In ovo leptin administration affects hepatic lipid metabolism and microRNA expression in newly hatched broiler chickens

Journal of Animal Science and Biotechnology

Ruqian Zhao¹  Roland Grossmann²  Jing Li¹  Yanhong Zhang¹  Rui Zhang¹  Yan Hu³ 

[1] Key Laboratory of Animal Physiology & Biochemistry, Nanjing Agricultural University, Nanjing, 210095, China;Department of Functional Genomics & Bioregulation, Institute of Animal Science Mariensee, 31535, Neustadt, Germany;Key Laboratory of Poultry Heredity & Breeding, Institute of Poultry Science of Jiangsu Province, Yangzhou, 225003, China

关键词: SREBPs;    MicroRNA;    Liver;    Lipid metabolism;    Leptin;    In ovo manipulation;    Broiler chickens;   

Others  :  814176
DOI  :  10.1186/2049-1891-3-16

 received in 2012-01-06, accepted in 2012-05-11,  发布年份 2012

【 摘 要 】

Background

A leptin-like immunoreactive substance has been found in chicken eggs and has been implicated in serving as a maternal signal to program offspring growth and metabolism. In the present study, we investigated the effects of in ovo leptin administration on hatch weight, serum and hepatic concentrations of metabolites and hormones, as well as on the expression of genes involved in hepatic lipid metabolism and the predicted microRNAs (miRNAs) targeting the affected genes. To this end we injected fertile eggs with either 0.5 μg of recombinant murine leptin or vehicle (PBS) before incubation.

Results

Prenatally leptin-exposed chicks showed lower hatch weight, but higher liver weight relative to the body weight, compared to the control group. In ovo leptin treatment increased the hepatic content and serum concentration of leptin in newly hatched chickens. The hepatic contents of triglycerides (TG) and total cholesterol (Tch) were decreased, whereas the serum levels of TG, Tch and apolipoprotein B (ApoB) were increased. The hepatic mRNA expression of sterol regulator element binding protein 1 (SREBP-1c), SREBP-2, hydroxy-3-methylglutaryl coenzyme A reductase (HMGCR) and cholesterol 7α-hydroxylase 1 (CYP7A1) was significantly up-regulated, as was the protein content of both SREBP-1c and SREBP-2 in hepatic nuclear extracts of leptin-treated chickens. Moreover, out of 12 miRNAs targeting SREBP-1c and/or HMGCR, five were significantly up-regulated in liver of leptin-treated chicks, including gga-miR-200b and gga-miR-429, which target both SREBP-1c and HMGCR.

Conclusions

These results suggest that leptin in ovo decreases hatch weight, and modifies hepatic leptin secretion and lipid metabolism in newly hatched broiler chickens, possibly via microRNA-mediated gene regulation.

【 授权许可】

   
2012 Hu et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Harvey J, Ashford ML: Leptin in the CNS: much more than a satiety signal. Neuropharmacology 2003, 44:845-854.
• [2]Muoio DM, Lynis DG: Peripheral metabolic actions of leptin. Best Pract Res Clin Endocrinol Metab 2002, 16:653-666.
• [3]Friedman-Einat M, Boswell T, Horev G, Girishvarma G, Dunn IC, Talbot RT, et al.: The chicken leptin gene: has it been cloned? Gen Comp Endocrinol 1999, 115:354-363.
• [4]Hu Y, Ni Y, Ren L, Dai J, Zhao R: Leptin is involved in the effects of cysteamine on egg laying of hens, characteristics of eggs, and posthatch growth of broiler offspring. Poult Sci 2008, 87:1810-1817.
• [5]Neglia S, Arcamone N, Gargiulo G, de Girolamo P: Immunocytochemical detection of leptin-like immunoreactivity in the chicken gastroenteric tract. Gen Comp Endocrinol 2008, 155:432-437.
• [6]Ohkubo T, Nishio M, Tsurudome M, Ito M, Ito Y: Existence of leptin receptor protein in chicken tissues: Isolation of a monoclonal antibody against chicken leptin receptor. Gen Comp Endocrinol 2007, 151:269-273.
• [7]Denbow DM, Meade S, Robertson A, McMurtry JP, Richards M, Ashwell C: Leptin-induced decrease in food intake in chickens. Physiol Behav 2000, 69(3):359-362.
• [8]Macajova M, Lamosova D, Zeman M: Role of Leptin in Japanese Quail Development. Acta Vet 2002, 71:473-479.
• [9]Vickers MH: Developmental programming and adult obesity: the role of leptin. Curr Opin Endocrinol Diabetes Obes 2007, 14:17-22.
• [10]McMillen IC, Edwards LJ, Duffield J, Muhlhausler BS: Regulation of leptin synthesis and secretion before birth: implications for the early programming of adult obesity. Reproduction 2006, 131:415-427.
• [11]Stocker C, O'Dowd J, Morton NM, Wargent E, Sennitt MV, Hislop D, et al.: Modulation of susceptibility to weight gain and insulin resistance in low birthweight rats by treatment of their mothers with leptin during pregnancy and lactation. Int J Obes Relat Metab Disord 2004, 28:129-136.
• [12]Yura S, Itoh H, Sagawa N, Yamamoto H, Masuzaki H, Nakao K, et al.: Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab 2005, 1:371-378.
• [13]Nilsson C, Swolin-Eide D, Ohlsson C, Eriksson E, Ho HP, Bjorntorp P, et al.: Reductions in adipose tissue and skeletal growth in rat adult offspring after prenatal leptin exposure. J Endocrinol 2003, 176:13-21.
• [14]Rao K, Xie J, Yang X, Chen L, Grossmann R, Zhao R: 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. Br J Nutr 2009, 102:848-857.
• [15]Lamosova D, Macajova M, Zeman M, Mozes S, Jezova D: Effect of in ovo leptin administration on the development of Japanese quail. Physiol Res 2003, 52:201-209.
• [16]Ashwell CM, Richards MP, McMurtry JP: The ontogeny of leptin mRNA expression in growing broilers and its relationship to metabolic body weight. Domest Anim Endocrinol 2001, 21:161-168.
• [17]Taouis M, Dridi S, Cassy S, Benomar Y, Raver N, Rideau N, et al.: Chicken leptin: properties and actions. Domest Anim Endocrinol 2001, 21:319-327.
• [18]Horton JD, Goldstein JL, Brown MS: SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 2002, 109:1125-1131.
• [19]Vanpatten S, Karkanias GB, Rossetti L, Cohen DE: Intracerebroventricular leptin regulates hepatic cholesterol metabolism. Biochem J 2004, 379:229-233.
• [20]Zhao Y, Srivastava D: A developmental view of microRNA function. Trends Biochem Sci 2007, 32:189-197.
• [21]Fernandez-Hernando C, Suarez Y, Rayner KJ, Moore KJ: MicroRNAs in lipid metabolism. Curr Opin Lipidol 2011, 22:86-92.
• [22]Moore KJ, Rayner KJ, Suarez Y, Fernandez-Hernando C: microRNAs and cholesterol metabolism. Trends Endocrinol Metab 2010, 21:699-706.
• [23]Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, et al.: MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 2010, 328:1566-1569.
• [24]Rayner KJ, Suarez Y, Davalos A, Parathath S, Fitzgerald ML, Tamehiro N, et al.: MiR-33 contributes to the regulation of cholesterol homeostasis. Science 2010, 328:1570-1573.
• [25]Takanabe R, Ono K, Abe Y, Takaya T, Horie T, Wada H, et al.: Up-regulated expression of microRNA-143 in association with obesity in adipose tissue of mice fed high-fat diet. Biochem Biophys Res Commun 2008, 376:728-732.
• [26]Xie H, Lim B, Lodish HF: MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes 2009, 58:1050-1057.
• [27]Shao P, Zhou H, Xiao ZD, He JH, Huang MB, Chen YQ, et al.: Identification of novel chicken microRNAs and analysis of their genomic organization. Gene 2008, 418:34-40.
• [28]Xu H, Wang X, Du Z, Li N: Identification of microRNAs from different tissues of chicken embryo and adult chicken. FEBS Lett 2006, 580:3610-3616.
• [29]Hicks JA, Tembhurne P, Liu HC: MicroRNA expression in chicken embryos. Poult Sci 2008, 87:2335-2343.
• [30]Hicks JA, Trakooljul N, Liu HC: Discovery of chicken microRNAs associated with lipogenesis and cell proliferation. Physiol Genomics 2010, 41:185-193.
• [31]Folch J, Lees M, Sloane Stanley GH: A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957, 226:497-509.
• [32]Li Y, Yuan L, Yang X, Ni Y, Xia D, Barth S, et al.: 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 2007, 98:310-319.
• [33]Shi R, Chiang VL: Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 2005, 39:519-525.
• [34]Lewis BP, Burge CB, Bartel DP: Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
• [35]Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP: MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007, 27:91-105.
• [36]Friedman RC, Farh KK, Burge CB, Bartel DP: Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009, 19:92-105.
• [37]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
• [38]Chen J, Tang X, Zhang Y, Ma H, Zou S: Effects of maternal treatment of dehydroepiandrosterone (DHEA) on serum lipid profile and hepatic lipid metabolism-related gene expression in embryonic chickens. Comp Biochem Physiol B Biochem Mol Biol 2010, 155:380-386.
• [39]Maurice DV, Bodine AB, Rehrer NJ: Metabolic effects of low aflatoxin B1 levels on broiler chicks. Appl Environ Microbiol 1983, 45:980-984.
• [40]Chen KL, Chi WT, Chu C, Chen RS, Chiou PW: Effect of caponization and testosterone implantation on hepatic lipids and lipogenic enzymes in male chickens. Poult Sci 2007, 86:1754-1759.
• [41]Bruggeman V, Onagbesan OM, Decuypere E: Body weight, fat content, liver weight and plasma leptin concentrations in broiler breeder females reared under ad libitum feeding, restricted feeding or combinations of both until age of first egg. Br Poultry Sci 2000, 41:57-59.
• [42]Smith JT, Waddell BJ: Leptin receptor expression in the rat placenta: changes in ob-ra, ob-rb, and ob-re with gestational age and suppression by glucocorticoids. Biol Reprod 2002, 67:1204-1210.
• [43]Smith JT, Waddell BJ: Leptin distribution and metabolism in the pregnant rat: transplacental leptin passage increases in late gestation but is reduced by excess glucocorticoids. Endocrinology 2003, 144:3024-3030.
• [44]Kirchgessner TG, Heinzmann C, Svenson KL, Gordon DA, Nicosia M, Lebherz HG, et al.: Regulation of chicken apolipoprotein B: cloning, tissue distribution, and estrogen induction of mRNA. Gene 1987, 59:241-251.
• [45]Tartaglia LA: The leptin receptor. J Biol Chem 1997, 272:6093-6096.
• [46]Cassy S, Derouet M, Crochet S, Dridi S, Taouis M: Leptin and insulin downregulate leptin receptor gene expression in chicken-derived leghorn male hepatoma cells. Poult Sci 2003, 82:1573-1579.
• [47]Lund AH: miR-10 in development and cancer. Cell Death Differ 2010, 17:209-214.