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The effect of baicalin on microRNA expression profiles in porcine aortic vascular endothelial cells infected by Haemophilus parasuis

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Abstract

Glässer’s disease, caused by Haemophilus parasuis (H. parasuis), is associated with vascular damage and vascular inflammation in pigs. Therefore, early assessment and treatment are essential to control the inflammatory disorder. MicroRNAs have been shown to be involved in the vascular pathology. Baicalin has important pharmacological functions, including anti-inflammatory, antimicrobial and antioxidant effects. In this study, we investigated the changes of microRNAs in porcine aortic vascular endothelial cells (PAVECs) induced by H. parasuis and the effect of baicalin in this model by utilizing high-throughput sequencing. The results showed that 155 novel microRNAs and 76 differentially expressed microRNAs were identified in all samples. Subsequently, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis of the target genes of the differentially expressed microRNAs demonstrated that regulation of actin cytoskeleton, focal adhesion, ECM-receptor interaction, bacterial invasion of epithelial cells, and adherens junction were the most interesting pathways after PAVECs were infected with H. parasuis. In addition, when the PAVECs were pretreated with baicalin, mismatch repair, peroxisome, oxidative phosphorylation, DNA replication, and ABC transporters were the most predominant signaling pathways. STRING analysis showed that most of the target genes of the differentially expressed microRNAs were associated with each other. The expression levels of the differentially expressed microRNAs were negatively co-regulated with their target genes’ mRNA following pretreatment with baicalin in the H. parasuis-induced PAVECs using co-expression networks analysis. This is the first report that microRNAs might have key roles in inflammatory damage of vascular tissue during H. parasuis infection. Baicalin regulated the microRNAs changes in the PAVECs following H. parasuis infection, which may represent useful novel targets to prevent or treat H. parasuis infection.

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References

  1. Ye C, Li RZ, Xu L et al (2019) Effects of Baicalin on piglet monocytes involving PKC-MAPK signaling pathways induced by Haemophilus parasuis. BMC Vet Res 15:98

    PubMed  PubMed Central  Google Scholar 

  2. Rafiee M, Blackall PJ (2000) Establishment, validation and use of the Kielstein-Rapp-Gabrielson serotyping scheme for Haemophilus parasuis. Aust Vet J 78:172–174

    CAS  PubMed  Google Scholar 

  3. Cai XW, Chen HC, Blackall PJ et al (2005) Serological characterization of Haemophilus parasuis isolates from China. Vet Microbiol 111:231–236

    PubMed  Google Scholar 

  4. Rosner H, Kielstein P, Muller W et al (1991) Relationship between serotype, virulence and SDS-PAGE protein patterns of Haemophilus parasuis. Dtsch Tierarztl Wochenschr 98:327–330

    CAS  PubMed  Google Scholar 

  5. Guo L, Guo J, Liu HS et al (2018) Tea polyphenols suppress growth and virulence-related factors of Haemophilus parasuis. J Vet Med Sci 80:1047–1053

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Shen YJ, Zhou NN, An JH et al (2019) Haemophilus parasuis infection in 3D4/21 cells induces autophagy through the AMPK pathway. Cell Microbiol 21:e13031

    PubMed  Google Scholar 

  7. Hua KX, Li YJ, Zhou HF et al (2018) Haemophilus parasuis infection disrupts adherens junctions and initializes EMT dependent on canonical Wnt/beta-catenin signaling pathway. Front Cell Infect Microbiol 8:324

    PubMed  PubMed Central  Google Scholar 

  8. Wen YP, Wen YP, Wen XT et al (2018) OxyR of Haemophilus parasuis is a global transcriptional regulator important in oxidative stress resistance and growth. Gene 643:107–116

    CAS  PubMed  Google Scholar 

  9. He LQ, Dai K, Wen XT et al (2018) QseC mediates osmotic stress resistance and biofilm formation in Haemophilus parasuis. Front Microbiol 9:212

    PubMed  PubMed Central  Google Scholar 

  10. Wang HY, Ding Q, Wang MJ et al (2019) miR-29b inhibits the progression of multiple myeloma through downregulating FOXP1. Hematology 24:32–38

    CAS  PubMed  Google Scholar 

  11. Mollaei H, Safaralizadeh R, Rostami Z (2019) MicroRNA replacement therapy in cancer. J Cell Physiol 234:12369–12384

    CAS  PubMed  Google Scholar 

  12. Tili E, Michaille JJ, Piurowski V et al (2017) MicroRNAs in intestinal barrier function, inflammatory bowel disease and related cancers-their effects and therapeutic potentials. Curr Opin Pharmacol 37:142–150

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Neudecker V, Yuan XY, Bowser JL et al (2017) MicroRNAs in mucosal inflammation. J Mol Med (Berlin) 95:935–949

    CAS  Google Scholar 

  14. Su W, Aloi MS, Garden GA (2016) MicroRNAs mediating CNS inflammation: Small regulators with powerful potential. Brain Behav Immun 52:1–8

    PubMed  Google Scholar 

  15. Guo L, Tsai SQ, Hardison NE et al (2013) Differentially expressed microRNAs and affected biological pathways revealed by modulated modularity clustering (MMC) analysis of human preeclamptic and IUGR placentas. Placenta 34:599–605

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Yang MZ, Kan L, Wu LY et al (2019) Effect of baicalin on renal function in patients with diabetic nephropathy and its therapeutic mechanism. Exp Ther Med 17:2071–2076

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Huang T, Liu YN, Zhang CL (2019) Pharmacokinetics and bioavailability enhancement of baicalin: a review. Eur J Drug Metab Pharmacokinet 44:159–168

    PubMed  Google Scholar 

  18. Yang XR, Zhang Q, Gao ZM et al (2018) Baicalin alleviates IL-1beta-induced inflammatory injury via down-regulating miR-126 in chondrocytes. Biomed Pharmacother 99:184–190

    CAS  PubMed  Google Scholar 

  19. Wang L, Zhang R, Chen J et al (2017) Baicalin protects against TNF-alpha-induced injury by down-regulating miR-191a that targets the tight junction protein ZO-1 in IEC-6 cells. Biol Pharm Bull 40:435–443

    CAS  PubMed  Google Scholar 

  20. Wu XJ, Zhi FC, Lun WJ et al (2018) Baicalin inhibits PDGF-BB-induced hepatic stellate cell proliferation, apoptosis, invasion, migration and activation via the miR-3595/ACSL4 axis. Int J Mol Med 41:1992–2002

    PubMed  PubMed Central  Google Scholar 

  21. Yue M, Yang F, Yang J et al (2009) Complete genome sequence of Haemophilus parasuis SH0165. J Bacteriol 191:1359–1360

    CAS  PubMed  Google Scholar 

  22. Fu SL, Guo J, Li RZ et al (2018) Transcriptional profiling of host cell responses to virulent Haemophilus parasuis: new insights into pathogenesis. Int J Mol Sci 19:1320

    PubMed Central  Google Scholar 

  23. Song J, Hu YJ, Jiang X et al (2018) Profiling of novel microRNAs elicited by EV71 and CA16 infection in human bronchial epithelial cells using high-throughput sequencing. Virus Res 247:111–119

    CAS  PubMed  Google Scholar 

  24. Kim SH, Kang DW, Huo ZG et al (2018) Meta-analytic principal component analysis in integrative omics application. Bioinformatics 34:1321–1328

    CAS  PubMed  Google Scholar 

  25. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    CAS  Google Scholar 

  26. Blake JA, Chan J, Kishore R et al (2015) Gene ontology consortium: going forward. Nucleic Acids Res 43:D1049–1056

    CAS  Google Scholar 

  27. Minoru K, Susumu G (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Google Scholar 

  28. Liu X, Wei HC, Liao S et al (2018) MicroRNA transcriptome analysis of porcine vital organ responses to immunosuppressive porcine cytomegalovirus infection. Virol J 15:16

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Li HM, Xiao YJ, Min ZS et al (2019) Identification and interaction analysis of key genes and microRNAs in atopic dermatitis by bioinformatics analysis. Clin Exp Dermatol 44:257–264

    CAS  PubMed  Google Scholar 

  30. Matouskova P, Hanouskova B, Skalova L (2018) MicroRNAs as potential regulators of glutathione peroxidases expression and their role in obesity and related pathologies. Int J Mol Sci 19:1199

    PubMed Central  Google Scholar 

  31. Huang Y, Ma XY, Yang YB et al (2016) Identification and characterization of microRNAs and their target genes from Nile tilapia (Oreochromis niloticus). Z Naturforsch C 71:215–223

    CAS  PubMed  Google Scholar 

  32. Taibi F, Metzinger-Le Meuth V, M'Baya-Moutoula E et al (2014) Possible involvement of microRNAs in vascular damage in experimental chronic kidney disease. Biochim Biophys Acta 1842:88–98

    CAS  PubMed  Google Scholar 

  33. Wilson R, Espinosa-Diez C, Kanner N et al (2016) MicroRNA regulation of endothelial TREX1 reprograms the tumour microenvironment. Nat Commun 7:13597

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Kingsley SMK, Bhat BV (2017) Role of microRNAs in sepsis. Inflamm Res 66:553–569

    CAS  PubMed  Google Scholar 

  35. Jaeger A, Hadlich F, Kemper N et al (2017) MicroRNA expression profiling of porcine mammary epithelial cells after challenge with Escherichia coli in vitro. BMC Genom 18:660

    CAS  Google Scholar 

  36. Ahmadi M, Yousefi M, Abbaspour-Aghdam S et al (2019) Disturbed Th17/Treg balance, cytokines, and miRNAs in peripheral blood of patients with Behcet's disease. J Cell Physiol 234:3985–3994

    CAS  PubMed  Google Scholar 

  37. Wang ZJ, Gai YD, Zhou JL et al (2019) miR-375 mediates the CRF signaling pathway to regulate catecholamine biosynthesis by targeting Sp1 in porcine adrenal gland. Stress 22:332–346

    CAS  PubMed  Google Scholar 

  38. Guo J, Yang C, Zhang SX et al (2019) MiR-375 induces ROS and apoptosis in ST cells by targeting the HIGD1A gene. Gene 685:136–142

    CAS  PubMed  Google Scholar 

  39. Garikipati VNS, Verma SK, Jolardarashi D et al (2017) Therapeutic inhibition of miR-375 attenuates post-myocardial infarction inflammatory response and left ventricular dysfunction via PDK-1-AKT signalling axis. Cardiovasc Res 113:938–949

    CAS  PubMed  Google Scholar 

  40. Wang X, Sun H, Liao H et al (2017) MicroRNA-155-3p mediates TNF-alpha-inhibited cementoblast differentiation. J Dent Res 96:1430–1437

    CAS  PubMed  Google Scholar 

  41. Mycko MP, Cichalewska M, Cwiklinska H et al (2015) miR-155-3p drives the development of autoimmune demyelination by regulation of heat shock protein 40. J Neurosci 35:16504–16515

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Shao N, Ma G, Zhang JY et al (2018) miR-221-5p enhances cell proliferation and metastasis through post-transcriptional regulation of SOCS1 in human prostate cancer. BMC Urol 18:14

    PubMed  PubMed Central  Google Scholar 

  43. Fang K, Sideri A, Law IKM et al (2015) Identification of a novel substance P-neurokinin-1 receptor microRNA-221-5p inflammatory network in human colonic epithelial cells. J Cell Mol Gastroenterol Hepatol 1:503–515

    Google Scholar 

  44. Xue L, Luo SY, Ding HY et al (2019) Upregulation of miR-146a-5p is associated with increased proliferation and migration of vascular smooth muscle cells in aortic dissection. J Clin Lab Anal 33:e22843

    PubMed  PubMed Central  Google Scholar 

  45. Fu L, Fu XY, Mo J et al (2019) miR-146a-5p enhances hepatitis B virus replication through autophagy to promote aggravation of chronic hepatitis B. IUBMB Life 71:1336–1346

    CAS  PubMed  Google Scholar 

  46. Huang Y, Wang QL, Cheng DD et al (2016) Adhesion and invasion of gastric mucosa epithelial cells by helicobacter pylori. Front Cell Infect Microbiol 6:159

    PubMed  PubMed Central  Google Scholar 

  47. Chakroun I, Cordero H, Mahdhi A et al (2017) Adhesion, invasion, cytotoxic effect and cytokine production in response to atypical Salmonella Typhimurium infection. Microb Pathog 106:40–49

    CAS  PubMed  Google Scholar 

  48. Kurosawa M, Oda M, Domon H et al (2018) Streptococcus pyogenes CAMP factor promotes bacterial adhesion and invasion in pharyngeal epithelial cells without serum via PI3K/Akt signaling pathway. Microbes Infect 20:9–18

    CAS  PubMed  Google Scholar 

  49. Liu Y, Han JK, Zhou ZY et al (2019) Paeoniflorin protects pancreatic beta cells from STZ-induced damage through inhibition of the p38 MAPK and JNK signaling pathways. Eur J Pharmacol 853:18–24

    CAS  PubMed  Google Scholar 

  50. Deng Y, Liu B, Mao W et al (2019) Regulatory roles of PGE in LPS-induced tissue damage in bovine endometrial explants. Eur J Pharmacol 852:207–217

    CAS  PubMed  Google Scholar 

  51. Habes QLM, Linssen V, Nooijen S et al (2017) Markers of intestinal damage and their relation to cytokine levels in cardiac surgery patients. Shock 47:709–714

    CAS  PubMed  Google Scholar 

  52. Martin-Alonso A, Cohen A, Quispe-Ricalde MA et al (2018) Differentially expressed microRNAs in experimental cerebral malaria and their involvement in endocytosis, adherens junctions, FoxO and TGF-beta signalling pathways. Sci Rep 8:11277

    PubMed  PubMed Central  Google Scholar 

  53. Pirro M, Bianconi V, Paciullo F et al (2017) Lipoprotein(a) and inflammation: a dangerous duet leading to endothelial loss of integrity. Pharmacol Res 119:178–187

    CAS  PubMed  Google Scholar 

  54. Al-Obaidi MMJ, Desa MNM (2018) Mechanisms of blood brain barrier disruption by different types of bacteria, and bacterial-host interactions facilitate the bacterial pathogen invading the brain. Cell Mol Neurobiol 38:1349–1368

    CAS  PubMed  Google Scholar 

  55. Sato H, Coburn J, Wunder E (2017) Leptospira interrogans causes quantitative and morphological disturbances in adherens junctions and other biological groups of proteins in human endothelial cells. PLoS Negl Trop Dis 11:e0005830

    PubMed  PubMed Central  Google Scholar 

  56. Wang XF, Gao L, Xiao LL et al (2019) 12(S)-hydroxyeicosatetraenoic acid impairs vascular endothelial permeability by altering adherens junction phosphorylation levels and affecting the binding and dissociation of its components in high glucose-induced vascular injury. J Diabetes Investig 10:639–649

    CAS  PubMed  Google Scholar 

  57. Xia J, Zhang HW, Gao XP et al (2016) E-cadherin-mediated contact of endothelial progenitor cells with mesenchymal stem cells through beta-catenin signaling. Cell Biol Int 40:407–418

    CAS  PubMed  Google Scholar 

  58. Li ZD, Pearlman AH, Hsieh P (2016) DNA mismatch repair and the DNA damage response. DNA Repair (Amst) 38:94–101

    Google Scholar 

  59. Fransen M, Lismont C, Walton P (2017) The peroxisome-mitochondria connection: How and why? Int J Mol Sci 18:1126

    PubMed Central  Google Scholar 

  60. Fu SL, Xu L, Li SL et al (2016) Baicalin suppresses NLRP3 inflammasome and nuclear factor-kappa B (NF-kappaB) signaling during Haemophilus parasuis infection. Vet Res 47:80

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 31572572, 31601922).

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Author notes

  1. Shulin Fu, Jun Liu and Jianfeng Xu have contributed equally to the work.

Authors and Affiliations

  1. Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University, Wuhan, 430023, People’s Republic of China

    Shulin Fu, Jun Liu, Jianfeng Xu, Sanling Zuo, Yunfei Zhang, Ling Guo, Yinsheng Qiu, Chun Ye, Yu Liu, Zhongyuan Wu, Yongqing Hou & Chien-An Andy Hu

  2. Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Wuhan, 430023, People’s Republic of China

    Shulin Fu, Jun Liu, Jianfeng Xu, Sanling Zuo, Yunfei Zhang, Ling Guo, Yinsheng Qiu, Chun Ye, Yu Liu, Zhongyuan Wu & Yongqing Hou

  3. Biochemistry and Molecular Biology, University of New Mexico School of Medicine, Albuquerque, NM, 87131, USA

    Chien-An Andy Hu

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Contributions

Material preparation, data collection and analysis were performed by SF, JL, JX, YZ, LG, CY, YL, ZW, YH, and C-AAH. The first draft of the manuscript was written by SF and YQ. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yinsheng Qiu.

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Fu, S., Liu, J., Xu, J. et al. The effect of baicalin on microRNA expression profiles in porcine aortic vascular endothelial cells infected by Haemophilus parasuis. Mol Cell Biochem 472, 45–56 (2020). https://doi.org/10.1007/s11010-020-03782-y

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