YY1 Controls Immunoglobulin Class Switch Recombination and Nuclear Activation-Induced Deaminase Levels

REFERENCES

• Aoufouchi S, et al. 2008. Proteasomal degradation restricts the nuclear lifespan of AID. J. Exp. Med. 205:1357–1368.
   PubMed Web of Science ®Google Scholar
• Atchison L, Ghias A, Wilkinson F, Bonini N, Atchison ML. 2003. The YY1 transcription factor functions as a PcG protein in vivo. EMBO J. 22:1347–1358.
   PubMed Web of Science ®Google Scholar
• Ballantyne J, Henry DL, Marcu KB. 1997. Antibody class switch recombinase activity is B cell stage specific and functions stochastically in the absence of ‘targeted accessibility’ control. Int. Immunol. 9:963–974.
   PubMedGoogle Scholar
• Basu U, et al. 2011. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell 144:353–363.
   PubMed Web of Science ®Google Scholar
• Brar SS, Watson M, Diaz M. 2004. Activation-induced cytosine deaminase (AID) is actively exported out of the nucleus but retained by the induction of DNA breaks. J. Biol. Chem. 279:26395–26401.
   PubMed Web of Science ®Google Scholar
• Bushmeyer S, Park K, Atchison ML. 1995. Characterization of functional domains within the multifunctional transcription factor, YY1. J. Biol. Chem. 270:30213–30220.
   PubMed Web of Science ®Google Scholar
• Bushmeyer SM, Atchison ML. 1998. Identification of YY1 sequences necessary for association with the nuclear matrix and for transcriptional repression functions. J. Cell Biochem. 68:484–499.
   PubMedGoogle Scholar
• Castellano G, et al. 2010. Yin Yang 1 overexpression in diffuse large B-cell lymphoma is associated with B-cell transformation and tumor progression. Cell Cycle 9:557–563.
   PubMed Web of Science ®Google Scholar
• Chu CC, Paul WE, Max EE. 1992. Quantitation of immunoglobulin mu to gamma 1 heavy chain switch region recombination by a digestion-circularization polymerase chain reaction method. Proc. Natl. Acad. Sci. U. S. A. 89:6978–6982.
   PubMed Web of Science ®Google Scholar
• Cobb RM, Oestreich KJ, Osipovich OA, Oltz EM. 2006. Accessibility control of V(D)J. recombination. Adv. Immunol. 91:45–109.
   PubMed Web of Science ®Google Scholar
• Conticello SG, et al. 2008. Interaction between antibody-diversification enzyme AID and spliceosome-associated factor CTNNBL1. Mol. Cell 31:474–484.
   PubMedGoogle Scholar
• Demorest Z, et al. 2010. The interaction between AID and CIB1 is nonessential for antibody gene diversification by gene conversion or class switch recombination. PLoS One 5:e11660.
   PubMedGoogle Scholar
• de Yebenes VG, et al. 2008. miR-181b negatively regulates activation-induced cytidine deaminase in B cells. J. Exp. Med. 205:2199–2206.
   PubMed Web of Science ®Google Scholar
• Donohoe ME, Zhang L-F, Xu N, Shi Y, Lee JT. 2007. Identification of a Ctcf cofactor, YY1, for the X chromosome binary switch. Mol. Cell 25:43–56.
   PubMed Web of Science ®Google Scholar
• Dorsett Y, et al. 2008. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity 28:630–638.
   PubMed Web of Science ®Google Scholar
• Ellyard JI, Benk AS, Taylor B, Rada C, Neuberger MS. 2011. The dependence of Ig class-switching on the nuclear export sequence of AID likely reflects interaction with factors additional to Crm1 exportin. Eur. J. Immunol. 41:485–490.
   PubMedGoogle Scholar
• Ficzycz A, et al. 2001. Expression, activity, and subcellular localization of the Yin Yang1 transcription factor in Xenopus oocytes and embryos. J. Biol. Chem. 276:22819–22825.
   PubMed Web of Science ®Google Scholar
• Ficzycz A, Ovsenek N. 2002. The Yin Yang 1 transcription factor associates with ribonucleoprotein (mRNP) complexes in the cytoplasm of Xenopus oocytes. J. Biol. Chem. 277:8382–8387.
   PubMed Web of Science ®Google Scholar
• Fugmann SD, Lee AI, Shockett PE, Villey IJ, Schatz DG. 2000. The RAG proteins and V(D)J. recombination: complexes, ends, and transposition. Annu. Rev. Immunol. 18:495–527.
   PubMed Web of Science ®Google Scholar
• Gordon S, Akopyan G, Garban H, Bonavida B. 2006. Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25:1125–1142.
   PubMed Web of Science ®Google Scholar
• Gordon SJ, Saleque S, Birshtein BK. 2003. Yin Yang 1 is a lipopolysaccharide-inducible activator of the murine 3′ Igh enhancer, hs3. J. Immunol. 170:5549–5557.
   PubMed Web of Science ®Google Scholar
• Green MR, et al. 2011. Signatures of murine B-cell development implicate Yy1 as a regulator of the germinal center-specific program. Proc. Natl. Acad. Sci. U. S. A. 108:2873–2878.
   PubMed Web of Science ®Google Scholar
• Han L, Masani S, Yu K. 2010. CTNNBL1 is dispensible for Ig class switch recombination. J. Immunol. 185:1379–1381.
   PubMedGoogle Scholar
• Hasler J, Rada C, Neuberger MS. 2011. Cytoplasmic activation-induced cytidine deaminase (AID) exists in stoichiometric complex with translation elongation factor 1a (eEF1A).
   Google Scholar
• Ito S, et al. 2004. Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1. Proc. Natl. Acad. Sci. U. S. A. 101:1975–1980.
   PubMed Web of Science ®Google Scholar
• Jeevan-Raj BP, et al. 2011. Epigenetic tethering of AID to the donor switch region during immunoglobulin class switch recombination. J. Exp. Med. 208:1649–1660.
   PubMed Web of Science ®Google Scholar
• Jung D, Giallourakis C, Mostoslavsky R, Alt FW. 2006. Mechanism and control of V(D)J recombination at the immunoglobulin heavy chain locus. Annu. Rev. Immunol. 24:541–570.
   PubMed Web of Science ®Google Scholar
• Kim JD, Hinz AK, Choo JH, Stubbs L, Kim J. 2007. YY1 as a controlling factor for the Peg3 and Gnas imprinted domains. Genomics 89:262–269.
   PubMed Web of Science ®Google Scholar
• Krippner-Heidenreich A, et al. 2005. Caspase-dependent regulation and subcellular redistribution of the transcriptional modulator YY1 during apoptosis. Mol. Cell. Biol. 25:3704–3714.
   PubMed Web of Science ®Google Scholar
• Liu H, et al. 2007. Yin Yang 1 is a critical regulator of B-cell development. Genes Dev. 21:1179–1189.
   PubMed Web of Science ®Google Scholar
• Liu M, Schatz DG. 2009. Balancing AID and DNA repair during somatic hypermutation. Trends Immunol. 30:173–181.
   PubMed Web of Science ®Google Scholar
• Maitra S, Atchison M. 2000. BSAP can repress enhancer activity by targeting PU.1 function. Mol. Cell Biol. 20:1911–1922.
   PubMedGoogle Scholar
• Martin A, Scharff MD. 2002. AID and mismatch repair in antibody diversification. Nat. Rev. Immunol. 2:605–614.
   PubMedGoogle Scholar
• McBride KM, Barreto V, Ramiro AR, Stavropoulos P, Nussenzweig MC. 2004. Somatic hypermutation is limited by CRM1-dependent nuclear export of activation-induced deaminase. J. Exp. Med. 199:1235–1244.
   PubMed Web of Science ®Google Scholar
• Muramatsu M, et al. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553–563.
   PubMed Web of Science ®Google Scholar
• Muramatsu M, et al. 1999. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J. Biol. Chem. 274:18470–18476.
   PubMed Web of Science ®Google Scholar
• Nagulapalli S, Pongubala JMR, Atchison ML. 1995. Multiple proteins physically interact with PU.1. J. Immunol. 155:4330–4338.
   PubMedGoogle Scholar
• Nowak U, Matthews AJ, Zheng S, Chaudhuri J. 2011. The splicing regulator PTBP2 interacts with the cytidine deaminase AID and promotes binding of AID to switch-region DNA. Nat. Immunol. 12:160–166.
   PubMedGoogle Scholar
• Okazaki I-M, Kotani A, Honjo T. 2007. Role of AID in tumorigensis. Adv. Immunol. 94:245–273.
   PubMedGoogle Scholar
• Orthwein A, et al. 2010. Regulation of activation-induced deaminase stability and antibody gene diversification by Hsp90. J. Exp. Med. 207:2751–2765.
   PubMed Web of Science ®Google Scholar
• Palko L, Bass HW, Beyrouthy MJ, Hurt MM. 2004. The Yin Yang-1 (YY1) protein undergoes a DNA-replication-associated switch in localization from the cytoplasm to the nucleus at the onset of S phase. J. Cell Sci. 117:465–476.
   PubMed Web of Science ®Google Scholar
• Park K, Atchison ML. 1991. Isolation of a candidate repressor/activator, NF-E1 (YY-1, δ), that binds to the immunoglobulin κ 3′ enhancer and the immunoglobulin heavy-chain μE1 site. Proc. Natl. Acad. Sci. U. S. A. 88:9804–9808.
   PubMed Web of Science ®Google Scholar
• Pasqualucci L, et al. 2008. AID is required for germinal center-derived lymphomagenesis. Nat. Gen. 40:108–112.
   PubMed Web of Science ®Google Scholar
• Pavri R, et al. 2010. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell 143:122–133.
   PubMed Web of Science ®Google Scholar
• Perkel JM, Atchison ML. 1998. A two-step mechanism for recruitment of Pip by PU.1. J. Immunol. 160:241–252.
   PubMedGoogle Scholar
• Pongubala JMR, Atchison ML. 1991. Functional characterization of the developmentally controlled immunoglobulin kappa 3′ enhancer: regulation by Id, a repressor of helix-loop-helix transcription factors. Mol. Cell. Biol. 11:1040–1047.
   PubMedGoogle Scholar
• Pongubala JMR, Atchison ML. 1997. PU.1 can participate in an active enhancer complex without its transcriptional activation domain. Proc. Natl. Acad. Sci. U. S. A. 94:127–132.
   PubMed Web of Science ®Google Scholar
• Pongubala JMR, et al. 1992. PU.1 recruits a second nuclear factor to a site important for immunoglobulin k 3′ enhancer activity. Mol. Cell. Biol. 12:368–378.
   PubMedGoogle Scholar
• Pongubala JMR, et al. 1993. Effect of PU.1 phosphorylation on interaction with NF-EM5 and transcriptional activation. Science 259:1622–1625.
   PubMedGoogle Scholar
• Rada C, Jarvis JM, Milstein C. 2002. AID-GFP chimeric protein increases hypermutation of Ig genes with no evidence of nuclear localization. Proc. Natl. Acad. Sci. U. S. A. 99:7003–7008.
   PubMed Web of Science ®Google Scholar
• Ranjit S, et al. 2011. AID binds cooperatively with UNG and Msh2-Msh6 to Ig switch regions dependent upon the AID C terminus. J. Immunol. 187:2464–2475.
   PubMedGoogle Scholar
• Revy P, et al. 2000. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the hyper-IgM syndrome (HIGM2). Cell 102:565–575.
   PubMed Web of Science ®Google Scholar
• Rizkallah R, Hurt MM. 2009. Regulation of the transcription factor YY1 in mitosis through phosphorylation of its DNA-binding domain. Mol. Cell. Biol. 20:4766–4776.
   Google Scholar
• Rush JS, Liu M, Odegard VH, Unniraman S, Schatz DG. 2005. Expression of activation-induced cytidine deaminase is regulated by cell division, providing a mechanistic basis for division-linked class switch recombination. Proc. Natl. Acad. Sci. U. S. A. 102:13242–13247.
   PubMed Web of Science ®Google Scholar
• Schreiber E, Matthias P, Muller MM, Schaffner W. 1989. Rapid detection of octamer binding proteins with ‘mini-extracts’, prepared from a small number of cells. Nucleic Acids Res. 17:6419.
   PubMed Web of Science ®Google Scholar
• Sernandez IV, de Yebenes VG, Dorsett Y, Ramiro AR. 2008. Haploinsufficiency of activation-induced deaminase for antibody diversification and chromosome translocations both in vitro and in vivo. PLoS One 3:e3927.
   PubMed Web of Science ®Google Scholar
• Stavnezer J. 2011. Complex regulation and function of activation-induced cytidine deaminase. Trends Immunol. 32:194–201.
   PubMedGoogle Scholar
• Storck S, Aoufouchi S, Weill J-C, Reynaud C-A. 2011. AID and partners: for better and (not) for worse. Curr. Opin. Immunol. 23:337–344.
   PubMed Web of Science ®Google Scholar
• Sucharov CC, et al. 2004. The Ku protein complex interacts with YY1, is up-regulated in human heart failure, and represses alpha myosin heavy-chain gene expression. Mol. Cell. Biol. 24:8705–8715.
   PubMedGoogle Scholar
• Sucharov CC, Mariner P, Long C, Bristow M, Leinwand L. 2003. Yin Yang 1 is increased in human heart failure and represses the activity of the human alpha-myosin heavy chain promoter. J. Biol. Chem. 278:31233–31239.
   PubMed Web of Science ®Google Scholar
• Sui G, et al. 2004. Yin Yang 1 is a negative regulator of p53. Cell 117:859–872.
   PubMed Web of Science ®Google Scholar
• Ta V-T, et al. 2003. AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat. Immunol. 4:843–848.
   PubMed Web of Science ®Google Scholar
• Takizawa M, et al. 2008. AID expression levels determine the extent of cMyc oncogenic tranlocations and the incidence of B cell tumor development. J. Exp. Med. 205:1949–1957.
   PubMed Web of Science ®Google Scholar
• Teng G, et al. 2008. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 28:621–629.
   PubMed Web of Science ®Google Scholar
• Thomas MJ, Seto E. 1999. Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key? Gene 236:197–208.
   PubMed Web of Science ®Google Scholar
• Walowitz JL, Bradley ME, Chen S, Lee T. 1998. Proteolytic regulation of the zinc finger transcription factor YY1, a repressor of muscle-restricted gene expression. J. Biol. Chem. 273:6656–6661.
   PubMedGoogle Scholar
• Wei F, Zaprazna K, Wang J, Atchison ML. 2009. PU.1 can recruit BCL6 to DNA to repress gene expression in germinal center B cells. Mol. Cell. Biol. 29:4612–4622.
   PubMedGoogle Scholar
• Wilkinson FH, Park K, Atchison ML. 2006. Polycomb recruitment to DNA in vivo by the YY1 REPO domain. Proc. Natl. Acad. Sci. U. S. A. 103:19296–19301.
   PubMed Web of Science ®Google Scholar
• Wu S, et al. 2007. A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat. Struct. Biol. 14:1665–1672.
   Google Scholar
• Wuerffel R, et al. 2007. S-S synapsis during class switch recombination is promoted by distantly located transcriptional elements and activation-induced deaminase. Immunity 27:711–722.
   PubMed Web of Science ®Google Scholar
• Xu Z, et al. 2010. 14-3-3 adaptor proteins recruit AID to 5′-AGCT-3′-rich switch regions for class switch recombination. Nat. Struct. Mol. Biol. 17:1124–1135.
   PubMed Web of Science ®Google Scholar
• Yue R, et al. 2009. Beta-arrestin1 regulates zebrafish hematopoiesis through binding to YY1 and relieving polycomb group repression. Cell 139:535–546.
   PubMedGoogle Scholar