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Frontiers in veterinary science2020; 7; 621; doi: 10.3389/fvets.2020.00621

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.

Abstract: Upper respiratory tract infections with Equid Herpesvirus 1 (EHV-1) typically result in a peripheral blood mononuclear cell-associated viremia, which can lead to vasculopathy in the central nervous system. Primary EHV-1 infection also likely establishes latency in trigeminal ganglia (TG) via retrograde axonal transport and in respiratory tract-associated lymphatic tissue. However, latency establishment and reactivation are poorly understood. To characterize the pathogenesis of EHV-1 latency establishment and maintenance, two separate groups of yearling horses were experimentally infected intranasally with EHV-1, strain Ab4, and euthanized 30 days post infection (dpi), ( = 9) and 70 dpi ( = 6). During necropsy, TG, sympathetic trunk (ST), retropharyngeal and mesenteric lymph nodes (RLn, MesLn) and kidney samples were collected. Viral DNA was detected by quantitative PCR (qPCR) in TG, ST, RLn, and MesLn samples in horses 30 and 70 dpi. The number of positive TG, RLn and MesLn samples was reduced when comparing horses 30 and 70 dpi and the viral copy number in TG and RLn significantly declined from 30 to 70 dpi. EHV-1 late gene glycoprotein B reverse transcriptase PCR and IHC results for viral protein were consistently negative, thus lytic replication was excluded in the present study. Mild inflammation could be detected in all neural tissue samples and inflammatory infiltrates mainly consisted of CD3+ T-lymphocytes (T-cells), frequently localized in close proximity to neuronal cell bodies. To identify latently infected cell types, hybridization (ISH, RNAScope®) detecting viral DNA was used on selected qPCR- positive neural tissue sections. In ganglia 30 dpi, EHV-1 ISH signal was located in the neurons of TG and ST, but also in non-neuronal support or interstitial cells surrounding the neuron. In contrast, distinct EHV-1 signal could only be observed in neurons of TG 70 dpi. Overall, detection of latent EHV-1 in abdominal tissue samples and non-neuronal cell localization suggests, that EHV-1 uses T-cells during viremia as alternative route toward latency locations in addition to retrograde neuronal transport. We therefore hypothesize that EHV-1 follows the same latency pathways as its close relative human pathogen Varicella Zoster Virus.
Publication Date: 2020-09-04 PubMed ID: 33102556PubMed Central: PMC7499125DOI: 10.3389/fvets.2020.00621Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study investigates how Equid Herpesvirus 1 (EHV-1), a virus causing upper respiratory tract infections in horses, establishes and maintains latency in different tissues over time. The researchers examined tissues from horses experimentally infected with EHV-1 at 30 and 70 days post-infection, and suggested the virus could use T-cells to reach latency locations.

Methodology and Experimental Design

  • The researchers experimentally infected two groups of yearling horses intranasally with EHV-1, strain Ab4. Post-infection at 30 and 70 days, the horses were euthanized and samples from various tissues were collected for analysis.
  • The samples examined included trigeminal ganglia (TG), sympathetic trunk (ST), retropharyngeal and mesenteric lymph nodes (RLn, MesLn), and kidneys.
  • They detected viral DNA in these samples using quantitative PCR (qPCR) and conducted additional tests to identify latently infected cell types.

Results and Findings

  • Viral DNA was detected in all types of samples in horses at both 30 and 70 days post-infection. However, the number of samples testing positive and the viral copy number declined from 30 to 70 days.
  • Despite the presence of viral DNA, there were no signs of active viral replication.
  • They found mild inflammation in all neural tissue samples. CD3+ T-cells, a type of immune cell, were frequently located close to neuronal cell bodies.
  • EHV-1 detection patterns in the TG and ST samples suggested that the virus initially targets a variety of cells (neuronal and non-neuronal), but later on only targets neurons, especially at 70 days post-infection.

Conclusions and Implications

  • The findings suggest that EHV-1 may use T-cells during the viremic phase (when the virus is present in the bloodstream) to reach various latency locations, in addition to using retrograde neuronal transport.
  • The researchers hypothesize that EHV-1 follows similar latency pathways as the Varicella Zoster Virus, a human pathogen closely related to EHV-1.
  • The findings may shed light on the pathogenesis of EHV-1 infection and the mechanisms underlying viral latency, which could inform future therapeutic strategies.

Cite This Article

APA
Giessler KS, Samoilowa S, Soboll Hussey G, Kiupel M, Matiasek K, Sledge DG, Liesche F, Schlegel J, Fux R, Goehring LS. (2020). 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, 7, 621. https://doi.org/10.3389/fvets.2020.00621

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 7
Pages: 621
PII: 621

Researcher Affiliations

Giessler, Kim S
  • Equine Hospital, Division of Medicine and Reproduction, Center for Clinical Veterinary Medicine, Ludwig-Maximilians University, Munich, Germany.
  • Department of Pathobiology and Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, East Lansing, MI, United States.
Samoilowa, Susanna
  • Equine Hospital, Division of Medicine and Reproduction, Center for Clinical Veterinary Medicine, Ludwig-Maximilians University, Munich, Germany.
Soboll Hussey, Gisela
  • Department of Pathobiology and Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, East Lansing, MI, United States.
Kiupel, Matti
  • Department of Pathobiology and Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, East Lansing, MI, United States.
  • Veterinary Diagnostic Laboratory, College of Veterinary Medicine, Michigan State University, Lansing, MI, United States.
Matiasek, Kaspar
  • Section of Clinical and Comparative Neuropathology, Centre for Clinical Veterinary Medicine, Ludwig-Maximilians University München, Munich, Germany.
Sledge, Dodd G
  • Veterinary Diagnostic Laboratory, College of Veterinary Medicine, Michigan State University, Lansing, MI, United States.
Liesche, Friederike
  • Department of Neuropathology, School of Medicine, Institute of Pathology, Technical University Munich, Munich, Germany.
Schlegel, Jürgen
  • Department of Neuropathology, School of Medicine, Institute of Pathology, Technical University Munich, Munich, Germany.
Fux, Robert
  • Veterinary Science Department, Institute of Infectious Diseases and Zoonoses, Ludwig-Maximilians University, Munich, Germany.
Goehring, Lutz S
  • Equine Hospital, Division of Medicine and Reproduction, Center for Clinical Veterinary Medicine, Ludwig-Maximilians University, Munich, Germany.

References

This article includes 68 references
  1. Hussey SB, Clark R, Lunn KF, Breathnach C, Soboll G, Whalley JM, Lunn DP. Detection and quantification of equine herpesvirus-1 viremia and nasal shedding by real-time polymerase chain reaction.. J Vet Diagn Invest 2006 Jul;18(4):335-42.
    doi: 10.1177/104063870601800403pubmed: 16921871google scholar: lookup
  2. Goehring LS, van Maanen C, Berendsen M, Cullinane A, de Groot RJ, Rottier PJ, Wesselingh JJ, Sloet van Oldruitenborgh-Oosterbaan MM. Experimental infection with neuropathogenic equid herpesvirus type 1 (EHV-1) in adult horses.. Vet J 2010 Nov;186(2):180-7.
    doi: 10.1016/j.tvjl.2009.08.007pubmed: 19726209google scholar: lookup
  3. Slater J. Equine herpesviruses. Equine Infectious Diseases St. Louis, MO: Elsevier; (2014). p. 151-168.e158.
  4. 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.
    doi: 10.1099/0022-1317-81-1-21pubmed: 10640538google scholar: lookup
  5. Vandekerckhove AP, Glorieux S, Gryspeerdt AC, Steukers L, Duchateau L, Osterrieder N, Van de Walle GR, Nauwynck HJ. Replication kinetics of neurovirulent versus non-neurovirulent equine herpesvirus type 1 strains in equine nasal mucosal explants.. J Gen Virol 2010 Aug;91(Pt 8):2019-2028.
    doi: 10.1099/vir.0.019257-0pubmed: 20427565google scholar: lookup
  6. 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.
    doi: 10.1016/j.vetmic.2010.10.004pubmed: 21093993google scholar: lookup
  7. 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).
    doi: 10.1128/JVI.02098-18pmc: PMC6430527pubmed: 30651370google scholar: lookup
  8. 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.
    doi: 10.1099/0022-1317-75-8-2007pubmed: 8046404google scholar: lookup
  9. Baxi MK, Efstathiou S, Lawrence G, Whalley JM, Slater JD, Field HJ. The detection of latency-associated transcripts of equine herpesvirus 1 in ganglionic neurons.. J Gen Virol 1995 Dec;76 ( Pt 12):3113-8.
    doi: 10.1099/0022-1317-76-12-3113pubmed: 8847517google scholar: lookup
  10. Efstathiou S, Preston CM. Towards an understanding of the molecular basis of herpes simplex virus latency.. Virus Res 2005 Aug;111(2):108-19.
  11. Reichelt M, Wang L, Sommer M, Perrino J, Nour AM, Sen N, Baiker A, Zerboni L, Arvin AM. Entrapment of viral capsids in nuclear PML cages is an intrinsic antiviral host defense against varicella-zoster virus.. PLoS Pathog 2011 Feb 3;7(2):e1001266.
  12. Jones C. Bovine Herpes Virus 1 (BHV-1) and Herpes Simplex Virus Type 1 (HSV-1) Promote Survival of Latently Infected Sensory Neurons, in Part by Inhibiting Apoptosis.. J Cell Death 2013;6:1-16.
    doi: 10.4137/JCD.S10803pmc: PMC4147773pubmed: 25278776google scholar: lookup
  13. Ramakrishnan R, Poliani PL, Levine M, Glorioso JC, Fink DJ. Detection of herpes simplex virus type 1 latency-associated transcript expression in trigeminal ganglia by in situ reverse transcriptase PCR.. J Virol 1996 Sep;70(9):6519-23.
  14. Pusterla N, Hussey SB, Mapes S, Johnson C, Collier JR, Hill J, Lunn DP, Wilson WD. Molecular investigation of the viral kinetics of equine herpesvirus-1 in blood and nasal secretions of horses after corticosteroid-induced recrudescence of latent infection.. J Vet Intern Med 2010 Sep-Oct;24(5):1153-7.
  15. 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.
    doi: 10.1136/vr.c3748pubmed: 20817899google scholar: lookup
  16. Liu T, Tang Q, Hendricks RL. Inflammatory infiltration of the trigeminal ganglion after herpes simplex virus type 1 corneal infection.. J Virol 1996 Jan;70(1):264-71.
    doi: 10.1128/JVI.70.1.264-271.1996pmc: PMC189813pubmed: 8523535google scholar: lookup
  17. Gilden DH, Vafai A, Shtram Y, Becker Y, Devlin M, Wellish M. Varicella-zoster virus DNA in human sensory ganglia.. Nature 1983 Dec 1-7;306(5942):478-80.
    doi: 10.1038/306478a0pubmed: 6316159google scholar: lookup
  18. Edington N, Bridges CG, Patel JR. Endothelial cell infection and thrombosis in paralysis caused by equid herpesvirus-1: equine stroke.. Arch Virol 1986;90(1-2):111-24.
    doi: 10.1007/BF01314149pubmed: 3015074google scholar: lookup
  19. Welch HM, Bridges CG, Lyon AM, Griffiths L, Edington N. Latent equid herpesviruses 1 and 4: detection and distinction using the polymerase chain reaction and co-cultivation from lymphoid tissues.. J Gen Virol 1992 Feb;73 ( Pt 2):261-8.
    doi: 10.1099/0022-1317-73-2-261pubmed: 1347078google scholar: lookup
  20. Kydd JH, Smith KC, Hannant D, Livesay GJ, Mumford JA. Distribution of equid herpesvirus-1 (EHV-1) in respiratory tract associated lymphoid tissue: implications for cellular immunity.. Equine Vet J 1994 Nov;26(6):470-3.
  21. Chesters PM, Allsop R, Purewal A, Edington N. Detection of latency-associated transcripts of equid herpesvirus 1 in equine leukocytes but not in trigeminal ganglia.. J Virol 1997 May;71(5):3437-43.
  22. Smith DJ, Iqbal J, Purewal A, Hamblin AS, Edington N. In vitro reactivation of latent equid herpesvirus-1 from CD5+/CD8+ leukocytes indirectly by IL-2 or chorionic gonadotrophin.. J Gen Virol 1998 Dec;79 ( Pt 12):2997-3004.
    doi: 10.1099/0022-1317-79-12-2997pubmed: 9880014google scholar: lookup
  23. Goehring L. Latency in Equid Herpesvirus-1 purpose-infected Horses, in 2017 ACVIM Forum Research Report Program. J Vet Int Med (2017) 31:1598–9.
    doi: 10.1111/jvim.14784google scholar: lookup
  24. Grigoryan S, Yee MB, Glick Y, Gerber D, Kepten E, Garini Y, Yang IH, Kinchington PR, Goldstein RS. Direct transfer of viral and cellular proteins from varicella-zoster virus-infected non-neuronal cells to human axons.. PLoS One 2015;10(5):e0126081.
  25. Depledge DP, Sadaoka T, Ouwendijk WJD. Molecular Aspects of Varicella-Zoster Virus Latency.. Viruses 2018 Jun 28;10(7).
    doi: 10.3390/v10070349pmc: PMC6070824pubmed: 29958408google scholar: lookup
  26. Kydd JH, Townsend HG, Hannant D. The equine immune response to equine herpesvirus-1: the virus and its vaccines.. Vet Immunol Immunopathol 2006 May 15;111(1-2):15-30.
    doi: 10.1016/j.vetimm.2006.01.005pubmed: 16476492google scholar: lookup
  27. Crowhurst FA, Dickinson G, Burrows R. An outbreak of paresis in mares and geldings associated with equid herpesvirus 1.. Vet Rec 1981 Dec 12;109(24):527-8.
    pubmed: 6280366
  28. 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.
    doi: 10.1099/jgv.0.000773pubmed: 28631601google scholar: lookup
  29. Pusterla N, Wilson WD, Conrad PA, Barr BC, Ferraro GL, Daft BM, Leutenegger CM. Cytokine gene signatures in neural tissue of horses with equine protozoal myeloencephalitis or equine herpes type 1 myeloencephalopathy.. Vet Rec 2006 Sep 9;159(11):341-6.
    doi: 10.1136/vr.159.11.341pubmed: 16963713google scholar: lookup
  30. Abdelgawad A, Damiani A, Ho SY, Strauss G, Szentiks CA, East ML, Osterrieder N, Greenwood AD. Zebra Alphaherpesviruses (EHV-1 and EHV-9): Genetic Diversity, Latency and Co-Infections.. Viruses 2016 Sep 20;8(9).
    doi: 10.3390/v8090262pmc: PMC5035975pubmed: 27657113google scholar: lookup
  31. Wang F, Flanagan J, Su N, Wang LC, Bui S, Nielson A, Wu X, Vo HT, Ma XJ, Luo Y. RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues.. J Mol Diagn 2012 Jan;14(1):22-9.
  32. Grabinski TM, Kneynsberg A, Manfredsson FP, Kanaan NM. A method for combining RNAscope in situ hybridization with immunohistochemistry in thick free-floating brain sections and primary neuronal cultures.. PLoS One 2015;10(3):e0120120.
  33. Pennington MR, Cossic BGA, Perkins GA, Duffy C, Duhamel GE, Van de Walle GR. First demonstration of equid gammaherpesviruses within the gastric mucosal epithelium of horses.. Virus Res 2017 Oct 15;242:30-36.
  34. Pannese E. The satellite cells of the sensory ganglia.. Adv Anat Embryol Cell Biol 1981;65:1-111.
    doi: 10.1007/978-3-642-67750-2_1pubmed: 7013430google scholar: lookup
  35. Gibson JS, Slater JD, Awan AR, Field HJ. Pathogenesis of equine herpesvirus-1 in specific pathogen-free foals: primary and secondary infections and reactivation.. Arch Virol 1992;123(3-4):351-66.
    doi: 10.1007/BF01317269pubmed: 1314051google scholar: lookup
  36. 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.
    doi: 10.2460/ajvr.69.12.1595pubmed: 19046006google scholar: lookup
  37. 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.
  38. Pusterla N, Wilson WD, Mapes S, Finno C, Isbell D, Arthur RM, Ferraro GL. Characterization of viral loads, strain and state of equine herpesvirus-1 using real-time PCR in horses following natural exposure at a racetrack in California.. Vet J 2009 Feb;179(2):230-9.
    doi: 10.1016/j.tvjl.2007.09.018pubmed: 18024200google scholar: lookup
  39. Pusterla N, Mapes S, David Wilson W. Prevalence of latent alpha-herpesviruses in Thoroughbred racing horses.. Vet J 2012 Aug;193(2):579-82.
    doi: 10.1016/j.tvjl.2012.01.030pubmed: 22405721google scholar: lookup
  40. Diefenbach RJ, Miranda-Saksena M, Douglas MW, Cunningham AL. Transport and egress of herpes simplex virus in neurons.. Rev Med Virol 2008 Jan-Feb;18(1):35-51.
    doi: 10.1002/rmv.560pubmed: 17992661google scholar: lookup
  41. Gilden DH, Rozenman Y, Murray R, Devlin M, Vafai A. Detection of varicella-zoster virus nucleic acid in neurons of normal human thoracic ganglia.. Ann Neurol 1987 Sep;22(3):377-80.
    doi: 10.1002/ana.410220315pubmed: 2823688google scholar: lookup
  42. Furuta Y, Takasu T, Fukuda S, Sato-Matsumura KC, Inuyama Y, Hondo R, Nagashima K. Detection of varicella-zoster virus DNA in human geniculate ganglia by polymerase chain reaction.. J Infect Dis 1992 Nov;166(5):1157-9.
    doi: 10.1093/infdis/166.5.1157pubmed: 1328403google scholar: lookup
  43. Mahalingam R, Wellish MC, Dueland AN, Cohrs RJ, Gilden DH. Localization of herpes simplex virus and varicella zoster virus DNA in human ganglia.. Ann Neurol 1992 Apr;31(4):444-8.
    doi: 10.1002/ana.410310417pubmed: 1316733google scholar: lookup
  44. Kennedy PG, Grinfeld E, Gow JW. Latent varicella-zoster virus is located predominantly in neurons in human trigeminal ganglia.. Proc Natl Acad Sci U S A 1998 Apr 14;95(8):4658-62.
    doi: 10.1073/pnas.95.8.4658pmc: PMC22546pubmed: 9539794google scholar: lookup
  45. Kennedy PG, Grinfeld E, Gow JW. Latent Varicella-zoster virus in human dorsal root ganglia.. Virology 1999 Jun 5;258(2):451-4.
    doi: 10.1006/viro.1999.9745pubmed: 10366583google scholar: lookup
  46. Nagel MA, Rempel A, Huntington J, Kim F, Choe A, Gilden D. Frequency and abundance of alphaherpesvirus DNA in human thoracic sympathetic ganglia.. J Virol 2014 Jul;88(14):8189-92.
    doi: 10.1128/JVI.01070-14pmc: PMC4097807pubmed: 24789785google scholar: lookup
  47. Zerboni L, Arvin AM. The pathogenesis of Varicella-Zoster virus neurotropism and infection. Neurotropic Viral Infections: Volume 2: Neurotropic Retroviruses, DNA Viruses, Immunity and Transmission Cham: Springer International Publishing; (2016).
  48. Croen KD, Ostrove JM, Dragovic LJ, Straus SE. Patterns of gene expression and sites of latency in human nerve ganglia are different for varicella-zoster and herpes simplex viruses.. Proc Natl Acad Sci U S A 1988 Dec;85(24):9773-7.
    doi: 10.1073/pnas.85.24.9773pmc: PMC282863pubmed: 2849116google scholar: lookup
  49. Cai GY, Pizer LI, Levin MJ. Fractionation of neurons and satellite cells from human sensory ganglia in order to study herpesvirus latency.. J Virol Methods 2002 Jun;104(1):21-32.
    doi: 10.1016/S0166-0934(02)00032-0pubmed: 12020789google scholar: lookup
  50. Levin MJ, Cai GY, Manchak MD, Pizer LI. Varicella-zoster virus DNA in cells isolated from human trigeminal ganglia.. J Virol 2003 Jun;77(12):6979-87.
  51. Wang QY, Zhou C, Johnson KE, Colgrove RC, Coen DM, Knipe DM. Herpesviral latency-associated transcript gene promotes assembly of heterochromatin on viral lytic-gene promoters in latent infection.. Proc Natl Acad Sci U S A 2005 Nov 1;102(44):16055-9.
    doi: 10.1073/pnas.0505850102pmc: PMC1266038pubmed: 16247011google scholar: lookup
  52. Liu T, Khanna KM, Carriere BN, Hendricks RL. Gamma interferon can prevent herpes simplex virus type 1 reactivation from latency in sensory neurons.. J Virol 2001 Nov;75(22):11178-84.
  53. Bloom DC. Alphaherpesvirus Latency: A Dynamic State of Transcription and Reactivation.. Adv Virus Res 2016;94:53-80.
    pubmed: 26997590doi: 10.1016/bs.aivir.2015.10.001google scholar: lookup
  54. Lungu O, Annunziato PW, Gershon A, Staugaitis SM, Josefson D, LaRussa P, Silverstein SJ. Reactivated and latent varicella-zoster virus in human dorsal root ganglia.. Proc Natl Acad Sci U S A 1995 Nov 21;92(24):10980-4.
    doi: 10.1073/pnas.92.24.10980pmc: PMC40554pubmed: 7479921google scholar: lookup
  55. Kennedy PG, Rovnak J, Badani H, Cohrs RJ. A comparison of herpes simplex virus type 1 and varicella-zoster virus latency and reactivation.. J Gen Virol 2015 Jul;96(Pt 7):1581-602.
    doi: 10.1099/vir.0.000128pmc: PMC4635449pubmed: 25794504google scholar: lookup
  56. Carossino M, Loynachan AT, James MacLachlan N, Drew C, Shuck KM, Timoney PJ, Del Piero F, Balasuriya UB. Detection of equine arteritis virus by two chromogenic RNA in situ hybridization assays (conventional and RNAscope(®)) and assessment of their performance in tissues from aborted equine fetuses.. Arch Virol 2016 Nov;161(11):3125-36.
    doi: 10.1007/s00705-016-3014-5pubmed: 27541817google scholar: lookup
  57. Hanani M. Satellite glial cells in sensory ganglia: from form to function.. Brain Res Brain Res Rev 2005 Jun;48(3):457-76.
  58. van Velzen M, Laman JD, Kleinjan A, Poot A, Osterhaus AD, Verjans GM. Neuron-interacting satellite glial cells in human trigeminal ganglia have an APC phenotype.. J Immunol 2009 Aug 15;183(4):2456-61.
    doi: 10.4049/jimmunol.0900890pubmed: 19635905google scholar: lookup
  59. Hu P, McLachlan EM. Macrophage and lymphocyte invasion of dorsal root ganglia after peripheral nerve lesions in the rat.. Neuroscience 2002;112(1):23-38.
    doi: 10.1016/S0306-4522(02)00065-9pubmed: 12044469google scholar: lookup
  60. Reichelt M, Zerboni L, Arvin AM. Mechanisms of varicella-zoster virus neuropathogenesis in human dorsal root ganglia.. J Virol 2008 Apr;82(8):3971-83.
    doi: 10.1128/JVI.02592-07pmc: PMC2292995pubmed: 18256143google scholar: lookup
  61. 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.
    doi: 10.1016/0378-1135(93)90189-Epubmed: 8296444google scholar: lookup
  62. Kydd JH, Smith KC, Hannant D, Livesay GJ, Mumford JA. Distribution of equid herpesvirus-1 (EHV-1) in the respiratory tract of ponies: implications for vaccination strategies.. Equine Vet J 1994 Nov;26(6):466-9.
  63. Gryspeerdt AC, Vandekerckhove AP, Baghi HB, Van de Walle GR, Nauwynck HJ. Expression of late viral proteins is restricted in nasal mucosal leucocytes but not in epithelial cells during early-stage equine herpes virus-1 infection.. Vet J 2012 Aug;193(2):576-8.
    doi: 10.1016/j.tvjl.2012.01.022pubmed: 22425309google scholar: lookup
  64. 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.
  65. 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.
    doi: 10.1099/vir.0.067363-0pubmed: 25239765google scholar: lookup
  66. Ku CC, Padilla JA, Grose C, Butcher EC, Arvin AM. Tropism of varicella-zoster virus for human tonsillar CD4(+) T lymphocytes that express activation, memory, and skin homing markers.. J Virol 2002 Nov;76(22):11425-33.
  67. Edington N, Welch HM, Griffiths L. The prevalence of latent Equid herpesviruses in the tissues of 40 abattoir horses.. Equine Vet J 1994 Mar;26(2):140-2.
  68. 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.
    doi: 10.1016/j.vetimm.2011.06.032pubmed: 21764140google scholar: lookup

Citations

This article has been cited 6 times.
  1. Samoilowa S, Giessler KS, Torres CEM, Hussey GS, Allum A, Fux R, Jerke C, Kiupel M, Matiasek K, Sledge DG, Goehring LS. Equid herpesvirus-1 Distribution in Equine Lymphoid and Neural Tissues 70 Days Post Infection. Pathogens 2021 Jun 5;10(6).
    doi: 10.3390/pathogens10060707pubmed: 34198884google scholar: lookup
  2. Laval K, Poelaert KCK, Van Cleemput J, Zhao J, Vandekerckhove AP, Gryspeerdt AC, Garré B, van der Meulen K, Baghi HB, Dubale HN, Zarak I, Van Crombrugge E, Nauwynck HJ. The Pathogenesis and Immune Evasive Mechanisms of Equine Herpesvirus Type 1. Front Microbiol 2021;12:662686.
    doi: 10.3389/fmicb.2021.662686pubmed: 33746936google scholar: lookup
  3. 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).
    doi: 10.3390/v13030356pubmed: 33668216google scholar: lookup
  4. Zarski LM, Weber PSD, Lee Y, Soboll Hussey G. Transcriptomic Profiling of Equine and Viral Genes in Peripheral Blood Mononuclear Cells in Horses during Equine Herpesvirus 1 Infection. Pathogens 2021 Jan 7;10(1).
    doi: 10.3390/pathogens10010043pubmed: 33430330google scholar: lookup
  5. Tallmadge RL, Laverack M, Lejeune M, Crossley B, Diel DG. A multiplex real-time PCR assay for detection of equid herpesvirus 1 and 4. Sci Rep 2025 Oct 31;15(1):38201.
    doi: 10.1038/s41598-025-22043-wpubmed: 41173927google scholar: lookup
  6. Nishimura F, Fukushi N, Sakai H, Fukushi H. Attenuation of the neuropathogenic equine herpesvirus type 1 strain Ab4p in hamsters by a single amino acid mutation (D752N) in viral DNA polymerase ORF30. J Vet Med Sci 2024 Dec 1;86(12):1273-1278.
    doi: 10.1292/jvms.24-0338pubmed: 39384384google scholar: lookup