Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases
The three Drosophila atypical soluble guanylyl cyclases, Gyc-89Da, Gyc-89Db, and Gyc-88E, have been proposed to act as oxygen detectors mediating behavioral responses to hypoxia. Drosophila larvae mutant in any of these subunits were defective in their hypoxia escape response-a rapid cessation of fe...
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| Veröffentlicht in: | Genetics (Austin) 2010-09, Vol.186 (1), p.183-196 |
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| creator | Vermehren-Schmaedick, Anke Ainsley, Joshua A Johnson, Wayne A Davies, Shireen-A Morton, David B |
| description | The three Drosophila atypical soluble guanylyl cyclases, Gyc-89Da, Gyc-89Db, and Gyc-88E, have been proposed to act as oxygen detectors mediating behavioral responses to hypoxia. Drosophila larvae mutant in any of these subunits were defective in their hypoxia escape response-a rapid cessation of feeding and withdrawal from their food. This response required cGMP and the cyclic nucleotide-gated ion channel, cng, but did not appear to be dependent on either of the cGMP-dependent protein kinases, dg1 and dg2. Specific activation of the Gyc-89Da neurons using channel rhodopsin showed that activation of these neurons was sufficient to trigger the escape behavior. The hypoxia escape response was restored by reintroducing either Gyc-89Da or Gyc-89Db into either Gyc-89Da or Gyc-89Db neurons in either mutation. This suggests that neurons that co-express both Gyc-89Da and Gyc-89Db subunits are primarily responsible for activating this behavior. These include sensory neurons that innervate the terminal sensory cones. Although the roles of Gyc-89Da and Gyc-89Db in the hypoxia escape behavior appeared to be identical, we also showed that changes in larval crawling behavior in response to either hypoxia or hyperoxia differed in their requirements for these two atypical sGCs, with responses to 15% oxygen requiring Gyc-89Da and responses to 19 and 25% requiring Gyc-89Db. For this behavior, the identity of the neurons appeared to be critical in determining the ability to respond appropriately. |
| doi_str_mv | 10.1534/genetics.110.118166 |
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Drosophila larvae mutant in any of these subunits were defective in their hypoxia escape response-a rapid cessation of feeding and withdrawal from their food. This response required cGMP and the cyclic nucleotide-gated ion channel, cng, but did not appear to be dependent on either of the cGMP-dependent protein kinases, dg1 and dg2. Specific activation of the Gyc-89Da neurons using channel rhodopsin showed that activation of these neurons was sufficient to trigger the escape behavior. The hypoxia escape response was restored by reintroducing either Gyc-89Da or Gyc-89Db into either Gyc-89Da or Gyc-89Db neurons in either mutation. This suggests that neurons that co-express both Gyc-89Da and Gyc-89Db subunits are primarily responsible for activating this behavior. These include sensory neurons that innervate the terminal sensory cones. Although the roles of Gyc-89Da and Gyc-89Db in the hypoxia escape behavior appeared to be identical, we also showed that changes in larval crawling behavior in response to either hypoxia or hyperoxia differed in their requirements for these two atypical sGCs, with responses to 15% oxygen requiring Gyc-89Da and responses to 19 and 25% requiring Gyc-89Db. For this behavior, the identity of the neurons appeared to be critical in determining the ability to respond appropriately.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.110.118166</identifier><identifier>PMID: 20592263</identifier><identifier>CODEN: GENTAE</identifier><language>eng</language><publisher>United States: Genetics Society of America</publisher><subject>Amino Acid Sequence ; Animals ; Behavior, Animal ; Cyclic GMP - metabolism ; Cyclic GMP-Dependent Protein Kinases - metabolism ; Down-Regulation ; Drosophila melanogaster - cytology ; Drosophila melanogaster - enzymology ; Drosophila melanogaster - genetics ; Drosophila melanogaster - metabolism ; Gene Expression Regulation, Enzymologic ; Guanylate Cyclase - chemistry ; Guanylate Cyclase - genetics ; Guanylate Cyclase - metabolism ; Hypoxia ; Hypoxia - enzymology ; Investigations ; Ion Channel Gating ; Ion Channels - metabolism ; Kinases ; Larva - cytology ; Larva - enzymology ; Larva - genetics ; Larva - metabolism ; Molecular Sequence Data ; Neurons - metabolism ; Nitric oxide ; Oxygen - metabolism ; Proteins ; Rats ; Scanning electron microscopy ; Solubility ; Studies</subject><ispartof>Genetics (Austin), 2010-09, Vol.186 (1), p.183-196</ispartof><rights>Copyright Genetics Society of America Sep 2010</rights><rights>Copyright © 2010 by the Genetics Society of America 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c497t-88b0747ed0926cc5177fdf3ecd79f46da0bd394c516f2b427dff41ad598928603</citedby><cites>FETCH-LOGICAL-c497t-88b0747ed0926cc5177fdf3ecd79f46da0bd394c516f2b427dff41ad598928603</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20592263$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Vermehren-Schmaedick, Anke</creatorcontrib><creatorcontrib>Ainsley, Joshua A</creatorcontrib><creatorcontrib>Johnson, Wayne A</creatorcontrib><creatorcontrib>Davies, Shireen-A</creatorcontrib><creatorcontrib>Morton, David B</creatorcontrib><title>Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>The three Drosophila atypical soluble guanylyl cyclases, Gyc-89Da, Gyc-89Db, and Gyc-88E, have been proposed to act as oxygen detectors mediating behavioral responses to hypoxia. Drosophila larvae mutant in any of these subunits were defective in their hypoxia escape response-a rapid cessation of feeding and withdrawal from their food. This response required cGMP and the cyclic nucleotide-gated ion channel, cng, but did not appear to be dependent on either of the cGMP-dependent protein kinases, dg1 and dg2. Specific activation of the Gyc-89Da neurons using channel rhodopsin showed that activation of these neurons was sufficient to trigger the escape behavior. The hypoxia escape response was restored by reintroducing either Gyc-89Da or Gyc-89Db into either Gyc-89Da or Gyc-89Db neurons in either mutation. This suggests that neurons that co-express both Gyc-89Da and Gyc-89Db subunits are primarily responsible for activating this behavior. These include sensory neurons that innervate the terminal sensory cones. Although the roles of Gyc-89Da and Gyc-89Db in the hypoxia escape behavior appeared to be identical, we also showed that changes in larval crawling behavior in response to either hypoxia or hyperoxia differed in their requirements for these two atypical sGCs, with responses to 15% oxygen requiring Gyc-89Da and responses to 19 and 25% requiring Gyc-89Db. For this behavior, the identity of the neurons appeared to be critical in determining the ability to respond appropriately.</description><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Behavior, Animal</subject><subject>Cyclic GMP - metabolism</subject><subject>Cyclic GMP-Dependent Protein Kinases - metabolism</subject><subject>Down-Regulation</subject><subject>Drosophila melanogaster - cytology</subject><subject>Drosophila melanogaster - enzymology</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Gene Expression Regulation, Enzymologic</subject><subject>Guanylate Cyclase - chemistry</subject><subject>Guanylate Cyclase - genetics</subject><subject>Guanylate Cyclase - metabolism</subject><subject>Hypoxia</subject><subject>Hypoxia - enzymology</subject><subject>Investigations</subject><subject>Ion Channel Gating</subject><subject>Ion Channels - metabolism</subject><subject>Kinases</subject><subject>Larva - cytology</subject><subject>Larva - enzymology</subject><subject>Larva - genetics</subject><subject>Larva - metabolism</subject><subject>Molecular Sequence Data</subject><subject>Neurons - metabolism</subject><subject>Nitric oxide</subject><subject>Oxygen - metabolism</subject><subject>Proteins</subject><subject>Rats</subject><subject>Scanning electron microscopy</subject><subject>Solubility</subject><subject>Studies</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpdkcuO1DAQRS0EYh7wBUjIYsOqB78SxxskGBhAGokNrK2KXen2yB0HO2mRv8fNPDSwslX31nGVLyGvOLvgjVTvtjjiHFy54McK73jbPiGn3Ci5Ea3kTx_dT8hZKTeMsdY03XNyIlhjRBVOyfYj7uAQUoZIM5YpjQULnRPdrVP6HYCGkX7KqaRpFyLQCPkASCEj3aMPMKOn_UphXqfgKqKkuPQR6XaBcY1rpG51ESryBXk2QCz48u48Jz-vPv-4_Lq5_v7l2-WH641TRs-bruuZVho9M6J1ruFaD36Q6Lw2g2o9sN5Lo6rQDqJXQvthUBx8YzojupbJc_L-ljstfZ3Q4TjX1eyUwx7yahME-68yhp3dpoMVRrFKqIC3d4Ccfi1YZrsPxWGMMGJaitVNfVtxKarzzX_Om7TksW5XTZopVVOqJnlrcvUTS8bhYRTO7DFGex-j5cfK3xhr1-vHWzz03Ocm_wC-wp3O</recordid><startdate>201009</startdate><enddate>201009</enddate><creator>Vermehren-Schmaedick, Anke</creator><creator>Ainsley, Joshua A</creator><creator>Johnson, Wayne A</creator><creator>Davies, Shireen-A</creator><creator>Morton, David B</creator><general>Genetics Society of America</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>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201009</creationdate><title>Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases</title><author>Vermehren-Schmaedick, Anke ; Ainsley, Joshua A ; Johnson, Wayne A ; Davies, Shireen-A ; Morton, David B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c497t-88b0747ed0926cc5177fdf3ecd79f46da0bd394c516f2b427dff41ad598928603</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Behavior, Animal</topic><topic>Cyclic GMP - metabolism</topic><topic>Cyclic GMP-Dependent Protein Kinases - metabolism</topic><topic>Down-Regulation</topic><topic>Drosophila melanogaster - cytology</topic><topic>Drosophila melanogaster - enzymology</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila melanogaster - metabolism</topic><topic>Gene Expression Regulation, Enzymologic</topic><topic>Guanylate Cyclase - chemistry</topic><topic>Guanylate Cyclase - genetics</topic><topic>Guanylate Cyclase - metabolism</topic><topic>Hypoxia</topic><topic>Hypoxia - enzymology</topic><topic>Investigations</topic><topic>Ion Channel Gating</topic><topic>Ion Channels - metabolism</topic><topic>Kinases</topic><topic>Larva - cytology</topic><topic>Larva - enzymology</topic><topic>Larva - genetics</topic><topic>Larva - metabolism</topic><topic>Molecular Sequence Data</topic><topic>Neurons - metabolism</topic><topic>Nitric oxide</topic><topic>Oxygen - metabolism</topic><topic>Proteins</topic><topic>Rats</topic><topic>Scanning electron microscopy</topic><topic>Solubility</topic><topic>Studies</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vermehren-Schmaedick, Anke</creatorcontrib><creatorcontrib>Ainsley, Joshua A</creatorcontrib><creatorcontrib>Johnson, Wayne A</creatorcontrib><creatorcontrib>Davies, Shireen-A</creatorcontrib><creatorcontrib>Morton, David B</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Docstoc</collection><collection>University Readers</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>SciTech Premium Collection</collection><collection>Consumer Health Database (Alumni Edition)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Consumer Health Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vermehren-Schmaedick, Anke</au><au>Ainsley, Joshua A</au><au>Johnson, Wayne A</au><au>Davies, Shireen-A</au><au>Morton, David B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2010-09</date><risdate>2010</risdate><volume>186</volume><issue>1</issue><spage>183</spage><epage>196</epage><pages>183-196</pages><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><coden>GENTAE</coden><abstract>The three Drosophila atypical soluble guanylyl cyclases, Gyc-89Da, Gyc-89Db, and Gyc-88E, have been proposed to act as oxygen detectors mediating behavioral responses to hypoxia. Drosophila larvae mutant in any of these subunits were defective in their hypoxia escape response-a rapid cessation of feeding and withdrawal from their food. This response required cGMP and the cyclic nucleotide-gated ion channel, cng, but did not appear to be dependent on either of the cGMP-dependent protein kinases, dg1 and dg2. Specific activation of the Gyc-89Da neurons using channel rhodopsin showed that activation of these neurons was sufficient to trigger the escape behavior. The hypoxia escape response was restored by reintroducing either Gyc-89Da or Gyc-89Db into either Gyc-89Da or Gyc-89Db neurons in either mutation. This suggests that neurons that co-express both Gyc-89Da and Gyc-89Db subunits are primarily responsible for activating this behavior. These include sensory neurons that innervate the terminal sensory cones. Although the roles of Gyc-89Da and Gyc-89Db in the hypoxia escape behavior appeared to be identical, we also showed that changes in larval crawling behavior in response to either hypoxia or hyperoxia differed in their requirements for these two atypical sGCs, with responses to 15% oxygen requiring Gyc-89Da and responses to 19 and 25% requiring Gyc-89Db. For this behavior, the identity of the neurons appeared to be critical in determining the ability to respond appropriately.</abstract><cop>United States</cop><pub>Genetics Society of America</pub><pmid>20592263</pmid><doi>10.1534/genetics.110.118166</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
| subjects | Amino Acid Sequence Animals Behavior, Animal Cyclic GMP - metabolism Cyclic GMP-Dependent Protein Kinases - metabolism Down-Regulation Drosophila melanogaster - cytology Drosophila melanogaster - enzymology Drosophila melanogaster - genetics Drosophila melanogaster - metabolism Gene Expression Regulation, Enzymologic Guanylate Cyclase - chemistry Guanylate Cyclase - genetics Guanylate Cyclase - metabolism Hypoxia Hypoxia - enzymology Investigations Ion Channel Gating Ion Channels - metabolism Kinases Larva - cytology Larva - enzymology Larva - genetics Larva - metabolism Molecular Sequence Data Neurons - metabolism Nitric oxide Oxygen - metabolism Proteins Rats Scanning electron microscopy Solubility Studies |
| title | Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases |
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