Duality of enhancer functioning mode revealed in a reduced TCRβ gene enhancer knockin mouse model

Journal of Immunology

Volumn 183, Issue 12, 2009, Pages 7939-7948

  Bonnet, Marie ^a,b,c   Huang, Fang ^a,b,c,d   Benoukraf, Touati ^a,b,c   Cabaud, Olivier ^a,b,c   Verthuy, Christophe ^a,b,c   Boucher, Anaelle ^a,b,c   Jaeger, Sébastien ^a,b,c   Ferrier, Pierre ^a,b,c   Spicuglia, Salvatore ^a,b,c  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b CNRS   (France)

^c INSERM   (France)

^d FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR BETA CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADAPTIVE IMMUNITY; ALLELE; ALLELIC EXCLUSION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CHROMATIN; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYONIC STEM CELL; ENHANCER REGION; GENE EXPRESSION; GENE REARRANGEMENT; GENE TARGETING; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; HOMOZYGOSITY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; THYMOCYTE; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; BIOSYNTHESIS; C57BL MOUSE; GENETICS; HYBRIDOMA; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; TRANSGENIC MOUSE;

ALLELES; ANIMALS; BINDING SITES; ENHANCER ELEMENTS, GENETIC; GENE KNOCK-IN TECHNIQUES; GENE REARRANGEMENT, BETA-CHAIN T-CELL ANTIGEN RECEPTOR; HYBRIDOMAS; IMMUNOGLOBULIN VARIABLE REGION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTES;

EID: 76249089777     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902179     Document Type: Article

References (60)

1. Szutorisz, H., N. Dillon, and L. Tora. 2005. The role of enhancers as centres for general transcription factor recruitment. Trends Biochem. Sci. 30: 593-599.
2. West, A. G., and P. Fraser. 2005. Remote control of gene transcription. Hum. Mol. Genet. 14 Spec No 1: R101-R111.
3. Merika, M., and D. Thanos. 2001. Enhanceosomes. Curr. Opin. Genet. Dev. 11: 205-208.
4. Fiering, S., E. Whitelaw, and D. I. Martin. 2000. To be or not to be active: the stochastic nature of enhancer action. BioEssays 22: 381-387. (Pubitemid 30213500)
5. Jung, D., and F. W. Alt. 2004. Unraveling V(D)J recombination; insights into gene regulation. Cell 116: 299-311.
6. Cobb, R. M., K. J. Oestreich, O. A. Osipovich, and E. M. Oltz. 2006. Accessibility control of V(D)J recombination. Adv. Immunol. 91: 45-109.
7. Spicuglia, S., D. M. Franchini, and P. Ferrier. 2006. Regulation of V(D)J recombination. Curr. Opin. Immunol. 18: 158-163.
8. Jackson, A. M., and M. S. Krangel. 2006. Turning T-cell receptor β recombination on and off: more questions than answers. Immunol. Rev. 209: 129-141.
9. Khor, B., and B. P. Sleckman. 2002. Allelic exclusion at the TCRβ locus. Curr. Opin. Immunol. 14: 230-234.
10. Michie, A. M., and J. C. Zuniga-Pflucker. 2002. Regulation of thymocyte differentiation: pre-TCR signals and β-selection. Semin. Immunol. 14: 311-323.
11. Krimpenfort, P., R. De Jong, Y. Uematsu, Z. Dembic, S. Ryser, H. von Boehmer, M. Steinmetz, and A. Berns. 1988. Transcription of T cell receptor β-chain genes is controlled by a downstream regulatory element. EMBO J. 7: 745-750.
12. McDougall, S., C. L. Peterson, and K. Calame. 1988. A transcription enhancer 3′ of Cβ2 in the T cell receptor β locus. Science 241: 205-208.
13. Bories, J. C., J. Demengeot, L. Davidson, and F. W. Alt. 1996. Gene-targeted deletion and replacement mutations of the T-cell receptor β-chain enhancer: the role of enhancer elements in controlling V(D)J recombinational accessibility. Proc. Natl. Acad. Sci. USA 93: 7871-7876.
14. Bouvier, G., F. Watrin, M. Naspetti, C. Verthuy, P. Naquet, and P. Ferrier. 1996. Deletion of the mouse T-cell receptor β gene enhancer blocks αβ T-cell development. Proc. Natl. Acad. Sci. USA 93: 7877-7881.
15. Leduc, I., W. M. Hempel, N. Mathieu, C. Verthuy, G. Bouvier, F. Watrin, and P. Ferrier. 2000. T cell development in TCRβ enhancer-deleted mice: implications for αβ T cell lineage commitment and differentiation. J. Immunol. 165: 1364-1373. (Pubitemid 30604567)
16. Mathieu, N., W. M. Hempel, S. Spicuglia, C. Verthuy, and P. Ferrier. 2000. Chromatin remodeling by the T cell receptor (TCR)-βgene enhancer during early T cell development: implications for the control of TCR-β locus recombination. J. Exp. Med. 192: 625-636.
17. Spicuglia, S., S. Kumar, J. H. Yeh, E. Vachez, L. Chasson, S. Gorbatch, J. Cautres, and P. Ferrier. 2002. Promoter activation by enhancer-dependent and -independent loading of activator and coactivator complexes. Mol. Cell 10: 1479-1487. (Pubitemid 36050887)
18. Ryu, C. J., B. B. Haines, D. D. Draganov, Y. H. Kang, C. E. Whitehurst, T. Schmidt, H. J. Hong, and J. Chen. 2003. The T cell receptor β enhancer promotes access and pairing of Dβ and Jβ gene segments during V(D)J recombination. Proc. Natl. Acad. Sci. USA 100: 13465-13470.
19. Oestreich, K. J., R. M. Cobb, S. Pierce, J. Chen, P. Ferrier, and E. M. Oltz. 2006. Regulation of TCRβ gene assembly by a promoter/enhancer holocomplex. Immunity 24: 381-391.
20. Busse, C. E., A. Krotkova, and K. Eichmann. 2005. The TCRβ enhancer is dispensable for the expression of rearranged TCRβ genes in thymic DN2/DN3 populations but not at later stages. J. Immunol. 175: 3067-3074.
21. Tripathi, R. K., N. Mathieu, S. Spicuglia, D. Payet, C. Verthuy, G. Bouvier, D. Depetris, M. G. Mattei, W. M. Hempel, and P. Ferrier. 2000. Definition of a T-cell receptor βgene core enhancer of V(D)J recombination by transgenic mapping. Mol. Cell. Biol. 20: 42-53.
22. Huang, F., O. Cabaud, C. Verthuy, A. O. Hueber, and P. Ferrier. 2003. αβT-cell development is not affected by inversion of TCRβ gene enhancer sequences: polar enhancement of gene expression regardless of enhancer orientation. Immunology 109: 510-514.
23. Shinkai, Y., G. Rathbun, K. P. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, K. Young, A. L. Stall, and F. W. Alt. 1992. RAG-2 deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68: 855-867.
24. Itohara, S., P. Mombaerts, J. Lafaille, J. Iacomini, A. Nelson, A. R. Clarkze, M. L. Hooper, A. Farr, and S. Tonegawa. 1993. T cell receptor δ gene mutant mice: independent generation of αβ T cells and programmed rearrangements of γδ TCR genes. Cell 72: 337-348.
25. Behlke, M. A., H. S. Chou, K. Huppi, and D. Y. Loh. 1986. Murine T-cell receptor mutants with deletion of β-chain variable region gene. Proc. Natl. Acad. Sci. USA 83: 767-771.
26. Gartner, F., F. W. Alt, R. Monroe, M. Chu, B. P. Sleckman, L. Davidson, and W. Swat. 1999. Immature thymocytes employ distinct signaling pathways for allelic exclusion versus differentiation and expansion. Immunity 10: 537-546. (Pubitemid 29262656)
27. Whitehurst, C. E., M. S. Schlissel, and J. Chen. 2000. Deletion of germline promoter PDβ1 from the TCRβlocus causes hypermethylation that impairs Dβ1 recombination by multiple mechanisms. Immunity 13: 703-714.
28. DuPont, J. M., J. Tost, H. Jammes, and I. G. Gut. 2004. De novo quantitative bisulfite sequencing using the pyrosequencing technology. Anal. Biochem. 333: 119-127.
29. Ren, B., F. Robert, J. J. Wyrick, O. Aparicio, E. G. Jennings, I. Simon, J. Zeitlinger, J. Schreiber, N. Hannett, E. Kanin, et al. 2000. Genome-wide location and function of DNA binding proteins. Science 290: 2306-2309.
30. Leiden, J. M. 1993. Transcriptional regulation of T cell receptor genes. Annu. Rev. Immunol. 11: 539-570.
31. Anderson, M. K. 2006. At the crossroads: diverse roles of early thymocyte transcriptional regulators. Immunol. Rev. 209: 191-211.
32. - (DN4) cells in the foetal thymus. Eur. J. Immunol. 37: 487-500.
33. Chang, H. H., M. Hemberg, M. Barahona, D. E. Ingber, and S. Huang. 2008. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453: 544-547.
34. Chen, F., L. Rowen, L. Hood, and E. V. Rothenberg. 2001. Differential transcriptional regulation of individual TCR Vβ segments before gene rearrangement. J. Immunol. 166: 1771-1780. (Pubitemid 32114662)
35. Wilson, A., C. Marechal, and H. R. MacDonald. 2001. Biased Vβ usage in immature thymocytes is independent of DJβ proximity and pTα pairing. J. Immunol. 166: 51-57. (Pubitemid 32038416)
36. Bendelac, A., P. B. Savage, and L. Teyton. 2007. The biology of NKT cells. Annu. Rev. Immunol. 25: 297-336.
37. Khor, B., and B. P. Sleckman. 2005. Intra- and inter-allelic ordering of T cell receptor β chain gene assembly. Eur. J. Immunol. 35: 964-970.
38. Almeida, A. R., J. A. Borghans, and A. A. Freitas. 2001. T cell homeostasis: thymus regeneration and peripheral T cell restoration in mice with a reduced fraction of competent precursors. J. Exp. Med. 194: 591-599.
39. Li, B., M. Carey, and J. L. Workman. 2007. The role of chromatin during transcription. Cell 128: 707-719.
40. Roberts, J. L., P. Lauzurica, and M. S. Krangel. 1997. Developmental regulation of VDJ recombination by the core fragment of the T cell receptor α enhancer. J. Exp. Med. 185: 131-140.
41. Bassing, C. H., R. E. Tillman, B. B. Woodman, D. Canty, R. J. Monroe, B. P. Sleckman, and F. W. Alt. 2003. T cell receptor (TCR) α/δ locus enhancer identity and position are critical for the assembly of TCR δ and αvariable region genes. Proc. Natl. Acad. Sci. USA 100: 2598-2603.
42. + thymocyte: implications for a new aspect in the regulation of TCRβ gene recombination. Int. Immunol. 13: 1405-1414.
43. Eyquem, S., C. Lagresle, M. Fasseu, F. Sigaux, and J. C. Bories. 2002. Disruption of the lineage restriction of TCRβ gene rearrangements. Eur. J. Immunol. 32: 3256-3266.
44. Inlay, M. A., T. Lin, H. H. Gao, and Y. Xu. 2006. Critical roles of the immunoglobulin intronic enhancers in maintaining the sequential rearrangement of IgH and Igk loci. J. Exp. Med. 203: 1721-1732.
45. Wallace, H., R. Ansell, J. Clark, and J. McWhir. 2000. Pre-selection of integration sites imparts repeatable transgene expression. Nucleic Acids Res. 28: 1455-1464. (Pubitemid 30142690)
46. Carvajal, I. M., and R. Sen. 2000. Functional analysis of the murine TCR β-chain gene enhancer. J. Immunol. 164: 6332-6339.
47. Agata, Y., N. Tamaki, S. Sakamoto, T. Ikawa, K. Masuda, H. Kawamoto, and C. Murre. 2007. Regulation of T cell receptor β gene rearrangements and allelic exclusion by the helix-loop-helix protein, E47. Immunity 27: 871-884. (Pubitemid 350251223)
48. Hebbar, P. B., and T. K. Archer. 2007. Chromatin-dependent cooperativity between site-specific transcription factors in vivo. J. Biol. Chem. 282: 8284-8291.
49. Wotton, D., J. Ghysdael, S. Wang, N. A. Speck, and M. J. Owen. 1994. Cooperative binding of Ets-1 and core binding factor to DNA. Mol. Cell. Biol. 14: 840-850.
50. Afshar, R., S. Pierce, D. J. Bolland, A. Corcoran, and E. M. Oltz. 2006. Regulation of IgH gene assembly: role of the intronic enhancer and 5′DQ52 region in targeting DHJH recombination. J. Immunol. 176: 2439-2447.
51. Collins, C., P. Azmi, M. Berru, X. Zhu, and M. J. Shulman. 2006. A weakened transcriptional enhancer yields variegated gene expression. PLoS ONE 1: e33.
52. Kaern, M., T. C. Elston, W. J. Blake, and J. J. Collins. 2005. Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6: 451-464.
53. Magor, B. G., D. A. Ross, L. Pilström, and G. W. Warr. 1999. Transcriptional enhancers and the evolution of the IgH locus. Immunol. Today 20: 13-17.
54. Heintzman, N. D., G. C. Hon, R. D. Hawkins, P. Kheradpour, A. Stark, L. F. Harp, Z. Ye, L. K. Lee, R. K. Stuart, C. W. Ching, et al. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
55. Schlimgen, R. J., K. L. Reddy, H. Singh, and M. S. Krangel. 2008. Initiation of allelic exclusion by stochastic interaction of Tcrb alleles with repressive nuclear compartments. Nat. Immunol. 9: 802-809.
56. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
57. Krangel, M. S. 2007. T cell development: better living through chromatin. Nat. Immunol. 7: 687-694.
58. Simpson, E., K. Takacs, and D. M. Altmann. 1994. Thymic repertoire selection by superantigens: presentation by human and mouse MHC molecules. Thymus 23: 1-13. (Pubitemid 24325695)
59. Carpenter, A. C., K. S. Yang-Iott, L. H. Chao, B. Nuskey, S. Whitlow, F. W. Alt, and C. H. Bassing. 2009. Assembled DJβ complexes influence TCRβ chain selection and peripheral Vβ repertoire. J. Immunol. 182: 5586-5595.
60. Mathieu, N., S. Spicuglia, S. Gorbatch, O. Cabaud, C. Fernex, C. Verthuy, W. M. Hempel, A. O. Hueber, and P. Ferrier. 2003. Assessing the role of the TCRβ gene enhancer in regulating coding joint formation during V(D)J recombination. J. Biol. Chem. 278: 18101-18109.