FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS One / Equid herpesvirus type 1 activates platelets.
PloS one2015; 10(4); e0122640; doi: 10.1371/journal.pone.0122640

Equid herpesvirus type 1 activates platelets.

Abstract: Equid herpesvirus type 1 (EHV-1) causes outbreaks of abortion and neurological disease in horses. One of the main causes of these clinical syndromes is thrombosis in placental and spinal cord vessels, however the mechanism for thrombus formation is unknown. Platelets form part of the thrombus and amplify and propagate thrombin generation. Here, we tested the hypothesis that EHV-1 activates platelets. We found that two EHV-1 strains, RacL11 and Ab4 at 0.5 or higher plaque forming unit/cell, activate platelets within 10 minutes, causing α-granule secretion (surface P-selectin expression) and platelet microvesiculation (increased small events double positive for CD41 and Annexin V). Microvesiculation was more pronounced with the RacL11 strain. Virus-induced P-selectin expression required plasma and 1.0 mM exogenous calcium. P-selectin expression was abolished and microvesiculation was significantly reduced in factor VII- or X-deficient human plasma. Both P-selectin expression and microvesiculation were re-established in factor VII-deficient human plasma with added purified human factor VIIa (1 nM). A glycoprotein C-deficient mutant of the Ab4 strain activated platelets as effectively as non-mutated Ab4. P-selectin expression was abolished and microvesiculation was significantly reduced by preincubation of virus with a goat polyclonal anti-rabbit tissue factor antibody. Infectious virus could be retrieved from washed EHV-1-exposed platelets, suggesting a direct platelet-virus interaction. Our results indicate that EHV-1 activates equine platelets and that α-granule secretion is a consequence of virus-associated tissue factor triggering factor X activation and thrombin generation. Microvesiculation was only partly tissue factor and thrombin-dependent, suggesting the virus causes microvesiculation through other mechanisms, potentially through direct binding. These findings suggest that EHV-1-induced platelet activation could contribute to the thrombosis that occurs in clinically infected horses and provides a new mechanism by which viruses activate hemostasis.
Get Full Text
Publication Date: 2015-04-23 PubMed ID: 25905776PubMed Central: PMC4407896DOI: 10.1371/journal.pone.0122640Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

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 research article provides evidence that equid herpesvirus type 1 (EHV-1), a virus that causes abortion and neurological disease in horses, activates platelets in the blood which may contribute to blood clots in infected horses.

Background of the Research

  • EHV-1 is known to lead to placental and spinal cord thrombosis (blood clots) in horses, which results in abortion and neurological disease. But the reason why these blood clots form remained unknown.
  • Platelets, the cell fragments in blood that help in clotting, were scrutinized as potential culprits because they take part in the formation of thrombus (blood clot) and in amplifying and propagating thrombin, an enzyme in blood plasma essential for blood coagulation.

Main Findings

  • The researchers found that two strains of EHV-1, RacL11 and Ab4, activate platelets within 10 minutes, causing secretion from their α-granules (a process that aids clotting) and their microvesiculation (formation and release of small vesicles).
  • Microvesiculation was more pronounced in the case of the RacL11 strain.
  • Virus-induced activation of platelets required plasma (the liquid component of blood) and exogenous calcium (calcium from outside the cell).
  • Activation of platelets was significantly reduced in the absence of factor VII or factor X, proteins involved in clotting. However, P-selectin expression was restored upon addition of purified human factor VIIa in the factor VII-deficient plasma.
  • Interestingly, a glycoprotein C-deficient strain of the virus also activated platelets effectively, suggesting other mechanisms apart from glycoprotein C may be involved in platelet activation by the virus.
  • The findings also revealed that the activation platelets could be a result of virus-associated tissue factor triggering factor X activation and thrombin generation.
  • On a note, even though activation of platelets was partly dependent on tissue factor and thrombin, the research proposes that the virus might be causing microvesiculation through other mechanisms, potentially through direct binding.

Implicative Conclusion

  • This research indicates that horses infected with EHV-1 can experience platelet activation that can lead to the formation of harmful blood clots.
  • This insight opens up new understanding of how not just EHV-1, but potentially other viruses as well, can manipulate the hemostasis (the body’s natural response to stop bleeding by clotting blood), leading to pathological outcomes.

Cite This Article

APA
Stokol T, Yeo WM, Burnett D, DeAngelis N, Huang T, Osterrieder N, Catalfamo J. (2015). Equid herpesvirus type 1 activates platelets. PLoS One, 10(4), e0122640. https://doi.org/10.1371/journal.pone.0122640

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 10
Issue: 4
Pages: e0122640
PII: e0122640

Researcher Affiliations

Stokol, Tracy
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America.
Yeo, Wee Ming
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America.
Burnett, Deborah
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America.
DeAngelis, Nicole
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America.
Huang, Teng
  • Institut für Virologie, Freie Universität Berlin, Berlin, Germany.
Osterrieder, Nikolaus
  • Institut für Virologie, Freie Universität Berlin, Berlin, Germany.
Catalfamo, James
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America.

MeSH Terms

  • Abortion, Spontaneous / metabolism
  • Abortion, Spontaneous / virology
  • Animals
  • Blood Platelets / metabolism
  • Blood Platelets / virology
  • Factor X / metabolism
  • Female
  • Herpesviridae Infections / metabolism
  • Herpesviridae Infections / virology
  • Herpesvirus 1, Equid / metabolism
  • Horses / metabolism
  • Horses / virology
  • P-Selectin / metabolism
  • Placenta / metabolism
  • Placenta / virology
  • Platelet Activation / physiology
  • Pregnancy
  • Rabbits
  • Thrombin / metabolism
  • Thrombosis / metabolism
  • Thrombosis / virology
  • Viral Envelope Proteins / metabolism

Conflict of Interest Statement

The authors have declared no competing interests exist.

References

This article includes 45 references
  1. McSorley J, Shapiro L, Brownstein MH, Hsu KC. Herpes simplex and varicella-zoster: comparative histopathology of 77 cases.. Int J Dermatol 1974 Mar-Apr;13(2):69-75.
    pubmed: 4596285doi: 10.1111/j.1365-4362.1974.tb01769.xgoogle scholar: lookup
  2. Bunce PE, High SM, Nadjafi M, Stanley K, Liles WC, Christian MD. Pandemic H1N1 influenza infection and vascular thrombosis.. Clin Infect Dis 2011 Jan 15;52(2):e14-7.
    doi: 10.1093/cid/ciq125pubmed: 21288835google scholar: lookup
  3. Geisbert TW, Young HA, Jahrling PB, Davis KJ, Kagan E, Hensley LE. Mechanisms underlying coagulation abnormalities in ebola hemorrhagic fever: overexpression of tissue factor in primate monocytes/macrophages is a key event.. J Infect Dis 2003 Dec 1;188(11):1618-29.
    pubmed: 14639531doi: 10.1086/379724google scholar: lookup
  4. Vercellotti GM. Proinflammatory and procoagulant effects of herpes simplex infection on human endothelium.. Blood Cells 1990;16(1):209-15; discussion 215-6.
    pubmed: 2190648
  5. de Witt SM, Verdoold R, Cosemans JM, Heemskerk JW. Insights into platelet-based control of coagulation.. Thromb Res 2014 May;133 Suppl 2:S139-48.
    doi: 10.1016/S0049-3848(14)50024-2pubmed: 24862135google scholar: lookup
  6. Sinauridze EI, Kireev DA, Popenko NY, Pichugin AV, Panteleev MA, Krymskaya OV, Ataullakhanov FI. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets.. Thromb Haemost 2007 Mar;97(3):425-34.
    pubmed: 17334510
  7. Yang J, Furie BC, Furie B. The biology of P-selectin glycoprotein ligand-1: its role as a selectin counterreceptor in leukocyte-endothelial and leukocyte-platelet interaction.. Thromb Haemost 1999 Jan;81(1):1-7.
    pubmed: 10348699
  8. Slotta JE, Braun OO, Menger MD, Thorlacius H. Capture of platelets to the endothelium of the femoral vein is mediated by CD62P and CD162.. Platelets 2009 Nov;20(7):505-12.
    doi: 10.3109/09537100903215417pubmed: 19852690google scholar: lookup
  9. Oostingh GJ, Pozgajova M, Ludwig RJ, Krahn T, Boehncke WH, Nieswandt B, Schön MP. Diminished thrombus formation and alleviation of myocardial infarction and reperfusion injury through antibody- or small-molecule-mediated inhibition of selectin-dependent platelet functions.. Haematologica 2007 Apr;92(4):502-12.
    pubmed: 17488661doi: 10.3324/haematol.10741google scholar: lookup
  10. Agbanyo FR, Wasi S. Human cytomegalovirus interaction with platelets and adhesive glycoproteins: significance in viral pathogenesis.. J Infect Dis 1994 Nov;170(5):1120-7.
    pubmed: 7963703doi: 10.1093/infdis/170.5.1120google scholar: lookup
  11. Pugliese A, Gennero L, Cutufia M, Enrietto M, Morra E, Pescarmona P, Ponzetto A. HCV infective virions can be carried by human platelets.. Cell Biochem Funct 2004 Nov-Dec;22(6):353-8.
    pubmed: 15386445doi: 10.1002/cbf.1113google scholar: lookup
  12. Youssefian T, Drouin A, Massé JM, Guichard J, Cramer EM. Host defense role of platelets: engulfment of HIV and Staphylococcus aureus occurs in a specific subcellular compartment and is enhanced by platelet activation.. Blood 2002 Jun 1;99(11):4021-9.
    pubmed: 12010803doi: 10.1182/blood-2001-12-0191google scholar: lookup
  13. Noisakran S, Gibbons RV, Songprakhon P, Jairungsri A, Ajariyakhajorn C, Nisalak A, Jarman RG, Malasit P, Chokephaibulkit K, Perng GC. Detection of dengue virus in platelets isolated from dengue patients.. Southeast Asian J Trop Med Public Health 2009 Mar;40(2):253-62.
    pubmed: 19323010
  14. Koupenova M, Vitseva O, MacKay CR, Beaulieu LM, Benjamin EJ, Mick E, Kurt-Jones EA, Ravid K, Freedman JE. Platelet-TLR7 mediates host survival and platelet count during viral infection in the absence of platelet-dependent thrombosis.. Blood 2014 Jul 31;124(5):791-802.
    doi: 10.1182/blood-2013-11-536003pmc: PMC4118487pubmed: 24755410google scholar: lookup
  15. Mayne E, Funderburg NT, Sieg SF, Asaad R, Kalinowska M, Rodriguez B, Schmaier AH, Stevens W, Lederman MM. Increased platelet and microparticle activation in HIV infection: upregulation of P-selectin and tissue factor expression.. J Acquir Immune Defic Syndr 2012 Apr 1;59(4):340-6.
    doi: 10.1097/QAI.0b013e3182439355pmc: PMC3299881pubmed: 22156911google scholar: lookup
  16. Hottz ED, Oliveira MF, Nunes PC, Nogueira RM, Valls-de-Souza R, Da Poian AT, Weyrich AS, Zimmerman GA, Bozza PT, Bozza FA. Dengue induces platelet activation, mitochondrial dysfunction and cell death through mechanisms that involve DC-SIGN and caspases.. J Thromb Haemost 2013 May;11(5):951-62.
    doi: 10.1111/jth.12178pmc: PMC3971842pubmed: 23433144google scholar: lookup
  17. 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.
    doi: 10.1111/j.1939-1676.2009.0304.xpubmed: 19645832google 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.
    pubmed: 3015074doi: 10.1007/BF01314149google scholar: lookup
  19. Smith KC, Mumford JA, Lakhani K. A comparison of equid herpesvirus-1 (EHV-1) vascular lesions in the early versus late pregnant equine uterus.. J Comp Pathol 1996 Apr;114(3):231-47.
    pubmed: 8762581doi: 10.1016/s0021-9975(96)80045-4google scholar: lookup
  20. Smith KC, Whitwell KE, Mumford JA, Gower SM, Hannant D, Tearle JP. An immunohistological study of the uterus of mares following experimental infection by equid herpesvirus 1.. Equine Vet J 1993 Jan;25(1):36-40.
    pubmed: 8380768doi: 10.1111/j.2042-3306.1993.tb02898.xgoogle scholar: lookup
  21. Szeredi L, Aupperle H, Steiger K. Detection of equine herpesvirus-1 in the fetal membranes of aborted equine fetuses by immunohistochemical and in-situ hybridization techniques.. J Comp Pathol 2003 Aug-Oct;129(2-3):147-53.
    pubmed: 12921720doi: 10.1016/s0021-9975(03)00022-7google scholar: lookup
  22. 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.
    doi: 10.1186/1297-9716-44-16pmc: PMC3618259pubmed: 23497076google scholar: lookup
  23. RECZKO E, MAYR A. [ON THE FINE STRUCTURE OF A VIRUS OF THE HERPES GROUP ISOLATED FROM HORSES (SHORT REPORT)].. Arch Gesamte Virusforsch 1963 Aug 26;13:591-3.
    pubmed: 14078849
  24. Tischer BK, von Einem J, Kaufer B, Osterrieder N. Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli.. Biotechniques 2006 Feb;40(2):191-7.
    pubmed: 16526409doi: 10.2144/000112096google scholar: lookup
  25. Kurtz BM, Singletary LB, Kelly SD, Frampton AR Jr. Equus caballus major histocompatibility complex class I is an entry receptor for equine herpesvirus type 1.. J Virol 2010 Sep;84(18):9027-34.
    doi: 10.1128/JVI.00287-10pmc: PMC2937649pubmed: 20610718google scholar: lookup
  26. Shah MD, Bergeron AL, Dong JF, López JA. Flow cytometric measurement of microparticles: pitfalls and protocol modifications.. Platelets 2008 Aug;19(5):365-72.
    doi: 10.1080/09537100802054107pubmed: 18791943google scholar: lookup
  27. Brooks MB, Divers TJ, Watts AE, Ness SL, Frye AH, Stokol T, Fubini SL. Effects of clopidogrel on the platelet activation response in horses.. Am J Vet Res 2013 Sep;74(9):1212-22.
    doi: 10.2460/ajvr.74.9.1212pubmed: 23977894google scholar: lookup
  28. Segura D, Monreal L, Espada Y, Pastor J, Mayós I, Homedes J. Assessment of a platelet function analyser in horses: reference range and influence of a platelet aggregation inhibitor.. Vet J 2005 Jul;170(1):108-12.
    pubmed: 15993794doi: 10.1016/j.tvjl.2004.05.013google scholar: lookup
  29. Sutherland MR, Raynor CM, Leenknegt H, Wright JF, Pryzdial EL. Coagulation initiated on herpesviruses.. Proc Natl Acad Sci U S A 1997 Dec 9;94(25):13510-4.
    pmc: PMC28336pubmed: 9391056doi: 10.1073/pnas.94.25.13510google scholar: lookup
  30. Gershom ES, Sutherland MR, Lollar P, Pryzdial EL. Involvement of the contact phase and intrinsic pathway in herpes simplex virus-initiated plasma coagulation.. J Thromb Haemost 2010 May;8(5):1037-43.
    doi: 10.1111/j.1538-7836.2010.03789.xpubmed: 20128864google scholar: lookup
  31. Sutherland MR, Friedman HM, Pryzdial EL. Herpes simplex virus type 1-encoded glycoprotein C enhances coagulation factor VIIa activity on the virus.. Thromb Haemost 2004 Nov;92(5):947-55.
    pubmed: 15543320doi: 10.1160/TH04-04-0242google scholar: lookup
  32. Sutherland MR, Ruf W, Pryzdial EL. Tissue factor and glycoprotein C on herpes simplex virus type 1 are protease-activated receptor 2 cofactors that enhance infection.. Blood 2012 Apr 12;119(15):3638-45.
    doi: 10.1182/blood-2011-08-376814pubmed: 22374699google scholar: lookup
  33. Hirni H, Lazary S, Gerber H. Serological and genetic study of the ELA W21 specificity.. Anim Genet 1988;19(4):391-4.
    pubmed: 2466423doi: 10.1111/j.1365-2052.1988.tb00830.xgoogle scholar: lookup
  34. Osterrieder N. Construction and characterization of an equine herpesvirus 1 glycoprotein C negative mutant.. Virus Res 1999 Feb;59(2):165-77.
    pubmed: 10082388doi: 10.1016/s0168-1702(98)00134-8google scholar: lookup
  35. Kim SK, Jang HK, Albrecht RA, Derbigny WA, Zhang Y, O'Callaghan DJ. Interaction of the equine herpesvirus 1 EICP0 protein with the immediate-early (IE) protein, TFIIB, and TBP may mediate the antagonism between the IE and EICP0 proteins.. J Virol 2003 Feb;77(4):2675-85.
    pmc: PMC141080pubmed: 12552007doi: 10.1128/jvi.77.4.2675-2685.2003google scholar: lookup
  36. Ma G, Feineis S, Osterrieder N, Van de Walle GR. Identification and characterization of equine herpesvirus type 1 pUL56 and its role in virus-induced downregulation of major histocompatibility complex class I.. J Virol 2012 Apr;86(7):3554-63.
    doi: 10.1128/JVI.06994-11pmc: PMC3302497pubmed: 22278226google scholar: lookup
  37. Akhtar J, Shukla D. Viral entry mechanisms: cellular and viral mediators of herpes simplex virus entry.. FEBS J 2009 Dec;276(24):7228-36.
    doi: 10.1111/j.1742-4658.2009.07402.xpmc: PMC2801626pubmed: 19878306google scholar: lookup
  38. Morizono K, Chen IS. Role of phosphatidylserine receptors in enveloped virus infection.. J Virol 2014 Apr;88(8):4275-90.
    doi: 10.1128/JVI.03287-13pmc: PMC3993771pubmed: 24478428google scholar: lookup
  39. Pryzdial EL, Wright JF. Prothrombinase assembly on an enveloped virus: evidence that the cytomegalovirus surface contains procoagulant phospholipid.. Blood 1994 Dec 1;84(11):3749-57.
    pubmed: 7949131
  40. Wang J, Zhang W, Nardi MA, Li Z. HIV-1 Tat-induced platelet activation and release of CD154 contribute to HIV-1-associated autoimmune thrombocytopenia.. J Thromb Haemost 2011 Mar;9(3):562-73.
    doi: 10.1111/j.1538-7836.2010.04168.xpmc: PMC3050111pubmed: 21143381google scholar: lookup
  41. Choi W, Karim ZA, Whiteheart SW. Protein expression in platelets from six species that differ in their open canalicular system.. Platelets 2010;21(3):167-75.
    doi: 10.3109/09537101003611385pmc: PMC3982968pubmed: 20196629google scholar: lookup
  42. Othman M, Labelle A, Mazzetti I, Elbatarny HS, Lillicrap D. Adenovirus-induced thrombocytopenia: the role of von Willebrand factor and P-selectin in mediating accelerated platelet clearance.. Blood 2007 Apr 1;109(7):2832-9.
    pubmed: 17148587doi: 10.1182/blood-2006-06-032524google scholar: lookup
  43. Alonzo MT, Lacuesta TL, Dimaano EM, Kurosu T, Suarez LA, Mapua CA, Akeda Y, Matias RR, Kuter DJ, Nagata S, Natividad FF, Oishi K. Platelet apoptosis and apoptotic platelet clearance by macrophages in secondary dengue virus infections.. J Infect Dis 2012 Apr 15;205(8):1321-9.
    doi: 10.1093/infdis/jis180pubmed: 22383677google scholar: lookup
  44. Passacquale G, Vamadevan P, Pereira L, Hamid C, Corrigall V, Ferro A. Monocyte-platelet interaction induces a pro-inflammatory phenotype in circulating monocytes.. PLoS One 2011;6(10):e25595.
    doi: 10.1371/journal.pone.0025595pmc: PMC3192052pubmed: 22022418google scholar: lookup
  45. Hottz ED, Lopes JF, Freitas C, Valls-de-Souza R, Oliveira MF, Bozza MT, Da Poian AT, Weyrich AS, Zimmerman GA, Bozza FA, Bozza PT. Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation.. Blood 2013 Nov 14;122(20):3405-14.
    doi: 10.1182/blood-2013-05-504449pmc: PMC3829114pubmed: 24009231google scholar: lookup

Citations

This article has been cited 11 times.
  1. Theuerkauf K, Obach-Schröck C, Staszyk C, Moritz A, Roscher KA. Activated platelets and platelet-leukocyte aggregates in the equine systemic inflammatory response syndrome.. J Vet Diagn Invest 2022 May;34(3):448-457.
    doi: 10.1177/10406387221077969pubmed: 35168432google scholar: lookup
  2. Perrin KL, Kristensen AT, Bertelsen MF, Denk D. Retrospective review of 27 European cases of fatal elephant endotheliotropic herpesvirus-haemorrhagic disease reveals evidence of disseminated intravascular coagulation.. Sci Rep 2021 Jul 8;11(1):14173.
    doi: 10.1038/s41598-021-93478-0pubmed: 34238966google 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. Stokol T, Yeo WM, Burnett D, DeAngelis N, Huang T, Osterrieder N, Catalfamo J. Correction: Equid Herpesvirus Type 1 Activates Platelets.. PLoS One 2020;15(8):e0237679.
    doi: 10.1371/journal.pone.0237679pubmed: 32813690google scholar: lookup
  6. Kamel M, Pavulraj S, Osterrieder K, Azab W. EHV-1 Pathogenesis: Current in vitro Models and Future Perspectives.. Front Vet Sci 2019;6:251.
    doi: 10.3389/fvets.2019.00251pubmed: 31417917google scholar: lookup
  7. Serpa PBS, Brooks MB, Divers T, Ness S, Birschmann I, Papich MG, Stokol T. Pharmacokinetics and Pharmacodynamics of an Oral Formulation of Apixaban in Horses After Oral and Intravenous Administration.. Front Vet Sci 2018;5:304.
    doi: 10.3389/fvets.2018.00304pubmed: 30564584google scholar: lookup
  8. Stokol T, Serpa PBS, Brooks MB, Divers T, Ness S. Subcutaneous Administration of Low-Molecular-Weight Heparin to Horses Inhibits Ex Vivo Equine Herpesvirus Type 1-Induced Platelet Activation.. Front Vet Sci 2018;5:106.
    doi: 10.3389/fvets.2018.00106pubmed: 29892605google scholar: lookup
  9. Górski A, Międzybrodzki R, Jończyk-Matysiak E, Weber-Dąbrowska B, Bagińska N, Borysowski J. Perspectives of Phage-Eukaryotic Cell Interactions to Control Epstein-Barr Virus Infections.. Front Microbiol 2018;9:630.
    doi: 10.3389/fmicb.2018.00630pubmed: 29666617google scholar: lookup
  10. 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.
    doi: 10.3389/fvets.2017.00211pubmed: 29312962google scholar: lookup
  11. Stokol T, Serpa PBS, Zahid MN, Brooks MB. Unfractionated and Low-Molecular-Weight Heparin and the Phosphodiesterase Inhibitors, IBMX and Cilostazol, Block Ex Vivo Equid Herpesvirus Type-1-Induced Platelet Activation.. Front Vet Sci 2016;3:99.
    doi: 10.3389/fvets.2016.00099pubmed: 27909693google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.