IFN-γ production by CD27+ NK cells exacerbates Listeria monocytogenes infection in mice by inhibiting granulocyte mobilization

European Journal of Immunology

Volumn 43, Issue 10, 2013, Pages 2626-2637

  Viegas, Nuno ^a   Andzinski, Lisa ^a   Wu, Ching Fang ^a   Komoll, Ronja Melinda ^a   Gekara, Nelson ^a   Dittmar, Kurt E ^a   Weiss, Siegfried ^a   Jablonska, Jadwiga ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Granulocytes; IFN ; Infection; Listeria monocytogenes; NK cells

Indexed keywords

CD27 ANTIGEN; CHEMOKINE RECEPTOR CXCR2; GAMMA INTERFERON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GRANULOCYTE; HOST RESISTANCE; INNATE IMMUNITY; INTERFERON PRODUCTION; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE ACTIVATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; SIGNAL TRANSDUCTION;

GRANULOCYTES; IFN-Γ; INFECTION; LISTERIA MONOCYTOGENES; NK CELLS;

ANIMALS; ANTIBODIES, BLOCKING; ANTIGENS, CD27; CELL MOVEMENT; CELLS, CULTURED; DOWN-REGULATION; FEMALE; GRANULOCYTES; IMMUNITY, INNATE; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, INBRED C57BL; RECEPTORS, INTERLEUKIN-8B; SIGNAL TRANSDUCTION;

EID: 84885764837     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242937     Document Type: Article

References (61)

1. Kiessling, R., Klein, E., Pross, H. and Wigzell, H., "Natural" killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur. J. Immunol. 1975. 5: 117-121.
2. Welsh, R. M., Jr., Mouse natural killer cells: induction specificity, and function. J. Immunol. 1978. 121: 1631-1635.
3. Caligiuri, M. A., Human natural killer cells. Blood 2008. 112: 461-469.
4. Lodoen, M. B. and Lanier, L. L., Natural killer cells as an initial defense against pathogens. Curr. Opin. Immunol. 2006. 18: 391-398.
5. Koyasu, S. and Moro, K., Role of innate lymphocytes in infection and inflammation. Front Immunol. 2012. 3: 101.
6. Agematsu, K., Kobata, T., Sugita, K., Freeman, G. J., Beckmann, M. P., Schlossman, S. F. and Morimoto, C., Role of CD27 in T cell immune response. Analysis by recombinant soluble CD27. J. Immunol. 1994. 153: 1421-1429.
7. Aggarwal, B. B., Signalling pathways of the TNF superfamily: a double-edged sword. Nat. Rev. Immunol. 2003. 3: 745-756.
8. Hayakawa, Y. and Smyth, M. J., CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 2006. 176: 1517-1524.
9. Hayakawa, Y., Huntington, N. D., Nutt, S. L. and Smyth, M. J., Functional subsets of mouse natural killer cells. Immunol. Rev. 2006. 214: 47-55.
10. Titanji, K., Sammicheli, S., De, M. A., Mantegani, P., Fortis, C., Berg, L., Karre, K. et al., Altered distribution of natural killer cell subsets identified by CD56, CD27 and CD70 in primary and chronic human immunodeficiency virus-1 infection. Immunology 2008. 123: 164-170.
11. Bertram, E. M., Dawicki, W. and Watts, T. H., Role of T cell costimulation in anti-viral immunity. Semin. Immunol. 2004. 16: 185-196.
12. Lanier, L. L., Evolutionary struggles between NK cells and viruses. Nat. Rev. Immunol. 2008. 8: 259-268.
13. Stetson, D. B., Mohrs, M., Reinhardt, R. L., Baron, J. L., Wang, Z. E., Gapin, L., Kronenberg, M. and Locksley, R. M., Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J. Exp. Med. 2003. 198: 1069-1076.
14. Biron, C. A., Nguyen, K. B., Pien, G. C., Cousens, L. P. and Salazar-Mather, T. P., Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 1999. 17: 189-220.
15. Martin-Fontecha, A., Thomsen, L. L., Brett, S., Gerard, C., Lipp, M., Lanzavecchia, A. and Sallusto, F., Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 2004. 5: 1260-1265.
16. Schoenborn, J. R. and Wilson, C. B., Regulation of interferon-gamma during innate and adaptive immune responses. Adv. Immunol. 2007. 96: 41-101.
17. Dunn, P. L. and North, R. J., Early gamma interferon production by natural killer cells is important in defense against murine listeriosis. Infect. Immun. 1991. 59: 2892-2900.
18. Ladel, C. H., Blum, C. and Kaufmann, S. H., Control of natural killer cell-mediated innate resistance against the intracellular pathogen Listeria monocytogenes by gamma/delta T lymphocytes. Infect. Immun. 1996. 64: 1744-1749.
19. Berg, R. E., Crossley, E., Murray, S. and Forman, J., Relative contributions of NK and CD8 T cells to IFN-gamma mediated innate immune protection against Listeria monocytogenes. J. Immunol. 2005. 175: 1751-1757.
20. Emoto, M., Yoshizawa, I., Emoto, Y., Miamoto, M., Hurwitz, R. and Kaufmann, S. H., Rapid development of a gamma interferon-secreting glycolipid/CD1d-specific Valpha14 +NK1.1-T-cell subset after bacterial infection. Infect. Immun. 2006. 74: 5903-5913.
21. Teixeira, H. C. and Kaufmann, S. H., Role of NK1.1+ cells in experimental listeriosis. NK1+ cells are early IFN-gamma producers but impair resistance to Listeria monocytogenes infection. J. Immunol. 1994. 152: 1873-1882.
22. Takada, H., Matsuzaki, G., Hiromatsu, K. and Nomoto, K., Analysis of the role of natural killer cells in Listeria monocytogenes infection: relation between natural killer cells and T-cell receptor gamma delta T cells in the host defence mechanism at the early stage of infection. Immunology 1994. 82: 106-112.
23. Badgwell, B., Parihar, R., Magro, C., Dierksheide, J., Russo, T. and Carson, W. E., III, Natural killer cells contribute to the lethality of a murine model of Escherichia coli infection. Surgery 2002. 132: 205-212.
24. Kerr, A. R., Kirkham, L. A., Kadioglu, A., Andrew, P. W., Garside, P., Thompson, H. and Mitchell, T. J., Identification of a detrimental role for NK cells in pneumococcal pneumonia and sepsis in immunocompromised hosts. Microbes Infect. 2005. 7: 845-852.
25. Kronenberg, M., Toward an understanding of NKT cell biology: progress and paradoxes. Annu. Rev. Immunol. 2005. 23: 877-900.
26. Godfrey, D. I. and Kronenberg, M., Going both ways: immune regulation via CD1d-dependent NKT cells. J. Clin. Invest. 2004. 114: 1379-1388.
27. Godfrey, D. I., MacDonald, H. R., Kronenberg, M., Smyth, M. J. and Van, K. L., NKT cells: what's in a name? Nat. Rev. Immunol. 2004. 4: 231-237.
28. Mebius, R. E. and Kraal, G., Structure and function of the spleen. Nat. Rev. Immunol. 2005. 5: 606-616.
29. Aoshi, T., Carrero, J. A., Konjufca, V., Koide, Y., Unanue, E. R. and Miller, M. J., The cellular niche of Listeria monocytogenes infection changes rapidly in the spleen. Eur. J. Immunol. 2009. 39: 417-425.
30. Jablonska, J., Dittmar, K. E., Kleinke, T., Buer, J. and Weiss, S., Essential role of CCL2 in clustering of splenic ERTR-9+ macrophages during infection of BALB/c mice by Listeria monocytogenes. Infect. Immun. 2007. 75: 462-470.
31. Gekara, N. O. and Weiss, S., Mast cells initiate early anti-Listeria host defences. Cell Microbiol. 2008. 10: 225-236.
32. Pamer, E. G., Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 2004. 4: 812-823.
33. Conlan, J. W. and North, R. J., Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J. Exp. Med. 1994. 179: 259-268.
34. Smyth, M. J., Cretney, E., Takeda, K., Wiltrout, R. H., Sedger, L. M., Kayagaki, N., Yagita, H.et al., Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) contributes to interferon gamma-dependent natural killer cell protection from tumor metastasis. J. Exp. Med. 2001. 193: 661-670.
35. Yang, X., Merchant, M. S., Romero, M. E., Tsokos, M., Wexler, L. H., Kontny, U., Mackall, C. L.et al., Induction of caspase 8 by interferon gamma renders some neuroblastoma (NB) cells sensitive to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) but reveals that a lack of membrane TR1/TR2 also contributes to TRAIL resistance in NB. Cancer Res. 2003. 63: 1122-1129.
36. Eash, K. J., Greenbaum, A. M., Gopalan, P. K. and Link, D. C., CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J. Clin. Invest. 2010. 120: 2423-2431.
37. Sogawa, Y., Ohyama, T., Maeda, H. and Hirahara, K., Inhibition of neutrophil migration in mice by mouse formyl peptide receptors 1 and 2 dual agonist: indication of cross-desensitization in vivo. Immunology 2011. 132: 441-450.
38. Mei, J., Liu, Y., Dai, N., Hoffmann, C., Hudock, K. M., Zhang, P., Guttentag, S. H. et al., Cxcr2 and Cxcl5 regulate the IL-17/G-CSF axis and neutrophil homeostasis in mice. J. Clin. Invest. 2012. 122: 974-986.
39. Lanier, L. L., Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 2008. 9: 495-502.
40. Takeda, K., Oshima, H., Hayakawa, Y., Akiba, H., Atsuta, M., Kobata, T., Kobayashi, K.et al., CD27-mediated activation of murine NK cells. J. Immunol. 2000. 164: 1741-1745.
41. Bach, E. A., Aguet, M. and Schreiber, R. D., The IFN gamma receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 1997. 15: 563-591.
42. Rottenberg, M. E., Gigliotti-Rothfuchs, A. and Wigzell, H., The role of IFN-gamma in the outcome of chlamydial infection. Curr. Opin. Immunol. 2002. 14: 444-451.
43. Bancroft, G. J., Schreiber, R. D., Bosma, G. C., Bosma, M. J. and Unanue, E. R., A T cell-independent mechanism of macrophage activation by interferon-gamma. J. Immunol. 1987. 139: 1104-1107.
44. Sun, K. and Metzger, D. W., Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat. Med. 2008. 14: 558-564.
45. Ellis, T. N. and Beaman, B. L., Interferon-gamma activation of polymorphonuclear neutrophil function. Immunology 2004. 112: 2-12.
46. Kang, S. J., Liang, H. E., Reizis, B. and Locksley, R. M., Regulation of hierarchical clustering and activation of innate immune cells by dendritic cells. Immunity 2008. 29: 819-833.
47. Alves-Filho, J. C., de, F. A., Spiller, F., Souto, F. O. and Cunha, F. Q., The role of neutrophils in severe sepsis. Shock 2008. 30 (Suppl 1): 3-9.
48. Alves-Filho, J. C., Freitas, A., Souto, F. O., Spiller, F., Paula-Neto, H., Silva, J. S., Gazzinelli, R. T.et al., Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc. Natl. Acad. Sci. USA 2009. 106: 4018-4023.
49. Czuprynski, C. J., Brown, J. F., Steinberg, H. and Carroll, D., Mice lacking the murine interleukin-8 receptor homologue demonstrate paradoxical responses to acute and chronic experimental infection with Listeria monocytogenes. Microb. Pathog. 1998. 24: 17-23.
50. Cacalano, G., Lee, J., Kikly, K., Ryan, A. M., Pitts-Meek, S., Hultgren, B., Wood, W. I.et al., Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 1994. 265: 682-684.
51. Shuster, D. E., Kehrli, M. E., Jr. and Ackermann, M. R., Neutrophilia in mice that lack the murine IL-8 receptor homolog. Science 1995. 269: 1590-1591.
52. Harty, J. T. and Bevan, M. J., Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity 1995. 3: 109-117.
53. Wu, X., Chen, Y., Sun, R., Wei, H. and Tian, Z., Impairment of hepatic NK cell development in IFN-gamma deficient mice. Cytokine 2012. 60: 616-625.
54. Shi, C., Hohl, T. M., Leiner, I., Equinda, M. J., Fan, X. and Pamer, E. G., Ly6G+ neutrophils are dispensable for defense against systemic Listeria monocytogenes infection. J. Immunol. 2011. 187: 5293-5298.
55. Carr, K. D., Sieve, A. N., Indramohan, M., Break, T. J., Lee, S. and Berg, R. E., Specific depletion reveals a novel role for neutrophil-mediated protection in the liver during Listeria monocytogenes infection. Eur. J. Immunol. 2011. 41: 2666-2676.
56. Edelson, B. T., Bradstreet, T. R., Hildner, K., Carrero, J. A., Frederick, K. E., KC, W., Belizaire, R., Aoshi, T.et al., CD8alpha(+) dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity 2011. 35: 236-248.
57. Goldmann, O., Chhatwal, G. S. and Medina, E., Contribution of natural killer cells to the pathogenesis of septic shock induced by Streptococcus pyogenes in mice. J. Infect. Dis. 2005. 191: 1280-1286.
58. Newton, D. W., Jr., Runnels, H. A. and Kearns, R. J., Enhanced splenic bacterial clearance and neutrophilia in anti-NK1.1-treated mice infected with Pseudomonas aeruginosa. Nat. Immun. 1992. 11: 335-344.
59. Stevenson, H. L., Estes, M. D., Thirumalapura, N. R., Walker, D. H. and Ismail, N., Natural killer cells promote tissue injury and systemic inflammatory responses during fatal Ehrlichia-induced toxic shock-like syndrome. Am. J. Pathol. 2010. 177: 766-776.
60. Nolte, M. A. and van Lier, R. A., The price of the CD27-CD70 costimulatory axis: you can't have it all. J. Exp. Med. 2006. 203: 2405-2408.
61. Huang, S., Hendriks, W., Althage, A., Hemmi, S., Bluethmann, H., Kamijo, R., Vilcek et al., Immune response in mice that lack the interferon-gamma receptor. Science 1993. 259: 1742-1745.