A role for nuclear NF-κB in B-cell-specific demethylation of the Igκ locus

Nature Genetics

Volumn 13, Issue 4, 1996, Pages 435-441

  Kirillov, Andrei ^a   Kistler, Barbara ^b   Mostoslavsky, Raul ^a   Cedar, Howard ^a   Wirth, Thomas ^b   Bergman, Yehudit ^a  

^a HEBREW UNIVERSITY   (Israel)

^b Zentrum fur Molec Biol Heidelberg   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN KAPPA CHAIN; TRANS ACTING FACTOR;

ARTICLE; B LYMPHOCYTE; CELL SPECIFICITY; CONTROLLED STUDY; DEMETHYLATION; ENHANCER REGION; GENE LOCUS; IMMUNOGLOBULIN GENE; PLASMACYTOMA; PRIORITY JOURNAL; TUMOR CELL LINE;

B-LYMPHOCYTES; BINDING SITES; CELL LINE; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REARRANGEMENT, BETA-CHAIN T-CELL ANTIGEN RECEPTOR; GENES, IMMUNOGLOBULIN; IMMUNOGLOBULIN KAPPA-CHAINS; IMMUNOGLOBULIN MU-CHAINS; METHYLATION; METHYLTRANSFERASES; NF-KAPPA B; NUCLEAR MATRIX; PROTO-ONCOGENE PROTEINS; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, MESSENGER; TRANSCRIPTION FACTOR RELB; TRANSCRIPTION FACTORS;

EID: 0030038608     PISSN: 10614036     EISSN: None     Source Type: Journal    
DOI: 10.1038/ng0895-435     Document Type: Article

References (52)

1. Kafri, T. et al. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germline. Genes Dev. 6, 705-714 (1992).
2. Brandeis, M. et al. Sp1 elements protect a CpG island from de novo methylation. Nature 371, 435-438 (1994).
3. Macleod, D., Chartton, J., Mullins, J. & Bird, A. Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev. 8, 2282-2292 (1994).
4. Paroush, Z., Keshet, I., Israeli, J. & Cedar, H. Dynamics of demethylation and activation of the α-actin gene in myoblasts. Cell 63, 1229 (1990).
5. Lichtenstein, M., Keini, G., Cedar, H. & Bergman, Y. B-cell-specific demethylation: A novel role for the intronic κ chain enhancer sequence. Cell 76, 913-923 (1994).
6. Chen, J. & Alt, F.W. Gene rearrangement and B-cell development. Curr. Opin. Immunol. 5, 194-200 (1993).
7. Storb, U. & Arp, B. Methylation patters of immunoglobulin genes in lymphoid cells: connection of expression and differentiation with undermethylation. Proc. Natl. Acad. Sci. USA 80, 6642-6646 (1983).
8. Mather, E.L. & Perry, R.P. Methylation status and DNasel sensitivity of immunoglobulin genes: changes associated with rearrangement. Proc. Natl. Acad. Sci. USA 78, 2072-2076 (1983).
9. Kelley, D.E., Pollok, B.A., Atchison, M.L. & Perry, R.P. The coupling between enhancer activity and hypomethylation of κ immunoglobulin genes is developmentally regulated. Mol. Cell. Biol. 8, 930-937 (1988).
10. Goodhardt, M., Cavelier, P., Doyen, N., Kallenbach, S., Babinet, C. & Rougeon, F. Methylation status of immunoglobulin κ gene segments correlates with their recombination potential. Eur. J. Immunol. 23, 1789-1795 (1993).
11. Engler, P. et al. A strain-specific modifier on mouse chromosome 4 controls the methylation of independent transgene loci. Cell 65, 1-20 (1991).
12. Hsieh, C-L. & Lieber, M.R. CpG methylated minichromosomes become inaccessible for V(D)J recombination after undergoing replication. EMBO J. 11, 315-325 (1992).
13. Engler, P., Weng, A. & Storb, U. Influence of CpG methylation and target spacing on V(D)J recombination in a transgenic substrate. Mol. Cell. Biol. 13, 571-577 (1993).
14. Atchison, M.L. & Perry, R.P. The role of kappa enhancer and its binding factor NF-kappa B in the developmental regulation of kappa gene transcription. Cell 48, 121-128 (1987).
15. Atchison, M.L. & Perry, R.P. Complementation between two cell lines lacking kappa enhancer activity: implications for the developmental control of immunoglobulin transcription. EMBO J. 7, 4213-4220 (1988).
16. Klehr, D., Maass, K. & Bode, J. Scaffold-attached regions from three human interferon β domains can be used to enhance the stable expression of genes under the control of various promoters. Biochemistry 30, 1264-1270 (1991).
17. Mirkovitch, J., Mirault, M.-E., & Laemmli, U.K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell 39, 223-232 (1984).
18. Dietz, A., Kay, V., Schlake, T.A., Landsmann, J. & Bode, J. Plant scaffold attached region detected close to a T-DNA integration site is active in mammalian cells. Nucl. Acids Res. 22, 2744-2751 (1994).
19. Cockerill, P.N., Yuen, M.-H., & Garrard, W.T. The enhancer of the immunoglobulin heavy chain locus is flanked by presumptive chromosomal loop anchorage elements. J. Biol. Chem. 262, 5394-5397 (1987).
20. Staudt, L.M. & Lenardo, M.J. Immunoglobulin gene transcription. Annu. Rev. Immunol. 9, 373-398 (1991).
21. Ernst, P. & Smale, S.T. Combinatorial regulation of transcription II: The immunoglobulin μ heavy chain gene. Immunity 2, 427-438 (1995).
22. Ben-Shushan, E., Pikarsky, E., Klar, A. & Bergman, Y. Extinction of Oct-3/4 gene expression in embryonal carcinoma x fibroblast somatic cell hybrids is accompanied by changes in the methylation status, chromatin structure, and transcriptional activity of the Oct-3/4 upstream region. Mol. Cell. Biol. 13, 891-901 (1993).
23. Lenardo, M., Pierce, J.W. & Baltimore, D. Protein binding sites in Ig gene enhancers determining transcriptional activity and inducibility. Science 236, 1573-1577 (1967).
24. Miyamoto, S. & Verma, I.M. REL/NF-κB/IκB story. Adv. Cancer Res. 66, 255-292 (1995).
25. Finco, T.M. & Baldwin, A.S. Mechanistic aspects of NF-κB regulation: The emerging rote of phosphorylation and proteolysis. Cell 3, 263-272 (1995).
26. Bergman, Y. Rice, D., Grosschedl, R. & Baltimore, D. Two regulatory elements for immunoglobulin κ light chain gene expression. Proc. Natl. Acad. Sci. USA 81, 7041-7045 (1984).
27. Scott, M.L, Fujita, T., Liou, H.-C., Nolan, G.P. & Baltimore, D. The p65 subunit of NF-κB regulates IκB by two distinct mechanisms. Genes Dev. 7, 1266-1276 (1993).
28. Sun, S.-C., Ganchi, P.A., Ballard, D.W. & Greene, W.C. NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway. Science 259, 1912-1915 (1993).
29. Baeuerle, P.A. & Baltimore, D. Activation of DNA binding activity in an apparently cytoplasmic precursor of the NF-κB transcription factor. Cell 53, 211-217 (1988).
30. Lembecher, T., Müller, U., & Wirth, T. Distinct NF-κB/Rel transcription factors are responsible for tissue-specific and inducible gene activation. Nature 365, 767-770 (1993).
31. Lembecher, T., Kistler, B. & Wirth, T. Two distinct mechanisms contribute to the constitutive activation of RelB in lymphoid cells. EMBO J. 13, 4060-4069 (1994).
32. Weih, F., Carrasco, D. & Bravo, R. Constitutive and inducible Rel/NF-kappa B activities in mouse thymus and spleen. Oncogene 9, 3289-3297 (1994).
33. Flyseck, R.-P. et al. RelB, a new Rel family transcription activator that can interact with p50 NF-κB. Mol. Cell. Biol. 12, 674-684 (1992).
34. Ruben, S.M. et al. Isolation of a rel-related human cDNA that potentially encodes the 65 kD subunit of NF-κB. Science 251, 1490 (1991).
35. Dobrzanski, P., Ryseck, R.-P. & Bravo, R. Differential interactions of Rel-NF-kappa B complexes with I kappa B alpha determine pools of constitutive and inducible NF-kappa B activity. EMBO J. 13, 4608-4616 (1994).
36. Demengeot, J., Oltz, E.M. & Alt, F.W. Promotion of V(D)J recombinational accessibility by the intronic Eκ element: role of the κB motif. Int. Immunol. 7, 1995-2003 (1995).
37. Israel, A. A role for phosphorylation and degradation in the control of NF-κB activity. Trends Genet 11, 203-205 (1995).
38. Thanos, D. & Maniatis, T. NF-κB: A lesson in family values. Cell 80, 529-532 (1995).
39. Verma, I.M., Stevenson, J.K., Schwarz, E.M., Van Antwerp, D. & Miyamoto, S. Rel/NF-κB/IκB family: intimate tales of association and dissociation. Genes Dev. 9, 2723-2735 (1995).
40. Laemmli, U.K., Kas, E., Poljak, L. & Adachi, Y. Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr. Opin. Genet. Dev. 2, 275-285 (1992).
41. Jenuwein, T.J., Forrester, W.C., Oiu, R.-G. & Grosschedl, R. The immunoglobulin μ enhancer core establishes local factor access in nuclear chromatin independent of transcriptional stimulation. Genes Dev. 7, 2016-2032 (1993).
42. Forrester, W.C., van Genderen, C., Jenuwein, T. & Grosschedl, R. Dependence of enhancer-mediated transcription of the immunoglobulin μ gene on nuclear matrix attachment regions. Science 265, 1221-1225 (1994).
43. Yeivin, A. & Razin, A. Gene methylation patterns and expression in DNA methylation. Molecular biology and biological significance. (eds Jost, J. P. & Saluz, H. P.) 524-568 (Birkhauser Verlag Basel, Switzerland, 1993).
44. Ferrier, P. et al. Separate elements control DJ and VDJ rearrangement in a transgenic recombination substrate. EMBO J. 9, 117-125 (1990).
45. Chen, J., Young, F., Bottaro, A., Stewart, V., Smith, R.K. & Alt, F.W. Mutations of the intronic IgH enhancer and its flanking sequences differentially affect accessibility of the JH locus. EMBO J. 12, 4635-4645 (1993).
46. Serwe, M. & Sablitzky, F.V. (D)J recombination in B cells is impaired but not blocked by targeted deletion of the immunoglobulin heavy chain intron enhancer. EMBO J. 12, 2321-2327 (1993).
47. Takeda, S., Zou, Y.-R., Bluethmann, H., Kitamura, D., Muller, U. & Rajewsky, K. Deletion of the immunoglobulin κ chain intron enhancer abolishes κ chain gene rearrangement in cis but not λ chain gene rearrangement in trans. EMBO J. 12, 2329-2336 (1993).
48. Fernex, C., Capone, M. & Ferrier, P. The V(D)J recombinational and transcriptional activities of the immunoglobulin heavy-chain intronic enhancer can be mediated through distinct protein-binding sites in a transgenic substrate. Mol. Cell. Biol. 15, 3217-3226 (1995).
49. Hiramatsu, R. et al. The 3′ enhancer region determines the B/T specificity and Pro-B/Pre-B specificity of immunoglobulin Vκ-Jκ joining. Cell 83, 1113-1123 (1995).
50. Oltz, E. et al. V(D)J recombinase-inducible B-cell line: role of transcriptional enhancer elements in directing V(D)J recombination. Mol. Cell. Biol. 13, 6223-6230 (1993).
51. Sompayrac, L.M. & Danna, K. J. Efficient injection of monkey cells with DNA of simian virus 40. Proc. Natl. Acad. Sci. USA 78, 7575-7578 (1981).
52. Wirth, T. & Baltimore, D. Nuclear factor NF-kappa B can interact functionally with its cognate binding site to provide lymphoid-specific promoter function. EMBO J. 7, 3109-3111 (1988).