Effects of nutritional programing on growth and metabolism caused by albumen removal in an avian model

Willems, Els; Koppenol, Astrid; Ketelaere, Bart De; Wang, Yufeng; Franssens, Lies; Buyse, Johan; Decuypere, Eddy; Everaert, Nadia

doi:10.1530/joe-14-0525

Cited by 11 publications

(27 citation statements)

References 33 publications

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“…Indeed, in one recent study, a lack of catch up growth was evident. Albumen removal from chicken eggs resulted in reduced body weight of the hens 55 weeks after hatching (Willems et al, 2015a), and egg laying performance of adult hens is also altered (Willems et al, 2013). Similar results occurred in a separate study by this research group, but feed intake was increased in juveniles undernourished as embryos, apparently without accompanying body mass increases up to normal levels (Willems et al, 2015b).…”

Section: Fetal Programming -Beyond Mammals To Birdssupporting

confidence: 80%

Cardio-respiratory development in bird embryos: new insights from a venerable animal model

2016

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-The avian embryo is a time-honored animal model for understanding vertebrate development. A key area of extensive study using bird embryos centers on developmental phenotypic plasticity of the cardio-respiratory system and how its normal development can be affected by abiotic factors such as temperature and oxygen availability. Through the investigation of the plasticity of development, we gain a better understanding of both the regulation of the developmental process and the embryo's capacity for self-repair. Additionally, experiments with abiotic and biotic stressors during development have helped delineate not just critical windows for avian cardio-respiratory development, but the general characteristics (e.g., timing and dose-dependence) of critical windows in all developing vertebrates. Avian embryos are useful in exploring fetal programming, in which early developmental experiences have implications (usually negative) later in life. The ability to experimentally manipulate the avian embryo without the interference of maternal behavior or physiology makes it particularly useful in future studies of fetal programming. The bird embryo is also a key participant in studies of transgenerational epigenetics, whether by egg provisioning or effects on the germline that are transmitted to the F1 generation (or beyond). Finally, the avian embryo is heavily exploited in toxicology, in which both toxicological testing of potential consumer products as well as the consequences of exposure to anthropogenic pollutants are routinely carried out in the avian embryo. The avian embryo thus proves useful on numerous experimental fronts as an animal model that is concurrently both of adequate complexity and sufficient simplicity for probing vertebrate cardio-respiratory development.

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Section: Fetal Programming -Beyond Mammals To Birdssupporting

confidence: 80%

Cardio-respiratory development in bird embryos: new insights from a venerable animal model

2016

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“…Previous results demonstrated long‐term effects of prenatal protein undernutrition by albumen removal (Willems et al . , ). Major phenotypical effects were not observed in the late embryonic phase before hatching (Willems et al .…”

Section: Discussionmentioning

confidence: 99%

Reduced protein availability by albumen removal during chicken embryogenesis decreases body weight and induces hormonal changes

Willems

Wang

Koppenol

et al. 2015

Experimental Physiology

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New Findings r What is the central question of this study?Prenatal protein undernutrition by albumen removal in an avian model of fetal programming leads to long-term programming effects, but when do these effects first appear and are these programming effects regulated by the same candidate genes as in mammals? r What is the main finding and its importance?The present results indicate that prenatal protein undernutrition by albumen removal induces phenotypical and hormonal changes in the early posthatch period, when the mismatch between the prenatal and postnatal environment first arises, but these changes are not accompanied by an altered gene expression of the selected candidate genes.Studies of the chicken offer a unique model for investigation of the direct effects of reduced prenatal protein availability by the partial replacement of albumen with saline in eggs at embryonic day 1 (albumen-deprived group). The results were compared with mock-treated sham chicks and non-treated control chicks. Although no differences in hatch weight were found, body weight and growth were reduced in the albumen-deprived chicks until 3 weeks of age. The feed intake of the albumen-deprived chicks, however, was increased compared with the control (day 13-21) and the sham chicks (day 16-18). In the albumen-deprived chicks, the ratio of thyroxine to 3,5,3 -triiodothyronine in the plasma was increased compared with the control chicks, whereas the plasma corticosterone level was increased only at day 7 compared with both other groups. The plasma glucose concentration and glucose tolerance were not affected by treatment. Several candidate genes previously associated with effects of prenatal protein deprivation in mammals were examined in the liver of newly hatched chicks. Gene expression of glycogen synthase 2, glycogen phosphorylase 1, peroxisome proliferator-activated receptor α and γ and glucocorticoid receptor was not affected by the treatment. In conclusion, reduction of prenatal protein availability led to differences in body weight and influenced hormones involved in metabolism and growth. Gene expression of the selected candidate genes was not altered, in contrast to mammals.

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“…All eggs were cleaned using a solution of 70% ethanol applied with a towel. At 2 days of embryonic development (E2), holes were carefully drilled on blunt end of eggs from the experimental group, and 3 ml of albumen extracted by means of sterile 5 mL disposable syringes (Willems et al, 2014b, 2015). This volume corresponds nearly to 10% of the total volume (average volume 32.49 cm 3 ).…”

Section: Methodsmentioning

confidence: 99%

“…Commonly, experimental manipulations for the purposes of studying malnutrition involve removal of either albumen or yolk via a hole in the egg shell (Finkler et al, 1998; Ferrari et al, 2006; Alquati et al, 2007; Bonisoli-Alquati et al, 2008; Everaert et al, 2013; Willems et al, 2013, 2014a,b, 2015). Several studies have identified changes generated by the removal of albumen in early ontogeny (after hatching), including time to hatching, begging behavior, reductions in body mass, decreased plasma T4, high plasma uric acid concentration, upregulation of TCA cycle enzymes in liver, morphology, survival, and hatching asynchrony (Finkler et al, 1998; Ferrari et al, 2006; Alquati et al, 2007; Bonisoli-Alquati et al, 2008; Willems et al, 2014b).…”

Section: Introductionmentioning

confidence: 99%

“…Several studies have identified changes generated by the removal of albumen in early ontogeny (after hatching), including time to hatching, begging behavior, reductions in body mass, decreased plasma T4, high plasma uric acid concentration, upregulation of TCA cycle enzymes in liver, morphology, survival, and hatching asynchrony (Finkler et al, 1998; Ferrari et al, 2006; Alquati et al, 2007; Bonisoli-Alquati et al, 2008; Willems et al, 2014b). Regarding responses generated in later ontogeny (juvenile growth and adulthood), an increase in immune response, higher mRNA expression of muscle ring finger-1 ( MuRF1 , a gene related to proteolysis), reduction of body mass, decreased egg production accompanied by higher proportion of yolk/ albumen, and long-term alteration of the hepatic transcriptome in chickens have been reported (Everaert et al, 2013; Willems et al, 2013, 2015, 2016). …”

Section: Introductionmentioning

confidence: 99%

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Energetic Effects of Pre-hatch Albumen Removal on Embryonic Development and Early Ontogeny in Gallus gallus

et al. 2017

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Studies on the yolk and albumen content in bird eggs, and the effects of variations in their relative loads in the phenotype of the birds, have revealed multiple consequences at different levels of biological organization, from biochemical traits to behavior. However, little is known about the effect of albumen variation on energetics performance during development and early ontogeny, despite the fact that variation in energy expenditure may have consequences in terms of fitness for both feral and domestic species. In this work, we evaluated experimentally whether variations in the content of albumen of Gallus gallus eggs could generate differences in metabolic rates during embryonic development. Additionally, we assessed changes in the activity of mitochondrial enzymes (cytochrome c oxidase and citrate synthase) in skeletal muscles and liver. Finally, we evaluated the success of hatching of these embryos and their metabolic rates (MR) post-hatching. The results revealed a significant reduction in MR in the last fifth of embryonic life, and reduced catabolic activities in the skeletal muscle of chicks hatched from albumen-removed eggs. However, the same group demonstrated an increase in catabolic activity in the liver, suggesting the existence of changes in energy allocation between tissues. Besides, we found a decrease in hatching success in the albumen-removed group, suggesting a negative effect of the lower albumen content on eggs, possibly due to lower catabolic activities in skeletal muscle. We also found a compensatory phenomenon in the first week after hatching, i.e., birds from albumen-removed eggs did not show a decrease in MR either at thermoneutral temperatures or at 10°C, compared to the control group. Collectively, our data suggest that a reduction in albumen may generate a trade-off between tissue metabolic activities, and may explain the differences in metabolic rates and hatching success, supporting the immediate adaptive response (IAR) hypothesis.

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Effects of nutritional programing on growth and metabolism caused by albumen removal in an avian model

Cited by 11 publications

References 33 publications

Cardio-respiratory development in bird embryos: new insights from a venerable animal model

Cardio-respiratory development in bird embryos: new insights from a venerable animal model

Reduced protein availability by albumen removal during chicken embryogenesis decreases body weight and induces hormonal changes

Energetic Effects of Pre-hatch Albumen Removal on Embryonic Development and Early Ontogeny in Gallus gallus

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