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Maternal low-protein 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

  • Kaiqing Rao (a1) (a2), Jingjing Xie (a1), Xiaojing Yang (a1), Lei Chen (a1), Roland Grossmann (a3) and Ruqian Zhao (a1)...

Abstract

The present study was aimed to investigate the mechanism underlying the influence of maternal low-protein (LP) diet on offspring growth in the chicken. One hundred and twenty Chinese inbred Langshan breeder hens were allocated randomly into two groups fed diets containing low (10 %, LP) or normal (15 %) crude protein levels. Low dietary protein did not affect the body weight of hens, but significantly decreased the laying rate and egg weight. The yolk leptin content was significantly lower in eggs laid by LP hens, while no differences were detected for yolk contents of corticosterone, tri-iodothyronine (T3) or thyroxine. Despite significantly lower hatch weight, the LP offspring demonstrated obviously higher serum T3 concentration, which is in accordance with the faster post-hatch growth rate achieving significantly heavier body weight and pectoralis major muscle weight 4 weeks post-hatching. Expression of 20-hydroxysteroid dehydrogenase (20-HSD) mRNA in the yolk-sac membrane was significantly down-regulated at embryonic day 14, whereas that of transthyretin and leptin receptor (LepR) was not altered. Moreover, hypothalamic expression of 20-HSD, glucocorticoid receptors, thyrotropin-releasing hormone and LepR mRNA was significantly up-regulated in the LP group compared with their control counterparts. In the pectoralis major muscle, significantly higher expression of insulin-like growth factor (IGF)-I and IGF-I receptor mRNA was observed in LP embryos. The present study provides evidence that maternal LP diet programmes post-hatch growth of the offspring. The associated alterations in yolk leptin deposition as well as in yolk-sac membrane, fetal hypothalamus and muscle gene expression may be involved in mediating such programming effect in the chicken.

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      Maternal low-protein 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
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      Maternal low-protein 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
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Corresponding author

*Corresponding author: Dr Ruqian Zhao, fax +86 2584398669, email zhao.ruqian@gmail.com

References

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1Symonds, ME, Stephenson, T, Gardner, DS, et al. (2007) Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reprod Fertil 19, 5363.
2Myatt, L (2006) Placental adaptive responses and fetal programming. J Physiol 572, 2530.
3Hanson, MA & Gluckman, PD (2008) Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol 102, 9093.
4Drake, AJ, Walker, BR & Seckl, JR (2005) Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol 288, R34R38.
5Mostyn, A, Sebert, S, Litten, JC, et al. (2006) Influence of porcine genotype on the abundance of thyroid hormones and leptin in sow milk and its impact on growth, metabolism and expression of key adipose tissue genes in offspring. J Endocrinol 190, 631639.
6Miralles, O, Sánchez, J, Palou, A, et al. (2006) A physiological role of breast milk leptin in body weight control in developing infants. Obesity (Silver Spring) 14, 13711377.
7Stewart, PM & Krozowski, ZS (1999) 11 beta-Hydroxysteroid dehydrogenase. Vitam Horm 57, 249324.
8Baratta, M (2002) Leptin – from a signal of adiposity to a hormonal mediator in peripheral tissues. Med Sci Monit 8, 282292.
9McKinnon, B, Li, H, Richard, K, et al. (2005) Synthesis of thyroid hormone binding proteins transthyretin and albumin by human trophoblast. J Clin Endocrinol Metab 90, 67146720.
10Dutriez-Casteloot, I, Breton, C, Coupé, B, et al. (2008) Tissue-specific programming expression of glucocorticoid receptors and 11 beta-HSDs by maternal perinatal undernutrition in the HPA axis of adult male rats. Horm Metab Res 40, 257261.
11Kapoor, A, Leen, J & Matthews, SG (2008) Molecular regulation of the hypothalamic–pituitary–adrenal axis in adult male guinea pigs after prenatal stress at different stages of gestation. J Physiol 586, 43174326.
12Arora, S (2008) Leptin and its metabolic interactions: an update. Diabetes Obes Metab 10, 973993.
13Adam, CL, Findlay, PA, Chanet, A, et al. (2008) Expression of energy balance regulatory genes in the developing ovine fetal hypothalamus at midgestation and the influence of hyperglycemia. Am J Physiol Regul Integr Comp Physiol 294, 18951900.
14Groothuis, TG & Schwabl, H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos Trans R Soc Lond B Biol Sci 363, 16471661.
15Groothuis, TG, Muller, W, von Engelhardt, N, et al. (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29, 329352.
16Hayward, LS, Satterlee, DG & Wingfield, JC (2005) Japanese quail selected for high plasma corticosterone response deposit high levels of corticosterone in their eggs. Physiol Biochem Zool 78, 10261031.
17Wilson, CM & McNabb, FM (1997) Maternal thyroid hormones in Japanese quail eggs and their influence on embryonic development. Gen Comp Endocrinol 107, 153165.
18Hu, Y, Ni, Y, Ren, L, et al. (2008) Leptin is involved in the effects of cysteamine on egg laying of hens, characteristics of eggs, and posthatch growth of broiler offspring. Poult Sci 87, 18101817.
19Scanes, CG & Griminger, P (1990) Endocrine–nutrition interactions in birds. J Exp Zool Suppl 4, 98105.
20De Pablo, F, Roth, J, Hernandez, E, et al. (1982) Insulin is present in chicken eggs and early chick embryos. Endocrinology 111, 19091916.
21Li, Y, Yuan, L, Yang, X, et al. (2007) Effect of early feed restriction on myofibre types and expression of growth-related genes in the gastrocnemius muscle of crossbred broiler chickens. Br J Nutr 98, 310319.
22Williams, TD, Ames, CE, Kiparissis, Y, et al. (2005) Laying-sequence-specific variation in yolk oestrogen levels, and relationship to plasma oestrogen in female zebra finches (Taeniopygia guttata). Proc Biol Sci 272, 173177.
23Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2( − Delta Delta C(T)) method. Methods 25, 402408.
24Lopez, G & Leeson, S (1995) Response of broiler breeders to low-protein diets. 2. Offspring performance. Poult Sci 74, 696701.
25Bowmaker, JE & Gous, RM (1991) The response of broiler breeder hens to dietary lysine and methionine. Br Poult Sci 32, 10691088.
26Sechman, A & Bobek, S (1988) Presence of iodothyronines in the yolk of the hen's egg. Gen Comp Endocrinol 69, 99105.
27Sharp, PJ, Dunn, IC, Waddington, D, et al. (2008) Chicken leptin. Gen Comp Endocrinol 158, 24.
28Dridi, S, Williams, J, Bruggeman, V, et al. (2000) A chicken leptin-specific radioimmunoassay. Domest Anim Endocrinol 18, 325335.
29Neglia, S, Arcamone, N, Gargiulo, G, et al. (2008) Immunocytochemical detection of leptin-like immunoreactivity in the chicken gastroenteric tract. Gen Comp Endocrinol 155, 432437.
30Adachi, H, Takemoto, Y, Bungo, T, et al. (2008) Chicken leptin receptor is functional in activating JAK-STAT pathway in vitro. J Endocrinol 197, 335342.
31Dridi, S, Taouis, M, Gertler, A, et al. (2007) The regulation of stearoyl-CoA desaturase gene expression is tissue specific in chickens. J Endocrinol 192, 229236.
32Figueiredo, D, Gertler, A, Cabello, G, et al. (2007) Leptin downregulates heat shock protein-70 (HSP-70) gene expression in chicken liver and hypothalamus. Cell Tissue Res 329, 91101.
33Yang, SJ & Denbow, DM (2007) Interaction of leptin and nitric oxide on food intake in broilers and leghorns. Physiol Behav 92, 651657.
34Sirotkin, AV & Grossmann, R (2007) Leptin directly controls proliferation, apoptosis and secretory activity of cultured chicken ovarian cells. Comp Biochem Physiol A Mol Integr Physiol 148, 422429.
35Fernandez-Twinn, DS, Ozanne, SE, Ekizoglou, S, et al. (2003) The maternal endocrine environment in the low-protein model of intra-uterine growth restriction. Br J Nutr 90, 815822.
36de Beer, M, McMurtry, JP, Brocht, DM, et al. (2008) An examination of the role of feeding regimens in regulating metabolism during the broiler breeder grower period. 2. Plasma hormones and metabolites. Poult Sci 87, 264275.
37Bautista, CJ, Boeck, L, Larrea, F, et al. (2008) Effects of a maternal low protein isocaloric diet on milk leptin and progeny serum leptin concentration and appetitive behavior in the first 21 days of neonatal life in the rat. Pediatr Res 63, 358363.
38Zambrano, E, Bautista, CJ, Deás, M, et al. (2006) A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol 571, 221230.
39McMillen, IC, Edwards, LJ, Duffield, J, et al. (2006) Regulation of leptin synthesis and secretion before birth: implications for the early programming of adult obesity. Reproduction 131, 415427.
40Holdsworth, CD & Wilson, TH (1967) Development of active sugar and amino acid transport in the yolk sac and intestine of the chicken. Am J Physiol 212, 233240.
41Powell, KA, Deans, EA & Speake, BK (2004) Fatty acid esterification in the yolk sac membrane of the avian embryo. J Comp Physiol B 174, 163168.
42Richards, MP & Poch, SM (2003) Molecular cloning and expression of the turkey leptin receptor gene. Comp Biochem Physiol B Biochem Mol Biol 136, 833847.
43Lesage, J, Sebaai, N, Leonhardt, M, et al. (2006) Perinatal maternal undernutrition programs the offspring hypothalamo–pituitary–adrenal (HPA) axis. Stress 9, 183198.
44Kucka, M, Vagnerová, K, Klusonová, P, et al. (2006) Corticosterone metabolism in chicken tissues: evidence for tissue-specific distribution of steroid dehydrogenases. Gen Comp Endocrinol 147, 377383.
45Gluckman, PD, Lillycrop, KA, Vickers, MH, et al. (2007) Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci U S A 104, 1279612800.
46Soprano, DR, Soprano, KJ & Goodman, DS (1986) Retinol-binding protein and transthyretin mRNA levels in visceral yolk sac and liver during fetal development in the rat. Proc Natl Acad Sci U S A 83, 73307334.
47Southwell, BR, Duan, W, Tu, GF, et al. (1991) Ontogenesis of transthyretin gene expression in chicken choroid plexus and liver. Comp Biochem Physiol B 100, 329338.
48Moran, ET Jr (2007) Nutrition of the developing embryo and hatchling. Poult Sci 86, 10431049.
49De Groef, B, Grommen, SV & Darras, VM (2008) The chicken embryo as a model for developmental endocrinology: development of the thyrotropic, corticotropic, and somatotropic axes. Mol Cell Endocrinol 293, 1724.
50Vieau, D, Sebaai, N, Leonhardt, M, et al. (2007) HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology 32, Suppl. 1, S16S20.
51McMillen, IC & Robinson, JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85, 571633.
52Go, KS, Lingas, R, Wheeler, MB, et al. (2001) Decreased CRH mRNA expression in the fetal guinea pig hypothalamus following maternal nutrient restriction. Brain Res 896, 179182.
53Vandenborne, K, De Groef, B, Geelissen, SM, et al. (2005) Corticosterone-induced negative feedback mechanisms within the hypothalamo–pituitary–adrenal axis of the chicken. J Endocrinol 185, 383391.
54Nillni, EA & Sevarino, KA (1999) The biology of pro-thyrotropin-releasing hormone-derived peptides. Endocr Rev 20, 599648.
55De Groef, B, Vandenborne, K, Van As, P, et al. (2005) Hypothalamic control of the thyroidal axis in the chicken: over the boundaries of the classical hormonal axes. Domest Anim Endocrinol 29, 104110.
56Duclos, MJ (2005) Insulin-like growth factor-I (IGF-1) mRNA levels and chicken muscle growth. J Physiol Pharmacol 56, Suppl. 3, 2535.
57Lu, JW, McMurtry, JP & Coon, CN (2007) Developmental changes of plasma insulin, glucagon, insulin-like growth factors, thyroid hormones, and glucose concentrations in chick embryos and hatched chicks. Poult Sci 86, 673683.
58Duclos, MJ (1998) Regulation of chicken muscle growth by insulin-like growth factors. Ann N Y Acad Sci 839, 166171.

Keywords

Maternal low-protein 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

  • Kaiqing Rao (a1) (a2), Jingjing Xie (a1), Xiaojing Yang (a1), Lei Chen (a1), Roland Grossmann (a3) and Ruqian Zhao (a1)...

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