Interrelationship between contractility, protein synthesis and metabolism in mantle of juvenile cuttlefish (Sepia officinalis)
| Main Author: | |
|---|---|
| Publication Date: | 2019 |
| Other Authors: | , , , , , , |
| 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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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. |
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2019 |
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2019-09-23T12:55:38Z 2019 2019-01-01T00:00:00Z |
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http://hdl.handle.net/10400.1/12773 |
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eng |
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1664-042X 10.3389/fphys.2019.01051 |
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Frontiers Media |
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Frontiers Media |
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