S-S Synapsis during Class Switch Recombination Is Promoted by Distantly Located Transcriptional Elements and Activation-Induced Deaminase

Immunity

Volumn 27, Issue 5, 2007, Pages 711-722

  Wuerffel, Robert ^a   Wang, Lili ^a   Grigera, Fernando ^a   Manis, John ^b   Selsing, Erik ^c   Perlot, Thomas ^b,d   Alt, Frederick W ^b   Cogne, Michel ^e   Pinaud, Eric ^e   Kenter, Amy L ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF VIENNA   (Austria)

^e UNIVERSITY OF LIMOGES   (France)

Author keywords

MOLIMMUNO

Indexed keywords

DEAMINASE; PROTEIN GLT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CHROMOSOME; CHROMOSOME PAIRING; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; ENZYME ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTOSOME;

ANIMALS; CELLS, CULTURED; CHROMOSOME PAIRING; CYTIDINE DEAMINASE; FLOW CYTOMETRY; GENES, IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN SWITCH REGION; LYMPHOCYTE ACTIVATION; MICE; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC;

EID: 36148940618     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2007.09.007     Document Type: Article

References (44)

1. Aten J.A., Stap J., Krawczyk P.M., van Oven C.H., Hoebe R.A., Essers J., and Kanaar R. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303 (2004) 92-95
2. Barreto V., Reina-San-Martin B., Ramiro A.R., McBride K.M., and Nussenzweig M.C. C-terminal deletion of AID uncouples class switch recombination from somatic hypermutation and gene conversion. Mol. Cell 12 (2003) 501-508
3. Bekker-Jensen S., Lukas C., Melander F., Bartek J., and Lukas J. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J. Cell Biol. 170 (2005) 201-211
4. Blanton J., Gaszner M., and Schedl P. Protein:protein interactions and the pairing of boundary elements in vivo. Genes Dev. 17 (2003) 664-675
5. Carter D., Chakalova L., Osborne C.S., Dai Y.F., and Fraser P. Long-range chromatin regulatory interactions in vivo. Nat. Genet. 32 (2002) 623-626
6. Casellas R., Nussenzweig A., Wuerffel R., Pelanda R., Reichlin A., Suh H., Qin X.F., Besmer E., Kenter A., Rajewsky K., and Nussenzweig M.C. Ku80 is required for immunoglobulin isotype switching. EMBO J. 17 (1998) 2404-2411
7. Catalan N., Selz F., Imai K., Revy P., Fischer A., and Durandy A. The block in immunoglobulin class switch recombination caused by activation-induced cytidine deaminase deficiency occurs prior to the generation of DNA double strand breaks in switch mu region. J. Immunol. 171 (2003) 2504-2509
8. Celeste A., Petersen S., Romanienko P.J., Fernandez-Capetillo O., Chen H.T., Sedelnikova O.A., Reina-San-Martin B., Coppola V., Meffre E., Difilippantonio M.J., et al. Genomic instability in mice lacking histone H2AX. Science 296 (2002) 922-927
9. Chevillard C., Ozaki J., Herring C.D., and Riblet R. A three-megabase yeast artificial chromosome contig spanning the C57BL mouse Igh locus. J. Immunol. 168 (2002) 5659-5666
10. Dekker J., Rippe K., Dekker M., and Kleckner N. Capturing chromosome conformation. Science 295 (2002) 1306-1311
11. Dudley D.D., Chaudhuri J., Bassing C.H., and Alt F.W. Mechanism and control of V(D)J recombination versus class switch recombination: similarities and differences. Adv. Immunol. 86 (2005) 43-112
12. Ernst P., and Smale S.T. Combinatorial regulation of transcription II: The immunoglobulin mu heavy chain gene. Immunity 2 (1995) 427-438
13. Garrett F.E., Emelyanov A.V., Sepulveda M.A., Flanagan P., Volpi S., Li F., Loukinov D., Eckhardt L.A., Lobanenkov V.V., and Birshtein B.K. Chromatin architecture near a potential 3′ end of the igh locus involves modular regulation of histone modifications during B-cell development and in vivo occupancy at CTCF sites. Mol. Cell. Biol. 25 (2005) 1511-1525
14. Horike S., Cai S., Miyano M., Cheng J.F., and Kohwi-Shigematsu T. Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat. Genet. 37 (2005) 31-40
15. Kenter A.L. Class switch recombination: an emerging mechanism. Curr. Top. Microbiol. Immunol. 290 (2005) 171-199
16. Kenter A.L., Wuerffel R., Dominguez C., Shanmugam A., and Zhang H. Mapping of a functional recombination motif that defines isotype specificity for μ→γ3 switch recombination implicates NF-κB p50 as the isotype specific switching factor. J. Exp. Med. 199 (2004) 617-627
17. Khamlichi A.A., Pinaud E., Decourt C., Chauveau C., and Cogne M. The 3′ IgH regulatory region: a complex structure in a search for a function. Adv. Immunol. 75 (2000) 317-345
18. Lisby M., Mortensen U.H., and Rothstein R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5 (2003) 572-577
19. Luby T.M., Schrader C.E., Stavnezer J., and Selsing E. The mu switch region tandem repeats are important, but not required, for antibody class switch recombination. J. Exp. Med. 193 (2001) 159-168
20. Ma L., Wortis H., and Kenter A.L. Two new isotype specific switching factors detected for Ig class switching. J. Immunol. 168 (2002) 2835-2846
21. Manis J.P., van der Stoep N., Tian M., Ferrini R., Davidson L., Bottaro A., and Alt F.W. Class switching in B cells lacking 3′ immunoglobulin heavy chain enhancers. J. Exp. Med. 188 (1998) 1421-1431
22. Manis J.P., Tian M., and Alt F.W. Mechanism and control of class-switch recombination. Trends Immunol. 23 (2002) 31-39
23. Mochan T.A., Venere M., DiTullio Jr. R.A., and Halazonetis T.D. 53BP1, an activator of ATM in response to DNA damage. DNA Repair (Amst.) 3 (2004) 945-952
24. Muramatsu M., Kinoshita K., Fagarasan S., Yamada S., Shinkai Y., and Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102 (2000) 553-563
25. Murrell A., Heeson S., and Reik W. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat. Genet. 36 (2004) 889-893
26. Perlot T., Alt F.W., Bassing C.H., Suh H., and Pinaud E. Elucidation of IgH intronic enhancer functions via germ-line deletion. Proc. Natl. Acad. Sci. USA 102 (2005) 14362-14367
27. Petersen S., Casellas R., Reina-San-Martin B., Chen H.T., Difilippantonio M.J., Wilson P.C., Hanitsch L., Celeste A., Muramatsu M., Pilch D.R., et al. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 414 (2001) 660-665
28. Pinaud E., Khamlichi A.A., Le Morvan C., Drouet M., Nalesso V., Le Bert M., and Cogne M. Localization of the 3′ IgH locus elements that effect long-distance regulation of class switch recombination. Immunity 15 (2001) 187-199
29. Reina-San-Martin B., Difilippantonio S., Hanitsch L., Masilamani R.F., Nussenzweig A., and Nussenzweig M.C. H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. J. Exp. Med. 197 (2003) 1767-1778
30. Reina-San-Martin B., Chen J., Nussenzweig A., and Nussenzweig M.C. Enhanced intra-switch region recombination during immunoglobulin class switch recombination in 53BP1(-/-) B cells. Eur. J. Immunol. 37 (2007) 235-239
31. Rogakou E.P., Boon C., Redon C., and Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146 (1999) 905-916
32. Rush J.S., Fugmann S.D., and Schatz D.G. Staggered AID-dependent DNA double strand breaks are the predominant DNA lesions targeted to S mu in Ig class switch recombination. Int. Immunol. 16 (2004) 549-557
33. Sakai E., Bottaro A., and Alt F.W. The Ig heavy chain intronic enhancer core region is necessary and sufficient to promote efficient class switch recombination. Int. Immunol. 11 (1999) 1709-1713
34. Schrader C.E., Linehan E.K., Mochegova S.N., Woodland R.T., and Stavnezer J. Inducible DNA breaks in Ig S regions are dependent on AID and UNG. J. Exp. Med. 202 (2005) 561-568
35. Shanmugam A., Shi M.-J., Yauch L., Stavnezer J., and Kenter A. Evidence for class specific factors in immunoglobulin isotype switching. J. Exp. Med. 191 (2000) 1365-1380
36. Smale S.T. The establishment and maintenance of lymphocyte identity through gene silencing. Nat. Immunol. 4 (2003) 607-615
37. Spilianakis C.G., and Flavell R.A. Long-range intrachromosomal interactions in the T helper type 2 cytokine locus. Nat. Immunol. 5 (2004) 1017-1027
38. Stavnezer J. Molecular processes that regulate class switching. Curr. Top. Microbiol. Immunol. 245 (2000) 127-168
39. Ta V.T., Nagaoka H., Catalan N., Durandy A., Fischer A., Imai K., Nonoyama S., Tashiro J., Ikegawa M., Ito S., et al. AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat. Immunol. 4 (2003) 843-848
40. Tolhuis B., Palstra R.J., Splinter E., Grosveld F., and de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 10 (2002) 1453-1465
41. Wang L., Whang N., Wuerffel R., and Kenter A.L. AID dependent histone acetylation is detected in immunoglobulin S regions. J. Exp. Med. 203 (2006) 215-226
42. Wuerffel R.A., Du J., Thompson R.J., and Kenter A.L. Ig Sgamma3 DNA-specifc double strand breaks are induced in mitogen-activated B cells and are implicated in switch recombination. J. Immunol. 159 (1997) 4139-4144
43. Zarrin A.A., Del Vecchio C., Tseng E., Gleason M., Zarin P., Tian M., and Alt F.W. Antibody class switching mediated by yeast rndonuclease-generated DNA breaks. Science 315 (2006) 377-381
44. Zhou J., Ashouian N., Delepine M., Matsuda F., Chevillard C., Riblet R., Schildkraut C.L., and Birshtein B.K. The origin of a developmentally regulated Igh replicon is located near the border of regulatory domains for Igh replication and expression. Proc. Natl. Acad. Sci. USA 99 (2002) 13693-13698