Maintenance of the marginal-zone B cell compartment specifically requires the RNA-binding protein ZFP36L1 (original) (raw)

• Cinamon, G., Zachariah, M.A., Lam, O.M., Foss, F.W. Jr. & Cyster, J.G. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 9, 54–62 (2008).
  Article CAS PubMed Google Scholar
• Arnon, T.I., Horton, R.M., Grigorova, I.L. & Cyster, J.G. Visualization of splenic marginal zone B-cell shuttling and follicular B-cell egress. Nature 493, 684–688 (2013).
  Article CAS PubMed Google Scholar
• Song, J. et al. Extracellular matrix of secondary lymphoid organs impacts on B-cell fate and survival. Proc. Natl. Acad. Sci. USA 110, E2915–E2924 (2013).
  CAS PubMed PubMed Central Google Scholar
• Simonetti, G. et al. IRF4 controls the positioning of mature B cells in the lymphoid microenvironments by regulating NOTCH2 expression and activity. J. Exp. Med. 210, 2887–2902 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Fasnacht, N. et al. Specific fibroblastic niches in secondary lymphoid organs orchestrate distinct Notch-regulated immune responses. J. Exp. Med. 211, 2265–2279 (2014).
  Article PubMed PubMed Central Google Scholar
• Cerutti, A., Cols, M. & Puga, I. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat. Rev. Immunol. 13, 118–132 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Pillai, S. & Cariappa, A. The follicular versus marginal zone B lymphocyte cell fate decision. Nat. Rev. Immunol. 9, 767–777 (2009).
  Article CAS PubMed Google Scholar
• Martin, F. & Kearney, J.F. Marginal-zone B cells. Nat. Rev. Immunol. 2, 323–335 (2002).
  Article CAS PubMed Google Scholar
• Srivastava, B., Quinn, W.J. III, Hazard, K., Erikson, J. & Allman, D. Characterization of marginal zone B cell precursors. J. Exp. Med. 202, 1225–1234 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Kleiman, E. et al. Distinct transcriptomic features are associated with transitional and mature B-cell populations in the mouse spleen. Front. Immunol. 6, 30 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Tan, J.B. et al. Lunatic and manic fringe cooperatively enhance marginal zone B cell precursor competition for delta-like 1 in splenic endothelial niches. Immunity 30, 254–263 (2009).
  Article PubMed CAS Google Scholar
• Witt, C.M., Won, W.J., Hurez, V. & Klug, C.A. Notch2 haploinsufficiency results in diminished B1 B cells and a severe reduction in marginal zone B cells. J. Immunol. 171, 2783–2788 (2003).
  Article CAS PubMed Google Scholar
• Feng, J. et al. IFN regulatory factor 8 restricts the size of the marginal zone and follicular B cell pools. J. Immunol. 186, 1458–1466 (2011).
  Article CAS PubMed Google Scholar
• Hart, G.T., Wang, X., Hogquist, K.A. & Jameson, S.C. Krüppel-like factor 2 (KLF2) regulates B-cell reactivity, subset differentiation, and trafficking molecule expression. Proc. Natl. Acad. Sci. USA 2, 1–6 (2010).
  Google Scholar
• Winkelmann, R. et al. B cell homeostasis and plasma cell homing controlled by Krüppel-like factor 2. Proc. Natl. Acad. Sci. USA 108, 710–715 (2011).
  Article CAS PubMed Google Scholar
• Vu, T.T. et al. Impaired B cell development in the absence of Krüppel-like factor 3. J. Immunol. 187, 5032–5042 (2011).
  Article CAS PubMed Google Scholar
• Clipson, A. et al. KLF2 mutation is the most frequent somatic change in splenic marginal zone lymphoma and identifies a subset with distinct genotype. Leukemia 29, 1177–1185 (2015).
  Article CAS PubMed Google Scholar
• Turner, M., Galloway, A. & Vigorito, E. Noncoding RNA and its associated proteins as regulatory elements of the immune system. Nat. Immunol. 15, 484–491 (2014).
  Article CAS PubMed Google Scholar
• Belver, L., de Yébenes, V.G. & Ramiro, A.R. MicroRNAs prevent the generation of autoreactive antibodies. Immunity 33, 713–722 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Kramer, N.J. et al. Altered lymphopoiesis and immunodeficiency in miR-142 null mice. Blood 125, 3720–3730 (2015).
  Article CAS PubMed Google Scholar
• Yuan, J., Nguyen, C.K., Liu, X., Kanellopoulou, C. & Muljo, S.A. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science 335, 1195–1200 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Zhou, Y. et al. Lin28b promotes fetal B lymphopoiesis through the transcription factor Arid3a. J. Exp. Med. 212, 569–580 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Galloway, A. et al. RNA-binding proteins ZFP36L1 and ZFP36L2 promote cell quiescence. Science 352, 453–459 (2016).
  Article CAS PubMed Google Scholar
• Kwon, K. et al. Instructive role of the transcription factor E2A in early B lymphopoiesis and germinal center B cell development. Immunity 28, 751–762 (2008).
  Article CAS PubMed Google Scholar
• Bell, S.E. et al. The RNA binding protein Zfp36l1 is required for normal vascularisation and post-transcriptionally regulates VEGF expression. Dev. Dyn. 235, 3144–3155 (2006).
  Article CAS PubMed Google Scholar
• Stumpo, D.J. et al. Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc finger protein of the Tristetraprolin family. Mol. Cell. Biol. 24, 6445–6455 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Allman, D. et al. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167, 6834–6840 (2001).
  Article CAS PubMed Google Scholar
• Vogel, K.U., Bell, L.S., Galloway, A., Ahlfors, H. & Turner, M. The RNA-binding proteins Zfp36l1 and Zfp36l2 enforce the thymic β-selection checkpoint by limiting DNA damage response signaling and cell cycle progression. J. Immunol. 197, 2673–2685 (2016).
  Article CAS PubMed Google Scholar
• Oliver, A.M., Martin, F., Gartland, G.L., Carter, R.H. & Kearney, J.F. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 27, 2366–2374 (1997).
  Article CAS PubMed Google Scholar
• Leadbetter, E.A. et al. NK T cells provide lipid antigen-specific cognate help for B cells. Proc. Natl. Acad. Sci. USA 105, 8339–8344 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Grajales-Reyes, G.E. et al. Batf3 maintains autoactivation of Irf8 for commitment of a CD8α+ conventional DC clonogenic progenitor. Nat. Immunol. 16, 708–717 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Winkelmann, R., Sandrock, L., Kirberg, J., Jäck, H.M. & Schuh, W. KLF2--a negative regulator of pre-B cell clonal expansion and B cell activation. PLoS One 9, e97953 (2014).
  Article PubMed PubMed Central CAS Google Scholar
• Yeo, J.C. et al. Klf2 is an essential factor that sustains ground state pluripotency. Cell Stem Cell 14, 864–872 (2014).
  Article CAS PubMed Google Scholar
• Revilla-i-Domingo, R. et al. The B-cell identity factor Pax5 regulates distinct transcriptional programmes in early and late B lymphopoiesis. EMBO J. 31, 3130–3146 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Keene, J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 8, 533–543 (2007).
  Article CAS PubMed Google Scholar
• Kaymak, E. & Ryder, S.P. RNA recognition by the Caenorhabditis elegans oocyte maturation determinant OMA-1. J. Biol. Chem. 288, 30463–30472 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Farley, B.M. & Ryder, S.P. POS-1 and GLD-1 repress glp-1 translation through a conserved binding-site cluster. Mol. Biol. Cell 23, 4473–4483 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Tamburino, A.M., Ryder, S.P. & Walhout, A.J.M. A compendium of Caenorhabditis elegans RNA binding proteins predicts extensive regulation at multiple levels. G3-Genes Genom. Genet. 3, 297–304 (2013).
  CAS Google Scholar
• Hoek, K.L. et al. Follicular B cell trafficking within the spleen actively restricts humoral immune responses. Immunity 33, 254–265 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Santio, N.M. et al. Pim kinases promote migration and metastatic growth of prostate cancer xenografts. PLoS One 10, e0130340 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Grundler, R. et al. Dissection of PIM serine/threonine kinases in FLT3-ITD-induced leukemogenesis reveals PIM1 as regulator of CXCL12-CXCR4-mediated homing and migration. J. Exp. Med. 206, 1957–1970 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Jain, M., Zhang, L., Patterson, E.E. & Kebebew, E. KIAA0101 is overexpressed, and promotes growth and invasion in adrenal cancer. PLoS One 6, e26866 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Aranda, J.F. et al. MYADM regulates Rac1 targeting to ordered membranes required for cell spreading and migration. Mol. Biol. Cell 22, 1252–1262 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Aranda, J.F. et al. MYADM controls endothelial barrier function through ERM-dependent regulation of ICAM-1 expression. Mol. Biol. Cell 24, 483–494 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Devis, L. et al. Activated leukocyte cell adhesion molecule (ALCAM) is a marker of recurrence and promotes cell migration, invasion and metastasis in early stage endometrioid endometrial cancer. J. Pathol. 241, 475–487 (2017).
  Article CAS PubMed Google Scholar
• Nalvarte, I., Damdimopoulos, A.E., Rüegg, J. & Spyrou, G. The expression and activity of thioredoxin reductase 1 splice variants v1 and v2 regulate the expression of genes associated with differentiation and adhesion. Biosci. Rep. 35, e00269 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Hsiao, S.P. & Chen, S.L. Myogenic regulatory factors regulate M-cadherin expression by targeting its proximal promoter elements. Biochem. J. 428, 223–233 (2010).
  Article CAS PubMed Google Scholar
• Reginato, M.J. et al. Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat. Cell Biol. 5, 733–740 (2003).
  Article CAS PubMed Google Scholar
• de Boer, J. et al. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur. J. Immunol. 33, 314–325 (2003).
  Article CAS PubMed Google Scholar
• Hobeika, E. et al. Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 103, 13789–13794 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• de Luca, C. et al. Complete rescue of obesity, diabetes, and infertility in db/db mice by neuron-specific LEPR-B transgenes. J. Clin. Invest. 115, 3484–3493 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Bouillet, P. et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286, 1735–1738 (1999).
  CAS PubMed Google Scholar
• Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Anders, S., Pyl, P.T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).
  CAS PubMed Google Scholar
• 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).
  Article PubMed PubMed Central CAS Google Scholar
• Robinson, J.T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Thorvaldsdóttir, H., Robinson, J.T. & Mesirov, J.P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14, 178–192 (2013).
  Article PubMed CAS Google Scholar
• Chen, J., Bardes, E.E., Aronow, B.J. & Jegga, A.G. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 37, W305–W311 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6, e21800 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Gautier, L., Cope, L., Bolstad, B.M. & Irizarry, R.A. affy--analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307–315 (2004).
  Article CAS PubMed Google Scholar
• Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
  Article PubMed PubMed Central CAS Google Scholar