Low guanylyl cyclase activity in Weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving
Nitric oxide (NO) is a potent vasodilator, which improves perfusion and oxygen delivery during tissue hypoxia in terrestrial animals. The vertebrate dive response involves vasoconstriction in select tissues, which persists despite profound hypoxia. Using tissues collected from Weddell seals at necro...
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Online Access: | http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6620652/ http://www.ncbi.nlm.nih.gov/pubmed/30892912 https://doi.org/10.1152/ajpregu.00283.2018 |
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ftpubmed:oai:pubmedcentral.nih.gov:6620652 2023-05-15T18:43:24+02:00 Low guanylyl cyclase activity in Weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving Hindle, Allyson G. Allen, Kaitlin N. Batten, Annabelle J. Hückstädt, Luis A. Turner-Maier, Jason Schulberg, S. Anne Johnson, Jeremy Karlsson, Elinor Lindblad-Toh, Kerstin Costa, Daniel P. Bloch, Donald B. Zapol, Warren M. Buys, Emmanuel S. 2019-06-01 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6620652/ http://www.ncbi.nlm.nih.gov/pubmed/30892912 https://doi.org/10.1152/ajpregu.00283.2018 en eng American Physiological Society http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6620652/ http://www.ncbi.nlm.nih.gov/pubmed/30892912 http://dx.doi.org/10.1152/ajpregu.00283.2018 Copyright © 2019 the American Physiological Society Am J Physiol Regul Integr Comp Physiol Research Article Text 2019 ftpubmed https://doi.org/10.1152/ajpregu.00283.2018 2020-06-07T00:25:06Z Nitric oxide (NO) is a potent vasodilator, which improves perfusion and oxygen delivery during tissue hypoxia in terrestrial animals. The vertebrate dive response involves vasoconstriction in select tissues, which persists despite profound hypoxia. Using tissues collected from Weddell seals at necropsy, we investigated whether vasoconstriction is aided by downregulation of local hypoxia signaling mechanisms. We focused on NO–soluble guanylyl cyclase (GC)-cGMP signaling, a well-known vasodilatory transduction pathway. Seals have a lower GC protein abundance, activity, and capacity to respond to NO stimulation than do terrestrial mammals. In seal lung homogenates, GC produced less cGMP (20.1 ± 3.7 pmol·mg protein(−1)·min(−1)) than the lungs of dogs (−80 ± 144 pmol·mg protein(−1)·min(−1) less than seals), sheep (−472 ± 96), rats (−664 ± 104) or mice (−1,160 ± 104, P < 0.0001). Amino acid sequences of the GC enzyme α-subunits differed between seals and terrestrial mammals, potentially affecting their structure and function. Vasoconstriction in diving Weddell seals is not consistent across tissues; perfusion is maintained in the brain and heart but decreased in other organs such as the kidney. A NO donor increased median GC activity 49.5-fold in the seal brain but only 27.4-fold in the kidney, consistent with the priority of cerebral perfusion during diving. Nos3 expression was high in the seal brain, which could improve NO production and vasodilatory potential. Conversely, Pde5a expression was high in the seal renal artery, which may increase cGMP breakdown and vasoconstriction in the kidney. Taken together, the results of this study suggest that alterations in the NO-cGMP pathway facilitate the diving response. Text Weddell Seals PubMed Central (PMC) Weddell American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 316 6 R704 R715 |
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English |
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Research Article |
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Research Article Hindle, Allyson G. Allen, Kaitlin N. Batten, Annabelle J. Hückstädt, Luis A. Turner-Maier, Jason Schulberg, S. Anne Johnson, Jeremy Karlsson, Elinor Lindblad-Toh, Kerstin Costa, Daniel P. Bloch, Donald B. Zapol, Warren M. Buys, Emmanuel S. Low guanylyl cyclase activity in Weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving |
topic_facet |
Research Article |
description |
Nitric oxide (NO) is a potent vasodilator, which improves perfusion and oxygen delivery during tissue hypoxia in terrestrial animals. The vertebrate dive response involves vasoconstriction in select tissues, which persists despite profound hypoxia. Using tissues collected from Weddell seals at necropsy, we investigated whether vasoconstriction is aided by downregulation of local hypoxia signaling mechanisms. We focused on NO–soluble guanylyl cyclase (GC)-cGMP signaling, a well-known vasodilatory transduction pathway. Seals have a lower GC protein abundance, activity, and capacity to respond to NO stimulation than do terrestrial mammals. In seal lung homogenates, GC produced less cGMP (20.1 ± 3.7 pmol·mg protein(−1)·min(−1)) than the lungs of dogs (−80 ± 144 pmol·mg protein(−1)·min(−1) less than seals), sheep (−472 ± 96), rats (−664 ± 104) or mice (−1,160 ± 104, P < 0.0001). Amino acid sequences of the GC enzyme α-subunits differed between seals and terrestrial mammals, potentially affecting their structure and function. Vasoconstriction in diving Weddell seals is not consistent across tissues; perfusion is maintained in the brain and heart but decreased in other organs such as the kidney. A NO donor increased median GC activity 49.5-fold in the seal brain but only 27.4-fold in the kidney, consistent with the priority of cerebral perfusion during diving. Nos3 expression was high in the seal brain, which could improve NO production and vasodilatory potential. Conversely, Pde5a expression was high in the seal renal artery, which may increase cGMP breakdown and vasoconstriction in the kidney. Taken together, the results of this study suggest that alterations in the NO-cGMP pathway facilitate the diving response. |
format |
Text |
author |
Hindle, Allyson G. Allen, Kaitlin N. Batten, Annabelle J. Hückstädt, Luis A. Turner-Maier, Jason Schulberg, S. Anne Johnson, Jeremy Karlsson, Elinor Lindblad-Toh, Kerstin Costa, Daniel P. Bloch, Donald B. Zapol, Warren M. Buys, Emmanuel S. |
author_facet |
Hindle, Allyson G. Allen, Kaitlin N. Batten, Annabelle J. Hückstädt, Luis A. Turner-Maier, Jason Schulberg, S. Anne Johnson, Jeremy Karlsson, Elinor Lindblad-Toh, Kerstin Costa, Daniel P. Bloch, Donald B. Zapol, Warren M. Buys, Emmanuel S. |
author_sort |
Hindle, Allyson G. |
title |
Low guanylyl cyclase activity in Weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving |
title_short |
Low guanylyl cyclase activity in Weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving |
title_full |
Low guanylyl cyclase activity in Weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving |
title_fullStr |
Low guanylyl cyclase activity in Weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving |
title_full_unstemmed |
Low guanylyl cyclase activity in Weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving |
title_sort |
low guanylyl cyclase activity in weddell seals: implications for peripheral vasoconstriction and perfusion of the brain during diving |
publisher |
American Physiological Society |
publishDate |
2019 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6620652/ http://www.ncbi.nlm.nih.gov/pubmed/30892912 https://doi.org/10.1152/ajpregu.00283.2018 |
geographic |
Weddell |
geographic_facet |
Weddell |
genre |
Weddell Seals |
genre_facet |
Weddell Seals |
op_source |
Am J Physiol Regul Integr Comp Physiol |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6620652/ http://www.ncbi.nlm.nih.gov/pubmed/30892912 http://dx.doi.org/10.1152/ajpregu.00283.2018 |
op_rights |
Copyright © 2019 the American Physiological Society |
op_doi |
https://doi.org/10.1152/ajpregu.00283.2018 |
container_title |
American Journal of Physiology-Regulatory, Integrative and Comparative Physiology |
container_volume |
316 |
container_issue |
6 |
container_start_page |
R704 |
op_container_end_page |
R715 |
_version_ |
1766233789541908480 |