Regulation of Numb during planar cell polarity establishment in the Drosophila eye
The establishment of planar cell polarity (PCP) in the Drosophila eye requires correct specification of the R3/R4 pair of photoreceptor cells, determined by a Frizzled mediated signaling event that specifies R3 and induces Delta to activate Notch signaling in the neighboring cell, specifying it as R...
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Veröffentlicht in: | Mechanisms of development 2019-12, Vol.160, p.103583-103583, Article 103583 |
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description | The establishment of planar cell polarity (PCP) in the Drosophila eye requires correct specification of the R3/R4 pair of photoreceptor cells, determined by a Frizzled mediated signaling event that specifies R3 and induces Delta to activate Notch signaling in the neighboring cell, specifying it as R4. Here, we investigated the role of the Notch signaling negative regulator Numb in the specification of R3/R4 fates and PCP establishment in the Drosophila eye. We observed that Numb is transiently upregulated in R3 at the time of R3/R4 specification. This regulation of Numb levels in developing photoreceptors occurs at the post-transcriptional level and is dependent on Dishevelled, an effector of Frizzled signaling, and Lethal Giant Larva. We detected PCP defects in cells homozygous for numb15, but these defects were due to a loss of function mutation in fat (fatQ805⁎) being present in the numb15 chromosome. However, mosaic overexpression of Numb in R4 precursors (only) caused PCP defects and numb loss-of-function alleles had a modifying effect on the defects found in a hypomorphic dishevelled mutation. Our results suggest that Numb levels are upregulated to reinforce the bias of Notch signaling activation in the R3/R4 pair, two post-mitotic cells that are not specified by asymmetric cell division.
•Numb is upregulated in R3 during PCP establishment in the Drosophila larval eye.•Mosaic overexpression of Numb results in PCP defects.•Numb levels are regulated by Lgl in the Drosophila larval eye.•The numb15 chromosome contains a non-sense mutation in fat (ft). |
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•Numb is upregulated in R3 during PCP establishment in the Drosophila larval eye.•Mosaic overexpression of Numb results in PCP defects.•Numb levels are regulated by Lgl in the Drosophila larval eye.•The numb15 chromosome contains a non-sense mutation in fat (ft).</description><identifier>ISSN: 0925-4773</identifier><identifier>EISSN: 1872-6356</identifier><identifier>DOI: 10.1016/j.mod.2019.103583</identifier><identifier>PMID: 31678471</identifier><language>eng</language><publisher>Ireland: Elsevier B.V</publisher><subject>Animals ; Cell Polarity ; Chromosomes - genetics ; Development Biology ; Drosophila eye development ; Drosophila melanogaster - cytology ; Drosophila melanogaster - genetics ; Drosophila melanogaster - metabolism ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Embryology and Organogenesis ; Eye - cytology ; Eye - metabolism ; Fat ; Gene Expression Regulation, Developmental ; Juvenile Hormones - metabolism ; Life Sciences ; Male ; Mutation - genetics ; Numb ; Phenotype ; Planar cell polarity ; Up-Regulation - genetics</subject><ispartof>Mechanisms of development, 2019-12, Vol.160, p.103583-103583, Article 103583</ispartof><rights>2019 Elsevier B.V.</rights><rights>Copyright © 2019 Elsevier B.V. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c485t-72794c6cf4b70f19812a787396da1d423fe046c79b99e95023c1377c2750823</citedby><cites>FETCH-LOGICAL-c485t-72794c6cf4b70f19812a787396da1d423fe046c79b99e95023c1377c2750823</cites><orcidid>0000-0003-4710-8185</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S092547731930139X$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31678471$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04895172$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Domingos, Pedro M.</creatorcontrib><creatorcontrib>Jenny, Andreas</creatorcontrib><creatorcontrib>Combie, Keon F.</creatorcontrib><creatorcontrib>del Alamo, David</creatorcontrib><creatorcontrib>Mlodzik, Marek</creatorcontrib><creatorcontrib>Steller, Hermann</creatorcontrib><creatorcontrib>Mollereau, Bertrand</creatorcontrib><title>Regulation of Numb during planar cell polarity establishment in the Drosophila eye</title><title>Mechanisms of development</title><addtitle>Mech Dev</addtitle><description>The establishment of planar cell polarity (PCP) in the Drosophila eye requires correct specification of the R3/R4 pair of photoreceptor cells, determined by a Frizzled mediated signaling event that specifies R3 and induces Delta to activate Notch signaling in the neighboring cell, specifying it as R4. Here, we investigated the role of the Notch signaling negative regulator Numb in the specification of R3/R4 fates and PCP establishment in the Drosophila eye. We observed that Numb is transiently upregulated in R3 at the time of R3/R4 specification. This regulation of Numb levels in developing photoreceptors occurs at the post-transcriptional level and is dependent on Dishevelled, an effector of Frizzled signaling, and Lethal Giant Larva. We detected PCP defects in cells homozygous for numb15, but these defects were due to a loss of function mutation in fat (fatQ805⁎) being present in the numb15 chromosome. However, mosaic overexpression of Numb in R4 precursors (only) caused PCP defects and numb loss-of-function alleles had a modifying effect on the defects found in a hypomorphic dishevelled mutation. Our results suggest that Numb levels are upregulated to reinforce the bias of Notch signaling activation in the R3/R4 pair, two post-mitotic cells that are not specified by asymmetric cell division.
•Numb is upregulated in R3 during PCP establishment in the Drosophila larval eye.•Mosaic overexpression of Numb results in PCP defects.•Numb levels are regulated by Lgl in the Drosophila larval eye.•The numb15 chromosome contains a non-sense mutation in fat (ft).</description><subject>Animals</subject><subject>Cell Polarity</subject><subject>Chromosomes - genetics</subject><subject>Development Biology</subject><subject>Drosophila eye development</subject><subject>Drosophila melanogaster - cytology</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Embryology and Organogenesis</subject><subject>Eye - cytology</subject><subject>Eye - metabolism</subject><subject>Fat</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Juvenile Hormones - metabolism</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Mutation - genetics</subject><subject>Numb</subject><subject>Phenotype</subject><subject>Planar cell polarity</subject><subject>Up-Regulation - genetics</subject><issn>0925-4773</issn><issn>1872-6356</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kcGP1CAYxYnRuOPqH-DFcNRDRz6gUGJislld12SiyeqdUEpnmLSlQjvJ_PfSdHejHjwR4PfeB-8h9BrIFgiI98dtH5otJaDynpUVe4I2UElaCFaKp2hDFC0LLiW7QC9SOhJCAAQ8RxcMhKy4hA26u3P7uTOTDwMOLf429zVu5uiHPR47M5iIres6PIbORD-dsUuTqTufDr0bJuwHPB0c_hRDCuPBdwa7s3uJnrWmS-7V_XqJftx8_nl9W-y-f_l6fbUrLK_KqZBUKm6FbXktSQuqAmpkJZkSjYGGU9Y6woWVqlbKqZJQZoFJaaksSUXZJfq4uo5z3bvG5udE0-kx-t7Esw7G679vBn_Q-3DSQlWEwWLwbjU4_CO7vdrp5YzwSpUg6Qky-_Z-WAy_5pyB7n1agjGDC3PSlAEoKrjiGYUVtTmUFF376A1EL63po86t6aU1vbaWNW_-_Muj4qGmDHxYAZfzPHkXdbLeDdY1Pjo76Sb4_9j_BhFYp0c</recordid><startdate>20191201</startdate><enddate>20191201</enddate><creator>Domingos, Pedro M.</creator><creator>Jenny, Andreas</creator><creator>Combie, Keon F.</creator><creator>del Alamo, David</creator><creator>Mlodzik, Marek</creator><creator>Steller, Hermann</creator><creator>Mollereau, Bertrand</creator><general>Elsevier B.V</general><general>Elsevier</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4710-8185</orcidid></search><sort><creationdate>20191201</creationdate><title>Regulation of Numb during planar cell polarity establishment in the Drosophila eye</title><author>Domingos, Pedro M. ; Jenny, Andreas ; Combie, Keon F. ; del Alamo, David ; Mlodzik, Marek ; Steller, Hermann ; Mollereau, Bertrand</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c485t-72794c6cf4b70f19812a787396da1d423fe046c79b99e95023c1377c2750823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Cell Polarity</topic><topic>Chromosomes - genetics</topic><topic>Development Biology</topic><topic>Drosophila eye development</topic><topic>Drosophila melanogaster - cytology</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila melanogaster - metabolism</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>Embryology and Organogenesis</topic><topic>Eye - cytology</topic><topic>Eye - metabolism</topic><topic>Fat</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Juvenile Hormones - metabolism</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Mutation - genetics</topic><topic>Numb</topic><topic>Phenotype</topic><topic>Planar cell polarity</topic><topic>Up-Regulation - genetics</topic><toplevel>online_resources</toplevel><creatorcontrib>Domingos, Pedro M.</creatorcontrib><creatorcontrib>Jenny, Andreas</creatorcontrib><creatorcontrib>Combie, Keon F.</creatorcontrib><creatorcontrib>del Alamo, David</creatorcontrib><creatorcontrib>Mlodzik, Marek</creatorcontrib><creatorcontrib>Steller, Hermann</creatorcontrib><creatorcontrib>Mollereau, Bertrand</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Mechanisms of development</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Domingos, Pedro M.</au><au>Jenny, Andreas</au><au>Combie, Keon F.</au><au>del Alamo, David</au><au>Mlodzik, Marek</au><au>Steller, Hermann</au><au>Mollereau, Bertrand</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of Numb during planar cell polarity establishment in the Drosophila eye</atitle><jtitle>Mechanisms of development</jtitle><addtitle>Mech Dev</addtitle><date>2019-12-01</date><risdate>2019</risdate><volume>160</volume><spage>103583</spage><epage>103583</epage><pages>103583-103583</pages><artnum>103583</artnum><issn>0925-4773</issn><eissn>1872-6356</eissn><abstract>The establishment of planar cell polarity (PCP) in the Drosophila eye requires correct specification of the R3/R4 pair of photoreceptor cells, determined by a Frizzled mediated signaling event that specifies R3 and induces Delta to activate Notch signaling in the neighboring cell, specifying it as R4. Here, we investigated the role of the Notch signaling negative regulator Numb in the specification of R3/R4 fates and PCP establishment in the Drosophila eye. We observed that Numb is transiently upregulated in R3 at the time of R3/R4 specification. This regulation of Numb levels in developing photoreceptors occurs at the post-transcriptional level and is dependent on Dishevelled, an effector of Frizzled signaling, and Lethal Giant Larva. We detected PCP defects in cells homozygous for numb15, but these defects were due to a loss of function mutation in fat (fatQ805⁎) being present in the numb15 chromosome. However, mosaic overexpression of Numb in R4 precursors (only) caused PCP defects and numb loss-of-function alleles had a modifying effect on the defects found in a hypomorphic dishevelled mutation. Our results suggest that Numb levels are upregulated to reinforce the bias of Notch signaling activation in the R3/R4 pair, two post-mitotic cells that are not specified by asymmetric cell division.
•Numb is upregulated in R3 during PCP establishment in the Drosophila larval eye.•Mosaic overexpression of Numb results in PCP defects.•Numb levels are regulated by Lgl in the Drosophila larval eye.•The numb15 chromosome contains a non-sense mutation in fat (ft).</abstract><cop>Ireland</cop><pub>Elsevier B.V</pub><pmid>31678471</pmid><doi>10.1016/j.mod.2019.103583</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-4710-8185</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Cell Polarity Chromosomes - genetics Development Biology Drosophila eye development Drosophila melanogaster - cytology Drosophila melanogaster - genetics Drosophila melanogaster - metabolism Drosophila Proteins - genetics Drosophila Proteins - metabolism Embryology and Organogenesis Eye - cytology Eye - metabolism Fat Gene Expression Regulation, Developmental Juvenile Hormones - metabolism Life Sciences Male Mutation - genetics Numb Phenotype Planar cell polarity Up-Regulation - genetics |
title | Regulation of Numb during planar cell polarity establishment in the Drosophila eye |
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