Regulatory T Cells: Molecular Actions on Effector Cells in Immune Regulation

Journal of Immunology Research

Volumn 2016, Issue , 2016, Pages

  Arce Sillas, Asiel ^a   Álvarez Luquín, Diana Denisse ^a   Tamaya Domínguez, Beatriz ^a   Gomez Fuentes, Sandra ^a   Trejo Garciá, Abel ^a   Melo Salas, Marlene ^a   Cárdenas, Graciela ^a   Rodríguez Ramírez, Juan ^a   Adalid Peralta, Laura ^a  

^a NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ATTENTION; EFFECTOR CELL; IMMUNE RESPONSE; IMMUNOREGULATION; REGULATORY T LYMPHOCYTE; TARGET CELL; ANIMAL; CELL COMMUNICATION; CYTOLOGY; CYTOTOXICITY; DENDRITIC CELL; HUMAN; IMMUNE SYSTEM; IMMUNITY; IMMUNOLOGY; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; METABOLISM; SIGNAL TRANSDUCTION;

CYTOKINE; GRANZYME; PERFORIN;

ANIMALS; CELL COMMUNICATION; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; GRANZYMES; HUMANS; IMMUNE SYSTEM; IMMUNITY; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; PERFORIN; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84973375365     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2016/1720827     Document Type: Review

References (80)

1. A. Schmidt, N. Oberle, P. H. Krammer, "Molecular mechanisms of treg-mediated T cell suppression, " Frontiers in Immunology, vol. 3, article 51, 2012.
2. A. L. Perdigoto, L. Chatenoud, J. A. Bluestone, K. C. Herold, "Inducing and administering tregs to treat human disease, " Frontiers in Immunology, vol. 6, article 654, 2016.
3. D. A. A. Vignali, L. W. Collison, C. J. Workman, "How regulatory T cells work, " Nature Reviews Immunology, vol. 8, no. 7, pp. 523-532, 2008.
4. M. Dhainaut and M. Moser, "Mechanisms of surveillance of dendritic cells by regulatory T lymphocytes, " Progress in Molecular Biology and Translational Science, vol. 136, pp. 131-154, 2015.
5. M. Saraiva and A. O'Garra, "The regulation of IL-10 production by immune cells, " Nature Reviews Immunology, vol. 10, no. 3, pp. 170-181, 2010.
6. K. N. Couper, D. G. Blount, E. M. Riley, "IL-10: the master regulator of immunity to infection, " Journal of Immunology, vol. 180, no. 9, pp. 5771-5777, 2008.
7. E. N. McNamee, K. M. Ryan, ?E. W. Griffin et al., "Noradrenaline acting at central adrenoceptors induces interleukin-10 and suppressor of cytokine signaling-3 expression in rat brain: implications for neurodegeneration, " Brain, Behavior, Immunity, vol. 24, no. 4, pp. 660-671, 2010.
8. G. Leposavic, I. Pilipovic, K. Radojevic, V. Pesic, M. Perisic, D. Kosec, "Catecholamines as immunomodulators: a role for adrenoceptor-mediated mechanisms in fine tuning of T-cell development, " Autonomic Neuroscience: Basic and Clinical, vol. 144, no. 1-2, pp. 1-12, 2008.
9. J. Loebbermann, C. Schnoeller, H. Thornton et al., "IL-10 regulates viral lung immunopathology during acute respiratory syncytial virus infection in mice, " PLoSONE, vol. 7, no. 2, Article ID e32371, 2012.
10. A. Taylor, J. Verhagen, K. Blaser, M. Akdis, C. A. Akdis, "Mechanisms of immune suppression by interleukin-10 and transforming growth factor-: the role of T regulatory cells, " Immunology, vol. 117, no. 4, pp. 433-442, 2006.
11. O. Palomares, M. Martn-Fontecha, R. Lauener et al., "Regulatory T cells and immune regulation of allergic diseases: roles of IL-10 and TGF-, " Genes and Immunity, vol. 15, no. 8, pp. 511-520, 2014.
12. A. J. Carey, C. K. Tan, G. C. Ulett, "Infection-induced IL-10 and JAK-STAT: a review of the molecular circuitry controlling immune hyperactivity in response to pathogenic microbes, " JAK-STAT, vol. 1, no. 3, pp. 159-167, 2012.
13. W.-H. Liu, J.-J. Liu, J. Wu et al., "Novelmechanism of inhibition of dendritic cells maturation by mesenchymal stem cells via interleukin-10 and the JAK1/STAT3 signaling pathway, " PLoS ONE, vol. 8, no. 1, Article ID e55487, 2013.
14. S. Cao, J. Liu, L. Song, X. Ma, "The protooncogene c-Maf is an essential transcription factor for IL-10 gene expression in macrophages, " Journal of Immunology, vol. 174, no. 6, pp. 3484-3492, 2005.
15. M. W. M. van den Bosch, E. Palsson-Mcdermott, D. S. Johnson, L. A. J. O'Neill, "LPS induces the degradation of programmed cell death protein 4 (PDCD4) to release Twist2, activating c-Maf transcription to promote interleukin-10 production, " The Journal of Biological Chemistry, vol. 289, no. 33, pp. 22980-22990, 2014.
16. G. den Hartog, H. F. J. Savelkoul, R. Schoemaker et al., "Modulation of human immune responses by bovine interleukin-10, " PLoS ONE, vol. 6, no. 3, Article ID e18188, 2011.
17. A. Chaudhry, R. M. Samstein, P. Treuting et al., "Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation, " Immunity, vol. 34, no. 4, pp. 566-578, 2011.
18. K. Nakamura, A. Kitani, W. Strober, "Cell contactdependent immunosuppression by CD4+CD25+ regulatory T cells is mediated by cell surface-bound transforming growth factor, " Journal of Experimental Medicine, vol. 194, no. 5, pp. 629-644, 2001.
19. M. Hagness, K. Henjum, J. Landskron et al., "Kinetics and activation requirements of contact-dependent immune suppression by human regulatory T cells, " The Journal of Immunology, vol. 188, no. 11, pp. 5459-5466, 2012.
20. A. Weiss and L. Attisano, "The TGFbeta superfamily signaling pathway, " Wiley Interdisciplinary Reviews: Developmental Biology, vol. 2, no. 1, pp. 47-63, 2013.
21. A. Yoshimura, Y. Wakabayashi, T. Mori, "Cellular and molecular basis for the regulation of inflammation by TGF-, " The Journal of Biochemistry, vol. 147, no. 6, pp. 781-792, 2010.
22. V. Syed, "TGF-signaling in cancer, " Journal of Cellular Biochemistry, vol. 117, no. 6, pp. 1279-1287, 2016.
23. H. Ma, Y. Wei, Y. Leng et al., "TGF-1-induced expression of Id-1 is associated with tumor progression in gastric cancer, " Medical Oncology, vol. 31, no. 7, article 19, 2014.
24. B. M. Olson, J. A. Sullivan, W. J. Burlingham, "Interleukin 35: a key mediator of suppression and the propagation of infectious tolerance, " Frontiers in Immunology, vol. 4, article 315, 2013.
25. L. W. Collison, G. M. Delgoffe, C. S. Guy et al., "The composition and signaling of the IL-35 receptor are unconventional, " Nature Immunology, vol. 13, no. 3, pp. 290-299, 2012.
26. R.-X. Wang, C.-R. Yu, I. M. Dambuza et al., "Interleukin-35 induces regulatory B cells that suppress autoimmune disease, " Nature Medicine, vol. 20, no. 6, pp. 633-641, 2014.
27. Y. Li, Y. Wang, Y. Liu et al., "The possible role of the novel cytokines IL-35 and IL-37 in inflammatory bowel disease, " Mediators of Inflammation, vol. 2014, Article ID 136329, 10 pages, 2014.
28. D. C. Gondek, L.-F. Lu, S. A. Quezada, S. Sakaguchi, R. J. Noelle, "Cutting edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independentmechanism, " The Journal of Immunology, vol. 174, no. 4, pp. 1783-1786, 2005.
29. D. C. Gondek, V. DeVries, E. C. Nowak et al., "Transplantation survival is maintained by granzyme B+ regulatory cells and adaptive regulatory T cells, " The Journal of Immunology, vol. 181, no. 7, pp. 4752-4760, 2008.
30. X. Cao, S. F. Cai, T. A. Fehniger et al., "Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance, " Immunity, vol. 27, no. 4, pp. 635-646, 2007.
31. B. D. Choi, P. C. Gedeon, J. E. Herndon et al., "Human regulatory T cells kill tumor cells through granzyme-dependent cytotoxicity upon retargetingwith a bispecific antibody, " Cancer Immunology Research, vol. 1, no. 3, p. 163, 2013.
32. C. W. Ashley and C. Baecher-Allan, "Cutting edge: responder T cells regulate human DR+ effector regulatory T cell activity via granzyme B, " The Journal of Immunology, vol. 183, no. 8, pp. 4843-4847, 2009.
33. C. L. Ewen, K. P. Kane, R. C. Bleackley, "A quarter century of granzymes, " Cell Death and Differentiation, vol. 19, no. 1, pp. 28-35, 2012.
34. C. J. Froelich, K. Orth, J. Turbov et al., "New paradigm for lymphocyte granule-mediated cytotoxicity. Target cells bind and internalize granzyme B, but an endosomolytic agent is necessary for cytosolic delivery and subsequent apoptosis, " The Journal of Biological Chemistry, vol. 271, no. 46, pp. 29073-29079, 1996.
35. J. Lieberman, "Granzyme A activates another way to die, " Immunological Reviews, vol. 235, no. 1, pp. 93-104, 2010.
36. M. J. Pinkoski, M. Hobman, J. A. Heibein et al., "Entry and trafficking of granzyme B in target cells during granzyme Bperforin-mediated apoptosis, " Blood, vol. 92, no. 3, pp. 1044-1054, 1998.
37. L. Shi, S. Mai, S. Israels, K. Browne, J. A. Trapani, A. H. Greenberg, "Granzyme B (GraB) autonomously crosses the cell membrane and perforin initiates apoptosis and GraB nuclear localization, "The Journal of ExperimentalMedicine, vol. 185, no. 5, pp. 855-866, 1997.
38. J. Li, S. K. Figueira, A. C. A. Vrazo et al., "Real-time detection of CTL function reveals distinct patterns of caspase activation mediated by Fas versus granzyme B, " The Journal of Immunology, vol. 193, no. 2, pp. 519-528, 2014.
39. G. Jacquemin, D. Margiotta, A. Kasahara et al., "Granzyme Binduced mitochondrial ROS are required for apoptosis, " Cell Death and Differentiation, vol. 22, no. 5, pp. 862-874, 2015.
40. G. MacDonald, L. Shi, C. Vande Velde, J. Lieberman, A. H. Greenberg, "Mitochondria-dependent and-independent regulation of granzyme B-induced apoptosis, " The Journal of Experimental Medicine, vol. 189, no. 1, pp. 131-143, 1999.
41. C. Metcalfe, P. Cresswell, A. N. Barclay, "Interleukin-2 signalling is modulated by a labile disulfide bond in the CD132 chain of its receptor, " Open Biology, vol. 2, Article ID 110036, 2012.
42. A. L. Bayer, A. Pugliese, T. R. Malek, "The IL-2/IL-2R system: from basic science to therapeutic applications to enhance immune regulation, " Immunologic Research, vol. 57, no. 1-3, pp. 197-209, 2013.
43. M. A. Burchill, J. Yang, K. B. Vang, M. A. Farrar, "Interleukin-2 receptor signaling in regulatory T cell development and homeostasis, " Immunology Letters, vol. 114, no. 1, pp. 1-8, 2007.
44. T. L. Whiteside, M. Mandapathil, P. Schuler, "The role of the adenosinergic pathway in immunosuppression mediated by human regulatory T cells (Treg), " CurrentMedicinal Chemistry, vol. 18, no. 34, pp. 5217-5223, 2011.
45. M. Almahariq, F. C. Mei, H. Wang et al., "Exchange protein directly activated by cAMP modulates regulatory T-cellmediated immunosuppression, " Biochemical Journal, vol. 465, pp. 295-303, 2015.
46. B. Huang, J. Zhao, Z. Lei et al., "miR-142-3p restricts cAMP production in CD4+CD25 T cells and CD4+CD25+TREG cells by targeting AC9mRNA, " EMBOReports, vol. 10, no. 2, pp. 180-185, 2009.
47. C.-W. Chow and R. J. Davis, "Integration of calcium and cyclic AMP signaling pathways by 14-3-3, " Molecular and Cellular Biology, vol. 20, no. 2, pp. 702-712, 2000.
48. C. W. Dessauer, "Adenylyl cyclase-A-kinase anchoring protein complexes: the next dimension in cAMP signaling, " Molecular Pharmacology, vol. 76, no. 5, pp. 935-941, 2009.
49. S. Vendetti, A. Riccomi, A. Sacchi, L. Gatta, C. Pioli, M. T. De Magistris, "Cyclic adenosine 5-monophosphate and calcium induce CD152 (CTLA-4) up-regulation in resting CD4+ T lymphocytes, "The Journal of Immunology, vol. 169, no. 11, pp. 6231-6235, 2002.
50. G. Borsellino, M. Kleinewietfeld, D. DiMitri et al., "Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression, " Blood, vol. 110, no. 4, pp. 1225-1232, 2007.
51. S. Deaglio, K. M. Dwyer, W. Gao et al., "Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression, " The Journal of Experimental Medicine, vol. 204, no. 6, pp. 1257-1265, 2007.
52. A. Ohta and M. Sitkovsky, "Extracellular adenosine-mediated modulation of regulatory T cells, " Frontiers in Immunology, vol. 5, article 304, 2014.
53. G. Hasko, D. G. Kuhel, J.-F. Chen et al., "Adenosine inhibits IL-12 and TNF-production via adenosine A2a receptordependent and independent mechanisms, " The FASEB Journal, vol. 14, no. 13, pp. 2065-2074, 2000.
54. B. Mayr and M. Montminy, "Transcriptional regulation by the phosphorylation-dependent factor CREB, " Nature Reviews Molecular Cell Biology, vol. 2, no. 8, pp. 599-609, 2001.
55. M. Fassbender, B. Gerlitzki, N. Ullrich et al., "Cyclic adenosine monophosphate and IL-10 coordinately contribute to nTreg cell-mediated suppression of dendritic cell activation, " Cellular Immunology, vol. 265, no. 2, pp. 91-96, 2010.
56. N. D. Khoa, M. C. Montesinos, A. B. Reiss, D. Delano, N. Awadallah, B. N. Cronstein, "Inflammatory cytokines regulate function and expression of adenosine A2A receptors in human monocytic THP-1 cells, " Journal of Immunology, vol. 167, no. 7, pp. 4026-4032, 2001.
57. S. Beissert, A. Schwarz, T. Schwarz, "Regulatory T cells, " Journal of Investigative Dermatology, vol. 126, no. 1, pp. 15-24, 2006.
58. A. Boasso, J.-P. Herbeuval, A. W. Hardy, C. Winkler, G. M. Shearer, "Regulation of indoleamine 2, 3-dioxygenase and tryptophanyl-tRNA-synthetase by CTLA-4-Fc in human CD4+ T cells, " Blood, vol. 105, no. 4, pp. 1574-1581, 2005.
59. B. Widner, M. Ledochowski, D. Fuchs, "Interferongamma-induced tryptophan degradation: neuropsychiatric and immunological consequences, " CurrentDrugMetabolism, vol. 1, no. 2, pp. 193-204, 2000.
60. D. H. Munn and A. L. Mellor, "Indoleamine 2, 3-dioxygenase and tumor-induced tolerance, "The Journal of Clinical Investigation, vol. 117, no. 5, pp. 1147-1154, 2007.
61. Y. Yan, G.-X. Zhang, B. Gran et al., "IDO upregulates regulatory T cells via tryptophan catabolite and suppresses encephalitogenic T cell responses in experimental autoimmune encephalomyelitis, " The Journal of Immunology, vol. 185, no. 10, pp. 5953-5961, 2010.
62. J. Dong, H. Qiu, M. Garcia-Barrio, J., erson, A. G. Hinnebusch, "Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain, " Molecular Cell, vol. 6, no. 2, pp. 269-279, 2000.
63. G. Hueso, R. Aparicio-Sanchis, C. Montesinos, S. Lorenz, J. R. Murgua, R. Serrano, "A novel role for protein kinase Gcn2 in yeast tolerance to intracellular acid stress, " Biochemical Journal, vol. 441, no. 1, pp. 255-264, 2012.
64. U. Grohmann, F. Fallarino, P. Puccetti, "Tolerance, DCs and tryptophan: much ado about IDO, " Trends in Immunology, vol. 24, no. 5, pp. 242-248, 2003.
65. S. L. Hwang, N. P.-Y. Chung, J. K.-Y. Chan, C.-L. S. Lin, "Indoleamine 2, 3-dioxygenase (IDO) is essential for dendritic cell activation and chemotactic responsiveness to chemokines, " Cell Research, vol. 15, no. 3, pp. 167-175, 2005.
66. D. E. Bredesen, P. Mehlen, S. Rabizadeh, "Apoptosis and dependence receptors: a molecular basis for cellular addiction, " Physiological Reviews, vol. 84, no. 2, pp. 411-430, 2004.
67. D. Acehan, X. Jiang, D. G. Morgan, J. E. Heuser, X. Wang, C. W. Akey, "Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, activation, " Molecular Cell, vol. 9, no. 2, pp. 423-432, 2002.
68. S.-M. Lee, Y.-S. Lee, J.-H. Choi et al., "Tryptophan metabolite 3-hydroxyanthranilic acid selectively induces activated T cell death via intracellular GSHdepletion, " Immunology Letters, vol. 132, no. 1-2, pp. 53-60, 2010.
69. K. G. Lyamzaev, D. S. Izyumov, A. V. Avetisyan, F. Yang, O. Y. Pletjushkina, B. V. Chernyak, "Inhibition of mitochondrial bioenergetics: the effects on structure of mitochondria in the cell and on apoptosis, " Acta Biochimica Polonica, vol. 51, no. 2, pp. 553-562, 2004.
70. J. D. Mezrich, J. H. Fechner, X. Zhang, B. P. Johnson, W. J. Burlingham, C. A. Bradfield, "An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells, " The Journal of Immunology, vol. 185, no. 6, pp. 3190-3198, 2010.
71. F. T. Xie, J. S. Cao, J. Zhao, Y. Yu, F. Qi, X. C. Dai, "IDO expressing dendritic cells suppress allograft rejection of small bowel transplantation in mice by expansion of Foxp3+ regulatory T cells, " Transplant Immunology, vol. 33, no. 2, pp. 69-77, 2015.
72. C.-T. Huang, C. J. Workman, D. Flies et al., "Role of LAG-3 in regulatory T cells, " Immunity, vol. 21, no. 4, pp. 503-513, 2004.
73. J. F. Grosso, C. C. Kelleher, T. J. Harris et al., "LAG-3 regulates CD8+ T cell accumulation and effector function in murine self-and tumor-tolerance systems, " The Journal of Clinical Investigation, vol. 117, no. 11, pp. 3383-3392, 2007.
74. C. J. Workman and D. A. A. Vignali, "Negative regulation of T cell homeostasis by lymphocyte activation gene-3 (CD223), "The Journal of Immunology, vol. 174, no. 2, pp. 688-695, 2005.
75. P. Hemon, F. Jean-Louis, K. Ramgolam et al., "MHC class II engagement by its ligand LAG-3 (CD223) contributes to melanoma resistance to apoptosis, " Journal of Immunology, vol. 186, no. 9, pp. 5173-5183, 2011.
76. S., reae, S. Buisson, F. Triebel, "MHC class II signal transduction in human dendritic cells induced by a natural ligand, the LAG-3 protein (CD223), " Blood, vol. 102, no. 6, pp. 2130-2137, 2003.
77. B. Liang, C. Workman, J. Lee et al., "Regulatory T cells inhibit dendritic cells by lymphocyte activation gene-3 engagement of MHC class II, " The Journal of Immunology, vol. 180, no. 9, pp. 5916-5926, 2008.
78. G. Gloire, C. Erneux, J. Piette, "The role of SHIP1 in Tlymphocyte life and death, " Biochemical Society Transactions, vol. 35, no. 2, pp. 277-280, 2007.
79. N. Gupta, P. Hegde, M. Lecerf et al., "Japanese encephalitis virus expands regulatory T cells by increasing the expression of PDL1 on dendritic cells, " European Journal of Immunology, vol. 44, no. 5, pp. 1363-1374, 2014.
80. L. Adalid-Peralta, A. Arce-Sillas, G. Fragoso et al., "Cysticerci drive dendritic cells to promote in vitro and in vivo tregs differentiation, " Clinical and Developmental Immunology, vol. 2013, Article ID981468, 9 pages, 2013.