Differential Binding of the Bombyx Silk Gland-specific Factor SGFB to Its Target DNA Sequence Drives Posterior-cell-restricted Expression

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 1997 Mar 1

PMID 9032285

Citations 10

Authors

B Horard

E Julien

P Nony

A Garel

P Couble

Affiliations

Soon will be listed here.

Abstract

The gene encoding the silk protein P25 in Bombyx mori is expressed in the posterior silk gland (PSG) cells and repressed in the middle silk gland (MSG) cells. To identify the factors involved in this transcription-dependent spatial restriction, we examined the P25 chromatin in PSG and MSG nuclei by DNase I-aided ligation-mediated PCR and analyzed the expression of various P25-lacZ constructs in biolistically treated silk glands. P25 promoter activation depends on two cis-acting elements. One coincides with the target sequence of SGFB, a silk gland-specific factor present in all silk gland nuclei, but bound to its target DNA sequence in only PSG cells. The interaction of the other element with a factor that we named PSGF is also exclusive to PSG cells. Placed ahead of a non-P25-related basal promoter, the SGFB and PSGF elements are sufficient to drive posterior-cell transcription. Collectively, our data support the hypothesis that the spatial restriction of P25 expression is driven by the stabilization of SGFB onto its target sequence by the action of PSGF.

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References

Garrity P, Wold B . Effects of different DNA polymerases in ligation-mediated PCR: enhanced genomic sequencing and in vivo footprinting. Proc Natl Acad Sci U S A. 1992; 89(3):1021-5. PMC: 48377. DOI: 10.1073/pnas.89.3.1021. View

Kikuchi Y, Mori K, Suzuki S, Yamaguchi K, Mizuno S . Structure of the Bombyx mori fibroin light-chain-encoding gene: upstream sequence elements common to the light and heavy chain. Gene. 1992; 110(2):151-8. DOI: 10.1016/0378-1119(92)90642-3. View

Bello B, Couble P . Specific expression of a silk-encoding gene of Bombyx in the anterior salivary gland of Drosophila. Nature. 1990; 346(6283):480-2. DOI: 10.1038/346480a0. View

Durand B, Drevet J, Couble P . P25 gene regulation in Bombyx mori silk gland: two promoter-binding factors have distinct tissue and developmental specificities. Mol Cell Biol. 1992; 12(12):5768-77. PMC: 360516. DOI: 10.1128/mcb.12.12.5768-5777.1992. View

Mach V, Takiya S, Ohno K, Handa H, Imai T, Suzuki Y . Silk gland factor-1 involved in the regulation of Bombyx sericin-1 gene contains fork head motif. J Biol Chem. 1995; 270(16):9340-6. DOI: 10.1074/jbc.270.16.9340. View

Rosenthal N . Identification of regulatory elements of cloned genes with functional assays. Methods Enzymol. 1987; 152:704-20. DOI: 10.1016/0076-6879(87)52075-4. View

Tanaka K, Mori K, Mizuno S . Immunological identification of the major disulfide-linked light component of silk fibroin. J Biochem. 1993; 114(1):1-4. DOI: 10.1093/oxfordjournals.jbchem.a124122. View

Janson L, Pettersson U . Cooperative interactions between transcription factors Sp1 and OTF-1. Proc Natl Acad Sci U S A. 1990; 87(12):4732-6. PMC: 54191. DOI: 10.1073/pnas.87.12.4732. View

Gerster T, Matthias P, Thali M, Jiricny J, Schaffner W . Cell type-specificity elements of the immunoglobulin heavy chain gene enhancer. EMBO J. 1987; 6(5):1323-30. PMC: 553936. DOI: 10.1002/j.1460-2075.1987.tb02371.x. View

10.

Tsukiyama T, Becker P, Wu C . ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature. 1994; 367(6463):525-32. DOI: 10.1038/367525a0. View

11.

Takiya S, Hui C, Suzuki Y . A contribution of the core-promoter and its surrounding regions to the preferential transcription of the fibroin gene in posterior silk gland extracts. EMBO J. 1990; 9(2):489-96. PMC: 551691. DOI: 10.1002/j.1460-2075.1990.tb08135.x. View

12.

Mialhe E, MILLER L . Biolistic techniques for transfection of mosquito embryos (Anopheles gambiae). Biotechniques. 1994; 16(5):924-31. View

13.

Mirkovitch J, Decker T, Darnell Jr J . Interferon induction of gene transcription analyzed by in vivo footprinting. Mol Cell Biol. 1992; 12(1):1-9. PMC: 364063. DOI: 10.1128/mcb.12.1.1-9.1992. View

14.

Nony P, Prudhomme J, Couble P . Regulation of the P25 gene transcription in the silk gland of Bombyx. Biol Cell. 1995; 84(1-2):43-52. DOI: 10.1016/0248-4900(96)81317-7. View

15.

Couble P, Chevillard M, Moine A, Ravel-Chapuis P, Prudhomme J . Structural organization of the P25 gene of Bombyx mori and comparative analysis of its 5' flanking DNA with that of the fibroin gene. Nucleic Acids Res. 1985; 13(5):1801-14. PMC: 341112. DOI: 10.1093/nar/13.5.1801. View

16.

Mange A, Julien E, Prudhomme J, Couble P . A strong inhibitory element down-regulates SRE-stimulated transcription of the A3 cytoplasmic actin gene of Bombyx mori. J Mol Biol. 1997; 265(3):266-74. DOI: 10.1006/jmbi.1996.0734. View

17.

Couble P, Moine A, Garel A, Prudhomme J . Developmental variations of a nonfibroin mRNA of Bombyx mori silkgland, encoding for a low-molecular-weight silk protein. Dev Biol. 1983; 97(2):398-407. DOI: 10.1016/0012-1606(83)90096-9. View

18.

McKnight S . Transcription revisited: a commentary on the 1995 Cold Spring Harbor Laboratory meeting, "Mechanisms of Eukaryotic Transcription". Genes Dev. 1996; 10(4):367-81. DOI: 10.1101/gad.10.4.367. View

19.

Fukuta M, Matsuno K, Hui C, Nagata T, Takiya S, Xu P . Molecular cloning of a POU domain-containing factor involved in the regulation of the Bombyx sericin-1 gene. J Biol Chem. 1993; 268(26):19471-5. View

20.

Hui C, Suzuki Y . Enhancement of transcription from the Ad2 major late promoter by upstream elements of the fibroin- and sericin-1-encoding genes in silk gland extracts. Gene. 1989; 85(2):403-11. DOI: 10.1016/0378-1119(89)90433-2. View