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Acute Stress in Lesser-Spotted Catshark (Scyliorhinus canicula Linnaeus, 1758) Promotes Amino Acid Catabolism and Osmoregulatory Imbalances

SIMPLE SUMMARY: In catsharks (Scyliorhinus canicula), air exposure induces amino acid catabolism altogether with osmoregulatory imbalances. This study describes a novel NHE isoform being expressed in gills that may be involved in ammonium excretion. ABSTRACT: Acute-stress situations in vertebrates i...

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Autores principales: Ruiz-Jarabo, Ignacio, Paullada-Salmerón, José A., Jerez-Cepa, Ismael, Gonçalves Neto, José Belquior, Bystriansky, Jason S., Mancera, Juan M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9105869/
https://www.ncbi.nlm.nih.gov/pubmed/35565621
http://dx.doi.org/10.3390/ani12091192
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author Ruiz-Jarabo, Ignacio
Paullada-Salmerón, José A.
Jerez-Cepa, Ismael
Gonçalves Neto, José Belquior
Bystriansky, Jason S.
Mancera, Juan M.
author_facet Ruiz-Jarabo, Ignacio
Paullada-Salmerón, José A.
Jerez-Cepa, Ismael
Gonçalves Neto, José Belquior
Bystriansky, Jason S.
Mancera, Juan M.
author_sort Ruiz-Jarabo, Ignacio
collection PubMed
description SIMPLE SUMMARY: In catsharks (Scyliorhinus canicula), air exposure induces amino acid catabolism altogether with osmoregulatory imbalances. This study describes a novel NHE isoform being expressed in gills that may be involved in ammonium excretion. ABSTRACT: Acute-stress situations in vertebrates induce a series of physiological responses to cope with the event. While common secondary stress responses include increased catabolism and osmoregulatory imbalances, specific processes depend on the taxa. In this sense, these processes are still largely unknown in ancient vertebrates such as marine elasmobranchs. Thus, we challenged the lesser spotted catshark (Scyliorhinus canicula) to 18 min of air exposure, and monitored their recovery after 0, 5, and 24 h. This study describes amino acid turnover in the liver, white muscle, gills, and rectal gland, and plasma parameters related to energy metabolism and osmoregulatory imbalances. Catsharks rely on white muscle amino acid catabolism to face the energy demand imposed by the stressor, producing NH(4)(+). While some plasma ions (K(+), Cl(−) and Ca(2+)) increased in concentration after 18 min of air exposure, returning to basal values after 5 h of recovery, Na(+) increased after just 5 h of recovery, coinciding with a decrease in plasma NH(4)(+). These changes were accompanied by increased activity of a branchial amiloride-sensitive ATPase. Therefore, we hypothesize that this enzyme may be a Na(+)/H(+) exchanger (NHE) related to NH(4)(+) excretion. The action of an omeprazole-sensitive ATPase, putatively associated to a H(+)/K(+)-ATPase (HKA), is also affected by these allostatic processes. Some complementary experiments were carried out to delve a little deeper into the possible branchial enzymes sensitive to amiloride, including in vivo and ex vivo approaches, and partial sequencing of a nhe1 in the gills. This study describes the possible presence of an HKA enzyme in the rectal gland, as well as a NHE in the gills, highlighting the importance of understanding the relationship between acute stress and osmoregulation in elasmobranchs.
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spelling pubmed-91058692022-05-14 Acute Stress in Lesser-Spotted Catshark (Scyliorhinus canicula Linnaeus, 1758) Promotes Amino Acid Catabolism and Osmoregulatory Imbalances Ruiz-Jarabo, Ignacio Paullada-Salmerón, José A. Jerez-Cepa, Ismael Gonçalves Neto, José Belquior Bystriansky, Jason S. Mancera, Juan M. Animals (Basel) Article SIMPLE SUMMARY: In catsharks (Scyliorhinus canicula), air exposure induces amino acid catabolism altogether with osmoregulatory imbalances. This study describes a novel NHE isoform being expressed in gills that may be involved in ammonium excretion. ABSTRACT: Acute-stress situations in vertebrates induce a series of physiological responses to cope with the event. While common secondary stress responses include increased catabolism and osmoregulatory imbalances, specific processes depend on the taxa. In this sense, these processes are still largely unknown in ancient vertebrates such as marine elasmobranchs. Thus, we challenged the lesser spotted catshark (Scyliorhinus canicula) to 18 min of air exposure, and monitored their recovery after 0, 5, and 24 h. This study describes amino acid turnover in the liver, white muscle, gills, and rectal gland, and plasma parameters related to energy metabolism and osmoregulatory imbalances. Catsharks rely on white muscle amino acid catabolism to face the energy demand imposed by the stressor, producing NH(4)(+). While some plasma ions (K(+), Cl(−) and Ca(2+)) increased in concentration after 18 min of air exposure, returning to basal values after 5 h of recovery, Na(+) increased after just 5 h of recovery, coinciding with a decrease in plasma NH(4)(+). These changes were accompanied by increased activity of a branchial amiloride-sensitive ATPase. Therefore, we hypothesize that this enzyme may be a Na(+)/H(+) exchanger (NHE) related to NH(4)(+) excretion. The action of an omeprazole-sensitive ATPase, putatively associated to a H(+)/K(+)-ATPase (HKA), is also affected by these allostatic processes. Some complementary experiments were carried out to delve a little deeper into the possible branchial enzymes sensitive to amiloride, including in vivo and ex vivo approaches, and partial sequencing of a nhe1 in the gills. This study describes the possible presence of an HKA enzyme in the rectal gland, as well as a NHE in the gills, highlighting the importance of understanding the relationship between acute stress and osmoregulation in elasmobranchs. MDPI 2022-05-06 /pmc/articles/PMC9105869/ /pubmed/35565621 http://dx.doi.org/10.3390/ani12091192 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Ruiz-Jarabo, Ignacio
Paullada-Salmerón, José A.
Jerez-Cepa, Ismael
Gonçalves Neto, José Belquior
Bystriansky, Jason S.
Mancera, Juan M.
Acute Stress in Lesser-Spotted Catshark (Scyliorhinus canicula Linnaeus, 1758) Promotes Amino Acid Catabolism and Osmoregulatory Imbalances
title Acute Stress in Lesser-Spotted Catshark (Scyliorhinus canicula Linnaeus, 1758) Promotes Amino Acid Catabolism and Osmoregulatory Imbalances
title_full Acute Stress in Lesser-Spotted Catshark (Scyliorhinus canicula Linnaeus, 1758) Promotes Amino Acid Catabolism and Osmoregulatory Imbalances
title_fullStr Acute Stress in Lesser-Spotted Catshark (Scyliorhinus canicula Linnaeus, 1758) Promotes Amino Acid Catabolism and Osmoregulatory Imbalances
title_full_unstemmed Acute Stress in Lesser-Spotted Catshark (Scyliorhinus canicula Linnaeus, 1758) Promotes Amino Acid Catabolism and Osmoregulatory Imbalances
title_short Acute Stress in Lesser-Spotted Catshark (Scyliorhinus canicula Linnaeus, 1758) Promotes Amino Acid Catabolism and Osmoregulatory Imbalances
title_sort acute stress in lesser-spotted catshark (scyliorhinus canicula linnaeus, 1758) promotes amino acid catabolism and osmoregulatory imbalances
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9105869/
https://www.ncbi.nlm.nih.gov/pubmed/35565621
http://dx.doi.org/10.3390/ani12091192
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