Gene ontology; Inflammation; Kyoto Encyclopedia of Genes and Genomes; Pathway; RNA sequencing; MicroRNAs; Inulin; Female; Cattle; Animals; Inulin/pharmacology; Lactation; MicroRNAs/genetics; Mastitis, Bovine; Extracellular Vesicles; Cattle Diseases; Animal Science and Zoology
Abstract :
[en] MicroRNA (miRNA) profiles vary with the nutritional and pathological conditions of cattle. In this study, we aimed to investigate the effects of inulin supplement on miRNA profiles derived from serum extracellular vesicles (EVs). Our goal was to determine the differences in miRNA expressions and analyse the pathways in which they are involved. Based on the results of California mastitis test and milk somatic cell counts, ten lactating cows with subclinical mastitis were randomly divided into two groups: an inulin group and a control group (n = 5 in each group). The inulin group received a daily supplement of 300 g of inulin while the control group did not receive any supplementation. After a 5-week treatment period, serum-derived EV-miRNAs from each cow were isolated. High-throughput sequencing was conducted to identify differentially expressed miRNAs. GO and KEGG bioinformatics analysis was performed to examine the target genes of these differentially expressed miRNAs. The EV-RNA concentration and small RNA content were not affected by the inulin treatment. A total of 162 known miRNAs and 180 novel miRNAs were identified from 10 samples in the two groups. Among the known miRNAs, 23 miRNAs were found to be differentially expressed between the two groups, with 18 upregulated and five downregulated in the inulin group compared to the control group. Pathway analysis revealed the involvement of these differentially expressed miRNAs in the regulation of cell structure and function, lipid oxidation and metabolism, immunity and inflammation, as well as digestion and absorption of nutrients. Overall, our study provides a molecular-level explanation for the reported beneficial health effects of inulin supplementation in cows with subclinical mastitis.
Disciplines :
Agriculture & agronomy
Author, co-author :
Yu, Wanjie ; Université de Liège - ULiège > TERRA Research Centre
Nan, X; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, PR China
Schroyen, Martine ; Université de Liège - ULiège > Département GxABT > Animal Sciences (AS)
Wang, Y; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, PR China
Xiong, B; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, PR China. Electronic address: xiongbenhai@caas.cn
Language :
English
Title :
Inulin-induced differences on serum extracellular vesicles derived miRNAs in dairy cows suffering from subclinical mastitis.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., Basic local alignment search tool. Journal of Molecular Biology 215 (1990), 403–410, 10.1006/jmbi.1990.9999.
Beninson, L.A., Fleshner, M., Exosomes in fetal bovine serum dampen primary macrophage IL-1 beta response to lipopolysaccharide (LPS) challenge. Immunology Letters 163 (2015), 187–192, 10.1016/j.imlet.2014.10.019.
Cai, M.C., Fan, W.Q., Li, X.Y., Sun, H.C., Dai, L.L., Lei, D.F., Dai, Y., Liao, Y.H., The regulation of staphylococcus aureus-induced inflammatory responses in bovine mammary epithelial cells. Frontiers in Veterinary Science, 8, 2021, 683886, 10.3389/fvets.2021.683886.
Chen, Y.F., Hu, F., Wang, X.G., Tang, Z., Tang, H.X., Xu, M., MicroRNA-23a-5p is involved in the regulation of lipopolysaccharide-induced acute lung injury by targeting HSP20/ASK1. Oxidative Medicine and Cellular Longevity, 2021, 2021, 9942557, 10.1155/2021/9942557.
Colitti, M., Sgorlon, S., Stefanon, B., Exosome cargo in milk as a potential marker of cow health. Journal of Dairy Research 87 (2020), 79–83, 10.1017/S0022029920000485 Pii S0022029920000485.
Dahl, G.E., McFadden, T.B., Symposium review: Environmental effects on mammary immunity and health. Journal of Dairy Science 105 (2022), 8586–8589, 10.3168/jds.2021-21433.
Duckett, S.K.K., Greene, M.A.A., Identification of microRNA transcriptome involved in bovine intramuscular fat deposition. Frontiers in Veterinary Science, 9, 2022, 10.3389/fvets.2022.883295.
Egea, V., Kessenbrock, K., Lawson, D., Bartelt, A., Weber, C., Ries, C., Let-7f miRNA regulates SDF-1 alpha- and hypoxia-promoted migration of mesenchymal stem cells and attenuates mammary tumor growth upon exosomal release. Cell Death & Disease, 12, 2021, ARTN 516, 10.1038/s41419-021-03789-3.
Gao, Z.J., Yuan, W.D., Yuan, J.Q., Yuan, K., Wang, Y., miR-486 as an unfavorable prognostic biomarker for patients with non-small cell lung cancer. Translational Cancer Research 9 (2020), 104–110, 10.21037/tcr.2019.11.19.
Garrido-Cano, I., Pla, L., Santiago-Felipe, S., Simon, S., Ortega, B., Bermejo, B., Lluch, A., Cejalvo, J.M., Eroles, P., Martinez-Manez, R., Nanoporous anodic alumina-based sensor for miR-99a-5p detection as an effective early breast cancer diagnostic tool. ACS Sensors 6 (2021), 1022–1029, 10.1021/acssensors.0c02222.
Gordon, A., Hannon, G.J., 2010. Fastx-toolkit. FASTQ/A short-reads pre-processing tools. Retrieved on 12 July 2022 from http://hannonlab.cshl.edu/fastx_toolkit/.
Griffiths-Jones, S., Bateman, A., Marshall, M., Khanna, A., Eddy, S.R., Rfam: an RNA family database. Nucleic Acids Research 31 (2003), 439–441, 10.1093/nar/gkg006.
He, Y.Y., He, Z.C., Leone, S., Liu, S.B., Milk exosomes transfer oligosaccharides into macrophages to modulate immunity and attenuate adherent-invasive E. coli (AIEC) infection. Nutrients, 13, 2021, 3198, 10.3390/nu13093198.
Hock, A., Miyake, H., Li, B., Lee, C., Ermini, L., Koike, Y., Chen, Y., Maattanen, P., Zani, A., Pierro, A., Breast milk-derived exosomes promote intestinal epithelial cell growth. Journal of Pediatric Surgery 52 (2017), 755–759, 10.1016/j.jpedsurg.2017.01.032.
Hu, J., Xu, Y.X., Hao, J.L., Wang, S.F., Li, C.F., Meng, S.D., MiR-122 in hepatic function and liver diseases. Protein & Cell 3 (2012), 364–371, 10.1007/s13238-012-2036-3.
Huang, J., Fu, X.L., Chen, X., Xu, S., Yu, J., Silencing of miR-486 alleviates LPS-stimulated inflammatory response of macrophages through targeting SIRT1. RSC Advances 9 (2019), 17057–17064, 10.1039/c9ra01374a.
Huang, Y.L., Huang, G.Y., Lv, J., Pan, L.N., Luo, X., Shen, J., miR-100 promotes the proliferation of spermatogonial stem cells via regulating Stat3. Molecular Reproduction and Development 84 (2017), 693–701, 10.1002/mrd.22843.
Kasimanickam, V., Kastelic, J., Circulating cell-free mature microRNAs and their target gene prediction in bovine metritis. Scientific Reports, 6, 2016, 29509, 10.1038/srep29509.
Khan, A., Ahmed, T., Rizwan, M., Khan, N., Comparative therapeutic efficacy of Phyllanthus emblica (Amla) fruit extract and procaine penicillin in the treatment of subclinical mastitis in dairy buffaloes. Microbial Pathogenesis 115 (2018), 8–11, 10.1016/j.micpath.2017.12.038.
Kosaka, N., Izumi, H., Sekine, K., Ochiya, T., microRNA as a new immune-regulatory agent in breast milk. Silence, 1, 2010, 7, 10.1186/1758-907X-1-7.
Kozomara, A., Birgaoanu, M., Griffiths-Jones, S., miRBase: from microRNA sequences to function. Nucleic Acids Research 47 (2019), D155–D162, 10.1093/nar/gky1141.
Lai, Y.C., Fujikawa, T., Maemura, T., Ando, T., Kitahara, G., Endo, Y., Yamato, O., Koiwa, M., Kubota, C., Miura, N., Inflammation-related microRNA expression level in the bovine milk is affected by mastitis. PLoS One1, 12, 2017, 10.1371/journal.pone.0177182.
Lai, Y.C., Habiby, G.H., Pathiranage, C.C.J., Rahman, M.M., Chen, H.W., Husna, A., Kubota, C., Miura, N., Bovine serum miR-21 expression affected by mastitis. Research in Veterinary Science 135 (2021), 290–292, 10.1016/j.rvsc.2020.10.001.
Lu, Z.Y., Wang, D.W., Wang, X.M., Zou, J.L., Sun, J.B., Bi, Z.G., MiR-206 regulates the progression of osteoporosis via targeting HDAC4. European Journal of Medical Research, 26, 2021, 10.1186/s40001-021-00480-3.
Lukasik, A., Zielenkiewicz, P., Plant MicroRNAs-novel players in natural medicine?. International Journal of Molecular Sciences, 18, 2017, 9, 10.3390/ijms18010009.
Manca, S., Upadhyaya, B., Mutai, E., Desaulniers, A.T., Cederberg, R.A., White, B.R., Zempleni, J., Milk exosomes are bioavailable and distinct microRNA cargos have unique tissue distribution patterns. Scientific Reports, 8, 2018, 11321, 10.1038/s41598-018-29780-1.
Mao, J., Wang, B., Li, Y.J., Associations of serum expressions of miR-499 and sex determining region Y-box 6 with prognosis of acute myocardial infarction patients. Revista Romana De Medicina De Laborator 30 (2022), 151–161, 10.2478/rrlm-2022-0011.
Munagala, R., Aqil, F., Jeyabalan, J., Gupta, R.C., Bovine milk-derived exosomes for drug delivery. Cancer Letters 371 (2016), 48–61, 10.1016/j.canlet.2015.10.020.
Naeem, A., Zhong, K., Moisa, S.J., Drackley, J.K., Moyes, K.M., Loor, J.J., Bioinformatics analysis of microRNA and putative target genes in bovine mammary tissue infected with Streptococcus uberis. Journal of Dairy Science 95 (2012), 6397–6408, 10.3168/jds.2011-5173.
Olagaray, K.E., Brouk, M.J., Mamedova, L.K., Sivinski, S.E., Liu, H., Robert, F., Dupuis, E., Zachut, M., Bradford, J., Dietary supplementation of Scutellaria baicalensis extract during early lactation decreases milk somatic cells and increases whole lactation milk yield in dairy cattle. PLoS One1, 14, 2019, 10.1371/journal.pone.0210744.
Ozdemir, S., Expression profiles of inflammation-related MicroRNAs in mycoplasma Bovis infected milk of Holstein-Friesian and Dogu Anadolu Kirmizisi cows. Ksu Tarim Ve Doga Dergisi-Ksu Journal of Agriculture and Nature 23 (2020), 762–771, 10.18016/ksutarimdoga.vi.661708.
Patel, R.K., Jain, M., NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One, 7, 2012, e30619.
Quan, S.Y., Nan, X.M., Wang, K., Jiang, L.S., Yao, J.H., Xiong, B.H., Different diets change the expression of bovine serum extracellular vesicle-miRNAs. Animals, 9, 2019, ARTN 1137, 10.3390/ani9121137.
Ran, H.B., Yang, Y., Luo, M.N., Liu, X.R., Yue, B.L., Chai, Z.X., Zhong, J.C., Wang, H., Molecular regulation of yak preadipocyte differentiation and proliferation by LncFAM200B and ceRNA regulatory network analysis. Cells, 11, 2022, 2366, 10.3390/cells11152366.
Romao, J.M., Jin, W., He, M., McAllister, T., Guan, L.L., Altered MicroRNA expression in bovine subcutaneous and visceral adipose tissues from cattle under different diet. PLoS One, 7, 2012, e40605.
Ross, M., Atalla, H., Karrow, N., Mallard, B.A., The bioactivity of colostrum and milk exosomes of high, average, and low immune responder cows on human intestinal epithelial cells. Journal of Dairy Science 104 (2021), 2499–2510, 10.3168/jds.2020-18405.
Saiyed, A.N., Vasavada, A.R., Johar, S.R.K., Recent trends in miRNA therapeutics and the application of plant miRNA for prevention and treatment of human diseases. Future Journal of Pharmaceutical Sciences, 8, 2022, 24, 10.1186/s43094-022-00413-9.
Samuel, M., Fonseka, P., Sanwlani, R., Gangoda, L., Chee, S.H., Keerthikumar, S., Spurling, A., Chitti, S.V., Zanker, D., Ang, C.S., Atukorala, I., Kang, T., Shahi, S., Marzan, A.L., Nedeva, C., Vennin, C., Lucas, M.C., Cheng, L., Herrmann, D., Pathan, M., Chisanga, D., Warren, S.C., Zhao, K.N., Abraham, N., Anand, S., Boukouris, S., Adda, C.G., Jiang, L.Z., Shekhar, T.M., Baschuk, N., Hawkins, C.J., Johnston, A.J., Orian, J.M., Hoogenraad, N.J., Poon, I.K., Hill, A.F., Jois, M., Timpson, P., Parker, B.S., Mathivanan, S., Oral administration of bovine milk-derived extracellular vesicles induces senescence in the primary tumor but accelerates cancer metastasis. Nature Communications, 12, 2021, 3950, 10.1038/s41467-021-24273-8.
Stoorvogel, W., Kleijmeer, M.J., Geuze, H.J., Raposo, G., The biogenesis and functions of exosomes. Traffic 3 (2002), 321–330, 10.1034/j.1600-0854.2002.30502.x.
Sui, G., Jia, L., Song, N., Min, D., Chen, S., Wu, Y., Yang, G., Aberrant expression of HDL-bound microRNA induced by a high-fat diet in a pig model: implications in the pathogenesis of dyslipidaemia. BMC Cardiovascular Disorders, 21, 2021, 280, 10.1186/s12872-021-02084-5.
Tang, X.L., Yang, M.Y., Wang, Z., Wu, X.Q., Wang, D.R., MicroRNA-23a promotes colorectal cancer cell migration and proliferation by targeting at MARK1. Acta Biochimica Et Biophysica Sinica 51 (2019), 661–668, 10.1093/abbs/gmz047.
Tino, P., Basic properties and information theory of Audic-Claverie statistic for analyzing cDNA arrays. BMC Bioinformatics, 10, 2009, 310, 10.1186/1471-2105-10-310.
Usman, M., Zhang, C.N., Patil, P.J., Mehmood, A., Li, X.T., Bilal, M., Haider, J., Ahmad, S., Potential applications of hydrophobically modified inulin as an active ingredient in functional foods and drugs – A review. Carbohydrate Polymers, 252, 2021, 10.1016/j.carbpol.2020.117176.
van Niel, G., Carter, D.R.F., Clayton, A., Lambert, D.W., Raposo, G., Vader, P., Challenges and directions in studying cell-cell communication by extracellular vesicles. Nature Reviews Molecular Cell Biology 23 (2022), 369–382, 10.1038/s41580-022-00460-3.
Wang, Y., Nan, X.M., Zhao, Y.G., Wang, H., Wang, M.L., Jiang, L.S., Zhang, F., Xue, F.G., Hua, D.K., Li, K.M., Liu, J., Yao, J.H., Xiong, B.H., Coupling 16S rDNA sequencing and untargeted mass spectrometry for milk microbial composition and metabolites from dairy cows with clinical and subclinical mastitis. Journal of Agricultural and Food Chemistry 68 (2020), 8496–8508, 10.1021/acs.jafc.0c03738.
Wang, Y., Nan, X.M., Zhao, Y.G., Jiang, L.S., Wang, H., Hua, D.K., Zhang, F., Wang, Y.P., Liu, J., Yao, J.H., Xiong, B.H., Dietary supplementation with inulin improves lactation performance and serum lipids by regulating the rumen microbiome and metabolome in dairy cows. Animal Nutrition 7 (2021), 1189–1204, 10.1016/j.aninu.2021.09.007.
Wang, Y., Nan, X.M., Zhao, Y.G., Jiang, L.S., Wang, H., Zhang, F., Hua, D.K., Liu, J., Yao, J.H., Yang, L., Xiong, B.H., Consumption of Supplementary Inulin Modulates Milk Microbiota and Metabolites in Dairy Cows with Subclinical Mastitis. Applied and Environmental Microbiology, 88, 2022, 10.1128/aem.02059-21.
Wang, W.G., Zhan, R.S., Zhou, J.H., Wang, J.L., Chen, S.J., MiR-10 targets NgR to modulate the proliferation of microglial cells and the secretion of inflammatory cytokines. Experimental and Molecular Pathology 105 (2018), 357–363, 10.1016/j.yexmp.2018.10.006.
Wu, X.L., Cheng, B., Li, P.Y., Huang, H.J., Zhao, Q., Dan, Z.L., Tian, D., Zhang, P., MicroRNA-143 suppresses gastric cancer cell growth and induces apoptosis by targeting COX-2. World Journal of Gastroenterology 19 (2013), 7758–7765, 10.3748/wjg.v19.i43.7758.
Wu, D., Kittana, H., Shu, J., Kachman, S.D., Cui, J., Ramer-Tait, A.E., Zempleni, J., Dietary depletion of milk exosomes and their MicroRNA cargos elicits a depletion of miR-200a-3p and elevated intestinal inflammation and chemokine (C-X-C Motif) ligand 9 expression in Mdr1a(-/-) mice. Current Developments Nutrition, 3, 2019, 10.1093/cdn/nzz122.
Wu, R.Y., Maattanen, P., Napper, S., Scruten, E., Li, B., Koike, Y., Johnson-Henry, K.C., Pierro, A., Rossi, L., Botts, S.R., Surette, M.G., Sherman, P.M., Non-digestible oligosaccharides directly regulate host kinome to modulate host inflammatory responses without alterations in the gut microbiota. Microbiome, 5, 2017, 135, 10.1186/s40168-017-0357-4.
Xie, H.G., Lei, N.F., Gong, A.Y., Chen, X.M., Hu, G.K., Cryptosporidium parvum induces SIRT1 expression in host epithelial cells through downregulating let-7i. Human Immunology 75 (2014), 760–765, 10.1016/j.humimm.2014.05.007.
Yang, P., Han, J.H., Li, S.G., Luo, S.N., Tu, X.S., Ye, Z.Q., miR-128-3p inhibits apoptosis and inflammation in LPS-induced sepsis by targeting TGFBR2. Open Medicine 16 (2021), 274–283, 10.1515/med-2021-0222.
Yu, J.H., Long, L., Luo, Z.X., Li, L.M., You, J.R., Anti-inflammatory role of microRNA let-7c in LPS treated alveolar macrophages by targeting STAT3. Asian Pacific Journal of Tropical Medicine 9 (2016), 69–72, 10.1016/j.apjtm.2015.12.015.
Yun, B., Kim, Y., Park, D.J., Oh, S., Comparative analysis of dietary exosome-derived microRNAs from human, bovine and caprine colostrum and mature milk. Journal of Animal Science and Technology 63 (2021), 593–602, 10.5187/jast.2021.e39.
Zempleni, J., Aguilar-Lozano, A., Sadri, M., Sukreet, S., Manca, S., Wu, D., Zhou, F., Mutai, E., Biological activities of extracellular vesicles and their cargos from bovine and human milk in humans and implications for infants. Journal of Nutrition 147 (2017), 3–10, 10.3945/jn.116.238949.
Zhang, B.H., Wang, Q.L., Pan, X.P., MicroRNAs and their regulatory roles in animals and plants. Journal of Cellular Physiology 210 (2007), 279–289, 10.1002/jcp.20869.
Zhao, K., Liang, G.X., Sun, X., Guan, L.L., Comparative miRNAome analysis revealed different miRNA expression profiles in bovine sera and exosomes. BMC Genomics, 17, 2016, 630, 10.1186/s12864-016-2962-1.
