Porcine reproductive and respiratory syndrome (PRRS): An immune dysregulatory pandemic

Immunologic Research

Volumn 59, Issue 1-3, 2014, Pages 81-108

  Butler, J E ^a   Lager, K M ^b   Golde, William ^c   Faaberg, Kay S ^b   Sinkora, Marek ^d   Loving, Crystal ^b   Zhang, Y I ^e  

^a UNIVERSITY OF IOWA   (United States)

^b NATIONAL ANIMAL DISEASE CENTER   (United States)

^c PLUM ISLAND ANIMAL DISEASE CENTER   (United States)

^d INSTITUTE OF MATHEMATICS   (Czech Republic)

^e UNIVERSITY OF MARYLAND   (United States)

Author keywords

Arterivirus; Economic loss; Hypothesis; Immune dysregulation; Pandemic

Indexed keywords

ARTERIVIRUS; B LYMPHOCYTE; HUMORAL IMMUNITY; IMMUNE DYSREGULATION; IMMUNE RESPONSE; IMMUNOMODULATION; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; LYMPHOCYTOPENIA; MACROPHAGE; NONHUMAN; PANDEMIC; PLASMACYTOID DENDRITIC CELL; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PRIORITY JOURNAL; REVIEW; THYMUS ATROPHY; ANIMAL; ART; CELL PROLIFERATION; DENDRITIC CELL; IMMUNOLOGY; PATHOLOGY; PLASMA CELL; SWINE; VIROLOGY;

ANIMALS; CELL PROLIFERATION; DENDRITIC CELLS; IMMUNITY, INNATE; MACROPHAGES; PANDEMICS; PLASMA CELLS; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; PORTRAITS AS TOPIC; SWINE;

EID: 84905743866     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-014-8549-5     Document Type: Review

References (248)

1. Rossow KD. Porcine reproductive and respiratory syndrome. Vet Path. 1998;35:1-20. (Pubitemid 128472843)
2. Albina E. Epidemiology of porcine reproductive and respiratory syndrome (PRRS): an overview. Vet Microbiol. 1997;55:309-16. (Pubitemid 27286226)
3. Collins JE, Benfield DA, Christianson WT, Harris L, Hennings JC, Shaw DP, Goyal SM, McCullough S, Morrison RB, Joo HS, et al. Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. J Vet Diagn Invest. 1992;4:117-26.
4. Wensvoort G, Terpstra C, Pol JM, ter Laak EA, Bloemraad M, de Kluyver EP, Kragten C, van Buiten L, den Besten A, Wagenaar F, et al. Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q. 1991;13:121-30.
5. 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;156:418-24.
6. Faaberg KS, Balasuriya UB, Brinton MA, Gorbalenya AE, Leung FC, Nauwynck H, Snijder EJ, Stadejek T, Yang H, Yoo D. Family Arteriviridae. In: King AMQ, editor. Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses. Amsterdam: Elsevier/Academic Press; 2012. p. 796-805.
7. Christianson WT, Choi CS, Collins JE, et al. Pathogenesis of porcine reproductive and respiratory syndrome virus infection in mid-gestation sows and fetuses. Can J Vet Res. 1993;57:262-8.
8. Feng WH, Laster M, et al. In vitro infection by procine reproductive and respiratory syndrome virus is sufficient to increase susceptibility of piglets to challenge by Streptococcus suis type II. J Virol. 2001;75:4889-91.
9. Butler JE. Immunoglobulins of the mammary secretions. In: Larson BL, Smith V, editors. Lactation, a comprehensive treatise, vol. 3. New York: Academic Press; 1974. p. 217-55.
10. Balasuriya UBR, MacLachlan NJ. The immune responses to equine arteritis virus: potential lessons for other Arteriviruses. Vet Immunol Immunopath. 2004;102:107-29. (Pubitemid 39422638)
11. Plagemann PG, Jones QA, Cafruny WA. Polyclonal activation of B cells by lactate dehydrogenase-elevating virus is mediated by N-glycans on short ectodomains of the primary envelope glycoprotein. Adv Exp Med Biol. 2001;494:375-84. (Pubitemid 34101954)
12. Rowland RR. The interaction between PRRSV and the late gestation pig fetus. Virus Res. 2010;154:114-22.
13. Rossow KD, Collins JE, Goyal SM, et al. Pathogenesis of porcine reproductive and respiratory syndrome virus infection in gnotobiotic pigs. Vet Pathol. 1995;32:361-73.
14. He Y, Wang G, Liu Y, et al. Characterization of thymus atrophy in piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Vet Microbiol. 2012;160:455-62.
15. Guo B, Lager KM, Henningson JN, Miller LC, Schlink SN, Kappes MA, Kehrli ME Jr, Brockmeier SL, Nicholson TL, Yang H-C, Faaberg KS. Experimental infection of United States swine with a Chinese highly pathogenic strain of porcine reproductive and respiratory syndrome virus. Virology. 2013;435:372-84.
16. Murtaugh MP, Ziao Z, Zuckermann F. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infections. Viral Immunol. 2002;15:533-47. (Pubitemid 35448769)
17. Murtaugh MP, Genzow M. Immunological solutions for treatment and prevention of porcine reproductive and respiratory syndrome (PRRS). Vaccine. 2011;29:8192-204.
18. Neumann EJ, Kliebenstein JB, Johnson CD, Mabry JW, Bush EJ, Seitzinger AH, Green AL, Zimmerman JJ. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J Am Vet Med Assoc. 2005;227:385-92. (Pubitemid 41098522)
19. Raymond C, Wilkie BN. Natural killer cell frequency and function in pigs selectively bred for high and low antibody and cell-mediated immune response: response to vaccination with modified live transmissible gastroenteritis virus. Nat Immuno. 1998;16:18-26. (Pubitemid 28499443)
20. Guderian H. Panzer leader. New York: E.P. Dutton & Co; 1952.
21. Coutelier JP, Coulie PG, Wauters P, Heremans H, der Logt JT. In vivo polyclonal B-lymphocyte activation elicited by murine viruses. J Virol. 1990;64:5383-8. (Pubitemid 20364529)
22. Lemke CD, Haynes JS, Spaete R, et al. Lymphoid hyperplasia resulting in immune dysregulation is caused by porcine reproductive and respiratory syndrome virus infection in neonatal pigs. J Immunol. 2004;172:1916-25. (Pubitemid 38116842)
23. Hunziker L, Recher M, Macpherson AJ, Ciurea A, Freigand S, Hengartner H, et al. Hypergammaglobulinemia and autoantibody induction mechanisms in viral infection. Nat Immunol. 2003;4:343-9. (Pubitemid 36432316)
24. Goens SD. The evolution of bovine viral diarrhea: a review. Can Vet J. 2002;43:946-54. (Pubitemid 36267498)
25. Brockmeier SL, et al. Effect of intranasal inoculation with Bordetella bronchiseptica, porcine reproductive and respiratory syndrome virus, or a combination of both organisms on subsequent infection with Pasturella multocida in pigs. Am J Vet Res. 2001;62:521-5. (Pubitemid 33605771)
26. Xu M, et al. Secondary infection with Streptococcus suis serotype 7 increase the virulence of highly pathogenic porcine reproductive and respiratory syndrome virus in pigs. Virol J. 2010;7:184.
27. Renukaradhya GJ, Alekseev K, Jong K, Fang Y, Saif LJ. Porcine reproductive and respiratory syndrome virus-induced suppression exacerbates the inflammatory response to porcine respiratory coronavirus in pigs. Viral Immunol. 2010;23:457-66.
28. van Reeth K, Nauwynck H. Proinflammatory cytokines and viral respiratory disease in pigs. Vet Res. 2000;31:187-213.
29. Kitikoon P, Vincent AL, Jones KR, Nuluboi D, Yu S, Janke BH, Thacker BJ, Thacker EL. Vaccine efficacy and immune response to swine influenza virus challenge in pigs infected with porcine reproductive and respiratory syndrome virus at the time of SIV vaccination. Vet Microbiol. 2009;139:235-44.
30. Thacker EL, Thacker BLJ, Young TY, Halbur PG. Effect of vaccination on the potentiation of porcine reproductive and respiratory syndrome virus (PRRSV)-induced pneumonia by Mycoplasma hyopneumoniae . Vaccine. 2000;18:1244-52. (Pubitemid 30001839)
31. Boddicker NJ, Bjorkquest A, Rowland RR, Lunney JK, Reey JM, Dekkers JC. Genome-wide associated and genomic prediction for host response to porcine reproductive and respiratory syndrome virus infection. Genet Sel Evol. 2014;46:18.
32. Robinson S, Schwartz J, Murtaugh M. Humoral response to porcine reproductive and respiratory syndrome virus. Oroc. 10th Int'l Vet. Immunol. Symposium (IVIS) 2013. Abstract P05.17, p 82.
33. Sanz-Parra A, Sobrino F, Ley V. Infection with foot-and-mouth disease virus results in a rapid reduction of MHC class I surface expression. J Gen Virol. 1998;79:433-6. (Pubitemid 28115865)
34. Khanna R, Burrows SR, Steigerwald-Mullen PM, Thonson SA, Kurilla MG, Moss DJ. Isolation of cytotoxic lymphocytes from healthy seropositive individuals specific for peptide epitopes from Epstein-Barr virus nuclear antigen 1: implications for viral persistence and tumor surveillance. Virology. 1995;214:633-7.
35. Gilbert MJ, Riddell SR, Li CR, Greenberg PD. Selective interference with class I major histocompatibility complex presentation of the major immediate-early proteins following infection with human cytomegalovirus. J Virol. 1993;67:3461-9. (Pubitemid 23143723)
36. Ahn K, Meyer TH, Uebel S, Sempe P, Djaballah H, Yang Y, Peterson PA, Fruh K, Tampe R. Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J. 1996;15:3247-55. (Pubitemid 26231930)
37. Lacaille VG, Androlewicz MJ. Herpes simplex virus inhibitor ICP47 destabilizes the transporter associated with antigen processing (YTAP) heterodimer. J Biol Chem. 1998;273:17386-90. (Pubitemid 28355065)
38. Cox JH, Bennink JR, Yewdell JW. Retention of adenovirus E19 glycoprotein in the endoplasmic reticulum is essential to its ability to block antigen presentation. J Exp Med. 1991;174:1629-37.
39. Tortorella D, Story CM, Huppa JB, Wiertz EJ, Jones TR, Bacik I, Benick JR, Yewdell JW, Ploegh HL. Dissociation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential. J Cell Biol. 1998;142:365376.
40. Piguet V, Schwartz O, Le Gall S, Trono D. The downregulation of CD4 and MHC-I by primate lentiviruses: a paradigm for the modulation of cell surface receptors. Immunol Rev. 1999;168:51-63. (Pubitemid 29276672)
41. Tong X, Boll W, Kirchhausen T, Howley PM. Interaction of the bovine papillomavirus E6 qirh rhw clathrin adapter complex. AP-1. J Virol. 1998;72:476-82. (Pubitemid 28048861)
42. Rinaldo CR. Modulation of the major histocompatibility complex antigen expression by viral infection. Am J Pathol. 1994;144:637-50.
43. Barry M, McFadden G. Apoptosis regulators from DNA viruses. Curr Opin Immunol. 1998;10:422-30. (Pubitemid 28393825)
44. Toka FN, Kenney M, Golde WT. Rapid and transient activation of cdT cells to interferon gamma production, NK cell-like killing and antigen processing during acute virus infection. J Immunol. 2011;186:4853-61.
45. Elsing A, Burgert HG. The adenovirus E3/10.4K-14.5 proteins down modulate the apoptosis receptor Fas/Apo-1 by inducing its internalization. Proc Natl Acad Sci USA. 1998;95:10072-746.
46. Tortorella D, Gewurz BE, Furman MH, Schust DJ, Ploegh HL. Subverison of the immune system. Ann Rev Immunol. 2000;18(861-926):47.
47. Pierson TC, Fremont DH, Kun RJ, Diamond MS. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe. 2008;4:229-38.
48. Dempsey PW, Allison ME, Akkaraju S, Goodnow CC, Fearon DT. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science. 1996;271:348-50.
49. Phillips NE, Parker DC. Fc-dependent inhibition of mouse B cell activation by whole anti-mu antibodies. J Immunol. 1983;130:602-6. (Pubitemid 13186273)
50. Ravenol K, Castelle C, Defranc T, Wild TF, Charron D, Lotteau V, Rabourdin-Combe C. Measles virus nucleocapsid protein binds to FcgammaRII and inhibits human B cell antibody production. J Exp Med. 1997;186:269-78. (Pubitemid 27328027)
51. Goncalvez AP, Engle RE, St.Claire M, Purcell RH, Lai CJ. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA. 2007;104:9422-7. (Pubitemid 47185795)
52. Vaugn DW, Green S, Kalayanarooj S, Innis S, Nimmannitya S, et al. Dengue viremia titer, antibody response pattern and virus serotype correlate with disease severity. J Infect Dis. 2000;181:2-9. (Pubitemid 30049026)
53. Kotwal GJ, Isaacs SN, McKenzie R, Frank MM, Moss B. Inhibition of the complement cascade by the major secretory protein of vaccine virus. Science. 1990;250:827-30.
54. McKenzie R, Kotwal GJ, Moss B, Hammer CH, Frank MM. Regulation of complement activity by vaccinia virus complement-control protein. J Infect Dis. 1992;166:1245-50.
55. McNearney TA, Odell C, Holerd VM, Spear PG, Atkinson JP. Herpes simplex virus glycoproteins gC-1 and gC-2 bind to the third component of complement and provide protection against complement-mediated neutralization of viral infectivity. J Exp Med. 1987;166:1525-35. (Pubitemid 18051441)
56. Friedman HM, Wang L, Fisman NOO, Lambris JD, Eisenberg RJ, Cohen GH, Lubinski J. Immune evasion properties of herpes simplex virus type 1 glycoprotein gC. J Virol. 1996;70:4253-60. (Pubitemid 26187425)
57. Weiland E, Weilabnd F, Grossman A. Lactate dehydrogenase-elevating virus induces anti-Golgi apparatus antibodies. J Gen Virol. 1987;68:1983-91. (Pubitemid 17120448)
58. Cafruny WA, Hovinen DE. Infection of mice with lactate dehydrogenase-elevating virus leads to stimulation of autoantibodies. J Gen Virol. 1988;69:723-9. (Pubitemid 18085891)
59. Weiland E, Weiland F. Autoantibodies against Golgi apparatus induced by Arteriviruses. Cell Mol Biol. 2002;48:279-84.
60. Grossmann A, Weiland F, Weiland E. Autoimmunity induced by lactate dehydrogenase-elevating virus: monoclonal autoantibodies against Golgi antigens and other subcellular elements. Autoimmunity. 1989;2:201-11. (Pubitemid 19061644)
61. Lamontague L, Page C, Larochelle R, Magar R. Polyclonal activation of B cells occurs in lymphoid organs from porcine reproductive and respiratory syndrome virus (PRRSV)-induced pigs. Vet Immunol Immunopathol. 2003;82:165-82.
62. Rowland RR, Even C, Anderson GW, Chen Z, Hu B, Plagemann PGW. Neonatal infection of mice with lactate dehydrogenase-elevating virus results in suppression of humoral anti-viral immune response but does not alter the course of viremia or the polyclonal activation of B cells and immune complex formation. J Gen Virol. 1994;75:1071-81. (Pubitemid 24143152)
63. Flavell KJ, Murray PG. Hodgkins disease and the Epstein-Barr virus. Mol Pathol. 2000;53:262-9.
64. Heil F, Ahmad-Nejad P, Hemmi H, Hochrein H, Ampenberger F, Gellert T, Dietrich H, Lipford G, Takeda K, Akira S, Wagner H, Bauer S. The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily. Eur J Immunol. 2003;33:2987-97. (Pubitemid 37428331)
65. Kawai T, Akira S. Innate immune recognition of viral infection. Nat Immunol. 2006;7:131-7. (Pubitemid 43135878)
66. Gonzalez-Navajas JM, Lee J, David M, Raz E. Immunomodulatory functions of type I interferons. Nat Rev Immunol. 2012;12:125-35.
67. Takaoka A, Yanai H. Interferon signalling network in innate defence. Cell Microbiol. 2006;8:907-22. (Pubitemid 43670834)
68. Brockmeier SL, Lager KM, Grubman MJ, Brough DE, Ettyreddy D, Sacco RE, Gauger PC, Loving CL, Vorwald AC, Kehrli ME Jr, Lehmkuhl HD. Adenovirus-mediated expression of interferon-alpha delays viral replication and reduces disease signs in swine challenged with porcine reproductive and respiratory syndrome virus. Viral Immunol. 2009;22:173-80.
69. Brockmeier SL, Loving CL, Nelson EA, Miller LC, Nicholson TL, Register KB, Grubman MJ, Brough DE, Kehrli ME Jr. The presence of alpha interferon at the time of infection alters the innate and adaptive immune responses to porcine reproductive and respiratory syndrome virus. Clin Vaccine Immunol. 2012;19:508-14.
70. Albina E, Carrat C, Charley B. Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J Interferon Cytokine Res. 1998;18:485-90. (Pubitemid 28363575)
71. Buddaert W, Van Reeth K, Pensaert M. In vivo and in vitro interferon (IFN) studies with the porcine reproductive and respiratory syndrome virus (PRRSV). Adv Exp Med Biol. 1998;440:461-7. (Pubitemid 28405924)
72. Calzada-Nova G, Schnitzlein W, Husmann R, Zuckermann FA. Characterization of the cytokine and maturation responses of pure populations of porcine plasmacytoid dendritic cells to porcine viruses and toll-like receptor agonists. Vet Immunol Immunopathol. 2010;135:20-33.
73. Calzada-Nova G, Schnitzlein WM, Husmann RJ, Zuckermann FA. North American porcine reproductive and respiratory syndrome viruses inhibit type I interferon production by plasmacytoid dendritic cells. J Virol. 2011;85:2703-13.
74. Loving CL, Brockmeier SL, Sacco RE. Differential type I interferon activation and susceptibility of dendritic cell populations to porcine arterivirus. Immunology. 2007;120:217-29. (Pubitemid 46046321)
75. Miller LC, Laegreid WW, Bono JL, Chitko-McKown CG, Fox JM. Interferon type I response in porcine reproductive and respiratory syndrome virus-infected MARC-145 cells. Arch Virol. 2004;149:2453-63. (Pubitemid 40059343)
76. Sun Y, Han M, Kim C, Calvert JG, Yoo D. Interplay between interferon-mediated innate immunity and porcine reproductive and respiratory syndrome virus. Viruses. 2012;4:424-46.
77. Chen Z, Lawson S, Sun Z, Zhou X, Guan X, Christopher-Hennings J, Nelson EA, Fang Y. Identification of two auto-cleavage products of nonstructural protein 1 (nsp1) in porcine reproductive and respiratory syndrome virus infected cells: nsp1 function as interferon antagonist. Virology. 2010;398:87-97.
78. Beura LK, Sarkar SN, Kwon B, Subramaniam S, Jones C, Pattnaik AK, Osorio FA. Porcine reproductive and respiratory syndrome virus nonstructural protein 1beta modulates host innate immune response by antagonizing IRF3 activation. J Virol. 2010;84:1574-84.
79. Kim O, Sun Y, Lai FW, Song C, Yoo D. Modulation of type I interferon induction by porcine reproductive and respiratory syndrome virus and degradation of CREB-binding protein by non-structural protein 1 in MARC-145 and HeLa cells. Virology. 2010;402:315-26.
80. Sun Z, Chen Z, Lawson SR, Fang Y. The cysteine domain of porcine reproductive and respiratory syndrome virus nonstructural protein 2 possesses deubiquitinating and interferon antagonism functions. J Virol. 2010;84:7832-46.
81. Sun Z, Li Y, Ransburgh R, Snijder EJ, Fang Y. Nonstructural protein 2 of porcine reproductive and respiratory syndrome virus inhibits the antiviral function of interferon-stimulated gene 15. J Virol. 2012;86:3839-50.
82. Sagong M, Lee C. Porcine reproductive and respiratory syndrome virus nucleocapsid protein modulates interferon-beta production by inhibiting IRF3 activation in immortalized porcine alveolar macrophages. Arch Virol. 2011;156:2187-95.
83. Darnell JE Jr, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science. 1994;264:1415-21. (Pubitemid 24217131)
84. Patel D, Nan Y, Shen M, Ritthipichai K, Zhu X, Zhang YJ. Porcine reproductive and respiratory syndrome virus inhibits type I interferon signaling by blocking STAT1/STAT2 nuclear translocation. J Virol. 2010;84:11045-55.
85. Wang R, Nan Y, Yu Y, Yang Z, Zhang YJ. Variable interference with interferon signal transduction by different strains of porcine reproductive and respiratory syndrome virus. Vet Microbiol. 2013;166:493-503.
86. Wang R, Nan Y, Yu Y, Zhang YJ. Porcine reproductive and respiratory syndrome virus Nsp1beta inhibits interferon-activated JAK/STAT signal transduction by inducing karyopherinalpha1 degradation. J Virol. 2013;87:5219-28.
87. Lee C, Hodgins D, Calvert JG, Welch SK, Jolie R, Yoo D. Mutations within the nuclear localization signal of the porcine reproductive and respiratory syndrome virus nucleocapsid protein attenuate virus replication. Virology. 2006;346:238-50. (Pubitemid 43254714)
88. Zhang H, Guo X, Nelson E, Christopher-Hennings J, Wang X. Porcine reproductive and respiratory syndrome virus activates the transcription of interferon alpha/beta (IFN-alpha/beta) in monocyte-derived dendritic cells (Mo-DC). Vet Microbiol. 2012;159:494-8.
89. Luo R, Xiao S, Jiang Y, Jin H, Wang D, Liu M, Chen H, Fang L. Porcine reproductive and respiratory syndrome virus (PRRSV) suppresses interferon-beta production by interfering with the RIG-I signaling pathway. Mol Immunol. 2008;45:2839-46.
90. Baumann A, Mateu E, Murtaugh MP, Summerfield A. Impact of genotype 1 and 2 of porcine reproductive and respiratory syndrome viruses on interferon-alpha responses by plasmacytoid dendritic cells. Vet Res. 2013;44:33.
91. Nan Y, Wang R, Shen M, Faaberg KS, Samal SK, Zhang YJ. Induction of type I interferons by a novel porcine reproductive and respiratory syndrome virus isolate. Virology. 2012;432:261-70.
92. Wang R, Xiao Y, Opriessnig T, Ding Y, Yu Y, Nan Y, Ma Z, Halbur PG, Zhang YJ. Enhancing neutralizing antibody production by an interferon-inducing porcine reproductive and respiratory syndrome virus strain. Vaccine. 2013;31:5537-43.
93. Brown E, Lawson S, Welbon C, Gnanandarajah J, Li J, Murtaugh MP, Nelson EA, Molina RM, Zimmerman JJ, Rowland RR, Fang Y. Antibody response to porcine reproductive and respiratory syndrome virus (PRRSV) nonstructural proteins and implications for diagnostic detection and differentiation of PRRSV types I and II. Clin Vaccine Immunol. 2009;16:628-35.
94. Alexandersen S, Quan M, Murphy C, Knight J, Zhang Z. Studies of quantitative parameters of virus excretion and transmission in pigs and cattle experimentally infected with foot-and-mouth disease virus. J Comp Pathol. 2003;129:268-82. (Pubitemid 37321492)
95. Allende R, Laegieid WW, Kutish GF, Galesta JA, Wills RW, Ososrio FA. Porcine reproductive and respiratory syndrome virus: description of persistence in individual pigs upon experimental infection. J Virol. 2000;74:10834-7.
96. Wills RW, Doster AR, Galeota JA, Sur JH, Osorio FA. Duration of infection and proportion of pigs persistently infected with porcine reproductive and respiratory syndrome virus. J Clin Microbiol. 2004;41:58-62.
97. Mulupuri P, Zimmerman JJ, Hermann J, Johnson CR, Cano JP, Yu W, Dee SA, Murtaugh MP. Antigen-specific B cell responses to porcine reproductive and respiratory syndrome virus infection. J Virol. 2008;82:358-70. (Pubitemid 350309151)
98. Yoo D, Song C, Sun Y, Du Y, Kim O, Liu HC. Modulation of host cell responses and evasion strategies for porcine reproductive and respiratory syndrome virus. Virus Res. 2010;154:48-60.
99. Benfield DA, Nelson E, Collins JE, Harris L, Goyal SM, Robison D, Christianson WT, Morrison RB, Gorcyca D, Chladek D. Characterization ofswine infertility and respiratory syndrome(SIRS) virus (isolate ATCC VR-2332). J Vet Diagn Invest. 1992;4:127-33.
100. Nelson EA, Christopher-Hennings J, Benfield DA. Serum immune response to the proteins of porcine reproductive and respiratory syndrome (PRRS) virus. J Vet Diagn Invest. 1994;6:410-5.
101. Lopez OJ, Oliveira MF, Alvarez-Garcia E, Kwon BJ, Doster A, Osoria FA. Protection against porcine reproductive and respiratory syndrome virus (PRRSV) infection through passive transfer of PRRSV-neutralizing antibodies is dose dependent. Clin Vaccine Immunol. 2007;14:269-75. (Pubitemid 46570283)
102. Vezina SA, Loemba H, Foutnier M, Dea S, Archibault D. Antibody production and blastogenesis response in pigs experimentally infected with porcine reproductive and respiratory syndrome virus. Can J Vet Res. 1996;60:94-9. (Pubitemid 126525775)
103. Mateu E, Diaz I. The challenge of PRRS immunology. Vet J. 2008;177:345-51. (Pubitemid 351899463)
104. Plagemann PG, Rowland RR, Faaberg KS. The primary neutralization epitope of porcine respiratory and reproductive syndrome virus strain VR-2332 is located in the middle of the GP5 ectodomain. Arch Virol. 2002;147:2327-47. (Pubitemid 36058931)
105. Wissink EH, van Wijk HA, Kroese MV, Weiland E, Meulenberg JI, Rottier PJ, et al. The major envelope proteins GP5 of a European reproductive and respiratory syndrome virus contains a neutralizing epitope in it N-terminal ectodomain. J Gen Virol. 2003;84:1535-43. (Pubitemid 36675524)
106. Weiland E, Wieczorek-Krohmer M, Kohl D, Conzelmann KK, Weiland F. Monoclonal antibodies to the GP5 of porcine reproductive and respiratory syndrome virus are more effective in virus neutralization than monoclonal antibodies to the GP4. Vet Microbiol. 1999;66:171-86. (Pubitemid 29179561)
107. Li J, Murtaugh MP. Dissociation of porcine reproductive and respiratory syndrome virus neutralization from antibodies specific to major envelope protein surface epitopes. Virology. 2012;433:367-76.
108. Vanhee M, Breedam W, Costers S, Geldhof M, Noppe Y, Nauwynck H. Characterization of antigenic regions in the porcine reproductive and respiratory syndrome virus by the use of peptide-specific serum antibodies. Vaccine. 2011;29:4794-804.
109. Lu Z, Zhang JK, Huang CM, Go YY, Faaber KS, Roland RR, Timoney PJ, Balasuriya UBR. Chimeric viruses containing the N-terminal ectodomains of GP5 and M proteins of porcine reproductive and respiratory syndrome virus do not change the cellular tropism of equine arteritis virus. Virology. 2012;432:99-109.
110. Diaz I, Darwich L, Pappaterra G, Pujois J, Mateu E. Different European-type vaccines against porcine reproductive and respiratory syndrome virus have different immunological properties and confer different protection to pigs. Virology. 2006;351:249-59. (Pubitemid 44108075)
111. Muelenberg JJ, van Nieuwstadt AP, van Essen-Zandergeht A, Langevald JP. Posttranslational processing and identification of a neutralization domain of the GP4 protein encoded in ORF4 of the Lelystadt virus. J Virol. 1997;71:6061-7.
112. Osorio FA, Galeota JA, Nelson E, Brodersen B, Doster A, Wills R, Zuckermann F, Laegreid WW. Passive transfer of virus-specific antibodies confer protection against reproductive failure induced by a virulent strain of porcine reproductive and respiratory syndrome virus and establishes sterilizing immunity. Virology. 2002;301:9-20. (Pubitemid 35356851)
113. Labarque GG, Nauwynck HJ, Van Reeth K, Pensaert MB. Effect of cellular changes and onset of humoral immunity on the replication of porcine reproductive and respiratory syndrome virus in the lungs of pigs. J Gen Virol. 2000;81:1327-34. (Pubitemid 30232719)
114. Drew TW. A review of evidence for immunosuppression due to porcine reproductive and respiratory syndrome virus. Vet Res. 2000;31:27-39.
115. Wongyanin P, Buranapradikun S, Yoo D, Thanawongnuwech R, Roth JA, Suradhat S. Role of porcine reproductive and respiratory syndrome virus Nucleocapsid protein in induction of interleukin-10 and regulatory T-lymphocytes (Treg). J Gen Virol. 2012;93:1236-46.
116. Wongyanin P, Buranapradikun S, Chokeshai-usaha K, Thanawongnuwech R, Suradhat S. Induction of inducible CD4+ CD25+ Foxp3+ regulatory T lymphocytes by porcine reproductive and respiratory syndrome virus (PRRSV). Vet Immunol Immunopathol. 2010;133:170-82.
117. Silva-Campa E, Mata-Haro V, Mateu E, Hernandez J. Porcine reproductive and respiratory syndrome virus induces CD4+ CD25+ Foxp3+ regulatory T cells (Tregs). Virology. 2012;430:73-80.
118. Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol. 2001;2:725-31. (Pubitemid 32747162)
119. Sinkora M, Butler JE, Lager KM, Potockova H, Sinkorova J. Comparative lymphocyte profile and the T and B cell spectra-type of germfree piglets infected with three important viruses. 2014. (In press).
120. Feng WH, Tompkins MB, Xu J-S, Brown TT, Laster SM, Xhang H-X, McCaw MB. Thymocyte and peripheral blood T lymphocyte subpopulation changes in piglets following in utero infection with porcine reproductive and respiratory syndrome virus. Virology. 2002;302:63-372.
121. Klinge KL, Vaugn EM, Roof MB, Bautista EM, Murtaugh MP. Age- dependent resistance to porcine reproductive and respiratory syndrome virus replication in swine. Virol J. 2009;6:177.
122. Vashisht K, Goldberg TL, Husmann KJ, Schnitzlein W, Zuckermann FA. Identification of immunodominant T cell epitopes present in glycoprotein 5 of the North American genotype of porcine reproductive and respiratory syndrome virus. Vaccine. 2008;S26:4747-53.
123. Bautista EM, Molitor TW. Cell-mediated immunity to porcine reproductive and respiratory syndrome virus in swine. Viral Immunol. 1997;10:83-94. (Pubitemid 27326747)
124. Lager KM, Mengling WI, Brockmeier SL. Evaluation of protective immunity in gilts inoculated with the NADC-8 isolate of porcine reproductive and respiratory syndrome virus (PRRSV) and challenged-exposed with an antigenically distinct isolate. Am J Vet Res. 1999;60:1022-7. (Pubitemid 129532661)
125. Corzo CA, Mondaca E, Wayne S, Torremorell M, Dee S, David P, et al. Control and elimination of porcine reproductive and respiratory syndrome virus. Virus Res. 2010;154:185-92.
126. Schaefer N, Morrison R. Effect on total pigs weaned of herd closure for elimination of porcine reproductive and respiratory syndrome virus. J Swine Health Prod. 2007;15:152-5. (Pubitemid 46749152)
127. Costers S, Lefebrve DJ, Goddeersi B, Deputte PL, Nauwycnck HJ. Functional impairment of PRRSV-specific peripheral CD3+ CD8 high cell. Vet Res. 2009;40:46.
128. Zhou P, Shaffer DR, Alvarez-Arias DA, Nakazaki Y, Pos W, Torres AJ, Cremasco V, Dougan SK, Cowley GS, Elpek K, Brogdon J, Lamb J, Turley SJ, Ploegh HL, Root DE, Love JC, Dranoff G, Hacohen N, Cantor H, Wucherpfennig KW. In vivo discovery of immunotherapy targets in the tumour microenvironment. Nature. 2014;506:52-7.
129. Liao Y-C, Lin H-H, Lin C-H, Chun W-B. Identification of cytotoxic T lymphocyte epitopes on swine viruses: multi-epitope design for universal T cell vaccine. PLoS One. 2013;8(12):e84443. PMCID: PMC3866179.
130. Olin MR, Bastista L, Xiao Z, Dee SA, Mirtaugh MP, Pijoan CC, Molitor TW. Gamma delta lymphocyte response to porcine reproductive and respiratory syndrome virus. Viral Immunol. 2005;18:490-9.
131. Martelli P, Gozio S, Ferrari L, Rosina S, Angelis E, Quintavalla C, Bottarelli E, Borghetti P. Efficacy of a modified live porcine reproductive and respiratory syndrome virus (PRRSV) vaccine in pigs naturally exposed to heterologous European (Italian cluster) field strain: clinical protection and cell-mediated immunity. Vaccine. 2009;27:3788-99.
132. Nielsen J, Botner A. Hematological and immunological parameters of 4 1/2-month old pigs infected with PRRS virus. Vet Microbiol. 1997;55:289-94. (Pubitemid 27286223)
133. Halbur RG, Pallares FJ, Rathje JA, et al. Effects of different us isolates of porcine reproductive and respiratory syndrome virus (PRRSV) on blood and bone marrow parameters of experimentally infected pigs. Vet Rec. 2002;151:344-8.
134. Rossow KD, Bautista EM, Goyal SM, et al. Experimental porcine reproductive and respiratory syndrome virus infection in one-, four-, and 10-week-old pigs. J Vet Diagn Invest. 1994;6:3-12.
135. Halbur PG, Miller LD, Paul PS, et al. Immunohistochemical identification of porcine reproductive and respiratory syndrome virus (PRRSV) antigen in the heart and lymphoid system of three-week-old colostrum-deprived pigs. Vet Pathol. 1995;32:200-4.
136. Halbur PG, Paul PS, Frey ML, et al. Comparison of the pathogenicity of two US porcine reproductive 138 and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol. 1995;32:648-60.
137. Ni YY, Opriessnig T, Zhou L, Cao D, Huang YW, Halbur PG, Meng XJ. Attenuation of porcine reproductive and respiratory syndrome virus by molecular breeding of the virus envelope genes from genetically divergent strains. J Virol. 2013;87:304-13.
138. Halbur PG, Paul PS, Meng XJ, et al. Comparative pathogenicity of nine US porcine reproductive and respiratory syndrome virus (PRRSV) isolates in a five-week-old cesarean-derived, colostrum-deprived pig model. J Vet Diagn Invest. 1996;8:11-201.
139. Haynes JS, Halbur PG, Sirinarumitr T, Paul PS, Meng XJ, Huffman EL. Temporal and morphologic characterization of the distribution of porcine reproductive and respiratory syndrome virus (PRRSV) by in situ hybridization in pigs infected with isolates of PRRSV that differ in virulence. Vet Pathol. 1997;34:39-43. (Pubitemid 127473821)
140. Tchao NK, Turka LA. Lymphodepletion and homeostatic proliferation: implications for transplantation. Am J Transplant. 2012;12:1079-90.
141. Dummer W, Ernst B, LeRoy E, et al. Autologous regulation of naive T cell homeostasis within the T cell compartment. J Immunol. 2001;166:2460-8. (Pubitemid 32173482)
142. Khoruts A, Fraser JM. A causal link between lymphopenia and autoimmunity. Immunol Lett. 2005;98:23-31. (Pubitemid 40409815)
143. Pescovitz MD, Hsu SM, et al. Characterization of a porcine CD1-specific mAb that distinguishes CD4/CD8 double-positive thymic from peripheral T lymphocytes. Tissue Antigens. 1990;35:151-6. (Pubitemid 20168328)
144. Klein L, Hinterberger M, Wirnsberger G, Kyewski B. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat Rev Immunol. 2009;9:833-44.
145. Butler JE, Lager KM, Splichal I, Francis D, Kacskovics I, Sinkora M, Wertz N, Sun J, Zhao Y, Brown WR, DeWald R, Dierks S, Muyldermanns S, Lunney JK, McCray PB, Rogers CS, Welsh MJ, Navarro P, Klobasa F, Habe F, Ramsoondar J. The piglet as a model for B cell and immune system. Dev Vet Immunol Immunopathol. 2009;128:147-70.
146. Miniatis P, Joh D. Gnotobiotic pigs derivation and rearing. Can J Comp Med. 1978;42:428.
147. Butler JE, Weber P, Sinkora M, Baker D, Schoenherr A, Mayer B, Francis D. Antibody repertoire development in fetal and neonatal piglets. VIII. Colonization is required for newborn piglets to make serum antibodies to T-dependent and type 2 T-independent antigens. J Immunol. 2002;169:6822-30. (Pubitemid 36899267)
148. Butler JE, Francis D, Freeling J, Weber P, Sun J, Krieg AM. Antibody repertoire development in fetal and neonatal piglets. IX. Three PAMPs act synergistically to allow germfree piglets to respond to TI-2 and TD antigens. J Immunol. 2005;175:6772-85. (Pubitemid 41598922)
149. Butler JE, Sun X-Z, Wertz N, Vincent A, Zanella E, Lager KM. Antibody repertoire development in fetal and neonatal piglets. XVI. Influenza stimulates adaptive immunity, class switch and diversification of the IgG repertoire encoded by downstream Cγ genes. Immunology (British). 2012;138:134-44.
150. Schultz RD, Wang JT, Dunne HW. Development of the humoral immune response of the pig. Am J Vet Res. 1971;32:1331-6.
151. Sun X-Z, Lager K, Tobin G, Nara P, Butler JE. Antibody repertoire development in fetal and neonatal piglets. XXIII. Fetal piglets infected with a vaccine strain of PRRS virus display the same immune dysregulation seen in isolator piglets. Vaccine. 2012;30:3646-52.
152. Butler JE, Lemke CD, Weber P, Sinkora M, Lager KD. Antibody repertoire development in fetal and neonatal piglets. XIX. Undiversified B cells with hydrophobic HCDR3s preferentially proliferate in PRRS. J Immunol. 2007;178:6320-31. (Pubitemid 46717416)
153. Butler JE, Weber P, Wertz N, Lager KM. Porcine reproductive and respiratory syndrome virus (PRRSV) subverts development of adaptive immunity by proliferation of germline-encoded B cells with hydrophobic HCDR3s. J Immunol. 2008;180:2347-56.
154. Plagemann PGW. Lactate dehydrogenase-elevating virus and related viruses. In: Fields BN, Knipe DM, Howley PM, editors. Fields virology. 3rd ed. New York: Lippincott-Raven; 1996. p. 1105-20.
155. Ippolito GC, Schelonka RL, Zemlin M, Zemlin C, Zhaung Y, Gartland GL, Nitschke L, Pelkonen J, Rajewsky K, Schroeder HW. Forced enrichment of hydrophobic amino acids in immunoglobulin CDR3-H3 impairs splenic B cell development but not antibody production. J Exp Med. 2006;203:1567-78. (Pubitemid 43877616)
156. Ramamoorty S, Meng XJ. Porcine circoviruses: a minuscule yet mammoth paradox. Anim Health Res Rev. 2009;10:1-20.
157. Sestak K, Lanza I, Park SK, Weilnau PA, Saif LJ. Contribution of passive immunity to porcine respiratory coronavirus to protection against transmissible gastroenteritis virus challenge exposure in suckling pigs. Am J Vet Res. 1996;57:664-71. (Pubitemid 126613622)
158. Wesley RD, Woods RD. Immunization of pregnant gilts with PRCV induces lactogenic immunity for protection of nursing piglets from challenge with TGEV. Vet Microbiol. 1993;38:31-40. (Pubitemid 24010320)
159. Butler JE, Rainard P, Lippolis J, Salmon H, Kacskovics I. The mammary gland in mucosal and regional immunity. In: Russell M, Mestecky J, editors. Mucosal immunology. 4th ed. New York: Academic Press; 2014.
160. Rhee K, Sethupathi JP, Driks A, Lanning DK, Knight KL. Role of commensal bacteria in development of gut-associated lymphoid tissues and preimmune antibody repertoire. J Immunol. 2004;172:1118-24. (Pubitemid 38113772)
161. de Groot RJ, Cowley JA, Enjuanes L, Faaberg KS, Perlman S, Rottier PJM, Snijder EJ, Ziebuhr J, Gorbalenya AE. Order nidovirales. In: King AMQ, editor. Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses. Amsterdam: Elsevier/Academic Press; 2012. p. 785-94.
162. Johnson CR, Griggs TF, Gnanandarajah J, Murtaugh MP. Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative ORF5 present in all arteriviruses. J Gen Virol. 2011;92:1107-16.
163. Fang Y, Treffers EE, Li Y, Tas A, Sun Z, van der Meer Y, de Ru AH, van Veelen PA, Atkins JF, Snijder EJ, Firth AE. Efficient -2 frameshifting by mammalian ribosomes to synthesize an additional 8. Arterivirus protein. Proc Natl Acad Sci USA. 2012;109:E2920-8.
164. Hanada K, Suzuki Y, Nakane T, Hirose O, Gojobori T. The origin and evolution of porcine reproductive and respiratory syndrome viruses. Mol Biol Evol. 2005;22:1024-31. (Pubitemid 40471415)
165. Snijder EJ, Kikkert M, Fang Y. Arterivirus molecular biology and pathogenesis. J Gen Virol. 2013;94:2141-63.
166. Forsberg R. Divergence time of porcine reproductive and respiratory syndrome virus subtypes. Mol Biol Evol. 2005;22:2131-4. (Pubitemid 41437812)
167. Kapur V, Elam MR, Pawlovich TM, Murtaugh MP. Genetic variation in porcine reproductive and respiratory syndrome virus isolates in the midwestern United States. J Gen Virol. 1996;77:1271-6. (Pubitemid 26185509)
168. Shi M, Holmes EC, Brar MS, Leung FC. Recombination is associated with an outbreak of novel highly pathogenic porcine reproductive and respiratory syndrome viruses in china. J Virol. 2013;87:10904-7.
169. Yuan S, Nelsen CJ, Murtaugh MP, Schmitt BJ, Faaberg KS. Recombination between North American strains of porcine reproductive and respiratory syndrome virus. Virus Res. 1999;61:87-98. (Pubitemid 29276874)
170. van Vugt JJ, Storgaard T, Oleksiewicz MB, Botner A. High frequency RNA recombination in porcine reproductive and respiratory syndrome virus occurs preferentially between parental sequences with high similarity. J Gen Virol. 2001;82:2615-20. (Pubitemid 32998639)
171. Nguyen VG, Kim HK, Moon HJ, Park SJ, Chung H C, Choi MK, Park BK. A Bayesian phylogeographical analysis of type 1 porcine reproductive and respiratory syndrome virus (PRRSV). Transbound Emerg Dis. 2013;2013:12058. doi:10.1111/tbed12058.
172. Stadejek T, Stankevicius A, Murtaugh MP, Oleksiewicz MB. Molecular evolution of PRRSV in Europe: current state of play. Vet Microbiol. 2013;165:21-8.
173. Liu D, Zhou R, Zhang J, Zhou L, Jiang Q, Guo X, Ge X, Yang H. Recombination analyses between two strains of porcine reproductive and respiratory syndrome virus in vivo. Virus Res. 2011;155:473-86.
174. Gauger PC, Faaberg KS, Guo B, Kappes MA, Opriessnig T. Genetic and phenotypic characterization of a 2006 United States porcine reproductive and respiratory virus isolate associated with high morbidity and mortality in the field. Virus Res. 2012;163:98-107.
175. Han J, Wang Y, Faaberg KS. Complete genome analysis of RFLP 184 isolates of porcine reproductive and respiratory syndrome virus. Virus Res. 2006;122:175-82. (Pubitemid 44637246)
176. Meulenberg JJ, Petersen den Besten A, DeKluyver EP, Moorman RJ, Schaaper WM, Wensvoort G. Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology. 1995;206:155-63.
177. Mardassi H, Massie B, Dea S. Intracellular synthesis, processing, and transport of proteins encoded by ORFs 5 to 7 of porcine reproductive and respiratory syndrome virus. Virology. 1996;221:98-112. (Pubitemid 26266546)
178. de Vries AA, Chirnside ED, Horzinek MC, Rottier PJ. Structural proteins of equine arteritis virus. J Virol. 1992;66:6294-303.
179. Faaberg KS, Plagemann PG. The envelope proteins of lactate dehydrogenase-elevating virus and their membrane topography. Virology. 1995;212:512-25.
180. Faaberg KS. Arterivirus structural proteins and assembly. In: Perlman S, Gallaher T, Snijder E, editors. The nidoviruses. Washington: ASM Press; 2007. p. 211-34.
181. Thaa B, Sinhadri BC, Tielesch C, Krause E, Veit M. Signal peptide cleavage from GP5 of PRRSV: a minor fraction of molecules retains the decoy epitope, a presumed molecular cause for viral persistence. PLoS ONE. 2013;8:e65548.
182. Faaberg KS, Hocker JD, Erdman MM, Harris DL, Nelson EA, Torremorell M, Plagemann PG. Neutralizing antibody responses of pigs infected with natural GP5 N-glycan mutants of porcine reproductive and respiratory syndrome virus. Viral Immunol. 2006;19:294-304. (Pubitemid 44050328)
183. Lopez OJ, Osorio FA. Role of neutralizing antibodies in PRRSV protective immunity. Vet Immunol Immunopathol. 2004;102:155-63. (Pubitemid 39422641)
184. Ostrowski M, Galeota JA, Jar AM, Platt KB, Osorio FA, Lopez OJ. Identification of neutralizing and nonneutralizing epitopes in the porcine reproductive and respiratory syndrome virus GP5 ectodomain. J Virol. 2002;76:4241-50. (Pubitemid 34309559)
185. Sur JH, Doster AR, Osorio FA. Apoptosis induced in vivo during acute infection by porcine reproductive and respiratory syndrome virus. Vet Pathol. 1998;35:506-14. (Pubitemid 128472823)
186. Plagemann PG. GP5 ectodomain epitope of porcine reproductive and respiratory syndrome virus, strain Lelystad virus. Virus Res. 2004;102:225-30. (Pubitemid 38490340)
187. Cancel-Tirado SM, Evans RB, Yoon KJ. Monoclonal antibody analysis of porcine reproductive and respiratory syndrome virus epitopes associated with antibody-dependent enhancement and neutralization of virus infection. Vet Immunol Immunopathol. 2004;102:249-62.
188. Delputte PL, Meerts P, Costers S, Nauwynck HJ. Effect of virus-specific antibodies on attachment, internalization and infection of porcine reproductive and respiratory syndrome virus in primary macrophages. Vet Immunol Immunopathol. 2004;102:179-88. (Pubitemid 39422643)
189. Delputte PL, Vanderheijden N, Nauwynck HJ, Pensaert MB. Involvement of the matrix protein in attachment of porcine reproductive and respiratory syndrome virus to a heparinlike receptor on porcine alveolar macrophages. J Virol. 2002;76:4312-20. (Pubitemid 34309567)
190. Costers S, Lefebvre DJ, Van Doorsselaere J, Vanhee M, Delputte PL, Nauwynck HJ. GP4 of porcine reproductive and respiratory syndrome virus contains a neutralizing epitope that is susceptible to immunoselection in vitro. Arch Virol. 2010;155:371-8.
191. Kim WI, Yoon KJ. Molecular assessment of the role of envelope-associated structural proteins in cross neutralization among different PRRS viruses. Virus Genes. 2008;37:380-91.
192. Vu HL, Kwon B, Yoon KJ, Laegreid WW, Pattnaik AK, Osorio FA. Immune evasion of porcine reproductive and respiratory syndrome virus through glycan shielding involves both glycoprotein 5 as well as glycoprotein 3. J Virol. 2011;85:5555-64.
193. Zhou L, Ni YY, Pineyro P, Cossaboom CM, Subramaniam S, Sanford BJ, Dryman BA, Huang YW, Meng XJ. Broadening the heterologous cross-neutralizing antibody inducing ability of porcine reproductive and respiratory syndrome virus by breeding the GP4 or M genes. PLoS ONE. 2013;8:e66645.
194. Zhou L, Ni YY, Pineyro P, Sanford BJ, Cossaboom CM, Dryman BA, Huang YW, Cao DJ, Meng XJ. DNA shuffling of the GP3 genes of porcine reproductive and respiratory syndrome virus (PRRSV) produces a chimeric virus with an improved cross-neutralizing ability against a heterologous PRRSV strain. Virology. 2012;434:96-109.
195. van Nieuwstadt AP, Meulenberg JJ, van Essen-Zanbergen A, Petersen-den Besten A, Bende RJ, Moormann RJ, Wensvoort G. Proteins encoded by open reading frames 3 and 4 of the genome of Lelystad virus (Arteriviridae) are structural proteins of the virion. J Virol. 1996;70:4767-72. (Pubitemid 26187471)
196. Das PB, Vu HL, Dinh PX, Cooney JL, Kwon B, Osorio FA, Pattnaik AK. Glycosylation of minor envelope glycoproteins of porcine reproductive and respiratory syndrome virus in infectious virus recovery, receptor interaction, and immune response. Virology. 2011;410:385-94.
197. Wieringa R, de Vries AA, Rottier PJ. Formation of disulfide-linked complexes between the three minor envelope glycoproteins (GP2b, GP3, and GP4) of equine arteritis virus. J Virol. 2003;77:6216-26. (Pubitemid 36588392)
198. Du Y, Pattnaik AK, Song C, Yoo D, Li G. Glycosyl-phosphatidylinositol (GPI)-anchored membrane association of the porcine reproductive and respiratory syndrome virus GP4 glycoprotein and its co-localization with CD163 in lipid rafts. Virology. 2012;424:18-32.
199. Pujhari S, Baig TT, Zakhartchouk AN. Potential role of porcine reproductive and respiratory syndrome virus structural protein GP2 in Apoptosis inhibition. Biomed Res Int. 2014;2014:160505. doi:10.1155/2014/160505.
200. Dokland T. The structural biology of PRRSV. Virus Res. 2010;154:86-97.
201. Spilman MS, Welbon C, Nelson E, Dokland T. Cryo-electron tomography of porcine reproductive and respiratory syndrome virus: organization of the nucleocapsid. J Gen Virol. 2009;90:527-35.
202. Tijms MA, van der Meer Y, Snijder EJ. Nuclear localization of non-structural protein 1 and nucleocapsid protein of equine arteritis virus. J Gen Virol. 2002;83:795-800. (Pubitemid 34284863)
203. Dea S, Wilson L, Therrien D, Cornaglia E. Competitive ELISA for detection of antibodies to porcine reproductive and respiratory syndrome virus using recombinant E. coli-expressed nucleocapsid protein as antigen. J Virol Methods. 2000;87:109-22. (Pubitemid 30345681)
204. Brown IH, Done SH, Spencer YI, Cooley WA, Harris PA, Alexander DJ. Pathogenicity of swine influenza H1N1 virus antigenically distinguishable from classical and European strains. Vet Rec. 1993;132:598-602.
205. de Lima M, Pattnaik AK, Flores EF, Osorio FA. Serologic marker candidates identified among B-cell linear epitopes of Nsp2 and structural proteins of a North American strain of porcine reproductive and respiratory syndrome virus. Virology. 2006;353:410-21. (Pubitemid 44397133)
206. Oleksiewicz MB, Botner A, Toft P, Normann P, Storgaard T. Epitope mapping porcine reproductive and respiratory syndrome virus by phage display: the nsp2 fragment of the replicase polyprotein contains a cluster of B-cell epitopes. J Virol. 2001;75:3277-90. (Pubitemid 32225891)
207. Yan Y, Guo X, Ge X, Chen Y, Cha Z, Yang H. Monoclonal antibody and porcine antisera recognized B-cell epitopes of Nsp2 protein of a Chinese strain of porcine reproductive and respiratory syndrome virus. Virus Res. 2007;126:207-15. (Pubitemid 46726714)
208. Kappes MA, Miller CL, Faaberg KS. Highly divergent strains of porcine reproductive and respiratory syndrome virus incorporate multiple isoforms of nonstructural protein 2 into virions. J Virol. 2013;87:13456-65.
209. Choi YJ, Yun SI, Kang SY, Lee YM. Identification of 5′ and 3′ cis-acting elements of the porcine reproductive and respiratory syndrome virus: acquisition of novel 5′ AU-rich sequences restored replication of a 5′-proximal 7-nucleotide deletion mutant. J Virol. 2006;80:723-36.
210. Fang Y, Rowland RR, Roof M, Lunney JK, Christopher-Hennings J, Nelson EA. A full-length cDNA infectious clone of North American type 1 porcine reproductive and respiratory syndrome virus: expression of green fluorescent protein in the Nsp2 region. J Virol. 2006;80:11447-55. (Pubitemid 44788860)
211. Han J, Liu G, Wang Y, Faaberg KS. Identification of nonessential regions of the nsp2 replicase protein of porcine reproductive and respiratory syndrome virus strain VR-2332 for replication in cell culture. J Virol. 2007;81:9878-90. (Pubitemid 350067691)
212. Kwon B, Ansari IH, Osorio FA, Pattnaik AK. Infectious clone-derived viruses from virulent and vaccine strains of porcine reproductive and respiratory syndrome virus mimic biological properties of their parental viruses in a pregnant sow model. Vaccine. 2006;24:7071-80. (Pubitemid 46107208)
213. Lee C, Calvert JG, Welch SK, Yoo D. A DNA-launched reverse genetics system for porcine reproductive and respiratory syndrome virus reveals that homodimerization of the nucleocapsid protein is essential for virus infectivity. Virology. 2005;331:47-62. (Pubitemid 39593632)
214. Lu J, Zhang J, Sun Z, Liu W, Yuan S. An infectious cDNA clone of a highly pathogenic porcine reproductive and respiratory syndrome virus variant associated with porcine high fever syndrome. J Gen Virol. 2008;89:2075-9.
215. Meulenberg JJ, Bos-de Ruijter JN, van de Graaf R, Wensvoort G, Moormann RJ. Infectious transcripts from cloned genomelength cDNA of porcine reproductive and respiratory syndrome virus. J Virol. 1998;72:380-7. (Pubitemid 28048849)
216. Nielsen HS, Liu G, Nielsen J, Oleksiewicz MB, Botner A, Storgaard T, Faaberg KS. Generation of an infectious clone of VR-2332, a highly virulent North American-type isolate of porcine reproductive and respiratory syndrome virus. J Virol. 2003;77:3702-11. (Pubitemid 36297289)
217. Ran ZG, Chen XY, Guo X, Ge XN, Yoon KJ, Yang HC. Recovery of viable porcine reproductive and respiratory syndrome virus from an infectious clone containing a partial deletion within the Nsp2-encoding region. Arch Virol. 2008;153:899-907.
218. Truong HM, Lu Z, Kutish GF, Galeota J, Osorio FA, Pattnaik AK. A highly pathogenic porcine reproductive and respiratory syndrome virus generated from an infectious cDNA clone retains the in vivo virulence and transmissibility properties of the parental virus. Virology. 2004;325:308-19. (Pubitemid 38902796)
219. Wang Y, Liang Y, Han J, Burkhart KM, Vaughn EM, Roof MB, Faaberg KS. Attenuation of porcine reproductive and respiratory syndrome virus strain MN184 using chimeric construction with vaccine sequence. Virology. 2008;371:418-29. (Pubitemid 351173225)
220. Zhou L, Zhang J, Zeng J, Yin S, Li Y, Zheng L, Guo X, Ge X, Yang H. The 30-amino-acid deletion in the nsp2 of highly pathogenic porcine reproductive and respiratory syndrome virus emerging in China is not related to its virulence. J Virol. 2009;83:5156-67.
221. Groot Bramel-Verheije MH, Rottier PJ, Meulenberg JJ. Expression of a foreign epitope by porcine reproductive and respiratory syndrome virus. Virology. 2000;278:380-9. (Pubitemid 32012773)
222. Ansari IH, Kwon B, Osorio FA, Pattnaik AK. Influence of N-linked glycosylation of porcine reproductive and respiratory syndrome virus GP5 on virus infectivity, antigenicity, and ability to induce neutralizing antibodies. J Virol. 2006;80:3994-4004.
223. Kroese MV, Zevenhoven-Dobbe JC, Bos-de Ruijter JN, Peeters BP, Meulenberg JJ, Cornelissen LA, Snijder EJ. The nsp1alpha and nsp1 papain-like autoproteinases are essential for porcine reproductive and respiratory syndrome virus RNA synthesis. J Gen Virol. 2008;89:494-9. (Pubitemid 351622446)
224. Lee C, Yoo D. Cysteine residues of the porcine reproductive and respiratory syndrome virus small envelope protein are nonessential for virus infectivity. J Gen Virol. 2005;86:3091-6. (Pubitemid 41555575)
225. Pei Y, Hodgins DC, Lee C, Calvert JG, Welch SK, Jolie R, Keith M, Yoo D. Functional mapping of the porcine reproductive and respiratory syndrome virus capsid protein nuclear localization signal and its pathogenic association. Virus Res. 2008;135:107-14.
226. Guo B, Lager KM, Schlink SN, Kehrli ME Jr, Brockmeier SL, Miller C, Swenson SL, Faaberg KS. Chinese and Vietnamese strains of HP-PRRSV cause different pathogenic outcomes in United States high health swine. Virology. 2013;446:238-50.
227. Kwon B, Ansari IH, Pattnaik AK, Osorio FA. Identification of virulence determinants of porcine reproductive and respiratory syndrome virus through construction of chimeric clones. Virology. 2008;380:371-8.
228. Verheije MH, Kroese MV, Rottier PJ, Meulenberg JJ. Viable porcine arteriviruses with deletions proximal to the 3′ end of the genome. J Gen Virol. 2001;82:2607-14. (Pubitemid 32998638)
229. Beura LK, Subramaniam S, Vu HL, Kwon B, Pattnaik AK, Osorio FA. Identification of amino acid residues important for anti-IFN activity of porcine reproductive and respiratory syndrome virus non-structural protein 1. Virology. 2012;433:431-9.
230. Subramaniam S, Sur JH, Kwon B, Pattnaik AK, Osorio RA. A virulent strain of porcine reproductive and respiratory syndrome virus does not up-regulate interleukin-10 in vitro and in vivo. Virus Res. 2011;155:415-22.
231. Dobbe JC, van der Meer Y, Spaan WJ, Snijder EJ. Construction of chimeric arteriviruses reveals that the ectodomain of the major glycoprotein is not the main determinant of equine arteritis virus tropism in cell culture. Virolgy. 2001;288:283-94. (Pubitemid 32929908)
232. Gao F, Yao H, Lu J, Wei Z, Zheng H, Zhuang J, Tong G, Yuan S. Replacement of the heterologous 5(′) untranslated region allows preservation of the fully functional activities of type 2 porcine reproductive and respiratory syndrome virus. Virology. 2013;439:1-12.
233. Tian D, Wei Z, Zevenhoven-Dobbe JC, Liu R, Tong G, Snijder EJ, Yuan S. Arterivirus minor envelope proteins are a major determinant of viral tropism in cell culture. J Virol. 2012;86:3701-12.
234. Verheije MH, Welting TJ, Jansen HT, Rottier PJ, Meulenberg JJ. Chimeric arteriviruses generated by swapping of the M protein ectodomain rule out a role of this domain in viral targeting. Virology. 2002;303:364-73. (Pubitemid 36069199)
235. Tian D, Zheng H, Zhang R, Zhuang J, Yuan S. Chimeric porcine reproductive and respiratory syndrome viruses reveal full function of genotype 1 envelope proteins in the backbone of genotype 2. Virology. 2011;412:1-8.
236. Ellingson JS, Wang Y, Layton S, Ciacci-Zanella J, Roof MB, Faaberg KS. Vaccine efficacy of porcine reproductive and respiratory syndrome virus chimeras. Vaccine. 2010;28:2679-86.
237. Butler JE, Sinkora M. The isolator piglet: a model for studying the development of adaptive immunity. Immunol Res. 2007;39:33-51. (Pubitemid 47574895)
238. Van Reeth K, Nauwynck H, Pensaert M. Dual infections of feeder pigs with porcine reproductive and respiratory syndrome virus followed by porcine respiratory coronavirus or swine influenza virus: a clinical and virological study. Vet Microbiol. 1996;S48:325-35. (Pubitemid 26090073)
239. Suradhat S, Kesdangsakonwut S, Sada W, Buranapraditkum S, Wongsawang S, Thanawongnuwech R. Negative impact of porcine reproductive and respiratory syndrome virus infection on the efficacy of classical swine fever vaccine. Vaccine. 2006;24:2634-42. (Pubitemid 43290395)
240. Xiao Z, Batista L, Dee S, Halbur P, Murtaugh MP. The level of virus-specific T-cell and macrophage recruitment in porcine reproductive and respiratory syndrome virus infection in pigs is independent of virus load. J Virol. 2004;78:5923-33. (Pubitemid 38661680)
241. Butler JE, Weber P, Wertz N. Antibody repertoire development in fetal and neonatal pigs. XIII. "Hybrid VH genes" and the preimmune repertoire re-visited. J Immunol. 2006;177:5459-70. (Pubitemid 44527619)
242. Butler JE, Sun X-Z, Wertz N, Lager KM, Chaloner K, Urban J Jr, Nara P, Tobin G. Antibody repertoire development in fetal and neonatal piglets. XXI. VH usage remains constant during development in fetal piglets and postnatally in pigs exposed to environmental antigen. Mol Immunol. 2011;49:483-94.
243. Syed-Hussain SS, Howe L, Pomroy WE, West DM, Smith SL, Williamson NB. Adaptation o a commercial ELISA to determine the IgG avidity in sweep experimentally and naturally infected with Neospora caninum. Vet Parasitol. 2014; doi:10.1016/j.vetpar.2014.01.003.
244. Butler JE, Wertz N, Deschacht N, Kacskovics I. Porcine IgG: structure, genetics and evolution. Immunogenetics. 2009;61:209-30.
245. Kloep A, Wertz N, Mendicino M, Butler JE. Linkage haplotype for IgG and IgA subclass genes. Immunogenetics. 2012;64:469-73.
246. Butler JE, Wertz N. Antibody repertoire development in fetal and neonatal piglets. XVII. IgG subclass transcription revisited with emphasis on new IgG3. J Immunol. 2006;177:5480-9. (Pubitemid 44527621)
247. Butler JE, Wertz N, Sun X-Z, Lunney JK, Muyldermanns S. Resolution of an immunodiagnostic dilemma: heavy chain chimeric antibodies for species in which plasmacytomas are unknown. Mol Immunol. 2012;53:140-8.
248. Patch JR, Peterson LE, Toka FN, Moreas M, Grubman MJ, Nielsen M, Jungersobn G, Buus S, Golde WT. Induction of foot and mouth disease virus (FMDV) specific cytotoxic T cells killing by vaccination. Clin Vaccine Immunol. 2011;18:280-8.