Epigenetic and 3-dimensional regulation of V(D)J rearrangement of immunoglobulin genes

Seminars in Immunology

Volumn 22, Issue 6, 2010, Pages 346-352

  Degner Leisso, Stephanie C ^a   Feeney, Ann J ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Epigenetics; Histone post translational modifications; Immunoglobulin genes; Locus contraction; Repertoire; V(D)J recombination

Indexed keywords

B LYMPHOCYTE RECEPTOR; HISTONE METHYLTRANSFERASE; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN LAMBDA CHAIN; PROTEIN H3K4ME2; PROTEIN H3K4ME3; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR E2A; UNCLASSIFIED DRUG;

B LYMPHOCYTE; CELL DIFFERENTIATION; EPIGENETICS; GENE REARRANGEMENT; GENETIC RECOMBINATION; HUMAN; PROMOTER REGION; PROTEIN MODIFICATION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; B-LYMPHOCYTES; ENHANCER ELEMENTS, GENETIC; EPIGENOMICS; GENE REARRANGEMENT, B-LYMPHOCYTE; GENES, IMMUNOGLOBULIN; HUMANS;

EID: 78249260638     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2010.08.002     Document Type: Review

References (52)

1. Yancopoulos G.D., Alt F.W. Regulation of the assembly and expression of variable-region genes. Ann Rev Immunol 1986, 4:339-368.
2. Alt F.W., Yancopoulos G.D., Blackwell T.K., Wood C., Thomas E., Boss M., et al. Ordered rearrangement of immunoglobulin heavy chain variable region segments. EMBO J 1984, 3:1209-1219.
3. Engel H., Rolink A., Weiss S. B cells are programmed to activate kappa and lambda for rearrangement at consecutive developmental stages. Eur J Immunol 1999, 29:2167-2176.
4. k gene. Cell 1981, 27:593-602.
5. H gene segments. Cell 1985, 40:271-281.
6. Abarrategui I., Krangel M.S. Regulation of T cell receptor-alpha gene recombination by transcription. Nat Immunol 2006, 7:1109-1115.
7. Xu C.R., Feeney A.J. The epigenetic profile of immunoglobulin genes is dynamically regulated during B cell differentiation and is modulated by pre-BCR signaling. J Immunol 2009, 182:1362-1369.
8. Morshead K.B., Ciccone D.N., Taverna S.D., Allis C.D., Oettinger M.A. Antigen receptor loci poised for V(D)J rearrangement are broadly associated with BRG1 and flanked by peaks of histone H3 dimethylated at lysine 4. Proc Natl Acad Sci U S A 2003, 100:11577-11582.
9. Liu Y., Subrahmanyam R., Chakraborty T., Sen R., Desiderio S. A plant homeodomain in RAG-2 that binds Hypermethylated lysine 4 of histone H3 is necessary for efficient antigen-receptor-gene rearrangement. Immunity 2007, 27:561-571.
10. Matthews A.G., Kuo A.J., Ramon-Maiques S., Han S., Champagne K.S., Ivanov D., et al. RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 2007, 450:1106-1110.
11. Ji Y., Resch W., Corbett E., Yamane A., Casellas R., Schatz D.G. The in vivo pattern of binding of RAG1 and RAG2 to antigen receptor loci. Cell 2010, 141:419-431.
12. Wood D.L., Coleclough C. Different joining region J elements of the murine k immunoglobulin light chain locus are used at markedly different frequencies. Proc Natl Acad Sci U S A 1984, 81:4756-4760.
13. Tiegs S.L., Russell D.M., Nemazee D. Receptor editing in self-reactive bone marrow B cells. J Exp Med 1993, 177:1009-1020.
14. Gay D., Saunders T., Camper S., Weigert M. Receptor editing: an approach by autoreactive B cells to escape tolerance. J Exp Med 1993, 177:999-1008.
15. Tze L.E., Schram B.R., Lam K.P., Hogquist K.A., Hippen K.L., Liu J., et al. Basal immunoglobulin signaling actively maintains developmental stage in immature B cells. PLoS Biol 2005, 3:e82.
16. Vela J.L., Ait-Azzouzene D., Duong B.H., Ota T., Nemazee D. Rearrangement of mouse immunoglobulin kappa deleting element recombining sequence promotes immune tolerance and lambda B cell production. Immunity 2008, 28:161-170.
17. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
18. Romanow W.J., Langerak A.W., Goebel P., Wolvers-Tettero I.L., van Dongen J.J., Feeney A.J., et al. E2A and EBF act in synergy with the V(D)J recombinase to generate a diverse immunoglobulin repertoire in nonlymphoid cells. Mol Cell 2000, 5:343-353.
19. Goebel P., Janney N., Valenzuela J.R., Romanow W.J., Murre C., Feeney A.J. Localized gene-specific induction of accessibility to V(D)J recombination induced by E2A and early B cell factor in nonlymphoid cells. J Exp Med 2001, 194:645-656.
20. Massari M.E., Grant P.A., Pray-Grant M.G., Berger S.L., Workman J.L., Murre C. A conserved motif present in a class of helix-loop-helix proteins activates transcription by direct recruitment of the SAGA complex. Mol Cell 1999, 4:63-73.
21. H genes does not correlate with promoter strength nor enhancer independence. Molecular Immunol 2000, 37:29-39.
22. Montalbano A., Ogwaro K.M., Tang A., Matthews A.G., Larijani M., Oettinger M.A., et al. V(D)J recombination frequencies can be profoundly affected by changes in the spacer sequence. J Immunol 2003, 171:5296-5304.
23. H genes in pro-B cells. J Immunol 2005, 175:6668-6675.
24. H genes. Mol Immunol 2007, 44:2675-2685.
25. Hesslein D.G., Pflugh D.L., Chowdhury D., Bothwell A.L., Sen R., Schatz D.G. Pax5 is required for recombination of transcribed, acetylated, 5' IgH V gene segments. Genes Dev 2003, 17:37-42.
26. Su I.H., Basavaraj A., Krutchinsky A.N., Hobert O., Ullrich A., Chait B.T., et al. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat Immunol 2003, 4:124-131.
27. Corcoran A.E., Riddell A., Krooshoop D., Venkitaraman A.R. Impaired immunoglobulin gene rearrangment in mice lacking the IL-7 receptor. Nature 1998, 391:904-907.
28. Liu H., Schmidt-Supprian M., Shi Y., Hobeika E., Barteneva N., Jumaa H., et al. Yin Yang 1 is a critical regulator of B-cell development. Genes Dev 2007, 21:1179-1189.
29. Roldan E., Fuxa M., Chong W., Martinez D., Novatchkova M., Busslinger M., et al. Locus 'decontraction' and centromeric recruitment contribute to allelic exclusion of the immunoglobulin heavy-chain gene. Nat Immunol 2005, 6:31-41.
30. Xu C.R., Schaffer L., Head S.R., Feeney A.J. Reciprocal patterns of methylation of H3K36 and H3K27 on proximal vs. distal IgVH genes are modulated by IL-7 and Pax5. Proc Natl Acad Sci U S A 2008, 105:8685-8690.
31. Zhang Z., Espinoza C.R., Yu Z., Stephan R., He T., Williams G.S., et al. Transcription factor Pax5 (BSAP) transactivates the RAG-mediated V(H)-to-DJ(H) rearrangement of immunoglobulin genes. Nat Immunol 2006, 7:616-624.
32. Chowdhury D., Sen R. Stepwise activation of the immunoglobulin mu heavy chain gene locus. EMBO J 2001, 20:6394-6403.
33. Skok J.A., Gisler R., Novatchkova M., Farmer D., de Laat W., Busslinger M. Reversible contraction by looping of the Tcra and Tcrb loci in rearranging thymocytes. Nat Immunol 2007, 8:378-387.
34. Jhunjhunwala S., van Zelm M.C., Peak M.M., Cutchin S., Riblet R., van Dongen J.J., et al. The 3D structure of the immunoglobulin heavy-chain locus: implications for long-range genomic interactions. Cell 2008, 133:265-279.
35. Bell A.C., West A.G., Felsenfeld G. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 1999, 98:387-396.
36. Gaszner M., Felsenfeld G. Insulators: exploiting transcriptional and epigenetic mechanisms. Nat Rev 2006, 7:703-713.
37. Phillips J.E., Corces V.G. CTCF: master weaver of the genome. Cell 2009, 137:1194-1211.
38. Degner S.C., Wong T.P., Jankevicius G., Feeney A.J. Cutting edge: developmental stage-specific recruitment of cohesin to CTCF sites throughout immunoglobulin loci during B lymphocyte development. J Immunol 2009, 182:44-48.
39. Parelho V., Hadjur S., Spivakov M., Leleu M., Sauer S., Gregson H.C., et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008, 132:422-433.
40. Wendt K.S., Yoshida K., Itoh T., Bando M., Koch B., Schirghuber E., et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 2008, 451:796-801.
41. Rubio E.D., Reiss D.J., Welcsh P.L., Disteche C.M., Filippova G.N., Baliga N.S., et al. CTCF physically links cohesin to chromatin. Proc Natl Acad Sci U S A 2008, 105:8309-8314.
42. Garrett F.E., Emelyanov A.V., Sepulveda M.A., Flanagan P., Volpi S., Li F., et al. 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 2005, 25:1511-1525.
43. Bates J.G., Cado D., Nolla H., Schlissel M.S. Chromosomal position of a VH gene segment determines its activation and inactivation as a substrate for V(D)J recombination. J Exp Med 2007, 204:3247-3256.
44. Featherstone K., Wood A.L., Bowen A.J., Corcoran A.E. The mouse immunoglobulin heavy chain V-D intergenic sequence contains insulators that may regulate ordered V(D)J recombination. J Biol Chem 2010, 285:9327-9338.
45. Liu Z., Widlak P., Zou Y., Xiao F., Oh M., Li S., et al. A recombination silencer that specifies heterochromatin positioning and ikaros association in the immunoglobulin kappa locus. Immunity 2006, 24:405-415.
46. Hawwari A., Krangel M.S. Regulation of TCR delta and alpha repertoires by local and long-distance control of variable gene segment chromatin structure. J Exp Med 2005, 202:467-472.
47. Heath H., Ribeiro de Almeida C., Sleutels F., Dingjan G., van de Nobelen S., Jonkers I., et al. CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J 2008, 27:2839-2850.
48. Defossez P.A., Kelly K.F., Filion G.J., Perez-Torrado R., Magdinier F., Menoni H., et al. The human enhancer blocker CTC-binding factor interacts with the transcription factor Kaiso. J Biol Chem 2005, 280:43017-43023.
49. Ishihara K., Oshimura M., Nakao M. CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell 2006, 23:733-742.
50. Chernukhin I., Shamsuddin S., Kang S.Y., Bergstrom R., Kwon Y.W., Yu W., et al. CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide. Mol Cell Biol 2007, 27:1631-1648.
51. Donohoe M.E., Zhang L.F., Xu N., Shi Y., Lee J.T. Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Mol Cell 2007, 25:43-56.
52. Weth O., Weth C., Bartkuhn M., Leers J., Uhle F., Renkawitz R. Modular insulators: genome wide search for composite CTCF/thyroid hormone receptor binding sites. PLoS One 2010, 5:e10119.