Browse > Article
http://dx.doi.org/10.5713/ajas.20.0237

Transcriptomic analysis of the liver in aged laying hens with different intensity of brown eggshell color  

Han, Gi Ppeum (Department of Animal Science and Technology, Chung-Ang University)
Kim, Jun-Mo (Department of Animal Science and Technology, Chung-Ang University)
Kang, Hwan Ku (Poultry Research Institute, National Institute of Animal Science, Rural Development Administration)
Kil, Dong Yong (Department of Animal Science and Technology, Chung-Ang University)
Publication Information
Animal Bioscience / v.34, no.5, 2021 , pp. 811-823 More about this Journal
Abstract
Objective: Eggshell color is an important indicator of egg quality for consumers, especially for brown eggs. Various factors related to laying hens and their environment affect brown eggshell coloration. However, there have been no studies investigating hepatic functions of laying hens with variable intensity of brown eggshell color. Therefore, this study was aimed to identify potential factors affecting brown eggshell coloration in aged laying hens at the hepatic transcriptomic level. Methods: Five hundred 92-wk-old Hy-line Brown laying hens were screened to select laying hens with different intensity of brown eggshell color based on eggshell color fans. Based on eggshell color scores, hens with dark brown eggshells (DBE; eggshell color fan score = 14.8) and hens with light brown eggshells (LBE; eggshell color fan score = 9.7) were finally selected for the liver sampling. We performed RNA-seq analysis using the liver samples through the paired-end sequencing libraries. Differentially expressed genes (DEGs) profiling was carried out to identify their biological meaning by bioinformatics. Results: A total of 290 DEGs were identified with 196 being up-regulated and 94 being down-regulated in DBE groups as compared to LBE groups. The Kyoto encyclopedia of genes and genomes (KEGG) analysis revealed that these DEGs belong to several biological pathways including herpes simplex infection (toll-like receptor 3 [TLR3], cyclin-dependent kinase 1, etc.) and influenza A (TLR3, radical S-adenosyl methionine domain containing 2, myxovirus [influenza virus] resistance 1, etc.). Genes related to stress response (ceremide kinase like) and nutrient metabolism (phosphoenolpyruvate carboxy-kinase 1, methylmalonic aciduria [cobalamin deficiency] cblB type, glycine receptor alpha 2, solute carrier family 7 member 11, etc.) were also identified to be differentially expressed. Conclusion: The current results provide new insights regarding hepatic molecular functions related to different intensity of brown eggshell color in aged laying hens. These insights will contribute to future studies aiming to optimize brown eggshell coloration in aged laying hens.
Keywords
Aged Laying Hen; Eggshell Color; Liver; Transcriptome;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Francis RE, Myatt SS, Krol J, et al. FoxM1 is a downstream target and marker of HER2 overexpression in breast cancer. Int J Oncol 2009;35:57-68. https://doi.org/10.3892/ijo_00000313   DOI
2 Zhong Z, Ji Y, Fu Y, Liu B, Zhu Q. Molecular characterization and expression analysis of the duck viperin gene. Gene 2015; 570:100-7. https://doi.org/10.1016/j.gene.2015.06.003   DOI
3 Jang JS, Lee JH, Jung NC, et al. Rsad2 is necessary for mouse dendritic cell maturation via the IRF7-mediated signaling pathway. Cell Death Dis 2018;9:823. https://doi.org/10.1038/s41419-018-0889-y   DOI
4 Mandal NA, Tran JTA, Saadi A, et al. Expression and localization of CERKL in the mammalian retina, its response to light-stress, and relationship with NeuroD1 gene. Exp Eye Res 2013;106:24-33. https://doi.org/10.1016/j.exer.2012.10.014   DOI
5 Tuson M, Garanto A, Gonzalez-Duarte R, Marfany G. Over-expression of CERKL, a gene responsible for retinitis pigmentosa in humans, protects cells from apoptosis induced by oxidative stress. Mol Vis 2009;15:168-80.
6 Odabasi AZ, Miles RD, Balaban MO, Portier KM. Changes in brown eggshell color as the hen ages. Poult Sci 2007;86: 356-63. https://doi.org/10.1093/ps/86.2.356   DOI
7 Liu HC, Cheng TK. Eggshell pigmentation: a review. J Chin Soc Anim Sci 2010;39:75-89.
8 Truong AD, Hong YH, Lillehoj HS. RNA-seq profiles of immune related genes in the spleen of necrotic enteritis-afflicted chicken lines. Asian-Australas J Anim Sci 2015;28: 1496-511. https://doi.org/10.5713/ajas.15.0143   DOI
9 Coble DJ, Fleming D, Persia ME, et al. RNA-seq analysis of broiler liver transcriptome reveals novel responses to high ambient temperature. BMC Genomics 2014;15:1084. https://doi.org/10.1186/1471-2164-15-1084   DOI
10 Li J, Liu X, Xing L, Liu H, Li X, Bao J. Gene expression profiling of broiler liver under cold stress by high-throughput sequencing technology. J Poult Sci 2017;54:185-96. https://doi.org/10.2141/jpsa.0160142   DOI
11 Li H, Wang T, Xu C, et al. Transcriptome profile of liver at different physiological stages reveals potential mode for lipid metabolism in laying hens. BMC Genomics 2015;16:763. https://doi.org/10.1186/s12864-015-1943-0   DOI
12 Wan Y, Jin S, Ma C, Wang Z, Fang Q, Jiang R. RNA-Seq reveals seven promising candidate genes affecting the proportion of thick egg albumen in layer-type chickens. Sci Rep 2017;7: 18083. https://doi.org/10.1038/s41598-017-18389-5   DOI
13 Meng S, Yang L, Xu C, et al. Recombinant chicken interferon-α inhibits H9N2 avian influenza virus replication in vivo by oral administration. J Interferon Cytokine Res 2011;31:533-8. http://doi.org/10.1089/jir.2010.0123   DOI
14 Riera M, Burguera D, Garcia-Fernandez J, Gonzalez-Duarte R. CERKL knockdown causes retinal degeneration in zebrafish. PLoS One 2013;8:e64048. https://doi.org/10.1371/journal.pone.0064048   DOI
15 Cai X, Conley SM, Naash MI. RPE65: role in the visual cycle, human retinal disease, and gene therapy. Ophthalmic Genet 2009;30:57-62. https://doi.org/10.1080/13816810802626399   DOI
16 Jacobson SG, Aleman TS, Cideciyan AV, et al. Human cone photoreceptor dependence on RPE65 isomerase. Proc Natl Acad Sci USA 2007;104:15123-8. https://doi.org/10.1073/pnas.0706367104   DOI
17 Millward CA, DeSantis D, Hsieh CW, et al. Phosphoenolpyruvate carboxykinase (Pck1) helps regulate the triglyceride/fatty acid cycle and development of insulin resistance in mice. J Lipid Res 2010;51:1452-63. https://doi.org/10.1194/jlr.M005363   DOI
18 Sah N, Kuehu DL, Khadka VS, et al. RNA sequencing-based analysis of the laying hen uterus revealed the novel genes and biological pathways involved in the eggshell biomineralization. Sci Rep 2018;8:16853. https://doi.org/10.1038/s41598-018-35203-y   DOI
19 Pasick J, Diederich S, Berhane Y, Embury-Hyatt C, Xu W. Imbalance between innate antiviral and pro-inflammatory immune responses may contribute to different outcomes involving low- and highly pathogenic avian influenza H5N3 infections in chickens. J Gen Virol 2017;98:1245-58. https://doi.org/10.1099/jgv.0.000801   DOI
20 Beale EG, Harvey BJ, Forest C. PCK1 and PCK2 as candidate diabetes and obesity genes. Cell Biochem Biophys 2007;48: 89-95. https://doi.org/10.1007/s12013-007-0025-6   DOI
21 Dobson CM, Wai T, Leclerc D, et al. Identification of the gene responsible for the cblB complementation group of vitamin B12-dependent methylmalonic aciduria. Hum Mol Genet 2002;11:3361-9. https://doi.org/10.1093/hmg/11.26.3361   DOI
22 Jiang L, Kon N, Li T, et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature 2015;520:57-62. https://doi.org/10.1038/nature14344   DOI
23 Rajendra S, Lynch JW, Schofield PR. The glycine receptor. Pharmacol Ther 1997;73:121-46. https://doi.org/10.1016/S0163-7258(96)00163-5   DOI
24 Young-Pearse TL, Ivic L, Kriegstein AR, Cepko CL. Characterization of mice with targeted deletion of glycine receptor alpha 2. Mol Cell Biol 2006;26:5728-34. https://doi.org/10.1128/MCB.00237-06   DOI
25 Hu K, Li K, Lv J, et al. Suppression of the SLC7A11/glutathione axis causes synthetic lethality in KRAS-mutant lung adenocarcinoma. J Clin Investig 2020;130:1752-66. https://doi.org/10.1172/JCI124049   DOI
26 Birerdinc A, Younossi ZM. Epigenome-wide association studies provide insight into the pathogenesis of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis. Ann Hepatol 2018;17:11-3. https://doi.org/10.5604/01.3001.0010.7530   DOI
27 Huang M, Chen L, Shen Y, Chen J, Guo X, Xu N. Integrated mRNA and miRNA profile expression in livers of Jinhua and Landrace pigs. Asian-Australas J Anim Sci 2019;32:1483-90. https://doi.org/10.5713/ajas.18.0807   DOI
28 Wang Z, Meng G, Bai Y, Liu R, Du Y, Su L. Comparative transcriptome analysis provides clues to molecular mechanisms underlying blue-green eggshell color in the Jinding duck (Anas platyrhynchos). BMC Genomics 2017;18:725. https://doi.org/10.1186/s12864-017-4135-2   DOI
29 Li G, Chen S, Duan Z, Qu L, Xu G, Yang N. Comparison of protoporphyrin IX content and related gene expression in the tissues of chickens laying brown-shelled eggs. Poult Sci 2013;92:3120-4. https://doi.org/10.3382/ps.2013-03484   DOI
30 Samiullah S, Roberts JR, Chousalkar K. Eggshell color in brown-egg laying hens-a review. Poult Sci 2015;94:2566-75. https://doi.org/10.3382/ps/pev202   DOI
31 Li G, Sun C, Wu G, Shi F, Liu A, Yang N. iTRAQ-based quantitative proteomics identifies potential regulatory proteins involved in chicken eggshell brownness. PLoS One 2016;11: e0168750. https://doi.org/10.1371/journal.pone.0168750   DOI
32 Zhang J, Li C, Tang X, Lu Q, Sa R, Zhang H. High concentrations of atmospheric ammonia induce alterations in the hepatic proteome of broilers (Gallus gallus): an iTRAQ-based quantitative proteomic analysis. PLoS One 2015;10:e0123596. https://doi.org/10.1371/journal.pone.0123596   DOI
33 Willer CJ, Sanna S, Jackson AU, et al. Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nat Genet 2008;40:161-9. https://doi.org/10.1038/ng.76   DOI
34 Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30: 2114-20. https://doi.org/10.1093/bioinformatics/btu170   DOI
35 Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods 2015;12:357-60. https://doi.org/10.1038/nmeth.3317   DOI
36 Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014;30:923-30. https://doi.org/10.1093/bioinformatics/btt656   DOI
37 Cunningham F, Amode MR, Barrell D, et al. Ensembl 2015. Nucleic Acids Res 2015;43:D662-9. https://doi.org/10.1093/nar/gku1010   DOI
38 Lu Y, Su X, Zhao M, et al. Comparative RNA-sequencing profiled the differential gene expression of liver in response to acetyl-CoA carboxylase inhibitor GS-0976 in a mouse model of NASH. PeerJ 2019;7:e8115. https://doi.org/10.7717/peerj.8115   DOI
39 Tunali NE, Marobbio CMT, Tiryakioglu NO, et al. A novel mutation in the SLC25A15 gene in a Turkish patient with HHH syndrome: functional analysis of the mutant protein. Mol Genet Metab 2014;112:25-9. https://doi.org/10.1016/j.ymgme.2014.03.002   DOI
40 Parvizi P, Mallick AI, Haq K, et al. A Toll-like receptor 3 ligand enhances protective effects of vaccination against Marek's disease virus and hinders tumor development in chickens. Viral Immunol 2012;25:394-401. https://doi.org/10.1089/vim.2012.0033   DOI
41 Haunshi S, Cheng HH. Differential expression of Toll-like receptor pathway genes in chicken embryo fibroblasts from chickens resistant and susceptible to Marek's disease. Poult Sci 2014;93:550-5. https://doi.org/10.3382/ps.2013-03597   DOI
42 Samiullah S, Roberts JR. The location of protoporphyrin in the eggshell of brown-shelled eggs. Poult Sci 2013;92:2783-8. https://doi.org/10.3382/ps.2013-03051   DOI
43 Mori M, Gahwiler BH, Gerber U. β‐Alanine and taurine as endogenous agonists at glycine receptors in rat hippocampus in vitro. J Physiol 2002;539:191-200. https://doi.org/10.1113/jphysiol.2001.013147   DOI
44 Aznar R, Alarcon B. On the specificity of PCR detection of Listeria monocytogenes in food: a comparison of published primers. Syst Appl Microbiol 2002;25:109-19. https://doi.org/10.1078/0723-2020-00079   DOI
45 Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139-40. https://doi.org/10.1093/bioinformatics/btp616   DOI
46 Zhou X, Lindsay H, Robinson MD. Robustly detecting differential expression in RNA sequencing data using observation weights. Nucleic Acids Res 2014;42:e91. https://doi.org/10.1093/nar/gku310   DOI
47 Huang DW, Sherman BT, Tan Q, et al. DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 2007;35(Suppl 2):W169-75. https://doi.org/10.1093/nar/gkm415   DOI
48 Qiu F, Xie L, Ma J, et al. Lower expression of SLC27A1 enhances intramuscular fat deposition in chicken via down-regulated fatty acid oxidation mediated by CPT1A. Front Physiol 2017;8:449. https://doi.org/10.3389/fphys.2017.00449   DOI
49 Butcher GD, Miles RD. Factors causing poor pigmentation of brown-shelled eggs. Gainesville, FL, USA: University of Florida Cooperative Extension Service, Institute of Food and Agriculture Sciences; 1995.
50 Zhou L, Shi Y, Guo R, Liang M, Zhu X, Wang C. Digital gene-expression profiling analysis of the cholesterol-lowering effects of alfalfa saponin extract on laying hens. PLoS One 2014;9: e98578. https://doi.org/10.1371/journal.pone.0098578   DOI
51 Fu X, Xing L, Xu W, Shu J. Treatment with estrogen protects against ovariectomy-induced hepatic steatosis by increasing AQP7 expression. Mol Med Rep 2016;14:425-31. https://doi.org/10.3892/mmr.2016.5236   DOI
52 Shen T, Yang L, Zhang Z, et al. KIF20A affects the prognosis of bladder cancer by promoting the proliferation and metastasis of bladder cancer cells. Dis Markers 2019;2019:4863182. https://doi.org/10.1155/2019/4863182   DOI
53 Bi H, Liu Z, Sun C, et al. Brown eggshell fading with layer ageing: dynamic change in the content of protoporphyrin IX. Poult Sci 2018;97:1948-53. https://doi.org/10.3382/ps/pey044   DOI
54 Guo J, Wang K, Qu L, et al. Genetic evaluation of eggshell color based on additive and dominance models in laying hens. Asian-Australas J Anim Sci 2020;33:1217-23. https://doi.org/10.5713/ajas.19.0345   DOI
55 Yang L, He T, Xiong F, et al. Identification of key genes and pathways associated with feed efficiency of native chickens based on transcriptome data via bioinformatics analysis. BMC Genomics 2020;21:292. https://doi.org/10.1186/s12864-020-6713-y   DOI
56 Kouprina N, Pavlicek A, Collins NK, et al. The microcephaly ASPM gene is expressed in proliferating tissues and encodes for a mitotic spindle protein. Hum Mol Genet 2005;14:2155-65. https://doi.org/10.1093/hmg/ddi220   DOI