Transcription factor Pax5 (BSAP) transactivates the RAG-mediated VH-to-DJH rearrangement of immunoglobulin genes

Nature Immunology

Volumn 7, Issue 6, 2006, Pages 616-624

  Zhang, Zhixin ^a,b,c,e   Espinoza, Celia R ^j   Yu, Zhihong ^a,b   Stephan, Robert ^a,b   He, Ti ^a,e   Williams, G Stuart ^j   Burrows, Peter D ^a,e,f   Hagman, James ⁱ   Feeney, Ann J ^j   Cooper, Max D ^a,b,d,e,g,h  

^a The University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d University of Alabama at Birmingham   (United States)

^e University of Alabama at Birmingham   (United States)

^f UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^g University of Alabama at Birmingham   (United States)

^h Howard Hughes Medical Institutes   (United States)

ⁱ NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^j SCRIPPS RESEARCH INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN HEAVY CHAIN; RAG1 PROTEIN; RAG2 PROTEIN; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR PAX5;

ARTICLE; B LYMPHOCYTE; BINDING SITE; CONTROLLED STUDY; GENE INTERACTION; GENE REARRANGEMENT; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; IMMUNOGLOBULIN GENE; IMMUNOGLOBULIN VARIABLE REGION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; THYMOCYTE; TRANSACTIVATION;

ANIMALS; B-CELL-SPECIFIC ACTIVATOR PROTEIN; BINDING SITES; CELL LINEAGE; DNA-BINDING PROTEINS; GENE REARRANGEMENT, B-LYMPHOCYTE, HEAVY CHAIN; GENES, IMMUNOGLOBULIN; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOGLOBULIN JOINING REGION; IMMUNOGLOBULIN VARIABLE REGION; MICE; MICE, MUTANT STRAINS; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPPING; TRANS-ACTIVATION (GENETICS);

EID: 33744462581     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1339     Document Type: Article

References (51)

1. Tonegawa, S. Somatic generation of antibody diversity. Nature 302, 575-581 (1983).
2. Rajewsky, K. Clonal selection and learning in the antibody system. Nature 381, 751-758 (1996).
3. Bassing, C.H., Swat, W. & Alt, F.W. The mechanism and regulation of chromosomal V(D)J recombination. Cell 109, S45-S55 (2002).
4. Schatz, D.G., Oettinger, M.A. & Baltimore, D. The V(D)J recombination activating gene, RAG-1. Cell 59, 1035-1048 (1989).
5. Oettinger, M.A., Schatz, D.G., Gorka, C. & Baltimore, D. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248, 1517-1523 (1990).
6. Lewis, S.M. The mechanism of V(D)J joining: Lessons from molecular, immunological, and comparative analyses. Adv. Immunol. 56, 27-150 (1994).
7. Gellert, M. V(D)J recombination: RAG proteins, repair factors, and regulation. Annu. Rev. Biochem. 71, 101-132 (2002).
8. Igarashi, H., Gregory, S.C., Yokota, T., Sakaguchi, N. & Kincade, P.W. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 17, 117-130 (2002).
9. Turka, L.A. et al. Thymocyte expression of RAG-1 and RAG-2: Termination by T cell receptor cross-linking. Science 253, 778-781 (1991).
10. Grawunder, U. et al. Down-regulation of RAG1 and RAG2 gene expression in preB cells after functional immunoglobulin heavy chain rearrangement. Immunity 3, 601-608 (1995).
11. Sleckman, B.P., Gorman, J.R. & Alt, F.W. Accessibility control of antigen-receptor variable-region gene assembly: Role of cis-acting elements. Annu. Rev. Immunol. 14, 459-481 (1996).
12. H gene segments. Cell 40, 271-281 (1985).
13. Blackwell, T.K. et al. Recombination between immunoglobulin variable region gene segments is enhanced by transcription. Nature 324, 585-589 (1986).
14. Schlissel, M.S. & Baltimore, D. Activation of immunoglobulin kappa gene rearrangement correlates with induction of germline κ gene transcription. Cell 58, 1001-1007 1989.
15. Stanhope-Baker, P., Hudson, K.M., Shaffer, A.L., Constantinescu, A. & Schlissel, M.S. Cell type-specific chromatin structure determines the targeting of V(D)J recombinase activity in vitro. Cell 85, 887-897 (1996).
16. Roth, D.B. & Roth, S.Y. Unequal access: Regulating V(D)J recombination through chromatin remodeling. Cell 103, 699-702 (2000).
17. Kwon, J., Imbalzano, A.N., Matthews, A. & Oettinger, M.A. Accessibility of nucleosomal DNA to V(D)J cleavage is modulated by RSS positioning and HMG1. Mol. Cell 2, 829-839 (1998).
18. Golding, A., Chandler, S., Ballestar, E., Wolffe, A.P. & Schlissel, M.S. Nucleosome structure completely inhibits in vitro cleavage by the V(D)J recombinase. EMBO J. 18, 3712-3723 (1999).
19. Kwon, J., Morshead, K.B., Guyon, J.R., Kingston, R.E. & Oettinger, M.A. Histone acetylation and hSWI/SNF remodeling act in concert to stimulate V(D)J cleavage of nucleosomal DNA. Mol. Cell 6, 1037-1048 (2000).
20. McMurry, M.T. & Krangel, M.S. A role for histone acetylation in the developmental regulation of V(D)J recombination. Science 287, 495-498 (2000).
21. Burrows, P., LeJeune, M. & Kearney, J.F. Evidence that murine pre-B cells synthesise μ heavy chains but no light chains. Nature 280, 838-840 (1979).
22. Kurosawa, Y. et al. Identification of D segments of immunoglobulin heavy-chain genes and their rearrangement in T lymphocytes. Nature 290, 565-570 (1981).
23. Lassoued, K. et al. Expression of surrogate light chain receptors is restricted to a late stage in pre-B cell differentiation. Cell 73, 73-86 (1993).
24. Karasuyama, H. et al. The expression of Vpre-B/λ5 surrogate light chain in early bone marrow precursor B cells of normal and B cell-deficient mutant mice. Cell 77, 133-143 (1994).
25. Schebesta, M., Heavey, B. & Busslinger, M. Transcriptional control of B-cell development. Curr. Opin. Immunol. 14, 216-223 (2002).
26. Bain, G. et al. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79, 885-892 (1994).
27. Zhuang, Y., Soriano, P. & Weintraub, H. The helix-loop-helix gene E2A is required for B cell formation. Cell 79, 875-884 (1994).
28. Lin, H. & Grosschedl, R. Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 376, 263-267 (1995).
29. Romanow, W.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 5, 343-353 (2000).
30. Ghosh, J.K., Romanow, W.J. & Murre, C. Induction of a diverse T cell receptor gamma/delta repertoire by the helix-loop-helix proteins E2A and HEB in nonlymphoid cells. J. Exp. Med. 193, 769-776 (2001).
31. Goebel, P. et al. 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. 194, 645-656 (2001).
32. Czerny, T., Schaffner, G. & Busslinger, M. DNA sequence recognition by Pax proteins: Bipartite structure of the paired domain and its binding site. Genes Dev. 7, 2048-2061 (1993).
33. Czerny, T. & Busslinger, M. DNA-binding and transactivation properties of Pax-6: Three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5). Mol. Cell. Biol. 15, 2858-2871 (1995).
34. Urbanek, P., Wang, Z.Q., Fetka, I., Wagner, E.F. & Busslinger, M. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 79, 901-912 (1994).
35. Hesslein, D.G. et al. Pax5 is required for recombination of transcribed, acetylated, 5′ IgH V gene segments. Genes Dev. 17, 37-42 (2003).
36. Roldan, E. et al. Locus 'decontraction' and centromeric recruitment contribute to allelic exclusion of the immunoglobulin heavy-chain gene. Nat. Immunol. 6, 31-41 (2005).
37. Fuxa, M. et al. Pax5 induces V-to-DJ rearrangements and locus contraction of the immunoglobulin heavy-chain gene. Genes Dev. 18, 411-422 (2004).
38. Hsu, L.Y., Liang, H.E., Johnson, K., Kang, C. & Schlissel, M.S. Pax5 activates immunoglobulin heavy chain V to DJ rearrangement in transgenic thymocytes. J. Exp. Med. 199, 825-830 (2004).
39. Sayegh, C., Jhunjhunwala, S., Riblet, R. & Murre, C. Visualization of looping involving the immunoglobulin heavy-chain locus in developing B cells. Genes Dev. 19, 322-327 (2005).
40. Wang, Y.H. et al. V(D)J recombinatorial repertoire diversification during intraclonal pro-B to B-cell differentiation. Blood 101, 1030-1037 (2003).
41. H gene replacement to the primary B cell repertoire. Immunity 19, 21-31 (2003).
42. Kitamura, D., Roes, J., Kuhn, R. & Rajewsky, K.A. B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350, 423-426 (1991).
43. Hiom, K. & Gellert, M. Assembly of a 12/23 paired signal complex: A critical control point in V(D)J recombination. Mol. Cell 1, 1011-1019 (1998).
44. H genes does not correlate with promoter strength nor enhancer-independence. Mol. Immunol. 37, 29-39 (2000).
45. Fitzsimmons, D. et al. Pax-5 (BSAP) recruits Ets proto-oncogene family proteins to form functional ternary complexes on a B cell-specific promoter. Genes Dev. 10, 2198-2211 (1996).
46. Garvie, C.W., Hagman, J. & Wolberger, C. Structural studies of Ets-1/ Pax5 complex formation on DNA. Mol. Cell 8, 1267-1276 (2001).
47. Eberhard, D., Jimenez, G., Heavey, B. & Busslinger, M. Transcriptional repression by Pax5 (BSAP) through interaction with corepressors of the Groucho family. EMBO J. 19, 2292-2303 (2000).
48. Eberhard, D. & Busslinger, M. The partial homeodomain of the transcription factor Pax-5 (BSAP) is an interaction motif for the retinoblastoma and TATA-binding proteins. Cancer Res. 59, 1716s-1724s (1999).
49. Emelyanov, A.V., Kovac, C.R., Sepulveda, M.A. & Birshtein, B.K. The interaction of Pax5 (BSAP) with Daxx can result in transcriptional activation in B cells. J. Biol. Chem. 277, 11156-11164 (2002).
50. Maier, H. et al. Requirements for selective recruitment of Ets proteins and activation of mb-1/Ig-α gene transcription by Pax-5 (BSAP). Nucleic Acids Res. 31, 5483-5489 (2003).
51. Lieber, M.R., Hesse, J.E., Mizuuchi, K. & Gellert, M. Lymphoid V(D)J recombination: Nucleotide insertion at signal joints as well as coding joints. Proc. Natl. Acad. Sci. USA 85, 8588-8592 (1988).