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Characteristics of circRNAs expression profiles in the piglets intestine induced by oxidative stress

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Abstract

Backgroud

Oxidative stress (OS) can affect the expression of key genes and destroy the intestinal structure. However, it is unclear how OS regulates the expression of circular RNAs (circRNAs), microRNAs (miRNAs) and mRNAs.

Objective

The aim of this study was to examine the expression of circRNAs, miRNAs and mRNAs exposed to OS.

Methods

Piglets were exposed to diquat (DQ), a herbicide, and the activity of antioxidant enzymes and the morphology of the intestine were investigated. We utilized whole transcriptome sequencing to examine the global expression of circRNAs, miRNAs and mRNAs in the jejunum.

Results

Compared to controls, 751 circRNAs, 731 miRNAs and 164 mRNAs were differentially expressed in diquat-treated piglets. Kyoto Encyclopedia of Genes and Genomes pathway analysis indicated that oxidative phosphorylation, RNA degradation and ubiquitin-mediated proteolysis were closely associated with OS.

Conclusions

Our results indicated that diquat-induced OS alters the intestinal structure, resulting in the differential expression of circRNAs, miRNAs and mRNAs in the jejunum of piglets. Meanwhile, OS weakened the enzyme antioxidant system in serum of piglets. Our results provide a foundation for further studies on the mechanisms involved in the response to OS in the jejunum.

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Fig. 1
Fig. 2

source genes of differentially expressed circRNAs. E KEGG pathway enrichment analysis of the source genes of differentially expressed circRNAs

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References

  • Azad M, Wang H, Yang H, Tan B, Zhou S, Guan G (2021) Effects of dietary carboxymethyl pachyman on oxidative stress and inflammation in weaned piglets challenged with diquat. Anim Feed Sci Technol 276:114922

    Article  CAS  Google Scholar 

  • Bachmayr-Heyda A, Reiner AT, Auer K, Sukhbaatar N, Aust S, Bachleitner-Hofmann T, Mesteri I, Grunt TW, Zeillinger R, Pils D (2015a) 134 Correlation of circular RNA abundance with proliferation—exemplified with human normal, benign and malignant tissues. Eur J Cancer 51:S10

    Article  Google Scholar 

  • Bachmayr-Heyda A, Reiner AT, Auer K, Sukhbaatar N, Aust S, Bachleitner-Hofmann T, Pils D (2015b) Correlation of circular RNA abundance with proliferation–exemplified with colorectal and ovarian cancer, idiopathic lung fibrosis and normal human tissues. Sci Rep 5(1):1–10

    Article  Google Scholar 

  • Campbell JM, Crenshaw JD, Polo J (2013) The biological stress of early weaned piglets. J Anim Sci Biotechnol 2:19

    Article  Google Scholar 

  • Chen B, Huang SL (2018) Circular RNA: An emerging non-coding RNA as a regulator and biomarker in cancer. Cancer Lett 418:41–50

    Article  CAS  PubMed  Google Scholar 

  • Daehwan K, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 4:357–360

    Google Scholar 

  • Fuschi P, Maimone B, Gaetano C, Martelli F (2019) Noncoding RNAs in the vascular system response to oxidative stress. Antioxid Redox Sign 7:992–1010

    Article  Google Scholar 

  • Gallagher EP, Buetler TM, Stapleton PL, Wang CH, Stahl DL, Eaton DL (1995) The effects of diquat and ciprofibrate on mRNA expression and catalytic activities of hepatic xenobiotic metabolizing and antioxidant enzymes in rat liver. Toxicol Appl Pharm 1:81–91

    Article  Google Scholar 

  • Gao Y, Wang JF, Zhao FQ (2015) CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol 1:4

    Article  Google Scholar 

  • Guo J, Wen N, Yang SF, Guan XH, Cang S (2018) MiR-92a regulates oral squamous cell carcinoma (OSCC) cell growth by targeting FOXP1 expression. Biomed Pharmacother 104:77–86

    Article  CAS  PubMed  Google Scholar 

  • Hansen TB, Kjems J, Damgaard CK (2013a) Circular RNA and miR-7 in cancer. Cancer Res 18:5609–5612

    Article  Google Scholar 

  • Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013b) Natural RNA circles function as efficient microRNA sponges. Nature 7441:384–388

    Article  Google Scholar 

  • Holdt LM, Kohlmaier A, Teupser D (2018) Molecular functions and specific roles of circRNAs in the cardiovascular system. Noncoding RNA Res 2:75–98

    Article  Google Scholar 

  • Jayaraman B, Charles M (2017) Husbandry practices and gut health outcomes in weaned piglets: a review. Anim Nutr 3:205–211

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeck WR, Sorrentino JA, Wang K, Slevin ML, Burd CE, Liu JZ, Marzluff MF, Sharpless NE (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2:141–157

    Article  Google Scholar 

  • Kang HN, Oh SC, Kim JS, Yoo YA (2012) Abrogation of Gli3 expression suppresses the growth of colon cancer cells via activation of p53. Exp Cell Res 5:539–549

    Article  Google Scholar 

  • Li F, Zhang LY, Li W, Deng JQ, Zheng J, An MX, Lu JC (2015) Zhou YF, Circular RNA ITCH has inhibitory effect on ESCC by suppressing the Wnt/β-catenin pathway. Oncotarget 8:6001–6013

    Article  Google Scholar 

  • Li X, Zhan J, Hou Y, Hou YH, Chen S, Luo D, Luan J, Wang L, Lin D (2019) Coenzyme Q10 regulation of apoptosis and oxidative stress in H2O2 Induced BMSC death by modulating the Nrf-2/NQO-1 signaling pathway and its application in a model of spinal cord injury. Oxid Med Cell Longev 2019:6493081

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang GM, Yang YL, Niu GL, Tang ZL (2017) Genome-wide profiling of Sus scrofa circular RNAs across nine organs and three developmental stages. DNA Res 5:523–535

    Article  Google Scholar 

  • Liang JQ, Shen YC, Zhang XY, Chen C, Zhao H, Hu JH (2020) Circular RNA HIPK3 downregulation mediates hydrogen peroxide-induced cytotoxicity in human osteoblasts. Aging 12:2

    Article  Google Scholar 

  • Lu T, Piao XL, Zhang Q, Wang D, Piao XS, Kim SW (2010) Protective effects of Forsythia suspensa extract against oxidative stress induced by diquat in rats. Food Chem Toxicol 2:764–770

    Article  Google Scholar 

  • Nathalie LF, Catherine J, Jacques MJ, Bernard S (2006) Importance of sanitary environment for growth performance and plasma nutrient homeostasis during the post-weaning period in piglets. Arch Anim Nutr 1:23–34

    Google Scholar 

  • Saaound F, Drummer CIV, Shao Y, Sun Y, Lu YF, Xu KM, Ni D, Jiang XH, Wang H, Yang XF (2021) Circular RNAs are a novel type of non-coding RNAs in ROS regulation, cardiovascular metabolic inflammations and cancers. Pharmacol. Therapeut. 220:107715

    Article  Google Scholar 

  • Schallreuter KU, Gibbons NC, Zother C, Abou Eloof MM, Wood JM (2013) Hydrogen peroxide-mediated oxidative stress disrupts calcium binding on calmodulin: more evidence for oxidative stress in vitiligo. Biochem Biophys Res Commun 1:70–75

    Google Scholar 

  • Schwarz EC, Wissenbach U, Niemeyer BA, Straub B, Philipp SE, Flockerzi V, Zheng P, Yu B, He J, Tian G, Luo YH, Mao XB, Zhang KY, Che LQ, Chen DW (2013) Protective effects of dietary arginine supplementation against oxidative stress in weaned piglets. B. J Nutr 12:2253–2260

    Google Scholar 

  • Sohal RS, Allen RG (1990) Oxidative stress as a causal factor in differentiation and aging: a unifying hypothesis. Exp Gerontol 5:11–17

    Google Scholar 

  • Thompson LP, AI-Hasen Y (2012) Impact of oxidative stress in fetal programming. J Pregn. 2012:582748

    Google Scholar 

  • Toiyama Y, Inoue Y, Yasuda H, Saigusa S, Yokoe T, Okugawa Y, Tanaka K, Miki C, Kusunoki M (2011) DPEP1, expressed in the early stages of colon carcinogenesis, affects cancer cell invasiveness. J Gastroenterol 46:153–163

    Article  CAS  PubMed  Google Scholar 

  • Toygar M, Aydin I, Agilli M, Aydin FN, Oztosun M, Gul H, Macit E, Karslioglu Y, Topal T, Uysal B, Honca M (2015) The relation between oxidative stress, inflammation, and neopterin in the paraquat-induced lung toxicity. Hum Exp Toxicol 2:198–204

    Article  Google Scholar 

  • Trnski D, Sabol M, Gojevic A, Martinic M, Ozretic P, Musani V, Ramic S, Levanat S (2015) GSK3β and Gli3 play a role in activation of Hedgehog-Gli pathway in human colon cancer-Targeting GSK3βdownregulates the signaling pathway and reduces cell proliferation. Biochim Biophys Acta 12:2574–2584

    Article  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 15:e115

    Article  Google Scholar 

  • Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 1:1–40

    Article  Google Scholar 

  • Wan J, Jiang F, Zhang J, Xu Q, Chen D, Yu B, Mao X, Yu J, Luo Y, He J (2017) Amniotic fluid metabolomics and biochemistry analysis provides novel insights into the diet-regulated foetal growth in a pig model. Sci Rep 7:44782

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang H (2013) Livestock development in China: animal production, consumption and genetic resources. J Anim Breed Genet 4:249–251

    Article  Google Scholar 

  • Yang W, Du WW, Li X, Yee AJ, Yang BB (2016) Foxo3 activity promoted by non-coding effects of circular RNA and Foxo3 pseudogene in the inhibition of tumor growth and angiogenesis. Oncogene 35:3919–3931

    Article  CAS  PubMed  Google Scholar 

  • Yin J, Ren W, Wu X, Yang G, Su D (2013) Oxidative stress-mediated signaling pathways: a review. J Food Agric Environ 2:132–139

    Google Scholar 

  • Yin J, Wu MM, Xiao H, Ren WK, Duan JL, Yang G, Li TJ, Yin YL (2014) Development of an antioxidant system after early weaning in piglets. J Anim Sci 2:612–619

    Article  Google Scholar 

  • Yin J, Liu MF, Ren WK, Duan JL, Yang G, Zhao YR, Fang RJ, Chen LX, Li TJ, Yin YL (2015) Effect of dietary supplementation with glutamate and aspartate on diquat-induced oxidative stress in piglets. PLos One 4:e0122893

    Article  Google Scholar 

  • Yuan SB, Chen DW, Zhang KY, Yu B (2007) Effects of oxidative stress on growth performance, nutrient digestibilities and activities of antioxidative enzymes of weanling pigs. Asian Aust J Anim 10:1600–1605

    Article  Google Scholar 

  • Zheng P, Yu B, Lv M, Chen DW (2010) Effects of oxidative stress induced by diquat on arginine metabolism of post weaning pigs. Asian Aust J Anim 1:98–105

    Google Scholar 

  • Zheng P, Yu B, He J, Tian G, Mao X, Zhang K, Che L, Chen D (2013) Protective effects of dietary arginine supplementation against oxidative stress in weaned piglets. Br J Nutr 12:2253–2260

    Article  Google Scholar 

  • Zhou C, Liu GB, Wang LJ, Lu YX, Yuan L, Zheng L, Chen F, Peng FL, Li XN (2013) MiR-339–5p regulates the growth, colony formation and metastasis of colorectal cancer cells by targeting PRL-1. PLos One 5:e63142

    Article  Google Scholar 

  • Zhu LH, Zhao KL, Chen XL, Xu JX (2012) Impact of weaning and an antioxidant blend on intestinal barrier function and antioxidant status in pigs. J Anim Sci 8:2581–2589

    Article  Google Scholar 

  • Zuo JH, Wang YX, Zhu BZ, Luo YB, Wang Q, Gao LP (2018) Analysis of the coding and non-coding RNA transcriptomes in response to bell pepper chilling. Int J Mol Sci 7:2001

    Article  Google Scholar 

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Acknowledgements

This study was supported financially by the Agricultural Animal Breeding Project of Shandong Province (2020LZGC012), Funds of Shandong “Double Tops” Program (SYL2017YSTD12), Shandong Modern Pig Technology & Industry System Project (SDAIT-08-02), Shandong Provincial Natural Science Foundation (ZR2018BC046, ZR2019MC053).

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Authors and Affiliations

  1. Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, No. 61 DaiZong Street, Tai’an City, 271018, Shandong Province, People’s Republic of China

    Zhi-xin Li, Wei Chen, Ming Qin, Li-xue Wang & Yong-qing Zeng

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  1. Zhi-xin Li
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  2. Wei Chen
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  3. Ming Qin
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Correspondence to Yong-qing Zeng.

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Li, Zx., Chen, W., Qin, M. et al. Characteristics of circRNAs expression profiles in the piglets intestine induced by oxidative stress. Genes Genom 44, 425–433 (2022). https://doi.org/10.1007/s13258-021-01154-4

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