Translational repression of pre-formed cytokine-encoding mRNA prevents chronic activation of memory T cells

Nature Immunology

Volumn 19, Issue 8, 2018, Pages 828-837

  Salerno, Fiamma ^a   Engels, Sander ^a   van den Biggelaar, Maartje ^b   van Alphen, Floris P J ^b   Guislain, Aurelie ^a   Zhao, Wanqi ^a   Hodge, Deborah L ^c   Bell, Sarah E ^d   Medema, Jan Paul ^a   von Lindern, Marieke ^a   Turner, Martin ^d   Young, Howard A ^c   Wolkers, Monika C ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b SANQUIN RESEARCH   (Netherlands)

^c NATIONAL CANCER INSTITUTE   (United States)

^d BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CYTOKINE; MESSENGER RNA; UNCLASSIFIED DRUG; ZFP36L2 PROTEIN; GAMMA INTERFERON; TRISTETRAPROLIN; ZFP36 PROTEIN, MOUSE;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AU RICH ELEMENT; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE DELETION; GENE REPRESSION; HUMAN; HUMAN CELL; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; CELL CULTURE; EPIGENETIC REPRESSION; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; RIBOSOME; T LYMPHOCYTE; TRANSGENIC MOUSE; TRANSLATION ELONGATION;

3' UNTRANSLATED REGIONS; ANIMALS; AU RICH ELEMENTS; CELLS, CULTURED; EPIGENETIC REPRESSION; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; RIBOSOMES; RNA, MESSENGER; T-LYMPHOCYTES; TRISTETRAPROLIN;

EID: 85049632671     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/s41590-018-0155-6     Document Type: Article

References (64)

1. Masopust, D. & Schenkel, J. M. The integration of T cell migration, differentiation and function. Nat. Rev. Immunol. 13, 309–320 (2013).
2. Sheridan, B. S. & Lefrançois, L. Regional and mucosal memory T cells. Nat. Immunol. 12, 485–491 (2011).
3. Harty, J. T., Tvinnereim, A. R. & White, D. W. CD8+ T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 18, 275–308 (2000).
4. +T cells to antigen stimulation in vivo. Nat. Immunol. 1, 47–53 (2000).
5. London, C. A., Lodge, M. P. & Abbas, A. K. Functional responses and costimulator dependence of memory CD4+ T cells. J. Immunol. 164, 265–272 (2000).
6. Whitmire, J. K., Eam, B. & Whitton, J. L. Tentative T cells: memory cells are quick to respond, but slow to divide. PLoS Pathog. 4, e1000041 (2008).
7. Guidotti, L. G. & Chisari, F. V. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu. Rev. Immunol. 19, 65–91 (2001).
8. +T and innate NK lymphocytes independent of cognate antigen during microbial pathogen invasion. Immunity 37, 549–562 (2012).
9. Weng, N. P., Araki, Y. & Subedi, K. The molecular basis of the memory T cell response: differential gene expression and its epigenetic regulation. Nat. Rev. Immunol. 12, 306–315 (2012).
10. Wherry, E. J. et al. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27, 670–684 (2007).
11. Philip, M. et al. Chromatin states define tumour-specific T cell dysfunction and reprogramming. Nature 545, 452–456 (2017).
12. Kaech, S. M., Hemby, S., Kersh, E. & Ahmed, R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111, 837–851 (2002).
13. Swanson, B. J., Murakami, M., Mitchell, T. C., Kappler, J. & Marrack, P. RANTES production by memory phenotype T cells is controlled by a posttranscriptional, TCR-dependent process. Immunity 17, 605–615 (2002).
14. Willinger, T., Freeman, T., Hasegawa, H., McMichael, A. J. & Callan, M. F. Molecular signatures distinguish human central memory from effector memory CD8 T cell subsets. J. Immunol. 175, 5895–5903 (2005).
15. +T cells. Proc. Natl. Acad. Sci. USA 114, 9677–9682 (2017).
16. Hodge, D. L. et al. IFN-gamma AU-rich element removal promotes chronic IFN-gamma expression and autoimmunity in mice. J. Autoimmun. 53, 33–45 (2014).
17. Kontoyiannis, D., Pasparakis, M., Pizarro, T. T., Cominelli, F. & Kollias, G. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 10, 387–398 (1999).
18. Turner, M. & Hodson, D. Regulation of lymphocyte development and function by RNA-binding proteins. Curr. Opin. Immunol. 24, 160–165 (2012).
19. Kafasla, P., Skliris, A. & Kontoyiannis, D. L. Post-transcriptional coordination of immunological responses by RNA-binding proteins. Nat. Immunol. 15, 492–502 (2014).
20. Salerno, F. & Wolkers, M. C. T-cells require post-transcriptional regulation for accurate immune responses. Biochem. Soc. Trans. 43, 1201–1207 (2015).
21. Bronevetsky, Y. et al. T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire. J. Exp. Med. 210, 417–432 (2013).
22. Wu, H. et al. miRNA profiling of naïve, effector and memory CD8 T cells. PLoS One 2, e1020 (2007).
23. Garneau, N. L., Wilusz, J. & Wilusz, C. J. The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8, 113–126 (2007).
24. Grammatikakis, I., Abdelmohsen, K. & Gorospe, M. Posttranslational control of HuR function. Wiley Interdiscip. Rev. RNA 8, e1372 (2017).
25. H17 differentiation. Nat. Immunol. 15, 1079–1089 (2014).
26. Vlasova-St Louis, I. & Bohjanen, P. R. Post-transcriptional regulation of cytokine signaling by AU-rich and GU-rich elements. J. Interferon Cytokine Res. 34, 233–241 (2014).
27. Beisang, D. & Bohjanen, P. R. Perspectives on the ARE as it turns 25 years old. Wiley Interdiscip. Rev. RNA 3, 719–731 (2012).
28. Schoenberg, D. R. & Maquat, L. E. Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet. 13, 246–259 (2012).
29. Zehn, D., Lee, S. Y. & Bevan, M. J. Complete but curtailed T-cell response to very low-affinity antigen. Nature 458, 211–214 (2009).
30. Penix, L., Weaver, W. M., Pang, Y., Young, H. A. & Wilson, C. B. Two essential regulatory elements in the human interferon gamma promoter confer activation specific expression in T cells. J. Exp. Med. 178, 1483–1496 (1993).
31. +T cells. Nat. Immunol. 7, 475–481 (2006).
32. Leppek, K. & Stoecklin, G. An optimized streptavidin-binding RNA aptamer for purification of ribonucleoprotein complexes identifies novel ARE-binding proteins. Nucleic Acids Res. 42, e13 (2014).
33. Brooks, S. A. & Blackshear, P. J. Tristetraprolin (TTP): interactions with mRNA and proteins, and current thoughts on mechanisms of action. Biochim. Biophys. Acta 1829, 666–679 (2013).
34. Galloway, A. et al. RNA-binding proteins ZFP36L1 and ZFP36L2 promote cell quiescence. Science 352, 453–459 (2016).
35. Ogilvie, R. L. et al. Tristetraprolin mediates interferon-gamma mRNA decay. J. Biol. Chem. 284, 11216–11223 (2009).
36. Taylor, G. A. et al. A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4, 445–454 (1996).
37. Hodson, D. J. et al. Deletion of the RNA-binding proteins ZFP36L1 and ZFP36L2 leads to perturbed thymic development and T lymphoblastic leukemia. Nat. Immunol. 11, 717–724 (2010).
38. Lindstein, T., June, C. H., Ledbetter, J. A., Stella, G. & Thompson, C. B. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244, 339–343 (1989).
39. Ma, F. et al. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-γ. Nat. Immunol. 12, 861–869 (2011).
40. Steiner, D. F. et al. MicroRNA-29 regulates T-box transcription factors and interferon-γ production in helper T cells. Immunity 35, 169–181 (2011).
41. Fleischer, T. C., Weaver, C. M., McAfee, K. J., Jennings, J. L. & Link, A. J. Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev. 20, 1294–1307 (2006).
42. Mackay, L. K. et al. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352, 459–463 (2016).
43. Hudson, B. P., Martinez-Yamout, M. A., Dyson, H. J. & Wright, P. E. Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat. Struct. Mol. Biol. 11, 257–264 (2004).
44. Goldrath, A. W. et al. Cytokine requirements for acute and basal homeostatic proliferation of naive and memory CD8+ T cells. J. Exp. Med. 195, 1515–1522 (2002).
45. Hochweller, K. et al. Dendritic cells control T cell tonic signaling required for responsiveness to foreign antigen. Proc. Natl. Acad. Sci. 107, 5931–5936 (2010).
46. Swamy, M. et al. A cholesterol-based allostery model of T cell receptor phosphorylation. Immunity 44, 1091–1101 (2016).
47. Abdelsamed, H. A. et al. Human memory CD8 T cell effector potential is epigenetically preserved during in vivo homeostasis. J. Exp. Med. 214, 1593–1606 (2017).
48. Piecyk, M. et al. TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha. EMBO J. 19, 4154–4163 (2000).
49. Gruber, A. R., Fallmann, J., Kratochvill, F., Kovarik, P. & Hofacker, I. L. AREsite: a database for the comprehensive investigation of AU-rich elements. Nucleic Acids Res. 39, D66–D69 (2011).
50. Stetson, D. B. et al. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J. Exp. Med. 198, 1069–1076 (2003).
51. Gessner, A., Mohrs, K. & Mohrs, M. Mast cells, basophils, and eosinophils acquire constitutive IL-4 and IL-13 transcripts during lineage differentiation that are sufficient for rapid cytokine production. J. Immunol. 174, 1063–1072 (2005).
52. Villarino, A. V. et al. Posttranscriptional silencing of effector cytokine mRNA underlies the anergic phenotype of self-reactive T cells. Immunity 34, 50–60 (2011).
53. +lung-resident memory T cells. Nat. Immunol. 17, 1467–1478 (2016).
54. Zhang, L. et al. ZFP36L2 is required for self-renewal of early burst-forming unit erythroid progenitors. Nature 499, 92–96 (2013).
55. Lee, P. P. et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15, 763–774 (2001).
56. Brummelkamp, T. R., Bernards, R. & Agami, R. Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2, 243–247 (2002).
57. Kessels, H. W., Wolkers, M. C., van den Boom, M. D., van der Valk, M. A. & Schumacher, T. N. Immunotherapy through TCR gene transfer. Nat. Immunol. 2, 957–961 (2001).
58. Salerno, F., Guislain, A., Cansever, D. & Wolkers, M. C. TLR-mediated innate production of IFN-γ by CD8+ T cells is independent of glycolysis. J. Immunol. 196, 3695–3705 (2016).
59. McCausland, M. M. et al. SAP regulation of follicular helper CD4 T cell development and humoral immunity is independent of SLAM and Fyn kinase. J. Immunol. 178, 817–828 (2007).
60. López de Silanes, I., Zhan, M., Lal, A., Yang, X. & Gorospe, M. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. USA 101, 2987–2992 (2004).
61. Rappsilber, J., Ishihama, Y. & Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663–670 (2003).
62. Kulak, N. A., Pichler, G., Paron, I., Nagaraj, N. & Mann, M. Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells. Nat. Methods 11, 319–324 (2014).
63. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008).
64. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).