Ligation of Fc gamma receptor IIB enhances levels of antiviral cytokine in response to PRRSV infection in vitro

Veterinary Microbiology

Volumn 160, Issue 3-4, 2012, Pages 473-480

  Zhang, Yina ^a   Zhou, Yonghui ^a   Yang, Qingyuan ^a   Mu, Chunlong ^a   Duan, Erzhen ^a   Chen, Jing ^a   Yang, Mingfan ^a   Xia, Pingan ^a   Cui, Baoan ^a  

^a HENAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Cytokine; Fc receptor; Fc RIIB; Pig; PRRSV

Indexed keywords

ALPHA INTERFERON; FC RECEPTOR IIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; MESSENGER RNA; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR ALPHA;

ARTERIVIRUS; ARTERIVIRUS INFECTION; ARTICLE; CELL ACTIVATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; HOST SUSCEPTIBILITY; IMMUNE RESPONSE; IN VITRO STUDY; NONHUMAN; PHAGOCYTOSIS; SIGNAL TRANSDUCTION; UPREGULATION; VIRAL CLEARANCE; VIRUS REPLICATION;

ANIMALS; CELLS, CULTURED; CYTOKINES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MACROPHAGES; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; RECEPTORS, IGG; RNA, MESSENGER; SWINE; TIME FACTORS;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE; SUS;

EID: 84869095601     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2012.06.021     Document Type: Article

References (64)

1. 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(7):485-490.
2. 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(22):10834-10837.
3. Berlato C., Cassatella M.A., Kinjyo I., Gatto L., Yoshimura A., Bazzoni F. Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J. Immunol. 2002, 168:6404-6411.
4. Beura L.K., Sarkar S.N., Kwon B., Subramaniam S., Jones C., Pattnaik A.K., Osorio F.A. Porcine reproductive and respiratory syndrome virus nonstructural protein 1beta modulates host innate immune response by antagonizing IRF3 activation. J. Virol. 2009, 84(3):1574-1584.
5. Brooks D.G., Trifilo M.J., Edelmann K.H., Teyton L., McGavern D.B., Oldstone M.B. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 2006, 12:1301-1309.
6. 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, 440:461-467.
7. Cancel-Tirado S.M., Yoon K.J. Antibody-dependent enhancement of virus infection and disease. Viral Immunol. 2003, 16:69-86.
8. Cancel-Tirado S.M., Evans R.B., Yoon K.J. 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, 102:249-262.
9. Chan K.R., Zhang S.L.X., Tan H.C., Chan Y.K., Chow A., Lim A.P.C., Vasudevan S.G., Hanson B.J., Ooi E.E. Ligation of Fc gamma receptor IIB inhibits antibody-dependent enhancement of dengue virus infection. PNAS 2011, 108:12479-12484.
10. 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.
11. Charerntantanakul W., Platt R., Roth J.A. Effects of porcine reproductive and respiratory syndrome virus-infected antigen-presenting cells on T cell activation and antiviral cytokine production. Viral Immunol. 2006, 19:646-661.
12. 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.
13. Cirino N.M., Panuska J.R., Villani A., Taraf H., Rebert N.A., Merolla R., Tsivitse P., Gilbert I.A. Restricted replication of respiratory syncytial virus in human alveolar macrophages. J. Gen. Virol. 1993, 74:1527-1537.
14. Clatworthy M.R., Smith K.G. FcgammaRIIB balances efficient pathogen clearance and the cytokine-mediated consequences of sepsis. J. Exp. Med. 2004, 199:717-723.
15. Da Silva D.M., Fausch S.C., Verbeek J.S., Kast W.M. Uptake of human papillomavirus virus-like particles by dendritic cells is mediated by Fc gamma receptors and contributes to acquisition of T cell immunity. J. Immunol. 2007, 178:7587-7597.
16. Davis R.S., Dennis G., Odom M.R., Gibson A.W., Kimberly R.P., Burrows P.D., Cooper M.D. Fc receptor homologs: newest members of a remarkably diverse Fc receptor gene family. Immunol. Rev. 2002, 190:123-136.
17. Duan X., Nauwynck H.J., Pensaert M.B. Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to PRRSV. Arch. Virol. 1997, 142:2483-2497.
18. Duan X., Nauwynck H.J., Favoreel H.W., Pensaert M.B. Porcine reproductive and respiratory syndrome virus infection of alveolar macrophages can be blocked by monoclonal antibodies against cell surface antigens. Adv. Exp. Med. Biol. 1998, 440:81-88.
19. 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.
20. Gerber J.S., Mosser D.M. Reversing lipopolysaccharide toxicity by ligating the macrophage Fcg receptors. J. Immunol. 2001, 166:6861-6868.
21. Gimeno M., Darwich L., Diaz I., de la Torre E., Pujols J., Martín M., Inumaru S., Cano E., Domingo M., Montoya M., Mateu E. Cytokine profiles and phenotype regulation of antigen presenting cells by genotype-I porcine reproductive and respiratory syndrome virus isolates. Vet. Res. 2011, 42:1-9.
22. Halloran P.J., Sweeney S.E., Strohmeier C.M., Kim Y.B. Molecular cloning and identification of the porcine cytolytic trigger molecule G7 as a Fc gamma RIII alpha (CD16) homologue. J. Immunol. 1994, 158:400-413.
23. Halstead S.B., Mahalingam S., Marovich M.A., Ubol S., Mosser D.M. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect. Dis. 2010, 10:712-722.
24. Heise M.T., Virgin H.W.T. The T-cell-independent role of gamma interferon and tumor necrosis factor alpha in macrophage activation during murine cytomegalovirus and herpes simplex virus infections. J. Virol. 1995, 69:904-909.
25. Ito B.S., Ansari P., Sakatsume M., Dickensheets H., Vazquez N., Donnelly R.P., Larner A.C., Finbloom D.S. Interleukin-10 inhibits expression of both interferon-a- and interferon-g-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 1999, 93:1456-1463.
26. Joshi T., Ganesan L.P., Cao X., Tridandapani S. Molecular analysis of expression and function of hFc[gamma]RIIB1 and b2 isoforms in myeloid cells. Mol. Immunol. 2006, 43:839-850.
27. Johnsen C.K., Botner A., Kamstrup S., Lind P., Nielsen J. 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 Immunol. 2002, 15:549-556.
28. Kimman T.G., Cornelissen L.A., Moormann R.J., Rebel J.M., Stockhofe-Zurwieden N. Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine 2009, 8(27):3704-3718.
29. Labarque G., Van Gucht S., Nauwynck H., Van Reeth K., Pensaert M. Apoptosis in the lungs of pigs infected with porcine reproductive and respiratory syndrome virus and associations with the production of apoptogenic cytokines. Vet. Res. 2003, 34:249-260.
30. Lee S.M., Schommer S.K., Kleiboeker S.B. Porcine reproductive and respiratory syndrome virus field isolates differ in in vitro interferon phenotypes. Vet. Immunol. Immunopathol. 2004, 102:217-231.
31. Lee S.M., Kleiboeker S.B. Porcine arterivirus activates the NF-κB pathway through IκB degradation. Virology 2005, 342:47-59.
32. Liu Y.S., Xia P.A., Zhao L., Fan X., Zhang F.H., Xu H.Y., Liu X.P., Zhang Z.Y., Cui B.A. Prokaryotic expression of recombinant swFcγRIIB protein and preparation of polyclonal antibody against swFcγRIIB. Chin. Vet. Sci. 2010, 40:70-74.
33. Lopez-Fuertes L., Campos E., Domenech N., Ezquerra A., Castro J.M., Dominguez J., Alonso F. Porcine reproductive and respiratory syndrome (PRRS) virus down-modulates TNF-alpha production in infected macrophages. Virus Res. 2000, 69:41-46.
34. Mahalingam S., Lidbury B.A. Suppression of lipopolysaccharide-induced antiviral transcription factor (STAT-1 and NF-kB) complexes by antibody-dependent enhancement of macrophage infection by Ross River virus. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13819-13824.
35. Mantzioris B., Berger M., Sewell W., Zola H. Expression of the Fc receptor for IgG (FcRII/CDw32) by human circulating T and B lymphocytes. J. Immunol. 1993, 150:5175-5184.
36. Mateu E., Diaz I. The challenge of PRRS immunology. Vet. J. 2008, 177:345-351.
37. McKenzie S.E., Schreiber A.D. Fc receptors in phagocytes. Curr. Opin. Hematol. 1998, 5:16-21.
38. Mechetina L.V., Najakshin A.M., Alabyev B.Y., Chikaev N.A., Taranin A.V. Identification of CD16-2, a novel mouse receptor homologous to CD16/Fc gamma RIII. Immunogenetics 2002, 54:463-468.
39. 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(1):18-31.
40. Muta T., Kurosaki T., Misulovin Z., Sanchez M., Nussenzweig M.C., Ravetch J.V. A 13-amino-acid motif in the cytoplasmic domain of Fc gammaRIIB. Nature 1994, 368:70-73.
41. Nimmerjahn F., Bruhns P., Horiuchi K., Ravetch J.V. FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity 2005, 23:41-51.
42. Nimmerjahn F., Ravetch J.V. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 2005, 310:1510-1512.
43. Park J.Y., Kim H.S., Seo S.H. Characterization of interaction between porcine reproductive and respiratory syndrome virus and porcine dendritic cells. J. Microbiol. Biotechnol. 2008, 18:1709-1716.
44. Qiao S.L., Zhang G.P., Xia C., Zhang H., Zhang Y.Y., Xi J., Song H.T., Li X.W. Cloning and characterization of porcine Fc gamma receptor II (FcγRII). Vet. Immunol. Immunopathol. 2006, 114:178-184.
45. Ravetch J.V., Bolland S. IgG Fc receptors. Annu. Rev. Immunol. 2001, 19:275-290.
46. Ravetch J.V., Kinet J.P. Fc receptors. Annu. Rev. Immunol. 1991, 9:457-492.
47. Ravetch J.V., Lanier L.L. Immune inhibitory receptors. Science 2000, 290:84-89.
48. Redpath S., Ghazal P., Gascoigne N.R. Hijacking and exploitation of IL-10 by intracellular pathogens. Trends Microbiol. 2001, 9(2):86-92.
49. Song M.M., Shuai K. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferonmediated antiviral and antiproliferative activities. J. Biol. Chem. 1998, 273:35056-35062.
50. Subramaniam S., Kwon B.J., Beura L.K., Kuszynski C., Pattnaik A.K., Osorio F.A. Porcine reproductive and respiratory syndrome virus non-structural protein 1 suppresses tumor necrosis factor-alpha promoter activation by inhibiting NF-κ B and Sp1. Virology 2010, 402:270-279.
51. Subramaniama S., Surb J.H., Kwona B., Pattnaika A.K., Osorioa F.A. A virulent strain of porcine reproductive and respiratory syndrome virus does not up-regulate interleukin-10 levels in vitro or in vivo. Virus Res. 2011, 155:415-422.
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. Sutterwala F.S., Noel G.J., Salgame P., Mosser D.M. Reversal of proinflammatory responses by ligating the macrophage Fcγ receptor type I. J. Exp. Med. 1998, 188:217.
54. Takai T. Roles of Fc receptors in autoimmunity. Nat. Rev. Immunol. 2002, 2:580-592.
55. Thanawongnuwech R., Thacker B., Halbur P., Thacker E.L. Increased production of proinflammatory cytokines following infection with porcine reproductive and respiratory syndrome virus and Mycoplasma hyopneumoniae. Clin. Diagn. Lab. Immunol. 2004, 11:901-908.
56. Tzeng S.J., Bolland S., Inabe K., Kurosaki T., Pierce S.K. The B cell inhibitory Fc receptor triggers apoptosis by a novel c-Abl-family kinase dependent pathway. J. Biol. Chem. 2005, 280:35247-35254.
57. Van de Winkel J.G., Capel P.J. Human IgG Fc receptor heterogeneity: molecular aspects and clinical implications. Immunology 1993, 14:215-221.
58. Van Gucht S., van Reeth K., Pensaert M. Interaction between porcine reproductive-respiratory syndrome virus and bacterial endotoxin in the lungs of pigs: potentiation of cytokine production and respiratory disease. J. Clin. Microbiol. 2003, 41:960-966.
59. Voicu I.L., Silim A., Morin M., Elazhary M.A. Interaction of porcine reproductive and respiratory syndrome virus with swine monocytes. Vet. Rec. 1994, 134:422-423.
60. Wootton S.K., Yoo D. Homo-oligomerization of the porcine reproductive and respiratory syndrome virus nucleocapsid protein and the role of disulfide linkages. J. Virol. 2003, 77:4546-4557.
61. Xia P.A., Liu Y.S., Liu X.P., Zhang Z.Y., Xu H.Y., Duan E.Z., Lu X.Y., Cui B.A. Molecular cloning and characterization of a porcine Fc gamma RIIB sub-isoform (FcγRIIB1). Vet. Immun. Pathol. 2011, 141:144-150.
62. Xia P.A., Liu X.P., Zhang Y.N., Duan E.Z., Zhang Z.Y., Chen J., Mu C.L., Cui B.A. Porcine Fc gamma RIIB sub-isoforms are generated by alternative splicing. Vet. Immun. Pathol. 2012, 145:386-394.
63. Yoon K.J., Wu L.L., Zimmerman J.J., Hill H.T., Platt K.B. Antibody-dependent enhancement (ADE) of porcine reproductive and respiratory syndrome virus (PRRSV) infection in pigs. Viral Immunol. 1996, 9:51-63.
64. Yoon K.J., Wu L.L., Zimmerman J.J., Platt K.B. Field isolates of porcine reproductive and respiratory syndrome virus (PRRSV) vary in their susceptibility to antibody dependent enhancement (ADE) of infection. Vet. Microbiol. 1997, 55:277-287.