Pathogenic potential of equine alphaherpesviruses: The importance of the mononuclear cell compartment in disease outcome

Veterinary Microbiology

Volumn 143, Issue 1, 2010, Pages 21-28

  Osterrieder, Nikolaus ^a   Van de Walle, Gerlinde R ^b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Alphaherpesviruses; Equine; GD; GG; Mononuclear cell compartment; Respiratory

Indexed keywords

CHEMOKINE; GLYCOPROTEIN D; THROMBOSPONDIN;

ALPHAHERPESVIRINAE; AMINO ACID SEQUENCE; ARTICLE; DISEASE COURSE; EQUINE ABORTION HERPETOVIRUS; EQUINE HERPES VIRUS; EQUINE HERPES VIRUS 4; EQUINE HERPES VIRUS 8; EQUINE HERPES VIRUS 9; EXTRACELLULAR SPACE; INNATE IMMUNITY; MONONUCLEAR CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN DOMAIN; PROTEIN MOTIF; VIRUS PATHOGENESIS;

AMINO ACID SEQUENCE; ANIMALS; CHEMOKINES; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 1, EQUID; HERPESVIRUS 4, EQUID; HORSE DISEASES; HORSES; IMMUNE EVASION; LEUKOCYTES, MONONUCLEAR; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EQUID HERPESVIRUS 1; EQUID HERPESVIRUS 4; EQUIDAE;

EID: 77952878890     PISSN: 03781135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetmic.2010.02.010     Document Type: Article

References (65)

1. Borchers K., Thein R., Sterner-Kock A. Pathogenesis of equine herpesvirus-associated neurological disease: a revised explanation. Equine Vet. J. 2006, 38:283-287.
2. Brosnahan, M.M., Osterrieder, N., in press. Equine herpesvirus-1: a review and update. Equine Vet. J.
3. Allen G.P., Breathnach C.C. Quantification by real-time PCR of the magnitude and duration of leucocyte-associated viraemia in horses infected with neuropathogenic vs. non-neuropathogenic strains of EHV-1. Equine Vet. J. 2006, 38:252-257.
4. Blunden A.S., Smith K.C., Binns M.M., Zhang L., Gower S.M., Mumford J.A. Replication of equid herpesvirus 4 in endothelial cells and synovia of a field case of viral pneumonia and synovitis in a foal. J. Comp. Pathol. 1995, 112:133-140.
5. Browning G.F., Ficorilli N., Studdert M.J. Asinine herpesvirus genomes: comparison with those of the equine herpesviruses. Arch. Virol. 1988, 101:183-190.
6. Bryant N.A., Davis-Poynter N., Vanderplasschen A., Alcami A. Glycoprotein G isoforms from some alphaherpesviruses function as broad-spectrum chemokine binding proteins. EMBO J. 2003, 22:833-846.
7. Crabb B.S., Allen G.P., Studdert M.J. Characterization of the major glycoproteins of equine herpesviruses 4 and 1 and asinine herpesvirus 3 using monoclonal antibodies. J. Gen. Virol. 1991, 72(Pt 9):2075-2082.
8. Crabb B.S., MacPherson C.M., Reubel G.H., Browning G.F., Studdert M.J., Drummer H.E. A type-specific serological test to distinguish antibodies to equine herpesviruses 4 and 1. Arch. Virol. 1995, 140:245-258.
9. Crabb B.S., Nagesha H.S., Studdert M.J. Identification of equine herpesvirus 4 glycoprotein G: a type-specific, secreted glycoprotein. Virology 1992, 190:143-154.
10. Crabb B.S., Studdert M.J. Comparative studies of the proteins of equine herpesviruses 4 and 1 and asinine herpesvirus 3: antibody response of the natural hosts. J. Gen. Virol. 1990, 71(Pt 9):2033-2041.
11. Crabb B.S., Studdert M.J. Epitopes of glycoprotein G of equine herpesviruses 4 and 1 located near the C termini elicit type-specific antibody responses in the natural host. J. Virol. 1993, 67:6332-6338.
12. Csellner H., Walker C., Wellington J.E., McLure L.E., Love D.N., Whalley J.M. 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, 145:2371-2385.
13. Davison A.J., Eberle R., Ehlers B., Hayward G.S., McGeoch D.J., Minson A.C., Pellett P.E., Roizman B., Studdert M.J., Thiry E. The order Herpesvirales. Arch. Virol. 2009, 154:171-177.
14. Drummer H.E., Studdert M.J., Crabb B.S. Equine herpesvirus-4 glycoprotein G is secreted as a disulphide-linked homodimer and is present as two homodimeric species in the virion. J. Gen. Virol. 1998, 79(Pt 5):1205-1213.
15. Ficorilli N., Studdert M.J., Crabb B.S. The nucleotide sequence of asinine herpesvirus 3 glycoprotein G indicates that the donkey virus is closely related to equine herpesvirus 1. Arch. Virol. 1995, 140:1653-1662.
16. Flowers C.C., O'Callaghan D.J. The equine herpesvirus type 1 (EHV-1) homolog of herpes simplex virus type 1 US9 and the nature of a major deletion within the unique short segment of the EHV-1 KyA strain genome. Virology 1992, 190:307-315.
17. Frampton A.R., Goins W.F., Cohen J.B., von Einem J., Osterrieder N., O'Callaghan D.J., Glorioso J.C. Equine herpesvirus 1 utilizes a novel herpesvirus entry receptor. J. Virol. 2005, 79:3169-3173.
18. Frampton A.R., Stolz D.B., Uchida H., Goins W.F., Cohen J.B., Glorioso J.C. Equine herpesvirus 1 enters cells by two different pathways, and infection requires the activation of the cellular kinase ROCK1. J. Virol. 2007, 81:10879-10889.
19. Frampton A.R., Uchida H., von Einem J., Goins W.F., Grandi P., Cohen J.B., Osterrieder N., Glorioso J.C. Equine herpesvirus type 1 (EHV-1) utilizes microtubules, dynein, and ROCK1 to productively infect cells. Vet. Microbiol. 2009, (Epub ahead of print).
20. Fukushi H., Tomita T., Taniguchi A., Ochiai Y., Kirisawa R., Matsumura T., Yanai T., Masegi T., Yamaguchi T., Hirai K. Gazelle herpesvirus 1: a new neurotropic herpesvirus immunologically related to equine herpesvirus 1. Virology 1997, 227:34-44.
21. Glass W.G., Rosenberg H.F., Murphy P.M. Chemokine regulation of inflammation during acute viral infection. Curr. Opin. Allergy Clin. Immunol. 2003, 3:467-473.
22. Goodman L.B., Loregian A., Perkins G.A., Nugent J., Buckles E.L., Mercorelli B., Kydd J.H., Palu G., Smith K.C., Osterrieder N., Davis-Poynter N. A point mutation in a herpesvirus polymerase determines neuropathogenicity. PLoS Pathog. 2007, 3:e160.
23. Goodman L.B., Wagner B., Flaminio M.J., Sussman K.H., Metzger S.M., Holland R., Osterrieder N. Comparison of the efficacy of inactivated combination and modified-live virus vaccines against challenge infection with neuropathogenic equine herpesvirus type 1 (EHV-1). Vaccine 2006, 24:3636-3645.
24. Gryspeerdt, A.C., Vandekerckhove A.P., Barbe F., Van de Walle, G.R., Nauwynck, H., 2009. Differences in replication kinetics and cell tropism between neurovirulent and non-neurovirulent EHV1 strains during the acute phase of infection in horses. Vet. Microbiol., doi:10.1016/j.vetmic.2009.1010.1015.
25. Hasebe R., Kimura T., Nakamura K., Ochiai K., Okazaki K., Wada R., Umemura T. Differential susceptibility of equine and mouse brain microvascular endothelial cells to equine herpesvirus 1 infection. Arch. Virol. 2006, 151:775-786.
26. Hasebe R., Sasaki M., Sawa H., Wada R., Umemura T., Kimura T. Infectious entry of equine herpesvirus-1 into host cells through different endocytic pathways. Virology 2009, (Epub ahead of print).
27. Heldens J.G., Hannant D., Cullinane A.A., Prendergast M.J., Mumford J.A., Nelly M., Kydd J.H., Weststrate M.W., van den Hoven R. Clinical and virological evaluation of the efficacy of an inactivated EHV1 and EHV4 whole virus vaccine (Duvaxyn EHV1,4). Vaccination/challenge experiments in foals and pregnant mares. Vaccine 2001, 19:4307-4317.
28. Kydd J.H., Smith K.C., Hannant D., Livesay G.J., Mumford J.A. Distribution of equid herpesvirus-1 (EHV-1) in respiratory tract associated lymphoid tissue: implications for cellular immunity. Equine Vet. J. 1994, 26:470-473.
29. Lunn D.P., Davis-Poynter N., Flaminio M.J., Horohov D.W., Osterrieder K., Pusterla N., Townsend H.G. Equine herpesvirus-1 consensus statement. J. Vet. Intern. Med. 2009, 23:450-461.
30. Matsumura T., Sugiura T., Imagawa H., Fukunaga Y., Kamada M. Epizootiological aspects of type 1 and type 4 equine herpesvirus infections among horse populations. J. Vet. Med. Sci. 1992, 54:207-211.
31. Matsumura T., Kondo T., Sugita S., Damiani A.M., O'Callaghan D.J., Imagawa H. An equine herpesvirus type 1 recombinant with a deletion in the gE and gI genes is avirulent in young horses. Virology 1998, 242:68-79.
32. Melchjorsen J., Sorensen L.N., Paludan S.R. Expression and function of chemokines during viral infections: from molecular mechanisms to in vivo function. J. Leukoc. Biol. 2003, 74:331-343.
33. Meyer H., Thein P., Hubert P. Characterization of two equine herpesvirus (EHV) isolates associated with neurological disorders in horses. Zentralbl. Veterinarmed. B 1987, 34:545-548.
34. Neubauer A., Osterrieder N. Equine herpesvirus type 1 (EHV-1) glycoprotein K is required for efficient cell-to-cell spread and virus egress. Virology 2004, 329:18-32.
35. Neubauer A., Braun B., Brandmuller C., Kaaden O.R., 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, 227:281-294.
36. Nugent J., Birch-Machin I., Smith K.C., Mumford J.A., Swann Z., Newton J.R., Bowden R.J., Allen G.P., Davis-Poynter N. Analysis of equid herpesvirus 1 strain variation reveals a point mutation of the DNA polymerase strongly associated with neuropathogenic versus nonneuropathogenic disease outbreaks. J. Virol. 2006, 80:4047-4060.
37. Osterrieder N. Construction and characterization of an equine herpesvirus 1 glycoprotein C negative mutant. Virus Res. 1999, 59:165-177.
38. Osterrieder, N., Neubauer, A., Brandmuller, C., Braun, B., Kaaden, O.R., Baines, J.D., 1996. 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.
39. Patel J.R., Edington N., Mumford J.A. Variation in cellular tropism between isolates of equine herpesvirus-1 in foals. Arch. Virol. 1982, 74:41-51.
40. Patel J.R., Foldi J., Bateman H., Williams J., Didlick S., Stark R. Equid herpesvirus (EHV-1) live vaccine strain C147: efficacy against respiratory diseases following EHV types 1 and 4 challenges. Vet. Microbiol. 2003, 92:1-17.
41. Patel J.R., Heldens J. Equine herpesviruses 1 (EHV-1) and 4 (EHV-4)-epidemiology, disease and immunoprophylaxis: a brief review. Vet. J. 2005, 170:14-23.
42. Pusterla N., David Wilson W., Madigan J.E., Ferraro G.L. Equine herpesvirus-1 myeloencephalopathy: a review of recent developments. Vet. J. 2009, 180:279-289.
43. Reed S.M., Toribio R.E. Equine herpesvirus 1 and 4. Vet. Clin. North Am. Equine Pract. 2004, 20:631-642.
44. Robertson G.R., Scott N.A., Miller J.M., Sabine M., Zheng M., Bell C.W., Whalley J.M. Sequence characteristics of a gene in equine herpesvirus 1 homologous to glycoprotein H of herpes simplex virus. DNA Seq. 1991, 1:241-249.
45. Rudolph J., Seyboldt C., Granzow H., Osterrieder N. The gene 10 (UL49.5) product of equine herpesvirus 1 is necessary and sufficient for functional processing of glycoprotein M. J. Virol. 2002, 76:2952-2963.
46. Rudolph J., Osterrieder N. Equine herpesvirus type 1 devoid of gM and gp2 is severely impaired in virus egress but not direct cell-to-cell spread. Virology 293: 2002, 356-367.
47. Smith P.M., Kahan S.M., Rorex C.B., von Einem J., Osterrieder N., O'Callaghan D.J. Expression of the full-length form of gp2 of equine herpesvirus 1 (EHV-1) completely restores respiratory virulence to the attenuated EHV-1 strain KyA in CBA mice. J. Virol. 2005, 79:5105-5115.
48. Smith K.C., Mumford J.A., Lakhani K. A comparison of equid herpesvirus-1 (EHV-1) vascular lesions in the early versus late pregnant equine uterus. J. Comp. Pathol. 1996, 114:231-247.
49. Stokes A., Alber D.G., Greensill J., Amellal B., Carvalho R., Taylor L.A., Doel T.R., Killington R.A., Halliburton I.W., Meredith D.M. The expression of the proteins of equine herpesvirus 1 which share homology with herpes simplex virus 1 glycoproteins H and L. Virus Res. 1996, 40:91-107.
50. Taniguchi A., Fukushi H., Matsumura T., Yanai T., Masegi T., Hirai K. Pathogenicity of a new neurotropic equine herpesvirus 9 (gazelle herpesvirus 1) in horses. J. Vet. Med. Sci. 2000, 62:215-218.
51. USDA-APHIS Equine Herpesvirus Myeloencephalopathy: A Potential Emerging Disease 2007.
52. Van de Walle G.R., Goupil R., Wishon C., Damiani A., Perkins G.A., Osterrieder N. A single-nucleotide polymorphism (SNP) in a herpesvirus DNA polymerase is sufficient to cause lethal neurological disease. J. Infect. Dis. 2009, 200:20-25.
53. Van de Walle G.R., Jarosinski K.W., Osterrieder N. Alphaherpesviruses and chemokines: Pas-de-Deux not yet brought to perfection. J. Virol. 2008, 82:6090-6097.
54. Van de Walle G.R., Kaufer B.B., Chbab N., Osterrieder N. Analysis of the herpesvirus chemokine-binding glycoprotein G residues essential for chemokine binding and biological activity. J. Biol. Chem. 2009, 284:5968-5976.
55. Van de Walle G.R., May M.L., Sukhumavasi W., von Einem J., Osterrieder N. Herpesvirus chemokine-binding glycoprotein G (gG) efficiently inhibits neutrophil chemotaxis in vitro and in vivo. J. Immunol. 2007, 179:4161-4169.
56. Van de Walle G.R., Peters S.T., VanderVen B.C., O'Callaghan D.J., Osterrieder N. Equine herpesvirus 1 entry via endocytosis is facilitated by alphaV integrins and an RSD motif in glycoprotein D. J. Virol. 2008, 82:11859-11868.
57. Van de Walle G.R., Sakamoto K., Osterrieder N. CCL3 and viral chemokine-binding protein gg modulate pulmonary inflammation and virus replication during equine herpesvirus 1 infection. J. Virol. 2008, 82:1714-1722.
58. van Maanen C. Equine herpesvirus 1 and 4 infections: an update. Vet. Q 2002, 24:58-78.
59. Verheyen K., Newton J.R., Wood J.L., Birch-Machin I., Hannant D., Humberstone R.W. Possible case of EHV-4 ataxia in warmblood mare. Vet. Rec. 1998, 143:456.
60. von Einem J., Smith P.M., Van de Walle G.R., O'Callaghan D.J., Osterrieder N. In vitro and in vivo characterization of equine herpesvirus type 1 (EHV-1) mutants devoid of the viral chemokine-binding glycoprotein G (gG). Virology 2007, 362:151-162.
61. von Einem J., Wellington J., Whalley J.M., Osterrieder K., O'Callaghan D.J., Osterrieder N. The truncated form of glycoprotein gp2 of equine herpesvirus 1 (EHV-1) vaccine strain KyA is not functionally equivalent to full-length gp2 encoded by EHV-1 wild-type strain RacL11. J. Virol. 2004, 78:3003-3013.
62. Wellington J.E., Love D.N., Whalley J.M. Evidence for involvement of equine herpesvirus 1 glycoprotein B in cell-cell fusion. Arch. Virol. 1996, 141:167-175.
63. Wilson W.D. Equine herpesvirus 1 myeloencephalopathy. Vet. Clin. N. Am. Equine Pract. 1997, 13:53-72.
64. Zhao Y., Holden V.R., Harty R.N., O'Callaghan D.J. Identification and transcriptional analyses of the UL3 and UL4 genes of equine herpesvirus 1, homologs of the ICP27 and glycoprotein K genes of herpes simplex virus. J. Virol. 1992, 66:5363-5372.
65. Ziegler C., Just F.T., Lischewski A., Elbers K., Neubauer A. A glycoprotein M-deleted equid herpesvirus 4 is severely impaired in virus egress and cell-to-cell spread. J. Gen. Virol. 2005, 86:11-21.