A matrix metalloproteinase mediates airway remodeling in Drosophila
Organ size typically increases dramatically during juvenile growth. This growth presents a fundamental tension, as organs need resiliency to resist stresses while still maintaining plasticity to accommodate growth. The extracellular matrix (ECM) is central to providing resiliency, but how ECM is rem...
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Veröffentlicht in: | Developmental biology 2010-08, Vol.344 (2), p.772-783 |
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creator | Glasheen, Bernadette M. Robbins, Renée M. Piette, Caitlin Beitel, Greg J. Page-McCaw, Andrea |
description | Organ size typically increases dramatically during juvenile growth. This growth presents a fundamental tension, as organs need resiliency to resist stresses while still maintaining plasticity to accommodate growth. The extracellular matrix (ECM) is central to providing resiliency, but how ECM is remodeled to accommodate growth is poorly understood. We investigated remodeling of
Drosophila respiratory tubes (tracheae) that elongate continually during larval growth, despite being lined with a rigid cuticular ECM. Cuticle is initially deposited with a characteristic pattern of repeating ridges and valleys known as taenidia. We find that for tubes to elongate, the extracellular protease Mmp1 is required for expansion of ECM between the taenidial ridges during each intermolt period. Mmp1 protein localizes in periodically spaced puncta that are in register with the taenidial spacing. Mmp1 also degrades old cuticle at molts, promotes apical membrane expansion in larval tracheae, and promotes tube elongation in embryonic tracheae. Whereas work in other developmental systems has demonstrated that MMPs are required for axial elongation occurring in localized growth zones, this study demonstrates that MMPs can also mediate interstitial matrix remodeling during growth of an organ system. |
doi_str_mv | 10.1016/j.ydbio.2010.05.504 |
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Drosophila respiratory tubes (tracheae) that elongate continually during larval growth, despite being lined with a rigid cuticular ECM. Cuticle is initially deposited with a characteristic pattern of repeating ridges and valleys known as taenidia. We find that for tubes to elongate, the extracellular protease Mmp1 is required for expansion of ECM between the taenidial ridges during each intermolt period. Mmp1 protein localizes in periodically spaced puncta that are in register with the taenidial spacing. Mmp1 also degrades old cuticle at molts, promotes apical membrane expansion in larval tracheae, and promotes tube elongation in embryonic tracheae. Whereas work in other developmental systems has demonstrated that MMPs are required for axial elongation occurring in localized growth zones, this study demonstrates that MMPs can also mediate interstitial matrix remodeling during growth of an organ system.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2010.05.504</identifier><identifier>PMID: 20513443</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Airway Remodeling ; Animals ; Chromium ; Cuticle ; Drosophila ; Drosophila - embryology ; Drosophila - metabolism ; Embryo, Nonmammalian ; Extracellular matrix ; Extracellular Matrix - metabolism ; Fusion cell ; Larva - metabolism ; Matrix metalloproteinases (MMPs) ; Matrix Metalloproteinases - metabolism ; Molting ; Remodeling ; Respiratory System - metabolism ; Trachea - embryology ; Trachea - metabolism ; Tracheae ; Tube elongation</subject><ispartof>Developmental biology, 2010-08, Vol.344 (2), p.772-783</ispartof><rights>2010 Elsevier Inc.</rights><rights>Copyright 2010 Elsevier Inc. All rights reserved.</rights><rights>2010 Elsevier Inc. All rights reserved. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c556t-686c1d034d8dc1945394afcedad1968cf31ccb040cd2104a8acf254cc5a431a03</citedby><cites>FETCH-LOGICAL-c556t-686c1d034d8dc1945394afcedad1968cf31ccb040cd2104a8acf254cc5a431a03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0012160610008079$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20513443$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Glasheen, Bernadette M.</creatorcontrib><creatorcontrib>Robbins, Renée M.</creatorcontrib><creatorcontrib>Piette, Caitlin</creatorcontrib><creatorcontrib>Beitel, Greg J.</creatorcontrib><creatorcontrib>Page-McCaw, Andrea</creatorcontrib><title>A matrix metalloproteinase mediates airway remodeling in Drosophila</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><description>Organ size typically increases dramatically during juvenile growth. This growth presents a fundamental tension, as organs need resiliency to resist stresses while still maintaining plasticity to accommodate growth. The extracellular matrix (ECM) is central to providing resiliency, but how ECM is remodeled to accommodate growth is poorly understood. We investigated remodeling of
Drosophila respiratory tubes (tracheae) that elongate continually during larval growth, despite being lined with a rigid cuticular ECM. Cuticle is initially deposited with a characteristic pattern of repeating ridges and valleys known as taenidia. We find that for tubes to elongate, the extracellular protease Mmp1 is required for expansion of ECM between the taenidial ridges during each intermolt period. Mmp1 protein localizes in periodically spaced puncta that are in register with the taenidial spacing. Mmp1 also degrades old cuticle at molts, promotes apical membrane expansion in larval tracheae, and promotes tube elongation in embryonic tracheae. Whereas work in other developmental systems has demonstrated that MMPs are required for axial elongation occurring in localized growth zones, this study demonstrates that MMPs can also mediate interstitial matrix remodeling during growth of an organ system.</description><subject>Airway Remodeling</subject><subject>Animals</subject><subject>Chromium</subject><subject>Cuticle</subject><subject>Drosophila</subject><subject>Drosophila - embryology</subject><subject>Drosophila - metabolism</subject><subject>Embryo, Nonmammalian</subject><subject>Extracellular matrix</subject><subject>Extracellular Matrix - metabolism</subject><subject>Fusion cell</subject><subject>Larva - metabolism</subject><subject>Matrix metalloproteinases (MMPs)</subject><subject>Matrix Metalloproteinases - metabolism</subject><subject>Molting</subject><subject>Remodeling</subject><subject>Respiratory System - metabolism</subject><subject>Trachea - embryology</subject><subject>Trachea - metabolism</subject><subject>Tracheae</subject><subject>Tube elongation</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU9v1DAQxS0EareFT4CEcuOU7UxsZ5MDSNX2H1IlLiBxs2btSetVEi92tu1-e1y2reACJ0vj37yZeU-I9whzBKxP1vOdW_kwryBXQM81qFdihtDqUtfqx2sxA8CqxBrqQ3GU0hoAZNPIA3FYgUaplJyJ5Wkx0BT9QzHwRH0fNjFM7EdKnCvO08SpIB_vaVdEHoLj3o83hR-LsxhS2Nz6nt6KNx31id89vcfi-8X5t-VVef318svy9Lq0WtdTWTe1RQdSucZZbJWWraLOsiOHbd3YTqK1K1BgXYWgqCHbVVpZq0lJJJDH4vNed7Nd5d0sj1Ok3myiHyjuTCBv_v4Z_a25CXemalFV2GSBj08CMfzccprM4JPlvqeRwzaZhVZNqxAW_yczWKlFi5mUe9JmP1Lk7mUfBPOYk1mb3zmZx5wMaJNzyl0f_jzlpec5mAx82gOcDb3zHE2ynsfslo9sJ-OC_-eAX_toptg</recordid><startdate>20100815</startdate><enddate>20100815</enddate><creator>Glasheen, Bernadette M.</creator><creator>Robbins, Renée M.</creator><creator>Piette, Caitlin</creator><creator>Beitel, Greg J.</creator><creator>Page-McCaw, Andrea</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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>7X8</scope><scope>7SS</scope><scope>5PM</scope></search><sort><creationdate>20100815</creationdate><title>A matrix metalloproteinase mediates airway remodeling in Drosophila</title><author>Glasheen, Bernadette M. ; Robbins, Renée M. ; Piette, Caitlin ; Beitel, Greg J. ; Page-McCaw, Andrea</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c556t-686c1d034d8dc1945394afcedad1968cf31ccb040cd2104a8acf254cc5a431a03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Airway Remodeling</topic><topic>Animals</topic><topic>Chromium</topic><topic>Cuticle</topic><topic>Drosophila</topic><topic>Drosophila - embryology</topic><topic>Drosophila - metabolism</topic><topic>Embryo, Nonmammalian</topic><topic>Extracellular matrix</topic><topic>Extracellular Matrix - metabolism</topic><topic>Fusion cell</topic><topic>Larva - metabolism</topic><topic>Matrix metalloproteinases (MMPs)</topic><topic>Matrix Metalloproteinases - metabolism</topic><topic>Molting</topic><topic>Remodeling</topic><topic>Respiratory System - metabolism</topic><topic>Trachea - embryology</topic><topic>Trachea - metabolism</topic><topic>Tracheae</topic><topic>Tube elongation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Glasheen, Bernadette M.</creatorcontrib><creatorcontrib>Robbins, Renée M.</creatorcontrib><creatorcontrib>Piette, Caitlin</creatorcontrib><creatorcontrib>Beitel, Greg J.</creatorcontrib><creatorcontrib>Page-McCaw, Andrea</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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>Entomology Abstracts (Full archive)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Glasheen, Bernadette M.</au><au>Robbins, Renée M.</au><au>Piette, Caitlin</au><au>Beitel, Greg J.</au><au>Page-McCaw, Andrea</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A matrix metalloproteinase mediates airway remodeling in Drosophila</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2010-08-15</date><risdate>2010</risdate><volume>344</volume><issue>2</issue><spage>772</spage><epage>783</epage><pages>772-783</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><abstract>Organ size typically increases dramatically during juvenile growth. This growth presents a fundamental tension, as organs need resiliency to resist stresses while still maintaining plasticity to accommodate growth. The extracellular matrix (ECM) is central to providing resiliency, but how ECM is remodeled to accommodate growth is poorly understood. We investigated remodeling of
Drosophila respiratory tubes (tracheae) that elongate continually during larval growth, despite being lined with a rigid cuticular ECM. Cuticle is initially deposited with a characteristic pattern of repeating ridges and valleys known as taenidia. We find that for tubes to elongate, the extracellular protease Mmp1 is required for expansion of ECM between the taenidial ridges during each intermolt period. Mmp1 protein localizes in periodically spaced puncta that are in register with the taenidial spacing. Mmp1 also degrades old cuticle at molts, promotes apical membrane expansion in larval tracheae, and promotes tube elongation in embryonic tracheae. Whereas work in other developmental systems has demonstrated that MMPs are required for axial elongation occurring in localized growth zones, this study demonstrates that MMPs can also mediate interstitial matrix remodeling during growth of an organ system.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>20513443</pmid><doi>10.1016/j.ydbio.2010.05.504</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Airway Remodeling Animals Chromium Cuticle Drosophila Drosophila - embryology Drosophila - metabolism Embryo, Nonmammalian Extracellular matrix Extracellular Matrix - metabolism Fusion cell Larva - metabolism Matrix metalloproteinases (MMPs) Matrix Metalloproteinases - metabolism Molting Remodeling Respiratory System - metabolism Trachea - embryology Trachea - metabolism Tracheae Tube elongation |
title | A matrix metalloproteinase mediates airway remodeling in Drosophila |
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