Abstract
Chromium (Cr) is one of the most important environmental pollutants which are released into the environment due to their wide usage in numerous industries. The excess of Cr (VI) can induce hepatotoxicity, while the molecular mechanism that is involved in Cr (VI)-induced hepatotoxicity is unclear. We demonstrated the induction of chromium poisoning model in chickens to identify the differentially expressed genes (DEGs), and their functions were analyzed under different physiological and pathological conditions. Histopathological examination and transcriptome data for chromium-poisoned livers and control livers were annotated with Illumina® HiSeq 2000. The histopathological examination in chromium poisoning groups showed diapedesis, hemolysis, degeneration, nucleus pycnosis, and central phlebectasia in the liver. A total of 334 genes were upregulated and 509 genes were downregulated. The most strongly upregulated genes were HKDC1, DDX4, ACACA, FDFT1, CYYR1, PPP1R3C, and SLC16A14, while the most downregulated genes were MYBPC3, CCKAR, PCK1, and CPT1A. A Gene Ontology (GO) term with the highest enrichment of DEGs is small molecule metabolic process. In cell component domain, the term with the highest enrichment is extracellular matrix. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways showed that glucose metabolism, lipid metabolism, and protein metabolism were the most important metabolic pathways in the liver. The current study first time provides important clues and evidence for identifying the differentially expressed genes in livers due to Cr (VI)-induced liver injury in chickens.
Similar content being viewed by others
References
Abbas HH, Ali FK (2007) Study the effect of hexavalent chromium on some biochemical, citotoxicological and histopathological aspects of the orechromis spp. fish. Pak J Biol Sci 10(22):3973–3982
Anderson RA (2004) Chromium and insulin resistance. Nutr Res Rev 16(2):267–275
Bislimi K, Behluli A, Bojniku H, Halili J, Mazreku I, Halili F (2012) Accumulation of chromium in hybro chickens liver treated with Cr(vi) and vitamin C. Int J Ecosyst Ecol Sci 2:201–206
Boşgelmez II, Soylemezoglu T, Guvendik G (2008) The protective and antidotal effects of taurine on hexavalent chromium-induced oxidative stress in mice liver tissue. Biol Trace Elem Res 125(1):46
Castro MP, de Moraes FR, Fujimoto RY, Da CC, Belo MA, de Moraes JR (2014) Acute toxicity by water containing hexavalent or trivalent chromium in native Brazilian fish, Piaractus mesopotamicus: anatomopathological alterations and mortality. Bull Environ Contam Toxicol 92(2):213–219
Clodfelder BJ, Emamaullee J, Hepburn DD, Chakov NE, Nettles HS, Vincent JB (2001) The trail of chromium(iii) in vivo from the blood to the urine: the roles of transferrin and chromodulin. J Biol Inorg Chem 6(5–6):608–617
Connell S, Meade KG, Allan B, Lloyd AT, Kenny E, Cormican P, Morris DW, Bradley DG, O'Farrelly C (2012) Avian resistance to Campylobacter jejuni colonization is associated with an intestinal immunogene expression signature identified by mRNA sequencing. PLoS One 7(8):e40409
Fang JY, Wu TH, Huang CH, Wang PW, Chen CC, Wu YC, Pan TL (2013) Proteomics reveals plasma profiles for monitoring the toxicity caused by chromium compounds. Clin Chim Acta 423:23–31
Fang Z, Zhao M, Zhen H, Chen L, Shi P, Huang Z (2014) Genotoxicity of tri- and hexavalent chromium compounds in vivo and their modes of action on DNA damage in vitro. PLoS One 9(8):e103194
Ge X, Wang Y, Nie J, Li Q, Tang L, Deng X, Wang F, Xu B, Wu X, Zhang X, You Q, Miao L (2017) The diagnostic/prognostic potential and molecular functions of long non-coding RNAs in the exosomes derived from the bile of human cholangiocarcinoma. Oncotarget 8(41):69995–70005
Huang S, Peng W, Jiang X, Shao K, Xia L, Tang Y, Qiu J (2014) The effect of chromium picolinate supplementation on the pancreas and macroangiopathy in type ii diabetes mellitus rats. J Diabetes Res 9:717219
Kan J, Liu T, Ma N, Li H, Li X, Wang J, Zhang B, Chang Y, Lin J (2017) Transcriptome analysis of Callery pear (Pyrus calleryana) reveals a comprehensive signalling network in response to Alternaria alternata. PLoS One 12(9):e0184988
Khan AZ, Kumbhar S, Hamid M, Afzal S, Parveen F, Liu Y, Shu H, Mengistu BM, Huang K (2016) Effects of selenium-enriched robiotics on heart lesions by influencing the mRNA expressions of selenoproteins and heat shock proteins in heat stressed broiler chickens. Pak Vet J 36(4):460–464
Matsumoto ST, Marin-Morales MA (2005) Toxic and genotoxic effects of trivalent and hexavalent chromium—a review. Rev Bras Toxicol 18(1):77–85
Mehmood K, Zhang H, Iqbal MK, Rehman MU, Shahzad M, Li K, Huang S, Nabi F, Zhang L, Li J (2017) In vitro effect of apigenin and danshen in tibial dyschondroplasia through inhibition of heat-shock protein 90 and vascular endothelial growth factor expressions in avian growth plate cells. Avian Dis 61(3):372–377
Mehmood K, Zhang H, Li K, Wang L, Rehman MU, Nabi F, Iqbal MK, Luo H, Shahzad M, Li J (2018) Effect of tetramethylpyrazine on tibial dyschondroplasia incidence, tibial angiogenesis, performance and characteristics via HIF-1α/VEGF signaling pathway in chickens. Sci Rep 8(1):2495
Mertz W, Roginski EE, Schroeder HA (1965) Some aspects of glucose metabolism of chromium-deficient rats raised in a strictly controlled environment. J Nutr 86(3):107
Nickens KP, Patierno SR, Ceryak S (2010) Chromium genotoxicity: a double-edged sword. Chem Biol Interact 188(2):276
NRC (National Research Council) (2001) Nutrient requirements of poultry, 9th Rev. Ed. National Academy Press, Washington DC
Olkowski AA (2007) Pathophysiology of heart failure in broiler chickens: structural, biochemical, and molecular characteristics. Poult Sci 86:999–1005
Pati A, Chaudhary R, Subramani S (2014) A review on management of chrome-tanned leather shavings: a holistic paradigm to combat the environmental issues. Environ Sci Pollut Res Int 21(19):11266–11282
Patlolla AK, Barnes C, Yedjou C, Velma VR, Tchounwou PB (2009) Oxidative stress, DNA damage, and antioxidant enzyme activity induced by hexavalent chromium in Sprague-Dawley rats. Environ Toxicol 24(1):66
Ray RR (2016) Adverse hematological effects of hexavalent chromium: an overview. Interdiscip Toxicol 9(2):55
Sadeghi M, Najaf Panah MJ, Bakhtiarizadeh MR, Emami A (2015) Transcription analysis of genes involved in lipid metabolism reveals the role of chromium in reducing body fat in animal models. J Trace Elem Med Biol 32:45–51
Sarkar S, Satheshkumar A, Pradeepa N, Premkumar R, Dist C, Tamil N (2013) Hexavalent chromium (cr (vi)) removal by live mycelium of a Trichoderma harzianum strain. Mol Soil Biol 4(1):1–6
Scawarz K, Mertz W (1959) Chromium (iii) and the glucose tolerance factor. Arch Biochem Biophys 85(1):292–295
Spears JW, Lloyd KE, Krafka K (2017) Chromium concentrations in ruminant feed ingredients. J Dairy Sci 100(5):3584
Sr JPW, Qin Q (2013) Hexavalent chromium and DNA, biological implications of interaction. Springer New York, New York
Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31(1):46–53
Tytłak A, Oleszczuk P, Dobrowolski R (2015) Sorption and desorption of cr(vi) ions from water by biochars in different environmental conditions. Environ Sci Pollut Res Int 22(8):5985
Vendruscolo F, Ferreira GLDR, Filho NRA (2017) Biosorption of hexavalent chromium by microorganisms. Int Biodeterior Biodegrad 119:87–95
Wang C, Guo F (2012) Effects of activating transcription factor 4 deficiency on carbohydrate and lipid metabolism in mammals. IUBMB Life 64(3):226–230
Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an r package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138
Wang Y, Liu Y, Wan H, Zhu Y, Chen P, Hao P, Cheng Z, Liu J (2017a) Moderate selenium dosing inhibited chromium (vi) toxicity in chicken liver. J Biochem Mol Toxicol 31(8):e21916
Wang Q, Liu M, Xu L, Wu Y, Huang Y (2017b) Transcriptome analysis reveals the molecular mechanism of hepatic fat metabolism disorder caused by Muscovy duck reovirus infection. Avian Pathol 10:1–13
Wu Q, Chen Z, Sun W, Deng T, Chen M (2016) De novo sequencing of the leaf transcriptome reveals complex light-responsive regulatory networks in Camellia sinensis cv. Baijiguan. Front Plant Sci 7:332
Yoshida M (2012) Is chromium an essential trace element in human nutrition? Nihon Eiseigaku Zasshi 67(4):485–491
Zatta S, Rehrauer H, Gram A, Boos A, Kowalewski MP (2017) Transcriptome analysis reveals differences in mechanisms regulating cessation of luteal function in pregnant and non-pregnant dogs. BMC Genomics 18(1):757
Zhang H, Wang Y, Li K, Rehman MU, Nabi F, Gui R, Lan Y, Luo H (2017a) Sero-prevalence and pathological examination of lymphoid leukosis virus subgroup a in chickens in Anhui province, China. Pak J Zool 49(3):1033–1037
Zhang H, Wu X, Mehmood K, Chang Z, Li K, Jiang X, Nabi F, Ijaz M, Rehman MU, Javed MT, Zhou D (2017b) Intestinal epithelial cell injury induced by copper containing nanoparticles in piglets. Environ Toxicol Pharmacol 56:151–156
Zhang H, Chang Z, Mehmood K, Abbas RZ, Nabi F, Rehman MU, Wu X, Tian X, Yuan X, Li Z, Zhou D (2018) Nano copper induces apoptosis in PK-15 cells via a mitochondria-mediated pathway. Biol Trace Elem Res 181(1):62–70
Zhao W, Liu W, Tian D, Tang B, Wang Y, Yu C, Li R, Ling Y, Wu J, Song S, Hu S (2011) WapRNA a web-based application for the processing of RNA sequences. Bioinformatics 27(21):3076–3077
Zhuang Y, Liu P, Zhang CY, Ye S, Hu G, Cao HB (2016) Effect of cadmium on the concentration of ceruloplasmin and its mRNA expression in goats under molybdenum stress. Pak Vet J 36(2):209–213
Funding
This study was supported by the National Key R&D Program of China (2016YFD0501208), National Natural Science Foundation of China (No: 30700588) and Hubei Provincial Natural Science Foundation of China (Grant No: 2014CFB244).
Author information
Authors and Affiliations
Contributions
X.T., H.Z., Y.Z., X.W., Z.C., M.L., and D.Z. were responsible for study conception and design; H.Z., D.Z., K.M., X.L., M.I., and M.T.J. were involved in the drafting of the manuscript.
Corresponding author
Ethics declarations
All the experiments were performed after the approval of the Institutional Animal Welfare and Research Ethics Committee of Huazhong Agricultural University Wuhan, China (approval number 31272556). All animal experiments and methods were conducted under the relevant procedure of Proclamation of the Standing Committee of Hubei People’s Congress (No. 29), China.
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Philippe Garrigues
Electronic supplementary material
ESM 1
(DOCX 250 kb)
Rights and permissions
About this article
Cite this article
Tian, X., Zhang, H., Zhao, Y. et al. Transcriptome analysis reveals the molecular mechanism of hepatic metabolism disorder caused by chromium poisoning in chickens. Environ Sci Pollut Res 25, 15411–15421 (2018). https://doi.org/10.1007/s11356-018-1653-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-1653-7