{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,19]],"date-time":"2025-12-19T21:38:32Z","timestamp":1766180312196},"reference-count":56,"publisher":"The Company of Biologists","issue":"17","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2010,9,1]]},"abstract":"<jats:p>The abdomen of adult Drosophila bears mechanosensory bristles with axons that connect directly to the CNS, each hemisegment contributing a separate nerve bundle. Here, we alter the amount of Engrailed protein and manipulate the Hedgehog signalling pathway in clones of cells to study their effects on nerve pathfinding within the peripheral nervous system. We find that high levels of Engrailed make the epidermal cells inhospitable to bristle neurons; sensory axons that are too near these cells are either deflected or fail to extend properly or at all. We then searched for the engrailed-dependent agent responsible for these repellent properties. We found slit to be expressed in the P compartment and, using genetic mosaics, present evidence that Slit is the responsible molecule. Blocking the activity of the three Robo genes (putative receptors for Slit) with RNAi supported this hypothesis. We conclude that, during normal development, gradients of Slit protein repel axons away from compartment boundaries \u2013 in consequence, the bristles from each segment send their nerves to the CNS in separated sets.<\/jats:p>","DOI":"10.1242\/dev.044552","type":"journal-article","created":{"date-parts":[[2010,7,29]],"date-time":"2010-07-29T07:13:52Z","timestamp":1280387632000},"page":"2885-2894","source":"Crossref","is-referenced-by-count":2,"title":["Mechanosensilla in the adult abdomen of<i>Drosophila<\/i>:<i>engrailed<\/i>and<i>slit<\/i>help to corral the peripheral sensory axons into segmental bundles"],"prefix":"10.1242","volume":"137","author":[{"given":"Caroline C. 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Rev. Cell Dev. Biol."},{"key":"2021042605560656000_R11","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/1749-8104-3-12","article-title":"The abdomen of Drosophila: does planar cell polarity orient the neurons of mechanosensory bristles?","volume":"3","author":"Fabre","year":"2008","journal-title":"Neural Dev."},{"key":"2021042605560656000_R12","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/S0896-6273(03)00591-9","article-title":"Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline","volume":"40","author":"Fan","year":"2003","journal-title":"Neuron"},{"key":"2021042605560656000_R13","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/344431a0","article-title":"Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions","volume":"344","author":"Fraser","year":"1990","journal-title":"Nature"},{"key":"2021042605560656000_R14","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/0012-1606(71)90126-6","article-title":"Clonal parameters of tergite development in Drosophila","volume":"26","author":"Garc\u00eda-Bellido","year":"1971","journal-title":"Dev. Biol."},{"key":"2021042605560656000_R15","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1038\/newbio245251a0","article-title":"Developmental compartmentalisation of the wing disk of Drosophila","volume":"245","author":"Garc\u00eda-Bellido","year":"1973","journal-title":"Nat. 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