YY1 controls immunoglobulin class switch recombination and nuclear activation-induced deaminase levels

Molecular and Cellular Biology

Volumn 32, Issue 8, 2012, Pages 1542-1554

  Zaprazna, Kristina ^a   Atchison, Michael L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; GLUTATHIONE TRANSFERASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR YY1;

ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL PROLIFERATION; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVITY; GENE CONSTRUCT; GENE REARRANGEMENT; GENE SILENCING; GENOTYPING TECHNIQUE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN CELL;

ANIMALS; B-LYMPHOCYTES; CELL LINE; CELL NUCLEUS; CYTIDINE DEAMINASE; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; MICE; MICE, INBRED C57BL; PROTEIN BINDING; SPLEEN; YY1 TRANSCRIPTION FACTOR;

EID: 84861326698     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05989-11     Document Type: Article

References (72)

1. Aoufouchi S, et al. 2008. Proteasomal degradation restricts the nuclear lifespan of AID. J. Exp. Med. 205:1357-1368.
2. 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.
3. 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.
4. 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.
5. 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.
6. Bushmeyer S, Park K, Atchison ML. 1995. Characterization of functional domains within the multifunctional transcription factor, YY1. J. Biol. Chem. 270:30213-30220.
7. 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.
8. 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.
9. Chu CC, Paul WE, Max EE. 1992. Quantitation of immunoglobulin mu to gamma 1 heavy chain switch region recombination by a digestioncircularization polymerase chain reaction method. Proc. Natl. Acad. Sci. U. S. A. 89:6978-6982.
10. Cobb RM, Oestreich KJ, Osipovich OA, Oltz EM. 2006. Accessibility control of V(D)J. recombination. Adv. Immunol. 91:45-109.
11. Conticello SG, et al. 2008. Interaction between antibody-diversification enzyme AID and spliceosome-associated factor CTNNBL1. Mol. Cell 31:474-484.
12. 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.
13. de Yebenes VG, et al. 2008. miR-181b negatively regulates activationinduced cytidine deaminase in B cells. J. Exp. Med. 205:2199-2206.
14. 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.
15. Dorsett Y, et al. 2008. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity 28:630-638.
16. 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.
17. 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.
18. 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.
19. 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.
20. Gordon S, Akopyan G, Garban H, Bonavida B. 2006. Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25:1125-1142.
21. 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.
22. 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.
23. Han L, Masani S, Yu K. 2010. CTNNBL1 is dispensible for Ig class switch recombination. J. Immunol. 185:1379-1381.
24. Hasler J, Rada C, Neuberger MS. 2011. Cytoplasmic activation-induced cytidine deaminase (AID) exists in stoichiometric complex with translation elongation factor 1a (eEF1A).
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. Liu H, et al. 2007. Yin Yang 1 is a critical regulator of B-cell development. Genes Dev. 21:1179-1189.
31. Liu M, Schatz DG. 2009. Balancing AID and DNA repair during somatic hypermutation. Trends Immunol. 30:173-181.
32. Maitra S, Atchison M. 2000. BSAP can repress enhancer activity by targeting PU.1 function. Mol. Cell Biol. 20:1911-1922.
33. Martin A, Scharff MD. 2002. AID and mismatch repair in antibody diversification. Nat. Rev. Immunol. 2:605-614.
34. 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.
35. 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.
36. 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.
37. Nagulapalli S, Pongubala JMR, Atchison ML. 1995. Multiple proteins physically interact with PU.1. J. Immunol. 155:4330-4338.
38. 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.
39. Okazaki I-M, Kotani A, Honjo T. 2007. Role of AID in tumorigensis. Adv. Immunol. 94:245-273.
40. Orthwein A, et al. 2010. Regulation of activation-induced deaminase stability and antibody gene diversification by Hsp90. J. Exp. Med. 207:2751-2765.
41. 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.
42. 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.
43. Pasqualucci L, et al. 2008. AID is required for germinal center-derived lymphomagenesis. Nat. Gen. 40:108-112.
44. 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.
45. Perkel JM, Atchison ML. 1998. A two-step mechanism for recruitment of Pip by PU.1. J. Immunol. 160:241-252.
46. 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.
47. 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.
48. 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.
49. Pongubala JMR, et al. 1993. Effect of PU.1 phosphorylation on interaction with NF-EM5 and transcriptional activation. Science 259:1622-1625.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. Stavnezer J. 2011. Complex regulation and function of activationinduced cytidine deaminase. Trends Immunol. 32:194-201.
58. 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.
59. Sucharov CC, et al. 2004. The Ku protein complex interacts with YY1, is up-regulated in human heart failure, and represses alpha myosin heavychain gene expression. Mol. Cell. Biol. 24:8705-8715.
60. 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.
61. Sui G, et al. 2004. Yin Yang 1 is a negative regulator of p53. Cell 117:859-872.
62. Ta V-T, et al. 2003. AID mutant analyses indicate requirement for classswitch-specific cofactors. Nat. Immunol. 4:843-848.
63. 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.
64. Teng G, et al. 2008. MicroRNA-155 is a negative regulator of activationinduced cytidine deaminase. Immunity 28:621-629.
65. Thomas MJ, Seto E. 1999. Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key? Gene 236:197-208.
66. 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.
67. 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.
68. 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.
69. Wu S, et al. 2007. A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat. Struct. Biol. 14:1665-1672.
70. Wuerffel R, et al. 2007. S-S synapsis during class switch recombination is promoted by distantly located transcriptional elements and activationinduced deaminase. Immunity 27:711-722.
71. 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.
72. Yue R, et al. 2009. Beta-arrestin1 regulates zebrafish hematopoiesis through binding to YY1 and relieving polycomb group repression. Cell 139:535-546.