Skip to main content

Advertisement

Log in

Genome-wide identification of chicken bursae of Fabricius miRNAs in response to very virulent infectious bursal disease virus

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Infectious bursal disease virus (IBDV) can cause a highly contagious immunosuppressive disease in young chickens. MicroRNAs (miRNAs) are crucial regulators of gene expression and are involved in the pathogenesis of IBDV infection. To investigate the roles of miRNA in chicken bursae of Fabricius in response to very virulent IBDV (vvIBDV) infection, RNA sequencing was performed to compare the small RNA libraries from uninfected and vvIBDV-infected group which was infected for 3 days. A total of 77 differentially expressed (DE) miRNAs were identified in BF, of which 42 DE miRNAs were upregulated and 35 DE miRNAs were downregulated. A gene ontology analysis showed that genes associated with cellular processes, cells, and binding were enriched. Moreover, pathway analyses suggested that apoptosis, T cell receptor signaling pathways, and chemokine signaling pathways may be activated following vvIBDV infection. In addition, we predicted the target genes of DE miRNAs and constructed an miRNA-mRNA regulatory network. In total, 189 pairs of miRNA-target genes were identified, comprising 67 DE miRNAs and 73 mRNAs. In this network, gga-miR-1684b-3p was identified with the highest fold change, as well as gga-miR-1788-3p and gga-miR-3530-5p showed a high degree of change. The above three miRNAs were considered to play vital roles in vvIBDV-host interactions. This study was the first to perform a comprehensive analysis of DE miRNAs in the bursa of Fabricius in response to vvIBDV infection, and it provided new insights into molecular mechanisms underlying vvIBDV infection and pathogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The raw data sets supporting the results of this article were available in the NCBI short reads archive and accession number is PRJNA635782. For information linking and citing, please refer to: https://www.ncbi.nlm.nih.gov/search/all/?term=PRJNA635782.

Abbreviations

vvIBDV:

Very virulent infectious bursal disease virus

BF:

Bursa of Fabricius

miRNA:

MicroRNA

TEM:

Transmission electron microscopy

DE:

Differentially expressed

PBS:

Phosphate-buffered saline

GO:

Gene ontology

KEGG:

Kyoto Encyclopedia of Genes and Genomes

References

  1. McFerran JB, McNulty MS, McKillop ER, Connor TJ, McCracken RM, Collins DS, Allan GM (1980) Isolation and serological studies with infectious bursal disease viruses from fowl, turkeys and ducks: demonstration of a second serotype. Avian Pathol 9(3):395–404

    Article  CAS  PubMed  Google Scholar 

  2. Ismail NM, Saif YM, Moorhead PD (1988) Lack of pathogenicity of five serotype 2 infectious bursal disease viruses in chickens. Avian Dis 32(4):757–759

    Article  CAS  PubMed  Google Scholar 

  3. Brandt M, Yao K, Liu M, Heckert RA, Vakharia VN (2001) Molecular determinants of virulence, cell tropism, and pathogenic phenotype of infectious bursal disease virus. J Virol 75(24):11974–11982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ruby T, Whittaker C, Withers DR, Chelbi-Alix MK, Morin V, Oudin A, Young JR, Zoorob R (2006) Transcriptional profiling reveals a possible role for the timing of the inflammatory response in determining susceptibility to a viral infection. J Virol 80(18):9207–9216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Becht H, Müller H (1991) Infectious bursal disease–B cell dependent immunodeficiency syndrome in chickens. Behring Inst Mitt 89:217–225

    Google Scholar 

  6. Huang X, Liu W, Zhang J, Liu Z, Wang M, Wang L, Zhou H, Jiang Y, Cui W, Qiao X et al (2021) Very virulent infectious bursal disease virus-induced immune injury is involved in inflammation, apoptosis, and inflammatory cytokines imbalance in the bursa of fabricius. Dev Comp Immunol 114:103839

    Article  CAS  PubMed  Google Scholar 

  7. Cardin SE, Borchert GM (2017) Viral MicroRNAs, host MicroRNAs regulating viruses, and bacterial MicroRNA-like RNAs. Methods Mol Biol (Clifton, NJ) 1617:39–56

    Article  CAS  Google Scholar 

  8. Gao L, Gao J, Liang Y, Li R, Xiao Q, Zhang Z, Fan X (2019) Integration analysis of a miRNA-mRNA expression in A549 cells infected with a novel H3N2 swine influenza virus and the 2009 H1N1 pandemic influenza virus. Infect Genet Evol 74:103922

    Article  CAS  PubMed  Google Scholar 

  9. Monsanto-Hearne V, Johnson KN (2018) miRNAs in Insects Infected by Animal and Plant Viruses. Viruses 10(7):354

    Article  PubMed Central  CAS  Google Scholar 

  10. Gao J, Gao L, Li R, Lai Z, Zhang Z, Fan X (2019) Integrated analysis of microRNA-mRNA expression in A549 cells infected with influenza A viruses (IAVs) from different host species. Virus Res 263:34–46

    Article  CAS  PubMed  Google Scholar 

  11. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S et al (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956):415–419

    Article  CAS  PubMed  Google Scholar 

  12. Ohtani K, Dimmeler S (2010) Control of cardiovascular differentiation by microRNAs. Basic Res Cardiol 106(1):5–11

    Article  PubMed  CAS  Google Scholar 

  13. O’Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA 104(5):1604–1609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are MicroRNA. Targets 120(1):1–15

    Google Scholar 

  15. Dong BS, Shi MJ, Su SB, Zhang H (2019) Insight into long noncoding competing endogenous RNA networks in hepatic fibrosis: the potential implications for mechanism and therapy. Gene 687:255–260

    Article  CAS  PubMed  Google Scholar 

  16. Zhang J, Cui J, Wang Y, Lin X, Teng X, Tang Y (2022) Complex molecular mechanism of ammonia-induced apoptosis in chicken peripheral blood lymphocytes: miR-27b-3p, heat shock proteins, immunosuppression, death receptor pathway, and mitochondrial pathway. Ecotoxicol Environ Saf 236:113471

    Article  CAS  PubMed  Google Scholar 

  17. Han Q, Tong J, Sun Q, Teng X, Zhang H, Teng X (2020) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Chen J, Zhang S, Tong J, Teng X, Zhang Z, Li S, Teng X (2020) Whole transcriptome-based miRNA-mRNA network analysis revealed the mechanism of inflammation-immunosuppressive damage caused by cadmium in common carp spleens. Sci Total Environ 717:137081

    Article  CAS  PubMed  Google Scholar 

  19. Ji J, Xu X, Wang X, Yao L, Shang H, Li H, Ma J, Bi Y, Xie Q (2019) Expression of dysregulated miRNA in vivo in DF-1 cells during the course of subgroup J avian leukosis virus infection. Microb Pathog 126:40–44

    Article  CAS  PubMed  Google Scholar 

  20. Wang X, Jia Y, Ren J, Liu H, Xiao S, Wang X, Yang Z (2019) MicroRNA gga-miR-455-5p suppresses Newcastle disease virus replication via targeting cellular suppressors of cytokine signaling 3. Vet Microbiol 239:108460

    Article  CAS  PubMed  Google Scholar 

  21. Liu H, Yang X, Zhang ZK, Zou WC, Wang HN (2018) miR-146a-5p promotes replication of infectious bronchitis virus by targeting IRAK2 and TNFRSF18. Microb Pathog 120:32–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Wu X, Jia R, Zhou J, Wang M, Chen S, Liu M, Zhu D, Zhao X, Sun K, Yang Q et al (2018) Virulent duck enteritis virus infected DEF cells generate a unique pattern of viral microRNAs and a novel set of host microRNAs. BMC Vet Res 14(1):144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Li Y, Chan EY, Li J, Ni C, Peng X, Rosenzweig E, Tumpey TM, Katze MG (2010) MicroRNA expression and virulence in pandemic influenza virus-infected mice. J Virol 84(6):3023–3032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li J, Zheng SJ (2020) Role of MicroRNAs in host defense against infectious bursal disease virus (IBDV) infection: a hidden front line. Viruses 12(5):543

    Article  CAS  PubMed Central  Google Scholar 

  25. Zhou L, Zheng SJ (2019) The roles of MicroRNAs (miRNAs) in avian response to viral infection and pathogenesis of avian immunosuppressive diseases. Int J Mol Sci 20(21):5454

    Article  CAS  PubMed Central  Google Scholar 

  26. Fu M, Wang B, Chen X, He Z, Wang Y, Li X, Cao H, Zheng SJ (2018) MicroRNA gga-miR-130b suppresses infectious bursal disease virus replication via targeting of the viral genome and cellular suppressors of cytokine signaling 5. J Virol. https://doi.org/10.1128/JVI.01646-17

    Article  PubMed  PubMed Central  Google Scholar 

  27. Wang B, Fu M, Liu Y, Wang Y, Li X, Cao H, Zheng SJ (2018) gga-miR-155 enhances type I interferon expression and suppresses infectious burse disease virus replication via targeting SOCS1 and TANK. Front Cell Infect Microbiol 8:55

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Huang X, Zhang J, Liu Z, Wang M, Fan X, Wang L, Zhou H, Jiang Y, Cui W, Qiao X et al (2020) Genome-wide analysis of differentially expressed mRNAs, lncRNAs, and circRNAs in chicken bursae of Fabricius during infection with very virulent infectious bursal disease virus. BMC Genomics 21(1):724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Han Q, Zhang J, Sun Q, Xu Y, Teng X (2020) Oxidative stress and mitochondrial dysfunction involved in ammonia-induced nephrocyte necroptosis in chickens. Ecotoxicol Environ Saf 203:110974

    Article  CAS  PubMed  Google Scholar 

  30. Xu Z, Chen J, Li X, Ge J, Pan J, Xu X (2013) Identification and characterization of microRNAs in channel catfish (Ictalurus punctatus) by using Solexa sequencing technology. PLoS ONE 8(1):e54174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kruger J, Rehmsmeier M (2006) RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Rese 34:W451-454

    Article  CAS  Google Scholar 

  32. Agarwal V, Subtelny AO, Thiru P, Ulitsky I, Bartel DP (2018) Predicting microRNA targeting efficacy in Drosophila. Genome Biol 19(1):152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57

    Article  CAS  Google Scholar 

  35. Huang X, Xu Y, Lin Q, Guo W, Zhao D, Wang C, Wang L, Zhou H, Jiang Y, Cui W et al (2020) Determination of antiviral action of long non-coding RNA loc107051710 during infectious bursal disease virus infection due to enhancement of interferon production. Virulence 11(1):68–79

    Article  PubMed  CAS  Google Scholar 

  36. Miao Z, Zhang K, Bao R, Li J, Tang Y, Teng X (2021) Th1/Th2 imbalance and heat shock protein mediated inflammatory damage triggered by manganese via activating NF-κB pathway in chicken nervous system in vivo and in vitro. Environ Sci Pollut Res Int 28(32):44361–44373

    Article  CAS  PubMed  Google Scholar 

  37. Chen J, Xu Y, Han Q, Yao Y, Xing H, Teng X (2019) Immunosuppression, oxidative stress, and glycometabolism disorder caused by cadmium in common carp (Cyprinus carpio L.): Application of transcriptome analysis in risk assessment of environmental contaminant cadmium. J Hazard Mater 366:386–394

    Article  CAS  PubMed  Google Scholar 

  38. Bartel DP (2018) Metazoan MicroRNAs. Cell 173(1):20–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Müller H, Islam MR, Raue R (2003) Research on infectious bursal disease–the past, the present and the future. Vet Microbiol 97(1–2):153–165

    Article  PubMed  Google Scholar 

  40. Sharma JM, Kim IJ, Rautenschlein S, Yeh HY (2000) Infectious bursal disease virus of chickens: pathogenesis and immunosuppression. Dev Comp Immunol 24(2–3):223–235

    Article  CAS  PubMed  Google Scholar 

  41. Yang X, Gao W, Liu H, Li J, Chen D, Yuan F, Zhang Z, Wang H (2017) MicroRNA transcriptome analysis in chicken kidneys in response to differing virulent infectious bronchitis virus infections. Adv Virol 162(11):3397–3405

    CAS  Google Scholar 

  42. Zhu W, Yang M, Shang J, Xu Y, Wang Y, Tao Q, Zhang L, Ding Y, Chen Y, Zhao D et al (2019) MiR-222 inhibits apoptosis in porcine follicular granulosa cells by targeting the THBS1 gene. Animal Sci J 90(6):719–727

    Article  CAS  Google Scholar 

  43. Zhang X, Shan P, Alam J, Fu XY, Lee PJ (2005) Carbon monoxide differentially modulates STAT1 and STAT3 and inhibits apoptosis via a phosphatidylinositol 3-kinase/Akt and p38 kinase-dependent STAT3 pathway during anoxia-reoxygenation injury. J Biol Chem 280(10):8714–8721

    Article  CAS  PubMed  Google Scholar 

  44. Meraz MA, White JM, Sheehan KC, Bach EA, Rodig SJ, Dighe AS, Kaplan DH, Riley JK, Greenlund AC, Campbell D et al (1996) Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84(3):431–442

    Article  CAS  PubMed  Google Scholar 

  45. Durbin JE, Hackenmiller R, Simon MC, Levy DE (1996) Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84(3):443–450

    Article  CAS  PubMed  Google Scholar 

  46. Guo L, Luo X, Li R, Xu Y, Zhang J, Ge J, Bu Z, Feng L, Wang Y (2016) Porcine epidemic diarrhea virus infection inhibits interferon signaling by targeted degradation of STAT1. J Virol 90(18):8281–8292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank the Harbin Institute of Veterinary Medicine for supplying us the specific pathogen-free chickens and Novel Bioinformatics Ltd., Co for the support of bioinformatics analysis. We also thank GENE DENOVO for the support of uploading the sequencing data.

Funding

This work is supported by the National Science and Technology Support Program in Rural Areas of the12th Five-Year Plan [Grant 2015BAD12B01].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lijie Tang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

Animal experiments were carried out in accordance with the recommendations in the institutional and national guidelines for animal were and use. The protocol was approved by the Committee on the Ethics of Animal Experiments of Northeast Agricultural University, Harbin, China (2016NEFU-315, 13 April 2017).

Additional information

Handling Editor: Ana Cristina Bratanich.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, X., Li, Y., Wang, X. et al. Genome-wide identification of chicken bursae of Fabricius miRNAs in response to very virulent infectious bursal disease virus. Arch Virol 167, 1855–1864 (2022). https://doi.org/10.1007/s00705-022-05496-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-022-05496-6

Navigation