IgH class switching exploits a general property of two DNA breaks to be joined in cis over long chromosomal distances

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 7, 2014, Pages 2644-2649

  Gostissa, Monica ^a,b,c   Schwer, Bjoern ^a,b,c   Chang, Amelia ^a,b,c   Dong, Junchao ^a,b,c   Meyers, Robin M ^a,b,c   Marecki, Gregory T ^a,b,c   Choi, Vivian W ^a,b,c,d   Chiarle, Roberto ^a,b,c,e   Zarrin, Ali A ^a,b,c,f   Alt, Frederick W ^a,b,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^e UNIVERSITY OF TURIN   (Italy)

^f GENENTECH INC   (United States)

Author keywords

Double strand break synapsis; Intrachromosomal joining; Topological domains

Indexed keywords

ENDONUCLEASE; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN M;

ANIMAL CELL; ANTIBODY CLASS SWITCH RECOMBINATION; ARTICLE; B LYMPHOCYTE ACTIVATION; CANCER GENETICS; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FIBROBLAST; GENE DELETION; GENE LOCUS; GENE SEQUENCE; GENETIC RECOMBINATION; IMMUNOGLOBULIN HEAVY CHAIN GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE C MYC; PRIORITY JOURNAL; T LYMPHOCYTE;

DOUBLE-STRAND BREAK SYNAPSIS; INTRACHROMOSOMAL JOINING; TOPOLOGICAL DOMAINS;

B-LYMPHOCYTES; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA BREAKS, DOUBLE-STRANDED; DNA PRIMERS; DNA REPAIR; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN HEAVY CHAINS; NEOPLASMS; POLYMERASE CHAIN REACTION; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84894302814     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1324176111     Document Type: Article

References (33)

1. Chaudhuri J, et al. (2007) Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv Immunol 94:157-214.
2. Boboila C, Alt FW, Schwer B (2012) Classical and alternative end-joining pathways for repair of lymphocyte-specific and general DNA double-strand breaks. Adv Immunol 116:1-49.
3. Cheng HL, et al. (2009) Integrity of the AID serine-38 phosphorylation site is critical for class switch recombination and somatic hypermutation in mice. Proc Natl Acad Sci USA 106(8):2717-2722.
4. Alt FW, Zhang Y, Meng FL, Guo C, Schwer B (2013) Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 152(3):417-429.
5. Zarrin AA, et al. (2007) Antibody class switching mediated by yeast endonucleasegenerated DNA breaks. Science 315(5810):377-381.
6. Manis JP, et al. (2004) 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat Immunol 5(5):481-487.
7. Ward IM, et al. (2004) 53BP1 is required for class switch recombination. J Cell Biol 165(4):459-464.
8. Reina-San-Martin B, Chen J, Nussenzweig A, Nussenzweig MC (2007) Enhanced intraswitch region recombination during immunoglobulin class switch recombination in 53BP1-/-B cells. Eur J Immunol 37(1):235-239.
9. Kenter AL, et al. (2012) Three-dimensional architecture of the IgH locus facilitates class switch recombination. Ann N Y Acad Sci 1267:86-94.
10. Dixon JR, et al. (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485(7398):376-380.
11. Lieberman-Aiden E, et al. (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326(5950):289-293.
12. Nagano T, et al. (2013) Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502(7469):59-64.
13. Zhang Y, et al. (2012) Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148(5):908-921.
14. Chen J, Lansford R, Stewart V, Young F, Alt FW (1993) RAG-2-deficient blastocyst complementation: An assay of gene function in lymphocyte development. Proc Natl Acad Sci USA 90(10):4528-4532.
15. Chiarle R, et al. (2011) Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147(1):107-119.
16. Cong L, et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819-823.
17. Ran FA, et al. (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8(11):2281-2308.
18. Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci USA 109(39):E2579-E2586.
19. Jinek M, et al. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096):816-821.
20. Mali P, et al. (2013) RNA-guided human genome engineering via Cas9. Science 339(6121):823-826.
21. Richardson C, Elliott B, Jasin M (1999) Chromosomal double-strand breaks introduced in mammalian cells by expression of I-Sce I endonuclease. Methods Mol Biol 113: 453-463.
22. Bassing CH, Alt FW (2004) H2AX may function as an anchor to hold broken chromosomal DNA ends in close proximity. Cell Cycle 3(2):149-153.
23. Dimitrova N, Chen Y-CM, Spector DL, de Lange T (2008) 53BP1 promotes nonhomologous end joining of telomeres by increasing chromatin mobility. Nature 456(7221):524-528.
24. Marshall WF, et al. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol 7(12):930-939.
25. Naumova N, et al. (2013) Organization of the mitotic chromosome. Science 342(6161): 948-953.
26. Nora EP, et al. (2012) Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485(7398):381-385.
27. Larmonie NS, et al. (2013) Breakpoint sites disclose the role of the V(D)J recombination machinery in the formation of T-cell receptor (TCR) and non-TCR associated aberrations in T-cell acute lymphoblastic leukemia. Haematologica 98(8): 1173-1184.
28. Onozawa M, Aplan PD (2012) Illegitimate V(D)J recombination involving nonantigen receptor loci in lymphoid malignancy. Genes Chromosomes Cancer 51(6):525-535.
29. Zhang J, et al. (2012) The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481(7380):157-163.
30. Beroukhim R, et al. (2010) The landscape of somatic copy-number alteration across human cancers. Nature 463(7283):899-905.
31. Solimini NL, et al. (2012) Recurrent hemizygous deletions in cancers may optimize proliferative potential. Science 337(6090):104-109.
32. Zarrin AA, Tian M, Wang J, Borjeson T, Alt FW (2005) Influence of switch region length on immunoglobulin class switch recombination. Proc Natl Acad Sci USA 102(7): 2466-2470.
33. Zarrin AA, et al. (2004) An evolutionarily conserved target motif for immunoglobulin class-switch recombination. Nat Immunol 5(12):1275-1281.