Elucidation of IgH 3′ region regulatory role during class switch recombination via germline deletion

Nature Communications

Volumn 6, Issue , 2015, Pages

  Saintamand, Alexis ^a   Rouaud, Pauline ^a   Saad, Faten ^a   Rios, Géraldine ^b   Cogné, Michel ^a,c   Denizot, Yves ^a  

^a UNIVERSITÉ DE LIMOGES   (France)

^b CNRS   (France)

^c INSTITUT UNIVERSITAIRE DE FRANCE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; MICRORNA; RNA POLYMERASE II; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; RECOMBINANT PROTEIN;

GENE EXPRESSION; GENETIC VARIATION; MUTATION; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLASS SWITCH RECOMBINATION; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENHANCER REGION; GENE CONTROL; GENE DELETION; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; IMMUNOGLOBULIN HEAVY CHAIN GENE; MOUSE; NONHUMAN; RNA TRANSCRIPTION; SPLEEN CELL; ANIMAL; CYTOLOGY; FEMALE; GENETIC EPIGENESIS; GENETICS; IMMUNOGLOBULIN GENE; MALE; METABOLISM; MOLECULAR CLONING; PHYSIOLOGY; REGULATORY SEQUENCE; SPLEEN;

MUS;

ANIMALS; CLONING, MOLECULAR; EPIGENESIS, GENETIC; FEMALE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN SWITCH REGION; MALE; MICE; RECOMBINANT PROTEINS; REGULATORY SEQUENCES, NUCLEIC ACID; SPLEEN;

EID: 84929153200     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8084     Document Type: Article

References (51)

1. Henderson, A. & Calame, K. Transcription regulation during B cell development. Annu. Rev. Immunol. 16, 163-200 (1998).
2. Pinaud, E. et al. The IgH locus 3' regulatory region: pulling the strings from behind. Adv. Immunol. 110, 27-70 (2011).
3. Perlot, T., Alt, F. W., Bassing, C. H., Suh, H. & Pinaud, E. Elucidation of IgH intronic enhancer functions via germ-line deletion. Proc. Natl Acad. Sci. USA 42, 14362-14367 (2005).
4. Marquet, M. et al. The Em enhancer region influences H chain expression and B cell fate without impacting IgVH repertoire and immune response in vivo. J. Immunol. 193, 1171-1183 (2014).
5. Saintamand, A. et al. The IgH 3' regulatory region governs m chain transcription in mature B lymphocytes and the B cell fate. Oncotarget 6, 4845-4852 (2015).
6. Vincent-Fabert, C. et al. Genomic deletion of the whole IgH 3' regulatory region (hs3a, hs1,2, hs3b, hs4) dramatically affects class switch recombination and Ig secretion to all isotypes. Blood 116, 1895-1898 (2010).
7. Rouaud, P. et al. Elucidation of the enigmatic IgD class switch recombination via germ-line deletion of the IgH 3' regulatory region. J. Exp. Med. 211, 975-985 (2014).
8. Rouaud, P. et al. The IgH 3' regulatory region controls AID-induced somatic hypermutation in germinal centre B-cells in mice. J. Exp. Med. 210, 1501-1507 (2013).
9. Rouaud, P. et al. Enhancers located in heavy chain regulatory region (hs3a, hs1,2, hs3b and hs4) are dispensable for diversity of VDJ recombination. J. Biol. Chem. 287, 8356-8360 (2012).
10. Medvedovic, J. et al. Flexible long-range loops in the VH gene region of the Igh locus that likely facilitate the generation of a diverse antibody repertoire. Immunity 39, 229-244 (2013).
11. Yan, T. C. et al. IgH class switching and translocations used a robust nonclassical end-joining pathway. Nature 449, 478-483 (2007).
12. Stavnezer, J., Björkman, A., Du, L., Cagigi, A. & Pan-Hammarström, Q. Mapping of switch recombination junctions, a tool for studying DNA repair pathways during immunoglobulin class switching. Adv. Immunol. 108, 45-109 (2010).
13. Boboila, C., Alt, F. W. & Schwer, B. Classical and alternative end-joining pathways for repair of lymphocyte-specific and general DNA double-strand breaks. Adv. Immunol. 116, 1-45 (2012).
14. Matthews, A. J., Zheng, S., DiMenna, L. J. & Chaudhuri, J. Regulation of immunoglobulin class-switch recombination: choreography of noncoding transcription, targeted DNA deamination, and long-range DNA repair. Adv. Immunol. 122, 1-57 (2014).
15. Vaidyanathan, B., Yen, W. F., Pucella, J. N. & Chaudhuri, J. AIDing chromatin and transcription-coupled orchestration of immunoglobulin class-switch recombination. Front. Immunol. 5, 120 (2014).
16. Wuerffel, R. et al. S-S synapsis during class switch recombination is promoted by distantly located transcriptional elements and activation-induced deaminase. Immunity 27, 711-722 (2007).
17. Cogné, M. et al. A class switch control region at the 3' end of the immunoglobulin heavy chain locus. Cell 77, 737-747 (1994).
18. Pinaud, E. et al. Localization of the 3' IgH locus elements that effect longdistance regulation of class switch recombination. Immunity 15, 187-199 (2001).
19. Xu, M. & Stavnezer, J. Regulation of transcription of immunoglobulin germline γ1 RNA: analysis of the promoter/enhancer. EMBO J. 11, 145-155 (1992).
20. Boboila, C. et al. Alternative end-joining catalyses robust IgH locus deletions and tranlocations in the combined absence of ligase 4 and ku70. Proc. Natl Acad. Sci. USA 107, 3034-3039 (2010).
21. Laffleur, B. et al. AID-induced remodelling of immunoglobulin genes and B cell fate. Oncotarget 5, 1118-1131 (2014).
22. Zan, H. & Casali, P. AID- and UNG-dependent generation of staggered douvlestrand DNA breaks in immunoglobulin class switch DNA recombination: a post-cleavage role for AID. Mol. Immunol. 46, 45-61 (2008).
23. Kracker, S. et al. Impaired induction of DNA lesions during immunoglobulin class-switch recombination in humans influences end-joining repair. Proc. Natl Acad. Sci. USA 107, 22225-22230 (2010).
24. Kenter, A. L. AID targeting is dependent on RNA polymerase II pausing. Semin. Immunol. 24, 281-286 (2012).
25. Kuang, F. L., Luo, Z. & Scharff, M. D. H3 trimethyl K9 and H3 acetyl K9 chromatin modifications are associated with class switch recombination. Proc. Natl Acad. Sci. USA 106, 5288-5293 (2009).
26. Stanlie, A., Masatoshi, A., Muramatsu, M., Honjo, T. & Begum, N. A. Histone3 lysine4 trimethylation regulated by the facilitates chromatin transcription complex is critical for DNA cleavage in class switch recombination. Proc. Natl Acad. Sci. USA 107, 22190-22195 (2010).
27. Jeevan-Raj, B. P. et al. Epigenetic tethering of AID to the donor switch region during immunoglobulin class switch recombination. J. Exp. Med. 208, 1649-1660 (2011).
28. Daniel, J. A. & Nessenzweig, A. Roles for histone H3K4 methyltransferase activities during immunoglobulin class-switch recombination. Biochim. Biophys. Acta 1819, 733-738 (2012).
29. Bühler, M., Mohn, F., Stalder, L. & Mühlemann, O. Transcriptional silencing of nonsense codon-containing immunoglobulin minigenes. Mol. Cell. 18, 307-317 (2005).
30. Lu, Z. P., Ju, Z. L., Shi, G. Y., Zhang, J. W. & Sun, J. Histone deacetylase inhibitor trichostatin A reduces anti-DNA autoantibody production and represses IgH gene transcription. Biochem. Biophys. Res. Commun. 330, 204-209 (2005).
31. Kurosawa, K., Lin, W. & Ohta, K. Distinct roles of HDAC1 and HDAC2 in transcription and recombination at the immunoglobulin loci in the chivken B cell line DT40. J. Biochem. 148, 201-207 (2010).
32. Fritz, E. L. et al. A comprehensive analysis of the effects of the deaminase AID on the transcriptome and methylome of activated B cells. Nat. Immunol. 14, 749-755 (2013).
33. Yang, S. H. et al. The SOSS1 single-stranded DNA binding complex promotes DNA end resection in concert with Exo1. EMBO J. 32, 126-139 (2013).
34. Loizou, J. I. et al. ATMIN is required for maintenance of genomic stability and suppression of B cell lymphoma. Cancer Cell. 19, 587-600 (2011).
35. Bolderson, E. et al. Phosphorylation of Exo1 modulates homologous recombination repair of DNA double-strand breaks. Nucleic Acids Res. 38, 1821-1831 (2010).
36. Bennett, G., Papamichos-Chronakis, M. & Peterson, C. L. DNA repair choice defines a common pathway for recruitment of chromatin regulators. Nat. Commun 4, 2084 (2013).
37. Costelloe, T. et al. The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA and resection. Nature 489, 581-586 (2012).
38. Wu, P., Takai, H. & de Lange, T. Telomeric 3'overhangs derive from resection by Exo1 and Apollo and fill-in by POT1b-associated CST. Cell 150, 39-52 (2012).
39. Kotian, S., Liyanarachchi, S., Zelent, A. & Parvin, J. D. Histone deacetylases 9 and 10 are required for homologous recombination. J. Biol. Chem. 286, 7722-7726 (2011).
40. Yan, K. et al. Histone deacetylase 9 deficiency protects against effector T cell-mediated systemic autoimmunity. J. Biol. Chem. 286, 28833-28843 (2011).
41. Rulten, S. L. et al. PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell. 41, 33-45 (2011).
42. Sjögren, C. & Ström, L. S-phase and DNA damage activated establishment of sister chromatid cohesion-importance for DNA repair. Exp. Cell. Res. 316, 1445-1453 (2010).
43. Thomas-Claudepierre, A. S. et al. The cohesion complex regulates immunoglobulin class switch recombination. J. Exp. Med. 210, 2495-2502 (2013).
44. Truffinet, V. et al. The 3' IgH locus control region is sufficient to deregulate a c-myc transgene and promote mature B cell malignancies with a predominant Burkitt-like phenotype. J. Immunol. 179, 6033-6042 (2007).
45. Vincent-Fabert, C. et al. Ig synthesis and class switching do not require the presence of the hs4 enhancer in the 3' IgH regulatory region. J. Immunol. 182, 6926-6932 (2009).
46. Yu, K., Chedin, F., Hsieh, C. L., Wilson, T. E. & Lieber, M. R. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol. 4, 442-451 (2003).
47. Rouaud, P. et al. Mantle cell lymphoma-like lymphomas in c-myc-3'RR/p53+/- mice and c-myc-3'RR/Cdk4R24C mice: differential oncogenic mechanisms but similar cellular origin. Oncotarget 3, 586-593 (2012).
48. Le Brigand, K. & Barbry, P. MEDIANTE: a web-based microarray data manager. Bioinformatics 23, 1304-1306 (2007).
49. Le Brigand, K. et al. An open-access long oligonucleotide microarray resource for analysis of the human and mouse transcriptomes. Nucleic Acids Res. 34, e87 (2006).
50. Smyth, G. K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol 3, article 3 (2004).
51. Wang, X. & El Naqa, I. M. Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 24, 325-332 (2008).