Noncoding RNA transcription targets AID to divergently transcribed loci in B cells

Nature

Volumn 514, Issue 7522, 2014, Pages 389-393

  Pefanis, Evangelos ^a,b   Wang, Jiguang ^a   Rothschild, Gerson ^a   Lim, Junghyun ^a   Chao, Jaime ^a   Rabadan, Raul ^a   Economides, Aris N ^b   Basu, Uttiya ^a  

^a Department of Microbiology and Immunology College of Physicians and Surgeons Columbia University ^*  (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; DOUBLE STRANDED DNA; SINGLE STRANDED DNA; TRANSCRIPTOME; UNTRANSLATED RNA; AICDA (ACTIVATION INDUCED CYTIDINE DEAMINASE); AICDA (ACTIVATION-INDUCED CYTIDINE DEAMINASE); COMPLEMENTARY RNA; CYTIDINE DEAMINASE; EXOSC3 PROTEIN, MOUSE; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; IMMUNOGLOBULIN HEAVY CHAIN; RNA BINDING PROTEIN;

ANTIBODY; ENZYME ACTIVITY; GENE EXPRESSION; GENOME; MAMMAL; RECOMBINATION; RNA;

ARTICLE; B LYMPHOCYTE; BACTERIAL ARTIFICIAL CHROMOSOME; DNA RNA HYBRIDIZATION; EXOSOME; GENE LOCUS; GENETIC CODE; MOUSE MODEL; NONHUMAN; NORTHERN BLOTTING; NUCLEAR LOCALIZATION SIGNAL; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; SOMATIC HYPERMUTATION; SOMATIC MUTATION; TRANSCRIPTION INITIATION SITE; ANIMAL; BASE PAIRING; BIOSYNTHESIS; CHEMISTRY; DOUBLE STRANDED DNA BREAK; ENZYME SPECIFICITY; FEMALE; GENE REARRANGEMENT; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; GENETICS; GENOME; GENOMIC INSTABILITY; MALE; METABOLISM; MOUSE; NUCLEIC ACID HYBRIDIZATION;

ANIMALS; B-LYMPHOCYTES; BASE PAIRING; CYTIDINE DEAMINASE; DNA BREAKS, DOUBLE-STRANDED; DNA, SINGLE-STRANDED; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; EXOSOMES; FEMALE; GENOME; GENOMIC INSTABILITY; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN HEAVY CHAINS; MALE; MICE; NUCLEIC ACID HYBRIDIZATION; RNA, ANTISENSE; RNA, UNTRANSLATED; RNA-BINDING PROTEINS; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; SUBSTRATE SPECIFICITY; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC; TRANSLOCATION, GENETIC;

EID: 84908162142     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13580     Document Type: Article

References (40)

1. Schneider, C. & Tollervey, D. Threading the barrel of the RNA exosome. Trends Biochem. Sci. 38, 485-493 (2013).
2. Alt, F. W., Zhang, Y., Meng, F. L., Guo, C. & Schwer, B. Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 152, 417-429 (2013).
3. Keim, C., Kazadi, D., Rothschild, G. & Basu, U. Regulation of AID, the B-cell genome mutator. Genes Dev. 27, 1-17 (2013).
4. Klein, I. A. et al. Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell 147, 95-106 (2011).
5. Chiarle, R. et al. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147, 107-119 (2011).
6. Storb, U. Why does somatic hypermutation by AID require transcription of its target genes? Adv. Immunol. 122, 253-277 (2014).
7. Pavri, R. et al. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell 143, 122-133 (2010).
8. Basu, U. et al. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell 144, 353-363 (2011).
9. Sun, J. et al. E3-ubiquitin ligase Nedd4 determines the fate of AID-associated RNA polymerase II in B cells. Genes Dev. 27, 1821-1833 (2013).
10. Andrulis, E. D. et al. The RNA processing exosome is linked to elongating RNA polymerase II in Drosophila. Nature 420, 837-841 (2002).
11. Richard, P. & Manley, J. L. Transcription termination by nuclear RNA polymerases. Genes Dev. 23, 1247-1269 (2009).
12. Economides, A. N. et al. Conditionals by inversion provide a universal method for the generation of conditional alleles. Proc. Natl Acad. Sci. USA 110, E3179-E3188 (2013).
13. Flynn, R. A., Almada, A. E., Zamudio, J. R. &Sharp, P. A. AntisenseRNA polymerase II divergent transcripts are P-TEFb dependent and substrates for the RNA exosome. Proc. Natl Acad. Sci. USA 108, 10460-10465 (2011).
14. Almada, A. E., Wu, X., Kriz, A. J., Burge, C. B. & Sharp, P. A. Promoter directionality is controlled by U1 snRNP and polyadenylation signals. Nature 499, 360-363 (2013).
15. Wu, X. & Sharp, P. A. Divergent transcription: a driving force for new gene origination? Cell 155, 990-996 (2013).
16. Preker, P. et al. RNA exosome depletion reveals transcription upstream of active human promoters. Science 322, 1851-1854 (2008).
17. Andersen, P. R. et al. The human cap-binding complex is functionally connected to the nuclear RNA exosome. Nature Struct. Mol. Biol. 20, 1367-1376 (2013).
18. Andersen, P. K., Jensen, T. H. & Lykke-Andersen, S. Making ends meet: coordination between RNA 39-end processing and transcription initiation. Wiley Interdiscip. Rev. RNA 4, 233-246 (2013).
19. Flynn, R. A. & Chang, H. Y. Active chromatin and noncoding RNAs: an intimate relationship. Curr. Opin. Genet. Dev. 22, 172-178 (2012).
20. Seila, A. C. et al. Divergent transcription from active promoters. Science 322, 1849-1851 (2008).
21. Allmang, C. et al. Functions of the exosome in rRNA, snoRNAand snRNAsynthesis. EMBO J. 18, 5399-5410 (1999).
22. Ntini, E. et al. Polyadenylation site-induced decay of upstreamtranscripts enforces promoter directionality. Nature Struct. Mol. Biol. 20, 923-928 (2013).
23. Liu, M. et al. Two levels of protection for the B cell genome during somatic hypermutation. Nature 451, 841-845 (2008).
24. Pasqualucci, L. et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nature Genet. 43, 830-837 (2011).
25. Lohr, J. G. et al. Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing. Proc. Natl Acad. Sci. USA 109, 3879-3884 (2012).
26. Rhee, H. S. & Pugh, B. F. Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483, 295-301 (2012).
27. Schulz, D. et al. Transcriptome surveillance by selective termination of noncoding RNA synthesis. Cell 155, 1075-1087 (2013).
28. Hakim, O. et al. DNA damage defines sites of recurrent chromosomal translocations in B lymphocytes. Nature 484, 69-74 (2012).
29. Castellano-Pozo, M. et al. R-loops are linked to histone H3 S10 phosphorylation and chromatin condensation. Mol. Cell 52, 583-590 (2013).
30. Ginno, P. A., Lott, P. L., Christensen, H. C., Korf, I. & Chedin, F. R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol. Cell 45, 814-825 (2012).
31. Zhang, Y., Buchholz, F., Muyrers, J. P. & Stewart, A. F. A new logic for DNA engineering using recombination in Escherichia coli. Nature Genet. 20, 123-128 (1998).
32. Frendewey, D. et al. The loss-of-allele assay for ES cell screening and mouse genotyping. Methods Enzymol. 476, 295-307 (2010).
33. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
34. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnol. 28, 511-515 (2010).
35. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
36. Jolly, C. J., Klix, N. & Neuberger, M. S. Rapid methods for the analysis of immunoglobulin gene hypermutation: application to transgenic and gene targeted mice. Nucleic Acids Res. 25, 1913-1919 (1997).
37. Oliveira, T. Y. et al. Translocation capture sequencing: a method for high throughput mapping of chromosomal rearrangements. J. Immunol. Methods 375, 176-181 (2012).
38. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
39. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
40. Ran, F. A. et al. Double nicking byRNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389 (2013).