Functional characterisation of UCP1 in the common carp: uncoupling activity in liver mitochondria and cold-induced expression in the brain |
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Authors: | Martin Jastroch Julie A Buckingham Michael Helwig Martin Klingenspor Martin D Brand |
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Institution: | (1) Animal Physiology, Department of Biology, Philipps University Marburg, Karl-von-Frisch-Str. 8, Marburg, 35032, Germany;(2) Medical Research Council Dunn Human Nutrition Unit, Hills Road, Cambridge, CB2 2XY, UK |
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Abstract: | Mammalian uncoupling protein 1 (UCP1) mediates nonshivering thermogenesis in brown adipose tissue. We previously reported
on the presence of a UCP1 orthologue in ectothermic fish and observed downregulation of UCP1 gene expression in the liver
of the common carp. Neither the function of UCP1, nor the mode of UCP1 activation is known in carp liver mitochondria. Here,
we compared the proton conductance at 25°C of liver mitochondria isolated from carp either maintained at 20°C (warm-acclimated,
WA) or exposed to 8°C (cold-acclimated, CA) water temperature for 7–10 days. Liver mitochondria from WA carp had higher state
four rates of oxygen consumption and greater proton conductance at high membrane potential. Liver mitochondria from WA, but
not from CA, carp showed a strong increase in proton conductance when palmitate (or 4-hydroxy-trans-2-nonenal, HNE) was added, and this inducible proton conductance was prevented by addition of GDP. This fatty acid sensitive
proton leak is likely due to the expression of UCP1 in the liver of WA carp. The observed biochemical properties of proton
leak strongly suggest that carp UCP1 is a functional uncoupling protein with broadly the same activatory and inhibitory characteristics
as mammalian UCP1. Significant UCP1 expression was also detected in our previous study in whole brain of the carp. We here
observed a twofold increase of UCP1 mRNA in carp brain following cold exposure, suggesting a role of UCP1 in the thermal adaptation
of brain metabolism. In situ hybridization located the UCP1 gene expression to the optic tectum responsible for visual system
control, the descending trigeminal tract and the solitary tract. Taken together, this study characterises uncoupling protein
activity in an ectotherm for the first time.
Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. |
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Keywords: | Uncoupling protein 1 Proton leak Cyprinus carpio 4-hydroxynonenal Liver |
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