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Screening candidate microR-15a- IRAK2 regulatory pairs for predicting the response to Staphylococcus aureus-induced mastitis in dairy cows

Published online by Cambridge University Press:  14 November 2019

Zhi Chen ,
Jingpeng Zhou ,
Xiaolong Wang ,
Yang Zhang ,
Xubin Lu ,
Yongliang Fan ,
Yongjiang Mao ,
Juan J. Loor  and
Zhangping Yang
Zhi Chen
Affiliation:
College of Animal Science and Technology, Yangzhou University, Yangzhou225009, PR China Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education, Yangzhou University, Yangzhou225009, China
Jingpeng Zhou
Affiliation:
College of Animal Science and Technology, Yangzhou University, Yangzhou225009, PR China Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education, Yangzhou University, Yangzhou225009, China
Xiaolong Wang
Affiliation:
College of Animal Science and Technology, Yangzhou University, Yangzhou225009, PR China Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education, Yangzhou University, Yangzhou225009, China
Yang Zhang
Affiliation:
Animal husbandry and veterinary station of Zhiqian, Jintan District, Changzhou, 213200, China
Xubin Lu
Affiliation:
College of Animal Science and Technology, Yangzhou University, Yangzhou225009, PR China Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education, Yangzhou University, Yangzhou225009, China
Yongliang Fan
Affiliation:
College of Animal Science and Technology, Yangzhou University, Yangzhou225009, PR China Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education, Yangzhou University, Yangzhou225009, China
Yongjiang Mao
Affiliation:
College of Animal Science and Technology, Yangzhou University, Yangzhou225009, PR China Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education, Yangzhou University, Yangzhou225009, China
Juan J. Loor
Affiliation:
Mammalian Nutrition Physiology Genomics, Department of Animal Sciences and Division of Nutritional Sciences, University of Illinois, Urbana, IL61801, USA
Zhangping Yang*
Affiliation:
College of Animal Science and Technology, Yangzhou University, Yangzhou225009, PR China Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education, Yangzhou University, Yangzhou225009, China
*
Author for correspondence: Zhangping Yang, Email: yzp@yzu.edu.cn
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Abstract

We established a mastitis model using exogenous infection of the mammary gland of Chinese Holstein cows with Staphylococcus aureus and extracted total RNA from S. aureus-infected and healthy mammary quarters. Differential expression of genes due to mastitis was evaluated using Affymetrix technology and results revealed a total of 1230 differentially expressed mRNAs. A subset of affected genes was verified via Q-PCR and pathway analysis. In addition, Solexa high-throughput sequencing technology was used to analyze profiles of miRNA in infected and healthy quarters. These analyses revealed a total of 52 differentially expressed miRNAs. A subset of those results was verified via Q-PCR. Bioinformatics techniques were used to predict and analyze the correlations among differentially expressed miRNA and mRNA. Results revealed a total of 329 pairs of negatively associated miRNA/mRNA, with 31 upregulated pairs of mRNA and 298 downregulated pairs of mRNA. Differential expression of miR-15a and interleukin-1 receptor-associated kinase-like 2 (IRAK2), were evaluated by western blot and luciferase reporter assays. We conclude that miR-15a and miR-15a target genes (IRAK2) constitute potential miRNA–mRNA regulatory pairs for use as biomarkers to predict a mastitis response.

Keywords

Differential genes and microRNAsIRAK2MastitisMicroRNA-mRNA networkmiR-15aStaphylococcus aureus
Type
Research Article
Information
Journal of Dairy Research , Volume 86 , Issue 4 , November 2019 , pp. 425 - 431
Copyright
Copyright © Hannah Dairy Research Foundation 2019

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References

Allard, M, Ster, C, Jacob, CL, Scholl, D, Diarra, MS, Lacasse, P and Malouin, F (2013) The expression of a putative exotoxin and an ABC transporter during bovine intramammary infection contributes to the virulence of Staphylococcus aureus. Veterinary Microbiology 162, 761–770.CrossRefGoogle ScholarPubMed
Anderson, KL and Lyman, RL (2006) Long-term persistence of specific genetic types of mastitis-causing Staphylococcus aureus on three dairies. Journal of Dairy Science 89, 4551–4556.CrossRefGoogle ScholarPubMed
Bayega, A, Fahiminiya, S, Oikonomopoulos, S and Ragoussis, J (2018) Current and future methods for mRNA analysis: a drive toward single molecule sequencing. Methods in Molecular Biology 1783, 209–241.CrossRefGoogle ScholarPubMed
Calin, GA, Amelia, C, Muller, F, Manuela, F, Sylwia, EW, Masayoshi, S, Cristian, T, Nicola, Z, Ramiro, G, Rami, IA, Hansjuerg, A, Stefano, V, Laura, R, Liu, X, Liu, C, Thomas, J, Massimo, N and Carlo, MC (2008) MiR-15a and miR-16-1 cluster functions in human leukemia. Proceedings of the National Academy of Sciences of the United States of America 105, 5166–5171.CrossRefGoogle ScholarPubMed
Chen, Z, Luo, J, Zhang, C, Ma, Y, Sun, S, Zhang, T and Loor, JJ (2018a) Mechanism of prolactin inhibition of miR-135b via methylation in goat mammary epithelial cells. Journal of Cellular Physiology 233, 651–662.CrossRefGoogle Scholar
Chen, Z, Xia, H, Shen, H, Xu, X, Arbab, AAI, Li, M, Zhang, H, Mao, Y and Yang, Z (2018b) Pathological features of Staphylococcus aureus induced mastitis in dairy cows and isobaric-tags-for-relative-and-absolute-quantitation proteomic analyses. Journal of Agricultural and Food Chemistry 66, 3880–3890.CrossRefGoogle Scholar
Firth, CL, Kasbohrer, A, Schleicher, C, Fuchs, K, Egger-Danner, C, Mayerhofer, M, Schobesberger, H, Kofer, HJ and Obritzhauser, W (2017) Antimicrobial consumption on Austrian dairy farms: an observational study of udder disease treatments based on veterinary medication records. PeerJ 5, e4072.Google ScholarPubMed
Jia, L, Zhou, X, Huang, X, Xu, X, Jia, Y, Wu, Y, Yao, J, Wu, Y and Wang, K (2018) Maternal and umbilical cord serum-derived exosomes enhance endothelial cell proliferation and migration. FASEB Journal 32, fj201701337RR.CrossRefGoogle ScholarPubMed
Jin, W, Ibeagha-Awemu, EM and Liang, G (2014) Transcriptome microRNA profiling of bovine mammary epithelial cells challenged with Escherichia coli or Staphylococcus aureus bacteria reveals pathogen directed microRNA expression profiles. BMC Genomics 15, 181.CrossRefGoogle ScholarPubMed
Kung, LHW, Ravi, V, Rowley, L, Bell, KM, Little, CB and Bateman, JF (2017) Comprehensive expression analysis of microRNAs and mRNAs in synovial tissue from a mouse model of early post-traumatic osteoarthritis. Scientific Reports 7, 17701.CrossRefGoogle ScholarPubMed
Lewandowska-Sabat, AM, Boman, GM, Downing, A, Talbot, R, Storset, AK and Olsaker, L (2013) The early phase transcriptome of bovine monocyte-derived macrophages infected with Staphylococcus aureus in vitro. BMC Genomics 14, 891.CrossRefGoogle ScholarPubMed
Li, R, Zhang, C, Liao, X, Chen, D, Wang, W, Zhu, Y, Geng, X, Ji, D, Mao, Y, Gong, Y and Yang, Z (2015) Transcriptome MicroRNA profiling of bovine mammary glands infected with Staphylococcus aureus. International Journal of Molecular Sciences 16, 4997–5013.CrossRefGoogle ScholarPubMed
Li, C, Ding, X, Liu, Z and Zhu, J (2017) Rapid identification of Candida spp. frequently involved in invasive mycoses by using flow-through hybridization and gene chip (FHGC) technology. Journal of Microbiological Methods 132, 160–165.CrossRefGoogle ScholarPubMed
Liu, N, Yang, J, Fu, X, Zhang, L, Tang, K, Guy, KM, Hu, Z, Guo, S, Xu, Y and Zhang, M (2016) Genome-wide identification and comparative analysis of grafting-responsive mRNA in watermelon grafted onto bottle gourd and squash rootstocks by high-throughput sequencing. Molecular Genetics And Genomics: MGG 291, 621–633.CrossRefGoogle ScholarPubMed
Liu, J, Chen, Y, Huang, Q, Liu, W, Ji, X, Hu, F, Zhu, Y, Zhang, L and Dong, G (2018) IRAK2 counterbalances oncogenic Smurf1 in colon cancer cells by dictating ER stress. Cellular Signalling 48, 69–80.CrossRefGoogle ScholarPubMed
Love, MI, Huber, W and Anders, S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 550.CrossRefGoogle ScholarPubMed
Luo, ZM, Wang, XP, Mei, CG and Zan, LS (2018a) Expression profiling of peripheral blood miRNA using RNAseq technology in dairy cows with Escherichia coli-induced mastitis. Scientific Reports 8, 12693.Google Scholar
Luo, ZM, Wang, XP and Zan, LS (2018b) Comparison of microRNA profiles between bovine mammary glands infected with Staphylococcus aureus and Escherichia coli. International Journal of Biological Science 14, 87–99.Google Scholar
Mao, YJ, Zhu, XR, Li, R, Chen, D, Xin, SY, Zhu, YH, Liao, XX, Wang, XL, Zhang, HM and Yang, ZP (2015) Methylation analysis of CXCR1 in mammary gland tissue of cows with mastitis induced by Staphylococcus aureus. Genetics and Molecular Research: GMR 14, 12606–12615.CrossRefGoogle ScholarPubMed
Moon, HG, Yang, J, Zheng, Y and Jin, Y (2014) miR-15a/16 regulates macrophage phagocytosis after bacterial infection. Journal of Immunology 193, 4558–4567.CrossRefGoogle ScholarPubMed
Medina-Estrada, I, Lopez-Meza, JE and Ochoa-Zarzosa, A (2016) Anti-inflammatory and antimicrobial effects of estradiol in bovine mammary epithelial cells during Staphylococcus aureus internalization. Mediators of Inflammation 2016, 6120509.CrossRefGoogle ScholarPubMed
Nozaki, T, Sasaki, Y, Fukuda, I, Isumi, M, Nakamoto, K, Onodera, T and Masutani, M (2018) Next-generation sequencing-based miRNA expression analysis in Parp1-deficient embryonic stem cell-derived exosomes. Biochemical and Biophysical Research Communications 499, 410–415.CrossRefGoogle ScholarPubMed
Piechota, M, Korostynski, M, Ficek, J, Tomski, A and Przewlocki, R (2016) Seqinspector: position-based navigation through the ChIP-seq data landscape to identify gene expression regulators. BMC Bioinformatics 17, 85.CrossRefGoogle ScholarPubMed
Pokorska, J, Dusza, M, Kulaj, D, Zukowski, K and Makulska, J (2016) Single nucleotide polymorphisms in the CXCR1 gene and its association with clinical mastitis incidence in Polish Holstein-Friesian cows. Genetics and Molecular Research : GMR 15, 1–8.CrossRefGoogle ScholarPubMed
Pu, J, Li, R, Zhang, C, Chen, D, Liao, X, Zhu, Y, Geng, X, Ji, D, Mao, Y, Gong, Y and Yang, Z (2017) Expression profiles of miRNAs from bovine mammary glands in response to Streptococcus agalactiae-induced mastitis. Journal of Dairy Research 84, 300–308.CrossRefGoogle ScholarPubMed
Ramirez, HA, Pastar, I, Jozic, I, Stojadinovic, O, Stone, RC, Ojeh, N, Gil, J, Davis, SC, Kirsner, RS and Tomic-Canic, M (2018) Staphylococcus aureus triggers induction of miR-15B-5P to diminish DNA repair and deregulate inflammatory response in diabetic foot ulcers. The Journal of Investigative Dermatology 138, 1187–1196.CrossRefGoogle ScholarPubMed
Sun, J, Aswath, K, Schroeder, SG, Lippolis, JD, Reinhardt, TA and Sonstegard, TS (2015) MicroRNA expression profiles of bovine milk exosomes in response to Staphylococcus aureus infection. BMC Genomics 16, 806.CrossRefGoogle ScholarPubMed
Tino, P (2009) Basic properties and information theory of Audic-Claverie statistic for analyzing cDNA arrays. BMC Bioinformatics 10, 310.CrossRefGoogle ScholarPubMed
Wang, R, Ma, WG, Gao, GD, Mao, QX, Zheng, J, Sun, LZ and Liu, YL (2011) Fluoro jade-C staining in the assessment of brain injury after deep hypothermia circulatory arrest. Brain Research 1372, 127–132.CrossRefGoogle ScholarPubMed
Zbinden, C, Pilo, P, Frey, J, Bruckmaier, RM and Wellnitz, O (2015) The immune response of bovine mammary epithelial cells to live or heat-inactivated Mycoplasma bovis. Veterinary Microbiology 179, 336–340.CrossRefGoogle ScholarPubMed
Zhang, H, Li, H, Liu, Y, Li, Q, Bi, Y and Fang, G (2016) Upregulated effects of miR-7 in methicillin-resistant Staphylococcus aureus. Experimental and Therapeutic Medicine 12, 3571–3574.CrossRefGoogle ScholarPubMed
Zhang, X, Li, K, Xing, R, Liu, S, Chen, X, Yang, H and Li, P (2018) miRNA and mRNA expression profiles reveal insight into chitosan-mediated regulation of plant growth. Journal of Agricultural and Food Chemistry 66, 3810–3822.CrossRefGoogle ScholarPubMed
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