Generation of cellular immune memory and B-cell immunity is impaired by natural killer cells

Nature Communications

Volumn 6, Issue , 2015, Pages

  Rydyznski, Carolyn ^a   Daniels, Keith A ^b   Karmele, Erik P ^a   Brooks, Taylor R ^a   Mahl, Sarah E ^a   Moran, Michael T ^a   Li, Caimei ^a   Sutiwisesak, Rujapak ^b   Welsh, Raymond M ^b   Waggoner, Stephen N ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PERFORIN; VIRUS ANTIBODY; CYTOKINE; MONOCLONAL ANTIBODY;

ANTIBODY; CYTOLOGY; IMMUNE RESPONSE; IMMUNITY; MEMORY; VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARENAVIRUS INFECTION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CELLULAR IMMUNODEFICIENCY; CONTROLLED STUDY; GERMINAL CENTER; HELPER CELL; HUMORAL IMMUNITY; IMMUNOLOGICAL MEMORY; INFECTION CONTROL; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; MEMORY CELL; MEMORY T LYMPHOCYTE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PICHINDE VIRUS; VIRUS MENINGITIS; VIRUS REPLICATION; ANIMAL; B LYMPHOCYTE; C57BL MOUSE; FLOW CYTOMETRY; GAS CHROMATOGRAPHY; IMMUNOLOGY; KNOCKOUT MOUSE; VIRAL PLAQUE ASSAY;

HEPATITIS C VIRUS;

ANIMALS; ANTIBODIES, MONOCLONAL; ARENAVIRIDAE INFECTIONS; B-LYMPHOCYTES; CHROMATOGRAPHY, GAS; CYTOKINES; FLOW CYTOMETRY; IMMUNITY, CELLULAR; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; VIRAL PLAQUE ASSAY;

EID: 84924027468     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7375     Document Type: Article

References (57)

1. Plotkin, S. A. Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 17, 1055-1065 (2010).
2. Swadling, L., Klenerman, P. & Barnes, E. Ever closer to a prophylactic vaccine for HCV. Exp. Opin. Biol. Ther. 13, 1109-1124 (2013).
3. Kwong, P. D., Mascola, J. R. & Nabel, G. J. The changing face of HIV vaccine research. J. Int. AIDS Soc. 15, 17407 (2012).
4. Lanier, L. L. Evolutionary struggles between NK cells and viruses. Nat. Rev. Immunol. 8, 259-268 (2008).
5. Welsh, R. M. & Waggoner, S. N. NK cells controlling virus-specific T cells: rheostats for acute vs. persistent infections. Virology 435, 37-45 (2013).
6. Michael, A., Hackett, J. J., Bennett, M., Kumar, V. & Yuan, D. Regulation of B lymphocytes by natural killer cells. Role of IFN-gamma. J. Immunol. 142, 1095-1101 (1989).
7. Wilder, J. A., Koh, C. Y. & Yuan, D. The role of NK cells during in vivo antigen-specific antibody responses. J. Immunol. 156, 146-152 (1996).
8. Krebs, P. et al. NK-cell-mediated killing of target cells triggers robust antigenspecific T-cell-mediated and humoral responses. Blood 113, 6593-6602 (2009).
9. Kelly, J. M. et al. Induction of tumor-specific T cell memory by NK cell-mediated tumor rejection. Nat. Immunol. 3, 83-90 (2002).
10. Westwood, J. A. et al. Cutting edge: novel priming of tumor-specific immunity by NKG2D-triggered NK cell-mediated tumor rejection and Th1-independent CD4+ T cell pathway. J. Immunol. 172, 757-761 (2004).
11. Robbins, S. H. et al. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog. 3, e123 (2007).
12. Lee, S. H., Kim, K. S., Fodil-Cornu, N., Vidal, S. M. & Biron, C. A. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J. Exp. Med. 206, 2235-2251 (2009).
13. Andrews, D. M. et al. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J. Exp. Med. 207, 1333-1343 (2010).
14. Mitrovic, M. et al. The NK cell response to mouse cytomegalovirus infection affects the level and kinetics of the early CD8+ T-cell response. J. Virol. 86, 2165-2175 (2012).
15. Stadnisky, M. D., Xie, X., Coats, E. R., Bullock, T. N. & Brown, M. G. Self MHC class I-licensed NK cells enhance adaptive CD8 T-cell viral immunity. Blood 117, 5133-5141 (2011).
16. Waggoner, S. N., Cornberg, M., Selin, L. K. & Welsh, R. M. Natural killer cells act as rheostats modulating antiviral T cells. Nature 481, 394-398 (2012).
17. Peppa, D. et al. Up-regulation of a death receptor renders antiviral T cells susceptible to NK cell-mediated deletion. J. Exp. Med. 210, 99-114 (2013).
18. Lang, P. A. et al. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc. Natl Acad. Sci. USA 109, 1210-1215 (2012).
19. Cook, K. D. & Whitmire, J. K. The depletion of NK cells prevents T cell exhaustion to efficiently control disseminating virus infection. J. Immunol. 190, 641-649 (2013).
20. Bukowski, J. F., Woda, B. A., Habu, S., Okumura, K. & Welsh, R. M. Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J. Immunol. 131, 1531-1538 (1983).
21. Waggoner, S. N., Taniguchi, R. T., Mathew, P. A., Kumar, V. & Welsh, R. M. Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8+ T cells, leading to prolonged viral persistence and altered pathogenesis. J. Clin. Invest. 120, 1925-1938 (2010).
22. Joshi, N. S. et al. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27, 281-295 (2007).
23. Brehm, M. A. et al. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat. Immunol. 3, 627-634 (2002).
24. Soderquest, K. et al. Cutting edge: CD8+ T cell priming in the absence of NK cells leads to enhanced memory responses. J. Immunol. 186, 3304-3308 (2011).
25. Crotty, S. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29, 621-663 (2011).
26. Iyer, S. S. et al. Identification of novel markers for mouse CD4(+) T follicular helper cells. Eur. J. Immunol. 43, 3219-3232 (2013).
27. Dong, C. et al. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 409, 97-101 (2001).
28. McAdam, A. J. et al. ICOS is critical for CD40-mediated antibody class switching. Nature 409, 102-105 (2001).
29. Yang, H., Yogeeswaran, G., Bukowski, J. F. & Welsh, R. M. Expression of asialo GM1 and other antigens and glycolipids on natural killer cells and spleen leukocytes in virus-infected mice. Nat. Immun. Cell Growth Regul. 4, 21-39 (1985).
30. Victora, G. D. & Nussenzweig, M. C. Germinal centers. Annu. Rev. Immunol. 30, 429-457 (2012).
31. Bruns, M., Cihak, J., Muller, G. & Lehmann-Grube, F. Lymphocytic choriomeningitis virus. VI. Isolation of a glycoprotein mediating neutralization. Virology 130, 247-251 (1983).
32. Hangartner, L., Zinkernagel, R. M. & Hengartner, H. Antiviral antibody responses: the two extremes of a wide spectrum. Nat. Rev. Immunol. 6, 231-243 (2006).
33. Pinschewer, D. D. et al. Kinetics of protective antibodies are determined by the viral surface antigen. J. Clin. Invest. 114, 988-993 (2004).
34. Battegay, M. et al. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J. Virol. Methods 33, 191-198 (1991).
35. Kitamura, D., Roes, J., Kuhn, R. & Rajewsky, K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350, 423-426 (1991).
36. Rahemtulla, A. et al. Normal development and function of CD8+ cells but markedly decreased helper cell activity in mice lacking CD4. Nature 353, 180-184 (1991).
37. Kagi, D. et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369, 31-37 (1994).
38. Watanabe-Fukunaga, R., Brannan, C. I., Copeland, N. G., Jenkins, N. A. & Nagata, S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356, 314-317 (1992).
39. Alter, G., Malenfant, J. M. & Altfeld, M. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294, 15-22 (2004).
40. Herberman, R. B., Nunn, M. E. & Lavrin, D. H. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int. J. Cancer. 16, 216-229 (1975).
41. Denzel, A. et al. Basophils enhance immunological memory responses. Nat. Immunol. 9, 733-742 (2008).
42. Maggi, E. et al. Th2-like CD8+ T cells showing B cell helper function and reduced cytolytic activity in human immunodeficiency virus type 1 infection. J. Exp. Med. 180, 489-495 (1994).
43. Galli, G. et al. CD1d-restricted help to B cells by human invariant natural killer T lymphocytes. J. Exp. Med. 197, 1051-1057 (2003).
44. Yokoyama, S. et al. Expression of the Blast-1 activation/adhesion molecule and its identification as CD48. J. Immunol. 146, 2192-2200 (1991).
45. Lee, K. M. et al. 2B4 acts as a non-major histocompatibility complex binding inhibitory receptor on mouse natural killer cells. J. Exp. Med. 199, 1245-1254 (2004).
46. Wilson, J. L. et al. Targeting of human dendritic cells by autologous NK cells. J. Immunol. 163, 6365-6370 (1999).
47. Hayakawa, Y. et al. NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J. Immunol. 172, 123-129 (2004).
48. Kalia, V. et al. Prolonged interleukin-2Ralpha expression on virus-specific CD8+ T cells favors terminal-effector differentiation in vivo. Immunity 32, 91-103 (2010).
49. Kaech, S. M. et al. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4, 1191-1198 (2003).
50. Arsenio, J. et al. Early specification of CD8 T lymphocyte fates during adaptive immunity revealed by single-cell gene-expression analyses. Nat. Immunol. 15, 365-372 (2014).
51. Zafirova, B. et al. Altered NK cell development and enhanced NK cell-mediated resistance to mouse cytomegalovirus in NKG2D-deficient mice. Immunity 31, 270-282 (2009).
52. Huber, S., Sartini, D. & Exley, M. Role of CD1d in coxsackievirus B3-induced myocarditis. J. Immunol. 170, 3147-3153 (2003).
53. Mendiratta, S. K. et al. CD1d1 mutant mice are deficient in natural T cells that promptly produce IL-4. Immunity 6, 469-477 (1997).
54. Welsh, R. M. & Seedhom, M. O. Lymphocytic choriomeningitis virus (LCMV): propagation, quantitation, and storage. Curr. Protoc. Microbiol. Chapter 15, Unit 15A 11 (2008).
55. Selin, L. K., Nahill, S. R. & Welsh, R. M. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J. Exp. Med. 179, 1933-1943 (1994).
56. Rowe, J. H., Ertelt, J. M., Xin, L. & Way, S. S. Listeria monocytogenes cytoplasmic entry induces fetal wastage by disrupting maternal Foxp3+ regulatory T cell-sustained fetal tolerance. PLoS Pathog. 8, e1002873 (2012).
57. Shen, Z. T. et al. Bi-specific MHC heterodimers for characterization of cross-reactive T cells. J. Biol. Chem. 285, 33144-33153 (2010).