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Mucosal vaccines to prevent porcine reproductive and respiratory syndrome: a new perspective

Published online by Cambridge University Press:  02 May 2012

Gourapura J. Renukaradhya*
Affiliation:
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Department of Veterinary Preventive Medicine, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA
Varun Dwivedi
Affiliation:
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Department of Veterinary Preventive Medicine, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA
Cordelia Manickam
Affiliation:
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Department of Veterinary Preventive Medicine, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA
Basavaraj Binjawadagi
Affiliation:
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Department of Veterinary Preventive Medicine, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA
David Benfield
Affiliation:
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Department of Veterinary Preventive Medicine, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA
*
*Corresponding author. E-mail: [email protected]

Abstract

Porcine reproductive and respiratory syndrome (PRRS) is an economically important infectious disease of swine. Constant emergence of variant strains of PRRS virus (PPRSV) and virus-mediated immune evasion followed by viral persistence result in increased incidence and recurrence of PRRS in swine herds. Current live and killed PRRSV vaccines administered by a parenteral route are ineffective in inducing complete protection. Thus, new approaches in design and delivery of PRRSV vaccines are needed to reduce the disease burden of the swine industry. Induction of an effective mucosal immunity to several respiratory pathogens by direct delivery of a vaccine to mucosal sites has proven to be effective in a mouse model. However, there are challenges in eliciting mucosal immunity to PRRS due to our limited understanding of safe and potent mucosal adjuvants, which could potentiate the mucosal immune response to PRRSV. The purpose of this review is to discuss methods for induction of protective mucosal immune responses in the respiratory tract of pigs. The manuscript also discusses how PRRSV modulates innate, adaptive and immunoregulatory responses at both mucosal and systemic sites of infected and/or vaccinated pigs. This information may help in the design of innovative mucosal vaccines to elicit superior cross-protective immunity against divergent field strains of PRRSV.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2012

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References

Aasted, B, Bach, P, Nielsen, J and Lind, P (2002). Cytokine profiles in peripheral blood mononuclear cells and lymph node cells from piglets infected in utero with porcine reproductive and respiratory syndrome virus. Clinical and Diagnostic Laboratory Immunology 9: 12291234.Google ScholarPubMed
Acker, H (2005). The oxygen sensing signal cascade under the influence of reactive oxygen species. Philosophical Transactions of the Royal Society B: Biological Sciences 360: 22012210.CrossRefGoogle ScholarPubMed
Akerstrom, S, Mousavi-Jazi, M, Klingstrom, J, Leijon, M, Lundkvist, A and Mirazimi, A (2005). Nitric oxide inhibits the replication cycle of severe acute respiratory syndrome coronavirus. Journal of Virology 79: 19661969.CrossRefGoogle ScholarPubMed
Albina, E (1997). Epidemiology of porcine reproductive and respiratory syndrome (PRRS): an overview. Veterinary Microbiology 55: 309316.CrossRefGoogle ScholarPubMed
Albina, E, Carrat, C and Charley, B (1998). Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. Journal of Interferon and Cytokine Research 18: 485490.CrossRefGoogle ScholarPubMed
Allan, CH, Mendrick, DL and Trier, JS (1993). Rat intestinal M cells contain acidic endosomal–lysosomal compartments and express class II major histocompatibility complex determinants. Gastroenterology 104: 698708.CrossRefGoogle ScholarPubMed
Avdic, S, Cao, JZ, Cheung, AK, Abendroth, A and Slobedman, B (2011). Viral IL-10 expressed by human cytomegalovirus during the latent phase of infection modulates latently infected myeloid cell differentiation. Journal of Virology 85: 74657471.CrossRefGoogle ScholarPubMed
Bansal, K, Elluru, SR, Narayana, Y, Chaturvedi, R, Patil, SA, Kaveri, SV, Bayry, J and Balaji, KN (2010). PE_PGRS antigens of Mycobacterium tuberculosis induce maturation and activation of human dendritic cells. Journal of Immunology 184: 34953504.CrossRefGoogle ScholarPubMed
Barral, DC and Brenner, MB (2007). CD1 antigen presentation: how it works. Nature Reviews Immunology 7: 929941.CrossRefGoogle ScholarPubMed
Bastos, RG, Dellagostin, OA, Barletta, RG, Doster, AR, Nelson, E, Zuckermann, F and Osorio, FA (2004). Immune response of pigs inoculated with Mycobacterium bovis BCG expressing a truncated form of GP5 and M protein of porcine reproductive and respiratory syndrome virus. Vaccine 22: 467474.CrossRefGoogle Scholar
Bautista, EM and Molitor, TW (1999). IFN gamma inhibits porcine reproductive and respiratory syndrome virus replication in macrophages. Archives of Virology 144: 11911200.CrossRefGoogle ScholarPubMed
Beetz, S, Marischen, L, Kabelitz, D and Wesch, D (2007). Human gamma delta T cells: candidates for the development of immunotherapeutic strategies. Immunologic Research 37: 97111.CrossRefGoogle ScholarPubMed
Bekierkunst, A (1968). Acute granulomatous response produced in mice by trehalose-6,6-dimycolate. Journal of Bacteriology 96: 958961.CrossRefGoogle ScholarPubMed
Bekierkunst, A, Yarkoni, E, Flechner, I, Morecki, S, Vilkas, E and Lederer, E (1971). Immune response to sheep red blood cells in mice pretreated with mycobacterial fractions. Infection and Immunity 4: 256263.CrossRefGoogle ScholarPubMed
Belshe, R, Lee, MS, Walker, RE, Stoddard, J and Mendelman, PM (2004). Safety, immunogenicity and efficacy of intranasal, live attenuated influenza vaccine. Expert Review of Vaccines 3: 643654.CrossRefGoogle ScholarPubMed
Beyer, J, Fichtner, D, Schirrmeier, H, Polster, U, Weiland, E and Wege, H (2000). Porcine reproductive and respiratory syndrome virus (PRRSV): kinetics of infection in lymphatic organs and lung. Journal of Veterinary Medicine B Infectious Diseases Veterinary Public Health 47: 925.CrossRefGoogle ScholarPubMed
Binjawadagi, B, Dwivedi, V, Manickam, C, Torrelles, JB and Renukaradhya, GJ (2011). Intranasal delivery of an adjuvanted modified live porcine reproductive and respiratory syndrome virus vaccine reduces the ROS production. Viral Immunology 24: 475482.CrossRefGoogle ScholarPubMed
Binns, RM (1982). Organisation of the lymphoreticular system and lymphocyte markers in the pig. Veterinary Immunology and Immunopathology 3: 95146.CrossRefGoogle ScholarPubMed
Biron, CA, Nguyen, KB, Pien, GC, Cousens, LP and Salazar-Mather, TP (1999). Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annual Review of Immunology 17: 189220.CrossRefGoogle ScholarPubMed
Bonavida, B, Katz, J and Hoshino, T (1986). Mechanism of NK activation by OK-432 (Streptococcus pyogenes). I. Spontaneous release of NKCF and augmentation of NKCF production following stimulation with NK target cells. Cellular Immunology 102: 126135.CrossRefGoogle ScholarPubMed
Botner, A, Strandbygaard, B, Sorensen, KJ, Have, P, Madsen, KG, Madsen, ES and Alexandersen, S (1997). Appearance of acute PRRS-like symptoms in sow herds after vaccination with a modified live PRRS vaccine. Veterinary Record 141: 497499.CrossRefGoogle ScholarPubMed
Brayden, DJ, Jepson, MA and Baird, AW (2005). Keynote review: intestinal Peyer's patch M cells and oral vaccine targeting. Drug Discovery Today 10: 11451157.CrossRefGoogle ScholarPubMed
Buda, A, Sands, C and Jepson, MA (2005). Use of fluorescence imaging to investigate the structure and function of intestinal M cells. Advanced Drug Delivery Reviews 57: 123134.CrossRefGoogle Scholar
Buddaert, W, Van Reeth, K and Pensaert, M (1998). In vivo and in vitro interferon (IFN) studies with the porcine reproductive and respiratory syndrome virus (PRRSV). Advances in Experimental Medicine and Biology 440: 461467.CrossRefGoogle ScholarPubMed
Canessa, C, Vierucci, S, Azzari, C and Vierucci, A (2010). The immunity of upper airways. International Journal of Immunopathology and Pharmacology 23: 812.CrossRefGoogle ScholarPubMed
Cano, JP, Dee, SA, Murtaugh, MP and Pijoan, C (2007). Impact of a modified-live porcine reproductive and respiratory syndrome virus vaccine intervention on a population of pigs infected with a heterologous isolate. Vaccine 25: 43824391.CrossRefGoogle ScholarPubMed
Charerntantanakul, W (2009). Adjuvants for porcine reproductive and respiratory syndrome virus vaccines. Veterinary Immunology and Immunopathology 129: 113.CrossRefGoogle ScholarPubMed
Charerntantanakul, W, Platt, R and Roth, JA (2006). Effects of porcine reproductive and respiratory syndrome virus-infected antigen-presenting cells on T cell activation and antiviral cytokine production. Viral Immunology 19: 646661.CrossRefGoogle Scholar
Che, TM, Johnson, RW, Kelley, KW, Van Alstine, WG, Dawson, KA, Moran, CA and Pettigrew, JE (2011). Mannan oligosaccharide improves immune responses and growth efficiency of nursery pigs experimentally infected with porcine reproductive and respiratory syndrome virus. Journal of Animal Science 89: 25922602.CrossRefGoogle ScholarPubMed
Choudhary, RK, Mukhopadhyay, S, Chakhaiyar, P, Sharma, N, Murthy, KJ, Katoch, VM and Hasnain, SE (2003). PPE antigen Rv2430c of Mycobacterium tuberculosis induces a strong B-cell response. Infection and Immunity 71: 63386343.CrossRefGoogle ScholarPubMed
Christopher-Hennings, J, Nelson, EA, Hines, RJ, Nelson, JK, Swenson, SL, Zimmerman, JJ, Chase, CL, Yaeger, MJ and Benfield, DA (1995). Persistence of porcine reproductive and respiratory syndrome virus in serum and semen of adult boars. Journal of Veterinary Diagnostic Investigation 7: 456464.CrossRefGoogle ScholarPubMed
Christopher-Hennings, J, Nelson, EA, Nelson, JK, Rossow, KD, Shivers, JL, Yaeger, MJ, Chase, CC, Garduno, RA, Collins, JE and Benfield, DA (1998). Identification of porcine reproductive and respiratory syndrome virus in semen and tissues from vasectomized and nonvasectomized boars. Veterinary Pathology 35: 260267.CrossRefGoogle ScholarPubMed
Chvanov, M, Petersen, OH and Tepikin, A (2005). Free radicals and the pancreatic acinar cells: role in physiology and pathology. Philosophical Transactions of the Royal Society B: Biological Sciences 360: 22732284.CrossRefGoogle ScholarPubMed
Clutton, S (1997). The importance of oxidative stress in apoptosis. British Medical Bulletin 53: 662668.CrossRefGoogle ScholarPubMed
Collins, JE, Benfield, DA, Christianson, WT, Harris, L, Hennings, JC, Shaw, DP, Goyal, SM, McCullough, S, Morrison, RB, Joo, HS, Gorcyca, D and Chladek, D (1992). Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. Journal of Veterinary Diagnostic Investigation 4: 117126.CrossRefGoogle ScholarPubMed
Corr, SC, Gahan, CC and Hill, C (2008). M-cells: origin, morphology and role in mucosal immunity and microbial pathogenesis. FEMS Immunology and Medical Microbiology 52: 212.CrossRefGoogle ScholarPubMed
Cox, RJ, Brokstad, KA and Ogra, P (2004). Influenza virus: immunity and vaccination strategies. Comparison of the immune response to inactivated and live, attenuated influenza vaccines. Scandinavian Journal of Immunology 59: 115.CrossRefGoogle ScholarPubMed
Croen, KD (1993). Evidence for antiviral effect of nitric oxide. Inhibition of herpes simplex virus type 1 replication. Journal of Clinical Investigation 91: 24462452.CrossRefGoogle ScholarPubMed
Czerkinsky, C and Holmgren, J (2010). Topical immunization strategies. Mucosal Immunology 3: 545555.CrossRefGoogle ScholarPubMed
Darwich, L, Diaz, I and Mateu, E (2010). Certainties, doubts and hypotheses in porcine reproductive and respiratory syndrome virus immunobiology. Virus Research 154: 123132.CrossRefGoogle ScholarPubMed
Davis, SS (2001). Nasal vaccines. Advanced Drug Delivery Reviews 51: 2142.CrossRefGoogle ScholarPubMed
Diaz, I, Darwich, L, Pappaterra, G, Pujols, J and Mateu, E (2005). Immune responses of pigs after experimental infection with a European strain of porcine reproductive and respiratory syndrome virus. Journal of General Virology 86: 19431951.CrossRefGoogle ScholarPubMed
Didierlaurent, A, Goulding, J and Hussell, T (2007). The impact of successive infections on the lung microenvironment. Immunology 122: 457465.CrossRefGoogle ScholarPubMed
Done, SH and Paton, DJ (1995). Porcine reproductive and respiratory syndrome: clinical disease, pathology and immunosuppression. Veterinary Record 136: 3235.CrossRefGoogle ScholarPubMed
Drew, TW (2000). A review of evidence for immunosuppression due to porcine reproductive and respiratory syndrome virus. Veterinary Research 31: 2739.Google ScholarPubMed
Duan, X, Nauwynck, HJ and Pensaert, MB (1997). Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to porcine reproductive and respiratory syndrome virus (PRRSV). Archives of Virology 142: 24832497.CrossRefGoogle ScholarPubMed
Duncan, R (2005). Nanomedicine gets clinical. Materials Today 8: 1617.CrossRefGoogle Scholar
Dwivedi, V, Manickam, C, Binjawadagi, B, Linhares, D, Murtaugh, MP and Renukaradhya, GJ (2012). Evaluation of immune responses to porcine reproductive and respiratory syndrome virus in pigs during early stage of infection under farm conditions. Virology Journal 9: 45.CrossRefGoogle ScholarPubMed
Dwivedi, V, Manickam, C, Patterson, R, Dodson, K, Murtaugh, M, Torrelles, JB, Schlesinger, LS and Renukaradhya, GJ (2011a). Cross-protective immunity to porcine reproductive and respiratory syndrome virus by intranasal delivery of a live virus vaccine with a potent adjuvant. Vaccine 29: 40584066.CrossRefGoogle ScholarPubMed
Dwivedi, V, Manickam, C, Patterson, R, Dodson, K, Weeman, M and Renukaradhya, GJ (2011b). Intranasal delivery of whole cell lysate of Mycobacterium tuberculosis induces protective immune responses to a modified live porcine reproductive and respiratory syndrome virus vaccine in pigs. Vaccine 29: 40674076.CrossRefGoogle ScholarPubMed
Etchart, N, Wild, F and Kaiserlian, D (1996). Mucosal and systemic immune responses to measles virus haemagglutinin in mice immunized with a recombinant vaccinia virus. Journal of General Virology 77 (Pt 10): 24712478.CrossRefGoogle ScholarPubMed
Faaberg, KS, Hocker, JD, Erdman, MM, Harris, DL, Nelson, EA, Torremorell, M and Plagemann, PG (2006). Neutralizing antibody responses of pigs infected with natural GP5 N-glycan mutants of porcine reproductive and respiratory syndrome virus. Viral Immunology 19: 294304.CrossRefGoogle ScholarPubMed
Foo, SY and Phipps, S (2010). Regulation of inducible BALT formation and contribution to immunity and pathology. Mucosal Immunology 3: 537544.CrossRefGoogle ScholarPubMed
Foss, DL and Murtaugh, MP (1999). Mucosal immunogenicity and adjuvanticity of cholera toxin in swine. Vaccine 17: 788801.CrossRefGoogle ScholarPubMed
Foss, DL, Zilliox, MJ, Meier, W, Zuckermann, F and Murtaugh, MP (2002). Adjuvant danger signals increase the immune response to porcine reproductive and respiratory syndrome virus. Viral Immunology 15: 557566.CrossRefGoogle ScholarPubMed
Gebert, A, Rothkotter, HJ and Pabst, R (1994). Cytokeratin 18 is an M-cell marker in porcine Peyer's patches. Cell and Tissue Research 276: 213221.CrossRefGoogle ScholarPubMed
Gerner, W, Kaser, T and Saalmuller, A (2009). Porcine T lymphocytes and NK cells – an update. Developmental and Comparative Immunology 33: 310320.CrossRefGoogle ScholarPubMed
Geurtsvankessel, CH, Willart, MA, Bergen, IM, Van Rijt, LS, Muskens, F, Elewaut, D, Osterhaus, AD, Hendriks, R, Rimmelzwaan, GF and Lambrecht, BN (2009). Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. Journal of Experimental Medicine 206: 23392349.CrossRefGoogle ScholarPubMed
Gomez-Laguna, J, Salguero, FJ, Barranco, I, Pallares, FJ, Rodriguez-Gomez, IM, Bernabe, A and Carrasco, L (2010). Cytokine expression by macrophages in the lung of pigs infected with the porcine reproductive and respiratory syndrome virus. Journal of Comparative Pathology 142: 5160.CrossRefGoogle ScholarPubMed
Guillonneau, C, Mintern, JD, Hubert, FX, Hurt, AC, Besra, GS, Porcelli, S, Barr, IG, Doherty, PC, Godfrey, DI and Turner, SJ (2009). Combined NKT cell activation and influenza virus vaccination boosts memory CTL generation and protective immunity. Proceedings of the National Academy of Sciences of the USA 106: 33303335.CrossRefGoogle ScholarPubMed
Gupta, RK, Chang, AC and Siber, GR (1998). Biodegradable polymer microspheres as vaccine adjuvants and delivery systems. Developments in Biological Standardization 92: 6378.Google ScholarPubMed
Halbur, PG, Miller, LD, Paul, PS, Meng, XJ, Huffman, EL and Andrews, JJ (1995). Immunohistochemical identification of porcine reproductive and respiratory syndrome virus (PRRSV) antigen in the heart and lymphoid system of three-week-old colostrum-deprived pigs. Veterinary Pathology 32: 200204.CrossRefGoogle ScholarPubMed
Halliwell, B and Gutteridge, JMC (2006). Free Radicals in Biology and Medicine. 4th edn. Clarendon Press, Oxford.Google Scholar
Harmala, LA, Ingulli, EG, Curtsinger, JM, Lucido, MM, Schmidt, CS, Weigel, BJ, Blazar, BR, Mescher, MF and Pennell, CA (2002). The adjuvant effects of Mycobacterium tuberculosis heat shock protein 70 result from the rapid and prolonged activation of antigen-specific CD8+ T cells in vivo. Journal of Immunology 169: 56225629.CrossRefGoogle ScholarPubMed
Holmgren, J and Czerkinsky, C (2005). Mucosal immunity and vaccines. Nature Medicine 11: S4553.CrossRefGoogle ScholarPubMed
Holmgren, J, Czerkinsky, C, Lycke, N and Svennerholm, AM (1992). Mucosal immunity: implications for vaccine development. Immunobiology 184: 157179.CrossRefGoogle ScholarPubMed
Holtkamp, D and Kliebenstein, J (2011). PRRS costs industry $664 million annually. Pork Checkoff Study, http://www.pork.org/News/1265/PRRSCostsIndustry664Million.aspxGoogle Scholar
Huang, YW and Meng, XJ (2010). Novel strategies and approaches to develop the next generation of vaccines against porcine reproductive and respiratory syndrome virus (PRRSV). Virus Research 154: 141149.CrossRefGoogle ScholarPubMed
Humphreys, IR, De Trez, C, Kinkade, A, Benedict, CA, Croft, M and Ware, CF (2007). Cytomegalovirus exploits IL-10-mediated immune regulation in the salivary glands. Journal of Experimental Medicine 204: 12171225.CrossRefGoogle ScholarPubMed
Hyland, K, Foss, DL, Johnson, CR and Murtaugh, MP (2004). Oral immunization induces local and distant mucosal immunity in swine. Veterinary Immunology and Immunopathology 102: 329338.CrossRefGoogle ScholarPubMed
Ichinohe, T, Kawaguchi, A, Tamura, S, Takahashi, H, Sawa, H, Ninomiya, A, Imai, M, Itamura, S, Odagiri, T, Tashiro, M, Chiba, J, Sata, T, Kurata, T and Hasegawa, H (2007a). Intranasal immunization with H5N1 vaccine plus Poly I:Poly C12U, a Toll-like receptor agonist, protects mice against homologous and heterologous virus challenge. Microbes and Infection 9: 13331340.CrossRefGoogle ScholarPubMed
Ichinohe, T, Tamura, S, Kawaguchi, A, Ninomiya, A, Imai, M, Itamura, S, Odagiri, T, Tashiro, M, Takahashi, H, Sawa, H, Mitchell, WM, Strayer, DR, Carter, WA, Chiba, J, Kurata, T, Sata, T and Hasegawa, H (2007b). Cross-protection against H5N1 influenza virus infection is afforded by intranasal inoculation with seasonal trivalent inactivated influenza vaccine. Journal of Infectious Diseases 196: 13131320.CrossRefGoogle ScholarPubMed
Imaoka, K, Miller, CJ, Kubota, M, Mcchesney, MB, Lohman, B, Yamamoto, M, Fujihashi, K, Someya, K, Honda, M, McGhee, JR and Kiyono, H (1998). Nasal immunization of nonhuman primates with simian immunodeficiency virus p55gag and cholera toxin adjuvant induces Th1/Th2 help for virus-specific immune responses in reproductive tissues. Journal of Immunology 161: 59525958.CrossRefGoogle ScholarPubMed
Inaba, K, Inaba, M, Naito, M and Steinman, RM (1993). Dendritic cell progenitors phagocytose particulates, including bacillus Calmette–Guerin organisms, and sensitize mice to mycobacterial antigens in vivo. Journal of Experimental Medicine 178: 479488.CrossRefGoogle ScholarPubMed
Jepson, MA, Clark, MA, Foster, N, Mason, CM, Bennett, MK, Simmons, NL and Hirst, BH (1996). Targeting to intestinal M cells. Journal of Anatomy 189(Pt 3): 507516.Google ScholarPubMed
Johansson, EL, Bergquist, C, Edebo, A, Johansson, C and Svennerholm, AM (2004). Comparison of different routes of vaccination for eliciting antibody responses in the human stomach. Vaccine 22: 984990.CrossRefGoogle ScholarPubMed
Johansson, EL, Wassen, L, Holmgren, J, Jertborn, M and Rudin, A (2001). Nasal and vaginal vaccinations have differential effects on antibody responses in vaginal and cervical secretions in humans. Infection and Immunity 69: 74817486.CrossRefGoogle ScholarPubMed
Johnsen, CK, Botner, A, Kamstrup, S, Lind, P and Nielsen, J (2002). Cytokine mRNA profiles in bronchoalveolar cells of piglets experimentally infected in utero with porcine reproductive and respiratory syndrome virus: association of sustained expression of IFN-gamma and IL-10 after viral clearance. Viral Immunology 15: 549556.CrossRefGoogle ScholarPubMed
Jung, K, Renukaradhya, GJ, Alekseev, KP, Fang, Y, Tang, Y and Saif, LJ (2009). Porcine reproductive and respiratory syndrome virus modifies innate immunity and alters disease outcome in pigs subsequently infected with porcine respiratory coronavirus: implications for respiratory viral co-infections. Journal of General Virology 90: 27132723.CrossRefGoogle ScholarPubMed
Kamijuku, H, Nagata, Y, Jiang, X, Ichinohe, T, Tashiro, T, Mori, K, Taniguchi, M, Hase, K, Ohno, H, Shimaoka, T, Yonehara, S, Odagiri, T, Tashiro, M, Sata, T, Hasegawa, H and Seino, KI (2008). Mechanism of NKT cell activation by intranasal coadministration of alpha-galactosylceramide, which can induce cross-protection against influenza viruses. Mucosal Immunology 1: 208218.CrossRefGoogle ScholarPubMed
Karron, RA, Wright, PF, Hall, SL, Makhene, M, Thompson, J, Burns, BA, Tollefson, S, Steinhoff, MC, Wilson, MH, Harris, DO, Clements, ML and Murphy, BR (1995). A live attenuated bovine parainfluenza virus type 3 vaccine is safe, infectious, immunogenic, and phenotypically stable in infants and children. Journal of Infectious Diseases 171: 11071114.CrossRefGoogle ScholarPubMed
Kaser, T, Gerner, W, Hammer, SE, Patzl, M and Saalmuller, A (2008). Phenotypic and functional characterisation of porcine CD4(+)CD25(high) regulatory T cells. Veterinary Immunology and Immunopathology 122: 153158.CrossRefGoogle ScholarPubMed
Key, KF, Guenette, DK, Yoon, KJ, Halbur, PG, Toth, TE and Meng, XJ (2003). Development of a heteroduplex mobility assay to identify field isolates of porcine reproductive and respiratory syndrome virus with nucleotide sequences closely related to those of modified live-attenuated vaccines. Journal of Clinical Microbiology 41: 24332439.CrossRefGoogle ScholarPubMed
Kim, DY, Sato, A, Fukuyama, S, Sagara, H, Nagatake, T, Kong, IG, Goda, K, Nochi, T, Kunisawa, J, Sato, S, Yokota, Y, Lee, CH and Kiyono, H (2011). The airway antigen sampling system: respiratory M cells as an alternative gateway for inhaled antigens. Journal of Immunology 186: 42534262.CrossRefGoogle ScholarPubMed
Kim, WI, Lee, DS, Johnson, W, Roof, M, Cha, SH and Yoon, KJ (2007). Effect of genotypic and biotypic differences among PRRS viruses on the serologic assessment of pigs for virus infection. Veterinary Microbiology 123: 114.CrossRefGoogle ScholarPubMed
Kimman, TG, Cornelissen, LA, Moormann, RJ, Rebel, JM and Stockhofe-Zurwieden, N (2009). Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine 27: 37043718.CrossRefGoogle ScholarPubMed
Kinter, AL, Hennessey, M, Bell, A, Kern, S, Lin, Y, Daucher, M, Planta, M, McGlaughlin, M, Jackson, R, Ziegler, SF and Fauci, AS (2004). CD25(+)CD4(+) regulatory T cells from the peripheral blood of asymptomatic HIV-infected individuals regulate CD4(+) and CD8(+) HIV-specific T cell immune responses in vitro and are associated with favorable clinical markers of disease status. Journal of Experimental Medicine 200: 331343.CrossRefGoogle ScholarPubMed
Kit, S (1990). Genetically engineered vaccines for control of Aujeszky's disease (pseudorabies). Vaccine 8: 420424.CrossRefGoogle ScholarPubMed
Kiyono, H and Fukuyama, S (2004). NALT- versus Peyer's-patch-mediated mucosal immunity. Nature Reviews Immunology 4: 699710.CrossRefGoogle ScholarPubMed
Klinge, KL, Vaughn, EM, Roof, MB, Bautista, EM and Murtaugh, MP (2009). Age-dependent resistance to Porcine reproductive and respiratory syndrome virus replication in swine. Virology Journal 6: 177.CrossRefGoogle ScholarPubMed
Kozlowski, PA, Cu-Uvin, S, Neutra, MR and Flanigan, TP (1997). Comparison of the oral, rectal, and vaginal immunization routes for induction of antibodies in rectal and genital tract secretions of women. Infection and Immunity 65: 13871394.CrossRefGoogle ScholarPubMed
Kraehenbuhl, JP and Neutra, MR (2000). Epithelial M cells: differentiation and function. Annual Review of Cell and Developmental Biology 16: 301332.CrossRefGoogle ScholarPubMed
Kuroki, H, Morisaki, T, Matsumoto, K, Onishi, H, Baba, E, Tanaka, M and Katano, M (2003). Streptococcal preparation OK-432: a new maturation factor of monocyte-derived dendritic cells for clinical use. Cancer Immunology, Immunotherapy 52: 561568.CrossRefGoogle ScholarPubMed
Lamontagne, L, Page, C, Larochelle, R, Longtin, D and Magar, R (2001). Polyclonal activation of B cells occurs in lymphoid organs from porcine reproductive and respiratory syndrome virus (PRRSV)-infected pigs. Veterinary Immunology and Immunopathology 82: 165182.CrossRefGoogle ScholarPubMed
Lawson, LB, Norton, EB and Clements, JD (2011). Defending the mucosa: adjuvant and carrier formulations for mucosal immunity. Current Opinion in Immunology 23: 414420.CrossRefGoogle ScholarPubMed
Lawson, SR, Rossow, KD, Collins, JE, Benfield, DA and Rowland, RR (1997). Porcine reproductive and respiratory syndrome virus infection of gnotobiotic pigs: sites of virus replication and co-localization with MAC-387 staining at 21 days post-infection. Virus Research 51: 105113.CrossRefGoogle ScholarPubMed
Lee, CH, Yeh, TH, Lai, HC, Wu, SY, Su, IJ, Takada, K and Chang, Y (2011). Epstein–Barr virus Zta-induced immunomodulators from nasopharyngeal carcinoma cells upregulate interleukin-10 production from monocytes. Journal of Virology 85: 73337342.CrossRefGoogle ScholarPubMed
Lemke, CD, Haynes, JS, Spaete, R, Adolphson, D, Vorwald, A, Lager, K and Butler, JE (2004). Lymphoid hyperplasia resulting in immune dysregulation is caused by porcine reproductive and respiratory syndrome virus infection in neonatal pigs. Journal of Immunology 172: 19161925.CrossRefGoogle ScholarPubMed
Leroith, T, Hammond, S, Todd, SM, Ni, Y, Cecere, T and Pelzer, KD (2011). A modified live PRRSV vaccine and the pathogenic parent strain induce regulatory T cells in pigs naturally infected with Mycoplasma hyopneumoniae. Veterinary Immunology and Immunopathology 14: 312316.CrossRefGoogle Scholar
Li, B, Fang, L, Xu, Z, Liu, S, Gao, J, Jiang, Y, Chen, H and Xiao, S (2009). Recombination in vaccine and circulating strains of porcine reproductive and respiratory syndrome viruses. Emerging Infectious Diseases 15: 20322035.CrossRefGoogle ScholarPubMed
Li, Y, Xue, C, Wang, L, Chen, X, Chen, F and Cao, Y (2010). Genomic analysis of two Chinese strains of porcine reproductive and respiratory syndrome viruses with different virulence. Virus Genes 40: 374381.CrossRefGoogle ScholarPubMed
Loemba, HD, Mounir, S, Mardassi, H, Archambault, D and Dea, S (1996). Kinetics of humoral immune response to the major structural proteins of the porcine reproductive and respiratory syndrome virus. Archives of Virology 141: 751761.CrossRefGoogle Scholar
Lohse, L, Nielsen, J and Eriksen, L (2004). Temporary CD8+ T-cell depletion in pigs does not exacerbate infection with porcine reproductive and respiratory syndrome virus (PRRSV). Viral Immunology 17: 594603.CrossRefGoogle Scholar
Lopez Fuertes, L, Domenech, N, Alvarez, B, Ezquerra, A, Dominguez, J, Castro, JM and Alonso, F (1999). Analysis of cellular immune response in pigs recovered from porcine respiratory and reproductive syndrome infection. Virus Research 64: 3342.CrossRefGoogle ScholarPubMed
Lopez, OJ, Oliveira, MF, Garcia, EA, Kwon, BJ, Doster, A and Osorio, FA (2007). Protection against porcine reproductive and respiratory syndrome virus (PRRSV) infection through passive transfer of PRRSV-neutralizing antibodies is dose dependent. Clinical and Vaccine Immunology 14: 269275.CrossRefGoogle ScholarPubMed
Lopez, OJ and Osorio, FA (2004). Role of neutralizing antibodies in PRRSV protective immunity. Veterinary Immunology and Immunopathology 102: 155163.CrossRefGoogle ScholarPubMed
Madsen, KG, Hansen, CM, Madsen, ES, Strandbygaard, B, Botner, A and Sorensen, KJ (1998). Sequence analysis of porcine reproductive and respiratory syndrome virus of the American type collected from Danish swine herds. Archives of Virology 143: 16831700.CrossRefGoogle ScholarPubMed
Mann, JF, Acevedo, R, Campo, JD, Perez, O and Ferro, VA (2009). Delivery systems: a vaccine strategy for overcoming mucosal tolerance? Expert Review of Vaccines 8: 103112.CrossRefGoogle ScholarPubMed
Martelli, P, Gozio, S, Ferrari, L, Rosina, S, De Angelis, E, Quintavalla, C, Bottarelli, E and Borghetti, P (2009). Efficacy of a modified live porcine reproductive and respiratory syndrome virus (PRRSV) vaccine in pigs naturally exposed to a heterologous European (Italian cluster) field strain: Clinical protection and cell-mediated immunity. Vaccine 27: 37883799.CrossRefGoogle ScholarPubMed
Martin, JH and Edwards, SW (1993). Changes in mechanisms of monocyte/macrophage-mediated cytotoxicity during culture. Reactive oxygen intermediates are involved in monocyte-mediated cytotoxicity, whereas reactive nitrogen intermediates are employed by macrophages in tumor cell killing. Journal of Immunology 150: 34783486.CrossRefGoogle ScholarPubMed
Mateu, E and Diaz, I (2008). The challenge of PRRS immunology. Veterinary Journal 177: 345351.CrossRefGoogle ScholarPubMed
Mateu, E, Diaz, I, Darwich, L, Casal, J, Martin, M and Pujols, J (2006). Evolution of ORF5 of Spanish porcine reproductive and respiratory syndrome virus strains from 1991 to 2005. Virus Research 115: 198206.CrossRefGoogle ScholarPubMed
McNeil, SE (2005). Nanotechnology for the biologist. Journal of Leukocyte Biology 78: 585594.CrossRefGoogle ScholarPubMed
Meier, WA, Galeota, J, Osorio, FA, Husmann, RJ, Schnitzlein, WM and Zuckermann, FA (2003). Gradual development of the interferon-gamma response of swine to porcine reproductive and respiratory syndrome virus infection or vaccination. Virology 309: 1831.CrossRefGoogle ScholarPubMed
Meng, XJ (2000). Heterogeneity of porcine reproductive and respiratory syndrome virus: implications for current vaccine efficacy and future vaccine development. Veterinary Microbiology 74: 309329.CrossRefGoogle ScholarPubMed
Mengeling, WL, Clouser, DF, Vorwald, AC and Lager, KM (2002). The potential role of genetic recombination in the evolution of new strains of porcine reproductive and respiratory syndrome virus (PRRSV). Journal of Swine Health and Production 10: 273275.Google Scholar
Mengeling, WL, Lager, KM and Vorwald, AC (1998). Clinical consequences of exposing pregnant gilts to strains of porcine reproductive and respiratory syndrome (PRRS) virus isolated from field cases of “atypical” PRRS. American Journal of Veterinary Research 59: 15401544.CrossRefGoogle ScholarPubMed
Mengeling, WL, Lager, KM, Vorwald, AC and Clouser, DF (2003a). Comparative safety and efficacy of attenuated single-strain and multi-strain vaccines for porcine reproductive and respiratory syndrome. Veterinary Microbiology 93: 2538.CrossRefGoogle ScholarPubMed
Mengeling, WL, Lager, KM, Vorwald, AC and Koehler, KJ (2003b). Strain specificity of the immune response of pigs following vaccination with various strains of porcine reproductive and respiratory syndrome virus. Veterinary Microbiology 93: 1324.CrossRefGoogle ScholarPubMed
Meulenberg, JJ (2000). PRRSV, the virus. Veterinary Research 31: 1121.Google ScholarPubMed
Mowat, AM (2003). Anatomical basis of tolerance and immunity to intestinal antigens. Nature Reviews Immunology 3: 331341.CrossRefGoogle ScholarPubMed
Moyron-Quiroz, J, Rangel-Moreno, J, Carragher, DM and Randall, TD (2007). The function of local lymphoid tissues in pulmonary immune responses. Advances in Experimental Medicine and Biology 590: 5568.CrossRefGoogle ScholarPubMed
Murtaugh, MP, Xiao, Z and Zuckermann, F (2002a). Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunology 15: 533547.CrossRefGoogle ScholarPubMed
Murtaugh, MP, Yuan, S, Nelson, EA and Faaberg, KS (2002b). Genetic interaction between porcine reproductive and respiratory syndrome virus (PRRSV) strains in cell culture and in animals. Journal of Swine Health and Production 10: 1521.Google Scholar
Nardelli-Haefliger, D, Wirthner, D, Schiller, JT, Lowy, DR, Hildesheim, A, Ponci, F and De Grandi, P (2003). Specific antibody levels at the cervix during the menstrual cycle of women vaccinated with human papillomavirus 16 virus-like particles. Journal of the National Cancer Institute 95: 11281137.CrossRefGoogle ScholarPubMed
Nayak, B, Panda, AK, Ray, P and Ray, AR (2009). Formulation, characterization and evaluation of rotavirus encapsulated PLA and PLGA particles for oral vaccination. Journal of Microencapsulation 26: 154165.CrossRefGoogle ScholarPubMed
Nel, A, Xia, T, Madler, L and Li, N (2006). Toxic potential of materials at the nanolevel. Science 311: 622627.CrossRefGoogle ScholarPubMed
Nelson, EA, Christopher-Hennings, J and Benfield, DA (1994). Serum immune responses to the proteins of porcine reproductive and respiratory syndrome (PRRS) virus. Journal of Veterinary Diagnostic Investigation 6: 410415.CrossRefGoogle Scholar
Neutra, MR and Kozlowski, PA (2006). Mucosal vaccines: the promise and the challenge. Nature Reviews Immunology 6: 148158.CrossRefGoogle ScholarPubMed
Neutra, MR, Mantis, NJ, Frey, A and Giannasca, PJ (1999). The composition and function of M cell apical membranes: implications for microbial pathogenesis. Seminars in Immunology 11: 171181.CrossRefGoogle ScholarPubMed
Nielsen, HS, Oleksiewicz, MB, Forsberg, R, Stadejek, T, Botner, A and Storgaard, T (2001). Reversion of a live porcine reproductive and respiratory syndrome virus vaccine investigated by parallel mutations. Journal of General Virology 82: 12631272.CrossRefGoogle ScholarPubMed
Nielsen, J, Botner, A, Bille-Hansen, V, Oleksiewicz, MB and Storgaard, T (2002). Experimental inoculation of late term pregnant sows with a field isolate of porcine reproductive and respiratory syndrome vaccine-derived virus. Veterinary Microbiology 84: 113.CrossRefGoogle ScholarPubMed
Ogra, PL (1984). Mucosal immune response to poliovirus vaccines in childhood. Review of Infectious Diseases 6 (Suppl. 2): S361368.CrossRefGoogle ScholarPubMed
Opriessnig, T, Halbur, PG, Yoon, KJ, Pogranichniy, RM, Harmon, KM, Evans, R, Key, KF, Pallares, FJ, Thomas, P and Meng, XJ (2002). Comparison of molecular and biological characteristics of a modified live porcine reproductive and respiratory syndrome virus (PRRSV) vaccine (ingelvac PRRS MLV), the parent strain of the vaccine (ATCC VR2332), ATCC VR2385, and two recent field isolates of PRRSV. Journal of Virology 76: 1183711844.CrossRefGoogle ScholarPubMed
Osorio, FA, Galeota, JA, Nelson, E, Brodersen, B, Doster, A, Wills, R, Zuckermann, F and Laegreid, WW (2002). Passive transfer of virus-specific antibodies confers protection against reproductive failure induced by a virulent strain of porcine reproductive and respiratory syndrome virus and establishes sterilizing immunity. Virology 302: 920.CrossRefGoogle ScholarPubMed
Ostrowski, M, Galeota, JA, Jar, AM, Platt, KB, Osorio, FA and Lopez, OJ (2002). Identification of neutralizing and nonneutralizing epitopes in the porcine reproductive and respiratory syndrome virus GP5 ectodomain. Journal of Virology 76: 42414250.CrossRefGoogle ScholarPubMed
Otake, S, Dee, S, Corzo, C, Oliveira, S and Deen, J (2010). Long-distance airborne transport of infectious PRRSV and Mycoplasma hyopneumoniae from a swine population infected with multiple viral variants. Veterinary Microbiology 145: 198208.CrossRefGoogle ScholarPubMed
Pabst, R and Binns, RM (1989). Heterogeneity of lymphocyte homing physiology: several mechanisms operate in the control of migration to lymphoid and non-lymphoid organs in vivo. Immunological Reviews 108: 83109.CrossRefGoogle ScholarPubMed
Panyam, J and Labhasetwar, V (2003). Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Advanced Drug Delivery Reviews 55: 329347.CrossRefGoogle ScholarPubMed
Peng, G, Li, S, Wu, W, Sun, Z, Chen, Y and Chen, Z (2008). Circulating CD4+ CD25+ regulatory T cells correlate with chronic hepatitis B infection. Immunology 123: 5765.CrossRefGoogle ScholarPubMed
Petrovsky, N and Aguilar, JC (2004). Vaccine adjuvants: current state and future trends. Immunology and Cell Biology 82: 488496.CrossRefGoogle ScholarPubMed
Pitkin, A, Deen, J and Dee, S (2009). Further assessment of fomites and personnel as vehicles for the mechanical transport and transmission of porcine reproductive and respiratory syndrome virus. Canadian Journal of Veterinary Research 73: 298302.Google ScholarPubMed
Plotkin, SA (2005). Vaccines: past, present and future. Nature Medicine 11: S511.CrossRefGoogle ScholarPubMed
Quinn, MT and Gauss, KA (2004). Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. Journal of Leukocyte Biology 76: 760781.CrossRefGoogle ScholarPubMed
Randall, TD (2010). Bronchus-associated lymphoid tissue (BALT) structure and function. Advances in Immunology 107: 187241.CrossRefGoogle ScholarPubMed
Read, S, Malmstrom, V and Powrie, F (2000). Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. Journal of Experimental Medicine 192: 295302.CrossRefGoogle ScholarPubMed
Renukaradhya, GJ, Alekseev, K, Jung, K, Fang, Y and Saif, LJ (2010). Porcine reproductive and respiratory syndrome virus-induced immunosuppression exacerbates the inflammatory response to porcine respiratory coronavirus in pigs. Viral Immunology 23: 457466.CrossRefGoogle ScholarPubMed
Rimmelzwaan, GF, Baars, MM, De Lijster, P, Fouchier, RA and Osterhaus, AD (1999). Inhibition of influenza virus replication by nitric oxide. Journal of Virology 73: 88808883.CrossRefGoogle ScholarPubMed
Roberts, P, Jeffery, PK, Mitchell, TJ, Andrew, PW, Boulnois, GJ, Feldman, C, Cole, PJ and Wilson, R (1992). Effect of immunization with Freund's adjuvant and pneumolysin on histologic features of pneumococcal infection in the rat lung in vivo. Infection and Immunity 60: 49694972.CrossRefGoogle ScholarPubMed
Rodriguez, A, Troye-Blomberg, M, Lindroth, K, Ivanyi, J, Singh, M and Fernandez, C (2003). B- and T-cell responses to the mycobacterium surface antigen PstS-1 in the respiratory tract and adjacent tissues. Role of adjuvants and routes of immunization. Vaccine 21: 458467.CrossRefGoogle Scholar
Rossow, KD, Bautista, EM, Goyal, SM, Molitor, TW, Murtaugh, MP, Morrison, RB, Benfield, DA and Collins, JE (1994). Experimental porcine reproductive and respiratory syndrome virus infection in one-, four-, and 10-week-old pigs. Journal of Veterinary Diagnostic Investigations 6: 312.CrossRefGoogle ScholarPubMed
Rossow, KD, Benfield, DA, Goyal, SM, Nelson, EA, Christopher-Hennings, J and Collins, JE (1996). Chronological immunohistochemical detection and localization of porcine reproductive and respiratory syndrome virus in gnotobiotic pigs. Veterinary Pathology 33: 551556.CrossRefGoogle ScholarPubMed
Rowland, RR (2007). The stealthy nature of PRRSV infection: the dangers posed by that ever-changing mystery swine disease. Veterinary Journal 174: 451.CrossRefGoogle ScholarPubMed
Royaee, AR, Husmann, RJ, Dawson, HD, Calzada-Nova, G, Schnitzlein, WM, Zuckermann, FA and Lunney, JK (2004). Deciphering the involvement of innate immune factors in the development of the host response to PRRSV vaccination. Veterinary Immunology and Immunopathology 102: 199216.CrossRefGoogle ScholarPubMed
Sakaguchi, S, Wing, K, Onishi, Y, Prieto-Martin, P and Yamaguchi, T (2009). Regulatory T cells: how do they suppress immune responses? International Immunology 21: 11051111.CrossRefGoogle ScholarPubMed
Schmidt, AC, Wenzke, DR, Mcauliffe, JM, St Claire, M, Elkins, WR, Murphy, BR and Collins, PL (2002). Mucosal immunization of rhesus monkeys against respiratory syncytial virus subgroups A and B and human parainfluenza virus type 3 by using a live cDNA-derived vaccine based on a host range-attenuated bovine parainfluenza virus type 3 vector backbone. Journal of Virology 76: 10891099.CrossRefGoogle Scholar
Semete, B, Booysen, L, Lemmer, Y, Kalombo, L, Katata, L, Verschoor, J and Swai, HS (2010). In vivo evaluation of the biodistribution and safety of PLGA nanoparticles as drug delivery systems. Nanomedicine 6: 662671.CrossRefGoogle ScholarPubMed
Shephard, MJ, Todd, D, Adair, BM, Po, AL, Mackie, DP and Scott, EM (2003). Immunogenicity of bovine parainfluenza type 3 virus proteins encapsulated in nanoparticle vaccines, following intranasal administration to mice. Research in Veterinary Science 74: 187190.CrossRefGoogle ScholarPubMed
Silva-Campa, E, Cordoba, L, Fraile, L, Flores-Mendoza, L, Montoya, M and Hernandez, J (2009a). European genotype of porcine reproductive and respiratory syndrome (PRRSV) infects monocyte-derived dendritic cells but does not induce Treg cells. Virology 396: 264271.CrossRefGoogle Scholar
Silva-Campa, E, Flores-Mendoza, L, Resendiz, M, Pinelli-Saavedra, A, Mata-Haro, V, Mwangi, W and Hernandez, J (2009b). Induction of T helper 3 regulatory cells by dendritic cells infected with porcine reproductive and respiratory syndrome virus. Virology 387: 373379.CrossRefGoogle ScholarPubMed
Singh, M, Briones, M and O'hagan, DT (2001). A novel bioadhesive intranasal delivery system for inactivated influenza vaccines. Journal of Controlled Release 70: 267276.CrossRefGoogle ScholarPubMed
Sirinarumitr, T, Zhang, Y, Kluge, JP, Halbur, PG and Paul, PS (1998). A pneumo-virulent United States isolate of porcine reproductive and respiratory syndrome virus induces apoptosis in bystander cells both in vitro and in vivo. Journal of General Virology 79 (Pt 12): 29892995.CrossRefGoogle ScholarPubMed
Sminia, T, Van Der Brugge-Gamelkoorn, GJ and Jeurissen, SH (1989). Structure and function of bronchus-associated lymphoid tissue (BALT). Critical Reviews in Immunology 9: 119150.Google ScholarPubMed
Srivastava, P (2002). Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annual Reviews in Immunology 20: 395425.CrossRefGoogle ScholarPubMed
Sun, J, Dodd, H, Moser, EK, Sharma, R and Braciale, TJ (2011). CD4+ T cell help and innate-derived IL-27 induce Blimp-1-dependent IL-10 production by antiviral CTLs. Nature Immunology 12: 327334.CrossRefGoogle ScholarPubMed
Suradhat, S and Thanawongnuwech, R (2003). Upregulation of interleukin-10 gene expression in the leukocytes of pigs infected with porcine reproductive and respiratory syndrome virus. Journal of General Virology 84: 27552760.CrossRefGoogle ScholarPubMed
Suradhat, S, Thanawongnuwech, R and Poovorawan, Y (2003). Upregulation of IL-10 gene expression in porcine peripheral blood mononuclear cells by porcine reproductive and respiratory syndrome virus. Journal of General Virology 84: 453459.CrossRefGoogle ScholarPubMed
Suvas, S, Azkur, AK, Kim, BS, Kumaraguru, U and Rouse, BT (2004). CD4+CD25+ regulatory T cells control the severity of viral immunoinflammatory lesions. Journal of Immunology 172: 41234132.CrossRefGoogle ScholarPubMed
Suzuki, H, Sekine, S, Kataoka, K, Pascual, DW, Maddaloni, M, Kobayashi, R, Fujihashi, K, Kozono, H and McGhee, JR (2008). Ovalbumin-protein sigma 1 M-cell targeting facilitates oral tolerance with reduction of antigen-specific CD4+ T cells. Gastroenterology 135: 917925.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Young, TF, Thacker, BJ and Thacker, EL (2001). Differential production of proinflammatory cytokines: in vitro PRRSV and Mycoplasma hyopneumoniae co-infection model. Veterinary Immunology and Immunopathology 79: 115127.CrossRefGoogle ScholarPubMed
Thiel, V and Weber, F (2008). Interferon and cytokine responses to SARS-coronavirus infection. Cytokine Growth Factor Reviews 19: 121132.CrossRefGoogle ScholarPubMed
Thomas, C, Gupta, V and Ahsan, F (2009). Influence of surface charge of PLGA particles of recombinant hepatitis B surface antigen in enhancing systemic and mucosal immune responses. International Journal of Pharmacology 379: 4150.CrossRefGoogle ScholarPubMed
Trandem, K, Jin, Q, Weiss, KA, James, BR, Zhao, J and Perlman, S (2011a). Virally expressed IL-10 ameliorates acute encephalomyelitis and chronic demyelination in coronavirus-infected mice. Journal of Virology 85: 68226831.CrossRefGoogle ScholarPubMed
Trandem, K, Zhao, J, Fleming, E and Perlman, S (2011b). Highly activated cytotoxic CD8 T cells express protective IL-10 at the peak of coronavirus-induced encephalitis. Journal of Immunology 186: 36423652.CrossRefGoogle ScholarPubMed
Tschernig, T and Pabst, R (2000). Bronchus-associated lymphoid tissue (BALT) is not present in the normal adult lung but in different diseases. Pathobiology 68: 18.CrossRefGoogle Scholar
Vahlenkamp, TW, Tompkins, MB and Tompkins, WA (2005). The role of CD4+CD25+ regulatory T cells in viral infections. Veterinary Immunology and Immunopathology 108: 219225.CrossRefGoogle ScholarPubMed
Van Der Poel, WH, Kramps, JA, Quak, J, Brand, A and Van Oirschot, JT (1995). Persistence of bovine herpesvirus-1-specific antibodies in cattle after intranasal vaccination with a live virus vaccine. Veterinary Record 137: 347348.CrossRefGoogle ScholarPubMed
Van Oirschot, JT, Rziha, HJ, Moonen, PJ, Pol, JM and Van Zaane, D (1986). Differentiation of serum antibodies from pigs vaccinated or infected with Aujeszky's disease virus by a competitive enzyme immunoassay. Journal of General Virology 67 (Pt 6): 11791182.CrossRefGoogle ScholarPubMed
Van Reeth, K, Labarque, G, Nauwynck, H and Pensaert, M (1999). Differential production of proinflammatory cytokines in the pig lung during different respiratory virus infections: correlations with pathogenicity. Research in Veterinary Science 67: 4752.CrossRefGoogle ScholarPubMed
Van Reeth, K, Van Gucht, S and Pensaert, M (2002). In vivo studies on cytokine involvement during acute viral respiratory disease of swine: troublesome but rewarding. Veterinary Immunology and Immunopathology 87: 161168.CrossRefGoogle ScholarPubMed
Vaughan, M (1997). Oxidative modification of macromolecules, Minireviews Series. Journal of Biological Chemistry 272: 18513.CrossRefGoogle Scholar
Vanhee, M, Delputte, PL, Delrue, I, Geldhof, MF and Nauwynck, HJ (2009). Development of an experimental inactivated PRRSV vaccine that induces virus-neutralizing antibodies. Veterinary Research 40: 6377.CrossRefGoogle ScholarPubMed
Voicu, IL, Silim, A, Morin, M and Elazhary, MA (1994). Interaction of porcine reproductive and respiratory syndrome virus with swine monocytes. Veterinary Record 134: 422423.CrossRefGoogle ScholarPubMed
Vu, HL, Kwon, B, Yoon, KJ, Laegreid, WW, Pattnaik, AK and Osorio, FA (2011). Immune evasion of porcine reproductive and respiratory syndrome virus through glycan shielding involves both glycoprotein 5 as well as glycoprotein 3. Journal of Virology 85: 55555564.CrossRefGoogle ScholarPubMed
Wagstrom, EA, Chang, CC, Yoon, KJ and Zimmerman, JJ (2001). Shedding of porcine reproductive and respiratory syndrome virus in mammary gland secretions of sows. American Journal of Veterinary Research 62: 18761880.CrossRefGoogle ScholarPubMed
Wensvoort, G, Terpstra, C, Pol, JM, Ter Laak, EA, Bloemraad, M, De Kluyver, EP, Kragten, C, Van Buiten, L, Den Besten, A, Wagenaar, F, Broekhuijsen, JM, Moonen, PLJM, Zetstra, T, de Boer, EA, Tibben, HJ, de Jong, MF, Van't Veld, P, Groenland, GJR, Van Gennep, JA, Voets, MT, Verheijden, JHM and Braamskamp, J (1991). Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Veterinary Quarterly 13: 121130.CrossRefGoogle ScholarPubMed
Werner, GH, Maral, R, Floch, F, Migliore-Samour, D and Jolles, P (1975). Adjuvant and immunostimulating activities of water-soluble substances extracted from Mycobacterium tuberculosis (var. hominis). Biomedicine 22: 440452.Google ScholarPubMed
White, RG, Coons, AH and Connolly, JM (1955). Studies on antibody production. IV. The role of a wax fraction of Mycobacterium tuberculosis in adjuvant emulsions on the production of antibody to egg albumin. Journal of Experimental Medicine 102: 83104.CrossRefGoogle ScholarPubMed
Wongyanin, P, Buranapraditkun, S, Chokeshai-Usaha, K, Thanawonguwech, R and Suradhat, S (2010). Induction of inducible CD4+CD25+Foxp3+ regulatory T lymphocytes by porcine reproductive and respiratory syndrome virus (PRRSV). Veterinary Immunology and Immunopathology 133: 170182.CrossRefGoogle ScholarPubMed
Wongyanin, P, Buranapraditkun, S, Thanawonguwech, R, Roth, JA and Suradhat, S (2009). Effect of nucleocapsid protein of PRRSV on the induction of interleuklin-10 producing lymphocytes. International PRRS Symposium, December 4–5, 2009, Chicago, IL, Abstract p. 95.Google Scholar
Woodland, DL and Randall, TD (2004). Anatomical features of anti-viral immunity in the respiratory tract. Seminars in Immunology 16: 163170.CrossRefGoogle ScholarPubMed
Yang, H and Parkhouse, RM (1996). Phenotypic classification of porcine lymphocyte subpopulations in blood and lymphoid tissues. Immunology 89: 7683.CrossRefGoogle ScholarPubMed
Yang, H and Parkhouse, RM (1997). Differential expression of CD8 epitopes amongst porcine CD8-positive functional lymphocyte subsets. Immunology 92: 4552.CrossRefGoogle ScholarPubMed
Yoo, D, Song, C, Sun, Y, Du, Y, Kim, O and Liu, HC (2010). Modulation of host cell responses and evasion strategies for porcine reproductive and respiratory syndrome virus. Virus Research 154: 4860.CrossRefGoogle ScholarPubMed
Yoon, KJ, Zimmerman, JJ, Swenson, SL, McGinley, MJ, Eernisse, KA, Brevik, A, Rhinehart, LL, Frey, ML, Hill, HT and Platt, KB (1995). Characterization of the humoral immune response to porcine reproductive and respiratory syndrome (PRRS) virus infection. Journal of Veterinary Diagnostic Investigation 7: 305312.CrossRefGoogle ScholarPubMed
Zhang, L, Tian, X and Zhou, F (2006). In vivo effects of oligodeoxynucleotides containing synthetic immunostimulatory motifs in weaned piglets. International Immunopharmacology 6: 16231631.CrossRefGoogle ScholarPubMed
Zhang, L, Tian, X and Zhou, F (2007). Intranasal administration of CpG oligonucleotides induces mucosal and systemic Type 1 immune responses and adjuvant activity to porcine reproductive and respiratory syndrome killed virus vaccine in piglets in vivo. International Immunopharmacology 7: 17321740.CrossRefGoogle ScholarPubMed
Zimmerman, J (2003). PRRS virus – what happens after a pig becomes infected with PRRS virus? In 2003 PRRS Compendium Producer Edition, Chapter V, Des Moines, Iowa: National Pork Board, pp. 3643.Google Scholar
Zimmerman, J, Benfield, DA, Murtaugh, MPEA, Straw, BE, Zimmerman, JJ, D'Allaire, S and Taylor, DJ (2006). Porcine reproductive and respiratory syndrome virus (porcine arterivirus). In: Straw, BE, Zimmerman, J, D'Allaire, S et al. (eds) Diseases of Swine. 9th edn.Ames, Iowa: Blackwell Publishing, pp. 387418.Google Scholar
Zuckermann, FA (1999). Extrathymic CD4/CD8 double positive T cells. Veterinary Immunology and Immunopathology 72: 5566.CrossRefGoogle ScholarPubMed