Differential activity of the -2.7 kb chicken lysozyme enhancer in macrophages of different ontogenic origins is regulated by C/EBP and PU.1 transcription factors

DNA and Cell Biology

Volumn 18, Issue 8, 1999, Pages 631-642

  Faust, Nicole ^a,b   Bonifer, Constanze ^a,c   Sippel, Albrecht E ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Artemis Pharmaceuticals GmbH   (Germany)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; LYSOZYME;

ANIMAL CELL; ARTICLE; CHICKEN; CONTROLLED STUDY; DNA BINDING; GENE EXPRESSION; GENETIC TRANSFECTION; MACROPHAGE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS;

AGING; ANIMALS; BONE MARROW CELLS; CCAAT-ENHANCER-BINDING PROTEINS; CELL LINE; CHICK EMBRYO; CHICKENS; DNA; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MURAMIDASE; MUTATION; NUCLEAR PROTEINS; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS; RESPONSE ELEMENTS; TRANS-ACTIVATORS; TRANSFECTION;

ANIMALIA; AVES; GALLUS GALLUS;

EID: 0032790347     PISSN: 10445498     EISSN: None     Source Type: Journal    
DOI: 10.1089/104454999315042     Document Type: Article

References (68)

1. AHNE, B., and STRÄTLING, W.H. (1994). Characterization of a myeloid-specific enhancer of the chicken lysozyme gene: major role for an Ets transcription factor-binding site. J. Biol. Chem. 269, 17794-17801.
2. AKIRA, S., ISSHIKI, H., SUGITA, T., TANABE, O., KINOSHITA, S., NISHIO, Y., NAKAJIMA, T., HIRANO, T., and KISHIMOTO, T. (1990). A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 9, 1897-1906.
3. ALTSCHMIED, J., MULLER, M., BANIAHMAD, A., STEINER, C., and RENKAWITZ, R. (1989). Cooperative interaction of chicken lysozyme enhancer sub-domains partially overlapping with a steroid receptor binding site. Nucleic Acids Res. 17, 4975-4991.
4. ANGEL, P., IMAGAWA, M., CHIU, R., STEIN, B., IMBRA, R.J., RAHMSDORF, H.J., JONAT, C., HERRLICH, P., and KARIN, M. (1987). Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell 49, 729-739.
5. BEUG, H., VON KIRCHBACH, A., DODERLEIN, G., CONSCIENCE, J.F., and GRAF, T. (1979). Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18, 375-390.
6. BEUG, H., HAYMAN, M.J., and GRAF, T. (1982). Myeloblasts transformed by the avian acute leukemia virus E26 are hormone-dependent for growth and for the expression of a putative myb-containing protein, p135 E26. EMBO J. 1, 1069-1073.
7. BONIFER, C., BOSCH, F.X., FAUST, N., SCHUHMANN, A., and SIPPEL, A.E. (1994). Evolution of gene regulation as revealed by differential regulation of the chicken lysozyme transgene and the endogenous mouse lysozyme gene in mouse macrophages. Eur. J. Biochem. 226, 227-235.
8. BONIFER, C., FAUST, N., GEIGER, H., and MÜLLER, A.M. (1998). Developmental changes in the differentiation capacity of haematopoietic stem cells. Immunol. Today 19, 236-241.
9. BONIFER, C., FAUST, N., HUBER, M.C., SAUERESSIG, H., and SIPPEL, A.E. (1997). The chicken lysozyme chromatin domain. In Nuclear Organization, Chromatin Structure, and Gene Expression. R. van Driel and A.P. Otte, eds. (Oxford University Press, Oxford) pp. 116-128.
10. BONIFER, C., HUBER, M.C., JÄGLE, U., FAUST, N., and SIPPEL, A.E. (1996). Prerequisites for tissue specific and position independent expression of a gene locus in transgenic mice. J. Mol. Med. 74, 663-671.
11. BORGMEYER, U., NOWOCK, J., and SIPPEL, A.E. (1984). The TGGCA-binding protein: a eukaryotic nuclear protein recognizing a symmetrical sequence on double-stranded linear DNA. Nucleic Acids Res. 12, 4295-4311.
12. BRETZ, J.D., WILLIAMS, S.C., BAER, M., JOHNSON, P.F., and SCHWARTZ, R.C. (1994). C/EBP-related protein 2 confers lipopolysaccharide-inducible expression of interleukin 6 and monocyte chemoattractant protein 1 to a lymphoblastic cell line. Proc. Natl. Acad. Sci. USA 91, 7306-7310.
13. CHOMCZYNSKI, P., and SACCHI, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
14. CLEVELAND, D.W., LOPATA, M.A., MACDONALD, R.J., COWAN, N.J., RUTTER, W.J., and KIRSCHNER, M.W. (1980). Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell 20, 95-105.
15. DE WET, J.R., WOOD, K.V., DELUCA, M., HELINSKI, D.R., and SUBRAMANI, S. (1987). Firefly luciferase gene: structure and expression in mammalian cells. Mol. Cell. Biol. 7, 725-737.
16. DESCOMBES, P., and SCHIBLER, U. (1991). A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein. LIP, are translated from the same mRNA. Cell 67, 569-579.
17. FAUST, N., HUBER, M.C., SIPPEL, A.E., and BONIFER, C. (1997). Different macrophage populations develop from embryonic/fetal and adult hematopoietic tissues. Exp. Hematol. 25, 432-444.
18. FRITTON, H.P., IGO-KEMENES, T., NOWOCK, J., STRECH-JURK, U., THEISEN, M., and SIPPEL, A.E. (1984). Alternative sets of DNase I-hypersensitive sites characterize the various functional states of the chicken lysozyme gene. Nature 311, 163-165.
19. FRITTON, H.P., IGO-KEMENES, T., NOWOCK, J., STRECH-JURK, U., THEISEN, M., and SIPPEL, A.E. (1987). DNase I-hypersensitive sites in the chromatin structure of the lysozyme gene in steroid hormone target and non-target cells. Biol. Chem. Hoppe Seyler 368, 111-119.
20. GOETHE, R., and PHI VAN, L. (1994). The far upstream chicken lysozyme enhancer at -6.1 kilobase, by interacting with NF-M, mediates lipopolysaccharide-induced expression of the chicken lysozyme gene in chicken myelomonocytic cells. J. Biol. Chem. 269, 31302-31309.
21. GREWAL, T., THEISEN, M., BORGMEYER, U., GRUSSENMEYER, T., RUPP, R.A.W., STIEF, A., QIAN, F., HECHT, A., and SIPPEL, A.E. (1992). The -6.1 -kilobase chicken lysozyme enhancer is a multifactorial complex containing several cell-type-specific elements. Mol. Cell. Biol. 12, 2339-2350.
22. GREZ, M., LAND, H., GIESECKE, K., SCHÜTZ, G., JUNG, A., and SIPPEL, A.E. (1981). Multiple mRNAs are generated from the chicken lysozyme gene. Cell 25, 743-752.
23. HECHT, A. (1990). Strukturelle und funktionelle Charakterisierung des steroidhormonabhängigen Enhancerelements des Lysozymgens und seine Zellspezifität. (Ph. D. Thesis, University of Heidelberg).
24. HOHAUS, S., PETROVICK, M.S., VOSO, M.T., SUN, Z., ZHANG, D.E., and TENEN, D.G. (1995). PU.1 (Spi-1) and C/EBP alpha regulate expression of the granulocyte-macrophage colony-stimulating factor receptor alpha gene. Mol. Cell. Biol. 15, 5830-5845.
25. HROMAS, R., ORAZI, A., NEIMAN, R.S., MAKI, R., VAN BEVERAN, C., MOORE, J., and KLEMSZ, M. (1993). Hematopoietic lineage- and stage-restricted expression of the ETS oncogene family member PU.1. Blood 82, 2998-3004.
26. HU, H.M., BAER, M., WILLIAMS, S.C., JOHNSON, P.F., and SCHWARTZ, R.C. (1998). Redundancy of C/EBP alpha, -beta, and -delta in supporting the lipopolysaccharide-induced transcription of IL-6 and monocyte chemoattractant protein-1. J. Immunol. 160, 2334-2342.
27. HUBER, M.C., GRAF, T., SIPPEL, A.E., and BONIFER, C. (1995). Dynamic changes in the chromatin of the chicken lysozyme gene domain during differentiation of multipotent progenitors to macrophages. DNA Cell Biol. 14, 397-402.
28. HUBER, M.C., JAGLE, U., KRUGER, G., and BONIFER, C. (1997). The developmental activation of the chicken lysozyme locus in transgenic mice requires the interaction of a subset of enhancer elements with the promoter. Nucleic Acids Res. 25, 2992-3000.
29. JOHNSON, P.F., LANDSCHULZ, W.H., GRAVES, B.J., and MCKNIGHT, S.L. (1987). Identification of a rat liver nuclear protein that binds to the enhancer core element of three animal viruses. Genes Dev. 1, 133-146.
30. JÄGLE, U., MÜLLER, A.M., KOHLER, H., and BONIFER, C. (1997). Role of positive and negative cis-regulatory elements in the transcriptional activation of the lysozyme locus in developing macrophages of transgenic mice. J. Biol. Chem. 272, 5871-5879.
31. KATZ, S., KOWENZ-LEUTZ, E., MULLER, C., MEESE, K., NESS, S.A., and LEUTZ, A. (1993). The NF-M transcription factor is related to C/EBP beta and plays a role in signal transduction, differentiation and leukemogenesis of avian myelomonocytic cells. EMBO J. 12, 1321-1332.
32. LAVERY, D.J., and SCHIBLER, U. (1993). Circadian transcription of the cholesterol 7 alpha hydroxylase gene may involve the liver-enriched bZIP protein DBP. Genes Dev. 7, 1871-1884.
33. LEUTZ, A., BEUG, H., and GRAF, T. (1984). Purification and characterization of cMGF, a novel chicken myelomonocytic growth factor. EMBO J. 3, 3191-3197.
34. LICHANSKA, A.M., BROWNE, C.M., HENKEL, G.W., MURPHY, K.M., OSTROWSKI, M.C., MCKERCHER, S.R., MAKI, R.A., and HUME, D.A. (1999). Differentiation of the embryonic mononuclear phagocyte system: the role of transcription factor PU.1. Blood (in press).
35. LIN, F.T., MACDOUGALD, O.A., DIEHL, A.M., and LANE, M.D. (1993). A 30-kDa alternative translation product of the CCAAT/enhancer binding protein alpha message: transcriptional activator lacking antimitotic activity. Proc. Natl. Acad. Sci. USA 90, 9606-9610.
36. LUCKOW, B., and SCHÜTZ, G. (1987). CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements. Nucleic Acids Res. 15, 5490.
37. MAXAM, A.M., and GILBERT, W. (1980). Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65, 499-560.
38. MCKERCHER, S.R., TORBETT, B.E., ANDERSON, K.L., HENKEL, G.W., VESTAL, D.J., BARIBAULT, H., KLEMSZ, M., FEENEY, A.J., WU, G.E., PAIGE, C.J., and MAKI, R.A. (1996). Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 15, 5647-5658.
39. MCKNIGHT, S.L. (1992). CCAAT/enhancer binding protein. In Transcriptional Regulation. S.L. McKnight and K.R. Yamamoto, eds. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY) pp. 771-795.
40. MCNAGNY, K.M., SIEWEKE, M.H., DÖDERLEIN, G., GRAF, T., and NERLOV, C. (1998). Regulation of eosinophil-specific gene expression by a C/EBP-Ets complex and GATA-1. EMBO J. 17, 3669-3680.
41. MORIOKA, Y., NAITO, M., SATO, T., and TAKAHASHI, K. (1994). Immunophenotypic and ultrastructural heterogeneity of macrophage differentiation in bone marrow and fetal hematopoiesis of mouse in vitro and in vivo. J. Leukocyte Biol. 55, 642-651.
42. NAITO, M., UMEDA, S., YAMAMOTO, T., MORIYAMA, H., UMEZU, H., HASEGAWA, G., USUDA, H., SHULTZ, L.D., and TAKAHASHI, K. (1996). Development, differentiation, and phenotypic heterogeneity of murine tissue macrophages. J. Leukocyte Biol. 59, 133-138.
43. NATSUKA, S., AKIRA, S., NISHIO, Y., HASHIMOTO, S., SUGITA, T., ISSHIKI, H., and KISHIMOTO, T. (1992). Macrophage differentiation-specific expression of NF-IL6, a transcription factor for interleukin-6. Blood 79, 460-466.
44. NERLOV, C., and GRAF, T. (1998). PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev. 12, 2403-2412.
45. NERLOV, C., MCNAGNY, K.M., DODERLEIN, G., KOWENZLEUTZ, E., and GRAF, T. (1998). Distinct C/EBP functions are required for eosinophil lineage commitment and maturation. Genes Dev. 12, 2413-2423.
46. OLSON, M.C., SCOTT, E.W., HACK, A.A., SU, G.H., TENEN, D.G., SINGH, H., and SIMON, M.C. (1995). PU.1 is not essential for early myeloid gene expression but is required for terminal myeloid differentiation. Immunity 3, 703-714.
47. ORKIN, S.H. (1995). Transcription factors and hematopoietic development. J. Biol. Chem. 270, 4955-4958.
48. PAHL, H.L., SCHEIBE, R.J., ZHANG, D.E., CHEN, H.M., GALSON, D.L., MAKI, R.A., and TENEN, D.G. (1993). The proto-oncogene PU.1 regulates expression of the myeloid-specific CD11b promoter. J. Biol. Chem. 268, 5014-5020.
49. PAUPLIN, Y., and RECH, J. (1987). Nucleotide sequence of hare adult beta-globin gene with flanking regions. Nucleic Acids Res. 15, 5899.
50. RAY, A., and RAY, B.K. (1995). Lipopolysaccharide-mediated induction of the bovine interleukin-6 gene in monocytes requires both NF-kappa B and C/EBP binding sites. DNA Cell Biol. 14, 795-802.
51. RON, D., and HABENER, J.F. (1992). CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6, 439-453.
52. 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.
53. SCOTT, E.W., FISHER, R.C., OLSON, M.C., KEHRLI, E.W., SIMON, M.C., and SINGH, H. (1997). PU.1 functions in a cell-autonomous manner to control the differentiation of multipotential lymphoid-myeloid progenitors. Immunity 6, 437-447.
54. SCOTT, L.M., CIVIN, C.I., RORTH, P., and FRIEDMAN, A.D. (1992). A novel temporal expression pattern of three C/EBP family members in differentiating myelomonocytic cells. Blood 80, 1725-1735.
55. SCREPANTI, I., ROMANI, L., MUSIANI, P., MODESTI, A., FATTORI, E., LAZZARO, D., SELLITTO, C., SCARPA, S., BELLAVIA, D., LATTANZIO, G., BISTONI, F., FRATI, L., CORTESE, R., GULINO, A., CILIBERTO, G., COSTANTINI, F., and POLI, V. (1995). Lymphoproliferative disorder and imbalanced T-helper response in C/EBP beta-deficient mice. EMBO J. 14, 1932-1941.
56. SHAPIRO, D.J., SHARP, P.A., WAHLI, W.W., and KELLER, M.J. (1988). A high-efficiency HeLa cell nuclear transcription extract. DNA 7, 47-55.
57. SIPPEL, A.E., THEISEN, M., BORGMEYER, U., STRECH-JURK, U., RUPP, R.A.W., PUSCHEL, A.W., MÜLLER, A., HECHT, A., STIEF, A., and GRUSSENMEYER, T. (1988). Regulatory function and molecular structure of DNase I-hypersensitive elements in the chromatin domain of a gene. In The Architecture of Eukaryotic Genes. G. Kahl, ed. (Verlagsgesellschaft Chemie, Weinheim) pp. 355-369.
58. SIPPEL, A.E., SCHÄFER, G., FAUST, N., SAUERESSIG, H., HECHT, A., and BONIFER, C. (1993). Chromatin domains constitute regulatory units for the control of eukaryotic genes. Cold Spring Harbor Symp. Quant. Biol. 58, 37-44.
59. SIPPEL, A.E., SAUERESSIG, H., HUBER, M.C., HOEFER, H.C., STIEF, A., BORGMEYER, U., and BONIFER, C. (1996). Identification of cis-acting elements as DNase I hypersensitive sites in lysozyme gene chromatin. Methods Enzymol. 274, 233-246.
60. STEINER, C., MULLER, M., BANIAHMAD, A., and RENKAWITZ, R. (1987). Lysozyme gene activity in chicken macrophages is controlled by positive and negative regulatory elements. Nucleic Acids Res. 15, 4163-4178.
61. TANAKA, T., AKIRA, S., YOSHIDA, K., UMEMOTO, M., YONEDA, Y., SHIRAFUJI, N., FUJIWARA, H., SUEMATSU, S., YOSHIDA, N., and KISHIMOTO, T. (1995). Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages. Cell 80, 353-361.
62. TANAKA, T., YOSHIDA, N., KISHIMOTO, T., and AKIRA, S. (1997). Defective adipocyte differentiation in mice lacking the C/EBP-beta and/or C/EBP-delta gene. EMBO J. 16, 7432-7443.
63. THEISEN, M., STIEF, A., and SIPPEL, A.E. (1986). The lysozyme enhancer: cell-specific activation of the chicken lysozyme gene by a far-upstream element. EMBO J. 5, 719-724.
64. VINSON, C.R., SIGLER, P.B., and MCKNIGHT, S.L. (1989). Scissors-grip model for DNA recognition by a family of leucine zipper proteins. Science 246, 911-916.
65. VOSO, M.T., BURN, T.C., WULF, G., LIM, B., LEONE, G., and TENEN, D.G. (1994). Inhibition of hematopoiesis by competitive binding of transcription factor PU.1. Proc. Natl. Acad. Sci. USA 91, 7932-7936.
66. ZHANG, D.E., HETHERINGTON, C.J., MEYERS, S., RHOADES, K.L., LARSON, C.J., CHEN, H.M., HIEBERT, S.W., and TENEN, D.G. (1996a). CCAAT enhancer-binding protein (C/EBP) and AML1 (CBF alpha2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol. Cell. Biol. 16, 1231-1240.
67. ZHANG, D.E., HOHAUS, S., VOSO, M.T., CHEN, H.M., SMITH, L.T., HETHERINGTON, C.J., and TENEN, D.G. (1996b). Function of PU.1 (Spi-1), C/EBP, and AML1 in early myelopoiesis: regulation of multiple myeloid CSF receptor promoters. Curr. Top. Microbiol. Immunol. 211, 137-147.
68. ZHANG, D.E., ZHANG, P., WANG, N.D., HETHERINGTON, C.J., DARLINGTON, G.J., and TENEN, D.G. (1997). Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc. Natl. Acad. Sci. USA 94, 569-574.