Embryonic protein undernutrition by albumen removal programs the hepatic amino acid and glucose metabolism during the perinatal period in an avian model

Different animal models have been used to study the effects of prenatal protein undernutrition and the mechanisms by which these occur. In mammals, the maternal diet is manipulated, exerting both direct nutritional and indirect hormonal effects. Chicken embryos develop independent from the hen in th...

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Veröffentlicht in:PloS one 2014-04, Vol.9 (4), p.e94902-e94902
Hauptverfasser: Willems, Els, Hu, Tjing-Tjing, Soler Vasco, Laura, Buyse, Johan, Decuypere, Eddy, Arckens, Lutgarde, Everaert, Nadia
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container_title PloS one
container_volume 9
creator Willems, Els
Hu, Tjing-Tjing
Soler Vasco, Laura
Buyse, Johan
Decuypere, Eddy
Arckens, Lutgarde
Everaert, Nadia
description Different animal models have been used to study the effects of prenatal protein undernutrition and the mechanisms by which these occur. In mammals, the maternal diet is manipulated, exerting both direct nutritional and indirect hormonal effects. Chicken embryos develop independent from the hen in the egg. Therefore, in the chicken, the direct effects of protein deficiency by albumen removal early during incubation can be examined. Prenatal protein undernutrition was established in layer-type eggs by the partial replacement of albumen by saline at embryonic day 1 (albumen-deprived group), compared to a mock-treated sham and a non-treated control group. At hatch, survival of the albumen-deprived group was lower compared to the control and sham group due to increased early mortality by the manipulation. No treatment differences in yolk-free body weight or yolk weight could be detected. The water content of the yolk was reduced, whereas the water content of the carcass was increased in the albumen-deprived group, compared to the control group, indicating less uptake of nutrients from the yolk. At embryonic day 16, 20 and at hatch, plasma triiodothyronine (T3), corticosterone, lactate or glucose concentrations and hepatic glycogen content were not affected by treatment. At embryonic day 20, the plasma thyroxine (T4) concentrations of the albumen-deprived embryos was reduced compared to the control group, indicating a decreased metabolic rate. Screening for differential protein expression in the liver at hatch using two-dimensional difference gel electrophoresis revealed not only changed abundance of proteins important for amino acid metabolism, but also of enzymes related to energy and glucose metabolism. Interestingly, GLUT1, a glucose transporter, and PCK2 and FBP1, two out of three regulatory enzymes of the gluconeogenesis were dysregulated. No parallel differences in gene expressions causing the differences in protein abundance could be detected pointing to post-transcriptional or post-translational regulation of the observed differences.
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In mammals, the maternal diet is manipulated, exerting both direct nutritional and indirect hormonal effects. Chicken embryos develop independent from the hen in the egg. Therefore, in the chicken, the direct effects of protein deficiency by albumen removal early during incubation can be examined. Prenatal protein undernutrition was established in layer-type eggs by the partial replacement of albumen by saline at embryonic day 1 (albumen-deprived group), compared to a mock-treated sham and a non-treated control group. At hatch, survival of the albumen-deprived group was lower compared to the control and sham group due to increased early mortality by the manipulation. No treatment differences in yolk-free body weight or yolk weight could be detected. The water content of the yolk was reduced, whereas the water content of the carcass was increased in the albumen-deprived group, compared to the control group, indicating less uptake of nutrients from the yolk. At embryonic day 16, 20 and at hatch, plasma triiodothyronine (T3), corticosterone, lactate or glucose concentrations and hepatic glycogen content were not affected by treatment. At embryonic day 20, the plasma thyroxine (T4) concentrations of the albumen-deprived embryos was reduced compared to the control group, indicating a decreased metabolic rate. Screening for differential protein expression in the liver at hatch using two-dimensional difference gel electrophoresis revealed not only changed abundance of proteins important for amino acid metabolism, but also of enzymes related to energy and glucose metabolism. Interestingly, GLUT1, a glucose transporter, and PCK2 and FBP1, two out of three regulatory enzymes of the gluconeogenesis were dysregulated. No parallel differences in gene expressions causing the differences in protein abundance could be detected pointing to post-transcriptional or post-translational regulation of the observed differences.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0094902</identifier><identifier>PMID: 24740266</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abundance ; Acids ; Albumen ; Albumins - deficiency ; Albumins - pharmacology ; Amino acids ; Amino Acids - metabolism ; Animal models ; Animal production &amp; animal husbandry ; Animals ; Animals, Newborn ; Avian Proteins - genetics ; Avian Proteins - metabolism ; Biology and Life Sciences ; Body weight ; Chick Embryo ; Chickens ; Corticosterone ; Dehydrogenases ; Diet ; Disease Models, Animal ; Eggs ; Eggs - analysis ; Electrophoresis, Gel, Two-Dimensional ; Embryo ; Embryos ; Endocrinology ; Energy metabolism ; Enzymes ; Female ; Fetuses ; Fructose-Bisphosphatase - genetics ; Fructose-Bisphosphatase - metabolism ; Gel electrophoresis ; Gene expression ; Gene Expression Regulation, Developmental ; Gene regulation ; Gluconeogenesis ; Glucose ; Glucose - metabolism ; Glucose transporter ; Glucose Transporter Type 1 - genetics ; Glucose Transporter Type 1 - metabolism ; Glycogen ; Glycogen - metabolism ; Health aspects ; Hormonal effects ; Humans ; Hypotheses ; Incubation ; Infertility ; Insulin resistance ; Kwashiorkor - embryology ; Kwashiorkor - genetics ; Kwashiorkor - metabolism ; Laboratories ; Lactic acid ; Life Sciences ; Liver ; Liver - drug effects ; Liver - embryology ; Liver - metabolism ; Livestock ; Malnutrition ; Metabolic rate ; Metabolism ; Metabolites ; Moisture content ; Mortality ; Nutrient uptake ; Nutrients ; Nutrition ; Phosphoenolpyruvate Carboxykinase (ATP) - genetics ; Phosphoenolpyruvate Carboxykinase (ATP) - metabolism ; Physiological aspects ; Physiology ; Post-transcription ; Post-translation ; Poultry ; Poultry Diseases - embryology ; Poultry Diseases - genetics ; Poultry Diseases - metabolism ; Productions animales &amp; zootechnie ; Protein deficiency ; Proteins ; Research and Analysis Methods ; Reverse Transcriptase Polymerase Chain Reaction ; Rodents ; Sciences du vivant ; Studies ; Survival Analysis ; Tandem Mass Spectrometry ; Thyroid hormones ; Thyroxine ; Thyroxine - blood ; Undernutrition ; Water content ; Weight reduction ; Yolk</subject><ispartof>PloS one, 2014-04, Vol.9 (4), p.e94902-e94902</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Willems et al. 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In mammals, the maternal diet is manipulated, exerting both direct nutritional and indirect hormonal effects. Chicken embryos develop independent from the hen in the egg. Therefore, in the chicken, the direct effects of protein deficiency by albumen removal early during incubation can be examined. Prenatal protein undernutrition was established in layer-type eggs by the partial replacement of albumen by saline at embryonic day 1 (albumen-deprived group), compared to a mock-treated sham and a non-treated control group. At hatch, survival of the albumen-deprived group was lower compared to the control and sham group due to increased early mortality by the manipulation. No treatment differences in yolk-free body weight or yolk weight could be detected. The water content of the yolk was reduced, whereas the water content of the carcass was increased in the albumen-deprived group, compared to the control group, indicating less uptake of nutrients from the yolk. At embryonic day 16, 20 and at hatch, plasma triiodothyronine (T3), corticosterone, lactate or glucose concentrations and hepatic glycogen content were not affected by treatment. At embryonic day 20, the plasma thyroxine (T4) concentrations of the albumen-deprived embryos was reduced compared to the control group, indicating a decreased metabolic rate. Screening for differential protein expression in the liver at hatch using two-dimensional difference gel electrophoresis revealed not only changed abundance of proteins important for amino acid metabolism, but also of enzymes related to energy and glucose metabolism. Interestingly, GLUT1, a glucose transporter, and PCK2 and FBP1, two out of three regulatory enzymes of the gluconeogenesis were dysregulated. No parallel differences in gene expressions causing the differences in protein abundance could be detected pointing to post-transcriptional or post-translational regulation of the observed differences.</description><subject>Abundance</subject><subject>Acids</subject><subject>Albumen</subject><subject>Albumins - deficiency</subject><subject>Albumins - pharmacology</subject><subject>Amino acids</subject><subject>Amino Acids - metabolism</subject><subject>Animal models</subject><subject>Animal production &amp; animal husbandry</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Avian Proteins - genetics</subject><subject>Avian Proteins - metabolism</subject><subject>Biology and Life Sciences</subject><subject>Body weight</subject><subject>Chick Embryo</subject><subject>Chickens</subject><subject>Corticosterone</subject><subject>Dehydrogenases</subject><subject>Diet</subject><subject>Disease Models, Animal</subject><subject>Eggs</subject><subject>Eggs - analysis</subject><subject>Electrophoresis, Gel, Two-Dimensional</subject><subject>Embryo</subject><subject>Embryos</subject><subject>Endocrinology</subject><subject>Energy metabolism</subject><subject>Enzymes</subject><subject>Female</subject><subject>Fetuses</subject><subject>Fructose-Bisphosphatase - genetics</subject><subject>Fructose-Bisphosphatase - metabolism</subject><subject>Gel electrophoresis</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene regulation</subject><subject>Gluconeogenesis</subject><subject>Glucose</subject><subject>Glucose - metabolism</subject><subject>Glucose transporter</subject><subject>Glucose Transporter Type 1 - genetics</subject><subject>Glucose Transporter Type 1 - metabolism</subject><subject>Glycogen</subject><subject>Glycogen - metabolism</subject><subject>Health aspects</subject><subject>Hormonal effects</subject><subject>Humans</subject><subject>Hypotheses</subject><subject>Incubation</subject><subject>Infertility</subject><subject>Insulin resistance</subject><subject>Kwashiorkor - embryology</subject><subject>Kwashiorkor - genetics</subject><subject>Kwashiorkor - metabolism</subject><subject>Laboratories</subject><subject>Lactic acid</subject><subject>Life Sciences</subject><subject>Liver</subject><subject>Liver - drug effects</subject><subject>Liver - embryology</subject><subject>Liver - metabolism</subject><subject>Livestock</subject><subject>Malnutrition</subject><subject>Metabolic rate</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Moisture content</subject><subject>Mortality</subject><subject>Nutrient uptake</subject><subject>Nutrients</subject><subject>Nutrition</subject><subject>Phosphoenolpyruvate Carboxykinase (ATP) - genetics</subject><subject>Phosphoenolpyruvate Carboxykinase (ATP) - metabolism</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Post-transcription</subject><subject>Post-translation</subject><subject>Poultry</subject><subject>Poultry Diseases - embryology</subject><subject>Poultry Diseases - genetics</subject><subject>Poultry Diseases - metabolism</subject><subject>Productions animales &amp; zootechnie</subject><subject>Protein deficiency</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Rodents</subject><subject>Sciences du vivant</subject><subject>Studies</subject><subject>Survival Analysis</subject><subject>Tandem Mass Spectrometry</subject><subject>Thyroid hormones</subject><subject>Thyroxine</subject><subject>Thyroxine - blood</subject><subject>Undernutrition</subject><subject>Water content</subject><subject>Weight reduction</subject><subject>Yolk</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk9tq3DAQhk1padK0b1BaQ6E0F7vVwZLtm0IIaRMIBHq6FTrMehVkaSPZS_MmfdzKu5uQDbkoNvYw_v5_xoOmKN5iNMe0xp-vwxi9dPNV8DBHqK1aRJ4Vh7ilZMYJos8fxAfFq5SuEWK04fxlcUCqukKE88Pi71mv4m3wVperGAawvhy9gejHIdrBBl-q21I6Nfbgywh9WEs3kV2UfSqHJZRLWMkhy2VvfSiltqaU3pSdG3VIUPYwSBWcTX1pxmh9txGtIIdymLxyFEyZ68p8r21-9sGAe128WEiX4M3ufVT8-nr28_R8dnn17eL05HKm6xoNM2BUUaQUUpgpgyvFTYsaqjSWnBGDEKI1kahVWjeNZhS4IopxgyVGRFeMHhXvt74rF5LYDTUJzDBvWcXrJhMXW8IEeS1W0fYy3oogrdgkQuyEjHkCDkSNZZZwpiupK8qaXAkAMM1GuSHVZq8vu2qj6sFo8EOUbs90_4u3S9GFtaBt09JNu3Rr4Cx0kIsrK9ZkI9zEo8vdaKFAEMIbgTmvq6ns8Va1fFTs_ORSTDmEOWJ1xdc4s592LcZwM0IaRG-TBuekhzBuJlM3DWqayfbDI_Tp-e2oTuYRWb8I-c_0ZCpOaM1YU6GWZGr-BJUvA73V-YwvbM7vCY73BJkZ4M_QyTElcfHj-_-zV7_32Y8P2CVINyxTcOO0DGkfrLagjiGlCIv7yWIkphW9m4aYVlTsVjTL3j08Aveiu52k_wD-iDeM</recordid><startdate>20140401</startdate><enddate>20140401</enddate><creator>Willems, Els</creator><creator>Hu, Tjing-Tjing</creator><creator>Soler Vasco, Laura</creator><creator>Buyse, Johan</creator><creator>Decuypere, Eddy</creator><creator>Arckens, Lutgarde</creator><creator>Everaert, Nadia</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>Q33</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140401</creationdate><title>Embryonic protein undernutrition by albumen removal programs the hepatic amino acid and glucose metabolism during the perinatal period in an avian model</title><author>Willems, Els ; Hu, Tjing-Tjing ; Soler Vasco, Laura ; Buyse, Johan ; Decuypere, Eddy ; Arckens, Lutgarde ; Everaert, Nadia</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c770t-e53b30bb0b15bd14b6d9083bc1a652d000372a09bcc88c53e6b2b56d1a102c453</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Abundance</topic><topic>Acids</topic><topic>Albumen</topic><topic>Albumins - deficiency</topic><topic>Albumins - pharmacology</topic><topic>Amino acids</topic><topic>Amino Acids - metabolism</topic><topic>Animal models</topic><topic>Animal production &amp; animal husbandry</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Avian Proteins - genetics</topic><topic>Avian Proteins - metabolism</topic><topic>Biology and Life Sciences</topic><topic>Body weight</topic><topic>Chick Embryo</topic><topic>Chickens</topic><topic>Corticosterone</topic><topic>Dehydrogenases</topic><topic>Diet</topic><topic>Disease Models, Animal</topic><topic>Eggs</topic><topic>Eggs - analysis</topic><topic>Electrophoresis, Gel, Two-Dimensional</topic><topic>Embryo</topic><topic>Embryos</topic><topic>Endocrinology</topic><topic>Energy metabolism</topic><topic>Enzymes</topic><topic>Female</topic><topic>Fetuses</topic><topic>Fructose-Bisphosphatase - genetics</topic><topic>Fructose-Bisphosphatase - metabolism</topic><topic>Gel electrophoresis</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene regulation</topic><topic>Gluconeogenesis</topic><topic>Glucose</topic><topic>Glucose - metabolism</topic><topic>Glucose transporter</topic><topic>Glucose Transporter Type 1 - genetics</topic><topic>Glucose Transporter Type 1 - metabolism</topic><topic>Glycogen</topic><topic>Glycogen - metabolism</topic><topic>Health aspects</topic><topic>Hormonal effects</topic><topic>Humans</topic><topic>Hypotheses</topic><topic>Incubation</topic><topic>Infertility</topic><topic>Insulin resistance</topic><topic>Kwashiorkor - embryology</topic><topic>Kwashiorkor - genetics</topic><topic>Kwashiorkor - metabolism</topic><topic>Laboratories</topic><topic>Lactic acid</topic><topic>Life Sciences</topic><topic>Liver</topic><topic>Liver - drug effects</topic><topic>Liver - embryology</topic><topic>Liver - metabolism</topic><topic>Livestock</topic><topic>Malnutrition</topic><topic>Metabolic rate</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Moisture content</topic><topic>Mortality</topic><topic>Nutrient uptake</topic><topic>Nutrients</topic><topic>Nutrition</topic><topic>Phosphoenolpyruvate Carboxykinase (ATP) - genetics</topic><topic>Phosphoenolpyruvate Carboxykinase (ATP) - metabolism</topic><topic>Physiological aspects</topic><topic>Physiology</topic><topic>Post-transcription</topic><topic>Post-translation</topic><topic>Poultry</topic><topic>Poultry Diseases - embryology</topic><topic>Poultry Diseases - genetics</topic><topic>Poultry Diseases - metabolism</topic><topic>Productions animales &amp; 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In mammals, the maternal diet is manipulated, exerting both direct nutritional and indirect hormonal effects. Chicken embryos develop independent from the hen in the egg. Therefore, in the chicken, the direct effects of protein deficiency by albumen removal early during incubation can be examined. Prenatal protein undernutrition was established in layer-type eggs by the partial replacement of albumen by saline at embryonic day 1 (albumen-deprived group), compared to a mock-treated sham and a non-treated control group. At hatch, survival of the albumen-deprived group was lower compared to the control and sham group due to increased early mortality by the manipulation. No treatment differences in yolk-free body weight or yolk weight could be detected. The water content of the yolk was reduced, whereas the water content of the carcass was increased in the albumen-deprived group, compared to the control group, indicating less uptake of nutrients from the yolk. At embryonic day 16, 20 and at hatch, plasma triiodothyronine (T3), corticosterone, lactate or glucose concentrations and hepatic glycogen content were not affected by treatment. At embryonic day 20, the plasma thyroxine (T4) concentrations of the albumen-deprived embryos was reduced compared to the control group, indicating a decreased metabolic rate. Screening for differential protein expression in the liver at hatch using two-dimensional difference gel electrophoresis revealed not only changed abundance of proteins important for amino acid metabolism, but also of enzymes related to energy and glucose metabolism. Interestingly, GLUT1, a glucose transporter, and PCK2 and FBP1, two out of three regulatory enzymes of the gluconeogenesis were dysregulated. No parallel differences in gene expressions causing the differences in protein abundance could be detected pointing to post-transcriptional or post-translational regulation of the observed differences.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24740266</pmid><doi>10.1371/journal.pone.0094902</doi><oa>free_for_read</oa></addata></record>
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subjects Abundance
Acids
Albumen
Albumins - deficiency
Albumins - pharmacology
Amino acids
Amino Acids - metabolism
Animal models
Animal production & animal husbandry
Animals
Animals, Newborn
Avian Proteins - genetics
Avian Proteins - metabolism
Biology and Life Sciences
Body weight
Chick Embryo
Chickens
Corticosterone
Dehydrogenases
Diet
Disease Models, Animal
Eggs
Eggs - analysis
Electrophoresis, Gel, Two-Dimensional
Embryo
Embryos
Endocrinology
Energy metabolism
Enzymes
Female
Fetuses
Fructose-Bisphosphatase - genetics
Fructose-Bisphosphatase - metabolism
Gel electrophoresis
Gene expression
Gene Expression Regulation, Developmental
Gene regulation
Gluconeogenesis
Glucose
Glucose - metabolism
Glucose transporter
Glucose Transporter Type 1 - genetics
Glucose Transporter Type 1 - metabolism
Glycogen
Glycogen - metabolism
Health aspects
Hormonal effects
Humans
Hypotheses
Incubation
Infertility
Insulin resistance
Kwashiorkor - embryology
Kwashiorkor - genetics
Kwashiorkor - metabolism
Laboratories
Lactic acid
Life Sciences
Liver
Liver - drug effects
Liver - embryology
Liver - metabolism
Livestock
Malnutrition
Metabolic rate
Metabolism
Metabolites
Moisture content
Mortality
Nutrient uptake
Nutrients
Nutrition
Phosphoenolpyruvate Carboxykinase (ATP) - genetics
Phosphoenolpyruvate Carboxykinase (ATP) - metabolism
Physiological aspects
Physiology
Post-transcription
Post-translation
Poultry
Poultry Diseases - embryology
Poultry Diseases - genetics
Poultry Diseases - metabolism
Productions animales & zootechnie
Protein deficiency
Proteins
Research and Analysis Methods
Reverse Transcriptase Polymerase Chain Reaction
Rodents
Sciences du vivant
Studies
Survival Analysis
Tandem Mass Spectrometry
Thyroid hormones
Thyroxine
Thyroxine - blood
Undernutrition
Water content
Weight reduction
Yolk
title Embryonic protein undernutrition by albumen removal programs the hepatic amino acid and glucose metabolism during the perinatal period in an avian model
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