Functional impairment of PRRSV-specific peripheral CD3+CD8 high cells

Veterinary Research

Volumn 40, Issue 5, 2009, Pages

  Costers, Sarah ^a   Lefebvre, David J ^a   Goddeeris, Bruno ^b   Delputte, Peter L ^a   Nauwynck, Hans J ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Alveolar macrophage; Cell mediated immune response; Cytotoxic T lymphocyte; PRRSV

Indexed keywords

ANIMAL CELL; ARTERIVIRUS; ARTICLE; AUTOGRAFT; CELL ASSAY; CELL ISOLATION; CELL SPECIFICITY; CELL STIMULATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; IMMUNOMODULATION; LUNG ALVEOLUS MACROPHAGE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PSEUDORABIES HERPETOVIRUS; SWINE; T LYMPHOCYTE ACTIVATION; TARGET CELL; VIRUS INFECTION; VIRUS NEUTRALIZATION; VIRUS STRAIN; ANIMAL; CELL CULTURE; FLOW CYTOMETRY; IMMUNOLOGY; MACROPHAGE; METABOLISM; VIREMIA; VIROLOGY;

BEGONIA; LELYSTAD VIRUS; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUID HERPESVIRUS 1; SUIDAE;

CD3 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON;

ANIMALS; ANTIGENS, CD3; ANTIGENS, CD8; CELLS, CULTURED; FLOW CYTOMETRY; INTERFERON-GAMMA; MACROPHAGES; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SWINE; T-LYMPHOCYTES, CYTOTOXIC; VIREMIA;

EID: 67650983118     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1051/vetres/2009029     Document Type: Article

References (65)

1. Aandahl E.M., Michaelsson J., Moretto W.J., Hecht F.M., Nixon D.F., Human CD4+ CD25+ regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens, J. Virol. (2004) 78:2454-2459. (Pubitemid 38228938)
2. 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) 18:485-490.
3. Albina E., Piriou L., Hutet E., Cariolet R., L'Hospitalier R., Immune responses in pigs infected with porcine reproductive and respiratory syndrome virus (PRRSV), Vet. Immunol. Immunopathol. (1998) 61:49-66.
4. Allende R., Laegreid W.W., Kutish G.F., Galeota J.A., Wills R.W., Osorio F.A., Porcine reproductive and respiratory syndrome virus: description of persistence in individual pigs upon experimental infection, J. Virol. (2000) 74:10834-10837. (Pubitemid 30815410)
5. Andries K., Pensaert M.B., Vandeputte J., Effect of experimental infection with pseudorabies (Aujeszky's disease) virus on pigs with maternal immunity from vaccinated sows, Am. J. Vet. Res. (1978) 39:1282-1285. (Pubitemid 10206320)
6. Aubert M., Jerome K.R., Apoptosis prevention as a mechanism of immune evasion, Int. Rev. Immunol. (2003) 22:361-371. (Pubitemid 37247658)
7. Batista L., Pijoan C., Dee S., Olin M., Molitor T., Joo H.S., et al., Virological and immunological responses to porcine reproductive and respiratory syndrome virus in a large population of gilts, Can. J. Vet. Res. (2004) 68:267-273. (Pubitemid 39562436)
8. Bautista E.M., Molitor T.W., Cell-mediated immunity to porcine reproductive and respiratory syndrome virus in swine, Viral Immunol. (1997) 10:83-94. (Pubitemid 27326747)
9. Beckebaum S., Cicinnati V.R., Zhang X., Ferencik S., Frilling A., Grosse-Wilde H., et al., Hepatitis B virusinduced defect of monocyte-derived dendritic cells leads to impairedThelper type 1 response in vitro:mechanisms for viral immune escape, Immunology (2003) 109: 487-495. (Pubitemid 36930163)
10. Cavanagh D., Nidovirales: a new order comprising Coronaviridae and Arteriviridae, Arch. Virol. (1997) 142:629-633.
11. Chang H.C., Peng Y.T., Chang H.L., Chaung H.C., Chung W.B., Phenotypic and functional modulation of bone marrow-derived dendritic cells by porcine reproductive and respiratory syndrome virus, Vet. Microbiol. (2008) 129:281-293.
12. Charerntantanakul W., Platt R., Johnson W., Roof M., Vaughn E., Roth J.A., Immune responses and protection by vaccine and various vaccine adjuvant candidates to virulent porcine reproductive and respiratory syndrome virus, Vet. Immunol. Immunopathol. (2006) 109:99-115. (Pubitemid 41739680)
13. Chung H.K., Chae C., Expression of interleukin-10 and interleukin-12 in piglets experimentally infected with porcine reproductive and respiratory syndrome virus (PRRSV), J. Comp. Pathol. (2003) 129:205-212. (Pubitemid 37069336)
14. Collins J.E., Benfield D.A., Christianson W.T., Harris L., Hennings J.C., Shaw D.P., 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) 4:117-126.
15. Costers S., Delputte P.L., Nauwynck H.J., Porcine reproductive and respiratory syndrome virusinfected alveolar macrophages contain no detectable levels of viral proteins in their plasma membrane and are protected against antibody-dependent, complement-mediated cell lysis, J. Gen. Virol. (2006) 87: 2341-2351. (Pubitemid 44178110)
16. De Bruin M.G., De Visser Y.E., Kimman T.G., Bianchi A.T., Time course of the porcine cellular and humoral immune responses in vivo against pseudorabies virus after inoculation and challenge: significance of in vitro antigenic restimulation, Vet. Immunol. Immunopathol. (1998) 65:75-87.
17. Delputte P.L., Vanderheijden N., Nauwynck H.J., Pensaert M.B., 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) 76:4312-4320. (Pubitemid 34309567)
18. Diaz I., Darwich L., Pappaterra G., Pujols J., Mateu E., Immune responses of pigs after experimental infection with a European strain of porcine reproductive and respiratory syndrome virus, J. Gen. Virol. (2005) 86:1943-1951.
19. Diaz I., Darwich L., Pappaterra G., Pujols 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: 249-259. (Pubitemid 44108075)
20. Duan X., Nauwynck H.J., Pensaert M.B., Virus quantification and identification of cellular targets in the lungs and lymphoid tissues of pigs at different time intervals after inoculation with porcine reproductive and respiratory syndrome virus (PRRSV), Vet. Microbiol. (1997) 56:9-19. (Pubitemid 27286178)
21. Even C., Rowland R.R., Plagemann P.G., Cytotoxic T cells are elicited during acute infection of mice with lactate dehydrogenase-elevating virus but disappear during the chronic phase of infection, J. Virol. (1995) 69:5666-5676.
22. Favoreel H.W., Nauwynck H.J., Van Oostveldt P., Mettenleiter T.C., Pensaert M.B., Antibody-induced and cytoskeleton-mediated redistribution and shedding of viral glycoproteins, expressed on pseudorabies virus-infected cells, J. Virol. (1997) 71:8254-8261. (Pubitemid 27446401)
23. Flores-Mendoza L., Silva-Campa E., Resendiz M., Osorio F.A., Hernandez J., Porcine reproductive and respiratory syndrome virus infects mature porcine dendritic cells and up-regulates interleukin-10 production, Clin. Vaccine Immunol. (2008) 15:720-725.
24. Gerdes J., Schwab U., Lemke H., Stein H., Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation, Int. J. Cancer (1983) 31:13-20. (Pubitemid 13179545)
25. Grakoui A., John Wherry E., Hanson H.L., Walker C., Ahmed R., Turning on the off switch: regulation of anti-viral T cell responses in the liver by the PD-1/PD-L1 pathway, J. Hepatol. (2006) 45: 468-472. (Pubitemid 44307391)
26. Hewitt E.W., The MHC class I antigen presentation pathway: strategies for viral immune evasion, Immunology (2003) 110:163-169. (Pubitemid 37249255)
27. Janeway C.A., Travers P., Walport M., Schlomchik M., Immunobiology, the immune system in health and disease, 6th edn., Garland Science Publishing, New York, USA, 2005.
28. Kawashima K., Narita M., Yamada S., Changes in macrophage and lymphocyte subpopulations of lymphoid tissues from pigs infected with the porcine reproductive and respiratory syndrome virus (PRRSV), Vet. Immunol. Immunopathol. (1999) 71: 257-262.
29. Kim W.I., Lee D.S., Johnson W., Roof M., Cha S.H., Yoon K.J., Effect of genotypic and biotypic differences among PRRS viruses on the serologic assessment of pigs for virus infection, Vet. Microbiol. (2007) 123:1-14.
30. Kinter A.L., Horak R., Sion M., Riggin L., McNally J., Lin Y., et al., CD25+ regulatory T cells isolated from HIV-infected individuals suppress the cytolytic and nonlytic antiviral activity of HIV-specific CD8+ T cells in vitro, AIDS Res. Hum. Retroviruses (2007) 23:438-450.
31. Labarque G.G., Nauwynck H.J., Van Reeth K., Pensaert M.B., 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) 81:1327-1334.
32. Lamontagne L., Page C., Larochelle R., Longtin D., Magar R., Polyclonal activation of B cells occurs in lymphoid organs from porcine reproductive and respiratory syndrome virus (PRRSV)-infected pigs, Vet. Immunol. Immunopathol. (2001) 82:165-182. (Pubitemid 32913116)
33. Lamontagne L., Page C., Larochelle R., Magar R., Porcine reproductive and respiratory syndrome virus persistence in blood, spleen, lymph nodes, and tonsils of experimentally infected pigs depends on the level of CD8high T cells, Viral Immunol. (2003) 16:395-406.
34. Lefebvre D.J., Costers S., Van Doorsselaere J., Misinzo G., Delputte P.L., Nauwynck H.J., Antigenic differences among porcine circovirus type 2 strains, as demonstrated by the use of monoclonal antibodies, J. Gen. Virol. (2008) 89:177-187.
35. Levings M.K., Bacchetta R., Schulz U., Roncarolo M.G., The role of IL-10 and TGF-beta in the differentiation and effector function of T regulatory cells, Int. Arch. Allergy Immunol. (2002) 129: 263-276.
36. Lopez Fuertes L., Domenech N., Alvarez B., Ezquerra A., Dominguez J., Castro J.M., Alonso F., Analysis of cellular immune response in pigs recovered from porcine respiratory and reproductive syndrome infection, Virus Res. (1999) 64:33-42. (Pubitemid 29438674)
37. Lopez O.J., Osorio F.A., Role of neutralizing antibodies in PRRSV protective immunity, Vet. Immunol. Immunopathol. (2004) 102:155-163. (Pubitemid 39422641)
38. Loving C.L., Brockmeier S.L., Sacco R.E., Differential type I interferon activation and susceptibility of dendritic cell populations to porcine arterivirus, Immunology (2007) 120:217-229.
39. Mahic M., Henjum K., Yaqub S., Bjornbeth B.A., Torgersen K.M., Tasken K., Aandahl E.M., Generation of highly suppressive adaptive CD8(+) CD25(+)FOXP3(+) regulatory T cells by continuous antigen stimulation, Eur. J. Immunol. (2008) 38: 640-646.
40. Mateu E., Diaz I., The challenge of PRRS immunology, Vet. J. (2008) 177:345-351.
41. Meier W.A., Galeota J., Osorio F.A., Husmann R.J., Schnitzlein W.M., Zuckermann F.A., Gradual development of the interferon-gamma response of swine to porcine reproductive and respiratory syndrome virus infection or vaccination, Virology (2003) 309:18-31. (Pubitemid 36511403)
42. Mescher M.F., Curtsinger J.M., Agarwal P., Casey K.A., Gerner M., Hammerbeck C.D., et al., Signals required for programming effector and memory development by CD8+ T cells, Immunol. Rev. (2006) 211:81-92.
43. Moutaftsi M., Mehl A.M., Borysiewicz L.K., Tabi Z., Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells, Blood (2002) 99:2913-2921. (Pubitemid 34525381)
44. Olin M.R., Batista L., Xiao Z., Dee S.A., Murtaugh M.P., Pijoan C.C., Molitor T.W., Gammadelta lymphocyte response to porcine reproductive and respiratory syndrome virus, Viral Immunol. (2005) 18:490-499.
45. Penna A., Pilli M., Zerbini A., Orlandini A., Mezzadri S., Sacchelli L., et al., Dysfunction and functional restoration of HCV-specific CD8 responses in chronic hepatitis C virus infection, Hepatology (2007) 45:588-601. (Pubitemid 46450610)
46. Piriou-Guzylack L., Salmon H., Membrane markers of the immune cells in swine: an update, Vet. Res. (2008) 39:54.
47. Pollara G., Speidel K., Samady L., Rajpopat M., McGrath Y., Ledermann J., et al., Herpes simplex virus infection of dendritic cells: balance among activation, inhibition, and immunity, J. Infect. Dis. (2003) 187:165-178. (Pubitemid 36132630)
48. Sakaguchi S., Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses, Annu. Rev. Immunol. (2004) 22:531-562. (Pubitemid 38680433)
49. Samsom J.N., de Bruin T.G., Voermans J.J., Meulenberg J.J., Pol J.M., Bianchi A.T., Changes of leukocyte phenotype and function in the bronchoalveolar lavage fluid of pigs infected with porcine reproductive and respiratory syndrome virus: a role for CD8(+) cells, J. Gen. Virol. (2000) 81:497-505.
50. Shimizu M., Yamada S., Kawashima K., Ohashi S., Shimizu S., Ogawa T., Changes of lymphocyte subpopulations in pigs infected with porcine reproductive and respiratory syndrome (PRRS) virus, Vet. Immunol. Immunopathol. (1996) 50:19-27. (Pubitemid 26174882)
51. Silva-Campa E., Flores-Mendoza L., Resendiz M., Pinelli-Saavedra A., Mata-Haro V., Mwangi W., Hernandez J., Induction of T helper 3 regulatory cells by dendritic cells infected with porcine reproductive and respiratory syndrome virus, Virology (2009) 387:373-379.
52. Suradhat S., Thanawongnuwech R., Poovorawan Y., Upregulation of IL-10 gene expression in porcine peripheral blood mononuclear cells by porcine reproductive and respiratory syndrome virus, J. Gen. Virol. (2003) 84:453-459.
53. Thanawongnuwech R., Thacker E.L., Interleukin-10, interleukin-12, and interferon-gamma levels in the respiratory tract following Mycoplasma hyopneumoniae and PRRSV infection in pigs, Viral Immunol. (2003) 16:357-367.
54. Unutmaz D., Pileri P., Abrignani S., Antigenindependent activation of naive and memory resting T cells by a cytokine combination, J. Exp. Med. (1994) 180:1159-1164.
55. Vallbracht S., Unsold H., Ehl S., Functional impairment of cytotoxic T cells in the lung airways following respiratory virus infections, Eur. J. Immunol. (2006) 36:1434-1442.
56. Van Reeth K., Labarque G., Nauwynck H., Pensaert M., Differential production of proinflammatory cytokines in the pig lung during different respiratory virus infections: correlations with pathogenicity, Res. Vet. Sci. (1999) 67:47-52. (Pubitemid 129545147)
57. Visser N., Lütticken D.,Vaccination and control of Aujeszky's disease, Dordrecht, Kluwer Academic, 1989, p. 37.
58. Wang X., Eaton M., Mayer M., Li H., He D., Nelson E., Christopher-Hennings J., Porcine reproductive and respiratory syndrome virus productively infects monocyte-derived dendritic cells and compromises their antigen-presenting ability, Arch. Virol. (2007) 152:289-303.
59. Wensvoort G., Terpstra C., Pol J.M., ter Laak E.A., Bloemraad M., de Kluyver E.P., et al., Mystery swine disease in The Netherlands: the isolation of Lelystad virus, Vet. Q. (1991) 13:121-130.
60. Wensvoort G., Lelystad virus and the porcine epidemic abortion and respiratory syndrome, Vet. Res. (1993) 24:117-124.
61. Wherry E.J., Blattman J.N., Murali-Krishna K., van der Most R., Ahmed R., Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment, J. Virol. (2003) 77:4911-4927. (Pubitemid 36402840)
62. Wills R.W., Doster A.R., Galeota J.A., Sur J.H., Osorio F.A., Duration of infection and proportion of pigs persistently infected with porcine reproductive and respiratory syndrome virus, J. Clin. Microbiol. (2003) 41:58-62.
63. Xiao Z., Batista L., Dee S., Halbur P., Murtaugh M.P., 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) 78:5923-5933. (Pubitemid 38661680)
64. Zajac A.J., Blattman J.N., Murali-Krishna K., Sourdive D.J., Suresh M., Altman J.D., Ahmed R., Viral immune evasion due to persistence of activated T cells without effector function, J. Exp. Med. (1998) 188:2205-2213.
65. Zuckermann F.A., Garcia E.A., Luque I.D., Christopher-Hennings J., Doster A., Brito M., Osorio F., Assessment of the efficacy of commercial porcine reproductive and respiratory syndrome virus (PRRSV) vaccines based on measurement of serologic response frequency of gamma-IFN-producing cells and virological parameters of protection upon challenge, Vet. Microbiol. (2007) 123:69-85.