Glucocorticoid-induced tumour necrosis factor receptor-related protein: a key marker of functional regulatory T cells

Simona Ronchetti ¹, Erika Ricci ¹, Maria Grazia Petrillo ¹, Luigi Cari ¹, Graziella Migliorati ¹, Giuseppe Nocentini ¹, Carlo Riccardi ¹

Affiliations

¹ Section of Pharmacology, Department of Medicine, University of Perugia, Piazza Severi 1, 06132 Perugia, Italy.

PMID: 25961057
155 References
49 citations

Abstract

Glucocorticoid-induced tumour necrosis factor receptor-related protein (GITR, TNFRSF18, and CD357) is expressed at high levels in activated T cells and regulatory T cells (Tregs). In this review, we present data from mouse and human studies suggesting that GITR is a crucial player in the differentiation of thymic Tregs (tTregs), and expansion of both tTregs and peripheral Tregs (pTregs). The role of GITR in Treg expansion is confirmed by the association of GITR expression with markers of memory T cells. In this context, it is not surprising that GITR appears to be a marker of active Tregs, as suggested by the association of GITR expression with other markers of Treg activation or cytokines with suppressive activity (e.g., IL-10 and TGF-β), the presence of GITR(+) cells in tissues where Tregs are active (e.g., solid tumours), or functional studies on Tregs. Furthermore, some Treg subsets including Tr1 cells express either low or no classical Treg markers (e.g., FoxP3 and CD25) and do express GITR. Therefore, when evaluating changes in the number of Tregs in human diseases, GITR expression must be evaluated. Moreover, GITR should be considered as a marker for isolating Tregs.

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Gene expression in the Gitr locus is regulated by NF-κB and Foxp3 through an enhancer. Yukiko Tone, Yoko Kidani, +5 authors, Masahide Tone. less J Immunol, 2014 Mar 19; 192(8). PMID: 24634496 Free PMC article.
Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. Nabila Seddiki, Brigitte Santner-Nanan, +9 authors, Barbara Fazekas de St Groth. less J Exp Med, 2006 Jul 05; 203(7). PMID: 16818676 Free PMC article. Highly Cited.
In vivo expansion of naïve CD4+ CD25(high) FOXP3+ regulatory T cells in patients with colorectal carcinoma after IL-2 administration. Marc Beyer, Beatrix Schumak, +7 authors, Joachim L Schultze. less PLoS One, 2012 Jan 26; 7(1). PMID: 22276195 Free PMC article.
Nature and nurture in Foxp3(+) regulatory T cell development, stability, and function. Terrence L Geiger, Sharyn Tauro. Hum Immunol, 2012 Jan 14; 73(3). PMID: 22240298 Free PMC article. Review.
Glucocorticoid-induced tumor necrosis factor receptor-related (GITR)-Fc fusion protein inhibits GITR triggering and protects from the inflammatory response after spinal cord injury. Giuseppe Nocentini, Salvatore Cuzzocrea, +7 authors, Carlo Riccardi. less Mol Pharmacol, 2008 Mar 07; 73(6). PMID: 18322000
Correlation of increased blood levels of GITR and GITRL with disease severity in patients with primary Sjögren's syndrome. Xiaoxia Gan, Xiaoke Feng, +4 authors, Miaojia Zhang. less Clin Dev Immunol, 2013 Aug 13; 2013. PMID: 23935647 Free PMC article.
GITR-dependent regulation of 4-1BB expression: implications for T cell memory and anti-4-1BB-induced pathology. Gloria H Y Lin, Laura M Snell, +2 authors, Tania H Watts. less J Immunol, 2013 Mar 29; 190(9). PMID: 23536631
Tumour cell generation of inducible regulatory T-cells in multiple myeloma is contact-dependent and antigen-presenting cell-independent. Sylvia Feyler, Gina B Scott, +6 authors, Gordon Cook. less PLoS One, 2012 Jun 06; 7(5). PMID: 22666318 Free PMC article.
Phenotypic characterization of ex vivo CD4+CD25highCD127low immune regulatory T cells in allergic asthma: pathogenesis relevance of their FoxP3, GITR, CTLA-4 and FAS expressions. M Pietruczuk, M Eusebio, +2 authors, L Kraszula, M Kupczyk, P Kuna. less J Biol Regul Homeost Agents, 2012 Dec 18; 26(4). PMID: 23241113
Glucocorticoid-induced TNFR family-related receptor (GITR)-expression in tumor infiltrating leucocytes (TILs) is associated with the pathogenesis of esophageal adenocarcinomas with and without Barrett's mucosa. Burkhard H A von Rahden, S Kircher, +5 authors, M Grimm. less Cancer Biomark, 2010 Jan 01; 7(6). PMID: 21694467
Depletion of regulatory T cells by anti-GITR mAb as a novel mechanism for cancer immunotherapy. David Coe, Shaima Begom, +3 authors, Jian-Guo Chai. less Cancer Immunol Immunother, 2010 May 19; 59(9). PMID: 20480365
A subset of CD8+ T cells acquiring selective suppressive properties may play a role in GvHD management. Irit Avivi, Dina Stroopinsky, Jacob M Rowe, Tamar Katz. Transpl Immunol, 2012 Dec 01; 28(1). PMID: 23196257
CD4⁺CD25⁺/highCD127low/⁻ regulatory T cells are enriched in rheumatoid arthritis and osteoarthritis joints--analysis of frequency and phenotype in synovial membrane, synovial fluid and peripheral blood. Babak Moradi, Philipp Schnatzer, +7 authors, Theresa Tretter. less Arthritis Res Ther, 2014 Apr 20; 16(2). PMID: 24742142 Free PMC article.
Glucocorticoid-induced tumor necrosis factor receptor family-related ligand triggering upregulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 and promotes leukocyte adhesion. Pedro Miguel Lacal, Maria Grazia Petrillo, +7 authors, Giuseppe Nocentini. less J Pharmacol Exp Ther, 2013 Jul 31; 347(1). PMID: 23892569
Treatment of advanced tumors with agonistic anti-GITR mAb and its effects on tumor-infiltrating Foxp3+CD25+CD4+ regulatory T cells. Kuibeom Ko, Sayuri Yamazaki, +7 authors, Shimon Sakaguchi. less J Exp Med, 2005 Sep 28; 202(7). PMID: 16186187 Free PMC article. Highly Cited.
Expression of GITR ligand abrogates immunosuppressive function of ocular tissue and differentially modulates inflammatory cytokines and chemokines. Sankaranarayana P Mahesh, Zhuqing Li, +2 authors, Baoying Liu, Robert N Fariss, Robert B Nussenblatt. less Eur J Immunol, 2006 Jul 29; 36(8). PMID: 16874737
GITR pathway activation abrogates tumor immune suppression through loss of regulatory T cell lineage stability. David A Schaer, Sadna Budhu, +8 authors, Jedd D Wolchok. less Cancer Immunol Res, 2014 Jan 15; 1(5). PMID: 24416730 Free PMC article. Highly Cited.
GITR gene deletion and GITR-FC soluble protein administration inhibit multiple organ failure induced by zymosan. Maria Galuppo, Giuseppe Nocentini, +7 authors, Salvatore Cuzzocrea. less Shock, 2011 Jun 10; 36(3). PMID: 21654556
GITR, a member of the TNF receptor superfamily, is costimulatory to mouse T lymphocyte subpopulations. Simona Ronchetti, Ornella Zollo, +5 authors, Carlo Riccardi. less Eur J Immunol, 2004 Mar 03; 34(3). PMID: 14991590
Decrease in dendritic cells in endomyocardial biopsies of human dilated cardiomyopathy. Rudin Pistulli, Sebastian König, +8 authors, Atilla Yilmaz. less Eur J Heart Fail, 2013 Apr 23; 15(9). PMID: 23603088
TLR5 signaling enhances the proliferation of human allogeneic CD40-activated B cell induced CD4hiCD25+ regulatory T cells. Ping-Lung Chan, Jian Zheng, +7 authors, Wenwei Tu. less PLoS One, 2013 Jul 12; 8(7). PMID: 23844139 Free PMC article.
IL-15-dependent upregulation of GITR on CD8 memory phenotype T cells in the bone marrow relative to spleen and lymph node suggests the bone marrow as a site of superior bioavailability of IL-15. Laura M Snell, Gloria H Y Lin, Tania H Watts. J Immunol, 2012 May 15; 188(12). PMID: 22581858
Regulatory T cell microRNA expression changes in children with acute Kawasaki disease. F-F Ni, C-R Li, +3 authors, Q Li, Y Xia, G-B Wang, J Yang. less Clin Exp Immunol, 2014 Jul 22; 178(2). PMID: 25039241 Free PMC article.
The plasticity and stability of regulatory T cells. Shimon Sakaguchi, Dario A A Vignali, +2 authors, Alexander Y Rudensky, Rachel E Niec, Herman Waldmann. less Nat Rev Immunol, 2013 May 18; 13(6). PMID: 23681097 Highly Cited.
IFN-β induces the proliferation of CD4+CD25+Foxp3+ regulatory T cells through upregulation of GITRL on dendritic cells in the treatment of multiple sclerosis. Meiyue Chen, Guangjie Chen, +3 authors, Jian Hong. less J Neuroimmunol, 2011 Nov 25; 242(1-2). PMID: 22112394
Role of glucocorticoid-induced TNF receptor family gene (GITR) in collagen-induced arthritis. Salvatore Cuzzocrea, Emira Ayroldi, +7 authors, Carlo Riccardi. less FASEB J, 2005 Jul 30; 19(10). PMID: 16051692
Human CD25+CD4+ T suppressor cell clones produce transforming growth factor beta, but not interleukin 10, and are distinct from type 1 T regulatory cells. Megan K Levings, Romina Sangregorio, +4 authors, Maria-Grazia Roncarolo. less J Exp Med, 2002 Nov 20; 196(10). PMID: 12438424 Free PMC article.
The contextual role of TNFR family members in CD8(+) T-cell control of viral infections. Michael E Wortzman, Derek L Clouthier, +2 authors, Ann J McPherson, Gloria H Y Lin, Tania H Watts. less Immunol Rev, 2013 Aug 21; 255(1). PMID: 23947352 Review.
Enhanced GITR/GITRL interactions augment IL-27 expression and induce IL-10-producing Tr-1 like cells. Yijun Carrier, Matthew J Whitters, +10 authors, Quintus G Medley. less Eur J Immunol, 2012 Jun 09; 42(6). PMID: 22678896
Genetic evidence of regulatory gene variants of the STAT6, IL10R and FOXP3 locus as a susceptibility factor in uncomplicated malaria and parasitaemia in Congolese children. Felix Koukouikila-Koussounda, Francine Ntoumi, +3 authors, Thirumalaisamy P Velavan. less Malar J, 2013 Jan 10; 12. PMID: 23297791 Free PMC article.
Modulation of Treg cells/T effector function by GITR signaling is context-dependent. Amal Ephrem, Alan L Epstein, +3 authors, Ethan M Shevach. less Eur J Immunol, 2013 Jun 01; 43(9). PMID: 23722868
MicroRNA-126 regulates the induction and function of CD4(+) Foxp3(+) regulatory T cells through PI3K/AKT pathway. Andong Qin, Zhenke Wen, +5 authors, Lin Xu. less J Cell Mol Med, 2013 Jan 11; 17(2). PMID: 23301798 Free PMC article.
GITR: a modulator of immune response and inflammation. Giuseppe Nocentini, Carlo Riccardi. Adv Exp Med Biol, 2009 Sep 18; 647. PMID: 19760073 Review.
CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Rebecca S McHugh, Matthew J Whitters, +4 authors, Michael C Byrne. less Immunity, 2002 Mar 01; 16(2). PMID: 11869690 Highly Cited.
Mouse glucocorticoid-induced tumor necrosis factor receptor ligand is costimulatory for T cells. Masahide Tone, Yukiko Tone, +4 authors, Herman Waldmann. less Proc Natl Acad Sci U S A, 2003 Nov 11; 100(25). PMID: 14608036 Free PMC article.
PIM1 kinase phosphorylates the human transcription factor FOXP3 at serine 422 to negatively regulate its activity under inflammation. Zhiyuan Li, Fang Lin, +10 authors, Bin Li. less J Biol Chem, 2014 Aug 07; 289(39). PMID: 25096571 Free PMC article.
Tr1 cells and the counter-regulation of immunity: natural mechanisms and therapeutic applications. Maria Grazia Roncarolo, Silvia Gregori, Rosa Bacchetta, Manuela Battaglia. Curr Top Microbiol Immunol, 2014 Jul 10; 380. PMID: 25004813 Highly Cited. Review.
Cell-specific and context-dependent effects of GITR in cancer, autoimmunity, and infection. Derek L Clouthier, Tania H Watts. Cytokine Growth Factor Rev, 2014 Feb 04; 25(2). PMID: 24484736 Review.
GITR-GITRL system, a novel player in shock and inflammation. Ludovic Tibor Krausz, Rodolfo Bianchini, +3 authors, Carlo Riccardi. less ScientificWorldJournal, 2007 May 26; 7. PMID: 17525820 Free PMC article. Review.
Generation of induced regulatory T cells from primary human naïve and memory T cells. Gavin I Ellis, Mary Catherine Reneer, +2 authors, Francesc Martí. less J Vis Exp, 2012 Apr 25; (62). PMID: 22525890 Free PMC article.
A unique subset of CD4+CD25highFoxp3+ T cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Laura Strauss, Christoph Bergmann, +3 authors, Theresa L Whiteside. less Clin Cancer Res, 2007 Aug 03; 13(15 Pt 1). PMID: 17671115 Highly Cited.
Alteration in frequency and function of CD4⁺CD25⁺FOXP3⁺ regulatory T cells in patients with immune thrombocytopenic purpura. Nargess Arandi, Abbas Mirshafiey, +6 authors, Asghar Aghamohammadi. less Iran J Allergy Asthma Immunol, 2013 Dec 18; 13(2). PMID: 24338252
IL10 polymorphisms influence neonatal immune responses, atopic dermatitis, and wheeze at age 3 years. Diana Raedler, Sabina Illi, +4 authors, Bianca Schaub. less J Allergy Clin Immunol, 2012 Oct 02; 131(3). PMID: 23021880

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