In vivo occupancy of the κ light chain enhancers in primary pro- and pre-B cells: A model for κ locus activation

Immunity

Volumn 6, Issue 2, 1997, Pages 131-143

  Shaffer, A L ^a   Peng, Albert ^a   Schlissel, Mark S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN KAPPA CHAIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL LINE; DEVELOPMENT; GENE REARRANGEMENT; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

EID: 0030958199     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80420-3     Document Type: Article

References (71)

1. Atchison, M., and Perry, R. (1987). The Role of the κ enhancer and its binding factor NF-κB in the developmental regulation of κ gene transcription. Cell 48, 121-128.
2. Ausubel, F., Brent, R., Kingston, R., Moore, D., Seidman, J., Smith, J., and Struhl, K. (1987). Current Protocols in Molecular Biology (New York: John Wiley & Sons).
3. Baeuerle, P.A., and Baltimore, D. (1988). Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-κB transcription factor. Cell 53, 211-217.
4. Bain, G., Robanus-Maandag, E., te Riele, H., Izon, D., Amsen, D., Kruisbeek, A., Krop, I., Schlissel, M., Feeny, A.J., van Roon, M., van der Valk, M., Berns, A., and Murre, C. (1994). E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79, 885-892.
5. Beg, A.A., Sha, W.C., Bronson, R.T., Ghosh, S., and Baltimore, D. (1995). Embryonic lethality and liver degeneration in mice lacking the ReIA component of NFκB. Nature 376, 167-170.
6. Blasquez, V.C., Hale, M.H., Trevorrow, K.W., and Garrard, W.T. (1993). Immunoglobulin κ gene enhancers synergistically activate gene expression but independently determine chromatin structure. J. Biol. Chem. 267, 23888-23893.
7. Busslinger, M., and Urbanek, P. (1995). The role of BSAP (Pax-5) in B-cell development. Curr. Opin. Genet. Dev. 5, 595-601.
8. Chen, Y.Y., Wang, L.C., Huang, M.S., and Rosenberg, N. (1994). An active v-abl protein tyrosine kinase blocks immunoglobulin light-chain gene rearrangement. Genes Dev. 8, 688-697.
9. Cockerill, P.N., and Garrard, W.T. (1986). Chromosomal loop anchorage of the κ immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell 44, 273-282.
10. Costa, M.W., and Atchison, M.L. (1996). Identification of an Sp1-like element within the immunoglobulin κ 3′ enhancer necessary for maximal enhancer activity. Biochemistry 35, 8662-8669.
11. Desiderio, S. (1996). Lymphopoiesis: transcription factors controlling B-cell development. Curr. Biol. 5, 605-608.
12. Eisenbeis, C.F., Singh, H., and Storb, U. (1993). PU.1 is a component of a multiprotein complex which binds an essential site in the murine X2-4 enhancer. Mol. Cell. Biol. 13, 6452-6461.
13. Emorine, L., Kuehl, M., Weir, L., Leder, P., and Max, E.E. (1983). A conserved sequence on the immunoglobulin Jκ-Cκ intron: possible enhancer element. Nature 304, 447-449.
14. Fitzsimmons, D., Hodson, W., Wheat, W., Maira, S.-M., Bohdan, W., and Hagman, J. (1996). 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.
15. Fujita, T., Nolan, G.P., Ghosh, S., and Baltimore, D. (1992). Independent modes of transcriptional activation by the p50 and p65 subunits of NF-κB. Genes Dev. 6, 775-787.
16. Garrity, P.A., and Wold, B.J. (1992). Effects of different DNA polymerases in ligation-mediated PCR: enhanced genomic sequencing and in vivo footprinting. Proc. Natl. Acad. Sci. USA 89, 1021-1025.
17. Goodhardt, M., Babinet, C., Lutfalla, G., Kallenbach, S., Cavelier, P., and Rougeon, R. (1989). Immunoglobulin κ light chain gene promoter and enhancer are not responsible for B-cell restricted gene rearrangement. Nucl. Acids Res. 17, 7403-7415.
18. Gorman, J.R., van der Stoep, N., Monroe, R., Gogne, M., Davidson, L., and Alt, F.W. (1996). The Igκ 3′ enhancer influences the ratio of Igκ versus Igλ B lymphocytes. Immunity 5, 241-252.
19. Grilli, M., Chiu, J.J., and Lenardo, M.J. (1993). NF-κB and rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 743, 1-62.
20. Hiramatsu, R., Akagi, K., Matsuoka, M., Nakamura, H., Kingsbury, L., David, C., Hardy, R.R., Yamamura, K., and Sakano, H. (1995). The 3′ enhancer region determines the B/T specificity and pro-B/ pre-B specificity of immunoglobulin Vκ-Jκ joining. Cell 83, 1113-1123.
21. Hromas, R., Pauli, U., Marcuzzi, A., Lafrenz, D., Nick, H., Stein, J., Stein, G., and Van Ness, B. (1988). Inducible DNA-protein interactions of the murine κ immunoglobulin enhancer in intact cells: comparison with in vitro interactions. Nucl. Acids Res. 16, 953-967.
22. Klug, C.A., Gerety, S.J., Shah, P.C., Chen, Y.Y., Rice, N.R., Rosenberg, N., and Singh, H. (1994). The v-abl tyrosine kinase negatively regulates NF-κB/Rel factors and blocks κ gene transcription in pre-B lymphocytes. Genes Dev. 8, 678-687.
23. Kontgen, F., Grumont, R.J., Strasser, A., Metcalf, D., Li, R., Tarlinton, D., and Gerondakis, S. (1995). Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9, 1965-1977.
24. Krop, I., de Fougerolles, A.R., Hardy, R.R., Allison, M., Schlissel, M., and Fearon, D.T. (1996). Self-renewal of B-1 lymphocytes is dependent on CD19. Eur. J. Immunol. 26, 238-242.
25. Lenardo, M., Pierce, J.W., and Baltimore, D. (1987). Protein-binding sites in Ig gene enhancers determine transcriptional activity and inducibility. Science 236, 1573-1577.
26. Li, Y.-L., Hayakawa, K., and Hardy, R.R. (1993). The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 178, 951-960.
27. Liou, H.C., and Baltimore, D. (1993). Regulation of the NF-κB/rel transcription factor and IκB inhibitor system. Curr. Opin. Cell Biol. 5, 477-487.
28. Max, E.E., Maizel, J.V.J., and Leder, P. (1981). The nucleotide sequence of a 5.5 kilobase DNA segment containing the mouse κ immunoglobulin J and C region genes. J. Biol. Chem. 256, 5116-5120.
29. Meyer, K.B., and Ireland, J. (1994). Activation of the immunoglobulin κ 3′ enhancer in pre-B cells correlates with the suppression of a nuclear factor binding to a sequence flanking the active core. Nucl. Acids Res. 22, 1576-1582.
30. Meyer, K.B., and Neuberger, M.S. (1989). The immunoglobulin κ locus contains a second, stronger B-cell specific enhancer which is located downstream of the constant region. EMBO J. 8, 1959-1964.
31. Meyer, K.B., Sharpe, M.J., Surani, M.A., and Neuberger, M.S. (1990). The importance of the 3′-enhancer region in immunoglobulin κ gene expression. Nucl. Acids Res. 18, 5609-5615.
32. Mueller, P.R., and Wold, B. (1989). In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science 246, 780-786.
33. Nelson, K.J., Mather, E.L., and Perry, R.P. (1984). Lipopolysaccharide-induced transcription of the κ immunoglobulin locus occurs on both alleles and is independent of methylation status. Nucl. Acids Res. 4, 1911-1923.
34. Nelson, K., Kelley, D., and Perry, R. (1985). Inducible transcription of the unrearranged κ constant region locus is a common feature of pre-B cells and does not require DNA or protein synthesis. Proc. Natl. Acad. Sci. USA 82, 5305-5309.
35. Neurath, M.F., Strober, W., and Wakatsuki, Y. (1994). The murine Ig 3′ α enhancer is a target site with repressor function for the B cell lineage-specific transcription factor BSAP (NF-HB, Sα-BP). J. Immunol. 153, 730-742.
36. Neurath, M.F., Max, E.E., and Strober, W. (1995). Pax5 (BSAP) regulates the murine immunoglobulin 3′α enhancer by suppressing binding of NF-αP, a protein that controls heavy chain transcription. Proc. Natl. Acad. Sci. USA 92, 5336-5340.
37. Oltz, E.M., Alt, F.W., Lin, W.C., Taccioli, G., Desiderio, S., and Rathbun, G. (1993). A 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.
38. Parslow, T., and Granner, D. (1982). Chromatin changes accompany immunoglobulin κ gene activation: a potential control region within the gene. Nature 299, 449-451.
39. Picard, D., and Schaffner, W. (1986). A lymphocyte-specific enhancer in the mouse immunoglobulin κ gene. Nature 307, 80-82.
40. Pierce, J.W., Gifford, A.M., and Baltimore, D. (1991). Silencing of the expression of the immunoglobulin κ gene in non-B cells. Mol. Cell. Biol. 11, 1431-1437.
41. Pongubala, J.M.R., and Atchison, M.L (1995). Activating transcription factor 1 and cyclic AMP response element modulator can modulate the activity of the immunoglobulin κ 3′ enhancer. J. Biol. Chem. 270, 10304-10313.
42. Pongubala, J.M.R., Nagulapalli, S., Klemsz, M.J., McKercher, S.R., Maki, R.A., and Atchison, M.L. (1992). PU.1 recruits a second nuclear factor to a site important for immunoglobulin κ 3′ enhancer activity. Mol. Cell. Biol. 12, 368-378.
43. Queen, C., and Baltimore, D. (1983). Immunoglobulin gene transcription is activated by downstream sequence elements. Cell 33, 741-748.
44. Roque, M.C., Smith, P.A., and Blasquez, V.C. (1996). A developmentally modulated chromatin structure at the mouse immunoglobulin κ 3′ enhancer. Mol. Cell. Biol. 16, 3138-3155.
45. Schanke, J.T., Marcuzzi, A., Podzorski, R.P., and Van Ness, B. (1994). An AP1 binding site upstream of the κ immunoglobulin intron enhancer binds inducible factors and contributes to expression. Nucl. Acids Res. 22, 5425-5432.
46. Schatz, D.G., Oettinger, M.A., and Schlissel, M.S. (1992). V(D)J recombination: molecular biology and regulation. Annu. Rev. Immunol. 10, 359-383.
47. Schlissel, M., and Baltimore, D. (1989). Activation of immunoglobulin κ gene rearrangement correlates with induction of germline κ gene transcription. Cell 58, 1001-1007.
48. Schlissel, M.S., and Morrow, T. (1994). Immunoglobulin heavy-chain protein controls B cell development by regulating germline transcription and retargeting V(D)J recombination. J. Immunol. 153, 1645-1657.
49. Schrieber, E., Mattias, P., Muller, M.M., and Schaffner, W. (1989). Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small numer of cells. Nucl. Acids Res. 17, 6419.
50. Scott, E.W., Simon, M.C., Anastasi, J., and Singh, H. (1994). Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265, 1573-1577.
51. Sen, R., and Baltimore, D. (1986a). Inducibility of κ immunoglobulin enhancer-binding protein NF-κB by a posttranslational mechanism. Cell 47, 921-928.
52. Sen, R., and Baltimore, D. (1986b). Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46, 705-716.
53. Sha, W.C., Hsiou-Chi, L., Toumanen, E.I., and Baltimore, D. (1995). Targeted disruption of the p50 subunit of NF-κB leads to multifocal defects in immune responses. Cell 80, 321-330.
54. Shinkai, Y., Rathbun, G., Lam, K., Oltz, E., Stewart, V., Mendelsohn, M., Charron, J., Datta, M., Young, F., Stall, A.M., and Alt, F.W. (1992). RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68, 855-867.
55. Singh, M., and Birshtein, B.K. (1993). NF-HB (BSAP) is a repressor of the murine immunoglobulin heavy-chain 3′ α enhancer at early stages of B-cell differentiation. Mol. Cell. Biol. 13, 3611-3622.
56. Sleckman, B.P., Gorman, J.R., and Alt, F.W. (1996). Accessibility control of antigen-receptor variable-region gene assembly: role of cis-acting elements. Annu. Rev. Immunol. 14, 459-481.
57. Spanopoulou, E., Roman, C.A., Corcoran, L.M., Schlissel, M.S., Silver, D.P., Nemazee, D., Nussenzweig, M.C., Shinton, S.A., Hardy, R.R., and Baltimore, D. (1994). Functional immunoglobulin transgenes guide ordered B-cell differentiation in Rag-1-deficient mice. Genes Dev. 8, 1030-1042.
58. Spolski, R., Miescher, G., Erard, R., Risser, R., MacDonald, H.R., and Mak, T.W. (1988). Regulation of expression of T cell γ chain, L3T4 and Ly-2 messages in Abelson/Moloney virus-transformed T cell lines. Eur. J. Immunol. 18, 295-300.
59. Stanhope-Baker, P., Hudson, K.M., Shaffer, A.L., Constantinuescu, A., and Schlissel, M.S. (1996). Cell type-specific chromatin structure determines the targeting of V(D)J recombinase activity in vitro. Cell 85, 887-897.
60. Staudt, L.M., and Lenardo, M.J. (1991). Immunoglobulin gene transcription. Annu. Rev. Immunol. 9, 373-398.
61. Staudt, L.M., Clerc, R.G., Singh, H., LeBowitz, J.H., Sharp, P.A., and Baltimore, D. (1988). Cloning of a lymphoid-specific cDNA encoding a protein binding the regulatory octamer DNA motif. Science 241, 577-580.
62. Takeda, S., Zou, Y.-T., Bluethmann, H., Kitamura, D., Muller, U., and Rajewsky, K. (1993). Deletion of the immunoglobulin κ chain enhancer abolishes κ chain gene rearrangement in cis but not λ chain gene rearrangement in trans. EMBO J. 12, 2329-2336.
63. Urbanek, P., Wang, Z.-Q., Fetka, I., Wagner, E.F., and Busslinger, M. (1994). Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 79, 901-912.
64. Van Ness, B., Weigert, M., Coleclough, C., Mather, E., Kelley, D., and Perry, R. (1981). Transcription of the unrearranged mouse Cκ locus: sequence of the initiation region and comparison of activity with a rearranged Vκ-Cκ gene. Cell 27, 593-602.
65. Weih, F., Carrasco, D., Durham, S.K., Barton, D.S., Rizzo, C.A., Ryseck, R.-P., Lira, S.A., and Bravo, R. (1995). Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of ReIB, a member of the NFκB/Rel family. Cell 80, 331-340.
66. Xu, Y., Davidson, L., Alt, F.W., and Baltimore, D. (1996). Deletion of the Igκ light chain intronic enhancer/matrix attachment region impairs but does not abolish VκJκ rearrangement. Immunity 4, 377-385.
67. Young, F., Ardman, B., Shinkai, Y., Lansford, R., Blackwell, K., Mendelsohn, M., Rolink, A., Melchers, F., and Alt, F.W. (1994). Influence of immunoglobulin heavy-and light-chain expression on B-cell differentiation. Genes Dev. 8, 1043-1057.
68. Zhuang, Y., Soriano, P., and Weintraub, H. (1994). The helix-loop-helix gene E2A is required for B cell formation. Cell 79, 875-884.
69. Zou, Y.R., Takeda, S., and Rajewsky, K. (1993). Gene targeting in the Igκ locus: efficient generation of λ chain-expressing B cells, independent of gene rearrangements in Igκ. EMBO J. 12, 811-820.
70. Zuniga-Pflucker, J.C., Schwartz, H.L., and Lenardo, M.J. (1993). Gene transcription in differentiating immature T cell receptor(neg) thymocytes resembles antigen-activated mature T cells. J. Exp. Med. 178, 1139-1149.
71. Zwollo, P., and Desiderio, S. (1994). Specific recognition of the bIk promoter by the B-lymphoid transcription factor B-cell-specific activator protein. J. Biol. Chem. 269, 15310-15317.