The negative costimulatory molecule PD-1 modulates the balance between immunity and tolerance via miR-21

European Journal of Immunology

Volumn 41, Issue 6, 2011, Pages 1754-1763

  Iliopoulos, Dimitrios ^a   Kavousanaki, Melina ^b,c   Ioannou, Marianna ^b,c   Boumpas, Dimitrios ^b,c   Verginis, Panayotis ^b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CRETE   (Greece)

^c INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

Autoimmunity; MicroRNA; Programmed death 1; Tolerance

Indexed keywords

ANTISENSE MICRORNA 21; CELL MEMBRANE PROTEIN; GAMMA INTERFERON; INTERLEUKIN 17; MICRORNA; MICRORNA 21; PROGRAMMED DEATH 1 RECEPTOR; PROGRAMMED DEATH 4 PROTEIN; SILVER; SMALL INTERFERING RNA; STAT5 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE SEVERITY; DOWN REGULATION; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IN VITRO GENE TRANSFER; KNOCKOUT MOUSE; LYMPHOCYTE PROLIFERATION; MALE; MATHEMATICAL ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SILVER INDUCED ARTHRITIS; TRANSCRIPTION REGULATION; UPREGULATION; WILD TYPE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, DIFFERENTIATION; APOPTOSIS REGULATORY PROTEINS; ARTHRITIS, EXPERIMENTAL; CD4-POSITIVE T-LYMPHOCYTES; CELL GROWTH PROCESSES; CELLS, CULTURED; GENE EXPRESSION REGULATION; INTERFERON-GAMMA; INTERLEUKIN-17; MICE; MICE, KNOCKOUT; MICRORNAS; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN BINDING; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SELF TOLERANCE; STAT5 TRANSCRIPTION FACTOR; TRANSGENES;

EID: 79957574865     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040646     Document Type: Article

References (40)

1. Keir, M. E., Butte, M. J., Freeman, G. J. and Sharpe, A. H., PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 2008. 26: 677-704.
2. Fife, B. T. and Bluestone, J. A., Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol. Rev. 2008. 224: 166-182.
3. Nishimura, H., Nose, M., Hiai, H., Minato, N. and Honjo, T., Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999. 11: 141-151.
4. Nishimura, H., Okazaki, T., Tanaka, Y., Nakatani, K., Hara, M., Matsumori, A., Sasayama, S. et al., Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001. 291: 319-322.
5. -/- mice as an efficient animal model of type I diabetes. Proc. Natl. Acad. Sci. USA 2005. 102: 11823-11828.
6. Bertsias, G. K., Nakou, M., Choulaki, C., Raptopoulou, A., Papadimitraki, E., Goulielmos, G., Kritikos, H. et al., Genetic, immunologic, and immunohistochemical analysis of the programmed death 1/programmed death ligand 1 pathway in human systemic lupus erythematosus. Arthritis Rheum. 2009. 60: 207-218.
7. Nielsen, C., Hansen, D., Husby, S., Jacobsen, B. B. and Lillevang, S. T., Association of a putative regulatory polymorphism in the PD-1 gene with susceptibility to type 1 diabetes. Tissue Antigens 2003. 62: 492-497.
8. Kroner, A., Mehling, M., Hemmer, B., Rieckmann, P., Toyka, K. V., Maurer, M. and Wiendl, H., A PD-1 polymorphism is associated with disease progression in multiple sclerosis. Ann. Neurol. 2005. 58: 50-57.
9. Prokunina, L., Padyukov, L., Bennet, A., de Faire, U., Wiman, B., Prince, J., Alfredsson, L. et al., Association of the PD-1.3A allele of the PDCD1 gene in patients with rheumatoid arthritis negative for rheumatoid factor and the shared epitope. Arthritis Rheum. 2004. 50: 1770-1773.
10. Tivol, E. A., Borriello, F., Schweitzer, A. N., Lynch, W. P., Bluestone, J. A. and Sharpe, A. H., Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 1995. 3: 541-547.
11. Nishimura, H. and Honjo, T., PD-1: an inhibitory immunoreceptor involved in peripheral tolerance. Trends Immunol. 2001. 22: 265-268.
12. Bartel, D. P., MicroRNAs: target recognition and regulatory functions. Cell 2009. 136: 215-233.
13. Croce, C. M., Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 2009. 10: 704-714.
14. Xiao, C. and Rajewsky, K., MicroRNA control in the immune system: basic principles. Cell 2009. 136: 26-36.
15. Taganov, K. D., Boldin, M. P., Chang, K. J. and Baltimore, D., NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. USA 2006. 103: 12481-12486.
16. Tili, E., Michaille, J. J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., Fabbri, M. et al., Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 2007. 179: 5082-5089.
17. Bennett, F., Luxenberg, D., Ling, V., Wang, I. M., Marquette, K., Lowe, D., Khan, N. et al., Program death-1 engagement upon TCR activation has distinct effects on costimulation and cytokine-driven proliferation: attenuation of ICOS, IL-4, and IL-21, but not CD28, IL-7, and IL-15 responses. J. Immunol. 2003. 170: 711-718.
18. Ozsolak, F., Poling, L. L., Wang, Z., Liu, H., Liu, X. S., Roeder, R. G., Zhang, X. et al., Chromatin structure analyses identify miRNA promoters. Genes Dev. 2008. 22: 3172-3183.
19. Pauley, K. M., Cha, S. and Chan, E. K., MicroRNA in autoimmunity and autoimmune diseases. J. Autoimmun. 2009. 32: 189-194.
20. Xiao, C., Srinivasan, L., Calado, D. P., Patterson, H. C., Zhang, B., Wang, J., Henderson, J. M. et al., Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat. Immunol. 2008. 9: 405-414.
21. Liston, A., Lu, L. F., O'Carroll, D., Tarakhovsky, A. and Rudensky, A. Y., Dicer-dependent microRNA pathway safeguards regulatory T cell function. J. Exp. Med. 2008. 205: 1993-2004.
22. Zhou, X., Jeker, L. T., Fife, B. T., Zhu, S., Anderson, M. S., McManus, M. T. and Bluestone, J. A., Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 2008. 205: 1983-1991.
23. Yu, D., Tan, A. H., Hu, X., Athanasopoulos, V., Simpson, N., Silva, D. G., Hutloff, A. et al., Roquin represses autoimmunity by limiting inducible T-cell co-stimulator messenger RNA. Nature 2007. 450: 299-303.
24. Du, C., Liu, C., Kang, J., Zhao, G., Ye, Z., Huang, S., Li, Z. et al., MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat. Immunol. 2009. 10: 1252-1259.
25. Pauley, K. M., Satoh, M., Chan, A. L., Bubb, M. R., Reeves, W. H. and Chan, E. K., Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res. Ther. 2008. 10: R101.
26. Nakasa, T., Miyaki, S., Okubo, A., Hashimoto, M., Nishida, K., Ochi, M. and Asahara, H., Expression of microRNA-146 in rheumatoid arthritis synovial tissue. Arthritis Rheum. 2008. 58: 1284-1292.
27. Calin, G. A. and Croce, C. M., MicroRNA signatures in human cancers. Nat. Rev. Cancer 2006. 6: 857-866.
28. Cho, W. C., OncomiRs: the discovery and progress of microRNAs in cancers. Mol. Cancer 2007. 6: 60.
29. Seike, M., Goto, A., Okano, T., Bowman, E. D., Schetter, A. J., Horikawa, I., Mathe, E. A. et al., MiR-21 is an EGFR-regulated anti-apoptotic factor in lung cancer in never-smokers. Proc. Natl. Acad. Sci. USA 2009. 106: 12085-12090.
30. Sonkoly, E., Wei, T., Janson, P. C., Saaf, A., Lundeberg, L., Tengvall-Linder, M., Norstedt, G. et al., MicroRNAs: novel regulators involved in the pathogenesis of psoriasis? PLoS One 2007. 2: e610.
31. Iliopoulos, D., Malizos, K. N., Oikonomou, P. and Tsezou, A., Integrative microRNA and proteomic approaches identify novel osteoarthritis genes and their collaborative metabolic and inflammatory networks. PLoS One 2008. 3: e3740.
32. Wu, F., Zikusoka, M., Trindade, A., Dassopoulos, T., Harris, M. L., Bayless, T. M., Brant, S. R. et al., MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology 2008. 135: 1624-1635; e1624.
33. Furtado, G. C., Curotto de Lafaille, M. A., Kutchukhidze, N. and Lafaille, J. J., Interleukin 2 signaling is required for CD4(+) regulatory T cell function. J. Exp. Med. 2002. 196: 851-857.
34. Snow, J. W., Abraham, N., Ma, M. C., Herndier, B. G., Pastuszak, A. W. and Goldsmith, M. A., Loss of tolerance and autoimmunity affecting multiple organs in STAT5A/5B-deficient mice. J. Immunol. 2003. 171: 5042-5050.
35. Franceschini, D., Paroli, M., Francavilla, V., Videtta, M., Morrone, S., Labbadia, G., Cerino, A. et al., PD-L1 negatively regulates CD4+CD25+Foxp3+Tregs by limiting STAT-5 phosphorylation in patients chronically infected with HCV. J. Clin. Invest. 2009. 119: 551-564.
36. Asangani, I. A., Rasheed, S. A., Nikolova, D. A., Leupold, J. H., Colburn, N. H., Post, S. and Allgayer, H., MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008. 27: 2128-2136.
37. Lu, Z., Liu, M., Stribinskis, V., Klinge, C. M., Ramos, K. S., Colburn, N. H. and Li, Y., MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 2008. 27: 4373-4379.
38. Frankel, L. B., Christoffersen, N. R., Jacobsen, A., Lindow, M., Krogh, A. and Lund, A. H., Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J. Biol. Chem. 2008. 283: 1026-1033.
39. Hilliard, A., Hilliard, B., Zheng, S. J., Sun, H., Miwa, T., Song, W., Goke, R. and Chen, Y. H., Translational regulation of autoimmune inflammation and lymphoma genesis by programmed cell death 4. J. Immunol. 2006. 177: 8095-8102.
40. LeBaron, M. J., Xie, J. and Rui, H., Evaluation of genome-wide chromatin library of Stat5 binding sites in human breast cancer. Mol. Cancer 2005. 4: 6.