Natural killer cell dysfunction during acute infection with foot-and-mouth disease virus

Clinical and Vaccine Immunology

Volumn 16, Issue 12, 2009, Pages 1738-1749

  Toka, Felix N ^a,b   Nfon, Charles ^a   Dawson, Harry ^c   Golde, William T ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 15 RECEPTOR; MESSENGER RNA; NATURAL KILLER CELL RECEPTOR NKG2A; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; PROTEIN P30; PROTEIN P46; PROTEIN P80; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; SRC HOMOLOGY 2 DOMAIN PROTEIN 1B; SUPPRESSOR OF CYTOKINE SIGNALING 3; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; CYTOTOXICITY; EX VIVO STUDY; FOOT AND MOUTH DISEASE; FOOT AND MOUTH DISEASE VIRUS; GENE EXPRESSION REGULATION; IN VIVO STUDY; INNATE IMMUNITY; NATURAL KILLER CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; TUMOR CELL; VIRUS TITRATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL DEGRANULATION; CYTOKINES; FOOT-AND-MOUTH DISEASE; FOOT-AND-MOUTH DISEASE VIRUS; KILLER CELLS, NATURAL; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; PERFORIN; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; SWINE; TOLL-LIKE RECEPTOR 3;

EID: 73449090445     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00280-09     Document Type: Article

References (58)

1. Alter, G., J. M. Malenfant, and M. Altfeld. 2004. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294:15-22.
2. Arase, H., E. S. Mocarski, A. E. Campbell, A. B. Hill, and L. L. Lanier. 2002. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296:1323-1326.
3. Barnett, P. V., S. J. Cox, N. Aggarwal, H. Gerber, and K. C. McCullough. 2002. Further studies on the early protective responses of pigs following immunisation with high potency foot and mouth disease vaccine. Vaccine 20:3197-3208.
4. Bautista, E. M., G. S. Ferman, and W. T. Golde. 2003. Induction of lymphopenia and inhibition of T cell function during acute infection of swine with foot and mouth disease virus (FMDV). Vet. Immunol. Immunopathol. 92:61-73.
5. Bautista, E. M., G. S. Ferman, D. Gregg, M. C. Brum, M. J. Grubman, and W. T. Golde. 2005. Constitutive expression of alpha interferon by skin dendritic cells confers resistance to infection by foot-and-mouth disease virus. J. Virol. 79:4838-4847.
6. Bittleman, D. B., K. K. Maves, J. A. Bertolatus, S. M. Bonsib, P. Densen, Z. K. Ballas, and J. M. Weiler. 1994. Recurrent infections, pericarditis and renal disease in a patient with total C2 deficiency and decreased NK cell function consistent with acute rheumatic fever and systemic lupus erythematosus. Ann. Rheum. Dis. 53:280-281.
7. Blanco, E., M. Garcia-Briones, A. Sanz-Parra, P. Gomes, E. De Oliveira, M. L. Valero, D. Andreu, V. Ley, and F. Sobrino. 2001. Identification of T-cell epitopes in nonstructural proteins of foot-and-mouth disease virus. J. Virol. 75:3164-3174.
8. Borysiewicz, L. K., B. Rodgers, S. Morris, S. Graham, and J. G. Sissons. 1985. Lysis of human cytomegalovirus infected fibroblasts by natural killer cells: demonstration of an interferon-independent component requiring expression of early viral proteins and characterization of effector cells. J. Immunol. 134:2695-2701.
9. Boysen, P., and A. K. Storset. 2009. Bovine natural killer cells. Vet. Immunol. Immunopathol. 130:163-177.
10. Carr, D. J. J., T. Wuest, and J. Ash. 2008. An increase in herpes simplex virus type 1 in the anterior segment of the eye is linked to a deficiency in NK cell infiltration in mice deficient in CXCR3. J. Interferon Cytokine Res. 28:245-251.
11. Carr, W. H., A.-M. Little, E. Mocarski, and P. Parham. 2002. NK cellmediated lysis of autologous HCMV-infected skin fibroblasts is highly variable among NK cell clones and polyclonal NK cell lines. Clin. Immunol. 105:126-140.
12. Cerwenka, A., and L. L. Lanier. 2001. Ligands for natural killer cell receptors: redundancy or specificity. Immunol. Rev. 181:158-169.
13. Chinsangaram, J., M. Koster, and M. J. Grubman. 2001. Inhibition of L-deleted foot-and-mouth disease virus replication by alpha/beta interferon involves double-stranded RNA-dependent protein kinase. J. Virol. 75:5498-5503.
14. Cohen, G. B., R. T. Gandhi, D. M. Davis, O. Mandelboim, B. K. Chen, J. L. Strominger, and D. Baltimore. 1999. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10:661-671.
15. Cottam, E. M., D. T. Haydon, D. J. Paton, J. Gloster, J. W. Wilesmith, N. P. Ferris, G. H. Hutchings, and D. P. King. 2006. Molecular epidemiology of the foot-and-mouth disease virus outbreak in the United Kingdom in 2001. J. Virol. 80:11274-11282.
16. Delano, M. L., and D. G. Brownstein. 1995. Innate resistance to lethal mousepox is genetically linked to the NK gene complex on chromosome 6 and correlates with early restriction of virus replication by cells with an NK phenotype. J. Virol. 69:5875-5877.
17. Denyer, M. S., T. E. Wileman, C. M. Stirling, B. Zuber, and H. H. Takamatsu. 2006. Perforin expression can define CD8 positive lymphocyte subsets in pigs allowing phenotypic and functional analysis of natural killer, cytotoxic T, natural killer T and MHC un-restricted cytotoxic T-cells. Vet. Immunol. Immunopathol. 110:279-292.
18. Derbyshire, J. B., and C. E. Lesnick. 1990. Hyporeactivity to interferon induction in newborn piglets. J. Interferon Res. 10:47-53.
19. Devaney, M. A., V. N. Vakharia, R. E. Lloyd, E. Ehrenfeld, and M. J. Grubman. 1988. Leader protein of foot-and-mouth disease virus is required for cleavage of the p220 component of the cap-binding protein complex. J. Virol. 62:4407-4409.
20. Gerner, W., T. Käser, and A. Saalmüller. 2009. Porcine T lymphocytes and NK cells-an update. Dev. Comp. Immunol. 33:310-320.
21. Gerosa, F., B. Baldani-Guerra, C. Nisii, V. Marchesini, G. Carra, and G. Trinchieri. 2002. Reciprocal activating interaction between natural killer cells and dendritic cells. J. Exp. Med. 195:327-333.
22. Golde, W. T., J. M. Pacheco, H. Duque, T. Doel, B. Penfold, G. S. Ferman, D. R. Gregg, and L. L. Rodriguez. 2005. Vaccination against foot-and-mouth disease virus confers complete clinical protection in 7 days and partial protection in 4 days: use in emergency outbreak response. Vaccine 23:5775-5782.
23. Gorski, K. S., E. L. Waller, J. Bjornton-Severson, J. A. Hanten, C. L. Riter, W. C. Kieper, K. B. Gorden, J. S. Miller, J. P. Vasilakos, M. A. Tomai, and S. S. Alkan. 2006. Distinct indirect pathways govern human NK-cell activation by TLR-7 and TLR-8 agonists. Int. Immunol. 18:1115-1126.
24. Gray, J. D., C. G. Brooks, and R. W. Baldwin. 1981. Detection of either rapidly cytolytic macrophages or NK cells in "activated" peritoneal exudates depends on the method of analysis and the target cell type. Immunology 42:561-568.
25. Grubman, M. J., and B. Baxt. 2004. Foot-and-mouth disease. Clin. Microbiol. Rev. 17:465-493.
26. + T-cell response is induced in cattle by foot-andmouth disease virus (FMDV) infection and also following vaccination with inactivated FMDV. J. Gen. Virol. 89:667-675.
27. Harada, H., T. Murakami, S. S. Tea, A. Takeuchi, T. Koga, S. Okada, M. A. Suico, T. Shuto, and H. Kai. 2007. Heat shock suppresses human NK cell cytotoxicity via regulation of perforin. Int. J. Hyperthermia 23:657-665.
28. He, X. S., M. Draghi, K. Mahmood, T. H. Holmes, G. W. Kemble, C. L. Dekker, A. M. Arvin, P. Parham, and H. B. Greenberg. 2004. T cell-dependent production of IFN-gamma by NK cells in response to influenza A virus. J. Clin. Investig. 114:1812-1819.
29. Koga, T., H. Harada, T. S. Shi, S. Okada, M. A. Suico, T. Shuto, and H. Kai. 2005. Hyperthermia suppresses the cytotoxicity of NK cells via down-regulation of perforin/granzyme B expression. Biochem. Biophys. Res. Commun. 337:1319-1323.
30. Kottilil, S., T. W. Chun, S. Moir, S. Liu, M. McLaughlin, C. W. Hallahan, F. Maldarelli, L. Corey, and A. S. Fauci. 2003. Innate immunity in human immunodeficiency virus infection: effect of viremia on natural killer cell function. J. Infect. Dis. 187:1038-1045.
31. Kottilil, S., K. Shin, J. O. Jackson, K. N. Reitano, M. A. O'Shea, J. Yang, C. W. Hallahan, R. Lempicki, J. Arthos, and A. S. Fauci. 2006. Innate immune dysfunction in HIV infection: effect of HIV envelope-NK cell interactions. J. Immunol. 176:1107-1114.
32. + T cells and NK cells in vivo. Nat. Immunol. 3:529-535.
33. Lang, R., A.-L. Pauleau, E. Parganas, Y. Takahashi, J. Mages, J. N. Ihle, R. Rutschman, and P. J. Murray. 2003. SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. 4:546-550.
34. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23:225-274.
35. Long, B. R., J. Michaelsson, C. P. Loo, W. M. Ballan, B.-A. N. Vu, F. M. Hecht, L. L. Lanier, J. M. Chapman, and D. F. Nixon. 2008. Elevated frequency of gamma interferon-producing NK cells in healthy adults vaccinated against influenza virus. Clin. Vaccine Immunol. 15:120-130.
36. Mateu, M. G. 1995. Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Res. 38:1-24.
37. Mavilio, D., J. Benjamin, M. Daucher, G. Lombardo, S. Kottilil, M. A. Planta, E. Marcenaro, C. Bottino, L. Moretta, A. Moretta, and A. S. Fauci. 2003. Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc. Natl. Acad. Sci. USA 100:15011-15016.
38. Mohan, M., M. Gajendragad, S. Gopalakrishna, and N. Singh. 2008. Com-parative study of experimental foot-and-mouth disease in cattle (Bos indicus) and buffaloes (Bubalis bubalus). Vet. Res. Comm. 32:481-489.
39. Nfon, C. K., G. S. Ferman, F. N. Toka, D. A. Gregg, and W. T. Golde. 2008. Interferon-alpha production by swine dendritic cells is inhibited during acute infection with foot-and-mouth disease virus. Viral Immunol. 21:68-77.
40. Nfon, C. K., F. N. Toka, M. Kenney, J. M. Pacheco, and W. T. Golde. Loss of plasmacytoid dendritic cell function coincides with lymphopenia and viremia during foot-and-mouth disease virus (FMDV) infection. Viral Immunol., in press.
41. Pacheco, J. M., T. M. Henry, V. K. O'Donnell, J. B. Gregory, and P. W. Mason. 2003. Role of nonstructural proteins 3A and 3B in host range and pathogenicity of foot-and-mouth disease virus. J. Virol. 77:13017-13027.
42. Parker, A. K., S. Parker, W. M. Yokoyama, J. A. Corbett, and R. M. L. Buller. 2007. Induction of natural killer cell responses by ectromelia virus controls infection. J. Virol. 81:4070-4079.
43. Pintaric, M., W. Gerner, and A. Saalmüller. 2008. Synergistic effects of IL-2, IL-12 and IL-18 on cytolytic activity, perforin expression and IFN-gamma production of porcine natural killer cells. Vet. Immunol. Immunopathol. 121:68-82.
44. Pothlichet, J., M. Chignard, and M. Si-Tahar. 2008. Cutting edge: innate immune response triggered by influenza a virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/IFNAR1-dependent pathway. J. Immunol. 180:2034-2038.
45. Rager-Zisman, B., P. C. Quan, M. Rosner, J. R. Moller, and B. R. Bloom. 1987. Role of NK cells in protection of mice against herpes simplex virus-1 infection. J. Immunol. 138:884-888.
46. Ravet, S., D. Scott-Algara, E. Bonnet, H. K. Tran, T. Tran, N. Nguyen, L. X. Truong, I. Theodorou, F. Barre-Sinoussi, G. Pancino, and P. Paul. 2007. Distinctive NK-cell receptor repertoires sustain high-level constitutive NKcell activation in HIV-exposed uninfected individuals. Blood 109:4296-4305.
47. Reed, D. S., L. E. Hensley, J. B. Geisbert, P. B. Jahrling, and T. W. Geisbertl. 2004. Depletion of peripheral blood T lymphocytes and NK cells during the course of Ebola hemorrhagic fever in cynomolgus macaques. Viral Immunol. 17:390-400.
48. Reschner, A., P. Hubert, P. Delvenne, J. Boniver, and N. Jacobs. 2008. Innate lymphocyte and dendritic cell cross-talk: a key factor in the regulation of the immune response. Clin. Exp. Immunol. 152:219-226.
49. Sanz-Parra, A., F. Sobrino, and V. Ley. 1998. Infection with foot-and-mouth disease virus results in a rapid reduction of MHC class I surface expression. J. Gen. Virol. 79:433-436.
50. Schmidt, K. N., B. Leung, M. Kwong, K. A. Zarember, S. Satyal, T. A. Navas, F. Wang, and P. J. Godowski. 2004. APC-independent activation of NK cells by the Toll-like receptor 3 agonist double-stranded RNA. J. Immunol. 172:138-143.
51. Scott-Algara, D., F. Vuillier, A. Cayota, and G. Dighiero. 1992. Natural killer (NK) cell activity during HIV infection: a decrease in NK activity is observed at the clonal level and is not restored after in vitro long-term culture of NK cells. Clin. Exp. Immunol. 90:181-187.
52. Sivori, S., M. Falco, M. D. Chiesa, S. Carlomagno, M. Vitale, L. Moretta, and A. Moretta. 2004. CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc. Natl. Acad. Sci. USA 101:10116-10121.
53. Thapa, M., R. S. Welner, R. Pelayo, and D. J. J. Carr. 2008. cxcl9 and cxcl10 expression are critical for control of genital herpes simplex virus type 2 infection through mobilization of HSV-specific CTL and NK cells to the nervous system. J. Immunol. 180:1098-1106.
54. Toka, F. N., C. K. Nfon, H. Dawson, and W. T. Golde. 2009. Accessory-cellmediated activation of porcine NK cells by Toll-like receptor 7 (TLR7) and TLR8 agonists. Clin. Vaccine Immunol. 16:866-878.
55. Toka, F. N., C. K. Nfon, H. Dawson, D. Mark Estes, and W. T. Golde. 2009. Activation of Porcine Natural Killer (NK) Cells and Lysis of Foot-and-Mouth Disease Virus (FMDV) Infected Cells. J. Interferon Cytokine Res. 29:179-192.
56. Tomasec, P., V. M. Braud, C. Rickards, M. B. Powell, B. P. McSharry, S. Gadola, V. Cerundolo, L. K. Borysiewicz, A. J. McMichael, and G. W. Wilkinson. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031-1033.
57. Tomescu, C., J. Chehimi, V. C. Maino, and L. J. Montaner. 2007. NK cell lysis of HIV-1-infected autologous CD4 primary T cells: requirement for IFN-mediated NK activation by plasmacytoid dendritic Cells. J. Immunol. 179:2097-2104.
58. Zitvogel, L., M. Terme, C. Borg, and G. Trinchieri. 2006. Dendritic cell-NK cell cross-talk: regulation and physiopathology. Curr. Top. Microbiol. Immunol. 298:157-174.