Expression and Functional Characterization of Four Aquaporin Water Channels From the European Eel ( Anguilla anguilla )
The European eel is a euryhaline teleost which has been shown to differentially up- and downregulate aquaporin (AQP) water channels in response to changes in environmental salinity. We have characterized the transport properties of four aquaporins localized to osmoregulatory organs – gill, esophagus...
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ftgeorgiasouth:oai:digitalcommons.georgiasouthern.edu:biology-facpubs-1050 2023-09-26T15:09:25+02:00 Expression and Functional Characterization of Four Aquaporin Water Channels From the European Eel ( Anguilla anguilla ) MacIver, Bryce Cutler, Christopher P. Yin, Jia Hill, Miles G. Zeidel, Mark L. Hill, Warren 2009-08-14T07:00:00Z https://digitalcommons.georgiasouthern.edu/biology-facpubs/48 https://doi.org/10.1242/jeb.025882 unknown Digital Commons@Georgia Southern https://digitalcommons.georgiasouthern.edu/biology-facpubs/48 doi:10.1242/jeb.025882 https://doi.org/10.1242/jeb.025882 Department of Biology Faculty Publications Expression Functional characterization Aquaporin water channels European eel Anguilla anguilla Biochemistry Biophysics and Structural Biology Biology text 2009 ftgeorgiasouth https://doi.org/10.1242/jeb.025882 2023-08-27T21:40:49Z The European eel is a euryhaline teleost which has been shown to differentially up- and downregulate aquaporin (AQP) water channels in response to changes in environmental salinity. We have characterized the transport properties of four aquaporins localized to osmoregulatory organs – gill, esophagus, intestine and kidney. By sequence comparison these four AQP orthologs resemble human AQP1 (eel AQP1), AQP3 (eel AQP3) and AQP10 (AQPe). The fourth member is a duplicate form of AQP1 (AQP1dup) thought to arise from a duplication of the teleost genome. Using heterologous expression in Xenopus oocytes we demonstrate that all four eel orthologs transport water and are mercury inhibitable. Eel AQP3 and AQPe also transport urea and glycerol, making them aquaglyceroporins. Eel AQP3 is dramatically inhibited by extracellular acidity (91% and 69% inhibition of water and glycerol transport respectively at pH 6.5) consistent with channel gating by protons. Maximal water flux of eel AQP3 occurred around pH 8.2 – close to the physiological pH of plasma in the eel. Exposure of AQP-expressing oocytes to heavy metals revealed that eel AQP3 is highly sensitive to extracellular nickel and zinc (88.3% and 86.3% inhibition, respectively) but less sensitive to copper (56.4% inhibition). Surprisingly, copper had a stimulatory effect on eel AQP1 (153.7% activity of control). Copper, nickel and zinc did not affect AQP1dup or AQPe. We establish that all four eel AQP orthologs have similar transport profiles to their human counterparts, with eel AQP3 exhibiting some differences in its sensitivity to metals. This is the first investigation of the transport properties and inhibitor sensitivity of salinity-regulated aquaporins from a euryhaline species. Our results indicate a need to further investigate the deleterious effects of metal pollutants on AQP-containing epithelial cells of the gill and gastrointestinal tract at environmentally appropriate concentrations. Text Anguilla anguilla European eel Georgia Southern University: Digital Commons@Georgia Southern Journal of Experimental Biology 212 17 2856 2863 |
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Open Polar |
collection |
Georgia Southern University: Digital Commons@Georgia Southern |
op_collection_id |
ftgeorgiasouth |
language |
unknown |
topic |
Expression Functional characterization Aquaporin water channels European eel Anguilla anguilla Biochemistry Biophysics and Structural Biology Biology |
spellingShingle |
Expression Functional characterization Aquaporin water channels European eel Anguilla anguilla Biochemistry Biophysics and Structural Biology Biology MacIver, Bryce Cutler, Christopher P. Yin, Jia Hill, Miles G. Zeidel, Mark L. Hill, Warren Expression and Functional Characterization of Four Aquaporin Water Channels From the European Eel ( Anguilla anguilla ) |
topic_facet |
Expression Functional characterization Aquaporin water channels European eel Anguilla anguilla Biochemistry Biophysics and Structural Biology Biology |
description |
The European eel is a euryhaline teleost which has been shown to differentially up- and downregulate aquaporin (AQP) water channels in response to changes in environmental salinity. We have characterized the transport properties of four aquaporins localized to osmoregulatory organs – gill, esophagus, intestine and kidney. By sequence comparison these four AQP orthologs resemble human AQP1 (eel AQP1), AQP3 (eel AQP3) and AQP10 (AQPe). The fourth member is a duplicate form of AQP1 (AQP1dup) thought to arise from a duplication of the teleost genome. Using heterologous expression in Xenopus oocytes we demonstrate that all four eel orthologs transport water and are mercury inhibitable. Eel AQP3 and AQPe also transport urea and glycerol, making them aquaglyceroporins. Eel AQP3 is dramatically inhibited by extracellular acidity (91% and 69% inhibition of water and glycerol transport respectively at pH 6.5) consistent with channel gating by protons. Maximal water flux of eel AQP3 occurred around pH 8.2 – close to the physiological pH of plasma in the eel. Exposure of AQP-expressing oocytes to heavy metals revealed that eel AQP3 is highly sensitive to extracellular nickel and zinc (88.3% and 86.3% inhibition, respectively) but less sensitive to copper (56.4% inhibition). Surprisingly, copper had a stimulatory effect on eel AQP1 (153.7% activity of control). Copper, nickel and zinc did not affect AQP1dup or AQPe. We establish that all four eel AQP orthologs have similar transport profiles to their human counterparts, with eel AQP3 exhibiting some differences in its sensitivity to metals. This is the first investigation of the transport properties and inhibitor sensitivity of salinity-regulated aquaporins from a euryhaline species. Our results indicate a need to further investigate the deleterious effects of metal pollutants on AQP-containing epithelial cells of the gill and gastrointestinal tract at environmentally appropriate concentrations. |
format |
Text |
author |
MacIver, Bryce Cutler, Christopher P. Yin, Jia Hill, Miles G. Zeidel, Mark L. Hill, Warren |
author_facet |
MacIver, Bryce Cutler, Christopher P. Yin, Jia Hill, Miles G. Zeidel, Mark L. Hill, Warren |
author_sort |
MacIver, Bryce |
title |
Expression and Functional Characterization of Four Aquaporin Water Channels From the European Eel ( Anguilla anguilla ) |
title_short |
Expression and Functional Characterization of Four Aquaporin Water Channels From the European Eel ( Anguilla anguilla ) |
title_full |
Expression and Functional Characterization of Four Aquaporin Water Channels From the European Eel ( Anguilla anguilla ) |
title_fullStr |
Expression and Functional Characterization of Four Aquaporin Water Channels From the European Eel ( Anguilla anguilla ) |
title_full_unstemmed |
Expression and Functional Characterization of Four Aquaporin Water Channels From the European Eel ( Anguilla anguilla ) |
title_sort |
expression and functional characterization of four aquaporin water channels from the european eel ( anguilla anguilla ) |
publisher |
Digital Commons@Georgia Southern |
publishDate |
2009 |
url |
https://digitalcommons.georgiasouthern.edu/biology-facpubs/48 https://doi.org/10.1242/jeb.025882 |
genre |
Anguilla anguilla European eel |
genre_facet |
Anguilla anguilla European eel |
op_source |
Department of Biology Faculty Publications |
op_relation |
https://digitalcommons.georgiasouthern.edu/biology-facpubs/48 doi:10.1242/jeb.025882 https://doi.org/10.1242/jeb.025882 |
op_doi |
https://doi.org/10.1242/jeb.025882 |
container_title |
Journal of Experimental Biology |
container_volume |
212 |
container_issue |
17 |
container_start_page |
2856 |
op_container_end_page |
2863 |
_version_ |
1778135731904970752 |