Transcriptome analysis reveals the molecular mechanism of hepatic metabolism disorder caused by chromium poisoning in chickens

  • Xinxin Tian
  • Hui Zhang
  • Yali Zhao
  • Khalid Mehmood
  • Xiaoxing Wu
  • Zhenyu Chang
  • Min Luo
  • Xueting Liu
  • Muhammad Ijaz
  • Muhammad Tariq Javed
  • Donghai Zhou
Research Article

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.

Keywords

Transcriptome Chromium Hepatotoxicity Hepatic metabolism Liver 

Notes

Author 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.

Compliance with ethical standards

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.

Supplementary material

11356_2018_1653_MOESM1_ESM.docx (250 kb)
ESM 1 (DOCX 250 kb)

References

  1. 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):3973–3982CrossRefGoogle Scholar
  2. Anderson RA (2004) Chromium and insulin resistance. Nutr Res Rev 16(2):267–275CrossRefGoogle Scholar
  3. 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 2:201–206Google Scholar
  4. 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):46CrossRefGoogle Scholar
  5. 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):213–219CrossRefGoogle Scholar
  6. 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):608–617CrossRefGoogle Scholar
  7. 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):e40409CrossRefGoogle Scholar
  8. 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 423:23–31CrossRefGoogle Scholar
  9. 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):e103194CrossRefGoogle Scholar
  10. 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):69995–70005CrossRefGoogle Scholar
  11. 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 9:717219Google Scholar
  12. 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):e0184988CrossRefGoogle Scholar
  13. 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):460–464Google Scholar
  14. Matsumoto ST, Marin-Morales MA (2005) Toxic and genotoxic effects of trivalent and hexavalent chromium—a review. Rev Bras Toxicol 18(1):77–85Google Scholar
  15. 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):372–377CrossRefGoogle Scholar
  16. 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):2495CrossRefGoogle Scholar
  17. 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):107CrossRefGoogle Scholar
  18. Nickens KP, Patierno SR, Ceryak S (2010) Chromium genotoxicity: a double-edged sword. Chem Biol Interact 188(2):276CrossRefGoogle Scholar
  19. NRC (National Research Council) (2001) Nutrient requirements of poultry, 9th Rev. Ed. National Academy Press, Washington DCGoogle Scholar
  20. Olkowski AA (2007) Pathophysiology of heart failure in broiler chickens: structural, biochemical, and molecular characteristics. Poult Sci 86:999–1005CrossRefGoogle Scholar
  21. 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):11266–11282CrossRefGoogle Scholar
  22. 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):66CrossRefGoogle Scholar
  23. Ray RR (2016) Adverse hematological effects of hexavalent chromium: an overview. Interdiscip Toxicol 9(2):55CrossRefGoogle Scholar
  24. 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 32:45–51CrossRefGoogle Scholar
  25. 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):1–6Google Scholar
  26. Scawarz K, Mertz W (1959) Chromium (iii) and the glucose tolerance factor. Arch Biochem Biophys 85(1):292–295CrossRefGoogle Scholar
  27. Spears JW, Lloyd KE, Krafka K (2017) Chromium concentrations in ruminant feed ingredients. J Dairy Sci 100(5):3584CrossRefGoogle Scholar
  28. Sr JPW, Qin Q (2013) Hexavalent chromium and DNA, biological implications of interaction. Springer New York, New YorkGoogle Scholar
  29. 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):46–53CrossRefGoogle Scholar
  30. 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):5985CrossRefGoogle Scholar
  31. Vendruscolo F, Ferreira GLDR, Filho NRA (2017) Biosorption of hexavalent chromium by microorganisms. Int Biodeterior Biodegrad 119:87–95CrossRefGoogle Scholar
  32. Wang C, Guo F (2012) Effects of activating transcription factor 4 deficiency on carbohydrate and lipid metabolism in mammals. IUBMB Life 64(3):226–230CrossRefGoogle Scholar
  33. 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):136–138CrossRefGoogle Scholar
  34. 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):e21916CrossRefGoogle Scholar
  35. 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 10:1–13Google Scholar
  36. 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 7:332Google Scholar
  37. Yoshida M (2012) Is chromium an essential trace element in human nutrition? Nihon Eiseigaku Zasshi 67(4):485–491CrossRefGoogle Scholar
  38. 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):757CrossRefGoogle Scholar
  39. 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):1033–1037CrossRefGoogle Scholar
  40. 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 56:151–156CrossRefGoogle Scholar
  41. 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):62–70CrossRefGoogle Scholar
  42. 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):3076–3077CrossRefGoogle Scholar
  43. 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):209–213Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Veterinary MedicineHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  2. 2.University College of Veterinary and Animal SciencesIslamia University of BahawalpurBahawalpurPakistan
  3. 3.Key Laboratory of Clinical Veterinary Medicine in TibetXiZang Agriculture and Animal Husbandry CollegeLinzhiPeople’s Republic of China
  4. 4.Department of Clinical Medicine and SurgeryUniversity of Veterinary and Animal SciencesLahorePakistan
  5. 5.University of AgricultureFaisalabadPakistan

Personalised recommendations