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      Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals

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          Abstract

          Heat as a stressor of poultry has been studied extensively for many decades; it affects poultry production on a worldwide basis and has significant impact on well-being and production. More recently, the involvement of heat stress in inducing oxidative stress has received much interest. Oxidative stress is defined as the presence of reactive species in excess of the available antioxidant capacity of animal cells. Reactive species can modify several biologically cellular macromolecules and can interfere with cell signaling pathways. Furthermore, during the last decade, there has been an ever-increasing interest in the use of a wide array of natural feed-delivered phytochemicals that have potential antioxidant properties for poultry. In light of this, the current review aims to (1) summarize the mechanisms through which heat stress triggers excessive superoxide radical production in the mitochondrion and progresses into oxidative stress, (2) illustrate that this pathophysiology is dependent on the intensity and duration of heat stress, (3) present different nutritional strategies for mitigation of mitochondrial dysfunction, with particular focus on antioxidant phytochemicals.

          Oxidative stress that occurs with heat exposure can be manifest in all parts of the body; however, mitochondrial dysfunction underlies oxidative stress. In the initial phase of acute heat stress, mitochondrial substrate oxidation and electron transport chain activity are increased resulting in excessive superoxide production. During the later stage of acute heat stress, down-regulation of avian uncoupling protein worsens the oxidative stress situation causing mitochondrial dysfunction and tissue damage. Typically, antioxidant enzyme activities are upregulated. Chronic heat stress, however, leads to downsizing of mitochondrial metabolic oxidative capacity, up-regulation of avian uncoupling protein, a clear alteration in the pattern of antioxidant enzyme activities, and depletion of antioxidant reserves.

          Some phytochemicals, such as various types of flavonoids and related compounds, were shown to be beneficial in chronic heat-stressed poultry, but were less or not effective in non-heat-stressed counterparts. This supports the contention that antioxidant phytochemicals have potential under challenging conditions. Though substantial progress has been made in our understanding of the association between heat stress and oxidative stress, the means by which phytochemicals can alleviate oxidative stress have been sparsely explored.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s40104-016-0097-5) contains supplementary material, which is available to authorized users.

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          Most cited references63

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          Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling.

          Eukaryotic 2-Cys peroxiredoxins (2-Cys Prxs) not only act as antioxidants, but also appear to regulate hydrogen peroxide-mediated signal transduction. We show that bacterial 2-Cys Prxs are much less sensitive to oxidative inactivation than are eukaryotic 2-Cys Prxs. By identifying two sequence motifs unique to the sensitive 2-Cys Prxs and comparing the crystal structure of a bacterial 2-Cys Prx at 2.2 angstrom resolution with other Prx structures, we define the structural origins of sensitivity. We suggest this adaptation allows 2-Cys Prxs to act as floodgates, keeping resting levels of hydrogen peroxide low, while permitting higher levels during signal transduction.
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            A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling.

            Oxidative stress and mitochondrial dysfunction are associated with disease and aging. Oxidative stress results from overproduction of reactive oxygen species (ROS), often leading to peroxidation of membrane phospholipids and production of reactive aldehydes, particularly 4-hydroxy-2-nonenal. Mild uncoupling of oxidative phosphorylation protects by decreasing mitochondrial ROS production. We find that hydroxynonenal and structurally related compounds (such as trans-retinoic acid, trans-retinal and other 2-alkenals) specifically induce uncoupling of mitochondria through the uncoupling proteins UCP1, UCP2 and UCP3 and the adenine nucleotide translocase (ANT). Hydroxynonenal-induced uncoupling was inhibited by potent inhibitors of ANT (carboxyatractylate and bongkrekate) and UCP (GDP). The GDP-sensitive proton conductance induced by hydroxynonenal correlated with tissue expression of UCPs, appeared in yeast mitochondria expressing UCP1 and was absent in skeletal muscle mitochondria from UCP3 knockout mice. The carboxyatractylate-sensitive hydroxynonenal stimulation correlated with ANT content in mitochondria from Drosophila melanogaster expressing different amounts of ANT. Our findings indicate that hydroxynonenal is not merely toxic, but may be a biological signal to induce uncoupling through UCPs and ANT and thus decrease mitochondrial ROS production.
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              Polyphenol compounds in the chicken/animal diet: from the past to the future.

              P F Surai (2014)
              Animal feed provides a range of antioxidants that help the body building an integrated antioxidant system responsible for a prevention of damaging effects of free radicals and products of their metabolism. Vitamin E is considered to be the main chain-breaking antioxidant located in the membranes and effectively protecting them against lipid peroxidation. Recently, various polyphenol compounds, especially flavonoids, have received substantial attention because of their antioxidant activities in various in vitro systems. However, it was shown that flavonoid compounds are poorly absorbed in the gut and their concentrations in target tissues are too low to perform an effective antioxidant defences. The aim of the present paper is to review existing evidence about possible roles of various plant extracts provided with the diet in animal/poultry nutrition with a specific emphasis to their antioxidant activities.
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                Author and article information

                Contributors
                joris.michiels@ugent.be
                Journal
                J Anim Sci Biotechnol
                J Anim Sci Biotechnol
                Journal of Animal Science and Biotechnology
                BioMed Central (London )
                1674-9782
                2049-1891
                28 June 2016
                28 June 2016
                2016
                : 7
                : 37
                Affiliations
                [ ]Department of Animal Production, Laboratory for Animal Nutrition and Animal Product Quality, Ghent University, Proefhoevestraat 10, Melle, 9090 Belgium
                [ ]Centre of Excellence in the Animal Science Department, Ferdowsi University of Mashhad, P.O. Box: 91775–1163, Mashhad, Iran
                [ ]Department of Applied Biosciences, Ghent University, Valentin Vaerwyckweg 1, Ghent, 9000 Belgium
                Article
                97
                10.1186/s40104-016-0097-5
                4924307
                27354915
                a291a88c-577b-4077-886e-9c397c4f5081
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 3 January 2016
                : 15 June 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100007229, Bijzonder Onderzoeksfonds;
                Award ID: 01SF2711
                Award Recipient :
                Categories
                Review
                Custom metadata
                © The Author(s) 2016

                Animal science & Zoology
                antioxidant enzymes,avian uncoupling protein,electron transport chain,flavonoids,heat stress,mitochondrion,oxidative stress,poultry

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