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Inhalation Toxicology
International Forum for Respiratory Research
Volume 34, 2022 - Issue 7-8
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Research Articles

Liver transcriptome analysis reveals biological pathways and transcription factors in response to high ammonia exposure

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Pages 219-229 | Received 01 Feb 2022, Accepted 23 May 2022, Published online: 01 Jun 2022

References

  • An Y, Xing H, Zhang Y, Jia P, Gu X, Teng X. 2019. The evaluation of potential immunotoxicity induced by environmental pollutant ammonia in broilers. Poult Sci. 98(8):3165–3175.
  • Anders S, Pyl PT, Huber W. 2015. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics. 31(2):166–169.
  • Andre R, Kwak D, Dong Q, Zhong W, Correa D, Mattoso L, Lei Y. 2018. Sensitive and selective NH3 monitoring at room temperature using ZnO ceramic nanofibers decorated with poly(styrene sulfonate). Sensors. 18(4):1058.
  • Bai S, Peng X, Wu C, Cai T, Liu J, Shu G. 2021. Effects of dietary inclusion of Radix Bupleuri extract on the growth performance, and ultrastructural changes and apoptosis of lung epithelial cells in broilers exposed to atmospheric ammonia. J Anim Sci. 99(11):1–13.
  • Braissant O, McLin VA, Cudalbu C. 2013. Ammonia toxicity to the brain. J Inherit Metab Dis 36(4):595–612.
  • Bruder ED, Lee PC, Raff H. 2004. Metabolomic analysis of adrenal lipids during hypoxia in the neonatal rat: implications in steroidogenesis. Am J Physiol Endocrinol Metab. 286(5):E697–703.
  • Caprara C, Thiersch M, Lange C, Joly S, Samardzija M, Grimm C. 2011. HIF1A is essential for the development of the intermediate plexus of the retinal vasculature. Invest Ophthalmol Vis Sci. 52(5):2109–2117.
  • Chen D, Miao Z, Peng M, Xing H, Zhang H, Teng X. 2019. The co-expression of circRNA and mRNA in the thymuses of chickens exposed to ammonia. Ecotoxicol Environ Saf. 176:146–152.
  • Cheng Z, O'Connor EA, Jia Q, Demmers TG, Wathes CM, Wathes DC. 2014. Chronic ammonia exposure does not influence hepatic gene expression in growing pigs. Animal. 8(2):331–337
  • Chida Y, Sudo N, Kubo C. 2006. Does stress exacerbate liver diseases? J Gastroenterol Hepatol. 21(1 Pt 2):202–208.
  • Chin CH, Chen SH, Wu HH, Ho CW, Ko MT, Lin CY. 2014. cytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol. 8(Suppl 4):S11.
  • da Silveira Cruz-Machado S, Carvalho-Sousa CE, Tamura EK, Pinato L, Cecon E, Fernandes PACM, de Avellar MCW, Ferreira ZS, Markus RP. 2010. TLR4 and CD14 receptors expressed in rat pineal gland trigger NFKB pathway. J Pineal Res. 49(2):183–192.
  • Di Gregorio J, Cilenti L, Ambivero CT, Andl T, Liao R, Zervos AS. 2021. UBXN7 cofactor of CRL3KEAP1 and CRL2VHL ubiquitin ligase complexes mediates reciprocal regulation of NRF2 and HIF-1α proteins. Biochim Biophys Acta Mol Cell Res. 1868(4):118963.
  • Dilli D, Bostanci I, Tiraş U, Hatipoğlu N, Dallar Y. 2005. A non-accidental poisoning with ammonia in adolescence. Child Care Health Dev. 31(6):737–739.
  • Dominguini D, Dall'igna DM, Nogueira L, Steckert AV, GonÇalves RC, Michels M, Quevedo J, Ritter C, Barichello T, Dal-Pizzol F, et al. 2020. Ammonia exposition during gestation induces neonatal oxidative damage in the brain and long-term cognitive alteration in rats. An Acad Bras Cienc. 92(4):e20190925.
  • Feron O. 2009. Pyruvate into lactate and back: From the Warburg effect to symbiotic energy fuel exchange in cancer cells. Radiother Oncol. 92(3):329–333.
  • Gu Z, Gu L, Eils R, Schlesner M, Brors B. 2014. circlize Implements and enhances circular visualization in R. Bioinformatics 30(19):2811–2812.
  • Han H, Cho JW, Lee S, Yun A, Kim H, Bae D, Yang S, Kim CY, Lee M, Kim E, et al. 2018. TRRUST v2: an expanded reference database of human and mouse transcriptional regulatory interactions. Nucleic Acids Res. 46(D1):D380–d386.
  • Han Q, Tong J, Sun Q, Teng X, Zhang H, Teng X. 2020a. The involvement of miR-6615-5p/Smad7 axis and immune imbalance in ammonia-caused inflammatory injury via NF-κB pathway in broiler kidneys. Poult Sci. 99(11):5378–5388.
  • Han Q, Zhang J, Sun Q, Xu Y, Teng X. 2020b. Oxidative stress and mitochondrial dysfunction involved in ammonia-induced nephrocyte necroptosis in chickens. Ecotoxicol Environ Saf 203:110974.
  • Hellwinkel OJC, Rogmann J-P, Asong LE, Luebke AM, Eichelberg C, Ahyai S, Isbarn H, Graefen M, Huland H, Schlomm T, et al. 2008. A comprehensive analysis of transcript signatures of the phosphatidylinositol-3 kinase/protein kinase B signal-transduction pathway in prostate cancer. BJU Int. 101(11):1454–1460.
  • Hu H, Miao YR, Jia LH, Yu QY, Zhang Q, Guo AY. 2019. AnimalTFDB 3.0: a comprehensive resource for annotation and prediction of animal transcription factors. Nucleic Acids Res 47(D1):D33–d38.
  • Huang DB, Chen YQ, Ruetsche M, Phelps CB, Ghosh G. 2001. X-ray crystal structure of proto-oncogene product c-Rel bound to the CD28 response element of IL-2. Structure. 9(8):669–678.
  • Humbert J, Salian S, Makrythanasis P, Lemire G, Rousseau J, Ehresmann S, Garcia T, Alasiri R, Bottani A, Hanquinet S, et al. 2020. De Novo KAT5 variants cause a syndrome with recognizable facial dysmorphisms, cerebellar atrophy, sleep disturbance, and epilepsy. Am J Hum Genet. 107(3):564–574.
  • Indovina P, Pentimalli F, Casini N, Vocca I, Giordano A. 2015. RB1 dual role in proliferation and apoptosis: cell fate control and implications for cancer therapy. Oncotarget. 6(20):17873–17890.
  • Ito K, Murphy D. 2013. Application of ggplot2 to pharmacometric graphics. CPT Pharmacometrics Syst Pharmacol. 2:e79.
  • Jang MK, Kim CH, Seong JK, Jung MH. 2012. ATF3 inhibits adipocyte differentiation of 3T3-L1 cells. Biochem Biophys Res Commun. 421(1):38–43.
  • Kim J-H, Park H-J, Hwang I-K, Han J-M, Kim D-H, Oh CW, Lee JS, Kang J-C. 2017. Alterations of growth performance, hematological parameters, and plasma constituents in the sablefish, Anoplopoma fimbria depending on ammonia concentrations. Fish Aquatic Sci. 20(1):4.
  • Kimball AS, Davis FM, denDekker A, Joshi AD, Schaller MA, Bermick J, Xing X, Burant CF, Obi AT, Nysz D, et al. 2019. The histone methyltransferase setdb2 modulates macrophage phenotype and uric acid production in diabetic wound repair. Immunity. 51(2):258–271.
  • Lada E, Anna M, Patrik M, Zbynek T, Miroslav J, Hynek M, Richard P, Sarah L, Vaclav L., 2020. Porcine liver anatomy applied to biomedicine. J Surg Res. 250:70–79.
  • Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods. 9(4):357–359.
  • Leshinsky-Silver E, Karban A, Cohen S, Fridlander M, Davidowich O, Kimmel G, Shamir R, Levine A. 2007. Lack of association of the 3'-UTR polymorphism in the NFKBIA gene with Crohn's disease in an Israeli cohort. Int J Colorectal Dis. 22(9):1021–1025.
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 25(4):402–408.
  • Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15(12):550.
  • Marelli SP, Terova G, Cozzi MC, Lasagna E, Sarti FM, Cavalchini LG. 2010. Gene expression of hepatic glucocorticoid receptor NR3C1 and correlation with plasmatic corticosterone in Italian chickens. Anim Biotechnol. 21(2):140–148.
  • Morris PD, Lenhart SW, Service WS. 1991. Respiratory symptoms and pulmonary function in chicken catchers in poultry confinement units. Am J Ind Med 19(2):195–204.
  • Naseem S, King AJ. 2018. Ammonia production in poultry houses can affect health of humans, birds, and the environment-techniques for its reduction during poultry production. Environ Sci Pollut Res Int. 25(16):15269–15293.
  • Nemeth E, Baird AW, O'Farrelly C. 2009. Microanatomy of the liver immune system. Semin Immunopathol. 31(3):333–343.
  • Oh HR, An CH, Yoo NJ, Lee SH. 2017. Frameshift mutations in the mononucleotide repeats of TAF1 and TAF1L genes in gastric and colorectal cancers with regional heterogeneity. Pathol Oncol Res. 23(1):125–130.
  • Owens NDL, De Domenico E, Gilchrist MJ. 2019. An RNA-seq protocol for differential expression analysis. Cold Spring Harb Protoc. 2019(6):pdb.prot098368.
  • Padappayil RP, Borger J, Copyright © 2021, 2021. Ammonia Toxicity, StatPearls. Treasure Island (FL): StatPearls Publishing; StatPearls Publishing LLC.
  • Qin W, Shen L, Wang Q, Gao Y, She M, Li X, Tan Z. 2021. Chronic exposure to ammonia induces oxidative stress and enhanced glycolysis in lung of piglets. Environ Toxicol. 37(2):179–191.
  • Rassidakis GZ, Thomaides A, Atwell C, Ford R, Jones D, Claret FX, Medeiros LJ. 2005. JunB expression is a common feature of CD30+ lymphomas and lymphomatoid papulosis. Mod Pathol. 18(10):1365–1370.
  • Reinke H, Asher G. 2016. Circadian clock control of liver metabolic functions. Gastroenterology. 150(3):574–580.
  • Shah SWA, Chen D, Zhang J, Liu Y, Ishfaq M, Tang Y, Teng X., 2020. The effect of ammonia exposure on energy metabolism and mitochondrial dynamic proteins in chicken thymus: Through oxidative stress, apoptosis, and autophagy. Ecotoxicol Environ Saf. 206:111413.
  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13(11):2498–2504.
  • Shi Q, Wang W, Chen M, Zhang H, Xu S. 2019. Ammonia induces Treg/Th1 imbalance with triggered NF-κB pathway leading to chicken respiratory inflammation response. Sci Total Environ. 659:354–362.
  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 102(43):15545–15550.
  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, et al. 2015. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43(Database issue):D447–452.
  • Takada Y, Ray N, Ikeda E, Kawaguchi T, Kuwahara M, Wagner EF, Matsuo K. 2010. Fos proteins suppress dextran sulfate sodium-induced colitis through inhibition of NF-kappaB. J Immunol. 184(2):1014–1021.
  • Tan SC, Suzairi MSM, Aizat AAA, Aminudin MM, Nurfatimah MSS, Bhavaraju VMK, Biswal BM, Ankathil R. 2013. Gender-specific association of NFKBIA promoter polymorphisms with the risk of sporadic colorectal cancer. Med Oncol. 30(4):693.
  • Tarantino G, Citro V, Esposito P, Giaquinto S, de Leone A, Milan G, Tripodi FS, Cirillo M, Lobello R. 2009. Blood ammonia levels in liver cirrhosis: a clue for the presence of portosystemic collateral veins. BMC Gastroenterol. 9(1):21.
  • Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 25(9):1105–1111.
  • Wang Q, Wang M, Liu C, Huang L, Gao Y, Yu M, Zhao S, Li X., 2020a. Ammonia exposure induced cilia dysfunction of nasal mucosa in the piglets. Biomed Res Int. 2020:1705387.
  • Wang T, He Q, Yao W, Shao Y, Li J, Huang F. 2019. The variation of nasal microbiota caused by low levels of gaseous ammonia exposure in growing pigs. Front Microbiol. 10:1083.
  • Wang V, Saab S. 2003. Ammonia levels and the severity of hepatic encephalopathy. Am J Med. 114(3):237–238.
  • Wang X, Wang M, Chen S, Wei B, Gao Y, Huang L, Liu C, Huang T, Yu M, Zhao SH, et al. 2020b. Ammonia exposure causes lung injuries and disturbs pulmonary circadian clock gene network in a pig study. Ecotoxicol Environ Saf. 205:111050.
  • Wang-Li L, Xu Y, Padavagod Shivkumar A, Williams M, Brake J. 2020. Effect of dietary coarse corn inclusion on broiler live performance, litter characteristics, and ammonia emission. Poult Sci. 99(2):869–878.
  • Wu T, Jia X, Feng H, Wu D. 2021. ACTG1 regulates intervertebral disc degeneration via the NF-κB-p65 and Akt pathways. Biochem Biophys Res Commun. 545:54–61.
  • Xing H, Peng M, Li Z, Chen J, Zhang H, Teng X. 2019. Ammonia inhalation-mediated mir-202-5p leads to cardiac autophagy through PTEN/AKT/mTOR pathway. Chemosphere. 235:858–866.
  • Xu Y, Li Z, Zhang S, Zhang H, Teng X. 2020. miR-187-5p/apaf-1 axis was involved in oxidative stress-mediated apoptosis caused by ammonia via mitochondrial pathway in chicken livers. Toxicol Appl Pharmacol. 388:114869.
  • Yi B, Chen L, Sa R, Zhong R, Xing H, Zhang H. 2016. High concentrations of atmospheric ammonia induce alterations of gene expression in the breast muscle of broilers (Gallus gallus) based on RNA-Seq. BMC Genomics. 17(1):598.
  • Yu G, Wang LG, Han Y, He QY. 2012. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 16(5):284–287.
  • Zeng X, Liu R, Li Y, Li J, Zhao Q, Li X, Bao J., 2021. Excessive ammonia inhalation causes liver damage and dysfunction by altering gene networks associated with oxidative stress and immune function. Ecotoxicol Environ Saf. 217:112203.
  • Zhou C, Jiang X, Liang A, Zhu R, Yang Y, Zhong L, Wan D. 2020. COX10-AS1 facilitates cell proliferation and inhibits cell apoptosis in glioblastoma cells at post-transcription level. Neurochem Res. 45(9):2196–2203.
  • Zuskin E, Mustajbegovic J, Schachter EN, Kern J, Rienzi N, Goswami S, Marom Z, Maayani S. 1995. Respiratory function in poultry workers and pharmacologic characterization of poultry dust extract. Environ Res. 70(1):11–19.

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