{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T13:33:50Z","timestamp":1789220030402,"version":"build-2803163510"},"reference-count":31,"publisher":"The Company of Biologists","issue":"3","license":[{"start":{"date-parts":[[1993,7,1]],"date-time":"1993-07-01T00:00:00Z","timestamp":741484800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[1993,7,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n               <jats:p>During Drosophila development, an important aspect of body patterning is the division of the embryo into repeating morphological units referred to as parasegments. The parasegmental domains are first defined at the blastoderm stage by alternating stripes of transcripts encoded by the pair-rule genes fushi tarazu (ftz) and even-skipped (eve) and later by stripes encoded by the segment polarity genes engrailed (en) and wingless. Here, we show that the runt gene (run) is required to generate asymmetries within these parasegmental domains. Using a heat-shock-inducible run transgene, we found that ectopic run expression leads to rapid repression of eve stripes and a somewhat delayed expansion of ftz stripes. Unexpectedly, we also found that ectopic run was a rapid and potent repressor of odd-numbered en stripes. Two remarkably different segmental phenotypes were generated as a consequence of these effects. In solving the mechanisms underlying these phenotypes, we discovered that the positioning of en stripes is largely determined by the actions of negative regulators. Our data indicate that run is required to limit the domains of en expression in the odd-numbered parasegments, while the odd-skipped gene is required to limit the domains of en expression in the even-numbered parasegments. Activation of en at the anterior margins of both sets of parasegments requires the repression of run and odd by the product of the eve gene. The spatial restriction of gene expression via negative and double negative pathways such as these is likely to be a common theme during development.<\/jats:p>","DOI":"10.1242\/dev.118.3.785","type":"journal-article","created":{"date-parts":[[2021,4,26]],"date-time":"2021-04-26T01:21:13Z","timestamp":1619400073000},"page":"785-796","source":"Crossref","is-referenced-by-count":62,"title":["Control of segmental asymmetry in <i>Drosophila<\/i> embryos"],"prefix":"10.1242","volume":"118","author":[{"given":"Armen S.","family":"Manoukian","sequence":"first","affiliation":[{"name":"University of Toronto Banting and Best Department of Medical Research, C. H. Best Institute , , 112 College Street, Toronto, Ontario, M5G 1L6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henry M.","family":"Krause","sequence":"additional","affiliation":[{"name":"University of Toronto Banting and Best Department of Medical Research, C. H. Best Institute , , 112 College Street, Toronto, Ontario, M5G 1L6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[1993,7,1]]},"reference":[{"key":"2024121723035232700_DEVELOP_118_3_785C1","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1016\/0092-8674(86)90543-X","article-title":"Zygotically active genes that affect the spatial expression of the fushi tarazu segmentation gene during early Drosophila embryogenesis","volume":"45","author":"Carroll","year":"1986","journal-title":"Cell"},{"key":"2024121723035232700_DEVELOP_118_3_785C2","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1242\/dev.107.3.673","article-title":"The zygotic control of Drosophila pair-rule gene expression II. Spatial repression by gap and pair-rule gene products","volume":"107","author":"Carroll","year":"1989","journal-title":"Development"},{"key":"2024121723035232700_DEVELOP_118_3_785C3","doi-asserted-by":"publisher","first-page":"1812","DOI":"10.1101\/gad.2.12b.1812","article-title":"Gene activities and segmental patterning in Drosophila: analysis of odd-skipped and pair-rule double mutants","volume":"2","author":"Coulter","year":"1988","journal-title":"Genes Dev"},{"key":"2024121723035232700_DEVELOP_118_3_785C4","doi-asserted-by":"publisher","first-page":"484","DOI":"10.1038\/356484b0","article-title":"Leukaemia\/Drosophila homology","volume":"356","author":"Daga","year":"1992","journal-title":"Nature"},{"key":"2024121723035232700_DEVELOP_118_3_785C5","doi-asserted-by":"publisher","first-page":"1212","DOI":"10.1101\/gad.1.10.1212","article-title":"Establishment and refinement of segmental pattern in the Drosophila embryo: spatial control of engrailed expression by pair-rule genes","volume":"1","author":"DiNardo","year":"1987","journal-title":"Genes Dev"},{"key":"2024121723035232700_DEVELOP_118_3_785C6","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/0092-8674(85)90012-1","article-title":"Development of the embryonic pattern as revealed by accumulation of the nuclear engrailed protein","volume":"43","author":"DiNardo","year":"1985","journal-title":"Cell"},{"key":"2024121723035232700_DEVELOP_118_3_785C7","doi-asserted-by":"publisher","first-page":"604","DOI":"10.1038\/332604a0","article-title":"Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis","volume":"332","author":"DiNardo","year":"1988","journal-title":"Nature"},{"key":"2024121723035232700_DEVELOP_118_3_785C8","first-page":"981995","article-title":"Complementary patterns of evenskipped and fushi tarazu involve their differential regulation by a common set of segmentation genes in Drosophila","volume":"2","author":"Frasch","year":"1987","journal-title":"Genes Dev"},{"key":"2024121723035232700_DEVELOP_118_3_785C9","doi-asserted-by":"publisher","first-page":"749","DOI":"10.1002\/j.1460-2075.1987.tb04817.x","article-title":"Characterization and localization of the even-skipped protein of Drosophila","volume":"6","author":"Frasch","year":"1987","journal-title":"EMBO J"},{"key":"2024121723035232700_DEVELOP_118_3_785C10","doi-asserted-by":"publisher","first-page":"1824","DOI":"10.1101\/gad.2.12b.1824","article-title":"Molecular analysis of even-skipped mutants in Drosophila development","volume":"2","author":"Frasch","year":"1988","journal-title":"Genes Dev"},{"key":"2024121723035232700_DEVELOP_118_3_785C11","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1016\/0012-1606(85)90459-2","article-title":"The localized requirements for a gene affecting segmentation in Drosophila: analysis of larvae mosaic for runt","volume":"109","author":"Gergen","year":"1985","journal-title":"Dev. 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