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Home / Equine Research Bank / J Virol / An Alphaherpesvirus Exploits Antimicrobial β-Defensins...
Journal of virology2020; 94(8); e01676-19; doi: 10.1128/JVI.01676-19

An Alphaherpesvirus Exploits Antimicrobial β-Defensins To Initiate Respiratory Tract Infection.

Abstract: β-Defensins protect the respiratory tract against the myriad of microbial pathogens entering the airways with each breath. However, this potentially hostile environment is known to serve as a portal of entry for herpesviruses. The lack of suitable respiratory model systems has precluded understanding of how herpesvirus virions overcome the abundant mucosal β-defensins during host invasion. We demonstrate how a central alphaherpesvirus, equine herpesvirus type 1 (EHV1), actually exploits β-defensins to invade its host and initiate viral spread. The equine β-defensins (eBDs) eBD1, -2, and -3 were produced and secreted along the upper respiratory tract. Despite the marked antimicrobial action of eBD2 and -3 against many bacterial and viral pathogens, EHV1 virions were resistant to eBDs through the action of the viral glycoprotein M envelope protein. Pretreatment of EHV1 virions with eBD2 and -3 increased the subsequent infection of rabbit kidney (RK13) cells, which was dependent on viral N-linked glycans. eBD2 and -3 also caused the aggregation of EHV1 virions on the cell surface of RK13 cells. Pretreatment of primary equine respiratory epithelial cells (EREC) with eBD1, -2, and -3 resulted in increased EHV1 virion binding to and infection of these cells. EHV1-infected EREC, in turn, showed an increased production of eBD2 and -3 compared to that seen in mock- and influenza virus-infected EREC. In addition, these eBDs attracted leukocytes, which are essential for EHV1 dissemination and which serve as latent infection reservoirs. These novel mechanisms provide new insights into herpesvirus respiratory tract infection and pathogenesis. How herpesviruses circumvent mucosal defenses to promote infection of new hosts through the respiratory tract remains unknown due to a lack of host-specific model systems. We used the alphaherpesvirus equine herpesvirus type 1 (EHV1) and equine respiratory tissues to decipher this key event in general alphaherpesvirus pathogenesis. In contrast to several respiratory viruses and bacteria, EHV1 resisted potent antimicrobial equine β-defensins (eBDs) eBD2 and eBD3 by the action of glycoprotein M. Instead, eBD2 and -3 facilitated EHV1 particle aggregation and infection of rabbit kidney (RK13) cells. In addition, virion binding to and subsequent infection of respiratory epithelial cells were increased upon preincubation of these cells with eBD1, -2, and -3. Infected cells synthesized eBD2 and -3, promoting further host cell invasion by EHV1. Finally, eBD1, -2, and -3 recruited leukocytes, which are well-known EHV1 dissemination and latency vessels. The exploitation of host innate defenses by herpesviruses during the early phase of host colonization indicates that highly specialized strategies have developed during host-pathogen coevolution.
Copyright © 2020 Van Cleemput et al.
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Publication Date: 2020-03-31 PubMed ID: 31996426PubMed Central: PMC7108845DOI: 10.1128/JVI.01676-19Google Scholar: Lookup
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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.

This research article explores how the equine herpesvirus type 1 (EHV1) utilizes β-defensins, compounds that ordinarily protect the respiratory tract against microbial pathogens, to initiate the infection in hosts. Rather than being hindered by these antimicrobial substances, EHV1 uses them to promote the binding of virus particles to host cells.

Research Methodology and Findings

  • Scientists carried out this study by observing the behavior of EHV1 in the presence of equine β-defensins (eBDs) eBD1, -2, and -3. Under normal circumstances, these proteins perform antimicrobial actions, warding off many bacterial and viral pathogens.
  • Unexpectedly, though, EHV1 virions were found to be resistant to eBDs, courtesy of the action of a specific viral protein, the glycoprotein M envelope protein.
  • After pre-treating EHV1 virions with eBD2 and -3, an increased infection rate was observed in rabbit kidney (RK13) cells. This observation suggested that the presence of the equine β-defensins somehow promoted the virus’s ability to infect host cells.
  • Through further observation, eBD2 and -3 were seen to lead to the aggregation of EHV1 virions on the surface of RK13 cells. Similarly, pre-treating primary equine respiratory epithelial cells (EREC) with eBD1, -2, and -3 also resulted in an increase in EHV1 virion binding and subsequent infection.
  • ERECs infected by EHV1 then showed an increased production of eBD2 and -3, suggesting a self-propagating cycle where the virus induces production of the very substances that help its propagation.
  • Finally, these equine β-defensins also attracted leukocytes, white blood cells essential for EHV1 dissemination and hiding places for latent infections. This event presents another means through which the virus is able to spread through its host.

Significance of the Findings

  • The discoveries made in this study provide vital insights into how herpesviruses may be capable of bypassing the body’s natural defenses to infect new hosts through the respiratory tract.
  • Understanding that the EHV1 virus is not only resistant to equine β-defensins eBD2 and eBD3, but can actually utilize these compounds to promote infection, opens up new fronts for the development of antiviral therapies.
  • The study also highlights the intricate strategies developed by pathogens during their coevolution with hosts, pointing to a need for further research to fully comprehend these mechanisms and utilize them in combating various herpesvirus infections.

Cite This Article

APA
Van Cleemput J, Poelaert KCK, Laval K, Vanderheijden N, Dhaenens M, Daled S, Boyen F, Pasmans F, Nauwynck HJ. (2020). An Alphaherpesvirus Exploits Antimicrobial β-Defensins To Initiate Respiratory Tract Infection. J Virol, 94(8), e01676-19. https://doi.org/10.1128/JVI.01676-19

Publication

Journal of virology
ISSN: 1098-5514
NlmUniqueID: 0113724
Country: United States
Language: English
Volume: 94
Issue: 8
PII: e01676-19

Researcher Affiliations

Van Cleemput, Jolien
  • Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
  • Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA.
Poelaert, Katrien C K
  • Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
  • Fox Chase Cancer Center, Philadelphia, Pennsylvania, USA.
Laval, Kathlyn
  • Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA.
Vanderheijden, Nathalie
  • Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Dhaenens, Maarten
  • Department of Pharmaceutics, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium.
Daled, Simon
  • Department of Pharmaceutics, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium.
Boyen, Filip
  • Department of Pathology, Bacteriology and Poultry Diseases, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Pasmans, Frank
  • Department of Pathology, Bacteriology and Poultry Diseases, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Nauwynck, Hans J
  • Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium hans.nauwynck@ugent.be.

MeSH Terms

  • Alphaherpesvirinae / physiology
  • Animals
  • Anti-Infective Agents / adverse effects
  • Anti-Infective Agents / pharmacology
  • Cell Line
  • Epithelial Cells / virology
  • Herpesviridae Infections / virology
  • Herpesvirus 1, Equid
  • Horse Diseases / virology
  • Horses
  • Host-Pathogen Interactions / physiology
  • Immune Evasion
  • Rabbits
  • Respiratory Tract Infections / drug therapy
  • Respiratory Tract Infections / immunology
  • Respiratory Tract Infections / virology
  • Viral Envelope Proteins
  • beta-Defensins / adverse effects
  • beta-Defensins / pharmacology

References

This article includes 70 references
  1. Karlin S, Mocarski ES, Schachtel GA. Molecular evolution of herpesviruses: genomic and protein sequence comparisons.. J Virol 1994 Mar;68(3):1886-902.
    doi: 10.1128/JVI.68.3.1886-1902.1994pmc: PMC236651pubmed: 8107249google scholar: lookup
  2. Grinde B. Herpesviruses: latency and reactivation - viral strategies and host response.. J Oral Microbiol 2013 Oct 25;5.
    doi: 10.3402/jom.v5i0.22766pmc: PMC3809354pubmed: 24167660google scholar: lookup
  3. Tan CS, Frederico B, Stevenson PG. Herpesvirus delivery to the murine respiratory tract.. J Virol Methods 2014 Sep;206:105-14.
    doi: 10.1016/j.jviromet.2014.06.003pubmed: 24928692google scholar: lookup
  4. Zerboni L, Sen N, Oliver SL, Arvin AM. Molecular mechanisms of varicella zoster virus pathogenesis.. Nat Rev Microbiol 2014 Mar;12(3):197-210.
    doi: 10.1038/nrmicro3215pmc: PMC4066823pubmed: 24509782google scholar: lookup
  5. Glorieux S, Bachert C, Favoreel HW, Vandekerckhove AP, Steukers L, Rekecki A, Van den Broeck W, Goossens J, Croubels S, Clayton RF, Nauwynck HJ. Herpes simplex virus type 1 penetrates the basement membrane in human nasal respiratory mucosa.. PLoS One 2011;6(7):e22160.
    doi: 10.1371/journal.pone.0022160pmc: PMC3137608pubmed: 21789229google scholar: lookup
  6. Ganz T. Defensins: antimicrobial peptides of innate immunity.. Nat Rev Immunol 2003 Sep;3(9):710-20.
    doi: 10.1038/nri1180pubmed: 12949495google scholar: lookup
  7. White SH, Wimley WC, Selsted ME. Structure, function, and membrane integration of defensins.. Curr Opin Struct Biol 1995 Aug;5(4):521-7.
    doi: 10.1016/0959-440x(95)80038-7pubmed: 8528769google scholar: lookup
  8. Pazgier M, Hoover DM, Yang D, Lu W, Lubkowski J. Human beta-defensins.. Cell Mol Life Sci 2006 Jun;63(11):1294-313.
    doi: 10.1007/s00018-005-5540-2pubmed: 16710608google scholar: lookup
  9. Yang D, Biragyn A, Kwak LW, Oppenheim JJ. Mammalian defensins in immunity: more than just microbicidal.. Trends Immunol 2002 Jun;23(6):291-6.
    doi: 10.1016/s1471-4906(02)02246-9pubmed: 12072367google scholar: lookup
  10. Meade KG, O'Farrelly C. β-Defensins: Farming the Microbiome for Homeostasis and Health.. Front Immunol 2018;9:3072.
    doi: 10.3389/fimmu.2018.03072pmc: PMC6362941pubmed: 30761155google scholar: lookup
  11. Doss M, White MR, Tecle T, Gantz D, Crouch EC, Jung G, Ruchala P, Waring AJ, Lehrer RI, Hartshorn KL. Interactions of alpha-, beta-, and theta-defensins with influenza A virus and surfactant protein D.. J Immunol 2009 Jun 15;182(12):7878-87.
    doi: 10.4049/jimmunol.0804049pubmed: 19494312google scholar: lookup
  12. Kota S, Sabbah A, Chang TH, Harnack R, Xiang Y, Meng X, Bose S. Role of human beta-defensin-2 during tumor necrosis factor-alpha/NF-kappaB-mediated innate antiviral response against human respiratory syncytial virus.. J Biol Chem 2008 Aug 15;283(33):22417-29.
    doi: 10.1074/jbc.M710415200pmc: PMC2504899pubmed: 18567888google scholar: lookup
  13. Wang W, Owen SM, Rudolph DL, Cole AM, Hong T, Waring AJ, Lal RB, Lehrer RI. Activity of alpha- and theta-defensins against primary isolates of HIV-1.. J Immunol 2004 Jul 1;173(1):515-20.
    doi: 10.4049/jimmunol.173.1.515pubmed: 15210812google scholar: lookup
  14. Dhople V, Krukemeyer A, Ramamoorthy A. The human beta-defensin-3, an antibacterial peptide with multiple biological functions.. Biochim Biophys Acta 2006 Sep;1758(9):1499-512.
    doi: 10.1016/j.bbamem.2006.07.007pubmed: 16978580google scholar: lookup
  15. Lehrer RI, Barton A, Daher KA, Harwig SS, Ganz T, Selsted ME. Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity.. J Clin Invest 1989 Aug;84(2):553-61.
    doi: 10.1172/JCI114198pmc: PMC548915pubmed: 2668334google scholar: lookup
  16. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A, Chertov O, Shirakawa AK, Farber JM, Segal DM, Oppenheim JJ, Kwak LW. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2.. Science 2002 Nov 1;298(5595):1025-9.
    doi: 10.1126/science.1075565pubmed: 12411706google scholar: lookup
  17. Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, Anderson M, Schröder JM, Wang JM, Howard OM, Oppenheim JJ. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6.. Science 1999 Oct 15;286(5439):525-8.
    doi: 10.1126/science.286.5439.525pubmed: 10521347google scholar: lookup
  18. Shivkumar M, Milho R, May JS, Nicoll MP, Efstathiou S, Stevenson PG. Herpes simplex virus 1 targets the murine olfactory neuroepithelium for host entry.. J Virol 2013 Oct;87(19):10477-88.
    doi: 10.1128/JVI.01748-13pmc: PMC3807398pubmed: 23903843google scholar: lookup
  19. Steiner I, Benninger F. Manifestations of Herpes Virus Infections in the Nervous System.. Neurol Clin 2018 Nov;36(4):725-738.
    doi: 10.1016/j.ncl.2018.06.005pubmed: 30366551google scholar: lookup
  20. Ghosh D, Porter E, Shen B, Lee SK, Wilk D, Drazba J, Yadav SP, Crabb JW, Ganz T, Bevins CL. Paneth cell trypsin is the processing enzyme for human defensin-5.. Nat Immunol 2002 Jun;3(6):583-90.
    doi: 10.1038/ni797pubmed: 12021776google scholar: lookup
  21. Harder J, Bartels J, Christophers E, Schroder JM. Isolation and characterization of human beta -defensin-3, a novel human inducible peptide antibiotic.. J Biol Chem 2001 Feb 23;276(8):5707-13.
    doi: 10.1074/jbc.M008557200pubmed: 11085990google scholar: lookup
  22. Bals R, Wang X, Wu Z, Freeman T, Bafna V, Zasloff M, Wilson JM. Human beta-defensin 2 is a salt-sensitive peptide antibiotic expressed in human lung.. J Clin Invest 1998 Sep 1;102(5):874-80.
    doi: 10.1172/JCI2410pmc: PMC508952pubmed: 9727055google scholar: lookup
  23. Schroeder BO, Wu Z, Nuding S, Groscurth S, Marcinowski M, Beisner J, Buchner J, Schaller M, Stange EF, Wehkamp J. Reduction of disulphide bonds unmasks potent antimicrobial activity of human β-defensin 1.. Nature 2011 Jan 20;469(7330):419-23.
    doi: 10.1038/nature09674pubmed: 21248850google scholar: lookup
  24. Hazrati E, Galen B, Lu W, Wang W, Ouyang Y, Keller MJ, Lehrer RI, Herold BC. Human alpha- and beta-defensins block multiple steps in herpes simplex virus infection.. J Immunol 2006 Dec 15;177(12):8658-66.
    doi: 10.4049/jimmunol.177.12.8658pubmed: 17142766google scholar: lookup
  25. Quiñones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, Rangel HR, Marotta ML, Mirza M, Jiang B, Kiser P, Medvik K, Sieg SF, Weinberg A. Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication.. AIDS 2003 Nov 7;17(16):F39-48.
    doi: 10.1097/00002030-200311070-00001pubmed: 14571200google scholar: lookup
  26. Van Cleemput J, Poelaert KCK, Laval K, Maes R, Hussey GS, Van den Broeck W, Nauwynck HJ. Access to a main alphaherpesvirus receptor, located basolaterally in the respiratory epithelium, is masked by intercellular junctions.. Sci Rep 2017 Nov 30;7(1):16656.
    doi: 10.1038/s41598-017-16804-5pmc: PMC5709510pubmed: 29192251google scholar: lookup
  27. 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.
    doi: 10.1016/j.vetmic.2005.11.048pubmed: 16387454google scholar: lookup
  28. Wilson SS, Wiens ME, Smith JG. Antiviral mechanisms of human defensins.. J Mol Biol 2013 Dec 13;425(24):4965-80.
    doi: 10.1016/j.jmb.2013.09.038pmc: PMC3842434pubmed: 24095897google scholar: lookup
  29. Tregidgo L, Cane J, Bafadhel M. S103 Non-typeable Haemophilus influenzae downregulates release of beta-defensin-1 from bronchial epithelial cells.. Thorax 71:A61.
    doi: 10.1136/thoraxjnl-2016-209333.109google scholar: lookup
  30. Lee SH, Kim JE, Lim HH, Lee HM, Choi JO. Antimicrobial defensin peptides of the human nasal mucosa.. Ann Otol Rhinol Laryngol 2002 Feb;111(2):135-41.
    doi: 10.1177/000348940211100205pubmed: 11860065google scholar: lookup
  31. Starner TD, Agerberth B, Gudmundsson GH, McCray PB Jr. Expression and activity of beta-defensins and LL-37 in the developing human lung.. J Immunol 2005 Feb 1;174(3):1608-15.
    doi: 10.4049/jimmunol.174.3.1608pubmed: 15661923google scholar: lookup
  32. Singh PK, Jia HP, Wiles K, Hesselberth J, Liu L, Conway BA, Greenberg EP, Valore EV, Welsh MJ, Ganz T, Tack BF, McCray PB Jr. Production of beta-defensins by human airway epithelia.. Proc Natl Acad Sci U S A 1998 Dec 8;95(25):14961-6.
    doi: 10.1073/pnas.95.25.14961pmc: PMC24558pubmed: 9843998google scholar: lookup
  33. Howell MD, Jones JF, Kisich KO, Streib JE, Gallo RL, Leung DY. Selective killing of vaccinia virus by LL-37: implications for eczema vaccinatum.. J Immunol 2004 Feb 1;172(3):1763-7.
    doi: 10.4049/jimmunol.172.3.1763pubmed: 14734759google scholar: lookup
  34. Raschig J, Mailänder-Sánchez D, Berscheid A, Berger J, Strömstedt AA, Courth LF, Malek NP, Brötz-Oesterhelt H, Wehkamp J. Ubiquitously expressed Human Beta Defensin 1 (hBD1) forms bacteria-entrapping nets in a redox dependent mode of action.. PLoS Pathog 2017 Mar;13(3):e1006261.
    doi: 10.1371/journal.ppat.1006261pmc: PMC5376342pubmed: 28323883google scholar: lookup
  35. Jia HP, Starner T, Ackermann M, Kirby P, Tack BF, McCray PB Jr. Abundant human beta-defensin-1 expression in milk and mammary gland epithelium.. J Pediatr 2001 Jan;138(1):109-12.
    doi: 10.1067/mpd.2001.109375pubmed: 11148522google scholar: lookup
  36. Osterrieder N, Neubauer A, Brandmuller C, Braun B, Kaaden OR, Baines JD. The equine herpesvirus 1 glycoprotein gp21/22a, the herpes simplex virus type 1 gM homolog, is involved in virus penetration and cell-to-cell spread of virions.. J Virol 1996 Jun;70(6):4110-5.
    doi: 10.1128/JVI.70.6.4110-4115.1996pmc: PMC190297pubmed: 8648751google scholar: lookup
  37. Pilling A, Davison AJ, Telford EA, Meredith DM. The equine herpesvirus type 1 glycoprotein homologous to herpes simplex virus type 1 glycoprotein M is a major constituent of the virus particle.. J Gen Virol 1994 Feb;75 ( Pt 2):439-42.
    doi: 10.1099/0022-1317-75-2-439pubmed: 8113768google scholar: lookup
  38. Daher KA, Selsted ME, Lehrer RI. Direct inactivation of viruses by human granulocyte defensins.. J Virol 1986 Dec;60(3):1068-74.
    doi: 10.1128/JVI.60.3.1068-1074.1986pmc: PMC253347pubmed: 3023659google scholar: lookup
  39. Klupp BG, Nixdorf R, Mettenleiter TC. Pseudorabies virus glycoprotein M inhibits membrane fusion.. J Virol 2000 Aug;74(15):6760-8.
    doi: 10.1128/jvi.74.15.6760-6768.2000pmc: PMC112192pubmed: 10888614google scholar: lookup
  40. Rapista A, Ding J, Benito B, Lo YT, Neiditch MB, Lu W, Chang TL. Human defensins 5 and 6 enhance HIV-1 infectivity through promoting HIV attachment.. Retrovirology 2011 Jun 14;8:45.
    doi: 10.1186/1742-4690-8-45pmc: PMC3146398pubmed: 21672195google scholar: lookup
  41. Wilson SS, Bromme BA, Holly MK, Wiens ME, Gounder AP, Sul Y, Smith JG. Alpha-defensin-dependent enhancement of enteric viral infection.. PLoS Pathog 2017 Jun;13(6):e1006446.
    doi: 10.1371/journal.ppat.1006446pmc: PMC5489213pubmed: 28622386google scholar: lookup
  42. Herrera R, Morris M, Rosbe K, Feng Z, Weinberg A, Tugizov S. Human beta-defensins 2 and -3 cointernalize with human immunodeficiency virus via heparan sulfate proteoglycans and reduce infectivity of intracellular virions in tonsil epithelial cells.. Virology 2016 Jan;487:172-87.
    doi: 10.1016/j.virol.2015.09.025pmc: PMC4679645pubmed: 26539799google scholar: lookup
  43. Gounder AP, Wiens ME, Wilson SS, Lu W, Smith JG. Critical determinants of human α-defensin 5 activity against non-enveloped viruses.. J Biol Chem 2012 Jul 13;287(29):24554-62.
    doi: 10.1074/jbc.M112.354068pmc: PMC3397880pubmed: 22637473google scholar: lookup
  44. Wang CH, Chan LW, Johnson RN, Chu DS, Shi J, Schellinger JG, Lieber A, Pun SH. The transduction of Coxsackie and Adenovirus Receptor-negative cells and protection against neutralizing antibodies by HPMA-co-oligolysine copolymer-coated adenovirus.. Biomaterials 2011 Dec;32(35):9536-45.
    doi: 10.1016/j.biomaterials.2011.08.069pmc: PMC3190026pubmed: 21959008google scholar: lookup
  45. Dugan AS, Maginnis MS, Jordan JA, Gasparovic ML, Manley K, Page R, Williams G, Porter E, O'Hara BA, Atwood WJ. Human alpha-defensins inhibit BK virus infection by aggregating virions and blocking binding to host cells.. J Biol Chem 2008 Nov 7;283(45):31125-32.
    doi: 10.1074/jbc.M805902200pmc: PMC2576552pubmed: 18782756google scholar: lookup
  46. Fujii G, Selsted ME, Eisenberg D. Defensins promote fusion and lysis of negatively charged membranes.. Protein Sci 1993 Aug;2(8):1301-12.
    doi: 10.1002/pro.5560020813pmc: PMC2142441pubmed: 8401215google scholar: lookup
  47. 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
  48. 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.
    doi: 10.1016/j.vetmic.2009.10.015pubmed: 19926232google scholar: lookup
  49. Tam JP, Wu CR, Liu W, Zhang JW. Disulfide bond formation in peptides by dimethyl sulfoxide. Scope and applications.. J Am Chem Soc 113:6657–6662.
    doi: 10.1021/ja00017a044google scholar: lookup
  50. Helm D, Vissers JP, Hughes CJ, Hahne H, Ruprecht B, Pachl F, Grzyb A, Richardson K, Wildgoose J, Maier SK, Marx H, Wilhelm M, Becher I, Lemeer S, Bantscheff M, Langridge JI, Kuster B. Ion mobility tandem mass spectrometry enhances performance of bottom-up proteomics.. Mol Cell Proteomics 2014 Dec;13(12):3709-15.
    doi: 10.1074/mcp.M114.041038pmc: PMC4256517pubmed: 25106551google scholar: lookup
  51. Schägger H. Tricine-SDS-PAGE.. Nat Protoc 2006;1(1):16-22.
    doi: 10.1038/nprot.2006.4pubmed: 17406207google scholar: lookup
  52. Jiang S, Liu S, Zhao C, Wu C. Developing protocols of tricine-SDS-PAGE for separation of polypeptides in the mass range 1–30 kDa with minigel electrophoresis system.. Int J Electrochem Sci 11:640–649.
  53. Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes.. J Biol Chem 1987 Jul 25;262(21):10035-8.
    pubmed: 3611052
  54. 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.
    doi: 10.1099/vir.0.18864-0pubmed: 12533704google scholar: lookup
  55. 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.
    doi: 10.1016/j.vetimm.2010.12.008pubmed: 21292331google scholar: lookup
  56. Kuhns DB, Priel DAL, Chu J, Zarember KA. Isolation and Functional Analysis of Human Neutrophils.. Curr Protoc Immunol 2015 Nov 2;111:7.23.1-7.23.16.
    doi: 10.1002/0471142735.im0723s111pmc: PMC4668800pubmed: 26528633google scholar: lookup
  57. Van Cleemput J, Poelaert KCK, Laval K, Nauwynck HJ. Unravelling the first key steps in equine herpesvirus type 5 (EHV5) pathogenesis using ex vivo and in vitro equine models.. Vet Res 2019 Feb 18;50(1):13.
    doi: 10.1186/s13567-019-0630-6pmc: PMC6380010pubmed: 30777128google scholar: lookup
  58. van der Meulen K, Vercauteren G, Nauwynck H, Pensaert M. A local epidemic of equine herpesvirus 1-induced neurological disorders in Belgium.. Vlaams Diergen Tijds 72:366–372.
  59. Mayr A, Pette J, Petzoldt K, Wagener K. [Studies on the development of a live vaccine against rhinopneumonitis (mare abortion) of horses].. Zentralbl Veterinarmed B 1968 Apr;15(3):406-18.
    doi: 10.1111/j.1439-0450.1968.tb00065.xpubmed: 5692868google scholar: lookup
  60. Rudolph J, O'Callaghan DJ, Osterrieder N. Cloning of the genomes of equine herpesvirus type 1 (EHV-1) strains KyA and racL11 as bacterial artificial chromosomes (BAC).. J Vet Med B Infect Dis Vet Public Health 2002 Feb;49(1):31-6.
    doi: 10.1046/j.1439-0450.2002.00534.xpubmed: 11911590google scholar: lookup
  61. Vairo S, Vandekerckhove A, Steukers L, Glorieux S, Van den Broeck W, Nauwynck H. Clinical and virological outcome of an infection with the Belgian equine arteritis virus strain 08P178.. Vet Microbiol 2012 Jun 15;157(3-4):333-44.
    doi: 10.1016/j.vetmic.2012.01.014pubmed: 22306037google scholar: lookup
  62. Laval K, Favoreel HW, Van Cleemput J, Poelaert KCK, Brown IK, Verhasselt B, Nauwynck HJ. Entry of equid herpesvirus 1 into CD172a+ monocytic cells.. J Gen Virol 2016 Mar;97(3):733-746.
    doi: 10.1099/jgv.0.000375pubmed: 26684016google scholar: lookup
  63. Davis EG, Sang Y, Blecha F. Equine beta-defensin-1: full-length cDNA sequence and tissue expression.. Vet Immunol Immunopathol 2004 May;99(1-2):127-32.
    doi: 10.1016/j.vetimm.2003.12.010pubmed: 15113660google scholar: lookup
  64. Marth CD, Young ND, Glenton LY, Noden DM, Browning GF, Krekeler N. Deep sequencing of the uterine immune response to bacteria during the equine oestrous cycle.. BMC Genomics 2015 Nov 14;16:934.
    doi: 10.1186/s12864-015-2139-3pmc: PMC4647707pubmed: 26572250google scholar: lookup
  65. Nina Hornickel I, Kacza J, Schnapper A, Beyerbach M, Schoennagel B, Seeger J, Meyer W. Demonstration of substances of innate immunity in the esophageal epithelium of domesticated mammals. Part I--Methods and evaluation of comparative fixation.. Acta Histochem 2011 Feb;113(2):163-74.
    doi: 10.1016/j.acthis.2009.09.009pubmed: 19850328google scholar: lookup
  66. Schoniger S, Grafe H, Schoon HA. Beta-defensin is a component of the endometrial immune defence in the mare.. Pferdeheilkunde 29:335–346.
    doi: 10.21836/PEM20130307google scholar: lookup
  67. Yasui T, Fukui K, Nara T, Habata I, Meyer W, Tsukise A. Immunocytochemical localization of lysozyme and beta-defensin in the apocrine glands of the equine scrotum.. Arch Dermatol Res 2007 Oct;299(8):393-7.
    doi: 10.1007/s00403-007-0766-5pubmed: 17639436google scholar: lookup
  68. Yasui T, Tsukise A, Fukui K, Kuwahara Y, Meyer W. Aspects of glycoconjugate production and lysozyme- and defensins-expression of the ceruminous glands of the horse (Equus przewalskii f. dom.).. Eur J Morphol 2005 Jul;42(3):127-34.
    doi: 10.1080/09243860500202507pubmed: 16393749google scholar: lookup
  69. Looft C, Paul S, Philipp U, Regenhard P, Kuiper H, Distl O, Chowdhary BP, Leeb T. Sequence analysis of a 212 kb defensin gene cluster on ECA 27q17.. Gene 2006 Jul 19;376(2):192-8.
    doi: 10.1016/j.gene.2006.03.006pubmed: 16723195google scholar: lookup
  70. Bruhn O, Grötzinger J, Cascorbi I, Jung S. Antimicrobial peptides and proteins of the horse--insights into a well-armed organism.. Vet Res 2011 Sep 2;42(1):98.
    doi: 10.1186/1297-9716-42-98pmc: PMC3179947pubmed: 21888650google scholar: lookup

Citations

This article has been cited 7 times.
  1. Li C, Wang M, Cheng A, Wu Y, Tian B, Yang Q, Gao Q, Sun D, Zhang S, Ou X, He Y, Huang J, Zhao X, Chen S, Zhu D, Liu M, Jia R. N-Linked Glycosylation and Expression of Duck Plague Virus pUL10 Promoted by pUL49.5.. Microbiol Spectr 2023 Aug 17;11(4):e0162523.
    doi: 10.1128/spectrum.01625-23pubmed: 37378543google scholar: lookup
  2. Pei L, Liu K, Wei W, Su H, Li F, Feng Y, Wang D, Li X, Hou Y, Cao G. Equus β-Defensin-1 Regulates Innate IMMUNE Response in S. aureus-Infected Mouse Monocyte Macrophage.. Animals (Basel) 2022 Oct 27;12(21).
    doi: 10.3390/ani12212958pubmed: 36359082google scholar: lookup
  3. Zhang Z, Chen D, Lu X, Zhao R, Chen Z, Li M, Xu T, Mao Y, Yang Y, Yang Z. Directed Expression of Tracheal Antimicrobial Peptide as a Treatment for Bovine-Associated Staphylococcus Aureus-Induced Mastitis in Mice.. Front Vet Sci 2021;8:700930.
    doi: 10.3389/fvets.2021.700930pubmed: 34671659google scholar: lookup
  4. Solanki SS, Singh P, Kashyap P, Sansi MS, Ali SA. Promising role of defensins peptides as therapeutics to combat against viral infection.. Microb Pathog 2021 Jun;155:104930.
    doi: 10.1016/j.micpath.2021.104930pubmed: 33933603google scholar: lookup
  5. 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
  6. Li C, Wang M, Cheng A, Jia R, Yang Q, Wu Y, Zhu D, Zhao X, Chen S, Liu M, Zhang S, Ou X, Mao S, Gao Q, Sun D, Wen X, Tian B. The Roles of Envelope Glycoprotein M in the Life Cycle of Some Alphaherpesviruses.. Front Microbiol 2021;12:631523.
    doi: 10.3389/fmicb.2021.631523pubmed: 33679658google scholar: lookup
  7. Xu D, Lu W. Defensins: A Double-Edged Sword in Host Immunity.. Front Immunol 2020;11:764.
    doi: 10.3389/fimmu.2020.00764pubmed: 32457744google scholar: lookup
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