Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)

Bibliographic Details
Main Author: Lamarre, Simon G.
Publication Date: 2019
Other Authors: MacCormack, Tyson J., Bourloutski, Émilie, Callaghan, Neal I., Pinto, Vanessa, Andrade, José Pedro, Sykes, António, Driedzic, William R.
Format: Article
Language: eng
Source: Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
Download full: http://hdl.handle.net/10400.1/12773
Summary: Young juvenile cuttlefish (Sepia officinalis) can grow at rates as high as 12% body weight per day. How the metabolic demands of such a massive growth rate impacts muscle performance that competes for ATP is unknown. Here, we integrate aspects of contractility, protein synthesis, and energy metabolism in mantle of specimens weighing 1.1 g to lend insight into the processes. Isolated mantle muscle preparations were electrically stimulated and isometric force development monitored. Preparations were forced to contract at 3 Hz for 30 s to simulate a jetting event. We then measured oxygen consumption, glucose uptake and protein synthesis in the hour following the stimulation. Protein synthesis was inhibited with cycloheximide and glycolysis was inhibited with iodoacetic acid in a subset of samples. Inhibition of protein synthesis impaired contractility and decreased oxygen consumption. An intact protein synthesis is required to maintain contractility possibly due to rapidly turning over proteins. At least, 41% of whole animal ṀO2 is used to support protein synthesis in mantle, while the cost of protein synthesis (50 μmol O2 mg protein-1) in mantle was in the range reported for other aquatic ectotherms. A single jetting challenge stimulated protein synthesis by approximately 25% (2.51-3.12% day-1) over a 1 h post contractile period, a similar response to that which occurs in mammalian skeletal muscle. Aerobic metabolism was not supported by extracellular glucose leading to the contention that at this life stage either glycogen or amino acids are catabolized. Regardless, an intact glycolysis is required to support contractile performance and protein synthesis in resting muscle. It is proposed that glycolysis is needed to maintain intracellular ionic gradients. Intracellular glucose at approximately 3 mmol L-1 was higher than the 1 mmol L-1 glucose in the bathing medium suggesting an active glucose transport mechanism. Octopine did not accumulate during a single physiologically relevant jetting challenge; however, octopine accumulation increased following a stress that is sufficient to lower Arg-P and increase free arginine.
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spelling Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)Anaerobic metabolismCycloheximideGlucoseIodoacetic acidJettingOctopineYoung juvenile cuttlefish (Sepia officinalis) can grow at rates as high as 12% body weight per day. How the metabolic demands of such a massive growth rate impacts muscle performance that competes for ATP is unknown. Here, we integrate aspects of contractility, protein synthesis, and energy metabolism in mantle of specimens weighing 1.1 g to lend insight into the processes. Isolated mantle muscle preparations were electrically stimulated and isometric force development monitored. Preparations were forced to contract at 3 Hz for 30 s to simulate a jetting event. We then measured oxygen consumption, glucose uptake and protein synthesis in the hour following the stimulation. Protein synthesis was inhibited with cycloheximide and glycolysis was inhibited with iodoacetic acid in a subset of samples. Inhibition of protein synthesis impaired contractility and decreased oxygen consumption. An intact protein synthesis is required to maintain contractility possibly due to rapidly turning over proteins. At least, 41% of whole animal ṀO2 is used to support protein synthesis in mantle, while the cost of protein synthesis (50 μmol O2 mg protein-1) in mantle was in the range reported for other aquatic ectotherms. A single jetting challenge stimulated protein synthesis by approximately 25% (2.51-3.12% day-1) over a 1 h post contractile period, a similar response to that which occurs in mammalian skeletal muscle. Aerobic metabolism was not supported by extracellular glucose leading to the contention that at this life stage either glycogen or amino acids are catabolized. Regardless, an intact glycolysis is required to support contractile performance and protein synthesis in resting muscle. It is proposed that glycolysis is needed to maintain intracellular ionic gradients. Intracellular glucose at approximately 3 mmol L-1 was higher than the 1 mmol L-1 glucose in the bathing medium suggesting an active glucose transport mechanism. Octopine did not accumulate during a single physiologically relevant jetting challenge; however, octopine accumulation increased following a stress that is sufficient to lower Arg-P and increase free arginine.Frontiers MediaSapientiaLamarre, Simon G.MacCormack, Tyson J.Bourloutski, ÉmilieCallaghan, Neal I.Pinto, VanessaAndrade, José PedroSykes, AntónioDriedzic, William R.2019-09-23T12:55:38Z20192019-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.1/12773eng1664-042X10.3389/fphys.2019.01051info:eu-repo/semantics/openAccessreponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiainstacron:RCAAP2025-02-18T17:23:51Zoai:sapientia.ualg.pt:10400.1/12773Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireinfo@rcaap.ptopendoar:https://opendoar.ac.uk/repository/71602025-05-28T20:20:40.227738Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiafalse
dc.title.none.fl_str_mv Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
title Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
spellingShingle Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
Lamarre, Simon G.
Anaerobic metabolism
Cycloheximide
Glucose
Iodoacetic acid
Jetting
Octopine
title_short Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
title_full Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
title_fullStr Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
title_full_unstemmed Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
title_sort Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
author Lamarre, Simon G.
author_facet Lamarre, Simon G.
MacCormack, Tyson J.
Bourloutski, Émilie
Callaghan, Neal I.
Pinto, Vanessa
Andrade, José Pedro
Sykes, António
Driedzic, William R.
author_role author
author2 MacCormack, Tyson J.
Bourloutski, Émilie
Callaghan, Neal I.
Pinto, Vanessa
Andrade, José Pedro
Sykes, António
Driedzic, William R.
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Sapientia
dc.contributor.author.fl_str_mv Lamarre, Simon G.
MacCormack, Tyson J.
Bourloutski, Émilie
Callaghan, Neal I.
Pinto, Vanessa
Andrade, José Pedro
Sykes, António
Driedzic, William R.
dc.subject.por.fl_str_mv Anaerobic metabolism
Cycloheximide
Glucose
Iodoacetic acid
Jetting
Octopine
topic Anaerobic metabolism
Cycloheximide
Glucose
Iodoacetic acid
Jetting
Octopine
description Young juvenile cuttlefish (Sepia officinalis) can grow at rates as high as 12% body weight per day. How the metabolic demands of such a massive growth rate impacts muscle performance that competes for ATP is unknown. Here, we integrate aspects of contractility, protein synthesis, and energy metabolism in mantle of specimens weighing 1.1 g to lend insight into the processes. Isolated mantle muscle preparations were electrically stimulated and isometric force development monitored. Preparations were forced to contract at 3 Hz for 30 s to simulate a jetting event. We then measured oxygen consumption, glucose uptake and protein synthesis in the hour following the stimulation. Protein synthesis was inhibited with cycloheximide and glycolysis was inhibited with iodoacetic acid in a subset of samples. Inhibition of protein synthesis impaired contractility and decreased oxygen consumption. An intact protein synthesis is required to maintain contractility possibly due to rapidly turning over proteins. At least, 41% of whole animal ṀO2 is used to support protein synthesis in mantle, while the cost of protein synthesis (50 μmol O2 mg protein-1) in mantle was in the range reported for other aquatic ectotherms. A single jetting challenge stimulated protein synthesis by approximately 25% (2.51-3.12% day-1) over a 1 h post contractile period, a similar response to that which occurs in mammalian skeletal muscle. Aerobic metabolism was not supported by extracellular glucose leading to the contention that at this life stage either glycogen or amino acids are catabolized. Regardless, an intact glycolysis is required to support contractile performance and protein synthesis in resting muscle. It is proposed that glycolysis is needed to maintain intracellular ionic gradients. Intracellular glucose at approximately 3 mmol L-1 was higher than the 1 mmol L-1 glucose in the bathing medium suggesting an active glucose transport mechanism. Octopine did not accumulate during a single physiologically relevant jetting challenge; however, octopine accumulation increased following a stress that is sufficient to lower Arg-P and increase free arginine.
publishDate 2019
dc.date.none.fl_str_mv 2019-09-23T12:55:38Z
2019
2019-01-01T00:00:00Z
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 http://hdl.handle.net/10400.1/12773
url http://hdl.handle.net/10400.1/12773
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 1664-042X
10.3389/fphys.2019.01051
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologia
instacron:RCAAP
instname_str FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologia
instacron_str RCAAP
institution RCAAP
reponame_str Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
collection Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
repository.name.fl_str_mv Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologia
repository.mail.fl_str_mv info@rcaap.pt
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