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Scientific reports2017; 7(1); 16656; doi: 10.1038/s41598-017-16804-5

Access to a main alphaherpesvirus receptor, located basolaterally in the respiratory epithelium, is masked by intercellular junctions.

Abstract: The respiratory epithelium of humans and animals is frequently exposed to alphaherpesviruses, originating from either external exposure or reactivation from latency. To date, the polarity of alphaherpesvirus infection in the respiratory epithelium and the role of respiratory epithelial integrity herein has not been studied. Equine herpesvirus type 1 (EHV1), a well-known member of the alphaherpesvirus family, was used to infect equine respiratory mucosal explants and primary equine respiratory epithelial cells (EREC), grown at the air-liquid interface. EHV1 binding to and infection of mucosal explants was greatly enhanced upon destruction of the respiratory epithelium integrity with EGTA or N-acetylcysteine. EHV1 preferentially bound to and entered EREC at basolateral cell surfaces. Restriction of infection via apical inoculation was overcome by disruption of intercellular junctions. Finally, basolateral but not apical EHV1 infection of EREC was dependent on cellular N-linked glycans. Overall, our findings demonstrate that integrity of the respiratory epithelium is crucial in the host's innate defence against primary alphaherpesvirus infections. In addition, by targeting a basolaterally located receptor in the respiratory epithelium, alphaherpesviruses have generated a strategy to efficiently escape from host defence mechanisms during reactivation from latency.
Publication Date: 2017-11-30 PubMed ID: 29192251PubMed Central: PMC5709510DOI: 10.1038/s41598-017-16804-5Google Scholar: Lookup
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  • 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 investigates how the integrity of the respiratory epithelium, a barrier of tissue lining the respiratory tract, affects infection by alphaherpesviruses, using the example of equine herpesvirus type 1 (EHV1). The study indicates that infection is more efficient when the respiratory epithelium is disrupted and that the virus specifically targets a receptor located on the side of cells facing away from the lumen of the respiratory tract to bypass host defense mechanisms.

Methodology and Key Findings

  • The researchers used equine herpesvirus type 1(EHV1) to infect equine respiratory mucosal explants and primary equine respiratory epithelial cells (ERECs), which were grown at the air-liquid interface.
  • They observed an increased EHV1 binding to and infection of the explants upon the destruction of respiratory epithelium integrity, achieved through the use of EGTA or N-acetylcysteine.
  • The researchers found that EHV1 preferentially bound to and entered EREC at the basolateral cell surfaces, that is, the side of the epithelial cells facing away from the lumen of the respiratory tract.
  • The access of EHV1 to the cells via the apical surface, facing the lumen, was restricted and could only be overcome by disrupting the intercellular junctions that hold cells together.
  • Additionally, basolateral EHV1 infection of the EREC was dependent on cellular N-linked glycans, but not when the infection occurred apically.

Implication of the Research

  • The findings indicate that the integrity of the respiratory epithelium, the presence of an intact cell barrier, is crucial in defending against primary alphaherpesvirus infections.
  • Alphaherpesviruses have developed a strategy to efficiently escape the host’s defense mechanisms by specifically targeting a receptor located basolaterally in the respiratory epithelium during reactivation from latency.

Conclusion

  • The research contributes to better understanding of the entry mechanisms of alphaherpesviruses, their strategies to evade host defenses and the role of the respiratory epithelia as a barrier in viral infections.
  • The outcomes of the research could potentially help design better therapeutic targets and preventive strategies against alphaherpesvirus infections.

Cite This Article

APA
Van Cleemput J, Poelaert KCK, Laval K, Maes R, Hussey GS, Van den Broeck W, Nauwynck HJ. (2017). Access to a main alphaherpesvirus receptor, located basolaterally in the respiratory epithelium, is masked by intercellular junctions. Sci Rep, 7(1), 16656. https://doi.org/10.1038/s41598-017-16804-5

Publication

ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 7
Issue: 1
Pages: 16656
PII: 16656

Researcher Affiliations

Van Cleemput, Jolien
  • Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium.
Poelaert, Katrien C K
  • Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium.
Laval, Kathlyn
  • Department of Molecular Biology and Princeton Neuroscience Institute, Princeton University, 119 Lewis Thomas Laboratory, Washington Road, Princeton, New Jersey, 08544, USA.
Maes, Roger
  • Department of Pathobiology and Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, 784 Wilson Road, East Lansing, Michigan, 48824, USA.
Hussey, Gisela S
  • Department of Pathobiology and Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, 784 Wilson Road, East Lansing, Michigan, 48824, USA.
Van den Broeck, Wim
  • Department of Morphology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium.
Nauwynck, Hans J
  • Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium. hans.nauwynck@ugent.be.

MeSH Terms

  • Alphaherpesvirinae / physiology
  • Animals
  • Herpesviridae Infections / veterinary
  • Herpesvirus 1, Equid / physiology
  • Horse Diseases / metabolism
  • Horse Diseases / virology
  • Horses
  • Intercellular Junctions / drug effects
  • Intercellular Junctions / metabolism
  • Polysaccharides / metabolism
  • Receptors, Virus / chemistry
  • Receptors, Virus / metabolism
  • Respiratory Mucosa / drug effects
  • Respiratory Mucosa / metabolism
  • Respiratory Mucosa / pathology
  • Respiratory Mucosa / virology
  • Viral Load
  • Virus Replication

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 76 references
  1. Grinde B. Herpesviruses: latency and reactivation - viral strategies and host response.. J Oral Microbiol 2013 Oct 25;5.
    pmc: PMC3809354pubmed: 24167660doi: 10.3402/jom.v5i0.22766google scholar: lookup
  2. Jacquot J, Spilmont C, de Bentzmann S, Dupuit F, Puchelle E. [Structure and secretory functions of the respiratory epithelium].. Arch Int Physiol Biochim Biophys 1992 Jul-Aug;100(4):A41-6.
    doi: 10.3109/13813459209000712pubmed: 1382688google scholar: lookup
  3. Yang X, Forier K, Steukers L, Van Vlierberghe S, Dubruel P, Braeckmans K, Glorieux S, Nauwynck HJ. Immobilization of pseudorabies virus in porcine tracheal respiratory mucus revealed by single particle tracking.. PLoS One 2012;7(12):e51054.
  4. Staehelin LA. Structure and function of intercellular junctions.. Int Rev Cytol 1974;39:191-283.
    doi: 10.1016/S0074-7696(08)60940-7pubmed: 4611943google scholar: lookup
  5. Matter K, Balda MS. Functional analysis of tight junctions.. Methods 2003 Jul;30(3):228-34.
    doi: 10.1016/S1046-2023(03)00029-Xpubmed: 12798137google scholar: lookup
  6. Balda MS, Matter K. Tight junctions as regulators of tissue remodelling.. Curr Opin Cell Biol 2016 Oct;42:94-101.
    doi: 10.1016/j.ceb.2016.05.006pubmed: 27236618google scholar: lookup
  7. Baum B, Georgiou M. Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling.. J Cell Biol 2011 Mar 21;192(6):907-17.
    doi: 10.1083/jcb.201009141pmc: PMC3063136pubmed: 21422226google scholar: lookup
  8. Clayson ET, Compans RW. Entry of simian virus 40 is restricted to apical surfaces of polarized epithelial cells.. Mol Cell Biol 1988 Aug;8(8):3391-6.
    doi: 10.1128/MCB.8.8.3391pmc: PMC363575pubmed: 2850491google scholar: lookup
  9. Zhang L, Peeples ME, Boucher RC, Collins PL, Pickles RJ. Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology.. J Virol 2002 Jun;76(11):5654-66.
  10. Zabner J, Freimuth P, Puga A, Fabrega A, Welsh MJ. Lack of high affinity fiber receptor activity explains the resistance of ciliated airway epithelia to adenovirus infection.. J Clin Invest 1997 Sep 1;100(5):1144-9.
    doi: 10.1172/JCI119625pmc: PMC508289pubmed: 9276731google scholar: lookup
  11. Blank CA, Anderson DA, Beard M, Lemon SM. Infection of polarized cultures of human intestinal epithelial cells with hepatitis A virus: vectorial release of progeny virions through apical cellular membranes.. J Virol 2000 Jul;74(14):6476-84.
  12. Chu JJH, Ng ML. Infection of polarized epithelial cells with flavivirus West Nile: polarized entry and egress of virus occur through the apical surface.. J Gen Virol 2002 Oct;83(Pt 10):2427-2435.
    doi: 10.1099/0022-1317-83-10-2427pubmed: 12237424google scholar: lookup
  13. Lim PJ, Chu JJ. A polarized cell model for Chikungunya virus infection: entry and egress of virus occurs at the apical domain of polarized cells.. PLoS Negl Trop Dis 2014 Feb;8(2):e2661.
  14. Galen B, Cheshenko N, Tuyama A, Ramratnam B, Herold BC. Access to nectin favors herpes simplex virus infection at the apical surface of polarized human epithelial cells.. J Virol 2006 Dec;80(24):12209-18.
    doi: 10.1128/JVI.01503-06pmc: PMC1676285pubmed: 17005657google scholar: lookup
  15. Marozin S, Prank U, Sodeik B. Herpes simplex virus type 1 infection of polarized epithelial cells requires microtubules and access to receptors present at cell-cell contact sites.. J Gen Virol 2004 Apr;85(Pt 4):775-786.
    doi: 10.1099/vir.0.19530-0pubmed: 15039520google scholar: lookup
  16. Topp KS, Rothman AL, Lavail JH. Herpes virus infection of RPE and MDCK cells: polarity of infection.. Exp Eye Res 1997 Mar;64(3):343-54.
    doi: 10.1006/exer.1996.0209pubmed: 9196385google scholar: lookup
  17. Allen GP, Bryans JT. Molecular epizootiology, pathogenesis, and prophylaxis of equine herpesvirus-1 infections.. Prog Vet Microbiol Immunol 1986;2:78-144.
    pubmed: 2856183
  18. 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.
  19. 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
  20. 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.
  21. Negussie H, Li Y, Tessema TS, Nauwynck HJ. Replication characteristics of equine herpesvirus 1 and equine herpesvirus 3: comparative analysis using ex vivo tissue cultures.. Vet Res 2016 Jan 15;47:19.
    doi: 10.1186/s13567-016-0305-5pmc: PMC4714513pubmed: 26768993google scholar: lookup
  22. Steukers L, Weyers S, Yang X, Vandekerckhove AP, Glorieux S, Cornelissen M, Van den Broeck W, Temmerman M, Nauwynck HJ. Mimicking herpes simplex virus 1 and herpes simplex virus 2 mucosal behavior in a well-characterized human genital organ culture.. J Infect Dis 2014 Jul 15;210(2):209-13.
    doi: 10.1093/infdis/jiu036pubmed: 24436451google scholar: lookup
  23. 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
  24. Dayaram A, Franz M, Schattschneider A, Damiani AM, Bischofberger S, Osterrieder N, Greenwood AD. Long term stability and infectivity of herpesviruses in water.. Sci Rep 2017 Apr 21;7:46559.
    doi: 10.1038/srep46559pmc: PMC5399353pubmed: 28429732google scholar: lookup
  25. Steukers L, Vandekerckhove AP, Van den Broeck W, Glorieux S, Nauwynck HJ. Kinetics of BoHV-1 dissemination in an in vitro culture of bovine upper respiratory tract mucosa explants.. ILAR J 2012;53(1):E43-54.
    doi: 10.1093/ilar.53.1.43pubmed: 23382270google scholar: lookup
  26. Glorieux S, Van den Broeck W, van der Meulen KM, Van Reeth K, Favoreel HW, Nauwynck HJ. In vitro culture of porcine respiratory nasal mucosa explants for studying the interaction of porcine viruses with the respiratory tract.. J Virol Methods 2007 Jun;142(1-2):105-12.
  27. Vandekerckhove A, Glorieux S, Broeck WV, Gryspeerdt A, van der Meulen KM, Nauwynck HJ. In vitro culture of equine respiratory mucosa explants.. Vet J 2009 Sep;181(3):280-7.
    doi: 10.1016/j.tvjl.2008.03.027pubmed: 18539059google scholar: lookup
  28. 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
  29. 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
  30. 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
  31. 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
  32. van der Meulen K, Vercauteren G, Nauwynck H, Pensaert M. A local epidemic of equine herpesvirus 1-induced neurological disorders in Belgium.. Vlaams diergeneeskundig tijdschrift 2003;72:366–372.
  33. 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
  34. Yang X, Steukers L, Forier K, Xiong R, Braeckmans K, Van Reeth K, Nauwynck H. A beneficiary role for neuraminidase in influenza virus penetration through the respiratory mucus.. PLoS One 2014;9(10):e110026.
  35. 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
  36. Vairo S, Van den Broeck W, Favoreel H, Scagliarini A, Nauwynck H. Development and use of a polarized equine upper respiratory tract mucosal explant system to study the early phase of pathogenesis of a European strain of equine arteritis virus.. Vet Res 2013 Mar 28;44(1):22.
    doi: 10.1186/1297-9716-44-22pmc: PMC3668984pubmed: 23537375google scholar: lookup
  37. Osterrieder N. Construction and characterization of an equine herpesvirus 1 glycoprotein C negative mutant.. Virus Res 1999 Feb;59(2):165-77.
    doi: 10.1016/S0168-1702(98)00134-8pubmed: 10082388google scholar: lookup
  38. Banfield BW, Leduc Y, Esford L, Visalli RJ, Brandt CR, Tufaro F. Evidence for an interaction of herpes simplex virus with chondroitin sulfate proteoglycans during infection.. Virology 1995 Apr 20;208(2):531-9.
    doi: 10.1006/viro.1995.1184pubmed: 7747425google scholar: lookup
  39. Spear PG. Entry of alphaherpesviruses into cells.. Seminars in virology 1993;4:167–180.
    doi: 10.1006/smvy.1993.1012google scholar: lookup
  40. Balda MS, Whitney JA, Flores C, González S, Cereijido M, Matter K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein.. J Cell Biol 1996 Aug;134(4):1031-49.
    doi: 10.1083/jcb.134.4.1031pmc: PMC2120963pubmed: 8769425google scholar: lookup
  41. Wang G, Zabner J, Deering C, Launspach J, Shao J, Bodner M, Jolly DJ, Davidson BL, McCray PB Jr. Increasing epithelial junction permeability enhances gene transfer to airway epithelia In vivo.. Am J Respir Cell Mol Biol 2000 Feb;22(2):129-38.
    doi: 10.1165/ajrcmb.22.2.3938pubmed: 10657931google scholar: lookup
  42. Vinhas R, Cortes L, Cardoso I, Mendes VM, Manadas B, Todo-Bom A, Pires E, Veríssimo P. Pollen proteases compromise the airway epithelial barrier through degradation of transmembrane adhesion proteins and lung bioactive peptides.. Allergy 2011 Aug;66(8):1088-98.
  43. Shasby DM, Shasby SS. Effects of calcium on transendothelial albumin transfer and electrical resistance.. J Appl Physiol (1985) 1986 Jan;60(1):71-9.
    pubmed: 3080401doi: 10.1152/jappl.1986.60.1.71google scholar: lookup
  44. Nilsson M, Fagman H, Ericson LE. Ca2+-dependent and Ca2+-independent regulation of the thyroid epithelial junction complex by protein kinases.. Exp Cell Res 1996 May 25;225(1):1-11.
    doi: 10.1006/excr.1996.0151pubmed: 8635501google scholar: lookup
  45. Brown RC, Davis TP. Calcium modulation of adherens and tight junction function: a potential mechanism for blood-brain barrier disruption after stroke.. Stroke 2002 Jun;33(6):1706-11.
  46. Volberg T, Geiger B, Kartenbeck J, Franke WW. Changes in membrane-microfilament interaction in intercellular adherens junctions upon removal of extracellular Ca2+ ions.. J Cell Biol 1986 May;102(5):1832-42.
    doi: 10.1083/jcb.102.5.1832pmc: PMC2114216pubmed: 3084500google scholar: lookup
  47. Nazıroğlu M, Senol N, Ghazizadeh V, Yürüker V. Neuroprotection induced by N-acetylcysteine and selenium against traumatic brain injury-induced apoptosis and calcium entry in hippocampus of rat.. Cell Mol Neurobiol 2014 Aug;34(6):895-903.
    doi: 10.1007/s10571-014-0069-2pubmed: 24842665google scholar: lookup
  48. Breuer D, Becker M. [Acetylcysteine (Fluimucil) in the treatment of COPD of the horse].. Tierarztl Prax 1983;11(2):209-12.
    pubmed: 6868068
  49. Mair TS, Derksen FJ. Chronic obstructive pulmonary disease: a review.. Equine Veterinary education 2000;12:35–44.
  50. Lopez-Souza N, Favoreto S, Wong H, Ward T, Yagi S, Schnurr D, Finkbeiner WE, Dolganov GM, Widdicombe JH, Boushey HA, Avila PC. In vitro susceptibility to rhinovirus infection is greater for bronchial than for nasal airway epithelial cells in human subjects.. J Allergy Clin Immunol 2009 Jun;123(6):1384-90.e2.
    doi: 10.1016/j.jaci.2009.03.010pmc: PMC2744461pubmed: 19428098google scholar: lookup
  51. Boucher RC, Stutts MJ, Gatzy JT. Regional differences in bioelectric properties and ion flow in excised canine airways.. J Appl Physiol Respir Environ Exerc Physiol 1981 Sep;51(3):706-14.
    pubmed: 7327972doi: 10.1152/jappl.1981.51.3.706google scholar: lookup
  52. Ballard ST, Schepens SM, Falcone JC, Meininger GA, Taylor AE. Regional bioelectric properties of porcine airway epithelium.. J Appl Physiol (1985) 1992 Nov;73(5):2021-7.
    pubmed: 1474081doi: 10.1152/jappl.1992.73.5.2021google scholar: lookup
  53. Fokkens WJ, Scheeren RA. Upper airway defence mechanisms.. Paediatr Respir Rev 2000 Dec;1(4):336-41.
    doi: 10.1053/prrv.2000.0073pubmed: 16263461google scholar: lookup
  54. REAS HW. The effect of N-acetylcysteine on the viscosity of tracheobronchial secretions in cystic fibrosis of the pancreas.. J Pediatr 1963 Jan;62:31-5.
    doi: 10.1016/S0022-3476(63)80067-0pubmed: 13973420google scholar: lookup
  55. Mateo M, Generous A, Sinn PL, Cattaneo R. Connections matter--how viruses use cell–cell adhesion components.. J Cell Sci 2015 Feb 1;128(3):431-9.
    doi: 10.1242/jcs.159400pmc: PMC4311127pubmed: 26046138google scholar: lookup
  56. Gerez JR, Pinton P, Callu P, Grosjean F, Oswald IP, Bracarense AP. Deoxynivalenol alone or in combination with nivalenol and zearalenone induce systemic histological changes in pigs.. Exp Toxicol Pathol 2015 Feb;67(2):89-98.
    doi: 10.1016/j.etp.2014.10.001pubmed: 25467749google scholar: lookup
  57. De Walle JV, Sergent T, Piront N, Toussaint O, Schneider YJ, Larondelle Y. Deoxynivalenol affects in vitro intestinal epithelial cell barrier integrity through inhibition of protein synthesis.. Toxicol Appl Pharmacol 2010 Jun 15;245(3):291-8.
    doi: 10.1016/j.taap.2010.03.012pubmed: 20362602google scholar: lookup
  58. Runswick S, Mitchell T, Davies P, Robinson C, Garrod DR. Pollen proteolytic enzymes degrade tight junctions.. Respirology 2007 Nov;12(6):834-42.
  59. Groten T, Pierce AA, Huen AC, Schnaper HW. 17 beta-estradiol transiently disrupts adherens junctions in endothelial cells.. FASEB J 2005 Aug;19(10):1368-70.
    pubmed: 15928195doi: 10.1096/fj.04-2558fjegoogle scholar: lookup
  60. Capaldo CT, Nusrat A. Cytokine regulation of tight junctions.. Biochim Biophys Acta 2009 Apr;1788(4):864-71.
  61. Kwak YK, Vikström E, Magnusson KE, Vécsey-Semjén B, Colque-Navarro P, Möllby R. The Staphylococcus aureus alpha-toxin perturbs the barrier function in Caco-2 epithelial cell monolayers by altering junctional integrity.. Infect Immun 2012 May;80(5):1670-80.
    doi: 10.1128/IAI.00001-12pmc: PMC3347457pubmed: 22354024google scholar: lookup
  62. Xiao C, Puddicombe SM, Field S, Haywood J, Broughton-Head V, Puxeddu I, Haitchi HM, Vernon-Wilson E, Sammut D, Bedke N, Cremin C, Sones J, Djukanović R, Howarth PH, Collins JE, Holgate ST, Monk P, Davies DE. Defective epithelial barrier function in asthma.. J Allergy Clin Immunol 2011 Sep;128(3):549-56.e1-12.
    doi: 10.1016/j.jaci.2011.05.038pubmed: 21752437google scholar: lookup
  63. Costa LR, Johnson JR, Baur ME, Beadle RE. Temporal clinical exacerbation of summer pasture-associated recurrent airway obstruction and relationship with climate and aeroallergens in horses.. Am J Vet Res 2006 Sep;67(9):1635-42.
    doi: 10.2460/ajvr.67.9.1635pubmed: 16948614google scholar: lookup
  64. Smith D, Hamblin A, Edington N. Equid herpesvirus 1 infection of endothelial cells requires activation of putative adhesion molecules: an in vitro model.. Clin Exp Immunol 2002 Aug;129(2):281-7.
  65. Caruso S, Roccasalva L, Di Fazio E, Sapienza G, Agnello C, Ficarra S, Di Mari L, Serra A. Cytologic aspects of the nasal respiratory epithelium in postmenopausal women treated with hormone therapy.. Fertil Steril 2003 Mar;79(3):543-9.
    doi: 10.1016/S0015-0282(02)04844-6pubmed: 12620437google scholar: lookup
  66. Walters RW, Freimuth P, Moninger TO, Ganske I, Zabner J, Welsh MJ. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape.. Cell 2002 Sep 20;110(6):789-99.
    doi: 10.1016/S0092-8674(02)00912-1pubmed: 12297051google scholar: lookup
  67. Neubauer A, Braun B, Brandmuller C, Kaaden OR, Osterrieder N. Analysis of the contributions of the equine herpesvirus 1 glycoprotein gB homolog to virus entry and direct cell-to-cell spread.. Virology 1997 Jan 20;227(2):281-94.
    doi: 10.1006/viro.1996.8336pubmed: 9018127google scholar: lookup
  68. Caplan MJ, Stow JL, Newman AP, Madri J, Anderson HC, Farquhar MG, Palade GE, Jamieson JD. Dependence on pH of polarized sorting of secreted proteins.. Nature 1987 Oct 15-21;329(6140):632-5.
    doi: 10.1038/329632a0pubmed: 2821405google scholar: lookup
  69. Rapraeger A, Jalkanen M, Bernfield M. Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells.. J Cell Biol 1986 Dec;103(6 Pt 2):2683-96.
    doi: 10.1083/jcb.103.6.2683pmc: PMC2114626pubmed: 3025223google scholar: lookup
  70. Csellner H, Walker C, Wellington JE, McLure LE, Love DN, Whalley JM. EHV-1 glycoprotein D (EHV-1 gD) is required for virus entry and cell-cell fusion, and an EHV-1 gD deletion mutant induces a protective immune response in mice.. Arch Virol 2000;145(11):2371-85.
    doi: 10.1007/s007050070027pubmed: 11205124google scholar: lookup
  71. Sasaki M, Hasebe R, Makino Y, Suzuki T, Fukushi H, Okamoto M, Matsuda K, Taniyama H, Sawa H, Kimura T. Equine major histocompatibility complex class I molecules act as entry receptors that bind to equine herpesvirus-1 glycoprotein D.. Genes Cells 2011 Apr;16(4):343-57.
  72. 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
  73. Van de Walle GR, Peters ST, VanderVen BC, O'Callaghan DJ, Osterrieder N. Equine herpesvirus 1 entry via endocytosis is facilitated by alphaV integrins and an RSD motif in glycoprotein D.. J Virol 2008 Dec;82(23):11859-68.
    doi: 10.1128/JVI.00868-08pmc: PMC2583640pubmed: 18815313google scholar: lookup
  74. Sheppard D. Functions of pulmonary epithelial integrins: from development to disease.. Physiol Rev 2003 Jul;83(3):673-86.
    doi: 10.1152/physrev.00033.2002pubmed: 12843406google scholar: lookup
  75. Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor.. Science 1998 Jun 5;280(5369):1618-20.
    doi: 10.1126/science.280.5369.1618pubmed: 9616127google scholar: lookup
  76. Frampton AR Jr, Goins WF, Cohen JB, von Einem J, Osterrieder N, O'Callaghan DJ, Glorioso JC. Equine herpesvirus 1 utilizes a novel herpesvirus entry receptor.. J Virol 2005 Mar;79(5):3169-73.

Citations

This article has been cited 11 times.
  1. Van Crombrugge E, Vanbeylen E, Van Cleemput J, Van den Broeck W, Laval K, Nauwynck H. Bacterial Toxins from Staphylococcus aureus and Bordetella bronchiseptica Predispose the Horse's Respiratory Tract to Equine Herpesvirus Type 1 Infection.. Viruses 2022 Jan 14;14(1).
    doi: 10.3390/v14010149pubmed: 35062352google scholar: lookup
  2. Zarski LM, Vaala WE, Barnett DC, Bain FT, Soboll Hussey G. A Live-Attenuated Equine Influenza Vaccine Stimulates Innate Immunity in Equine Respiratory Epithelial Cell Cultures That Could Provide Protection From Equine Herpesvirus 1.. Front Vet Sci 2021;8:674850.
    doi: 10.3389/fvets.2021.674850pubmed: 34179166google scholar: lookup
  3. 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
  4. Romero N, Van Waesberghe C, Favoreel HW. Pseudorabies Virus Infection of Epithelial Cells Leads to Persistent but Aberrant Activation of the NF-κB Pathway, Inhibiting Hallmark NF-κB-Induced Proinflammatory Gene Expression.. J Virol 2020 May 4;94(10).
    doi: 10.1128/JVI.00196-20pubmed: 32132236google scholar: lookup
  5. Van Cleemput J, Poelaert KCK, Laval K, Vanderheijden N, Dhaenens M, Daled S, Boyen F, Pasmans F, Nauwynck HJ. An Alphaherpesvirus Exploits Antimicrobial β-Defensins To Initiate Respiratory Tract Infection.. J Virol 2020 Mar 31;94(8).
    doi: 10.1128/JVI.01676-19pubmed: 31996426google scholar: lookup
  6. Cui T, Theuns S, Xie J, Nauwynck HJ. Porcine rotavirus mainly infects primary porcine enterocytes at the basolateral surface.. Vet Res 2019 Dec 19;50(1):110.
    doi: 10.1186/s13567-019-0728-xpubmed: 31856906google scholar: lookup
  7. 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
  8. Van Cleemput J, Poelaert KCK, Laval K, Impens F, Van den Broeck W, Gevaert K, Nauwynck HJ. Pollens destroy respiratory epithelial cell anchors and drive alphaherpesvirus infection.. Sci Rep 2019 Mar 18;9(1):4787.
    doi: 10.1038/s41598-019-41305-ypubmed: 30886217google scholar: lookup
  9. 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/s13567-019-0630-6pubmed: 30777128google scholar: lookup
  10. Yang B, Xie J, Van Cleemput J, Wei R, Opsomer G, Nauwynck HJ. Gammaherpesvirus BoHV-4 infects bovine respiratory epithelial cells mainly at the basolateral side.. Vet Res 2019 Feb 8;50(1):11.
    doi: 10.1186/s13567-019-0629-zpubmed: 30736853google scholar: lookup
  11. 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.
    doi: 10.3389/fcimb.2018.00312pubmed: 30258819google scholar: lookup