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Review

Noncoding RNAs in B cell responses

ORCID Icon & ORCID Icon
Pages 633-639 | Received 30 Jun 2020, Accepted 01 Feb 2021, Published online: 15 Feb 2021

References

  • Coffre M, Koralov SB. miRNAs in B cell development and lymphomagenesis. Trends Mol Med. 2017;23:721–736.
  • Zheng B, Xi Z, Liu R, et al. The function of MicroRNAs in B-Cell development, lymphoma, and their potential in clinical practice. Front Immunol. 2018;9:936.
  • Bottini S, Pratella D, Grandjean V, et al. Recent computational developments on CLIP-seq data analysis and microRNA targeting implications. Brief Bioinform. 2018;19:1290–1301.
  • Lee FCY, Ule J. Advances in CLIP technologies for studies of protein-RNA interactions. Mol Cell. 2018;69:354–369.
  • Ule J, Hwang HW, Darnell RB. The future of cross-linking and immunoprecipitation (CLIP). Cold Spring Harb Perspect Biol. 2018;10. DOI:10.1101/cshperspect.a032243
  • Cyster JG, Allen CDC. B cell responses: cell interaction dynamics and decisions. Cell. 2019;177:524–540.
  • Yewdell WT, Chaudhuri J. A transcriptional serenAID: the role of noncoding RNAs in class switch recombination. Int Immunol. 2017;29:183–196.
  • Yu K, Lieber MR. Current insights into the mechanism of mammalian immunoglobulin class switch recombination. Crit Rev Biochem Mol Biol. 2019;54:333–351.
  • Ramirez J, Lukin K, Hagman J. From hematopoietic progenitors to B cells: mechanisms of lineage restriction and commitment. Curr Opin Immunol. 2010;22:177–184.
  • Mesin L, Ersching J, Victora GD. Germinal center B cell dynamics. Immunity. 2016;45:471–482.
  • Roco JA, Mesin L, Binder SC, et al. Class-Switch recombination occurs infrequently in germinal centers. Immunity. 2019;51:337–350 e337.
  • Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–854.
  • O’Brien J, Hayder H, Zayed Y, et al. Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne). 2018;9:402.
  • Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297.
  • Broughton JP, Lovci MT, Huang JL, et al. Pairing beyond the seed supports MicroRNA targeting specificity. Mol Cell. 2016;64:320–333.
  • Jonas S, Izaurralde E. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet. 2015;16:421–433.
  • Wang T, Xiao G, Chu Y, et al. Design and bioinformatics analysis of genome-wide CLIP experiments. Nucleic Acids Res. 2015;43:5263–5274.
  • Chi SW, Zang JB, Mele A, et al. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature. 2009;460:479–486.
  • Hafner M, Landthaler M, Burger L, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell. 2010;141:129–141.
  • Hsin JP, Lu Y, Loeb GB, et al. The effect of cellular context on miR-155-mediated gene regulation in four major immune cell types. Nat Immunol. 2018;19:1137–1145.
  • Huppertz I, Attig J, D’Ambrogio A, et al. iCLIP: protein-RNA interactions at nucleotide resolution. Methods. 2014;65:274–287.
  • Loeb GB, Khan AA, Canner D, et al. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol Cell. 2012;48:760–770.
  • Jin HY, Oda H, Lai M, et al. MicroRNA-17~92 plays a causative role in lymphomagenesis by coordinating multiple oncogenic pathways. Embo J. 2013;32:2377–2391.
  • Gagnon JD, Kageyama R, Shehata HM, et al. miR-15/16 restrain memory T cell differentiation, cell cycle, and survival. Cell Rep. 2019;28:2169–2181 e2164.
  • Wang T, Xie Y, Xiao G. dCLIP: a computational approach for comparative CLIP-seq analyses. Genome Biol. 2014;15:R11.
  • Uren PJ, Bahrami-Samani E, Burns SC, et al. Site identification in high-throughput RNA-protein interaction data. Bioinformatics. 2012;28:3013–3020.
  • Erhard F, Dolken L, Jaskiewicz L, et al. PARma: identification of microRNA target sites in AGO-PAR-CLIP data. Genome Biol. 2013;14:R79.
  • Brandl A, Daum P, Brenner S, et al. The microprocessor component, DGCR8, is essential for early B-cell development in mice. Eur J Immunol. 2016;46:2710–2718.
  • Koralov SB, Muljo SA, Galler GR, et al. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell. 2008;132:860–874.
  • de Yebenes VG, Bartolome-Izquierdo N, Ramiro AR. Regulation of B-cell development and function by microRNAs. Immunol Rev. 2013;253:25–39.
  • Belver L, de Yebenes VG, Ramiro AR. MicroRNAs prevent the generation of autoreactive antibodies. Immunity. 2010;33:713–722.
  • Kramer NJ, Wang WL, Reyes EY, et al. Altered lymphopoiesis and immunodeficiency in miR-142 null mice. Blood. 2015;125:3720–3730.
  • King JK, Ung NM, Paing MH, et al. Regulation of marginal zone B-Cell differentiation by MicroRNA-146a. Front Immunol. 2016;7:670.
  • Xiao C, Calado DP, Galler G, et al. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell. 2007;131:146–159.
  • Akkaya M, Traba J, Roesler AS, et al. Second signals rescue B cells from activation-induced mitochondrial dysfunction and death. Nat Immunol. 2018;19:871–884.
  • Waters LR, Ahsan FM, Wolf DM, et al. Initial B cell activation induces metabolic reprogramming and mitochondrial remodeling. iScience. 2018;5:99–109.
  • Fowler T, Garruss AS, Ghosh A, et al. Divergence of transcriptional landscape occurs early in B cell activation. Epigenetics Chromatin. 2015;8:20.
  • Kuchen S, Resch W, Yamane A, et al. Regulation of microRNA expression and abundance during lymphopoiesis. Immunity. 2010;32:828–839.
  • Xu S, Guo K, Zeng Q, et al. The RNase III enzyme Dicer is essential for germinal center B-cell formation. Blood. 2012;119:767–776.
  • Clurman BE, Hayward WS. Multiple proto-oncogene activations in avian leukosis virus-induced lymphomas: evidence for stage-specific events. Mol Cell Biol. 1989;9:2657–2664.
  • Rodriguez A, Vigorito E, Clare S, et al. Requirement of bic/microRNA-155 for normal immune function. Science. 2007;316:608–611.
  • Thai TH, Calado DP, Casola S, et al. Regulation of the germinal center response by microRNA-155. Science. 2007;316:604–608.
  • Vigorito E, Perks KL, Abreu-Goodger C, et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity. 2007;27:847–859.
  • Arbore G, Henley T, Biggins L, et al. MicroRNA-155 is essential for the optimal proliferation and survival of plasmablast B cells. Life Sci Alliance. 2019;2. DOI:10.26508/lsa.201800244
  • Nakagawa R, Leyland R, Meyer-Hermann M, et al. MicroRNA-155 controls affinity-based selection by protecting c-MYC+ B cells from apoptosis. J Clin Invest. 2016;126:377–388.
  • Dorsett Y, McBride KM, Jankovic M, et al. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity. 2008;28:630–638.
  • Teng G, Hakimpour P, Landgraf P, et al. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity. 2008;28:621–629.
  • Lu D, Nakagawa R, Lazzaro S, et al. The miR-155-PU.1 axis acts on Pax5 to enable efficient terminal B cell differentiation. J Exp Med. 2014;211:2183–2198.
  • Lu LF, Gasteiger G, Yu IS, et al. A single miRNA-mRNA interaction affects the immune response in a context- and cell-type-specific manner. Immunity. 2015;43:52–64.
  • Jiang S, Yan W, Wang SE, et al. Let-7 suppresses B cell activation through restricting the availability of necessary nutrients. Cell Metab. 2018;27:393–403 e394.
  • Sanchez HN, Moroney JB, Gan H, et al. B cell-intrinsic epigenetic modulation of antibody responses by dietary fiber-derived short-chain fatty acids. Nat Commun. 2020;11:60.
  • Weisel FJ, Mullett SJ, Elsner RA, et al. Germinal center B cells selectively oxidize fatty acids for energy while conducting minimal glycolysis. Nat Immunol. 2020;21:331–342.
  • Xu S, Ou X, Huo J, et al. Mir-17-92 regulates bone marrow homing of plasma cells and production of immunoglobulin G2c. Nat Commun. 2015;6:6764.
  • Xiao C, Srinivasan L, Calado DP, et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol. 2008;9:405–414.
  • He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature. 2005;435:828–833.
  • Ventura A, Young AG, Winslow MM, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell. 2008;132:875–886.
  • Lai M, Gonzalez-Martin A, Cooper AB, et al. Regulation of B-cell development and tolerance by different members of the miR-17 approximately 92 family microRNAs. Nat Commun. 2016;7:12207.
  • Wu Y, Schutt S, Paz K, et al. MicroRNA-17-92 is required for T-cell and B-cell pathogenicity in chronic graft-versus-host disease in mice. Blood. 2018;131:1974–1986.
  • Olive V, Bennett MJ, Walker JC, et al. miR-19 is a key oncogenic component of mir-17-92. Genes Dev. 2009;23:2839–2849.
  • Simpson LJ, Patel S, Bhakta NR, et al. A microRNA upregulated in asthma airway T cells promotes TH2 cytokine production. Nat Immunol. 2014;15:1162–1170.
  • Psathas JN, Doonan PJ, Raman P, et al. The Myc-miR-17-92 axis amplifies B-cell receptor signaling via inhibition of ITIM proteins: a novel lymphomagenic feed-forward loop. Blood. 2013;122:4220–4229.
  • Hines MJ, Coffre M, Mudianto T, et al. miR-29 sustains B cell survival and controls terminal differentiation via regulation of PI3K signaling. Cell Rep. 2020;33:108436.
  • O’Connell RM, Chaudhuri AA, Rao DS, et al. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci U S A. 2009;106:7113–7118.
  • Fernandez-Messina L, Rodriguez-Galan A, de Yebenes VG, et al. Transfer of extracellular vesicle-microRNA controls germinal center reaction and antibody production. EMBO Rep. 2020;21:e48925.
  • Chiou NT, Kageyama R, Ansel KM. Selective export into extracellular vesicles and function of tRNA fragments during T cell activation. Cell Rep. 2018;25:3356–3370 e3354.
  • de Candia P, Torri A, Gorletta T, et al. Intracellular modulation, extracellular disposal and serum increase of MiR-150 mark lymphocyte activation. PLoS One. 2013;8:e75348.
  • de Yebenes VG, Belver L, Pisano DG, et al. miR-181b negatively regulates activation-induced cytidine deaminase in B cells. J Exp Med. 2008;205:2199–2206.
  • Recaldin T, Hobson PS, Mann EH, et al. miR-29b directly targets activation-induced cytidine deaminase in human B cells and can limit its inappropriate expression in naive B cells. Mol Immunol. 2018;101:419–428.
  • Pavri R. R loops in the regulation of antibody gene diversification. Genes (Basel). 2017;8. DOI:10.3390/genes8060154
  • Roy D, Yu K, Lieber MR. Mechanism of R-loop formation at immunoglobulin class switch sequences. Mol Cell Biol. 2008;28:50–60.
  • Shinkura R, Tian M, Smith M, et al. The influence of transcriptional orientation on endogenous switch region function. Nat Immunol. 2003;4:435–441.
  • Yeap LS, Hwang JK, Du Z, et al. Sequence-intrinsic mechanisms that target AID mutational outcomes on antibody genes. Cell. 2015;163:1124–1137.
  • Maul RW, Chon H, Sakhuja K, et al. R-loop depletion by over-expressed RNase H1 in mouse B cells increases activation-induced deaminase access to the transcribed strand without altering frequency of isotype switching. J Mol Biol. 2017;429:3255–3263.
  • Yu K, Chedin F, Hsieh CL, et al. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat Immunol. 2003;4:442–451.
  • Basu U, Meng FL, Keim C, et al. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell. 2011;144:353–363.
  • Qiao Q, Wang L, Meng FL, et al. AID Recognizes structured DNA for class switch recombination. Mol Cell. 2017;67:361–373 e364.
  • Zheng S, Vuong BQ, Vaidyanathan B, et al. Non-coding RNA generated following lariat debranching mediates targeting of AID to DNA. Cell. 2015;161:762–773.
  • de Almeida R, Dhir CS, Dhir A, et al. RNA helicase DDX1 converts RNA G-quadruplex structures into R-loops to promote IgH class switch recombination. Mol Cell. 2018;70:650–662 e658.
  • Laffleur B, Basu U, Lim J. RNA exosome and non-coding RNA-coupled mechanisms in AID-mediated genomic alterations. J Mol Biol. 2017;429:3230–3241.
  • Nambu Y, Sugai M, Gonda H, et al. Transcription-coupled events associating with immunoglobulin switch region chromatin. Science. 2003;302:2137–2140.
  • Pavri R, Gazumyan A, Jankovic M, et al. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell. 2010;143:122–133.
  • Wiedemann EM, Peycheva M, Pavri R. DNA replication origins in immunoglobulin switch regions regulate class switch recombination in an R-loop-dependent manner. Cell Rep. 2016;17:2927–2942.
  • Pefanis E, Wang J, Rothschild G, et al. Noncoding RNA transcription targets AID to divergently transcribed loci in B cells. Nature. 2014;514:389–393.
  • Pefanis E, Wang J, Rothschild G, et al. RNA exosome-regulated long non-coding RNA transcription controls super-enhancer activity. Cell. 2015;161:774–789.
  • Rothschild G, Zhang W, Lim J, et al. Noncoding RNA transcription alters chromosomal topology to promote isotype-specific class switch recombination. Sci Immunol. 2020;5. DOI:10.1126/sciimmunol.aay5864
  • Karreth FA, Reschke M, Ruocco A, et al. The BRAF pseudogene functions as a competitive endogenous RNA and induces lymphoma in vivo. Cell. 2015;161:319–332.
  • Nair L, Chung H, Basu U. Regulation of long non-coding RNAs and genome dynamics by the RNA surveillance machinery. Nat Rev Mol Cell Biol. 2020;21:123–136.
  • Zhang X, Zhang Y, Ba Z, et al. Fundamental roles of chromatin loop extrusion in antibody class switching. Nature. 2019;575:385–389.

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