Mechanism of R-Loop Formation at Immunoglobulin Class Switch Sequences

REFERENCES

• Bardwell, P. D., C. J. Woo, K. Wei, Z. Li, A. Martin, S. Z. Sack, T. Parris, W. Edelmann, and M. D. Scharff. 2004. Altered somatic hypermutation and reduced class-switch recombination in exonuclease 1-mutant mice. Nat. Immunol. 5:224–229.
   PubMed Web of Science ®Google Scholar
• Barreto, V. M., Q. Pan-Hammarstrom, Y. Zhao, L. Hammarstrom, Z. Misulovin, and M. C. Nussenzweig. 2005. AID from bony fish catalyzes class switch recombination. J. Exp. Med. 202:733–738.
   PubMedGoogle Scholar
• Basu, U., J. Chaudhuri, R. T. Phan, A. Datta, and F. W. Alt. 2007. Regulation of activation induced deaminase via phosphorylation. Adv. Exp. Med. Biol. 596:129–137.
   PubMedGoogle Scholar
• Bransteitter, R., P. Pham, M. D. Scharff, and M. F. Goodman. 2003. Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl. Acad. Sci. USA 100:4102–4107.
   PubMed Web of Science ®Google Scholar
• Chaudhuri, J., and F. W. Alt. 2004. Class-switch recombination: interplay of transcription, DNA deamination, and DNA repair. Nat. Rev. Immunol. 4:541–552.
   PubMed Web of Science ®Google Scholar
• Daniels, G. A., and M. R. Lieber. 1995. RNA:DNA complex formation upon transcription of immunoglobulin switch regions: implications for the mechanism and regulation of class switch recombination. Nucleic Acids Res. 23:5006–5011.
   PubMed Web of Science ®Google Scholar
• Drolet, M., S. Broccoli, F. Rallu, C. Hraiky, C. Fortin, E. Masse, and I. Baaklini. 2003. The problem of hypernegative supercoiling and R-loop formation in transcription. Front. Biosci. 8:d210–221.
   PubMedGoogle Scholar
• Dunnick, W. A., G. Z. Hertz, L. Scappino, and C. Gritzmacher. 1993. DNA sequence at immunoglobulin switch region recombination sites. Nucleic Acids Res. 21:365–372.
   PubMed Web of Science ®Google Scholar
• Duquette, M. L., P. Handa, J. A. Vincent, A. F. Taylor, and N. Maizels. 2004. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev. 18:1618–1629.
   PubMed Web of Science ®Google Scholar
• Fan, J., Y. Matsumoto, and D. M. Wilson. 2006. Nucleotide sequence and DNA secondary structure, as well as replication protein A, modulate the single-stranded abasic endonuclease activity of APE1. J. Biol. Chem. 281:3889–3898.
   PubMedGoogle Scholar
• Gritzmacher, C. A. 1989. Molecular aspects of heavy-chain class switching. Crit. Rev. Immunol. 9:173–200.
   PubMed Web of Science ®Google Scholar
• Huang, F.-T., K. Yu, B. B. Balter, E. Selsing, Z. Oruc, A. A. Khamlichi, C.-L. Hsieh, and M. R. Lieber. 2007. Sequence dependence of chromosomal R-loops at the immunoglobulin heavy chain Smu class switch region. Mol. Cell. Biol. 27:5921–5932.
   PubMed Web of Science ®Google Scholar
• Huang, F.-T., K. Yu, C.-L. Hsieh, and M. R. Lieber. 2006. The downstream boundary of chromosomal R-loops at murine switch regions: implications for the mechanism of class switch recombination. Proc. Natl. Acad. Sci. USA 103:5030–5035.
   PubMed Web of Science ®Google Scholar
• Huertas, P., and A. Aguilera. 2003. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 12:711–721.
   PubMed Web of Science ®Google Scholar
• Ichikawa, H. T., M. P. Sowden, A. T. Torelli, J. Bachl, P. Huang, G. S. Dance, S. H. Marr, J. Robert, J. E. Wedekind, H. C. Smith, and A. Bottaro. 2006. Structural phylogenetic analysis of activation-induced deaminase function. J. Immunol. 177:355–361.
   PubMedGoogle Scholar
• Imai, K., G. Slupphaug, W. I. Lee, P. Revy, S. Nonoyama, N. Catalan, L. Yel, M. Forveille, B. Kavli, H. E. Krokan, H. D. Ochs, A. Fischer, and A. Durandy. 2003. Human uracil-DNA glycosylase deficiency associated with profoundly impaired immunoglobulin class-switch recombination. Nat. Immunol. 4:1023–1028.
   PubMedGoogle Scholar
• Kramer, P. R., and R. R. Sinden. 1997. Measurement of unrestrained negative supercoiling and topological domain size in living human cells. Biochemistry 36:3151–3158.
   PubMed Web of Science ®Google Scholar
• Lee, D. Y., and D. A. Clayton. 1996. Properties of a primer RNA-DNA hybrid at the mouse mitochondrial DNA leading-strand origin of replication. J. Biol. Chem. 271:24262–24269.
   PubMedGoogle Scholar
• Li, X., and J. L. Manley. 2005. Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122:365–378.
   PubMed Web of Science ®Google Scholar
• Masukata, H., and J. Tomizawa. 1990. A mechanism of formation of a persistent hybrid between elongating RNA and template DNA. Cell 62:331–338.
   PubMed Web of Science ®Google Scholar
• Min, I. M., L. R. Rothlein, C. E. Schrader, J. Stavnezer, and E. Selsing. 2005. Shifts in targeting of class switch recombination sites in mice that lack mu switch region tandem repeats or Msh2. J. Exp. Med. 201:1885–1890.
   PubMed Web of Science ®Google Scholar
• Min, I. M., C. E. Schrader, J. Vardo, T. M. Luby, N. D'Avirro, J. Stavnezer, and E. Selsing. 2003. The Smu tandem repeat region is critical for Ig isotype switching in the absence of Msh2. Immunity 19:515–524.
   PubMed Web of Science ®Google Scholar
• Min, I. M., and E. Selsing. 2005. Antibody class switch recombination: roles for switch sequences and mismatch repair proteins. Adv. Immunol. 87:297–328.
   PubMedGoogle Scholar
• Muramatsu, M., V. Sankaranand, S. Anant, M. Sugai, K. Kinoshita, N. Davidson, and T. Honjo. 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
• Petersen-Mahrt, S. K., R. S. Harris, and M. S. Neuberger. 2002. AID mutates Escherichia coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418:99–103.
   PubMed Web of Science ®Google Scholar
• Petrini, J., and W. Dunnick. 1989. Products and implied mechanism of H chain switch recombination. J. Immunol. 142:2932–2935.
   PubMedGoogle Scholar
• Rada, C., G. T. Williams, H. Nilsen, D. E. Barnes, T. Lindahl, and M. S. Neuberger. 2002. Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr. Biol. 12:1748–1755.
   PubMed Web of Science ®Google Scholar
• Reaban, M. E., and J. A. Griffin. 1990. Induction of RNA-stabilized DNA conformers by transcription of an immunoglobulin switch region. Nature 348:342–344.
   PubMed Web of Science ®Google Scholar
• Reaban, M. E., J. Lebowitz, and J. A. Griffin. 1994. Transcription induces the formation of a stable RNA:DNA hybrid in the immunoglobulin alpha switch region. J. Biol. Chem. 269:21850–21857.
   PubMed Web of Science ®Google Scholar
• Roberts, R. W., and D. M. Crothers. 1992. Stability and properties of double and triple helices: dramatic effects of RNA or DNA backbone composition. Science 258:1463–1466.
   PubMed Web of Science ®Google Scholar
• Ronai, D., M. D. Iglesias-Ussel, M. Fan, Z. Li, A. Martin, and M. D. Scharff. 2007. Detection of chromatin-associated single-stranded DNA in regions targeted for somatic hypermutation. J. Exp. Med. 204:181–190.
   PubMed Web of Science ®Google Scholar
• Saenger, W. 1984. Principles of nucleic acid structure. Springer-Verlag, New York, NY.
   Google Scholar
• Selsing, E. 2006. Ig class switching: targeting the recombinational mechanism. Curr. Opin. Immunol. 18:249–254.
   PubMed Web of Science ®Google Scholar
• Shinkura, R., M. Tian, C. Khuong, K. Chua, E. Pinaud, and F. W. Alt. 2003. The influence of transcriptional orientation on endogenous switch region function. Nat. Immunol. 4:435–441.
   PubMed Web of Science ®Google Scholar
• Stavnezer, J., and C. T. Amemiya. 2004. Evolution of isotype switching. Semin. Immunol. 16:257–275.
   PubMed Web of Science ®Google Scholar
• Stavnezer, J., and S. Sirlin. 1986. Specificity of immunoglobulin heavy chain switch correlates with activity of germline heavy chain genes prior to switching. EMBO J. 5:95–102.
   PubMedGoogle Scholar
• Szurek, P., J. Petrini, and W. Dunnick. 1985. Complete nucleotide sequence of the murine g3 switch region and analysis of switch recombination sites in two γ3-expressing hybridomas. J. Immunol. 135:620–626.
   PubMedGoogle Scholar
• Tian, M., and F. W. Alt. 2000. Transcription induced cleavage of immunoglobulin switch regions by nucleotide excision repair nucleases in vitro. J. Biol. Chem. 275:24163–24172.
   PubMed Web of Science ®Google Scholar
• Wakae, K., B. G. Magor, H. Saunders, H. Nagaoka, A. Kawamura, K. Kinoshita, T. Honjo, and M. Muramatsu. 2006. Evolution of class switch recombination function in fish activation-induced cytidine deaminase, AID. Int. Immunol. 18:41–47.
   PubMedGoogle Scholar
• Westover, K. D., D. A. Bushnell, and R. D. Kornberg. 2004. Structural basis of transcription: separation of RNA from DNA by RNA polymerase II. Science 303:1014–1016.
   PubMed Web of Science ®Google Scholar
• Xu, B., and D. A. Clayton. 1996. RNA-DNA hybrid formation at the human mitochondrial heavy-strand origin ceases at replication start sites: an implication for RNA-DNA hybrids serving at primers. EMBO J. 15:3135–3143.
   PubMed Web of Science ®Google Scholar
• Xu, L., B. Gorham, S. C. Li, A. Bottaro, F. W. Alt, and P. Rothman. 1993. Replacement of germ-line ε promoter by gene targeting alters control of immunoglobulin heavy chain class switching. Proc. Natl. Acad. Sci. USA 90:3705–3709.
   PubMed Web of Science ®Google Scholar
• Yu, K., F. Chedin, C.-L. Hsieh, T. E. Wilson, and M. R. Lieber. 2003. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol. 4:442–451.
   PubMed Web of Science ®Google Scholar
• Yu, K., F. T. Huang, and M. R. Lieber. 2004. DNA substrate length and surrounding sequence affect the activation induced deaminase activity at cytidine. J. Biol. Chem. 279:6496–6500.
   PubMed Web of Science ®Google Scholar
• Yu, K., and M. R. Lieber. 2003. Nucleic acid structures and enzymes in the immunoglobulin class switch recombination mechanism. DNA Repair 2:1163–1174.
   PubMed Web of Science ®Google Scholar
• Yu, K., D. Roy, M. Bayramyan, I. S. Haworth, and M. R. Lieber. 2005. Fine-structure analysis of activation-induced deaminase accessbility to class switch region R-loops. Mol. Cell. Biol. 25:1730–1736.
   PubMed Web of Science ®Google Scholar
• Zarrin, A. A., F. W. Alt, J. Chaudhuri, N. Stokes, D. Kaushal, L. DuPasquier, and M. Tian. 2004. An evolutionarily conserved target motif for immunoglobulin class-switch recombination. Nat. Immunol. 5:1275–1281.
   PubMed Web of Science ®Google Scholar