Protein acetylation regulates both PU.1 transactivation and Igκ 3′ enhancer activity

Journal of Immunology

Volumn 175, Issue 8, 2005, Pages 5160-5169

  Bai, Yuchen ^a,b   Srinivasan, Lakshmi ^a   Perkins, Leslie ^a   Atchison, Michael L ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^b WYETH AYERST RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE H3; IMMUNOGLOBULIN KAPPA CHAIN; LYSINE; PROTEIN P300; TRANSCRIPTION FACTOR PU 1; TRICHOSTATIN A;

ACETYLATION; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CHROMATIN STRUCTURE; CONTROLLED STUDY; ENHANCER REGION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEMATOPOIESIS; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PLASMA CELL; PLASMACYTOMA; POLYMERASE CHAIN REACTION; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DNA BINDING; TRANSACTIVATION;

EID: 26844546178     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.8.5160     Document Type: Article

References (56)

1. Hardy, R. R., and K. Hayakawa. 2001. B cell developmental pathways. Annu. Rev. Immunol. 19: 595-621.
2. Krangel, M. S. 2003. Gene segment selection in V(D)J recombination: accessibility and beyond. Nat. Immunol. 4: 624-630.
3. Liu, X., A. Prabhu, and B. Van Ness. 1999. Developmental regulation of the κ locus involves both positive and negative sequence elements in the 3′ enhancer that affect synergy with the intron enhancer. J. Biol. Chem. 274: 3285-3293.
4. Pongubala, J. M. R., and M. L. Atchison. 1991. Functional characterization of the developmentally controlled immunoglobulin κ 3′ enhancer: regulation by Id, a repressor of helix-loop-helix transcription factors. Mol. Cell. Biol. 11: 1040-1047.
5. Klug, C. A., S. J. Gerety, P. C. Shah, Y. Y. Chen, N. R. Rice, N. Rosenberg, and H. Singh. 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.
6. Meyer, K. B., Y. M. Teh, and M. S. Neuberger. 1996. The IgK 3′-enhancer triggers gene expression in early B lymphocytes but its activity is enhanced on B cell activation. Int. Immunol. 8: 1561-1568.
7. Inlay, M., F. W. Alt, D. Baltimore, and Y. Xu. 2002. Essential roles of the κ light chain intronic enhancer and 3′ enhancer in κ rearrangement and methylation. Nat. Immunol. 3: 463-468.
8. Mather, E. L., and R. P. Perry. 1983. Methylation status and DNase I sensitivity of immunoglobulin genes: changes associated with rearrangement. Proc. Natl. Acad. Sci. USA 80: 4689-4693.
9. Parslow, T. G., and D. K. Granner. 1982. Chromatin changes accompany immunoglobulin κ gene activation: a potential control region within the gene. Nature 299: 449-451.
10. Roque, M. C., P. A. Smith, and V. C. Blazquez. 1996. A developmentally modulated chromatin structure at the mouse immunoglobulin κ 3′ enhancer. Mol. Cell. Biol. 16: 3138-3155.
11. Rose, S. M., and W. T. Garrard. 1984. Differentiation-dependent chromatin alterations precede and accompany transcription of immunoglobulin light chain genes. J. Biol. Chem. 259: 8534-8544.
12. Storb, U., and B. Arp. 1983. Methylation patterns of immunoglobulin genes in lymphoid cells: correlation of expression and differentiation with methylation. Proc. Natl. Acad. Sci. USA 80: 6642-6646.
13. Xu, M., M. B. Barnard, S. M. Rose, P. N. Cockerill, S. Huang, and W. T. Garrard. 1986. Transcription termination and chromatin structure of active immunoglobulin κ gene locus. J. Biol. Chem. 261: 3838-3845.
14. Shaffer, A. L., A. Peng, and M. S. Schlissel. 1997. In vivo occupancy of the κ light chain enhancers in primary pro- and pre-B cells: a model for κ locus activation. Immunity 6: 131-143.
15. Pongubala, J. M. R., S. Nagulapalli, M. J. Klemsz, S. R. McKercher, R. A. Maki, and M. L. Atchison. 1992. PU.1 recruits a second nuclear factor to a site important for immunoglobulin κ 3′ enhancer activity. Mol. Cell. Biol. 12: 368-378.
16. Pongubala, J. M. R., C. Van Beveren, S. Nagulapalli, M. J. Klemsz, S. R. McKercher, R. A. Maki, and M. L. Atchison. 1993. Effect of PU.1 phosphorylation on interaction with NF-EM5 and transcriptional activation. Science 259: 1622-1625.
17. Eisenbeis, C. F., H. Singh, and U. Storb. 1993. PU.1 is a component of a multiprotein complex which binds an essential site in the murine immunoglobulin λ2-4 enhancer. Mol. Cell. Biol. 13: 6452-6461.
18. Eisenbeis, C. F., H. Singh, and U. Storb. 1995. Pip, a novel IRF family member, is a lymphoid-specific PU.1-dependent transcriptional activator. Genes Dev. 9: 1377-1387.
19. Voso, M. T., T. C. Burn, G. Wulf, B. Lim, G. Leone, and D. G. Tenen. 1994. Inhibition of hematopoiesis by competitive binding of transcription factor PU.1. Proc. Natl. Acad. Sci. USA 91: 7932-7936.
20. Scott, E. W., R. C. Fisher, M. C. Olson, E. W. Kehrli, M. C. Simon, and H. Singh. 1997. PU.1 functions in a cel-autonomous manner to control the differentiation of multipotential lymphoid-myeloid progenitors. Immunity 6: 437-447.
21. Olson, M. C., E. W. Scott, A. A. Hack, G. H. Su, Tenen, D. G. H. Singh, and M. C. Simon. 1995. PU.1 is not essential for early myeloid gene expression but is required for terminal myeloid differentiation. Immunity 3: 703-714.
22. Celada, A., F. E. Borras, C. Soler, J. Lloberas, M. Klemsz, C. van Beveren, S. McKercher, and R. A. Maki. 1996. The transcription factor PU.1 is involved in macrophage proliferation. J. Exp. Med. 184: 61-69.
23. DeKoter, R. P., and H. Singh. 2000. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 288: 1439-1441.
24. DeKoter, R. P., J. C. Walsh, and H. Singh. 1998. PU.1 regulates both cytokine-dependent proliferation and differentiation of granulocyte/macrophage progenitors. EMBO J. 17: 4456-4468.
25. Nerlov, C., and T. Graf. 1998. PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev. 12: 2403-2412.
26. Schuetze, S., R. Paul, B. C. Gliniak, and D. Kabat. 1992. Role of the PU.1 transcription factor in controlling differentiation of Friend erythroleukemia cells. Mol. Cell. Biol. 12: 2967-2975.
27. Scott, E. W., M. C. Simon, J. Anastasi, and H. Singh. 1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265: 1573-1577.
28. McKercher, S. R., B. E. Torbett, K. L. Anderson, G. W. Henkel, D. J. Vestal, H. Baribault, M. Klemsz, A. J. Feeney, G. E. Wu, C. J. Paige, et al. 1996. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 15: 5647-5658.
29. Rekhtman, N., F. Radparvar, T. Evans, and A. I. Skoultchi. 1999. Direct interaction of hematopoietic transcription factors PU.1 and GATA-1: functional antagonism in erythroid cells. Genes Dev. 13: 1398-1411.
30. Zhang, P., G. Behre, J. Pan, A. Iwama, N. Wara-Aswapati, H. S. Radomska, P. E. Auron, D. G. Tenen, and Z. Sun. 1999. Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc. Natl. Acad. Sci. USA 96: 8705-8710.
31. Rosenbauer, F., K. Wagner, J. Kutok, H. Iwasaki, M. M. Le Beau, Y. Okuno, K. Asashi, S. Fiering, and D. G. Tenen. 2004. Acute myeloid leukemia induced by graded reduction of a lineage-specific transcription factor, PU.1. Nat. Genet. 36: 624-630.
32. Yamamoto, H., F. Kihara-Negishi, T. Yamada, Y. Hashimoto, and T. Oikawa. 1999. Physical and functional interactions between the transcription factor PU.1 and the coactivator CBP. Oncogene 18: 1495-1501.
33. Hong, W., A. Y. Kim, S. Ky, C. Rakowski, S. B. Seo, D. Chakravarti, M. Atchison, and G. A. Blobel. 2002. Inhibition of CBP-mediated protein acetylation by the Ets family oncoprotein PU.1. Mol. Cell. Biol. 22: 3729-3743.
34. Nikolajczyk, B. S., A. Sanchez, and R. Sen. 1999. ETS protein-dependent accessibility changes at the immunoglobulin μ heavy chain enhancer. Immunity 11: 11-20.
35. Sato, H., F. Saito-Ohara, J. Inazawa, and A. Kudo. 2004. Pax-5 is essential for κ sterile transcription during Igκ chain gene rearrangement. J. Immunol. 172: 4858-4865.
36. McDevit, D. C., L. Perkins, M. L. Atchison, and B. S. Nikolajczyk. 2005. The Igκ3′ enhancer is activated by gradients of chromatin accessibility and protein association. J. Immunol. 174: 2834-2842.
37. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
38. Perkel, J. M., and M. L. Atchison. 1998. A two-step mechanism for recruitment of Pip by PU.1. J. Immunol. 160: 241-252.
39. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475-1489.
40. Graham, F. L., and A. J. Van der Eb. 1973. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52: 456-467.
41. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2: 1044-1051.
42. Kaelin, W. G. J., D. C. Pallas, J. A. DeCaprio, F. J. Kaye, and D. M. Livingston. 1991. Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product. Cell 64: 521-532.
43. Takeda, S., Y. R. Zou, H. Bluethmann, D. Kitamura, U. Muller, and K. Rajewsky. 1993. 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.
44. Gorman, J. R., N. van der Stoep, R. Monroe, M. Cogne, L. Davidson, and F. W. Alt. 1996. The Igκ 3′ enhancer influences the ratio of Igκ versus Igλ B lymphocytes. Immunity 5: 241-252.
45. Xu, Y., L. Davidson, F. W. Alt, and D. Baltimore. 1996. Deletion of the Igκ light chain intronic enhancer/matrix attachment region impairs but does not abolish VκJκ rearrangement. Immunity 4: 377-385.
46. Hiramatsu, R., K. Akagi, M. Matsuoka, K. Sakumi, H. Nakamura, L. Kingsbury, C. David, R. R. Hardy, K.-i. Yamamura, and H. Sakano. 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.
47. Betz, A. G., C. Milstein, A. Gonzalel-Fernandez, R. Pannell, T. Larson, and M. S. Neuberger. 1994. Elements regulating somatic hypermutation of an Igκ gene: critical role of the intron enhancer/matrix attachment region. Cell 77: 239-248.
48. Pongubala, J. M. R., and M. L. Atchison. 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: 10304-10413.
49. Nagulapalli, S., and M. L. Atchison. 1998. Transcription factor Pip can enhance DNA binding by E47, leading to transcriptional synergy involving multiple protein domains. Mol. Cell. Biol. 18: 4639-4650.
50. Klemsz, M. J., and R. A. Maki. 1996. Activation of transcription by PU.1 requires both acidic and glutamine domains. Mol. Cell. Biol. 16: 390-397.
51. Marecki, S., K. McCarthy, and B. S. Nikolajczyk. 2004. PU.1 as a chromatin accessibility factor for immunoglobulin genes. Mol. Immunol. 40: 723-731.
52. Linderson, Y., D. Eberhard, S. Malin, A. Johansson, M. Busslinger, and S. Pettersson. 2004. Corecruitment of the Grg4 repressor by PU.1 is critical for Pax5-mediated repression of B-cell-specific genes. EMBO Rep. 5: 291-296.
53. Maitra, S., and M. Atchison. 2000. BSAP can repress enhancer activity by targeting PU.1 function. Mol. Cell. Biol. 20: 1911-1922.
54. Kodandapani, R., F. Pio, C.-Z. Ni, G. Piccialli, M. Klemsz, S. McKercher, R. A. Maki, and K. R. Ely. 1996. A new pattern for helix-turn-helix recognition revealed by the PU.1 ETS-domain-DNA complex. Nature 380: 456-460.
55. Henkel, G. W., S. R. McKercher, P. J. Leenen, and R. A. Maki. 1999. Commitment to the monocytic lineage occurs in the absence of the transcription factor PU.1. Blood 93: 2849-2858.
56. Chiang, M. Y., and J. G. Monroe. 1999. BSAP/Pax5A expression blocks survival and expansion of early myeloid cells implicating its involvement in maintaining commitment to the B-lymphocyte lineage. Blood 94: 3621-3632.