 2004 200 2 149 157
66. Shevach E. M., Stephens G. L., Opinion: the GITR-GITRL interaction: co-stimulation or contrasuppression of regulatory activity? Nature Reviews Immunology 2006 6 8 613 618
67. Smith C. A., Farrah T., Goodwin R. G., The TNF receptor superfamily of cellular and viral proteins: activation, costimulation, and death Cell 1994 76 6 959 962
68. 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 Nature Medicine 2007 13 5 579 586
69. Vecchiarelli A., Pericolini E., Gabrielli E., Agostini M., Bistoni F., Nocentini G., Cenci E., Riccardi C., The GITRL-GITR system alters TLR-4 expression on DC during fungal infection Cellular Immunology 2009 257 1-2 13 22
70. Lee H.-S., Shin H.-H., Kwon B. S., Choi H.-S., Soluble glucocorticoid-induced tumor necrosis factor receptor (sGITR) increased MMP-9 activity in murine macrophage Journal of Cellular Biochemistry 2003 88 5 1048 1056
71. Shin H.-H., Lee M.-H., Kim S.-G., Lee Y.-H., Kwon B. S., Choi H.-S., Recombinant glucocorticoid induced tumor necrosis factor receptor (rGITR) induces NOS in murine macrophage FEBS Letters 2002 514 2-3 275 280
72. Shin H.-H., Kwon B. S., Choi H.-S., Recombinant glucocorticoid induced tumour necrosis factor receptor (rGITR) induced COX-2 activity in murine macrophage Raw 264.7 cells Cytokine 2002 19 4 187 192
73. Shin H.-H., Kim S.-J., Lee H.-S., Choi H.-S., The soluble glucocorticoid-induced tumor necrosis factor receptor causes cell cycle arrest and apoptosis in murine macrophages Biochemical and Biophysical Research Communications 2004 316 1 24 32
74. Nishikawa H., Kato T., Hirayama M., Orito Y., Sato E., Harada N., Gnjatic S., Old L. J., Shiku H., Regulatory T cell-resistant CD4+ T cells induced by glucocorticoid-induced tumor necrosis factor receptor signaling Cancer Research 2008 68 14 5948 5954
75. Hu P., Arias R. S., Sadun R. E., Nien Y.-C., Zhang N., Sabzevari H., Lutsiak M. E. C., Khawli L. A., Epstein A. L., Construction and preclinical characterization of Fc-mGITRL for the immunotherapy of cancer Clinical Cancer Research 2008 14 2 579 588
76. Ko K., Yamazaki S., Nakamura K., Nishioka T., Hirota K., Yamaguchi T., Shimizu J., Nomura T., Chiba T., Sakaguchi S., Treatment of advanced tumors with agonistic anti-GITR mAb and its effects on tumor-infiltrating Foxp3+ CD25+ CD4+ regulatory T cells Journal of Experimental Medicine 2005 202 7 885 891
77. Turk M. J., Guevara-Patio J. A., Rizzuto G. A., Engelhorn M. E., Houghton A. N., Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells Journal of Experimental Medicine 2004 200 6 771 782
78. Cohen A. D., Diab A., Perales M.-A., Wolchok J. D., Rizzuto G., Merghoub T., Huggins D., Liu C., Turk M. J., Restifo N. P., Sakaguchi S., Houghton A. N., Agonist anti-GITR antibody enhances vaccine-induced CD8+ T-cell responses and tumor immunity Cancer Research 2006 66 9 4904 4912
79. Duan F., Lin Y., Liu C., Engelhorn M. E., Cohen A. D., Curran M., Sakaguchi S., Merghoub T., Terzulli S., Wolchok J. D., Houghton A. N., Immune rejection of mouse tumors expressing Mutated self Cancer Research 2009 69 8 3545 3553
80. Imai N., Ikeda H., Tawara I., Wang L., Wang L., Nishikawa H., Kato T., Shiku H., Glucocorticoid-induced tumor necrosis factor receptor stimulation enhances the multifunctionality of adoptively transferred tumor antigen-specific CD8+ T cells with tumor regression Cancer Science 2009 100 7 1317 1325
81. Coe D., Begom S., Addey C., White M., Dyson J., Chai J.-G., Depletion of regulatory T cells by anti-GITR mAb as a novel mechanism for cancer immunotherapy Cancer Immunology, Immunotherapy 2010 59 9 1367 1377
82. A. D. Cohen, Schaer D. A., Liu C., Agonist anti-GITR monoclonal antibody induces melanoma tumor immunity in mice by altering regulatory T cell stability and intra-tumor accumulation PLoS One 2010 5 5
83. Jin D. K., Shido K., Kopp H.-G., Petit I., Shmelkov S. V., Young L. M., Hooper A. T., Amano H., Avecilla S. T., Heissig B., Hattori K., Zhang F., Hicklin D. J., Wu Y., Zhu Z., Dunn A., Salari H., Werb Z., Hackett N. R., Crystal R. G., Lyden D., Rafii S., Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes Nature Medicine 2006 12 5 557 567
84. Palumbo J. S., Talmage K. E., Massari J. V., La Jeunesse C. M., Flick M. J., Kombrinck K. W., Jirouskov M., Degen J. L., Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells Blood 2005 105 1 178 185
85. Nocentini G., Riccardi C., GITR: a multifaceted regulator of immunity belonging to the tumor necrosis factor receptor superfamily European Journal of Immunology 2005 35 4 1016 1022
86. Krausz L. T., Bianchini R., Ronchetti S., Fettucciari K., Nocentini G., Riccardi C., GITR-GITRL system, a novel player in shock and inflammation TheScientificWorldJournal 2007 7 533 566
87. Esparza E. M., Arch R. H., TRAF4 functions as an intermediate of GITR-induced NF- B activation Cellular and Molecular Life Sciences 2004 61 24 3087 3092
88. Esparza E. M., Arch R. H., Glucocorticoid-induced TNF receptor, a costimulatory receptor on naive and activated T cells, uses TNF receptor-associated factor 2 in a novel fashion as an inhibitor of NF- B activation Journal of Immunology 2005 174 12 7875 7882
89. Esparza E. M., Lindsten T., Stockhausen J. M., Arch R. H., Tumor necrosis factor receptor (TNFR)-associated factor 5 is a critical intermediate of costimulatory signaling pathways triggered by glucocorticoid-induced TNFR in T cells The Journal of Biological Chemistry 2006 281 13 8559 8564