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Clinical and vaccine immunology : CVI2017; 24(10); doi: 10.1128/CVI.00215-17

Equine Arteritis Virus Elicits a Mucosal Antibody Response in the Reproductive Tract of Persistently Infected Stallions.

Abstract: Equine arteritis virus (EAV) has the ability to establish persistent infection in the reproductive tract of the stallion (carrier) and is continuously shed in its semen. We have recently demonstrated that EAV persists within stromal cells and a subset of lymphocytes in the stallion accessory sex glands in the presence of a significant local inflammatory response. In the present study, we demonstrated that EAV elicits a mucosal antibody response in the reproductive tract during persistent infection with homing of plasma cells into accessory sex glands. The EAV-specific immunoglobulin isotypes in seminal plasma included IgA, IgG1, IgG3/5, and IgG4/7. Interestingly, seminal plasma IgG1 and IgG4/7 possessed virus-neutralizing activity, while seminal plasma IgA and IgG3/5 did not. However, virus-neutralizing IgG1 and IgG4/7 in seminal plasma were not effective in preventing viral infectivity. In addition, the serological response was primarily mediated by virus-specific IgM and IgG1, while virus-specific serum IgA, IgG3/5, IgG4/7, and IgG6 isotype responses were not detected. This is the first report characterizing the immunoglobulin isotypes in equine serum and seminal plasma in response to EAV infection. The findings presented herein suggest that while a broader immunoglobulin isotype diversity is elicited in seminal plasma, EAV has the ability to persist in the reproductive tract, in spite of local mucosal antibody and inflammatory responses. This study provides further evidence that EAV employs complex immune evasion mechanisms during persistence in the reproductive tract that warrant further investigation.
Publication Date: 2017-10-05 PubMed ID: 28814389PubMed Central: PMC5629664DOI: 10.1128/CVI.00215-17Google Scholar: Lookup
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  • Journal Article

Summary

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

The research paper discusses the response of the equine arteritis virus (EAV) in the reproductive tract of persistently infected stallions. The researchers have observed how EAV triggers a immune system response in the reproductive tract, persisting despite these responses.

Persistence and Antibody Response of EAV

  • This paper establishes the persistence of the EAV within stromal cells and a subset of lymphocytes in the stallion accessory sex glands, despite a significant local inflammatory response triggered by the virus infection.
  • Furthermore, the paper highlights a mucosal antibody response in the reproductive tract during persistent infection, indicating the immune system’s attempts to neutralize the virus. Plasma cells home into accessory sex glands, contributing to this response.

Immunoglobulin Isotypes in Seminal Plasma

  • The researchers identified specific immunoglobulin isotypes in seminal plasma. These included IgA, IgG1, IgG3/5, and IgG4/7. These are immune system proteins that can potentially neutralize the virus in the seminal plasma.
  • They found that while IgG1 and IgG4/7 had virus-neutralizing activity, they were not able to prevent the viral infectivity fully. This implies that the virus has the capacity to resist these neutralizing antibodies, enabling it to persist.

Serum Response

  • The serological response of the infected subjects was primary by virus-specific IgM and IgG1. There was no noticeable response by other immunoglobulin isotypes, like serum IgA, IgG3/5, IgG4/7, and IgG6.

Conclusion and Implications

  • This research is significant in characterizing the immunoglobulin isotypes in equine serum and seminal plasma in response to EAV infection.
  • The researchers suggest that EAV has developed complex strategies to withstand local mucosal antibody and inflammatory responses within the reproductive system.
  • The findings could potentially pave the way for further research on EAV, its immune response, and how it manages to evade this response, thereby providing a better understanding of this equine disease condition.

Cite This Article

APA
Carossino M, Wagner B, Loynachan AT, Cook RF, Canisso IF, Chelvarajan L, Edwards CL, Nam B, Timoney JF, Timoney PJ, Balasuriya UBR. (2017). Equine Arteritis Virus Elicits a Mucosal Antibody Response in the Reproductive Tract of Persistently Infected Stallions. Clin Vaccine Immunol, 24(10). https://doi.org/10.1128/CVI.00215-17

Publication

ISSN: 1556-679X
NlmUniqueID: 101252125
Country: United States
Language: English
Volume: 24
Issue: 10

Researcher Affiliations

Carossino, Mariano
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Wagner, Bettina
  • Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.
Loynachan, Alan T
  • University of Kentucky Veterinary Diagnostic Laboratory, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Cook, R Frank
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Canisso, Igor F
  • Department of Veterinary Clinical Medicine and Department of Comparative Biosciences, College of Veterinary Medicine, University of Illinois Urbana-Champaign, Urbana, Illinois, USA.
Chelvarajan, Lakshman
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Edwards, Casey L
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Nam, Bora
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Timoney, John F
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Timoney, Peter J
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Balasuriya, Udeni B R
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA ubalasuriya@uky.edu.

MeSH Terms

  • Animals
  • Antibodies, Neutralizing / immunology
  • Antibodies, Viral / analysis
  • Antibodies, Viral / immunology
  • Arterivirus Infections / immunology
  • Arterivirus Infections / veterinary
  • Arterivirus Infections / virology
  • Equartevirus / immunology
  • Horse Diseases / immunology
  • Horse Diseases / virology
  • Horses
  • Immune Evasion
  • Immunity, Humoral
  • Immunity, Mucosal
  • Immunoglobulin G / analysis
  • Immunoglobulin G / immunology
  • Immunoglobulin M / analysis
  • Immunoglobulin M / immunology
  • Male
  • Reproductive Tract Infections / immunology
  • Reproductive Tract Infections / veterinary
  • Reproductive Tract Infections / virology
  • Semen / immunology
  • Viremia

References

This article includes 68 references
  1. Balasuriya UB, Go YY, MacLachlan NJ. Equine arteritis virus. Vet Microbiol 2013;167:93–122.
  2. Snijder EJ, van Tol H, Pedersen KW, Raamsman MJ, de Vries AA. Identification of a novel structural protein of arteriviruses. J Virol 1999;73:6335–6345.
    pmc: PMC112712pubmed: 10400725
  3. Firth AE, Zevenhoven-Dobbe JC, Wills NM, Go YY, Balasuriya UB, Atkins JF, Snijder EJ, Posthuma CC. Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production. J Gen Virol 2011;92:1097–1106.
    doi: 10.1099/vir.0.029264-0pmc: PMC3139419pubmed: 21307223google scholar: lookup
  4. Snijder EJ, Kikkert M, Fang Y. Arterivirus molecular biology and pathogenesis. J Gen Virol 2013;94:2141–2163.
    doi: 10.1099/vir.0.056341-0pubmed: 23939974google scholar: lookup
  5. Balasuriya U, MacLachlan NJ. Equine viral arteritis. 2013;p 169–181.
  6. Cavanagh D. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch Virol 1997;142:629–633.
    pubmed: 9349308
  7. Snijder EJ, Meulenberg JJ. The molecular biology of arteriviruses. J Gen Virol 1998;79(Pt 5):961–979.
    doi: 10.1099/0022-1317-79-5-961pubmed: 9603311google scholar: lookup
  8. Dunowska M, Biggs PJ, Zheng T, Perrott MR. Identification of a novel nidovirus associated with a neurological disease of the Australian brushtail possum (Trichosurus vulpecula). Vet Microbiol 2012;156:418–424.
  9. Bryans JT, Crowe ME, Doll ER, McCollum WH. Isolation of a filterable agent causing arteritis of horses and abortion by mares; its differentiation from the equine abortion (influenza) virus. Cornell Vet 1957;47:3–41.
    pubmed: 13397177
  10. Timoney PJ, McCollum WH. Equine viral arteritis. Can Vet J 1987;28:693–695.
    pmc: PMC1680490pubmed: 17422919
  11. Balasuriya U. Equine viral arteritis. Vet Clin North Am Equine Pract 2014;30:543–560.
    doi: 10.1016/j.cveq.2014.08.011pubmed: 25441113google scholar: lookup
  12. Balasuriya UBR, Carossino M, Timoney PJ. Equine viral arteritis: a respiratory and reproductive disease of significant economic importance to the equine industry. Equine Vet Educ 2016 Nov 10.
    doi: 10.1111/eve.12672google scholar: lookup
  13. Timoney PJ, McCollum WH, Roberts AW, Murphy TW. Demonstration of the carrier state in naturally acquired equine arteritis virus infection in the stallion. Res Vet Sci 1986;41:279–280.
    pubmed: 3022363
  14. Timoney PJ, McCollum WH, Murphy TW, Roberts AW, Willard JG, Carswell GD. The carrier state in equine arteritis virus infection in the stallion with specific emphasis on the venereal mode of virus transmission. J Reprod Fertil Suppl 1987;35:95–102.
    pubmed: 2824772
  15. Timoney PJ, McCollum WH. Equine viral arteritis. Vet Clin North Am Equine Pract 1993;9:295–309.
  16. Holyoak GR, Little TV, McCollum WH, Timoney PJ. Relationship between onset of puberty and establishment of persistent infection with equine arteritis virus in the experimentally infected colt. J Comp Pathol 1993;109:29–46.
  17. Balasuriya UB, Snijder EJ, van Dinten LC, Heidner HW, Wilson WD, Hedges JF, Hullinger PJ, MacLachlan NJ. Equine arteritis virus derived from an infectious cDNA clone is attenuated and genetically stable in infected stallions. Virology 1999;260:201–208.
    doi: 10.1006/viro.1999.9817pubmed: 10405372google scholar: lookup
  18. Glaser AL, de Vries AA, Rottier PJ, Horzinek MC, Colenbrander B. Equine arteritis virus: a review of clinical features and management aspects. Vet Q 1996;18:95–99.
    doi: 10.1080/01652176.1996.9694625pubmed: 8903141google scholar: lookup
  19. Balasuriya UB, Hedges JF, Smalley VL, Navarrette A, McCollum WH, Timoney PJ, Snijder EJ, MacLachlan NJ. Genetic characterization of equine arteritis virus during persistent infection of stallions. J Gen Virol 2004;85:379–390.
    doi: 10.1099/vir.0.19545-0pubmed: 14769895google scholar: lookup
  20. Balasuriya UBR, Sarkar S, Carossino M, Go YY, Chelvarajan L, Cook RF, Loynachan AT, Timoney PJ, Bailey E. Host factors that contribute to equine arteritis virus persistence in the stallion: an update. J Equine Vet Sci 2016;43:S11–S17.
  21. Timoney PJ, McCollum WH. Equine viral arteritis: further characterization of the carrier state in stallions. J Reprod Fertil Suppl 2000;56:3–11.
    pubmed: 20681110
  22. Sarkar S, Bailey E, Go YY, Cook RF, Kalbfleisch T, Eberth J, Chelvarajan RL, Shuck KM, Artiushin S, Timoney PJ, Balasuriya UB. Allelic variation in CXCL16 determines CD3+ T lymphocyte susceptibility to equine arteritis virus infection and establishment of long-term carrier state in the stallion. PLoS Genet 2016;12:e1006467.
  23. Go YY, Bailey E, Timoney PJ, Shuck KM, Balasuriya UB. Evidence that in vitro susceptibility of CD3+ T lymphocytes to equine arteritis virus infection reflects genetic predisposition of naturally infected stallions to become carriers of the virus. J Virol 2012;86:12407–12410.
    doi: 10.1128/JVI.01698-12pmc: PMC3486460pubmed: 22933293google scholar: lookup
  24. Miszczak F, Legrand L, Balasuriya UB, Ferry-Abitbol B, Zhang J, Hans A, Fortier G, Pronost S, Vabret A. Emergence of novel equine arteritis virus (EAV) variants during persistent infection in the stallion: origin of the 2007 French EAV outbreak was linked to an EAV strain present in the semen of a persistently infected carrier stallion. Virology 2012;423:165–174.
    doi: 10.1016/j.virol.2011.11.028pubmed: 22209234google scholar: lookup
  25. Zhang J, Timoney PJ, Shuck KM, Seoul G, Go YY, Lu Z, Powell DG, Meade BJ, Balasuriya UB. Molecular epidemiology and genetic characterization of equine arteritis virus isolates associated with the 2006-2007 multi-state disease occurrence in the USA. J Gen Virol 2010;91:2286–2301.
    doi: 10.1099/vir.0.019737-0pubmed: 20444993google scholar: lookup
  26. Hedges JF, Balasuriya UB, Timoney PJ, McCollum WH, MacLachlan NJ. Genetic divergence with emergence of novel phenotypic variants of equine arteritis virus during persistent infection of stallions. J Virol 1999;73:3672–3681.
    pmc: PMC104142pubmed: 10196259
  27. Balasuriya UB, Hedges JF, Nadler SA, McCollum WH, Timoney PJ, MacLachlan NJ. Genetic stability of equine arteritis virus during horizontal and vertical transmission in an outbreak of equine viral arteritis. J Gen Virol 1999;80:1949–1958.
    doi: 10.1099/0022-1317-80-8-1949pubmed: 10466790google scholar: lookup
  28. Balasuriya UB, Rossitto PV, DeMaula CD, MacLachlan NJ. A 29K envelope glycoprotein of equine arteritis virus expresses neutralization determinants recognized by murine monoclonal antibodies. J Gen Virol 1993;74(Pt 11):2525–2529.
    doi: 10.1099/0022-1317-74-11-2525pubmed: 7504076google scholar: lookup
  29. Balasuriya UB, MacLachlan NJ, De Vries AA, Rossitto PV, Rottier PJ. Identification of a neutralization site in the major envelope glycoprotein (GL) of equine arteritis virus. Virology 1995;207:518–527.
    doi: 10.1006/viro.1995.1112pubmed: 7533965google scholar: lookup
  30. Balasuriya UB, Patton JF, Rossitto PV, Timoney PJ, McCollum WH, MacLachlan NJ. Neutralization determinants of laboratory strains and field isolates of equine arteritis virus: identification of four neutralization sites in the amino-terminal ectodomain of the G(L) envelope glycoprotein. Virology 1997;232:114–128.
    doi: 10.1006/viro.1997.8551pubmed: 9185595google scholar: lookup
  31. Balasuriya UB, Dobbe JC, Heidner HW, Smalley VL, Navarrette A, Snijder EJ, MacLachlan NJ. Characterization of the neutralization determinants of equine arteritis virus using recombinant chimeric viruses and site-specific mutagenesis of an infectious cDNA clone. Virology 2004;321:235–246.
    doi: 10.1016/j.virol.2003.12.015pubmed: 15051384google scholar: lookup
  32. Balasuriya UB, MacLachlan NJ. The immune response to equine arteritis virus: potential lessons for other arteriviruses. Vet Immunol Immunopathol 2004;102:107–129.
    doi: 10.1016/j.vetimm.2004.09.003pubmed: 15507299google scholar: lookup
  33. Glaser AL, de Vries AA, Dubovi EJ. Comparison of equine arteritis virus isolates using neutralizing monoclonal antibodies and identification of sequence changes in GL associated with neutralization resistance. J Gen Virol 1995;76(Pt 9):2223–2233.
    doi: 10.1099/0022-1317-76-9-2223pubmed: 7561759google scholar: lookup
  34. Balasuriya UB, Heidner HW, Davis NL, Wagner HM, Hullinger PJ, Hedges JF, Williams JC, Johnston RE, Wilson WD, Liu IK, MacLachlan NJ. Alphavirus replicon particles expressing the two major envelope proteins of equine arteritis virus induce high level protection against challenge with virulent virus in vaccinated horses. Vaccine 2002;20:1609–1617.
    doi: 10.1016/S0264-410X(01)00485-6pubmed: 11858869google scholar: lookup
  35. McCollum WH. Development of a modified virus strain and vaccine for equine viral arteritis. J Am Vet Med Assoc 1969;155:318–322.
    pubmed: 4978804
  36. Fukunaga Y, McCollum WH. Complement-fixation reactions in equine viral arteritis. Am J Vet Res 1977;38:2043–2046.
    pubmed: 202179
  37. McCollum WH, Timoney PJ, Tengelsen LA. Clinical, virological and serological responses of donkeys to intranasal inoculation with the KY-84 strain of equine arteritis virus. J Comp Pathol 1995;112:207–211.
    doi: 10.1016/S0021-9975(05)80062-3pubmed: 7769149google scholar: lookup
  38. MacLachlan NJ, Balasuriya UB, Hedges JF, Schweidler TM, McCollum WH, Timoney PJ, Hullinger PJ, Patton JF. Serologic response of horses to the structural proteins of equine arteritis virus. J Vet Diagn Invest 1998;10:229–236.
    doi: 10.1177/104063879801000302pubmed: 9683071google scholar: lookup
  39. Go YY, Snijder EJ, Timoney PJ, Balasuriya UB. Characterization of equine humoral antibody response to the nonstructural proteins of equine arteritis virus. Clin Vaccine Immunol 2011;18:268–279.
    doi: 10.1128/CVI.00444-10pmc: PMC3067362pubmed: 21147938google scholar: lookup
  40. Carossino M, Loynachan AT, Canisso IF, Campos JR, Nam B, Go YY, Squires EL, Troedsson MHT, Cook RF, Swerczek T, Del Piero F, Bailey E, Timoney PJ, Balasuriya UBR. Equine arteritis virus has specific tropism for stromal cells and CD8+ T and CD21+ B lymphocytes but not for glandular epithelium at the primary site of persistent infection in the stallion reproductive tract. J Virol 2017;91:e00418-17.
    doi: 10.1128/JVI.00418-17pmc: PMC5469258pubmed: 28424285google scholar: lookup
  41. Campos JR, Breheny P, Araujo RR, Troedsson MH, Squires EL, Timoney PJ, Balasuriya UB. Semen quality of stallions challenged with the Kentucky 84 strain of equine arteritis virus. Theriogenology 2014;82:1068–1079.
  42. Keggan A, Freer H, Rollins A, Wagner B. Production of seven monoclonal equine immunoglobulins isotyped by multiplex analysis. Vet Immunol Immunopathol 2013;153:187–193.
  43. Wagner B. Immunoglobulins and immunoglobulin genes of the horse. Dev Comp Immunol 2006;30:155–164.
    doi: 10.1016/j.dci.2005.06.008pubmed: 16046236google scholar: lookup
  44. Lewis MJ, Wagner B, Woof JM. The different effector function capabilities of the seven equine IgG subclasses have implications for vaccine strategies. Mol Immunol 2008;45:818–827.
  45. Goodman LB, Wimer C, Dubovi EJ, Gold C, Wagner B. Immunological correlates of vaccination and infection for equine herpesvirus 1. Clin Vaccine Immunol 2012;19:235–241.
    doi: 10.1128/CVI.05522-11pmc: PMC3272919pubmed: 22205656google scholar: lookup
  46. Wagner B, Goodman LB, Babasyan S, Freer H, Torsteinsdottir S, Svansson V, Bjornsdottir S, Perkins GA. Antibody and cellular immune responses of naive mares to repeated vaccination with an inactivated equine herpesvirus vaccine. Vaccine 2015;33:5588–5597.
    doi: 10.1016/j.vaccine.2015.09.009pubmed: 26384446google scholar: lookup
  47. Khatibzadeh SM, Gold CB, Keggan AE, Perkins GA, Glaser AL, Dubovi EJ, Wagner B. West Nile virus-specific immunoglobulin isotype responses in vaccinated and infected horses. Am J Vet Res 2015;76:92–100.
    doi: 10.2460/ajvr.76.1.92pmc: PMC10959050pubmed: 25535666google scholar: lookup
  48. Soboll Hussey G, Hussey SB, Wagner B, Horohov DW, Van de Walle GR, Osterrieder N, Goehring LS, Rao S, Lunn DP. Evaluation of immune responses following infection of ponies with an EHV-1 ORF1/2 deletion mutant. Vet Res 2011;42:23.
    doi: 10.1186/1297-9716-42-23pmc: PMC3045331pubmed: 21314906google scholar: lookup
  49. Soboll G, Horohov DW, Aldridge BM, Olsen CW, McGregor MW, Drape RJ, Macklin MD, Swain WF, Lunn DP. Regional antibody and cellular immune responses to equine influenza virus infection, and particle mediated DNA vaccination. Vet Immunol Immunopathol 2003;94:47–62.
    doi: 10.1016/S0165-2427(03)00060-6pubmed: 12842611google scholar: lookup
  50. Hardiyanto L, Hasegawa A, Komori S. The N-linked carbohydrate moiety of male reproductive tract CD52 (mrt-CD52) interferes with the complement system via binding to C1q. J Reprod Immunol 2012;94:142–150.
    doi: 10.1016/j.jri.2012.01.002pubmed: 22386526google scholar: lookup
  51. Petersen BH, Lammel CJ, Stites DP, Brooks GF. Human seminal plasma inhibition of complement. J Lab Clin Med 1980;96:582–591.
    pubmed: 6775032
  52. Brooks GF, Lammel CJ, Petersen BH, Stites DP. Human seminal plasma inhibition of antibody complement-mediated killing and opsonization of Neisseria gonorrhoeae and other gram-negative organisms. J Clin Invest 1981;67:1523–1531.
    doi: 10.1172/JCI110183pmc: PMC370721pubmed: 6785314google scholar: lookup
  53. Troedsson MH, Loset K, Alghamdi AM, Dahms B, Crabo BG. Interaction between equine semen and the endometrium: the inflammatory response to semen. Anim Reprod Sci 2001;68:273–278.
    doi: 10.1016/S0378-4320(01)00164-6pubmed: 11744271google scholar: lookup
  54. Altan-Bonnet N. Extracellular vesicles are the Trojan horses of viral infection. Curr Opin Microbiol 2016;32:77–81.
    doi: 10.1016/j.mib.2016.05.004pmc: PMC4983493pubmed: 27232382google scholar: lookup
  55. Roos A, Bouwman LH, van Gijlswijk-Janssen DJ, Faber-Krol MC, Stahl GL, Daha MR. Human IgA activates the complement system via the mannan-binding lectin pathway. J Immunol 2001;167:2861–2868.
    doi: 10.4049/jimmunol.167.5.2861pubmed: 11509633google scholar: lookup
  56. Kaetzel CS. The polymeric immunoglobulin receptor: bridging innate and adaptive immune responses at mucosal surfaces. Immunol Rev 2005;206:83–99.
  57. Spiekermann GM, Finn PW, Ward ES, Dumont J, Dickinson BL, Blumberg RS, Lencer WI. Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life: functional expression of FcRn in the mammalian lung. J Exp Med 2002;196:303–310.
    doi: 10.1084/jem.20020400pmc: PMC2193935pubmed: 12163559google scholar: lookup
  58. Dickinson BL, Badizadegan K, Wu Z, Ahouse JC, Zhu X, Simister NE, Blumberg RS, Lencer WI. Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J Clin Invest 1999;104:903–911.
    doi: 10.1172/JCI6968pmc: PMC408555pubmed: 10510331google scholar: lookup
  59. Hedges JF, Demaula CD, Moore BD, McLaughlin BE, Simon SI, MacLachlan NJ. Characterization of equine E-selectin. Immunology 2001;103:498–504.
  60. World Organization for Animal Health (OIE). Equine viral arteritis. 2016.
  61. National Research Council. Guide for the care and use of laboratory animals. 2011.
  62. Balasuriya UB, Snijder EJ, Heidner HW, Zhang J, Zevenhoven-Dobbe JC, Boone JD, McCollum WH, Timoney PJ, MacLachlan NJ. Development and characterization of an infectious cDNA clone of the virulent Bucyrus strain of equine arteritis virus. J Gen Virol 2007;88:918–924.
    doi: 10.1099/vir.0.82415-0pubmed: 17325365google scholar: lookup
  63. Wagner B, Glaser A, Hillegas JM, Erb H, Gold C, Freer H. Monoclonal antibodies to equine IgM improve the sensitivity of West Nile virus-specific IgM detection in horses. Vet Immunol Immunopathol 2008;122:46–56.
    doi: 10.1016/j.vetimm.2007.10.013pubmed: 18054390google scholar: lookup
  64. Sheoran AS, Timoney JF, Holmes MA, Karzenski SS, Crisman MV. Immunoglobulin isotypes in sera and nasal mucosal secretions and their neonatal transfer and distribution in horses. Am J Vet Res 2000;61:1099–1105.
    doi: 10.2460/ajvr.2000.61.1099pubmed: 10976743google scholar: lookup
  65. Sheoran AS, Lunn DP, Holmes MA. Monoclonal antibodies to subclass-specific antigenic determinants on equine immunoglobulin gamma chains and their characterization. Vet Immunol Immunopathol 1998;62:153–165.
    doi: 10.1016/S0165-2427(97)00162-1pubmed: 9638859google scholar: lookup
  66. Go YY, Zhang J, Timoney PJ, Cook RF, Horohov DW, Balasuriya UB. Complex interactions between the major and minor envelope proteins of equine arteritis virus determine its tropism for equine CD3+ T lymphocytes and CD14+ monocytes. J Virol 2010;84:4898–4911.
    doi: 10.1128/JVI.02743-09pmc: PMC2863813pubmed: 20219931google scholar: lookup
  67. MacLachlan NJ, Balasuriya UB, Rossitto PV, Hullinger PA, Patton JF, Wilson WD. Fatal experimental equine arteritis virus infection of a pregnant mare: immunohistochemical staining of viral antigens. J Vet Diagn Invest 1996;8:367–374.
    doi: 10.1177/104063879600800316pubmed: 8844583google scholar: lookup
  68. Go YY, Wong SJ, Branscum AJ, Demarest VL, Shuck KM, Vickers ML, Zhang J, McCollum WH, Timoney PJ, Balasuriya UB. Development of a fluorescent-microsphere immunoassay for detection of antibodies specific to equine arteritis virus and comparison with the virus neutralization test. Clin Vaccine Immunol 2008;15:76–87.
    doi: 10.1128/CVI.00388-07pmc: PMC2223870pubmed: 18032597google scholar: lookup