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Acute transcriptomic changes in murine RAW 264.7 cells following pseudorabies virus infection

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Abstract

Next-generation sequencing enables the evaluation of gene expression changes resulting from virus–host interactions at the RNA level. Pseudorabies virus (PRV) causes substantial economic loss in the swine industry. Recent research has revealed that PRV can be transmitted to and infect humans as well. To identify physiopathological and pathological responses post-PRV infection, we characterized transcriptomic changes in the murine RAW 264.7 cell line over the course of 36 h. In total, 156, 153, and 190 differentially expressed genes were identified at 2 h, 12 h, and 36 h, respectively. Seven differentially expressed genes (Trim27, Ccdc117, Mrps12, Ccl4, Cerkl, Ubald1, and Hmga1-rs1) were present across all treatment groups. Our findings expand our knowledge of gene regulation and immune response following PRV infection. These differentially expressed genes can subsequently improve our understanding of PRV pathogenesis.

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Data availability

The sequence data of this study have been deposited in the Sequence Read Archive (http://www.ncbi.nlm.nih.gov/sra, accession number PRJNA689234). All datasets generated in this study are included in the article/Supplementary Material.

References

  1. Verpoest S, Cay B, Favoreel H, De Regge N (2017) Age-Dependent Differences in Pseudorabies Virus Neuropathogenesis and Associated Cytokine Expression. J Virol 91. https://doi.org/10.1128/JVI.02058-16

  2. Sehl J, Teifke JP (2020) Comparative Pathology of Pseudorabies in Different Naturally and Experimentally Infected Species-A Review. Pathogens 9. https://doi.org/10.3390/pathogens9080633

    Article  Google Scholar 

  3. Milicevic V, Radojicic S, Valcic M, Ivovic V, Radosavljevic V (2016) Evidence of Aujeszky’s disease in wild boar in Serbia. BMC Vet Res 12:134. https://doi.org/10.1186/s12917-016-0758-9

    Article  CAS  Google Scholar 

  4. Thawley DG, Wright JC (1982) Pseudorabies virus infection in raccoons: a review. J Wildl Dis 18:113–116. https://doi.org/10.7589/0090-3558-18.1.113

    Article  CAS  Google Scholar 

  5. Banks M, Torraca LS, Greenwood AG, Taylor DC (1999) Aujeszky’s disease in captive bears. Vet Rec 145:362–365. https://doi.org/10.1136/vr.145.13.362

    Article  CAS  Google Scholar 

  6. Glass CM, McLean RG, Katz JB, Maehr DS, Cropp CB, Kirk LJ, McKeirnan AJ, Evermann JF (1994) Isolation of pseudorabies (Aujeszky’s disease) virus from a Florida panther. J Wildl Dis 30:180–184. https://doi.org/10.7589/0090-3558-30.2.180

    Article  CAS  Google Scholar 

  7. Wang GS, Du Y, Wu JQ, Tian FL, Yu XJ, Wang JB (2018) Vaccine resistant pseudorabies virus causes mink infection in China. BMC Vet Res 14:20. https://doi.org/10.1186/s12917-018-1334-2

    Article  CAS  Google Scholar 

  8. Skinner GRB, Ahmad A, Davies JA (2001) The infrequency of transmission of herpesviruses between humans and animals; postulation of an unrecognised protective host mechanism. Comp Immunol Microbiol Infect Dis 24:255–269. https://doi.org/10.1016/S0147-9571(01)00014-5

    Article  CAS  Google Scholar 

  9. Ai JW, Weng SS, Cheng Q, Cui P, Li YJ, Wu HL, Zhu YM, Xu B, Zhang WH (2018) Human Endophthalmitis Caused By Pseudorabies Virus Infection, China, 2017. Emerg Infect Dis 24:1087–1090. https://doi.org/10.3201/eid2406.171612

    Article  Google Scholar 

  10. Guo Z, Chen XX, Zhang G (2021) Human PRV Infection in China: An Alarm to Accelerate Eradication of PRV in Domestic Pigs. Virol Sin 36:823–828. https://doi.org/10.1007/s12250-021-00347-1

    Article  Google Scholar 

  11. Wang D, Tao X, Fei M, Chen J, Guo W, Li P, Wang J (2020) Human encephalitis caused by pseudorabies virus infection: a case report. J Neurovirol 26:442–448. https://doi.org/10.1007/s13365-019-00822-2

    Article  CAS  Google Scholar 

  12. Yang H, Han H, Wang H, Cui Y, Liu H, Ding S (2019) A Case of Human Viral Encephalitis Caused by Pseudorabies Virus Infection in China. Front Neurol 10:534. https://doi.org/10.3389/fneur.2019.00534

    Article  Google Scholar 

  13. Yang X, Guan H, Li C, Li Y, Wang S, Zhao X, Zhao Y, Liu Y (2019) Characteristics of human encephalitis caused by pseudorabies virus: A case series study. Int J Infect Dis 87:92–99. https://doi.org/10.1016/j.ijid.2019.08.007

    Article  CAS  Google Scholar 

  14. Liu Q, Wang X, Xie C, Ding S, Yang H, Guo S, Li J, Qin L, Ban F, Wang D, Wang C, Feng L, Ma H, Wu B, Zhang L, Dong C, Xing L, Zhang J, Chen H, Yan R, Wang X, Li W (2020) A novel human acute encephalitis caused by pseudorabies virus variant strain. Clin Infect Dis. https://doi.org/10.1093/cid/ciaa987

    Article  Google Scholar 

  15. Ren Y, Khan FA, Pandupuspitasari NS, Zhang S (2017) Immune Evasion Strategies of Pathogens in Macrophages: the Potential for Limiting Pathogen Transmission. Curr Issues Mol Biol 21:21–40. https://doi.org/10.21775/cimb.021.021

    Article  Google Scholar 

  16. Nikitina E, Larionova I, Choinzonov E, Kzhyshkowska J (2018) Monocytes and Macrophages as Viral Targets and Reservoirs. Int J Mol Sci 19. https://doi.org/10.3390/ijms19092821

    Article  Google Scholar 

  17. Iglesias G, Pijoan C, Molitor T (1989) Interactions of pseudorabies virus with swine alveolar macrophages: effects of virus infection on cell functions. J Leukoc biol 45:410. https://doi.org/10.1002/hon.2900070307

    Article  CAS  Google Scholar 

  18. Lin HW, Chang TJ, Yang DJ, Chen YC, Wang ML, Chang YY (2012) Regulation of virus-induced inflammatory response by beta-carotene in RAW264.7 cells. Food Chem 134:2169–2175. https://doi.org/10.1016/j.foodchem.2012.04.024

    Article  CAS  Google Scholar 

  19. Flori L, Rogel-Gaillard C, Cochet M, Lemonnier G, Hugot K, Chardon P, Robin S, Lefevre F (2008) Transcriptomic analysis of the dialogue between Pseudorabies virus and porcine epithelial cells during infection. BMC Genomics 9. https://doi.org/10.1186/1471-2164-9-123

    Article  Google Scholar 

  20. Wang J, Lu SF, Wan B, Ming SL, Li GL, Su BQ, Liu JY, Wei YS, Yang GY, Chu BB (2018) Maintenance of cyclic GMP-AMP homeostasis by ENPP1 is involved in pseudorabies virus infection. Mol Immunol 95:56–63. https://doi.org/10.1016/j.molimm.2018.01.008

    Article  CAS  Google Scholar 

  21. Wang J, Wang CF, Ming SL, Li GL, Zeng L, Wang MD, Su BQ, Wang Q, Yang GY, Chu BB (2020) Porcine IFITM1 is a host restriction factor that inhibits pseudorabies virus infection. Int J Biol Macromol 151:1181–1193. https://doi.org/10.1016/j.ijbiomac.2019.10.162

    Article  CAS  Google Scholar 

  22. Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat protoc. 11:1650–1667. https://doi.org/10.1038/nprot.2016.095

  23. Mogensen TH, Paludan SR (2001) Molecular pathways in virus-induced cytokine production. Microbiol Mol Biol Rev 65:131–150. https://doi.org/10.1128/MMBR.65.1.131-150.2001

    Article  CAS  Google Scholar 

  24. Bystry RS, Aluvihare V, Welch KA, Kallikourdis M, Betz AG (2001) B cells and professional APCs recruit regulatory T cells via CCL4. Nat Immunol 2:1126–1132. https://doi.org/10.1038/ni735

    Article  CAS  Google Scholar 

  25. Al-Afif A, Alyazidi R, Oldford SA, Huang YY, King CA, Marr N, Haidl ID, Anderson R, Marshall JS (2015) Respiratory syncytial virus infection of primary human mast cells induces the selective production of type I interferons, CXCL10, and CCL4. J Allergy Clin Immun 136:1346. https://doi.org/10.1016/j.jaci.2015.01.042

    Article  CAS  Google Scholar 

  26. Ramirez-Martinez G, Cruz-Lagunas A, Jimenez-Alvarez L, Espinosa E, Ortiz-Quintero B, Santos-Mendoza T, Herrera MT, Canche-Pool E, Mendoza C, Banales JL, Garcia-Moreno SA, Moran J, Cabello C, Orozco L, Aguilar-Delfin I, Hidalgo-Miranda A, Romero S, Suratt BT, Selman M, Zuniga J (2013) Seasonal and pandemic influenza H1N1 viruses induce differential expression of SOCS-1 and RIG-I genes and cytokine/chemokine production in macrophages. Cytokine 62, 151–159. https://doi.org/0.1016/j.cyto.2013.01.018

  27. Kramer T, Enquist LW (2012) Alphaherpesvirus Infection Disrupts Mitochondrial Transport in Neurons. Cell Host Microbe 11:504–514. https://doi.org/10.1016/j.chom.2012.03.005

    Article  CAS  Google Scholar 

  28. Huang T, Xu ZP, Chen L, Cai YD, Kong XY (2011) Computational Analysis of HIV-1 Resistance Based on Gene Expression Profiles and the Virus-Host Interaction Network. https://doi.org/10.1371/journal.pone.0017291. Plos One 6

  29. Curty G, Beckerle GA, Iniguez LP, Furler RL, de Carvalho PS, Marston JL, Champiat S, Heymann JJ, Ormsby CE, Reyes-Teran G, Soares MA, Nixon DF, Bendall ML, Leal FE, Rougvie MD (2020) Human Endogenous Retrovirus Expression Is Upregulated in the Breast Cancer Microenvironment of HIV Infected Women: A Pilot Study. Front Oncol 10. https://doi.org/10.3389/fonc.2020.553983

    Article  Google Scholar 

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Acknowledgements

The authors would like to acknowledge Fang Liu for her outstanding help with data analysis.

Funding

This work was supported by grants from the Natural Science Foundation of Henan Province (202300410213).

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Authors

Contributions

Chao Tong, He-Shui Zhu and Jiang Wang designed the study, drafted the manuscript, and revised the manuscript. Peng-Fei Fu and Sheng-Li Ming collected the samples and performed the experiments. Peng-Fei Fu, Lei Zeng, and He-Shui Zhu analyzed the data. All authors read and approved of the final version of the manuscript that was submitted for publication.

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Correspondence to He-Shui Zhu or Jiang Wang.

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The authors have no relevant financial or non-financial interests to disclose.

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No animal work was performed for this study.

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Handling Editor: Zhongjie Shi

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Chao Tong and Peng-Fei Fu authors contributed equally to this work.

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Tong, C., Fu, PF., Ming, SL. et al. Acute transcriptomic changes in murine RAW 264.7 cells following pseudorabies virus infection. Arch Virol 167, 2623–2631 (2022). https://doi.org/10.1007/s00705-022-05598-1

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  • DOI: https://doi.org/10.1007/s00705-022-05598-1

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