Cargando…

An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins

BACKGROUND AND OBJECTIVES: Ischemic events, such as ischemic heart disease and stroke, are the number one cause of death globally. Ischemia prevents blood, carrying essential nutrients and oxygen, from reaching tissues, leading to cell and tissue death, and eventual organ failure. While humans are r...

Descripción completa

Detalles Bibliográficos
Autores principales: Blawas, Ashley M, Ware, Kathryn E, Schmaltz, Emma, Zheng, Larry, Spruance, Jacob, Allen, Austin S, West, Nicole, Devos, Nicolas, Corcoran, David L, Nowacek, Douglas P, Eward, William C, Fahlman, Andreas, Somarelli, Jason A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8833867/
https://www.ncbi.nlm.nih.gov/pubmed/35169481
http://dx.doi.org/10.1093/emph/eoab036
_version_ 1784649043945717760
author Blawas, Ashley M
Ware, Kathryn E
Schmaltz, Emma
Zheng, Larry
Spruance, Jacob
Allen, Austin S
West, Nicole
Devos, Nicolas
Corcoran, David L
Nowacek, Douglas P
Eward, William C
Fahlman, Andreas
Somarelli, Jason A
author_facet Blawas, Ashley M
Ware, Kathryn E
Schmaltz, Emma
Zheng, Larry
Spruance, Jacob
Allen, Austin S
West, Nicole
Devos, Nicolas
Corcoran, David L
Nowacek, Douglas P
Eward, William C
Fahlman, Andreas
Somarelli, Jason A
author_sort Blawas, Ashley M
collection PubMed
description BACKGROUND AND OBJECTIVES: Ischemic events, such as ischemic heart disease and stroke, are the number one cause of death globally. Ischemia prevents blood, carrying essential nutrients and oxygen, from reaching tissues, leading to cell and tissue death, and eventual organ failure. While humans are relatively intolerant to ischemic events, other species, such as marine mammals, have evolved a unique tolerance to chronic ischemia/reperfusion during apneic diving. To identify possible molecular features of an increased tolerance for apnea, we examined changes in gene expression in breath-holding dolphins. METHODOLOGY: Here, we capitalized on the adaptations possesed by bottlenose dolphins (Tursiops truncatus) for diving as a comparative model of ischemic stress and hypoxia tolerance to identify molecular features associated with breath holding. Given that signals in the blood may influence physiological changes during diving, we used RNA-Seq and enzyme assays to examine time-dependent changes in gene expression in the blood of breath-holding dolphins. RESULTS: We observed time-dependent upregulation of the arachidonate 5-lipoxygenase (ALOX5) gene and increased lipoxygenase activity during breath holding. ALOX5 has been shown to be activated during hypoxia in rodent models, and its metabolites, leukotrienes, induce vasoconstriction. CONCLUSIONS AND IMPLICATIONS: The upregulation of ALOX5 mRNA occurred within the calculated aerobic dive limit of the species, suggesting that ALOX5 may play a role in the dolphin’s physiological response to diving, particularly in a pro-inflammatory response to ischemia and in promoting vasoconstriction. These observations pinpoint a potential molecular mechanism by which dolphins, and perhaps other marine mammals, respond to the prolonged breath holds associated with diving.
format Online
Article
Text
id pubmed-8833867
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-88338672022-02-14 An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins Blawas, Ashley M Ware, Kathryn E Schmaltz, Emma Zheng, Larry Spruance, Jacob Allen, Austin S West, Nicole Devos, Nicolas Corcoran, David L Nowacek, Douglas P Eward, William C Fahlman, Andreas Somarelli, Jason A Evol Med Public Health Original Research Article BACKGROUND AND OBJECTIVES: Ischemic events, such as ischemic heart disease and stroke, are the number one cause of death globally. Ischemia prevents blood, carrying essential nutrients and oxygen, from reaching tissues, leading to cell and tissue death, and eventual organ failure. While humans are relatively intolerant to ischemic events, other species, such as marine mammals, have evolved a unique tolerance to chronic ischemia/reperfusion during apneic diving. To identify possible molecular features of an increased tolerance for apnea, we examined changes in gene expression in breath-holding dolphins. METHODOLOGY: Here, we capitalized on the adaptations possesed by bottlenose dolphins (Tursiops truncatus) for diving as a comparative model of ischemic stress and hypoxia tolerance to identify molecular features associated with breath holding. Given that signals in the blood may influence physiological changes during diving, we used RNA-Seq and enzyme assays to examine time-dependent changes in gene expression in the blood of breath-holding dolphins. RESULTS: We observed time-dependent upregulation of the arachidonate 5-lipoxygenase (ALOX5) gene and increased lipoxygenase activity during breath holding. ALOX5 has been shown to be activated during hypoxia in rodent models, and its metabolites, leukotrienes, induce vasoconstriction. CONCLUSIONS AND IMPLICATIONS: The upregulation of ALOX5 mRNA occurred within the calculated aerobic dive limit of the species, suggesting that ALOX5 may play a role in the dolphin’s physiological response to diving, particularly in a pro-inflammatory response to ischemia and in promoting vasoconstriction. These observations pinpoint a potential molecular mechanism by which dolphins, and perhaps other marine mammals, respond to the prolonged breath holds associated with diving. Oxford University Press 2021-10-28 /pmc/articles/PMC8833867/ /pubmed/35169481 http://dx.doi.org/10.1093/emph/eoab036 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Foundation for Evolution, Medicine, and Public Health. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research Article
Blawas, Ashley M
Ware, Kathryn E
Schmaltz, Emma
Zheng, Larry
Spruance, Jacob
Allen, Austin S
West, Nicole
Devos, Nicolas
Corcoran, David L
Nowacek, Douglas P
Eward, William C
Fahlman, Andreas
Somarelli, Jason A
An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins
title An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins
title_full An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins
title_fullStr An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins
title_full_unstemmed An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins
title_short An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins
title_sort integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins
topic Original Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8833867/
https://www.ncbi.nlm.nih.gov/pubmed/35169481
http://dx.doi.org/10.1093/emph/eoab036
work_keys_str_mv AT blawasashleym anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT warekathryne anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT schmaltzemma anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT zhenglarry anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT spruancejacob anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT allenaustins anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT westnicole anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT devosnicolas anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT corcorandavidl anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT nowacekdouglasp anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT ewardwilliamc anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT fahlmanandreas anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT somarellijasona anintegratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT blawasashleym integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT warekathryne integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT schmaltzemma integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT zhenglarry integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT spruancejacob integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT allenaustins integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT westnicole integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT devosnicolas integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT corcorandavidl integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT nowacekdouglasp integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT ewardwilliamc integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT fahlmanandreas integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins
AT somarellijasona integratedcomparativephysiologyandmolecularapproachpinpointsmediatorsofbreathholdcapacityindolphins