Oxygen Recovery Up-regulates Avian UCP and ANT in Newly Hatched Ducklings

Overview

Journal J Comp Physiol B

Specialties Biochemistry
Endocrinology
Physiology

Date 2009 Oct 10

PMID 19816693

Citations 3

Authors

Benjamin Rey

Marion Spee

Maud Belouze

Aurelie Girard

Josiane Prost

Damien Roussel

Claude Duchamp

Affiliations

Soon will be listed here.

Abstract

At hatching, breaking eggshell induces a surge in oxygen availability that is likely to generate oxidative stress in newborn chicks. To investigate the involvement of potential adaptive antioxidant mechanisms, we explored some markers of oxidative stress and the regulation of muscle avian uncoupling protein (avUCP) and adenine nucleotide translocase (ANT) in ducklings in the peri-hatching period. When compared with pre-hatching levels, the amount of peroxidized lipids were increased 24 h after external pipping in gastrocnemius muscle (+37%) and heart (+39%) as well as the muscle avUCP mRNA expression (+60%) but the susceptibility of red blood cells to free radicals (a functional test of oxidative status) was not affected. In order to relate these changes to the oxidative transition of hatching, an imposed hypoxia/re-oxygenation protocol was used. Hatched chicks that had spent the last 24 h of incubation in artificial severe hypoxia showed a rise in muscle (+50%) and heart (+69%) lipid peroxidation, an increased susceptibility of red blood cells to free radicals, a marked over-expression of avUCP mRNA (+105%) and a rise in mitochondrial ANT content (+54%). These results suggest that avian UCP and ANT may contribute to prepare incubating eggs to the oxidative stress generated by the hypoxia/re-oxygenation transition naturally occurring at hatching.

Citing Articles

investigation of uncoupling protein function in avian genomes.

Davoodi P, Ghaderi-Zefrehei M, Muhaghegh Dolatabady M, Razmkabir M, Kianpour S, Esfahani E Front Vet Sci. 2023; 9:1085112.

PMID: 36744229 PMC: 9893418. DOI: 10.3389/fvets.2022.1085112.

Hypoxia during incubation and its effects on broiler's embryonic development.

Haron A, Ruzal M, Shinder D, Druyan S Poult Sci. 2021; 100(3):100951.

PMID: 33652530 PMC: 7936217. DOI: 10.1016/j.psj.2020.12.048.

Up-regulation of avian uncoupling protein in cold-acclimated and hyperthyroid ducklings prevents reactive oxygen species production by skeletal muscle mitochondria.

Rey B, Roussel D, Romestaing C, Belouze M, Rouanet J, Desplanches D BMC Physiol. 2010; 10:5.

PMID: 20426850 PMC: 2867930. DOI: 10.1186/1472-6793-10-5.

References

Esposito L, Melov S, Panov A, Cottrell B, Wallace D . Mitochondrial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci U S A. 1999; 96(9):4820-5. PMC: 21775. DOI: 10.1073/pnas.96.9.4820. View

Talbot D, Hanuise N, Rey B, Rouanet J, Duchamp C, Brand M . Superoxide activates a GDP-sensitive proton conductance in skeletal muscle mitochondria from king penguin (Aptenodytes patagonicus). Biochem Biophys Res Commun. 2003; 312(4):983-8. DOI: 10.1016/j.bbrc.2003.11.022. View

Cadenas E, Davies K . Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med. 2000; 29(3-4):222-30. DOI: 10.1016/s0891-5849(00)00317-8. View

Surai P, Sparks N . Comparative evaluation of the effect of two maternal diets on fatty acids, vitamin E and carotenoids in the chick embryo. Br Poult Sci. 2001; 42(2):252-9. DOI: 10.1080/00071660120048519. View

Echtay K, Esteves T, Pakay J, Jekabsons M, Lambert A, Portero-Otin M . A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 2003; 22(16):4103-10. PMC: 175801. DOI: 10.1093/emboj/cdg412. View

Collin A, Buyse J, van As P, Darras V, Malheiros R, Moraes V . Cold-induced enhancement of avian uncoupling protein expression, heat production, and triiodothyronine concentrations in broiler chicks. Gen Comp Endocrinol. 2003; 130(1):70-7. DOI: 10.1016/s0016-6480(02)00571-3. View

Collin A, Cassy S, Buyse J, Decuypere E, Damon M . Potential involvement of mammalian and avian uncoupling proteins in the thermogenic effect of thyroid hormones. Domest Anim Endocrinol. 2005; 29(1):78-87. DOI: 10.1016/j.domaniend.2005.02.007. View

Semenza G . Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J. 2007; 405(1):1-9. DOI: 10.1042/BJ20070389. View

Collin A, Malheiros R, Moraes V, van As P, Darras V, Taouis M . Effects of dietary macronutrient content on energy metabolism and uncoupling protein mRNA expression in broiler chickens. Br J Nutr. 2003; 90(2):261-9. DOI: 10.1079/bjn2003910. View

10.

Issartel J, Hervant F, de Fraipont M, Clobert J, Voituron Y . High anoxia tolerance in the subterranean salamander Proteus anguinus without oxidative stress nor activation of antioxidant defenses during reoxygenation. J Comp Physiol B. 2009; 179(4):543-51. DOI: 10.1007/s00360-008-0338-9. View

11.

Mujahid A, Sato K, Akiba Y, Toyomizu M . Acute heat stress stimulates mitochondrial superoxide production in broiler skeletal muscle, possibly via downregulation of uncoupling protein content. Poult Sci. 2006; 85(7):1259-65. DOI: 10.1093/ps/85.7.1259. View

12.

Raimbault S, Dridi S, Denjean F, Lachuer J, Couplan E, Bouillaud F . An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. Biochem J. 2001; 353(Pt 3):441-4. PMC: 1221587. DOI: 10.1042/0264-6021:3530441. View

13.

Skulachev V . Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q Rev Biophys. 1996; 29(2):169-202. DOI: 10.1017/s0033583500005795. View

14.

Mujahid A, Akiba Y, Toyomizu M . Olive oil-supplemented diet alleviates acute heat stress-induced mitochondrial ROS production in chicken skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2009; 297(3):R690-8. DOI: 10.1152/ajpregu.90974.2008. View

15.

Rey B, Halsey L, Dolmazon V, Rouanet J, Roussel D, Handrich Y . Long-term fasting decreases mitochondrial avian UCP-mediated oxygen consumption in hypometabolic king penguins. Am J Physiol Regul Integr Comp Physiol. 2008; 295(1):R92-R100. PMC: 2494815. DOI: 10.1152/ajpregu.00271.2007. View

16.

Hermes-Lima M, Zenteno-Savin T . Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp Biochem Physiol C Toxicol Pharmacol. 2002; 133(4):537-56. DOI: 10.1016/s1532-0456(02)00080-7. View

17.

Lesgards J, Durand P, Lassarre M, Stocker P, Lesgards G, Lanteaume A . Assessment of lifestyle effects on the overall antioxidant capacity of healthy subjects. Environ Health Perspect. 2002; 110(5):479-86. PMC: 1240836. DOI: 10.1289/ehp.02110479. View

18.

Nohl H . Generation of superoxide radicals as byproduct of cellular respiration. Ann Biol Clin (Paris). 1994; 52(3):199-204. View

19.

Storey K . Oxidative stress: animal adaptations in nature. Braz J Med Biol Res. 1996; 29(12):1715-33. View

20.

Speake B, Surai P, Gaal T, Mezes M, Noble R . Tissue-specific development of antioxidant systems during avian embryogenesis. Biochem Soc Trans. 1996; 24(2):182S. DOI: 10.1042/bst024182s. View