Transcriptomic Profiling of Equine and Viral Genes in Peripheral Blood Mononuclear Cells in Horses during Equine Herpesvirus 1 Infection.
- Journal Article
Summary
This research investigates the changes in both horse and virus gene expression in peripheral blood mononuclear cells (PBMCs) during an infection of equine herpesvirus 1 (EHV-1), which can lead to various diseases in horses. The researchers performed RNA sequencing and found significant changes in gene expression during peak infection compared to pre-infection stages, which might indicate how the virus is transported and how it causes illness.
Objective of Research
The research focused on understanding the impact of EHV-1 virus infection in horses. It aimed to explore the changes in gene expression in PBMCs, which are vital in the infection and disease manifestation process. By leveraging RNA sequencing, the study was intent to identify differentially expressed genes during the peak infection stage and contrast it with the pre-infection state.
Research Methodology and Findings
- The researchers utilized RNA sequencing to analyze the gene expression in PBMCs during EHV-1 infection.
- Through comparative analysis, they discovered 51 differentially expressed horse genes (48 upregulated and 3 downregulated) during peak viremia as opposed to pre-infection.
- Several biological processes such as the interferon defense response, response to chemokines, the complement protein activation cascade, cell adhesion, and coagulation were overrepresented during viremia, suggesting these functions play a significant role in viral infection progression.
- The study also identified presence of transcripts for EHV-1, EHV-2, and EHV-5 in both pre- and post-infection samples.
- The research identified 278 known equine miRNAs and 855 potentially novel equine miRNAs, plus 57 and 41 new miRNAs that may be associated with EHV-2 and EHV-5 genomes, respectively.
- Among these, 1 EHV-5 and 4 equine miRNAs showed differential expression in PBMCs during viremia.
Conclusions and Future Implication
- The findings are expected to enhance our understanding of how PBMCs influence EHV-1 viremia. They provide interesting insights about gene expression alterations during virus infection, which could be crucial in understanding the pathology of the disease.
- The identified differentially expressed genes might play crucial roles in viral transport and subsequent disease manifestation, necessitating further exploration for potential therapeutic interventions.
Cite This Article
Publication
Researcher Affiliations
- Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, MI 48824, USA.
- Department of Large Animal Clinical Sciences, Michigan State University, East Lansing, MI 48824, USA.
- Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, MI 48824, USA.
- Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, MI 48824, USA.
Grant Funding
- N/A / Michigan State University College of Veterinary Medicine's Endowed Research Fund and the Freeman Fund for Equine Research
- 2018-67015-28242 / National Institute of Food and Agriculture
Conflict of Interest Statement
References
- Pellett P, Roizman B. Herpesviridae. Fields Virology 2013 pp. 1803–1822.
- Oladunni FS, Horohov DW, Chambers TM. EHV-1: A Constant Threat to the Horse Industry.. Front Microbiol 2019;10:2668.
- Pusterla N, Mapes S, Wilson WD. Prevalence of equine herpesvirus type 1 in trigeminal ganglia and submandibular lymph nodes of equids examined postmortem.. Vet Rec 2010 Sep 4;167(10):376-8.
- Allen GP. Antemortem detection of latent infection with neuropathogenic strains of equine herpesvirus-1 in horses.. Am J Vet Res 2006 Aug;67(8):1401-5.
- Allen GP, Bolin DC, Bryant U, Carter CN, Giles RC, Harrison LR, Hong CB, Jackson CB, Poonacha K, Wharton R, Williams NM. Prevalence of latent, neuropathogenic equine herpesvirus-1 in the Thoroughbred broodmare population of central Kentucky.. Equine Vet J 2008 Mar;40(2):105-10.
- Slater JD, Borchers K, Thackray AM, Field HJ. The trigeminal ganglion is a location for equine herpesvirus 1 latency and reactivation in the horse.. J Gen Virol 1994 Aug;75 ( Pt 8):2007-16.
- Giessler KS, Samoilowa S, Soboll Hussey G, Kiupel M, Matiasek K, Sledge DG, Liesche F, Schlegel J, Fux R, Goehring LS. Viral Load and Cell Tropism During Early Latent Equid Herpesvirus 1 Infection Differ Over Time in Lymphoid and Neural Tissue Samples From Experimentally Infected Horses.. Front Vet Sci 2020;7:621.
- Marenzoni ML, Stefanetti V, Danzetta ML, Timoney PJ. Gammaherpesvirus infections in equids: a review.. Vet Med (Auckl) 2015;6:91-101.
- Lunn DP, Davis-Poynter N, Flaminio MJ, Horohov DW, Osterrieder K, Pusterla N, Townsend HG. Equine herpesvirus-1 consensus statement.. J Vet Intern Med 2009 May-Jun;23(3):450-61.
- van Maanen C. Equine herpesvirus 1 and 4 infections: an update.. Vet Q 2002 Jun;24(2):58-78.
- Gryspeerdt AC, Vandekerckhove AP, Garré B, Barbé F, Van de Walle GR, Nauwynck HJ. Differences in replication kinetics and cell tropism between neurovirulent and non-neurovirulent EHV1 strains during the acute phase of infection in horses.. Vet Microbiol 2010 May 19;142(3-4):242-53.
- Wilsterman S, Soboll-Hussey G, Lunn DP, Ashton LV, Callan RJ, Hussey SB, Rao S, Goehring LS. Equine herpesvirus-1 infected peripheral blood mononuclear cell subpopulations during viremia.. Vet Microbiol 2011 Apr 21;149(1-2):40-7.
- Goodman LB, Loregian A, Perkins GA, Nugent J, Buckles EL, Mercorelli B, Kydd JH, Palù G, Smith KC, Osterrieder N, Davis-Poynter N. A point mutation in a herpesvirus polymerase determines neuropathogenicity.. PLoS Pathog 2007 Nov;3(11):e160.
- Scott JC, Dutta SK, Myrup AC. In vivo harboring of equine herpesvirus-1 in leukocyte populations and subpopulations and their quantitation from experimentally infected ponies.. Am J Vet Res 1983 Jul;44(7):1344-8.
- van Der Meulen KM, Nauwynck HJ, Bí¶®rt W, Pensaert MB. Replication of equine herpesvirus type 1 in freshly isolated equine peripheral blood mononuclear cells and changes in susceptibility following mitogen stimulation.. J Gen Virol 2000 Jan;81(Pt 1):21-5.
- Laval K, Favoreel HW, Nauwynck HJ. Equine herpesvirus type 1 replication is delayed in CD172a+ monocytic cells and controlled by histone deacetylases.. J Gen Virol 2015 Jan;96(Pt 1):118-130.
- Laval K, Favoreel HW, Poelaert KC, Van Cleemput J, Nauwynck HJ. Equine Herpesvirus Type 1 Enhances Viral Replication in CD172a+ Monocytic Cells upon Adhesion to Endothelial Cells.. J Virol 2015 Nov;89(21):10912-23.
- Poelaert KCK, Van Cleemput J, Laval K, Favoreel HW, Couck L, Van den Broeck W, Azab W, Nauwynck HJ. Equine Herpesvirus 1 Bridles T Lymphocytes To Reach Its Target Organs.. J Virol 2019 Apr 1;93(7).
- Allen GP. Risk factors for development of neurologic disease after experimental exposure to equine herpesvirus-1 in horses.. Am J Vet Res 2008 Dec;69(12):1595-600.
- Soboll Hussey G, Hussey SB, Wagner B, Horohov DW, Van de Walle GR, Osterrieder N, Goehring LS, Rao S, Lunn DP. Evaluation of immune responses following infection of ponies with an EHV-1 ORF1/2 deletion mutant.. Vet Res 2011 Feb 7;42(1):23.
- Holz CL, Nelli RK, Wilson ME, Zarski LM, Azab W, Baumgardner R, Osterrieder N, Pease A, Zhang L, Hession S, Goehring LS, Hussey SB, Soboll Hussey G. Viral genes and cellular markers associated with neurological complications during herpesvirus infections.. J Gen Virol 2017 Jun;98(6):1439-1454.
- Wimer CL, Damiani A, Osterrieder N, Wagner B. Equine herpesvirus type-1 modulates CCL2, CCL3, CCL5, CXCL9, and CXCL10 chemokine expression.. Vet Immunol Immunopathol 2011 Apr 15;140(3-4):266-74.
- Wagner B, Wimer C, Freer H, Osterrieder N, Erb HN. Infection of peripheral blood mononuclear cells with neuropathogenic equine herpesvirus type-1 strain Ab4 reveals intact interferon-α induction and induces suppression of anti-inflammatory interleukin-10 responses in comparison to other viral strains.. Vet Immunol Immunopathol 2011 Sep 15;143(1-2):116-24.
- Shukla GC, Singh J, Barik S. MicroRNAs: Processing, Maturation, Target Recognition and Regulatory Functions.. Mol Cell Pharmacol 2011;3(3):83-92.
- Zheng SQ, Li YX, Zhang Y, Li X, Tang H. MiR-101 regulates HSV-1 replication by targeting ATP5B.. Antiviral Res 2011 Mar;89(3):219-26.
- Boss IW, Renne R. Viral miRNAs and immune evasion.. Biochim Biophys Acta 2011 Nov-Dec;1809(11-12):708-14.
- Zarski L.M., Seong K.K., Lee Y., Holz C.L., Nelli R.K., Weber P.S.D., Soboll Hussey G. Administration of recombinant adenovirus expressing inhibitory IR2 protein for control of equine herpesvirus 1 infection and disease. 2020 prepare.
- Newman AM, Steen CB, Liu CL, Gentles AJ, Chaudhuri AA, Scherer F, Khodadoust MS, Esfahani MS, Luca BA, Steiner D, Diehn M, Alizadeh AA. Determining cell type abundance and expression from bulk tissues with digital cytometry.. Nat Biotechnol 2019 Jul;37(7):773-782.
- Matsumura T, Kondo T, Sugita S, Damiani AM, O'Callaghan DJ, Imagawa H. An equine herpesvirus type 1 recombinant with a deletion in the gE and gI genes is avirulent in young horses.. Virology 1998 Mar 1;242(1):68-79.
- Shakya AK, O'Callaghan DJ, Kim SK. Comparative Genomic Sequencing and Pathogenic Properties of Equine Herpesvirus 1 KyA and RacL11.. Front Vet Sci 2017;4:211.
- Said A, Osterrieder N. Equine herpesvirus type 1 (EHV-1) open reading frame 59 encodes an early protein that is localized to the cytosol and required for efficient virus growth.. Virology 2014 Jan 20;449:263-9.
- Lischka P, Sorg G, Kann M, Winkler M, Stamminger T. A nonconventional nuclear localization signal within the UL84 protein of human cytomegalovirus mediates nuclear import via the importin alpha/beta pathway.. J Virol 2003 Mar;77(6):3734-48.
- Huang R, Hu Z, Cao Y, Li H, Zhang H, Su W, Xu Y, Liang L, Melgiri ND, Jiang L. MiR-652-3p inhibition enhances endothelial repair and reduces atherosclerosis by promoting Cyclin D2 expression.. EBioMedicine 2019 Feb;40:685-694.
- Poudyal D, Herman A, Adelsberger JW, Yang J, Hu X, Chen Q, Bosche M, Sherman BT, Imamichi T. A novel microRNA, hsa-miR-6852 differentially regulated by Interleukin-27 induces necrosis in cervical cancer cells by downregulating the FoxM1 expression.. Sci Rep 2018 Jan 17;8(1):900.
- Brosnahan MM, Al Abri MA, Brooks SA, Antczak DF, Osterrieder N. Genome-wide association study of equine herpesvirus type 1-induced myeloencephalopathy identifies a significant single nucleotide polymorphism in a platelet-related gene.. Vet J 2019 Mar;245:49-54.
- Rubinstein E. The complexity of tetraspanins.. Biochem Soc Trans 2011 Apr;39(2):501-5.
- Haining EJ, Matthews AL, Noy PJ, Romanska HM, Harris HJ, Pike J, Morowski M, Gavin RL, Yang J, Milhiet PE, Berditchevski F, Nieswandt B, Poulter NS, Watson SP, Tomlinson MG. Tetraspanin Tspan9 regulates platelet collagen receptor GPVI lateral diffusion and activation.. Platelets 2017 Nov;28(7):629-642.
- Mossman KL, Ashkar AA. Herpesviruses and the innate immune response.. Viral Immunol 2005;18(2):267-81.
- Ivashkiv LB, Donlin LT. Regulation of type I interferon responses.. Nat Rev Immunol 2014 Jan;14(1):36-49.
- Kumari P, Narayanan S, Kumar H. Herpesviruses: interfering innate immunity by targeting viral sensing and interferon pathways.. Rev Med Virol 2015 May;25(3):187-201.
- Dupuis S, Jouanguy E, Al-Hajjar S, Fieschi C, Al-Mohsen IZ, Al-Jumaah S, Yang K, Chapgier A, Eidenschenk C, Eid P, Al Ghonaium A, Tufenkeji H, Frayha H, Al-Gazlan S, Al-Rayes H, Schreiber RD, Gresser I, Casanova JL. Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency.. Nat Genet 2003 Mar;33(3):388-91.
- Bin L, Edwards MG, Heiser R, Streib JE, Richers B, Hall CF, Leung DY. Identification of novel gene signatures in patients with atopic dermatitis complicated by eczema herpeticum.. J Allergy Clin Immunol 2014 Oct;134(4):848-55.
- Soboll Hussey G, Ashton LV, Quintana AM, Lunn DP, Goehring LS, Annis K, Landolt G. Innate immune responses of airway epithelial cells to infection with equine herpesvirus-1.. Vet Microbiol 2014 May 14;170(1-2):28-38.
- Soboll Hussey G, Ashton LV, Quintana AM, Van de Walle GR, Osterrieder N, Lunn DP. Equine herpesvirus type 1 pUL56 modulates innate responses of airway epithelial cells.. Virology 2014 Sep;464-465:76-86.
- Quintana AM, Landolt GA, Annis KM, Hussey GS. Immunological characterization of the equine airway epithelium and of a primary equine airway epithelial cell culture model.. Vet Immunol Immunopathol 2011 Apr 15;140(3-4):226-36.
- Poelaert KCK, Van Cleemput J, Laval K, Favoreel HW, Soboll Hussey G, Maes RK, Nauwynck HJ. Abortigenic but Not Neurotropic Equine Herpes Virus 1 Modulates the Interferon Antiviral Defense.. Front Cell Infect Microbiol 2018;8:312.
- Oladunni FS, Sarkar S, Reedy S, Balasuriya UBR, Horohov DW, Chambers TM. Equid Herpesvirus 1 Targets the Sensitization and Induction Steps To Inhibit the Type I Interferon Response in Equine Endothelial Cells.. J Virol 2019 Dec 1;93(23).
- Sarkar S, Balasuriya UB, Horohov DW, Chambers TM. Equine herpesvirus-1 suppresses type-I interferon induction in equine endothelial cells.. Vet Immunol Immunopathol 2015 Oct 15;167(3-4):122-9.
- Scherer CA, Magness CL, Steiger KV, Poitinger ND, Caputo CM, Miner DG, Winokur PL, Klinzman D, McKee J, Pilar C, Ward PA, Gillham MH, Haulman NJ, Stapleton JT, Iadonato SP. Distinct gene expression profiles in peripheral blood mononuclear cells from patients infected with vaccinia virus, yellow fever 17D virus, or upper respiratory infections.. Vaccine 2007 Aug 29;25(35):6458-73.
- Schmid S, Mordstein M, Kochs G, García-Sastre A, Tenoever BR. Transcription factor redundancy ensures induction of the antiviral state.. J Biol Chem 2010 Dec 31;285(53):42013-22.
- Groom JR, Luster AD. CXCR3 ligands: redundant, collaborative and antagonistic functions.. Immunol Cell Biol 2011 Feb;89(2):207-15.
- Poelaert KCK, Van Cleemput J, Laval K, Xie J, Favoreel HW, Nauwynck HJ. Equine herpesvirus 1 infection orchestrates the expression of chemokines in equine respiratory epithelial cells.. J Gen Virol 2019 Nov;100(11):1567-1579.
- Johnstone S, Barsova J, Campos I, Frampton AR. Equine herpesvirus type 1 modulates inflammatory host immune response genes in equine endothelial cells.. Vet Microbiol 2016 Aug 30;192:52-59.
- Proost P, Wuyts A, Van Damme J. Human monocyte chemotactic proteins-2 and -3: structural and functional comparison with MCP-1.. J Leukoc Biol 1996 Jan;59(1):67-74.
- Sun Y, Iglesias E, Samri A, Kamkamidze G, Decoville T, Carcelain G, Autran B. A systematic comparison of methods to measure HIV-1 specific CD8 T cells.. J Immunol Methods 2003 Jan 15;272(1-2):23-34.
- Guidotti LG, Chisari FV. Noncytolytic control of viral infections by the innate and adaptive immune response.. Annu Rev Immunol 2001;19:65-91.
- O'Neill T, Kydd JH, Allen GP, Wattrang E, Mumford JA, Hannant D. Determination of equid herpesvirus 1-specific, CD8+, cytotoxic T lymphocyte precursor frequencies in ponies.. Vet Immunol Immunopathol 1999 Sep 1;70(1-2):43-54.
- Kydd JH, Wattrang E, Hannant D. Pre-infection frequencies of equine herpesvirus-1 specific, cytotoxic T lymphocytes correlate with protection against abortion following experimental infection of pregnant mares.. Vet Immunol Immunopathol 2003 Dec 15;96(3-4):207-17.
- Paillot R, Ellis SA, Daly JM, Audonnet JC, Minke JM, Davis-Poynter N, Hannant D, Kydd JH. Characterisation of CTL and IFN-gamma synthesis in ponies following vaccination with a NYVAC-based construct coding for EHV-1 immediate early gene, followed by challenge infection.. Vaccine 2006 Mar 6;24(10):1490-500.
- Paillot R, Daly JM, Luce R, Montesso F, Davis-Poynter N, Hannant D, Kydd JH. Frequency and phenotype of EHV-1 specific, IFN-gamma synthesising lymphocytes in ponies: the effects of age, pregnancy and infection.. Dev Comp Immunol 2007;31(2):202-14.
- Breathnach CC, Soboll G, Suresh M, Lunn DP. Equine herpesvirus-1 infection induces IFN-gamma production by equine T lymphocyte subsets.. Vet Immunol Immunopathol 2005 Feb 10;103(3-4):207-15.
- Favoreel HW, Nauwynck HJ, Pensaert MB. Immunological hiding of herpesvirus-infected cells.. Arch Virol 2000;145(7):1269-90.
- van der Meulen KM, Nauwynck HJ, Pensaert MB. Absence of viral antigens on the surface of equine herpesvirus-1-infected peripheral blood mononuclear cells: a strategy to avoid complement-mediated lysis.. J Gen Virol 2003 Jan;84(Pt 1):93-97.
- Carroll MC. The complement system in B cell regulation.. Mol Immunol 2004 Jun;41(2-3):141-6.
- Wagner C, Hänsch GM. Receptors for complement C3 on T-lymphocytes: relics of evolution or functional molecules?. Mol Immunol 2006 Jan;43(1-2):22-30.
- Wagner C, Ochmann C, Schoels M, Giese T, Stegmaier S, Richter R, Hug F, Hänsch GM. The complement receptor 1, CR1 (CD35), mediates inhibitory signals in human T-lymphocytes.. Mol Immunol 2006 Feb;43(6):643-51.
- Wilson JG, Tedder TF, Fearon DT. Characterization of human T lymphocytes that express the C3b receptor.. J Immunol 1983 Aug;131(2):684-9.
- Werfel T, Kirchhoff K, Wittmann M, Begemann G, Kapp A, Heidenreich F, Götze O, Zwirner J. Activated human T lymphocytes express a functional C3a receptor.. J Immunol 2000 Dec 1;165(11):6599-605.
- Oikonomopoulou K, Ricklin D, Ward PA, Lambris JD. Interactions between coagulation and complement--their role in inflammation.. Semin Immunopathol 2012 Jan;34(1):151-65.
- Davis AE 3rd. Biological effects of C1 inhibitor.. Drug News Perspect 2004 Sep;17(7):439-46.
- Yeo WM, Osterrieder N, Stokol T. Equine herpesvirus type 1 infection induces procoagulant activity in equine monocytes.. Vet Res 2013 Mar 11;44(1):16.
- Stokol T, Yeo WM, Burnett D, DeAngelis N, Huang T, Osterrieder N, Catalfamo J. Equid herpesvirus type 1 activates platelets.. PLoS One 2015;10(4):e0122640.
- Goehring LS, Soboll Hussey G, Gomez Diez M, Benedict K, Maxwell LK, Morley PS, Sloet van Oldruitenborgh-Oosterbaan MM, Lunn DP. Plasma D-dimer concentrations during experimental EHV-1 infection of horses.. J Vet Intern Med 2013 Nov-Dec;27(6):1535-42.
- Wilson ME, Holz CL, Kopec AK, Dau JJ, Luyendyk JP, Soboll Hussey G. Coagulation parameters following equine herpesvirus type 1 infection in horses.. Equine Vet J 2019 Jan;51(1):102-107.
- Adams RL, Bird RJ. Review article: Coagulation cascade and therapeutics update: relevance to nephrology. Part 1: Overview of coagulation, thrombophilias and history of anticoagulants.. Nephrology (Carlton) 2009 Aug;14(5):462-70.
- Sang Y, Miller LC, Blecha F. Macrophage Polarization in Virus-Host Interactions.. J Clin Cell Immunol 2015 Apr;6(2).
- Sutton CE, Mielke LA, Mills KH. IL-17-producing γδ T cells and innate lymphoid cells.. Eur J Immunol 2012 Sep;42(9):2221-31.
- van der Meulen K, Caij B, Pensaert M, Nauwynck H. Absence of viral envelope proteins in equine herpesvirus 1-infected blood mononuclear cells during cell-associated viremia.. Vet Microbiol 2006 Mar 31;113(3-4):265-73.
- Lunn DP, Holmes MA, Gibson J, Field HJ, Kydd JH, Duffus WPH. Haematological changes and equine lymphocyte subpopulation kinetics during primary infection and attempted re-infection of specific pathogen free foals with EHV-1. Equine Vet. J. 1991;23:35–40.
- McCulloch J, Williamson SA, Powis SJ, Edington N. The effect of EHV-1 infection upon circulating leucocyte populations in the natural equine host.. Vet Microbiol 1993 Oct;37(1-2):147-61.
- Gilkerson JR, Whalley JM, Drummer HE, Studdert MJ, Love DN. Epidemiological studies of equine herpesvirus 1 (EHV-1) in Thoroughbred foals: a review of studies conducted in the Hunter Valley of New South Wales between 1995 and 1997.. Vet Microbiol 1999 Aug 16;68(1-2):15-25.
- Gilkerson JR, Whalley JM, Drummer HE, Studdert MJ, Love DN. Epidemiology of EHV-1 and EHV-4 in the mare and foal populations on a Hunter Valley stud farm: are mares the source of EHV-1 for unweaned foals.. Vet Microbiol 1999 Aug 16;68(1-2):27-34.
- Foote CE, Love DN, Gilkerson JR, Whalley JM. Detection of EHV-1 and EHV-4 DNA in unweaned Thoroughbred foals from vaccinated mares on a large stud farm.. Equine Vet J 2004 May;36(4):341-5.
- Mumford JA, Rossdale PD, Jessett DM, Gann SJ, Ousey J, Cook RF. Serological and virological investigations of an equid herpesvirus 1 (EHV-1) abortion storm on a stud farm in 1985.. J Reprod Fertil Suppl 1987;35:509-18.
- Cox E, Reddy S, Iofin I, Cohen JI. Varicella-zoster virus ORF57, unlike its pseudorabies virus UL3.5 homolog, is dispensable for viral replication in cell culture.. Virology 1998 Oct 10;250(1):205-9.
- Dean HJ, Cheung AK. A 3' coterminal gene cluster in pseudorabies virus contains herpes simplex virus UL1, UL2, and UL3 gene homologs and a unique UL3.5 open reading frame.. J Virol 1993 Oct;67(10):5955-61.
- Chaudhuri V, Sommer M, Rajamani J, Zerboni L, Arvin AM. Functions of Varicella-zoster virus ORF23 capsid protein in viral replication and the pathogenesis of skin infection.. J Virol 2008 Oct;82(20):10231-46.
- Sun Y, Brown SM. The open reading frames 1, 2, 71, and 75 are nonessential for the replication of equine herpesvirus type 1 in vitro.. Virology 1994 Mar;199(2):448-52.
- Hussey GS, Goehring LS, Lunn DP, Hussey SB, Huang T, Osterrieder N, Powell C, Hand J, Holz C, Slater J. Experimental infection with equine herpesvirus type 1 (EHV-1) induces chorioretinal lesions.. Vet Res 2013 Dec 5;44(1):118.
- Drummer HE, Reubel GH, Studdert MJ. Equine gammaherpesvirus 2 (EHV2) is latent in B lymphocytes.. Arch Virol 1996;141(3-4):495-504.
- Mekuria ZH, El-Hage C, Ficorilli NP, Washington EA, Gilkerson JR, Hartley CA. Mapping B lymphocytes as major reservoirs of naturally occurring latent equine herpesvirus 5 infection.. J Gen Virol 2017 Mar;98(3):461-470.
- Wang L, Raidal SL, Pizzirani A, Wilcox GE. Detection of respiratory herpesviruses in foals and adult horses determined by nested multiplex PCR.. Vet Microbiol 2007 Mar 31;121(1-2):18-28.
- Zarski LM, High EA, Nelli RK, Bolin SR, Williams KJ, Hussey G. Development and application of a quantitative PCR assay to study equine herpesvirus 5 invasion and replication in equine tissues in vitro and in vivo.. J Virol Methods 2017 Oct;248:44-53.
- Miglio A, Morelli C, Gialletti R, Lauteri E, Sforna M, Marenzoni ML, Antognoni MT. Clinical and immunophenotypic findings in 4 forms of equine lymphoma.. Can Vet J 2019 Jan;60(1):33-40.
- Miglio A, Antognoni MT, Morelli C, Gialletti R. Third Eyelid T-cell-Rich Large B-cell Lymphoma Positive to EHV-5 in a Mare—A Case Report. J. Equine Vet. Sci. 2018;70:52–56.
- Bell SA, Balasuriya UB, Gardner IA, Barry PA, Wilson WD, Ferraro GL, MacLachlan NJ. Temporal detection of equine herpesvirus infections of a cohort of mares and their foals.. Vet Microbiol 2006 Sep 10;116(4):249-57.
- Akkutay AZ, Osterrieder N, Damiani A, Tischer BK, Borchers K, Alkan F. Prevalence of equine gammaherpesviruses on breeding farms in Turkey and development of a TaqMan MGB real-time PCR to detect equine herpesvirus 5 (EHV-5).. Arch Virol 2014 Nov;159(11):2989-95.
- Anders S, Pyl PT, Huber W. HTSeq--a Python framework to work with high-throughput sequencing data.. Bioinformatics 2015 Jan 15;31(2):166-9.
- Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools.. Bioinformatics 2009 Aug 15;25(16):2078-9.
- Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown.. Nat Protoc 2016 Sep;11(9):1650-67.
- Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. .
- Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 2011;17:10–12.
- Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades.. Nucleic Acids Res 2012 Jan;40(1):37-52.
- Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics.. Nucleic Acids Res 2008 Jan;36(Database issue):D154-8.
- Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
- Yu G, Wang LG, Han Y, He QY. clusterProfiler: an R package for comparing biological themes among gene clusters.. OMICS 2012 May;16(5):284-7.
- Carlson M. org.Hs.eg.db: Genome Wide Annotation for Human. 2019.
- Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of gene ontology terms.. PLoS One 2011;6(7):e21800.
- Agarwal V, Bell GW, Nam JW, Bartel DP. Predicting effective microRNA target sites in mammalian mRNAs.. Elife 2015 Aug 12;4.
- Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. Integrative genomics viewer.. Nat Biotechnol 2011 Jan;29(1):24-6.
- Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.. Bioinformatics 2010 Jan 1;26(1):139-40.
Citations
This article has been cited 9 times.- Tombácz D, Torma G, Gulyás G, Fülöp Á, Dörmő Á, Prazsák I, Csabai Z, Mizik M, Hornyák Á, Zádori Z, Kakuk B, Boldogkői Z. Hybrid sequencing discloses unique aspects of the transcriptomic architecture in equid alphaherpesvirus 1. Heliyon 2023 Jul;9(7):e17716.
- Hu D, Tang Y, Wang C, Qi Y, Ente M, Li X, Zhang D, Li K, Chu H. The Role of Intestinal Microbial Metabolites in the Immunity of Equine Animals Infected With Horse Botflies. Front Vet Sci 2022;9:832062.
- Zarski LM, Giessler KS, Jacob SI, Weber PSD, McCauley AG, Lee Y, Soboll Hussey G. Identification of Host Factors Associated with the Development of Equine Herpesvirus Myeloencephalopathy by Transcriptomic Analysis of Peripheral Blood Mononuclear Cells from Horses. Viruses 2021 Feb 24;13(3).
- Cullen JN, Cieslak J, Petersen JL, Bellone RR, Finno CJ, Kalbfleisch TS, Calloe K, Capomaccio S, Cappelli K, Coleman SJ, Distl O, Durward-Akhurst SA, Giulotto E, Hamilton NA, Hill EW, Katz LM, Klaerke DA, Lindgren G, MacHugh DE, Mackowski M, MacLeod JN, Metzger J, Murphy BA, Orlando L, Raudsepp T, Silvestrelli M, Strand E, Tozaki T, Trachsel DS, Valderrama Figueroa LS, Velie BD, Wade CM, Waud B, Mickelson JR, McCue ME. Charting the equine miRNA landscape: An integrated pipeline and browser for annotating, quantifying, and visualizing expression. PLoS Genet 2025 Sep;21(9):e1011835.
- Ji Y, Xu D, Si W, Zhang Y, Khan MZ, Zhao X, Liu W. Transcriptomic and Proteomic Profiling of Rabbit Kidney Cells Infected with Equine Herpesvirus 8. Viruses 2025 Apr 29;17(5).
- Kosovsky GY, Glazko GV, Skobel OI. Bos taurus and Bison bison conservative retrotransposon recombination products. Front Vet Sci 2025;12:1516731.
- Tombácz D, Maróti Z, Oláh P, Dörmő Á, Gulyás G, Kalmár T, Csabai Z, Boldogkői Z. Temporal transcriptional profiling of host cells infected by a veterinary alphaherpesvirus using nanopore sequencing. Sci Rep 2025 Jan 25;15(1):3247.
- Holmes CM, Babasyan S, Eady N, Schnabel CL, Wagner B. Immune horses rapidly increase antileukoproteinase and lack type I interferon secretion during mucosal innate immune responses against equine herpesvirus type 1. Microbiol Spectr 2024 Oct 3;12(10):e0109224.
- Pusterla N, Dorman DC, Burgess BA, Goehring L, Gross M, Osterrieder K, Soboll Hussey G, Lunn DP. Viremia and nasal shedding for the diagnosis of equine herpesvirus-1 infection in domesticated horses. J Vet Intern Med 2024 May-Jun;38(3):1765-1791.