Position-dependent silencing of germline Vβ segments on TCRβ alleles containing preassembled VβDJβCβ1 genes

Journal of Immunology

Volumn 185, Issue 6, 2010, Pages 3564-3573

  Brady, Brenna L ^a,b   Oropallo, Michael A ^a   Yang Iott, Katherine S ^a,b   Serwold, Thomas ^c   Hochedlinger, Konrad ^d   Jaenisch, Rudolf ^e   Weissman, Irving L ^f   Bassing, Craig H ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^f STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR BETA CHAIN;

ACETYLATION; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; GENE EXPRESSION; GENE REARRANGEMENT; GENE SILENCING; GENETIC CORRELATION; GENETIC ORGANIZATION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; T LYMPHOCYTE; THYMOCYTE;

ALLELES; ANIMALS; CHROMATIN; GENE REARRANGEMENT, BETA-CHAIN T-CELL ANTIGEN RECEPTOR; GENE SILENCING; GENES, T-CELL RECEPTOR BETA; GERM-LINE MUTATION; HOMEODOMAIN PROTEINS; HYBRIDOMAS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOSUPPRESSION; MICE; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; TRANSCRIPTION, GENETIC;

EID: 78649825294     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903098     Document Type: Article

References (46)

1. von Boehmer, H. 2004. Selection of the T-cell repertoire: receptor-controlled checkpoints in T-cell development. Adv. Immunol. 84: 201-238.
2. Jackson, A. M., and M. S. Krangel. 2006. Turning T-cell receptor beta recombination on and off: more questions than answers. Immunol. Rev. 209: 129-141.
3. Glusman, G., L. Rowen, I. Lee, C. Boysen, J. C. Roach, A. F. Smit, K. Wang, B. F. Koop, and L. Hood. 2001. Comparative genomics of the human and mouse T cell receptor loci. Immunity 15: 337-349.
4. Khor, B., and B. P. Sleckman. 2005. Intra- and inter-allelic ordering of T cell receptor beta chain gene assembly. Eur. J. Immunol. 35: 964-970.
5. Skok, J. A., R. Gisler, M. Novatchkova, D. Farmer, W. de Laat, and M. Busslinger. 2007. Reversible contraction by looping of the Tcra and Tcrb loci in rearranging thymocytes. Nat. Immunol. 8: 378-387.
6. Tripathi, R., A. Jackson, and M. S. Krangel. 2002. A change in the structure of Vbeta chromatin associated with TCR beta allelic exclusion. J. Immunol. 168: 2316-2324.
7. Senoo, M., and Y. Shinkai. 1998. Regulation of Vbeta germline transcription in RAG-deficient mice by the CD3epsilon-mediated signals: implication of Vbeta transcriptional regulation in TCR beta allelic exclusion. Int. Immunol. 10: 553-560.
8. Jackson, A., H. D. Kondilis, B. Khor, B. P. Sleckman, and M. S. Krangel. 2005. Regulation of T cell receptor beta allelic exclusion at a level beyond accessibility. Nat. Immunol. 6: 189-197.
9. + thymocyte differentiation. J. Immunol. 160: 1256-1267.
10. Wang, L., M. Senoo, and S. Habu. 2002. Differential regulation between gene expression and histone H3 acetylation in the variable regions of the TCRbeta locus. Biochem. Biophys. Res. Commun. 298: 420-426.
11. Jackson, A. M., and M. S. Krangel. 2005. Allele-specific regulation of TCR beta variable gene segment chromatin structure. J. Immunol. 175: 5186-5191.
12. Serwold, T., K. Hochedlinger, M. A. Inlay, R. Jaenisch, and I. L. Weissman. 2007. Early TCR expression and aberrant T cell development in mice with endogenous prerearranged T cell receptor genes. J. Immunol. 179: 928-938.
13. Hochedlinger, K., and R. Jaenisch. 2002. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 415: 1035-1038.
14. Carpenter, A. C., K. S. Yang-Iott, L. H. Chao, B. Nuskey, S. Whitlow, F. W. Alt, and C. H. Bassing. 2009. Assembled DJ beta complexes influence TCR beta chain selection and peripheral V beta repertoire. J. Immunol. 182: 5586-5595.
15. Allman, D., A. Sambandam, S. Kim, J. P. Miller, A. Pagan, D. Well, A. Meraz, and A. Bhandoola. 2003. Thymopoiesis independent of common lymphoid progenitors. Nat. Immunol. 4: 168-174.
16. - thymocyte differentiation. J. Immunol. 152: 4783-4792.
17. Steinel, N. C., B. L. Brady, A. C. Carpenter, K. S. Yang-Iott, and C. H. Bassing. 2010. Posttranscriptional silencing of VbetaDJbetaCbeta genes contributes to TCRbeta allelic exclusion in mammalian lymphocytes. J. Immunol. 185: 1055-1062.
18. Sikes, M. L., A. Meade, R. Tripathi, M. S. Krangel, and E. M. Oltz. 2002. Regulation of V(D)J recombination: a dominant role for promoter positioning in gene segment accessibility. Proc. Natl. Acad. Sci. USA 99: 12309-12314.
19. Abarrategui, I., and M. S. Krangel. 2007. Noncoding transcription controls downstream promoters to regulate T-cell receptor alpha recombination. EMBO J. 26: 4380-4390.
20. Chakraborty, T., D. Chowdhury, A. Keyes, A. Jani, R. Subrahmanyam, I. Ivanova, and R. Sen. 2007. Repeat organization and epigenetic regulation of the DH-Cmu domain of the immunoglobulin heavy-chain gene locus. Mol. Cell 27: 842-850.
21. Bolland, D. J., A. L. Wood, R. Afshar, K. Featherstone, E. M. Oltz, and A. E. Corcoran. 2007. Antisense intergenic transcription precedes Igh D-to-J recombination and is controlled by the intronic enhancer Emu. Mol. Cell. Biol. 27: 5523-5533.
22. Bolland, D. J., A. L. Wood, C. M. Johnston, S. F. Bunting, G. Morgan, L. Chakalova, P. J. Fraser, and A. E. Corcoran. 2004. Antisense intergenic transcription in V(D)J recombination. Nat. Immunol. 5: 630-637.
23. Bird, A. 2002. DNA methylation patterns and epigenetic memory. Genes Dev. 16: 6-21.
24. Nakase, H., Y. Takahama, and Y. Akamatsu. 2003. Effect of CpG methylation on RAG1/RAG2 reactivity: implications of direct and indirect mechanisms for controlling V(D)J cleavage. EMBO Rep. 4: 774-780.
25. Mostoslavsky, R., N. Singh, A. Kirillov, R. Pelanda, H. Cedar, A. Chess, and Y. Bergman. 1998. Kappa chain monoallelic demethylation and the establishment of allelic exclusion. Genes Dev. 12: 1801-1811.
26. Osipovich, O., R. Milley, A. Meade, M. Tachibana, Y. Shinkai, M. S. Krangel, and E. M. Oltz. 2004. Targeted inhibition of V(D)J recombination by a histone methyltransferase. Nat. Immunol. 5: 309-316.
27. Hsieh, C. L., and M. R. Lieber. 1992. CpG methylated minichromosomes become inaccessible for V(D)J recombination after undergoing replication. EMBO J. 11: 315-325.
28. Grewal, S. I., and S. Jia. 2007. Heterochromatin revisited. Nat. Rev. Genet. 8: 35-46.
29. Davodeau, F., M. A. Peyrat, I. Houde, M. M. Hallet, G. De Libero, H. Vié, and M. Bonneville. 1993. Surface expression of two distinct functional antigen receptors on human gamma delta T cells. Science 260: 1800-1802.
30. Padovan, E., G. Casorati, P. Dellabona, S. Meyer, M. Brockhaus, and A. Lanzavecchia. 1993. Expression of two T cell receptor alpha chains: dual receptor T cells. Science 262: 422-424.
31. Balomenos, D., R. S. Balderas, K. P. Mulvany, J. Kaye, D. H. Kono, and A. N. Theofilopoulos. 1995. Incomplete T cell receptor V beta allelic exclusion and dual V beta-expressing cells. J. Immunol. 155: 3308-3312.
32. Shanbhag, N. M., I. U. Rafalska-Metcalf, C. Balane-Bolivar, S. M. Janicki, and R. A. Greenberg. 2010. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141: 970-981.
33. Hewitt, S. L., B. Yin, Y. Ji, J. Chaumeil, K. Marszalek, J. Tenthorey, G. Salvagiotto, N. Steinel, L. B. Ramsey, J. Ghysdael, et al. 2009. RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin loci. Nat. Immunol. 10: 655-664.
34. Senoo, M., L. Wang, D. Suzuki, N. Takeda, Y. Shinkai, and S. Habu. 2003. Increase of TCR V beta accessibility within E beta regulatory region influences its recombination frequency but not allelic exclusion. J. Immunol. 171: 829-835.
35. Mathieu, N., W. M. Hempel, S. Spicuglia, C. Verthuy, and P. Ferrier. 2000. Chromatin remodeling by the T cell receptor (TCR)-beta gene enhancer during early T cell development: implications for the control of TCR-beta locus recombination. J. Exp. Med. 192: 625-636.
36. Blackwood, E. M., and J. T. Kadonaga. 1998. Going the distance: a current view of enhancer action. Science 281: 60-63.
37. Sieh, P., and J. Chen. 2001. Distinct control of the frequency and allelic exclusion of the V beta gene rearrangement at the TCR beta locus. J. Immunol. 167: 2121-2129.
38. Oestreich, K. J., R. M. Cobb, S. Pierce, J. Chen, P. Ferrier, and E. M. Oltz. 2006. Regulation of TCRbeta gene assembly by a promoter/enhancer holocomplex. Immunity 24: 381-391.
39. Jia, J., M. Kondo, and Y. Zhuang. 2007. Germline transcription from T-cell receptor Vbeta gene is uncoupled from allelic exclusion. EMBO J. 26: 2387-2399.
40. Chen, F., L. Rowen, L. Hood, and E. V. Rothenberg. 2001. Differential transcriptional regulation of individual TCR V beta segments before gene rearrangement. J. Immunol. 166: 1771-1780.
41. Sakamoto, S., B. J. Mathieson, K. L. Komschlies, N. K. Bhat, and H. A. Young. 1989. The methylation state of the T cell antigen receptor beta chain gene in subpopulations of mouse thymocytes. Eur. J. Immunol. 19: 873-879.
42. + thymocytes with CD3 expression: evidence of T cell commitment in the thymus. Int. Immunol. 8: 1473-1481.
43. Whitehurst, C. E., M. S. Schlissel, and J. Chen. 2000. Deletion of germline promoter PD beta 1 from the TCR beta locus causes hypermethylation that impairs D beta 1 recombination by multiple mechanisms. Immunity 13: 703-714.
44. Chen, T., and E. Li. 2004. Structure and function of eukaryotic DNA methyltransferases. Curr. Top. Dev. Biol. 60: 55-89.
45. Hale, J. S., K. T. Ames, T. E. Boursalian, and P. J. Fink. 2010. Cutting edge: Rag deletion in peripheral T cells blocks TCR revision. J. Immunol. 184: 5964-5968.
46. Wing, K., and S. Sakaguchi. 2010. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 11: 7-13.