IFN-α Regulates Blimp-1 Expression via miR-23a and miR-125b in Both Monocytes-Derived DC and pDC

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Parlato, Stefania ^a   Bruni, Roberto ^a   Fragapane, Paola ^b   Salerno, Debora ^a   Marcantonio, Cinzia ^a   Borghi, Paola ^a   Tataseo, Paola ^c   Ciccaglione, Anna Rita ^a   Presutti, Carlo ^d   Romagnoli, Giulia ^a   Bozzoni, Irene ^d   Belardelli, Filippo ^a   Gabriele, Lucia ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b CNR   (Italy)

^c Transfusional Medicine and Molecular Biology Laboratory   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; MICRORNA; MICRORNA 125B; PROTEIN MIR 23A; UNCLASSIFIED DRUG; MIRN125 MICRORNA, HUMAN; MIRN23 MICRORNA, HUMAN; PRDM1 PROTEIN, HUMAN; REPRESSOR PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR MECHANICS; MONOCYTE; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REGULATORY MECHANISM; CYTOLOGY; DENDRITIC CELL; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; HELA CELL LINE; METABOLISM;

CELL DIFFERENTIATION; DENDRITIC CELLS; GENE EXPRESSION PROFILING; HELA CELLS; HUMANS; INTERFERON-ALPHA; MICRORNAS; MONOCYTES; PHENOTYPE; REPRESSOR PROTEINS;

EID: 84881564116     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072833     Document Type: Article

References (56)

1. Hervas-Stubbs S, Perez-Gracia JL, Rouzaut A, Sanmamed MF, Le Bon A, et al. (2011) Direct effects of type I interferons on cells of the immune system. Clin Cancer Res 17: 2619-2627. doi:10.1158/1078-0432.CCR-10-1114. PubMed: 21372217.
2. Santini SM, Lapenta C, Santodonato L, D'Agostino G, Belardelli F, et al. (2009) IFN-alpha in the generation of dendritic cells for cancer immunotherapy. Handb Exp Pharmacol: pp. 295-317. PubMed: 19031032.
3. Lapenta C, Santini SM, Spada M, Donati S, Urbani F, et al. (2006) IFN-alpha-conditioned dendritic cells are highly efficient in inducing cross-priming CD8(+) T cells against exogenous viral antigens. Eur J Immunol 36: 2046-2060. doi:10.1002/eji.200535579. PubMed: 16856207.
4. Vermi W, Fisogni S, Salogni L, Schärer L, Kutzner H, et al. (2011) Spontaneous regression of highly immunogenic Molluscum contagiosum virus (MCV)-induced skin lesions is associated with plasmacytoid dendritic cells and IFN-DC infiltration. J Invest Dermatol 131: 426-434. doi:10.1038/jid.2010.256. PubMed: 20739948.
5. Parlato S, Romagnoli G, Spadaro F, Canini I, Sirabella P, et al. (2010) LOX-1 as a natural IFN-alpha-mediated signal for apoptotic cell uptake and antigen presentation in dendritic cells. Blood 115: 1554-1563. doi:10.1182/blood-2009-07-234468. PubMed: 20009034.
6. Farkas A, Kemény L, (2012) Monocyte-derived interferon-alpha primed dendritic cells in the pathogenesis of psoriasis: new pieces in the puzzle. Int Immunopharmacol 13: 215-218. doi:10.1016/j.intimp.2012.04.003. PubMed: 22522054.
7. Li HS, Gelbard A, Martinez GJ, Esashi E, Zhang H, et al. (2011) Cell-intrinsic role for IFN-alpha-STAT1 signals in regulating murine Peyer patch plasmacytoid dendritic cells and conditioning an inflammatory response. Blood 118: 3879-3889. doi:10.1182/blood-2011-04-349761. PubMed: 21828128.
8. Swiecki M, Colonna M, (2010) Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol Rev 234: 142-162. doi:10.1111/j.0105-2896.2009.00881.x. PubMed: 20193017.
9. Vermi W, Soncini M, Melocchi L, Sozzani S, Facchetti F, (2011) Plasmacytoid dendritic cells and cancer. J Leukoc Biol.
10. Reizis B, (2010) Regulation of plasmacytoid dendritic cell development. Curr Opin Immunol 22: 206-211. doi:10.1016/j.coi.2010.01.005. PubMed: 20144853.
11. Keller AD, Maniatis T, (1991) Identification and characterization of a novel repressor of beta-interferon gene expression. Genes Dev 5: 868-879. doi:10.1101/gad.5.5.868. PubMed: 1851123.
12. Crotty S, Johnston RJ, Schoenberger SP, (2010) Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat Immunol 11: 114-120. doi:10.1038/ni.1837. PubMed: 20084069.
13. Xin A, Nutt SL, Belz GT, Kallies A, (2012) Blimp1: Driving Terminal Differentiation to a T. Adv Exp Med Biol 780: 85-100. PubMed: 21842367.
14. Alinikula J, Lassila O, (2011) Gene interaction network regulates plasma cell differentiation. Scand J Immunol 73: 512-519. doi:10.1111/j.1365-3083.2011.02556.x. PubMed: 21388429.
15. Chan YH, Chiang MF, Tsai YC, Su ST, Chen MH, et al. (2009) Absence of the transcriptional repressor Blimp-1 in hematopoietic lineages reveals its role in dendritic cell homeostatic development and function. J Immunol 183: 7039-7046. doi:10.4049/jimmunol.0901543. PubMed: 19915049.
16. Smith MA, Wright G, Wu J, Tailor P, Ozato K, et al. (2011) Positive regulatory domain I (PRDM1) and IRF8/PU.1 counter-regulate MHC class II transactivator (CIITA) expression during dendritic cell maturation. J Biol Chem 286: 7893-7904. doi:10.1074/jbc.M110.165431. PubMed: 21216962.
17. Ebert MS, Sharp PA, (2012) Roles for microRNAs in conferring robustness to biological processes. Cell 149: 515-524. doi:10.1016/j.cell.2012.04.005. PubMed: 22541426.
18. Turner ML, Schnorfeil FM, Brocker T, (2011) MicroRNAs regulate dendritic cell differentiation and function. J Immunol 187: 3911-3917. doi:10.4049/jimmunol.1101137. PubMed: 21969315.
19. Hashimi ST, Fulcher JA, Chang MH, Gov L, Wang S, et al. (2009) MicroRNA profiling identifies miR-34a and miR-21 and their target genes JAG1 and WNT1 in the coordinate regulation of dendritic cell differentiation. Blood 114: 404-414. doi:10.1182/blood-2008-09-179150. PubMed: 19398721.
20. Lu C, Huang X, Zhang X, Roensch K, Cao Q, et al. (2011) miR-221 and miR-155 regulate human dendritic cell development, apoptosis, and IL-12 production through targeting of p27kip1, KPC1, and SOCS-1. Blood 117: 4293-4303. doi:10.1182/blood-2010-12-322503. PubMed: 21355095.
21. Zhou H, Huang X, Cui H, Luo X, Tang Y, et al. (2010) miR-155 and its star-form partner miR-155* cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 116: 5885-5894. doi:10.1182/blood-2010-04-280156. PubMed: 20852130.
22. Kuipers H, Schnorfeil FM, Brocker T, (2010) Differentially expressed microRNAs regulate plasmacytoid vs. conventional dendritic cell development. Mol Immunol 48: 333-340. doi:10.1016/j.molimm.2010.07.007. PubMed: 20822813.
23. Gururajan M, Haga CL, Das S, Leu CM, Hodson D, et al. (2010) MicroRNA 125b inhibition of B cell differentiation in germinal centers. Int Immunol 22: 583-592. doi:10.1093/intimm/dxq042. PubMed: 20497960.
24. Schmittgen TD, Lee EJ, Jiang J, Sarkar A, Yang L, et al. (2008) Real-time PCR quantification of precursor and mature microRNA. Methods 44: 31-38. doi:10.1016/j.ymeth.2007.09.006. PubMed: 18158130.
25. Chhabra R, Adlakha YK, Hariharan M, Scaria V, Saini N, (2009) Upregulation of miR-23a-27a-24-2 cluster induces caspase-dependent and-independent apoptosis in human embryonic kidney cells. PLOS ONE 4: e5848. doi:10.1371/journal.pone.0005848. PubMed: 19513126.
26. Denti MA, Rosa A, Sthandier O, De Angelis FG, Bozzoni I, (2004) A new vector, based on the PolII promoter of the U1 snRNA gene, for the expression of siRNAs in mammalian cells. Mol Ther 10: 191-199. doi:10.1016/j.ymthe.2004.04.008. PubMed: 15272480.
27. Rinaldi A, Vincenti S, De Vito F, Bozzoni I, Oliverio A, et al. (2010) Stress induces region specific alterations in microRNAs expression in mice. Behav Brain Res 208: 265-269. doi:10.1016/j.bbr.2009.11.012. PubMed: 19913057.
28. Schiavoni G, Mattei F, Sestili P, Borghi P, Venditti M, et al. (2002) ICSBP is essential for the development of mouse type I interferon-producing cells and for the generation and activation of CD8alpha(+) dendritic cells. J Exp Med 196: 1415-1425. doi:10.1084/jem.20021263. PubMed: 12461077.
29. Rizza P, Moretti F, Belardelli F, (2010) Recent advances on the immunomodulatory effects of IFN-alpha: implications for cancer immunotherapy and autoimmunity. Autoimmunity 43: 204-209. doi:10.3109/08916930903510880. PubMed: 20187707.
30. Sethupathy P, Megraw M, Hatzigeorgiou AG, (2006) A guide through present computational approaches for the identification of mammalian microRNA targets. Nat Methods 3: 881-886. doi:10.1038/nmeth954. PubMed: 17060911.
31. Hon LS, Zhang Z, (2007) The roles of binding site arrangement and combinatorial targeting in microRNA repression of gene expression. Genome Biol 8: R166. doi:10.1186/gb-2007-8-8-r166. PubMed: 17697356.
32. Gabriele L, Borghi P, Rozera C, Sestili P, Andreotti M, et al. (2004) IFN-alpha promotes the rapid differentiation of monocytes from patients with chronic myeloid leukemia into activated dendritic cells tuned to undergo full maturation after LPS treatment. Blood 103: 980-987. PubMed: 14525781.
33. Smith MA, Maurin M, Cho HI, Becknell B, Freud AG, et al. (2010) PRDM1/Blimp-1 controls effector cytokine production in human NK cells. J Immunol 185: 6058-6067. doi:10.4049/jimmunol.1001682. PubMed: 20944005.
34. Schmidt D, Nayak A, Schumann JE, Schimpl A, Berberich I, et al. (2008) Blimp-1Deltaexon7: a naturally occurring Blimp-1 deletion mutant with auto-regulatory potential. Exp Cell Res 314: 3614-3627. doi:10.1016/j.yexcr.2008.09.008. PubMed: 18845144.
35. Kong KY, Owens KS, Rogers JH, Mullenix J, Velu CS, et al. (2010) MIR-23A microRNA cluster inhibits B-cell development. Exp Hematol 38: 629-640 e621 doi:10.1016/j.exphem.2010.04.004. PubMed: 20399246.
36. Enomoto Y, Kitaura J, Hatakeyama K, Watanuki J, Akasaka T, et al. (2011) Emu/miR-125b transgenic mice develop lethal B-cell malignancies. Leukemia 25: 1849-1856. doi:10.1038/leu.2011.166. PubMed: 21738213.
37. Farkas A, Kemény L, (2011) Interferon-alpha in the generation of monocyte-derived dendritic cells: recent advances and implications for dermatology. Br J Dermatol 165: 247-254. doi:10.1111/j.1365-2133.2011.10301.x. PubMed: 21410666.
38. Marafioti T, Paterson JC, Ballabio E, Reichard KK, Tedoldi S, et al. (2008) Novel markers of normal and neoplastic human plasmacytoid dendritic cells. Blood 111: 3778-3792. doi:10.1182/blood-2007-10-117531. PubMed: 18218851.
39. Gabriele L, Ozato K, (2007) The role of the interferon regulatory factor (IRF) family in dendritic cell development and function. Cytokine Growth Factor Rev 18: 503-510. doi:10.1016/j.cytogfr.2007.06.008. PubMed: 17702640.
40. David M, (2010) Interferons and microRNAs. J Interferon Cytokine Res 30: 825-828. doi:10.1089/jir.2010.0080. PubMed: 20939680.
41. El Gazzar M, McCall CE, (2011) MicroRNAs regulatory networks in myeloid lineage development and differentiation: regulators of the regulators. Immunol Cell Biol, 90: 587-93. PubMed: 21912420.
42. Zhan Y, Wu L, (2012) Functional regulation of monocyte-derived dendritic cells by microRNAs. Proteins Cell 3: 497-507. doi:10.1007/s13238-012-0042-0. PubMed: 22773340.
43. Dunand-Sauthier I, Santiago-Raber ML, Capponi L, Vejnar CE, Schaad O, et al. (2011) Silencing of c-Fos expression by microRNA-155 is critical for dendritic cell maturation and function. Blood 117: 4490-4500. doi:10.1182/blood-2010-09-308064. PubMed: 21385848.
44. Wang P, Hou J, Lin L, Wang C, Liu X, et al. (2010) Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J Immunol 185: 6226-6233. doi:10.4049/jimmunol.1000491. PubMed: 20937844.
45. Tili E, Croce CM, Michaille JJ, (2009) miR-155: on the crosstalk between inflammation and cancer. Int Rev Immunol 28: 264-284. doi:10.1080/08830180903093796. PubMed: 19811312.
46. Bai Y, Qian C, Qian L, Ma F, Hou J, et al. (2012) Integrin CD11b negatively regulates TLR9-triggered dendritic cell cross-priming by upregulating microRNA-146a. J Immunol 188: 5293-5302. doi:10.4049/jimmunol.1102371. PubMed: 22551553.
47. Chen T, Li Z, Jing T, Zhu W, Ge J, et al. (2011) MicroRNA-146a regulates the maturation process and pro-inflammatory cytokine secretion by targeting CD40L in oxLDL-stimulated dendritic cells. FEBS Lett 585: 567-573. doi:10.1016/j.febslet.2011.01.010. PubMed: 21236257.
48. Chaudhuri AA, So AY, Mehta A, Minisandram A, Sinha N, et al. (2012) Oncomir miR-125b regulates hematopoiesis by targeting the gene Lin28A. Proc Natl Acad Sci U S A 109: 4233-4238. PubMed: 22366319.
49. Morgan MA, Mould AW, Li L, Robertson EJ, Bikoff EK, (2012) Alternative splicing regulates Prdm1/Blimp-1 DNA binding activities and corepressor interactions. Mol Cell Biol 32: 3403-3413. doi:10.1128/MCB.00174-12. PubMed: 22733990.
50. Kim SJ, Gregersen PK, Diamond B, (2013) Regulation of dendritic cell activation by microRNA let-7c and BLIMP1. J Clin Invest 123: 823-833. PubMed: 23298838.
51. Kim SJ, Zou YR, Goldstein J, Reizis B, Diamond B, (2011) Tolerogenic function of Blimp-1 in dendritic cells. J Exp Med 208: 2193-2199. doi:10.1084/jem.20110658. PubMed: 21948081.
52. Savitsky D, Cimmino L, Kuo T, Martins GA, Calame K, (2007) Multiple roles for Blimp-1 in B and T lymphocytes. Adv Exp Med Biol 596: 9-30. doi:10.1007/0-387-46530-8_2. PubMed: 17338172.
53. Doody GM, Stephenson S, McManamy C, Tooze RM, (2007) PRDM1/BLIMP-1 modulates IFN-gamma-dependent control of the MHC class I antigen-processing and peptide-loading pathway. J Immunol 179: 7614-7623. PubMed: 18025207.
54. Liou LY, Blasius AL, Welch MJ, Colonna M, Oldstone MB, et al. (2008) In vivo conversion of BM plasmacytoid DC into CD11b+ conventional DC during virus infection. Eur J Immunol 38: 3388-3394. doi:10.1002/eji.200838282. PubMed: 18979509.
55. Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V, (2011) Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol 29: 163-183. doi:10.1146/annurev-immunol-031210-101345. PubMed: 21219184.
56. Tel J, Torensma R, Figdor CG, de Vries IJ, (2011) IL-4 and IL-13 alter plasmacytoid dendritic cell responsiveness to CpG DNA and herpes simplex virus-1. J Invest Dermatol 131: 900-906.