Embryonic Protein Undernutrition by Albumen Removal Programs the Hepatic Amino Acid and Glucose Metabolism during the Perinatal Period in an Avian Model.
[en] 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.
Embryonic Protein Undernutrition by Albumen Removal Programs the Hepatic Amino Acid and Glucose Metabolism during the Perinatal Period in an Avian Model.
Publication date :
2014
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, United States - California
Roseboom TJ, Painter RC, VanAbeelen AFM, Veenendaal MVE, DeRooij SR (2011) Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas 70: 141-145.
Ravelli ACJ, VanDerMeulen JHP, Michels RPJ, Osmond C, Barker DJP, et al. (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet 351: 173-177. (Pubitemid 28037007)
Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60: 5-20. (Pubitemid 34123501)
Gluckman PG, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305: 1733-1736. (Pubitemid 39249632)
Barker DJ (1995) The fetal and infant origins of disease. Eur J Clin Invest 25: 457-463.
Hill WL (1993) Importance of prenatal nutrition to the development of a precocial chick. Dev Psychobiol 26: 237-249.
Rao K, Xie J, Yang X, Chen L, Grossmann R, et al. (2009) Maternal lowprotein diet programmes offspring growth in association with alterations in yolk leptin deposition and gene expression in yolk-sac membrane, hypothalamus and muscle of developing Langshan chicken embryos. Br J Nutr 102: 848-857.
Everaert N, Metayer-Coustard S, Willemsen H, Han H, Song Z, et al. (2013) The effect of albumen removal before incubation (embryonic protein undernutrition) on the post-hatch performance, regulators of protein translation activation and proteolysis in neonatal broilers. Br J Nutr 110: 265-274.
Willems E, Wang Y, Willemsen H, Lesuisse J, Franssens L, et al. (2013) Partial albumen removal early during embryonic development of layer-type chickens has negative consequences on laying performance in adult life. Poult Sci 92: 1905-1915.
Willems E, Decuypere E, Buyse J, Everaert N (2014) Importance of albumen during embryonic development in avian species, with emphasis on domestic chicken. WPSJ (in press).
Freeman BM, VinceMA (1974) Development of the avian embryo: A behavioural and physiological study. London: Chapman And Hall, 362 p.
Darras VM, Katonen SP, Geris KL, Bergham LR, Kuhn ER (1996) Plasma thyroid levels and iodothyronine deiodinase activity following an acute glucocorticoid challenge in embryonic compared to posthatch chickens. Gen Comp Endocrinol 104: 203-212. (Pubitemid 26376479)
Dreiling CE, Brown DE, Casale L, Kelly L (1987) Musle glycogen: comparison of iodine binding and enzyme digestion assays and application to meat samples. Meat Sci 20: 167-177.
Van den Bergh G, Arckens L (2004) Fluorescent two-dimensional difference gel electrophoresis unveils the potential of gel-based proteomics. Curr Opin Biotechnol 15: 38-43. (Pubitemid 38224247)
Van den Bergh G, Clerens S, Cnops L, Vandesande F, Arckens L (2003) Fluorescent two-dimensional difference gel electrophoresis and mass spectrometry identify age-related protein expression differences for the primary visual cortex of kitten and adult cat. J Neurochem 85: 193-205. (Pubitemid 36389709)
VandenBergh G, Clerens S, Firestein BL, Burnat K, Arckens L (2006) Development and plasticity-related changes in protein expression patterns in cat visual cortex: A fluorescent two dimensional difference gel electrophoresis approach. Proteomics 6: 3821-3832. (Pubitemid 44065160)
Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: A single gel method for detecting changes in protein extracts. Electrophoresis 18: 2071- 2077. (Pubitemid 27501267)
Rasmussen R (2001) Quantification of the LightCycler. In: Meuer S, Wittwer C, Nakagawara K, editors. Rapid cycle real-time PCR, Methods and applications. Heidelberg: Springer Press, pp. 21-34.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCt method. Methods 25: 402-408. (Pubitemid 34164012)
Christensen VL, Wineland MJ, Fasenko GM, Donaldson WE (2001) Egg storage effects on plasma glucose and supply and demand tissue glycogen concentrations of broiler embryos. Poult Sci 80: 1729-1735. (Pubitemid 33659822)
Wang Y, Li Y, Willems E, Willemsen H, Franssens L, et al. (2014) Effects of spread of hatch and delayed feed access on broiler post-hatch performance up to day 5. Animal 8: 610-617.
Whorwood CB, Firth KM, Budge H, Symonds ME (2001) Maternal under nutrition during early to mid gestation programs tissuespecific alterations in the expression of the glucocorticoid receptor, 11b-hydroxysteroid dehydrogenase isoforms, and type 1 angiotensin II receptor in neonatal sheep. Endocrinology 142: 2854-2864. (Pubitemid 32575520)
Bertram C, Trowern AR, Copin N, Jackson AA, Whorwood CB (2001) The maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11b-hydroxysteroid dehydrogenase: potential molecular mechanisms underlying the programming of hypertension in utero. Endocrinology 142: 2841-2853. (Pubitemid 32575519)
Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135: 1382-1386. (Pubitemid 40799599)
McNabb FMA (2000) Thyroids. In: Whittow GC, editor. Avian Physiology. New York: Academic Press, pp. 461-471.
Kono T, Nishida M, Nishiki Y, Seki Y, Sato K, et al. (2005) Characterisation of glucose transporter (GLUT) gene expression in broiler chickens. Br Poult Sci 46: 510-515. (Pubitemid 41284633)
Lesage J, Hahn D, Leonhardt M, Blondeau B, Breant B, et al. (2002) Maternal undernutrition during late gestation-induced intrauterine growth restriction in the rat is associated with impaired placental GLUT3 expression, but does not correlate with endogenous corticosterone levels. J Endocrinol 174: 37-43. (Pubitemid 34830930)
Nguyen LT, Muhlhausler BS, Botting KJ, Morrison JL (2010) Maternal undernutrition alters fat cell size distribution, but not lipogenic gene expression in the visceral fat of the late gestation guinea pig fetus. Placenta 31: 902-909.
Seki Y, Sato K, Kono T, Abe H, Akiba Y (2003) Broiler chickens (Ross strain) lack insulin-responsive glucose transporter GLUT4 and have GLUT8 cDNA. Gen Comp Endocrinol 133: 80-87. (Pubitemid 36937136)
Hamada T, Matsumoto M (1984) Effects of nutrition and ontogeny of liver cytosolic and mitochondrial phosphoenolpyruvate carboxykinase activity of the rat, hamster, guinea-pig, pig, kid, calf and chick. Comp Biochem Physiol B77: 547-550.
Hod Y, Cook JS, Weldon SL, Short JM, Wynshaw-Boris A, et al. (1986) Differential expression of the genes for the mitochondrial and cytosolic forms of phosphoenolpyruvate carboxykinase. Ann N Y Acad Sci 478: 31-45. (Pubitemid 17010988)
Desai M, Byrne CD, Zhang J, Petry CJ, Lucas A, et al. (1997) Programming of hepatic insulin-sensitive enzymes in offspring of rat dams fed a protein-restricted diet. Am J Physiol Gastrointest Liver Physiol 272: G1083-G1090.
Lane RH, MacLennan NK, Hsu JL, Janke SM, Pham TD (2002) Increased hepatic peroxisome proliferator-activated receptor-c coactivator-1 gene expression in a rat model of intrauterine growth retardation and subsequent insulin resistance. Endocrinology 143: 2486-2490. (Pubitemid 34701309)
Matthiesen CF, Blache D, Thomsen PD, Hansen NE, Tauson A-H (2010) Effect of late gestation low protein supply to mink (Mustela vison) dams on reproductive performance and metabolism of dam and offspring. Arch Anim Nutr 64: 56-76.
Finkler MS, VanOrman JB, Sotherland PR (1998) Experimental manipulation of egg quality in chickens: influence of albumen and yolk on the size and body composition of near-term embryos in a precocial bird. J Comp Physiol B168: 17-24. (Pubitemid 28202450)
