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Maternal control of the Drosophila dorsal-ventral body axis
The pathway that generates the dorsal–ventral (DV) axis of the Drosophila embryo has been the subject of intense investigation over the previous three decades. The initial asymmetric signal originates during oogenesis by the movement of the oocyte nucleus to an anterior corner of the oocyte, which e...
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Published in: | Wiley interdisciplinary reviews. Developmental biology 2014-09, Vol.3 (5), p.301-330 |
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description | The pathway that generates the dorsal–ventral (DV) axis of the Drosophila embryo has been the subject of intense investigation over the previous three decades. The initial asymmetric signal originates during oogenesis by the movement of the oocyte nucleus to an anterior corner of the oocyte, which establishes DV polarity within the follicle through signaling between Gurken, the Drosophila Transforming Growth Factor (TGF)‐α homologue secreted from the oocyte, and the Drosophila Epidermal Growth Factor Receptor (EGFR) that is expressed by the follicular epithelium cells that envelop the oocyte. Follicle cells that are not exposed to Gurken follow a ventral fate and express Pipe, a sulfotransferase that enzymatically modifies components of the inner vitelline membrane layer of the eggshell, thereby transferring DV spatial information from the follicle to the egg. These ventrally sulfated eggshell proteins comprise a localized cue that directs the ventrally restricted formation of the active Spätzle ligand within the perivitelline space between the eggshell and the embryonic membrane. Spätzle activates Toll, a transmembrane receptor in the embryonic membrane. Transmission of the Toll signal into the embryo leads to the formation of a ventral‐to‐dorsal gradient of the transcription factor Dorsal within the nuclei of the syncytial blastoderm stage embryo. Dorsal controls the spatially specific expression of a large constellation of zygotic target genes, the Dorsal gene regulatory network, along the embryonic DV circumference. This article reviews classic studies and integrates them with the details of more recent work that has advanced our understanding of the complex pathway that establishes Drosophila embryo DV polarity.
This article is categorized under:
Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization
Establishment of Spatial and Temporal Patterns > Gradients
Signaling Pathways > Cell Fate Signaling
Early Embryonic Development > Development to the Basic Body Plan |
doi_str_mv | 10.1002/wdev.138 |
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This article is categorized under:
Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization
Establishment of Spatial and Temporal Patterns > Gradients
Signaling Pathways > Cell Fate Signaling
Early Embryonic Development > Development to the Basic Body Plan</description><identifier>ISSN: 1759-7684</identifier><identifier>EISSN: 1759-7692</identifier><identifier>DOI: 10.1002/wdev.138</identifier><identifier>PMID: 25124754</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Animals ; Blastoderm ; Body Patterning ; Cell fate ; Drosophila ; Drosophila - embryology ; Drosophila - genetics ; Drosophila - metabolism ; Egg shells ; Embryogenesis ; Epidermal growth factor ; Epidermal growth factor receptors ; Epistasis, Genetic ; Epithelium ; Gene Expression Regulation, Developmental ; Gene Regulatory Networks ; Growth factors ; Insects ; Localization ; Nuclei ; Oogenesis ; Polarity ; Signal transduction ; Sulfotransferase ; Transforming growth factor-a ; Vitelline membrane</subject><ispartof>Wiley interdisciplinary reviews. Developmental biology, 2014-09, Vol.3 (5), p.301-330</ispartof><rights>2014 Wiley Periodicals, Inc.</rights><rights>Copyright © 2014 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6368-937b63dbd45a6154f465e806d32839cebc02c97265734913419bc9c32b7b904c3</citedby><cites>FETCH-LOGICAL-c6368-937b63dbd45a6154f465e806d32839cebc02c97265734913419bc9c32b7b904c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25124754$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Stein, David S.</creatorcontrib><creatorcontrib>Stevens, Leslie M.</creatorcontrib><title>Maternal control of the Drosophila dorsal-ventral body axis</title><title>Wiley interdisciplinary reviews. Developmental biology</title><addtitle>WIREs Dev Biol</addtitle><description>The pathway that generates the dorsal–ventral (DV) axis of the Drosophila embryo has been the subject of intense investigation over the previous three decades. The initial asymmetric signal originates during oogenesis by the movement of the oocyte nucleus to an anterior corner of the oocyte, which establishes DV polarity within the follicle through signaling between Gurken, the Drosophila Transforming Growth Factor (TGF)‐α homologue secreted from the oocyte, and the Drosophila Epidermal Growth Factor Receptor (EGFR) that is expressed by the follicular epithelium cells that envelop the oocyte. Follicle cells that are not exposed to Gurken follow a ventral fate and express Pipe, a sulfotransferase that enzymatically modifies components of the inner vitelline membrane layer of the eggshell, thereby transferring DV spatial information from the follicle to the egg. These ventrally sulfated eggshell proteins comprise a localized cue that directs the ventrally restricted formation of the active Spätzle ligand within the perivitelline space between the eggshell and the embryonic membrane. Spätzle activates Toll, a transmembrane receptor in the embryonic membrane. Transmission of the Toll signal into the embryo leads to the formation of a ventral‐to‐dorsal gradient of the transcription factor Dorsal within the nuclei of the syncytial blastoderm stage embryo. Dorsal controls the spatially specific expression of a large constellation of zygotic target genes, the Dorsal gene regulatory network, along the embryonic DV circumference. This article reviews classic studies and integrates them with the details of more recent work that has advanced our understanding of the complex pathway that establishes Drosophila embryo DV polarity.
This article is categorized under:
Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization
Establishment of Spatial and Temporal Patterns > Gradients
Signaling Pathways > Cell Fate Signaling
Early Embryonic Development > Development to the Basic Body Plan</description><subject>Animals</subject><subject>Blastoderm</subject><subject>Body Patterning</subject><subject>Cell fate</subject><subject>Drosophila</subject><subject>Drosophila - embryology</subject><subject>Drosophila - genetics</subject><subject>Drosophila - metabolism</subject><subject>Egg shells</subject><subject>Embryogenesis</subject><subject>Epidermal growth factor</subject><subject>Epidermal growth factor receptors</subject><subject>Epistasis, Genetic</subject><subject>Epithelium</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Regulatory Networks</subject><subject>Growth factors</subject><subject>Insects</subject><subject>Localization</subject><subject>Nuclei</subject><subject>Oogenesis</subject><subject>Polarity</subject><subject>Signal transduction</subject><subject>Sulfotransferase</subject><subject>Transforming growth factor-a</subject><subject>Vitelline membrane</subject><issn>1759-7684</issn><issn>1759-7692</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNqFkV9rUzEYh4MobsyBn0AOeOPNmUneJG-CIMg6V2HTG7WXIScntWeeNl1y2q3f3tTW-gfU3CSQhydvfj9CnjJ6xijlL-_asD5joB-QY4bS1KgMf3g4a3FETnO-oWVppoXQj8kRl4wLlOKYvLp2Q0gL11c-LoYU-ypOq2EWqlGKOS5nXe-qNqbs-nodClDAJrabyt13-Ql5NHV9Dqf7_YR8envx8XxcX324fHf-5qr2CpSuDWCjoG1aIZ1iUkyFkkFT1QLXYHxoPOXeIFcSQRgGgpnGGw-8wcZQ4eGEvN55l6tmHlq_m8MuUzd3aWOj6-zvN4tuZr_EtRXIRbEVwYu9IMXbVciDnXfZh753ixBX2TItJUUE0P9HpQSkQnBW0Od_oDdxtY2yUMYAlLCp-ieFFEFKo_jPZ32JPacwPfyOUbtt2W5btuz7hM9-TeMA_ui0APUOuOv6sPmryE5GF593wj3f5SHcH3iXvlqFgNJO3l_a8YQhXo9GdgzfAEEtvX4</recordid><startdate>201409</startdate><enddate>201409</enddate><creator>Stein, David S.</creator><creator>Stevens, Leslie M.</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><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>7T5</scope><scope>7TM</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><scope>7SS</scope><scope>5PM</scope></search><sort><creationdate>201409</creationdate><title>Maternal control of the Drosophila dorsal-ventral body axis</title><author>Stein, David S. ; Stevens, Leslie M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6368-937b63dbd45a6154f465e806d32839cebc02c97265734913419bc9c32b7b904c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Blastoderm</topic><topic>Body Patterning</topic><topic>Cell fate</topic><topic>Drosophila</topic><topic>Drosophila - embryology</topic><topic>Drosophila - genetics</topic><topic>Drosophila - metabolism</topic><topic>Egg shells</topic><topic>Embryogenesis</topic><topic>Epidermal growth factor</topic><topic>Epidermal growth factor receptors</topic><topic>Epistasis, Genetic</topic><topic>Epithelium</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Regulatory Networks</topic><topic>Growth factors</topic><topic>Insects</topic><topic>Localization</topic><topic>Nuclei</topic><topic>Oogenesis</topic><topic>Polarity</topic><topic>Signal transduction</topic><topic>Sulfotransferase</topic><topic>Transforming growth factor-a</topic><topic>Vitelline membrane</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Stein, David S.</creatorcontrib><creatorcontrib>Stevens, Leslie M.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>Entomology Abstracts (Full archive)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Wiley interdisciplinary reviews. Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Stein, David S.</au><au>Stevens, Leslie M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Maternal control of the Drosophila dorsal-ventral body axis</atitle><jtitle>Wiley interdisciplinary reviews. Developmental biology</jtitle><addtitle>WIREs Dev Biol</addtitle><date>2014-09</date><risdate>2014</risdate><volume>3</volume><issue>5</issue><spage>301</spage><epage>330</epage><pages>301-330</pages><issn>1759-7684</issn><eissn>1759-7692</eissn><abstract>The pathway that generates the dorsal–ventral (DV) axis of the Drosophila embryo has been the subject of intense investigation over the previous three decades. The initial asymmetric signal originates during oogenesis by the movement of the oocyte nucleus to an anterior corner of the oocyte, which establishes DV polarity within the follicle through signaling between Gurken, the Drosophila Transforming Growth Factor (TGF)‐α homologue secreted from the oocyte, and the Drosophila Epidermal Growth Factor Receptor (EGFR) that is expressed by the follicular epithelium cells that envelop the oocyte. Follicle cells that are not exposed to Gurken follow a ventral fate and express Pipe, a sulfotransferase that enzymatically modifies components of the inner vitelline membrane layer of the eggshell, thereby transferring DV spatial information from the follicle to the egg. These ventrally sulfated eggshell proteins comprise a localized cue that directs the ventrally restricted formation of the active Spätzle ligand within the perivitelline space between the eggshell and the embryonic membrane. Spätzle activates Toll, a transmembrane receptor in the embryonic membrane. Transmission of the Toll signal into the embryo leads to the formation of a ventral‐to‐dorsal gradient of the transcription factor Dorsal within the nuclei of the syncytial blastoderm stage embryo. Dorsal controls the spatially specific expression of a large constellation of zygotic target genes, the Dorsal gene regulatory network, along the embryonic DV circumference. This article reviews classic studies and integrates them with the details of more recent work that has advanced our understanding of the complex pathway that establishes Drosophila embryo DV polarity.
This article is categorized under:
Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization
Establishment of Spatial and Temporal Patterns > Gradients
Signaling Pathways > Cell Fate Signaling
Early Embryonic Development > Development to the Basic Body Plan</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>25124754</pmid><doi>10.1002/wdev.138</doi><tpages>30</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Blastoderm Body Patterning Cell fate Drosophila Drosophila - embryology Drosophila - genetics Drosophila - metabolism Egg shells Embryogenesis Epidermal growth factor Epidermal growth factor receptors Epistasis, Genetic Epithelium Gene Expression Regulation, Developmental Gene Regulatory Networks Growth factors Insects Localization Nuclei Oogenesis Polarity Signal transduction Sulfotransferase Transforming growth factor-a Vitelline membrane |
title | Maternal control of the Drosophila dorsal-ventral body axis |
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