DGCR8-Mediated Production of Canonical Micrornas Is Critical for Regulatory T Cell Function and Stability

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Jeker, Lukas T ^a   Zhou, Xuyu ^a,c   Blelloch, Robert ^b   Bluestone, Jeffrey A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DGCR8 PROTEIN; MICRORNA; MICRORNA 150; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE;

ANIMALS; FORKHEAD TRANSCRIPTION FACTORS; GENE DELETION; GENE EXPRESSION REGULATION; GENES, LETHAL; LIVER; LUNG; MICE; MICE, TRANSGENIC; MICRORNAS; PROTEIN STABILITY; RNA-BINDING PROTEINS; T-LYMPHOCYTES, REGULATORY;

MUS;

EID: 84878579282     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066282     Document Type: Article

References (49)

1. Sakaguchi S, Miyara M, Costantino CM, Hafler DA, (2010) FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 10: 490-500.
2. Tang Q, Bluestone JA, (2008) The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nat Immunol 9: 239-244.
3. O'Shea JJ, Paul WE Mechanisms Underlying Lineage Commitment and Plasticity of Helper CD4+ T Cells. Science 327: 1098-1102.
4. Zhou X, Bailey-Bucktrout S, Jeker LT, Bluestone JA, (2009) Plasticity of CD4(+) FoxP3(+) T cells. Current opinion in immunology 21: 281-285.
5. Zhou X, Bailey-Bucktrout SL, Jeker LT, Penaranda C, Martinez-Llordella M, et al. (2009) Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nature immunology 10: 1000-1007.
6. Bailey-Bucktrout SL, Bluestone JA, (2011) Regulatory T cells: stability revisited. Trends in immunology 32: 301-306.
7. Komatsu N, Mariotti-Ferrandiz ME, Wang Y, Malissen B, Waldmann H, et al. (2009) Heterogeneity of natural Foxp3+ T cells: a committed regulatory T-cell lineage and an uncommitted minor population retaining plasticity. Proc Natl Acad Sci U S A 106: 1903-1908.
8. Hori S, (2011) Regulatory T cell plasticity: beyond the controversies. Trends in immunology 32: 295-300.
9. Tsuji M, Komatsu N, Kawamoto S, Suzuki K, Kanagawa O, et al. (2009) Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 323: 1488-1492.
10. Rudra D, Egawa T, Chong MM, Treuting P, Littman DR, et al. (2009) Runx-CBFbeta complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat Immunol 10: 1170-1177.
11. Kitoh A, Ono M, Naoe Y, Ohkura N, Yamaguchi T, et al. (2009) Indispensable role of the Runx1-Cbfbeta transcription complex for in vivo-suppressive function of FoxP3+ regulatory T cells. Immunity 31: 609-620.
12. Takahashi R, Nishimoto S, Muto G, Sekiya T, Tamiya T, et al. (2011) SOCS1 is essential for regulatory T cell functions by preventing loss of Foxp3 expression as well as IFN-γ and IL-17A production. The Journal of experimental medicine 208: 2055-2067.
13. Riley JL, June CH, Blazar BR, (2009) Human T regulatory cell therapy: take a billion or so and call me in the morning. Immunity 30: 656-665.
14. Gadina M, O'Shea JJ, (2009) Immune modulation: Turncoat regulatory T cells. Nature medicine 15: 1365.
15. Mendell JT, Olson EN, (2012) MicroRNAs in stress signaling and human disease. Cell 148: 1172-1187.
16. Ebert MS, Sharp PA, (2012) Roles for microRNAs in conferring robustness to biological processes. Cell 149: 515-524.
17. Jeker LT, Bluestone JA, (2013) MicroRNA regulation of T-cell differentiation and function. Immunological reviews 253: 65-81.
18. Zhou X, Jeker LT, Fife BT, Zhu S, Anderson MS, et al. (2008) Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. The Journal of experimental medicine 205: 1983-1991.
19. Chong MM, Rasmussen JP, Rudensky AY, Littman DR, (2008) The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. The Journal of experimental medicine 205: 2005-2017.
20. Liston A, Lu LF, O'Carroll D, Tarakhovsky A, Rudensky AY, (2008) Dicer-dependent microRNA pathway safeguards regulatory T cell function. The Journal of experimental medicine 205: 1993-2004.
21. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R, (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev 22: 2773-2785.
22. Babiarz JE, Hsu R, Melton C, Thomas M, Ullian EM, et al. (2011) A role for noncanonical microRNAs in the mammalian brain revealed by phenotypic differences in Dgcr8 versus Dicer1 knockouts and small RNA sequencing. Rna 17: 1489-1501.
23. Suh N, Baehner L, Moltzahn F, Melton C, Shenoy A, et al. (2010) MicroRNA function is globally suppressed in mouse oocytes and early embryos. Current biology: CB 20: 271-277.
24. Ma J, Flemr M, Stein P, Berninger P, Malik R, et al. (2010) MicroRNA activity is suppressed in mouse oocytes. Current biology: CB 20: 265-270.
25. Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R, (2007) DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 39: 380-385.
26. Macias S, Plass M, Stajuda A, Michlewski G, Eyras E, et al. (2012) DGCR8 HITS-CLIP reveals novel functions for the Microprocessor. Nature structural & molecular biology 19: 760-766.
27. Barad O, Mann M, Chapnik E, Shenoy A, Blelloch R, et al. (2012) Efficiency and specificity in microRNA biogenesis. Nature structural & molecular biology 19: 650-652.
28. Han J, Pedersen JS, Kwon SC, Belair CD, Kim YK, et al. (2009) Posttranscriptional crossregulation between Drosha and DGCR8. Cell 136: 75-84.
29. Shenoy A, Blelloch R, (2009) Genomic analysis suggests that mRNA destabilization by the microprocessor is specialized for the auto-regulation of Dgcr8. PLoS ONE 4: e6971.
30. Hsieh CS, Liang Y, Tyznik AJ, Self SG, Liggitt D, et al. (2004) Recognition of the peripheral self by naturally arising CD25+ CD4+ T cell receptors. Immunity 21: 267-277.
31. Hsieh CS, Zheng Y, Liang Y, Fontenot JD, Rudensky AY, (2006) An intersection between the self-reactive regulatory and nonregulatory T cell receptor repertoires. Nat Immunol 7: 401-410.
32. Friedman RC, Farh KK, Burge CB, Bartel DP, (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
33. Ravi A, Gurtan AM, Kumar MS, Bhutkar A, Chin C, et al. (2012) Proliferation and Tumorigenesis of a Murine Sarcoma Cell Line in the Absence of DICER1. Cancer cell 21: 848-855.
34. Cobb BS, Hertweck A, Smith J, O'Connor E, Graf D, et al. (2006) A role for Dicer in immune regulation. J Exp Med 203: 2519-2527.
35. Muljo SA, Ansel KM, Kanellopoulou C, Livingston DM, Rao A, et al. (2005) Aberrant T cell differentiation in the absence of Dicer. J Exp Med 202: 261-269.
36. Steiner DF, Thomas MF, Hu JK, Yang Z, Babiarz JE, et al. (2011) MicroRNA-29 regulates T-box transcription factors and interferon-gamma production in helper T cells. Immunity 35: 169-181.
37. Lu LF, Thai TH, Calado DP, Chaudhry A, Kubo M, et al. (2009) Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 30: 80-91.
38. Takahashi H, Kanno T, Nakayamada S, Hirahara K, Sciume G, et al. (2012) TGF-beta and retinoic acid induce the microRNA miR-10a, which targets Bcl-6 and constrains the plasticity of helper T cells. Nature immunology 13: 587-595.
39. Jeker LT, Zhou X, Gershberg K, de Kouchkovsky D, Morar MM, et al. (2012) MicroRNA 10a Marks Regulatory T Cells. PLoS ONE 7: e36684.
40. Ma F, Xu S, Liu X, Zhang Q, Xu X, et al. (2011) The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nature immunology 12: 861-869.
41. Kuchen S, Resch W, Yamane A, Kuo N, Li Z, et al. (2010) Regulation of microRNA expression and abundance during lymphopoiesis. Immunity 32: 828-839.
42. Smith KM, Guerau-de-Arellano M, Costinean S, Williams JL, Bottoni A, et al. (2012) miR-29ab1 deficiency identifies a negative feedback loop controlling Th1 bias that is dysregulated in multiple sclerosis. Journal of immunology 189: 1567-1576.
43. McClymont SA, Putnam AL, Lee MR, Esensten JH, Liu W, et al. (2011) Plasticity of human regulatory T cells in healthy subjects and patients with type 1 diabetes. Journal of immunology 186: 3918-3926.
44. Park CY, Jeker LT, Carver-Moore K, Oh A, Liu HJ, et al. (2012) A resource for the conditional ablation of microRNAs in the mouse. Cell Reports 1: 385-391.
45. Prosser HM, Koike-Yusa H, Cooper JD, Law FC, Bradley A, (2011) A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nature biotechnology 29: 840-845.
46. Moltzahn F, Olshen AB, Baehner L, Peek A, Fong L, et al. (2011) Microfluidic-based multiplex qRT-PCR identifies diagnostic and prognostic microRNA signatures in the sera of prostate cancer patients. Cancer research 71: 550-560.
47. Rao PK, Toyama Y, Chiang HR, Gupta S, Bauer M, et al. (2009) Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ Res 105: 585-594.
48. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, et al. (2005) Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22: 329-341.
49. Tang Q, Henriksen KJ, Bi M, Finger EB, Szot G, et al. (2004) In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 199: 1455-1465.