Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise
Autor(a) principal: | |
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Data de Publicação: | 2009 |
Outros Autores: | , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional do INPA |
Texto Completo: | https://repositorio.inpa.gov.br/handle/1/15045 |
Resumo: | Earlier studies demonstrated that oscars, endemic to ion-poor Amazonian waters, are extremely hypoxia tolerant, and exhibit a marked reduction in active unidirectional Na+ uptake rate (measured directly) but unchanged net Na+ balance during acute exposure to low Po2, indicating a comparable reduction in whole body Na+ efflux rate. However, branchial O2 transfer factor does not fall. The present study focused on the nature of the efflux reduction in the face of maintained gill O 2 permeability. Direct measurements of 22Na appearance in the water from bladder-catheterized fish confirmed a rapid 55% fall in unidirectional Na+ efflux rate across the gills upon acute exposure to hypoxia (PO2=10-20torr; 1 torr=133.3 Pa), which was quickly reversed upon return to normoxia. An exchange diffusion mechanism for Na + is not present, so the reduction in efflux was not directly linked to the reduction in Na+ influx. A quickly developing bradycardia occurred during hypoxia. Transepithelial potential, which was sensitive to water [Ca2+], became markedly less negative during hypoxia and was restored upon return to normoxia. Ammonia excretion, net K+ loss rates, and 3H2O exchange rates (diffusive water efflux rates) across the gills fell by 55-75% during hypoxia, with recovery during normoxia. Osmotic permeability to water also declined, but the fall (30%) was less than that in diffusive water permeability (70%). In total, these observations indicate a reduction in gill transcellular permeability during hypoxia, a conclusion supported by unchanged branchial efflux rates of the paracellular marker [3H]PEG-4000 during hypoxia and normoxic recovery. At the kidney, glomerular filtration rate, urine flow rate, and tubular Na+ reabsorption rate fell in parallel by 70% during hypoxia, facilitating additional reductions in costs and in urinary Na+, K+ and ammonia excretion rates. Scanning electron microscopy of the gill epithelium revealed no remodelling at a macro-level, but pronounced changes in surface morphology. Under normoxia, mitochondria-rich cells were exposed only through small apical crypts, and these decreased in number by 47% and in individual area by 65% during 3 h hypoxia. We suggest that a rapid closure of transcellular channels, perhaps effected by pavement cell coverage of the crypts, allows conservation of ions and reduction of ionoregulatory costs without compromise of O2 exchange capacity during acute hypoxia, a response very different from the traditional osmorespiratory compromise. |
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Wood, Chris M.Iftikar, Fathima I.Scott, Graham R.Boeck, Gudrun deSloman, Katherine A.Matey, Victoria E.Domingos, Fabíola Xochilt ValdezDuarte, Rafael MendonçaAlmeida-Val, Vera Maria FonsecaVal, Adalberto Luis2020-05-07T14:02:11Z2020-05-07T14:02:11Z2009https://repositorio.inpa.gov.br/handle/1/1504510.1242/jeb.028464Earlier studies demonstrated that oscars, endemic to ion-poor Amazonian waters, are extremely hypoxia tolerant, and exhibit a marked reduction in active unidirectional Na+ uptake rate (measured directly) but unchanged net Na+ balance during acute exposure to low Po2, indicating a comparable reduction in whole body Na+ efflux rate. However, branchial O2 transfer factor does not fall. The present study focused on the nature of the efflux reduction in the face of maintained gill O 2 permeability. Direct measurements of 22Na appearance in the water from bladder-catheterized fish confirmed a rapid 55% fall in unidirectional Na+ efflux rate across the gills upon acute exposure to hypoxia (PO2=10-20torr; 1 torr=133.3 Pa), which was quickly reversed upon return to normoxia. An exchange diffusion mechanism for Na + is not present, so the reduction in efflux was not directly linked to the reduction in Na+ influx. A quickly developing bradycardia occurred during hypoxia. Transepithelial potential, which was sensitive to water [Ca2+], became markedly less negative during hypoxia and was restored upon return to normoxia. Ammonia excretion, net K+ loss rates, and 3H2O exchange rates (diffusive water efflux rates) across the gills fell by 55-75% during hypoxia, with recovery during normoxia. Osmotic permeability to water also declined, but the fall (30%) was less than that in diffusive water permeability (70%). In total, these observations indicate a reduction in gill transcellular permeability during hypoxia, a conclusion supported by unchanged branchial efflux rates of the paracellular marker [3H]PEG-4000 during hypoxia and normoxic recovery. At the kidney, glomerular filtration rate, urine flow rate, and tubular Na+ reabsorption rate fell in parallel by 70% during hypoxia, facilitating additional reductions in costs and in urinary Na+, K+ and ammonia excretion rates. Scanning electron microscopy of the gill epithelium revealed no remodelling at a macro-level, but pronounced changes in surface morphology. Under normoxia, mitochondria-rich cells were exposed only through small apical crypts, and these decreased in number by 47% and in individual area by 65% during 3 h hypoxia. We suggest that a rapid closure of transcellular channels, perhaps effected by pavement cell coverage of the crypts, allows conservation of ions and reduction of ionoregulatory costs without compromise of O2 exchange capacity during acute hypoxia, a response very different from the traditional osmorespiratory compromise.Volume 212, Número 12, Pags. 1949-1964Attribution-NonCommercial-NoDerivs 3.0 Brazilhttp://creativecommons.org/licenses/by-nc-nd/3.0/br/info:eu-repo/semantics/openAccessAmmoniaMacrogol DerivativeOxygenPotassiumSodiumWaterAnimalsBreathingCell HypoxiaCichlidCytologyDiffusionGillGlomerulus Filtration RateHeart RateKidneyMetabolismOsmosisPermeabilityPhysiologyUrineAmmoniaAnimalCell HypoxiaCichlidsDiffusionGillsGlomerular Filtration RateHeart RateKidneyOsmosisOxygenPermeabilityPolyethylene GlycolsPotassiumRespirationSodiumWaterAstronotusAstronotus OcellatusRegulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromiseinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleJournal of Experimental Biologyengreponame:Repositório Institucional do INPAinstname:Instituto Nacional de Pesquisas da Amazônia (INPA)instacron:INPAORIGINALartigo-inpa.pdfapplication/pdf1206709https://repositorio.inpa.gov.br/bitstream/1/15045/1/artigo-inpa.pdf0d6fffefb1dc710e99350670a44060a8MD51CC-LICENSElicense_rdfapplication/octet-stream914https://repositorio.inpa.gov.br/bitstream/1/15045/2/license_rdf4d2950bda3d176f570a9f8b328dfbbefMD521/150452020-07-14 10:42:02.536oai:repositorio:1/15045Repositório de PublicaçõesPUBhttps://repositorio.inpa.gov.br/oai/requestopendoar:2020-07-14T14:42:02Repositório Institucional do INPA - Instituto Nacional de Pesquisas da Amazônia (INPA)false |
dc.title.en.fl_str_mv |
Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise |
title |
Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise |
spellingShingle |
Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise Wood, Chris M. Ammonia Macrogol Derivative Oxygen Potassium Sodium Water Animals Breathing Cell Hypoxia Cichlid Cytology Diffusion Gill Glomerulus Filtration Rate Heart Rate Kidney Metabolism Osmosis Permeability Physiology Urine Ammonia Animal Cell Hypoxia Cichlids Diffusion Gills Glomerular Filtration Rate Heart Rate Kidney Osmosis Oxygen Permeability Polyethylene Glycols Potassium Respiration Sodium Water Astronotus Astronotus Ocellatus |
title_short |
Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise |
title_full |
Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise |
title_fullStr |
Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise |
title_full_unstemmed |
Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise |
title_sort |
Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): New angles to the osmorespiratory compromise |
author |
Wood, Chris M. |
author_facet |
Wood, Chris M. Iftikar, Fathima I. Scott, Graham R. Boeck, Gudrun de Sloman, Katherine A. Matey, Victoria E. Domingos, Fabíola Xochilt Valdez Duarte, Rafael Mendonça Almeida-Val, Vera Maria Fonseca Val, Adalberto Luis |
author_role |
author |
author2 |
Iftikar, Fathima I. Scott, Graham R. Boeck, Gudrun de Sloman, Katherine A. Matey, Victoria E. Domingos, Fabíola Xochilt Valdez Duarte, Rafael Mendonça Almeida-Val, Vera Maria Fonseca Val, Adalberto Luis |
author2_role |
author author author author author author author author author |
dc.contributor.author.fl_str_mv |
Wood, Chris M. Iftikar, Fathima I. Scott, Graham R. Boeck, Gudrun de Sloman, Katherine A. Matey, Victoria E. Domingos, Fabíola Xochilt Valdez Duarte, Rafael Mendonça Almeida-Val, Vera Maria Fonseca Val, Adalberto Luis |
dc.subject.eng.fl_str_mv |
Ammonia Macrogol Derivative Oxygen Potassium Sodium Water Animals Breathing Cell Hypoxia Cichlid Cytology Diffusion Gill Glomerulus Filtration Rate Heart Rate Kidney Metabolism Osmosis Permeability Physiology Urine Ammonia Animal Cell Hypoxia Cichlids Diffusion Gills Glomerular Filtration Rate Heart Rate Kidney Osmosis Oxygen Permeability Polyethylene Glycols Potassium Respiration Sodium Water Astronotus Astronotus Ocellatus |
topic |
Ammonia Macrogol Derivative Oxygen Potassium Sodium Water Animals Breathing Cell Hypoxia Cichlid Cytology Diffusion Gill Glomerulus Filtration Rate Heart Rate Kidney Metabolism Osmosis Permeability Physiology Urine Ammonia Animal Cell Hypoxia Cichlids Diffusion Gills Glomerular Filtration Rate Heart Rate Kidney Osmosis Oxygen Permeability Polyethylene Glycols Potassium Respiration Sodium Water Astronotus Astronotus Ocellatus |
description |
Earlier studies demonstrated that oscars, endemic to ion-poor Amazonian waters, are extremely hypoxia tolerant, and exhibit a marked reduction in active unidirectional Na+ uptake rate (measured directly) but unchanged net Na+ balance during acute exposure to low Po2, indicating a comparable reduction in whole body Na+ efflux rate. However, branchial O2 transfer factor does not fall. The present study focused on the nature of the efflux reduction in the face of maintained gill O 2 permeability. Direct measurements of 22Na appearance in the water from bladder-catheterized fish confirmed a rapid 55% fall in unidirectional Na+ efflux rate across the gills upon acute exposure to hypoxia (PO2=10-20torr; 1 torr=133.3 Pa), which was quickly reversed upon return to normoxia. An exchange diffusion mechanism for Na + is not present, so the reduction in efflux was not directly linked to the reduction in Na+ influx. A quickly developing bradycardia occurred during hypoxia. Transepithelial potential, which was sensitive to water [Ca2+], became markedly less negative during hypoxia and was restored upon return to normoxia. Ammonia excretion, net K+ loss rates, and 3H2O exchange rates (diffusive water efflux rates) across the gills fell by 55-75% during hypoxia, with recovery during normoxia. Osmotic permeability to water also declined, but the fall (30%) was less than that in diffusive water permeability (70%). In total, these observations indicate a reduction in gill transcellular permeability during hypoxia, a conclusion supported by unchanged branchial efflux rates of the paracellular marker [3H]PEG-4000 during hypoxia and normoxic recovery. At the kidney, glomerular filtration rate, urine flow rate, and tubular Na+ reabsorption rate fell in parallel by 70% during hypoxia, facilitating additional reductions in costs and in urinary Na+, K+ and ammonia excretion rates. Scanning electron microscopy of the gill epithelium revealed no remodelling at a macro-level, but pronounced changes in surface morphology. Under normoxia, mitochondria-rich cells were exposed only through small apical crypts, and these decreased in number by 47% and in individual area by 65% during 3 h hypoxia. We suggest that a rapid closure of transcellular channels, perhaps effected by pavement cell coverage of the crypts, allows conservation of ions and reduction of ionoregulatory costs without compromise of O2 exchange capacity during acute hypoxia, a response very different from the traditional osmorespiratory compromise. |
publishDate |
2009 |
dc.date.issued.fl_str_mv |
2009 |
dc.date.accessioned.fl_str_mv |
2020-05-07T14:02:11Z |
dc.date.available.fl_str_mv |
2020-05-07T14:02:11Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
https://repositorio.inpa.gov.br/handle/1/15045 |
dc.identifier.doi.none.fl_str_mv |
10.1242/jeb.028464 |
url |
https://repositorio.inpa.gov.br/handle/1/15045 |
identifier_str_mv |
10.1242/jeb.028464 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.ispartof.pt_BR.fl_str_mv |
Volume 212, Número 12, Pags. 1949-1964 |
dc.rights.driver.fl_str_mv |
Attribution-NonCommercial-NoDerivs 3.0 Brazil http://creativecommons.org/licenses/by-nc-nd/3.0/br/ info:eu-repo/semantics/openAccess |
rights_invalid_str_mv |
Attribution-NonCommercial-NoDerivs 3.0 Brazil http://creativecommons.org/licenses/by-nc-nd/3.0/br/ |
eu_rights_str_mv |
openAccess |
dc.publisher.none.fl_str_mv |
Journal of Experimental Biology |
publisher.none.fl_str_mv |
Journal of Experimental Biology |
dc.source.none.fl_str_mv |
reponame:Repositório Institucional do INPA instname:Instituto Nacional de Pesquisas da Amazônia (INPA) instacron:INPA |
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INPA |
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INPA |
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Repositório Institucional do INPA |
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Repositório Institucional do INPA |
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