Analysis of liver transcriptome data to identify the genes affecting lipid metabolism during the embryonic and hatching periods in ROSS breeder broilers

Document Type : Original Research Article (Regular Paper)

Authors

1 Department of Animal Science, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran

2 Department of Animal Science, Faculty of Agriculture, University of Jiroft, Jiroft, Iran

3 Department of Animal Science, Faculty of Agriculture, University of Zabul, Iran

4 Department of Animal Science, Bila Tserkva National Agrarian University, Soborna, Bila Tserkva, Kiev, Ukraine

5 Department of Animal Science, Sumy National Agrarian University, Sumy, Ukraine

6 Animal Science and Production Department, School of Agriculture and Food Science, University of Queensland, Australia

Abstract

Upon transfer of incubating eggs from the setter stage to the hatcher, the metabolism of the energy source for the rapid metabolism also changes rapidly when the adipose tissue may play an important part. To comprehend the molecular processes underlying the alterations in fat metabolism, identification of genes, processes, and pathways related to fat metabolism is imperative. This research aimed to identify the important genes in lipid metabolism during the embryonic and hatching periods in Ross breeder broilers. The embryonic transcriptomics data were extracted from the Gene Expression Omnibus (GEO) database with accession number GSE109451 and analyzed using Gene Expression Omnibus 2R (GEO2R). Common genes between the setter and hatcher periods were identified with Venn web tool. The Database for Annotation, Visualization, and Integrated Discovery (DAVID) tool was used to identify the biological processes and pathways. The protein-protein network was drawn using the String software and analyzed with the Cytoscape software. Overall, 580 genes in the setter period and 711 genes in the hatcher period showed differential expressions, and 205 common genes were identified between these periods. The most important pathways and processes related to lipid metabolism with common genes between the setter and hatcher periods were the cell cycle, retinol metabolic process, activation of protein kinase activity, nucleic acid metabolism, and metabolic pathways. The key genes associated with lipid metabolism included PBK, CDK1, CCNB2, AURKA. The risks associated with excess fat tissue in chickens present a dual challenge that encompasses animal health and product quality. Targeted research in this area holds the potential to yield effective interventions, ultimately contributing to the sustainability and profitability of poultry production. Enhanced understanding and control of fat metabolism are essential for fostering a healthier and more productive poultry industry.

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References

References
Ailhaud, G., Grimaldi, P., Negrel, R., 1992. Cellular and molecular aspects of adipose tissue development. Annual Review of Nutrition 12(1), 207-233.

Barrett, T., Wilhite, S.E., Ledoux, P., Evangelista, C., Kim, I.F., Tomashevsky, M., Marshall, K.A., Phillippy, K.H., Sherman, P.M., Holko, M., 2012. NCBI GEO: archive for functional genomics data sets—update. Nucleic Acids Research 41(D1), D991-D995.

Blaner, W.S., 2019. Vitamin A signaling and homeostasis in obesity, diabetes, and metabolic disorders. Pharmacology & Therapeutics 197, 153-178.

Brandeis, M., Rosewell, I., Carrington, M., Crompton, T., Jacobs, M.A., Kirk, J., Gannon, J., Hunt, T., 1998. Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proceedings of the National Academy of Sciences 95(8), 4344-4349.

Bordbar, F., Mohammadabadi, M., Jensen, J., Xu, L., Li, J., Zhang, L., 2022. Identification of candidate genes regulating carcass depth and hind leg circumference in simmental beef cattle using Illumina Bovine Beadchip and next-generation sequencing analyses. Animals 12(9), e1103.

Chartrin, P., Bernadet, M.D., Guy, G., Mourot, J., Hocquette, J.F., Rideau, N., Duclos, M.J., Baéza, E., 2007. Do age and feeding levels have comparable effects on fat deposition in breast muscle of mule ducks? Animal 1(1), 113-123.

Chen, W., Chen, G., 2014. The roles of vitamin A in the regulation of carbohydrate, lipid, and protein metabolism. Journal of Clinical Medicine 3(2), 453-479.

Cui, H., Zheng, M., Zhao, G., Liu, R., Wen, J., (2018). Identification of differentially expressed genes and pathways for intramuscular fat metabolism between breast and thigh tissues of chickens. BMC Genomics 19(1), 1-9.

Diril, M.K., Ratnacaram, C.K., Padmakumar, V.C., Du, T., Wasser, M., Coppola, V., Tessarollo, L., Kaldis, P., 2012. Cyclin-dependent kinase 1 (Cdk1) is essential for cell division and suppression of DNA re-replication but not for liver regeneration. Proceedings of the National Academy of Sciences of the United States of America 109(10), 3826-3831.

Emmerson, D.A. 1997. Commercial approaches to genetic selection for growth and feed conversion in domestic poultry. Poultry Science 76(8), 1121-1125.

Fagone, P., Jackowski, S., 2013. Phosphatidylcholine and the CDP-choline cycle. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids 1831(3), 523-532.

Ge, W.H., Liu, J.H., Yang, Y.X., Zhao, Y., Ding, Z., Zhang, J.F., 2021. The role of adenine nucleotide and its metabolites in regulating the homeostasis of glucose and lipid metabolism. Sheng Li Xue Bao:[Acta Physiologica Sinica] 73(5), 707-722.

Guo, F.F., Xiao, M., Wang, S.Y., Zeng, T., Cheng, L., Xie, Q., 2020. Downregulation of mitogen-activated protein kinases (MAPKs) in chronic ethanol-induced fatty liver. Toxicology Mechanisms and Methods 30(6), 407-416.

Guo, L., Sun, B., Shang, Z., Leng, L., Wang, Y., Wang, N., Li, H., 2011. Comparison of adipose tissue cellularity in chicken lines divergently selected for fatness. Poultry Science 90(9), 2024-2034.

Halevy, O., 2020. Timing is everything—the high sensitivity of avian satellite cells to thermal conditions during embryonic and posthatch periods. Frontiers in Physiology 11, e235.

Hardie, D.G., Carling, D., Sim, A.T.R., 1989. The AMP-activated protein kinase: a multisubstrate regulator of lipid metabolism. Trends in Biochemical Sciences 14(1), 20-23.

Hicks, J.A., Liu, H.C., 2021. Expression signatures of microRNAs and their targeted pathways in the adipose tissue of chickens during the transition from embryonic to post-hatch development. Genes 12(2), 196.

Huang, D.W., Sherman, B.T., Tan, Q., Kir, J., Liu, D., Bryant, D., Guo, Y., Stephens, R., Baseler, M.W., Lane, H.C., 2007. DAVID Bioinformatics resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Research 35(suppl_2), W169-W175.

Huang, J., Zhou, Y., Wan, B., Wang, Q., Wan, X., 2017. Green tea polyphenols alter lipid metabolism in the livers of broiler chickens through increased phosphorylation of AMP-activated protein kinase. PLoS One 12(10), e0187061.

Hunt, G.P., Grassi, L., Henkin, R., Smeraldi, F., Spargo, T.P., Kabiljo, R., Koks, S., Ibrahim, Z., Dobson, R.J.B., Al-Chalabi, A., 2022. GEOexplorer: a webserver for gene expression analysis and visualisation. Nucleic Acids Research 50(W1), W367-W374.

Jackowski, S., 1994. Coordination of membrane phospholipid synthesis with the cell cycle. Journal of Biological Chemistry 269(5), 3858-3867.

Li, Y., Chen, Y., Jin, W., Fu, S., Li, D., Zhang, Y., Sun, G., Jiang, R., Han, R., Li, Z., 2019. Analyses of MicroRNA and mRNA expression profiles reveal the crucial interaction networks and pathways for regulation of chicken breast muscle development. Frontiers in Genetics 10, e197.

Lim, C., Lim, B., Kil, D.Y., Kim, J.M., 2022. Hepatic transcriptome profiling according to growth rate reveals acclimation in metabolic regulatory mechanisms to cyclic heat stress in broiler chickens. Poultry Science 101(12), e102167.

Liu, J., Fu, R., Liu, R., Zhao, G., Zheng, M., Cui, H., Li, Q., Song, J., Wang, J., Wen, J., 2016. Protein profiles for muscle development and intramuscular fat accumulation at different post-hatching ages in chickens. PLoS One 11(8), e0159722.

Liu, J., Lei, Q., Li, F., Zhou, Y., Gao, J., Liu, W., Han, H., Cao, D., 2020. Dynamic transcriptomic analysis of breast muscle development from the embryonic to post-hatching periods in chickens. Frontiers in Genetics 10, e1308.

Liu, L., Liu, X., Cui, H., Liu, R., Zhao, G., Wen, J., 2019. Transcriptional insights into key genes and pathways controlling muscle lipid metabolism in broiler chickens. BMC Genomics 20, 1-10.

Liu, Y., Shen, J., Yang, X., Sun, Q., Yang, X., 2018. Folic acid reduced triglycerides deposition in primary chicken hepatocytes. Journal of Agricultural and Food Chemistry 66(50), 13162-13172.

Liu, Y., Zhou, J., Musa, B.B., Khawar, H., Yang, X., Cao, Y., Yang, X., 2020. Developmental changes in hepatic lipid metabolism of chicks during the embryonic periods and the first week of posthatch. Poultry Science 99(3), 1655-1662.

Lu, J., Weil, J., Cerrate, S., Coon, C., 2020. Developmental changes in physiological amino acids and hepatic methionine remethylation enzyme activities in E10-21 chick embryos and D1-49 broilers. Journal of Animal Physiology and Animal Nutrition 104(6), 1727-1737.

Mellouk, N., Ramé, C., Delaveau, J., Rat, C., Maurer, E., Froment, P., Dupont, J., 2018. Adipokines expression profile in liver, adipose tissue and muscle during chicken embryo development. General and Comparative Endocrinology 267, 146-156.

Mohamadipoor Saadatabadi, L., Mohammadabadi, M., Amiri Ghanatsaman, Z., Babenko, O., Stavetska, R., Kalashnik, O., Kucher, D., Kochuk-Yashchenko, O., Asadollahpour Nanaei, H., 2021. Signature selection analysis reveals candidate genes associated with production traits in Iranian sheep breeds. BMC Veterinary Research 17(1), 1-9.

Moreira, G.C.M., Boschiero, C., Cesar, A.S.M., Reecy, J.M., Godoy, T.F., Pértille, F., Ledur, M.C., Moura, A.S.A.M.T., Garrick, D.J., Coutinho, L. L., 2018. Integration of genome wide association studies and whole genome sequencing provides novel insights into fat deposition in chicken. Scientific Reports 8(1), e16222.

Nematbakhsh, S., Pei Pei, C., Selamat, J., Nordin, N., Idris, L.H., Abdull Razis, A.F., 2021. Molecular regulation of lipogenesis, adipogenesis and fat deposition in chicken. Genes 12(3), e414.

Noble, R.C., Cocchi, M., 1990. Lipid metabolism and the neonatal chicken. Progress in Lipid Research 29(2), 107-140.

Nyuiadzi, D., Berri, C., Dusart, L., Travel, A., Méda, B., Bouvarel, I., Guilloteau, L.A., Chartrin, P., Coustham, V., Praud, C., 2020. Short cold exposures during incubation and postnatal cold temperature affect performance, breast meat quality, and welfare parameters in broiler chickens. Poultry Science 99(2), 857-868.

Ow, J.R., Caldez, M.J., Zafer, G., Foo, J.C., Li, H.Y., Ghosh, S., Wollmann, H., Cazenave-Gassiot, A., Ong, C.B., Wenk, M.R., 2020. Remodeling of whole-body lipid metabolism and a diabetic-like phenotype caused by loss of CDK1 and hepatocyte division. Elife 9, e63835.

Ruiz-Pérez, M.V, Henley, A.B., Arsenian-Henriksson, M., 2017. The MYCN protein in health and disease. Genes 8(4), e113.

Safaei, S.M.H., Dadpasand, M., Mohammadabadi, M., Atashi, H., Stavetska, R., Klopenko, N., Kalashnyk, O., 2022. An origanum majorana leaf diet influences myogenin gene expression, performance, and carcass characteristics in lambs. Animals 13(1), e14.

Safaei, S.M.H., Mohammadabadi, M., Moradi, B., Kalashnyk, O., Klopenko, N., Babenko, O., Borshch, O.O., Afanasenko, V., 2024. Role of fennel (foeniculum vulgare) seed powder in increasing testosterone and IGF1 gene expression in the testis of lamb. Gene Expression 23(2), 98-105.

Saito, R., Smoot, M.E., Ono, K., Ruscheinski, J., Wang, P.L., Lotia, S., Pico, A.R., Bader, G.D., Ideker, T., 2012. A travel guide to Cytoscape plugins. Nature Methods 9(11), 1069-1076.

Saitoh, S., Takahashi, K., Nabeshima, K., Yamashita, Y., Nakaseko, Y., Hirata, A., Yanagida, M., 1996. Aberrant mitosis in fission yeast mutants defective in fatty acid synthetase and acetyl CoA carboxylase. The Journal of Cell Biology 134(4), 949-961.

Sanchez-Alvarez, M., Zhang, Q., Finger, F., Wakelam, M.J.O., Bakal, C., 2015. Cell cycle progression is an essential regulatory component of phospholipid metabolism and membrane homeostasis. Open Biology 5(9), e150093.

Shi, H., Chen, L., Zhang, Z., Zhao, Y., Ou, J., 2023. COS Attenuates AFB1-induced liver injury in Medaka through inhibition of histopathological damage and oxidative stress. Sustainability 15(6), 5418.

Shokri, S., Khezri, A., Mohammadabadi, M., Kheyrodin, H., 2023. The expression of MYH7 gene in femur, humeral muscle and back muscle tissues of fattening lambs of the Kermani breed. Agricultural Biotechnology Journal 15(2), 217-236.

Su, S., Wang, Y., Chen, C., Suh, M., Azain, M., Kim, W.K., 2020. Fatty acid composition and regulatory gene expression in late-term embryos of ACRB and COBB broilers. Frontiers in Veterinary Science 7, e317.

Szklarczyk, D., Morris, J.H., Cook, H., Kuhn, M., Wyder, S., Simonovic, M., Santos, A., Doncheva, N.T., Roth, A., Bork, P., Jensen, L.J., Mering, C.V., 2017. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Research 45(D1, D362-D368.

Volgin, D.V., 2014. Gene Expression: analysis and quantitation. In: Ashish, S.V., Anchal, S. (Eds.), Animal Biotechnology, Academic Press, pp. 307-325.

Wang, R., Li, K., Sun, L., Jiao, H., Zhou, Y., Li, H., Wang, X., Zhao, J., Lin, H., 2022. L-Arginine/nitric oxide regulates skeletal muscle development via muscle fibre-specific nitric oxide/mTOR pathway in chickens. Animal Nutrition 10, 68-85.

Witkin, K.L., Chong, Y., Shao, S., Webster, M.T., Lahiri, S., Walters, A.D., Lee, B., Koh, J.L.Y., Prinz, W.A., Andrews, B.J., 2012. The budding yeast nuclear envelope adjacent to the nucleolus serves as a membrane sink during mitotic delay. Current Biology 22(12), 1128-1133.

Xiao, Y., Wang, G., Gerrard, M.E., Wieland, S., Davis, M., Cline, M.A., Siegel, P.B., Gilbert, E.R., 2019. Changes in adipose tissue physiology during the first two weeks posthatch in chicks from lines selected for low or high body weight. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 316(6), R802-R818.

Yano, K., 2012. Lipid metabolic pathways as lung cancer therapeutic targets: A computational study. International Journal of Molecular Medicine 29(4), 519-529.

Yuan, J., Roshdy, A.R., Guo, Y., Wang, Y., Guo, S., 2014. Effect of dietary vitamin A on reproductive performance and immune response of broiler breeders. PloS One 9(8), e105677.

Zhang, Y., Knapp, S., 2016. Glycosylation of nucleosides. The Journal of Organic Chemistry 81(6), 2228-2242.

Zhao, H., Wu, M., Tang, X., Li, Q., Yi, X., Wang, S., Jia, C., Wei, Z., Sun, X., 2021. Function of chick subcutaneous adipose tissue during the embryonic and posthatch period. Frontiers in Physiology 12, e684426.

Zhao, M., Jung, Y., Jiang, Z., Svensson, K.J., 2020. Regulation of energy metabolism by receptor tyrosine kinase ligands. Frontiers in Physiology 11, e354.
Journal of Livestock Science and Technologies
Volume 12, Issue 2
December 2024
Pages 61-67

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