Spatial and temporal patterns of E74 transcription during Drosophila development
Abstract
The E74 gene occupies one of the early puff loci (74EF) central to the Ashburner model for the ecdysone-induced puffing pattern in Drosophila. In support of this model, we show that the E74A promoter is directly activated by ecdysone and is subsequently repressed by ecdysone-induced proteins. Further support derives from the correspondence observed between 74EF puff size and the accumulation of nascent transcripts on the E74A unit. These transcripts elongate at 1.1 kb/min so that this 60 kb unit acts as a timer, delaying the appearance of its mRNA by 1 hr. E74A transcription is induced in a variety of ecdysone target tissues in late third instar larvae and during each of the ecdysone pulses that mark the six stages of Drosophila development. These results support an extension of the Ashburner model in which ecdysone pulses coordinate tissue development. The temporal pattern of E74B transcription overlaps but is distinct from that of E74A.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Pioneering biochemical studies estimated average RNA Pol II speed between 1.1 kb/min and 4.8 kb/min on a few genes.
“By monitoring the appearance of RNA by in situ hybridization, nuclear run‐on, slot blot, or RT–PCR after expression activation, RNA Pol II speed was estimated between 1.1 kb/min and 4.8 kb/min (Ucker & Yamamoto, 1984; Thummel et al, 1990; Shermoen & O'Farrell, 1991; O'Brien & Lis, 1993; Tennyson et al, 1995; Femino et al, 1998; Femino et al, 2003; Hanisch et al, 2013).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Thummel et al, 1990
RNA Pol II velocity has been suggested to affect the timing of mRNA accumulation and could thus play a role in the timing of some developmental regulatory processes.
“Nevertheless, RNA Pol II velocity has also been suggested to affect the timing of mRNA accumulation and could thus play a role in the timing of some developmental regulatory processes (Thummel et al, 1990; Fukaya et al, 2017; Maslon et al, 2019).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Thummel et al, 1990
Cites
Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease
Chirgwin, J. M., Przybyla, A., MacDonald, R. J., & Rutter, W. J. (1979) · Biochemistry · doi:10.1021/bi00591a005 · Cited by 21,725 · see citing works
Rigby, P. W. J., Dieckmann, M., Rhodes, C., & Berg, P. R. (1977) · Journal of Molecular Biology · doi:10.1016/0022-2836(77)90052-3 · Cited by 11,400 · see citing works
A membrane-filter technique for the detection of complementary DNA
Denhardt, D. T. (1966) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(66)90447-5 · Cited by 3,944 · see citing works
McMaster, G. K., & Carmichael, G. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.11.4835 · Cited by 2,406 · see citing works
Temporal control of puffing activity in polytene chromosomes
Ashburner, M., Chihara, C., Meltzer, P., & Richards, G. (1974) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1974.038.01.070 · Cited by 641 · see citing works
Sequence, structure, and codon preference of theDrosophilaribosomal protein 49 gene
O'Connell, P., & Rosbash, M. (1984) · Nucleic Acids Research · doi:10.1093/nar/12.13.5495 · Cited by 519 · see citing works
Segraves, W. A., & Hogness, D. S. (1990) · Genes & Development · doi:10.1101/gad.4.2.204 · Cited by 485 · see citing works
Self-citationBurtis, K. C., Thummel, C. S., Jones, C. W., Karim, F. D., & Hogness, D. S. (1990) · Cell · doi:10.1016/0092-8674(90)90217-3 · Cited by 409 · see citing works
Self-citationMAINTENANCE OF IMAGINAL DISCS OF DROSOPHILA MELANOGASTER IN CHEMICALLY DEFINED MEDIA
Robb, J. A. (1969) · The Journal of Cell Biology · doi:10.1083/jcb.41.3.876 · Cited by 305 · see citing works
Sequential gene activation by ecdysone in polytene chromosomes of Drosophila melanogaster
Ashburner, M. (1974) · Developmental Biology · doi:10.1016/s0012-1606(74)80016-3 · Cited by 270 · see citing works
Drosophila: A practical approach
Whittle, J. R. S. (1987) · FEBS Letters · doi:10.1016/0014-5793(87)80456-8 · Cited by 255 · see citing works
White, K. A., & Kankel, D. R. (1978) · Developmental Biology · doi:10.1016/0012-1606(78)90029-5 · Cited by 255 · see citing works
Patterns of puffing activity in the salivary gland chromosomes of Drosophila
Ashburner, M. (1972) · Chromosoma · doi:10.1007/bf00290925 · Cited by 231 · see citing works
Ecdysteroid titers during pupal and adult development in Drosophila melanogaster
Handler, A. M. (1982) · Developmental Biology · doi:10.1016/0012-1606(82)90240-8 · Cited by 218 · see citing works
Diazotizable arylamine cellulose papers for the coupling and hybridization of nucleic acids
Seed, B. (1982) · Nucleic Acids Research · doi:10.1093/nar/10.5.1799 · Cited by 217 · see citing works
Ecdysone titers during postembryonic development of Drosophila melanogaster
Hodgetts, R. B., Sage, B. A., & O’Connor, J. D. (1977) · Developmental Biology · doi:10.1016/0012-1606(77)90128-2 · Cited by 205 · see citing works
Ucker, D. S., & Yamamoto, K. R. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42806-7 · Cited by 190 · see citing works
The radioimmune assay of ecdysteroid titres in drosophila melanogaster
Richards, G. (1981) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(81)90013-7 · Cited by 190 · see citing works
Kraminsky, G., Clark, W. C., Estelle, M. A., et al. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.7.4175 · Cited by 179 · see citing works
Kafatos, F. C. (1972) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)60071-x · Cited by 149 · see citing works
Sequential gene activation by ecdysone in polytene chromosomes of Drosophila melanogaster,
Richards, G. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90303-1 · Cited by 98 · see citing works
INSECT HORMONES IN DEVELOPMENT
Richards, G. (1981) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1981.tb00358.x · Cited by 89 · see citing works
Molecular analysis of the ecdysterone‐inducible 2B5 ‘early’ puff in Drosophila melanogaster.
Chao, A. T., & Guild, G. M. (1986) · The EMBO Journal · doi:10.1002/j.1460-2075.1986.tb04188.x · Cited by 75 · see citing works
Sequential gene activation by ecdysone in polytene chromosomes of Drosophila melanogaster,
Richards, G. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90304-3 · Cited by 63 · see citing works
An analysis of dopa decarboxylase expression during embryogenesis in Drosophila melanogaster
Gietz, R. D., & Hodgetts, R. B. (1985) · Developmental Biology · doi:10.1016/0012-1606(85)90383-5 · Cited by 44 · see citing works
Richards, G. P. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90057-9 · Cited by 40 · see citing works
Sequential gene activation by ecdysteroids in polytene chromosomes ofDrosophila melanogaster
Richards, G. (1982) · Development Genes and Evolution · doi:10.1007/bf00848447 · Cited by 34 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Getting up to speed with transcription elongation by RNA polymerase II
Jonkers, I., & Lis, J. T. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3953 · Cited by 876 · see citing works
Ecdysone receptors and their biological actions
Riddiford, L. M., Cherbas, P., & Truman, J. W. (2000) · Vitamins & Hormones · doi:10.1016/s0083-6729(00)60016-x · Cited by 605 · see citing works
The ETS-domain: a new DNA-binding motif that recognizes a purine-rich core DNA sequence.
Karim, F. D., Urness, L. D., Thummel, C. S., Klemsz, M. J., McKercher, S. R., Celada, A., Van Beveren, C., Maki, R. A., Gunther, C. V., & Nye, J. A. (1990) · Genes & Development · doi:10.1101/gad.4.9.1451 · Cited by 499 · see citing works
Self-citationProgression of the cell cycle through mitosis leads to abortion of nascent transcripts
Shermoen, A. W., & O'Farrell, P. H. (1991) · Cell · doi:10.1016/0092-8674(91)90182-x · Cited by 360 · see citing works
Drosophila Ecdysone Receptor Mutations Reveal Functional Differences among Receptor Isoforms
Bender, M., Imam, F. B., Talbot, W. S., Ganetzky, B., & Hogness, D. S. (1997) · Cell · doi:10.1016/s0092-8674(00)80466-3 · Cited by 280 · see citing works
Self-citationRNA polymerase II speed: a key player in controlling and adapting transcriptome composition
Muniz, L., Nicolas, E., & Trouche, D. (2021) · The EMBO Journal · doi:10.15252/embj.2020105740 · Cited by 203 · see citing works
“…run-on, slot blot, or RT – PCR after expression activation, RNA Pol II speed was estimated between 1.1 kb/min and 4.8 kb/min (Ucker & Yamamoto, 1984; Thummel et al , 1990; Sher-moen & O’Farrell, 1991; O’Brien & Lis, 1993; Tennyson et al , 1995; Femino et al , 1998; Femino et al , 2003; Hanisch et…”
InfluentialSpt6 enhances the elongation rate of RNA polymerase II in vivo
Ardehali, M. B., Yao, J., Adelman, K., Fuda, N. J., Petesch, S. J., Webb, W. W., & Lis, J. T. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.56 · Cited by 157 · see citing works
Fletcher, J. C., Burtis, K. C., Hogness, D. S., & Thummel, C. S. (1995) · Development · doi:10.1242/dev.121.5.1455 · Cited by 133 · see citing works
Self-citationIntranuclear Distribution and Local Dynamics of RNA Polymerase II during Transcription Activation
Yao, J., Ardehali, M. B., Fecko, C. J., Webb, W. W., & Lis, J. T. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.10.017 · Cited by 111 · see citing works
Lan, Q., Hiruma, K., Hu, X., Jindra, M., & Riddiford, L. M. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.7.4897 · Cited by 107 · see citing works
Sequence and functional properties of Ets genes in the model organism Drosophila
Hsu, T., & Schulz, R. A. (2000) · Oncogene · doi:10.1038/sj.onc.1204033 · Cited by 85 · see citing works
Calcium-induced phosphorylation of ETS1 inhibits its specific DNA binding activity.
Rabault, B., & Ghysdael, J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)46906-2 · Cited by 94 · see citing works
Rapid Rates of Pol II Elongation in the Drosophila Embryo
Fukaya, T., Lim, B., & Levine, M. (2017) · Current Biology · doi:10.1016/j.cub.2017.03.069 · Cited by 84 · see citing works
Hindle, S. J., Munji, R. N., Dolghih, E., Gaskins, G., Orng, S., Ishimoto, H., Soung, A., DeSalvo, M., Kitamoto, T., Keiser, M. J., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.026 · Cited by 74 · see citing works
Developmentally programmed cell death in Drosophila
Denton, D., Aung-Htut, M. T., & Kumar, S. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.06.014 · Cited by 75 · see citing works
- Authors
- Thummel, C. S., Burtis, K. C., & Hogness, D. S.
- Affiliations
- Stanford Medicine (US)
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 1990-04
- Volume
- 61
- Issue
- 1
- Pages
- 101-111
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2052316171
- Cited by
- 262
- References
- 27
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 1 · 2022: 5 · 2021: 12 · 2020: 2 · 2019: 5 · 2018: 4 · 2017: 5 · 2016: 2 · 2015: 4 · 2014: 2 · 2013: 5 · 2012: 7
- FWCI
- 9.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- puffing, ecdysone, transcriptional regulation, nascent RNA, Drosophila development, larval development
- MeSH terms
- Aging, Animals, Chromosomes, Drosophila melanogaster, Ecdysone, Gene Expression Regulation, Larva, Nucleic Acid Hybridization, Organ Culture Techniques, Promoter Regions, Genetic, RNA, RNA, Messenger, Salivary Glands, Transcription, Genetic, Blotting, Northern
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review