DOI: 10.1101/gad.9.10.1278. P-element repressor autoregulation involves germ-line transcriptional repression and reduction of third intron splicing.

P-element repressor autoregulation involves germ-line transcriptional repression and reduction of third intron splicing.

10.1101/gad.9.10.1278

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

P cytotype is a regulatory state, characteristic of Drosophila P-strain females, in which P-element transposition is repressed. P cytotype is established maternally in the germ line but is also dependent on the presence of P elements in the zygote. One aspect of P cytotype involves transcriptional repression of the P-element promoter. Here, we show that transcriptional repression by P cytotype in the female germ line occurs by a general promoter-independent mechanism with heterologous promoters carried in P-element vectors. P-cytotype transcriptional repression results in low levels of pre-mRNA and a reduction in splicing of the P-element third intron (IVS3)-containing mRNA, thus causing an increase in the proportion of 66-kD repressor mRNA. Increased retention of IVS3 in P cytotype would result in an autoregulatory loop of 66-kD repressor production. This combination of germ-line transcriptional repression and splicing control provides a mechanism to maintain repression during the maternal inheritance of P cytotype. These findings suggest that transcriptional repression may play an additional role in the regulation of gene expression, namely allowing alteration of pre-mRNA splicing patterns.

Bibliography

Roche, S. E., Schiff, M., & Rio, D. C. (1995). P-element repressor autoregulation involves germ-line transcriptional repression and reduction of third intron splicing. Genes & Development, 9(10), 1278â1288.

Authors 3

S E Roche (first)
M Schiff (additional)
D C Rio (additional)

References 52 Referenced 53

Ashburner, M. 1989. Drosophila: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl, eds. 1987. Current protocols in molecular biology. Greene/John Wiley, New York.
10.1101/gad.2.6.754
10.1002/j.1460-2075.1987.tb02758.x / EMBO J. / KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. (1987)
10.1016/0955-0674(94)90032-9
10.1093/nar/15.4.1353
10.1093/genetics/126.4.949 / Genetics / P element regulatory products enhance zeste repression of a P[white duplicated] transgene in Drosophila melanogaster. (1990)
{'key': '2021111418224076000_9.10.1278.8', 'first-page': '3773', 'article-title': 'Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis.', 'volume': '13', 'year': '1993', 'journal-title': 'Mol Cell. Biol.'} / Mol Cell. Biol. / Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis. (1993)
10.1146/annurev.ge.17.120183.001531
Engels, W.R. 1989. P elements in Drosophila melanogaster. In Mobile DNA (ed. D.E. Berg, and M.M. Howe), pp. 437–484. American Society for Microbiology, Washington, D.C.
10.1002/j.1460-2075.1992.tb05364.x / EMBO J. / Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. (1992)
10.1101/gad.5.9.1513
10.1016/0092-8674(92)90358-J
10.1093/genetics/135.1.81 / Genetics / Type I repressors of P element mobility. (1993)
10.1242/dev.107.2.189 / Development / P-element-mediated enhancer detection applied to the study of oogenesis in Drosophila. (1989)
10.1002/j.1460-2075.1989.tb03493.x / EMBO J. / Autoregulatory and gap gene response elements of the evenskipped promoter of Drosophila. (1989)
10.1016/0092-8674(88)90216-4
10.1146/annurev.cb.09.110193.002403
10.1101/gad.5.12a.2288
10.1101/gad.5.10.1881
10.1016/0092-8674(93)90159-N
10.1016/0896-6273(90)90197-N
10.1073/pnas.88.7.2613
10.1101/gad.3.5.720
10.1016/0092-8674(86)90480-0
{'key': '2021111418224076000_9.10.1278.26', 'first-page': '611', 'article-title': 'The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A.', 'volume': '355', 'year': '1988', 'journal-title': 'Nature'} / Nature / The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. (1988)
{'key': '2021111418224076000_9.10.1278.27', 'first-page': '6059', 'article-title': 'Splicing precedes polyadenylation during Drosophila E74A transcription.', 'volume': '10', 'year': '1990', 'journal-title': 'Mol. Cell Biol.'} / Mol. Cell Biol. / Splicing precedes polyadenylation during Drosophila E74A transcription. (1990)
10.1073/pnas.88.10.4419
10.1093/genetics/135.1.149 / Genetics / Maternal repression of the P element promoter in the germline of Drosophila melanogaster: A model for the P cytotype. (1993)
10.1093/genetics/116.4.565 / Genetics / Analysis of the promoter of the ninaE opsin gene in Drosophila melanogaster. (1987)
10.1016/0092-8674(90)90365-L
10.1093/genetics/135.3.785 / Genetics / Cytotype control of Drosophila melanogaster P element transposition: Genomic position determines maternal repression. (1993)
10.1016/0092-8674(83)90133-2
10.1017/S0016672300030640 / Genet. Res. / Distribution and structure of cloned P elements from the Drosophila melanogaster P strain π2. (1992)
10.1073/pnas.84.24.9123
10.1016/0168-9525(90)90303-N
10.1093/genetics/133.3.605 / Genetics / Repression of hybrid dysgenesis in Drosophila melanogaster by individual naturally occurring P elements. (1993)
10.1016/0168-9525(91)90309-E / Trends Genet. / Regulation of Drosophila P element transposition. (1991)
10.1016/0959-437X(93)90093-5
10.1016/0092-8674(86)90481-2
10.1093/genetics/123.4.815 / Genetics / Modified P elements that mimic the P cytotype in Drosophila melanogaster. (1989)
10.1093/genetics/129.2.501 / Genetics / The maternally inherited regulation of P elements in Drosophila melanogaster can be elicted by two P copies at cytological site 1A on the X chromosome. (1991)
10.1007/BF00280208
10.1093/nar/11.18.6341
Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
10.1101/gad.8.14.1713
10.1101/gad.9.3.269
Spradling, A.C. 1986. P element-mediated transformation. In Drosophila: A practical approach (ed. D. Roberts), pp. 175–197. IRL Press, Oxford, UK.
10.1126/science.6289435
10.1016/0092-8674(81)90026-X
10.1016/0168-9525(92)90300-S
10.1016/0962-8924(93)90105-A

Dates

Type	When
Created	18 years, 2 months ago (June 5, 2007, 5:15 p.m.)
Deposited	3 years, 9 months ago (Nov. 14, 2021, 9:35 p.m.)
Indexed	2 weeks, 6 days ago (Aug. 6, 2025, 10 a.m.)
Issued	30 years, 3 months ago (May 15, 1995)
Published	30 years, 3 months ago (May 15, 1995)
Published Online	30 years, 3 months ago (May 15, 1995)
Published Print	30 years, 3 months ago (May 15, 1995)

Funders 0

None

BibTeX

@article{Roche_1995, title={P-element repressor autoregulation involves germ-line transcriptional repression and reduction of third intron splicing.}, volume={9}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.9.10.1278}, DOI={10.1101/gad.9.10.1278}, number={10}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Roche, S E and Schiff, M and Rio, D C}, year={1995}, month=may, pages={1278–1288} }

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