UV-B exposure reduces locomotor performance by impairing muscle function but not mitochondrial ATP production

Kazerouni, Ensiyeh Ghanizadeh, Franklin, Craig E. and Seebacher, Frank (2016) UV-B exposure reduces locomotor performance by impairing muscle function but not mitochondrial ATP production. Journal of Experimental Biology, 219 1: 96-102. doi:10.1242/jeb.131615

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Author Kazerouni, Ensiyeh Ghanizadeh
Franklin, Craig E.
Seebacher, Frank
Title UV-B exposure reduces locomotor performance by impairing muscle function but not mitochondrial ATP production
Journal name Journal of Experimental Biology   Check publisher's open access policy
ISSN 0022-0949
1477-9145
Publication date 2016-01-01
Year available 2015
Sub-type Article (original research)
DOI 10.1242/jeb.131615
Open Access Status File (Publisher version)
Volume 219
Issue 1
Start page 96
End page 102
Total pages 7
Place of publication Cambridge, United Kingdom
Publisher The Company of Biologists
Language eng
Subject 1105 Ecology, Evolution, Behavior and Systematics
1314 Physiology
1104 Aquatic Science
1103 Animal Science and Zoology
1312 Molecular Biology
1109 Insect Science
Abstract Ultraviolet B radiation (UV-B) can reduce swimming performance by increasing reactive oxygen species (ROS) formation. High concentrations of ROS can damage mitochondria, resulting in reduced ATP production. ROS can also damage muscle proteins, thereby leading to impaired muscle contractile function. We have shown previously that UV-B exposure reduces locomotor performance in mosquitofish (Gambusia holbrooki) without affecting metabolic scope. Our aim was therefore to test whether UV-B influences swimming performance of mosquitofish by ROS-induced damage to muscle proteins without affecting mitochondrial function. In a fully factorial design, we exposed mosquitofish to UV-B and no-UV-B controls in combination with exposure to N-acetylcysteine (NAC) plus no-NAC controls. We used NAC, a precursor of glutathione, as an antioxidant to test whether any effects of UV-B on swimming performance were at least partly due to UV-B-induced ROS. UV-B significantly reduced critical sustained swimming performance and tail beat frequencies, and it increased ROS-induced damage (protein carbonyl concentrations and lipid peroxidation) in muscle. However, UV-B did not affect the activity of sarco-endoplasmic reticulum ATPase (SERCA), an enzyme associated with muscle calcium cycling and muscle relaxation. UV-B did not affect ADP phosphorylation (state 3) rates of mitochondrial respiration, and it did not alter the amount of ATP produced per atom of oxygen consumed (P:O ratio). However, UV-B reduced the mitochondrial respiratory control ratio. Under UV-B exposure, fish treated with NAC showed greater swimming performance and tail beat frequencies, higher glutathione concentrations, and lower protein carbonyl concentrations and lipid peroxidation than untreated fish. Tail beat amplitude was not affected by any treatment. Our results showed, firstly, that the effects of UV-B on locomotor performance were mediated by ROS and, secondly, that reduced swimming performance was not caused by impaired mitochondrial ATP production. Instead, reduced tail beat frequencies indicate that muscle of UV-B exposed fish were slower, which was likely to have been caused by slower contraction rates, because SERCA activities remained unaffected.
Formatted abstract
Ultraviolet B radiation (UV-B) can reduce swimming performance by increasing reactive oxygen species (ROS) formation. High concentrations of ROS can damage mitochondria, resulting in reduced ATP production. ROS can also damage muscle proteins, thereby leading to impaired muscle contractile function. We have shown previously that UV-B exposure reduces locomotor performance in mosquitofish (Gambusia holbrooki) without affecting metabolic scope. Our aim was therefore to test whether UV-B influences swimming performance of mosquitofish by ROS-induced damage to muscle proteins without affecting mitochondrial function. In a fully factorial design, we exposed mosquitofish to UV-B and no-UV-B controls in combination with exposure to N-acetylcysteine (NAC) plus no-NAC controls. We used NAC, a precursor of glutathione, as an antioxidant to test whether any effects of UV-B on swimming performance were at least partly due to UV-B-induced ROS. UV-B significantly reduced critical sustained swimming performance and tail beat frequencies, and it increased ROS-induced damage (protein carbonyl concentrations and lipid peroxidation) in muscle. However, UV-B did not affect the activity of sarco-endoplasmic reticulum ATPase (SERCA), an enzyme associated with muscle calcium cycling and muscle relaxation. UV-B did not affect ADP phosphorylation (state 3) rates of mitochondrial respiration, and it did not alter the amount of ATP produced per atom of oxygen consumed (P:O ratio). However, UV-B reduced the mitochondrial respiratory control ratio. Under UV-B exposure, fish treated with NAC showed greater swimming performance and tail beat frequencies, higher glutathione concentrations, and lower protein carbonyl concentrations and lipid peroxidation than untreated fish. Tail beat amplitude was not affected by any treatment. Our results showed, firstly, that the effects of UV-B on locomotor performance were mediated by ROS and, secondly, that reduced swimming performance was not caused by impaired mitochondrial ATP production. Instead, reduced tail beat frequencies indicate that muscle of UV-B exposed fish were slower, which was likely to have been caused by slower contraction rates, because SERCA activities remained unaffected.
Keyword Reactive oxygen species
Swimming kinematic
Calcium cycling
SERCA
Mitochondrial respiration
Glutathione
Q-Index Code C1
Q-Index Status Provisional Code
Grant ID DP140102773
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Official 2016 Collection
School of Biological Sciences Publications
 
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