Critical role of natural killer cells in lung immunopathology during influenza infection in mice

Journal of Infectious Diseases

Volumn 206, Issue 2, 2012, Pages 167-177

  Abdul Careem, Mohamed F ^a,b   Firoz Mian, M ^a   Yue, Geoffry ^a   Gillgrass, Amy ^a   Chenoweth, Meghan J ^a   Barra, Nicole G ^a   Chew, Marianne V ^a   Chan, Tiffany ^a   Al Garawi, Amal A ^a   Jordana, Manel ^a   Ashkar, Ali A ^a  

^a MCMASTER UNIVERSITY MEDICAL CENTRE   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 6;

AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOPATHOLOGY; INFLAMMATION; INFLUENZA; LUNG DISEASE; LUNG INFECTION; LUNG INJURY; LUNG LAVAGE; MALE; MONONUCLEAR CELL; MOUSE; MOUSE STRAIN; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SURVIVAL TIME; VIRUS REPLICATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; INTERLEUKIN-15; KILLER CELLS, NATURAL; LUNG; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION;

EID: 84862893987     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jis340     Document Type: Article

References (50)

1. Grebe KM, Takeda K, Hickman HD, et al. Cutting edge: sympathetic nervous system increases proinflammatory cytokines and exacerbates influenza virus pathogenesis. J Immunol 2010; 184:540-4.
2. Lin KL, Suzuki Y, Nakano H, Ramsburg E, Gunn MD. CCR2+ monocytederived dendritic cells and exudate macrophages produce influenzainduced pulmonary immune pathology and mortality. J Immunol 2008; 180:2562-72.
3. Marsolais D, Hahm B, Walsh KB, et al. A critical role for the sphingosine analog AAL-R in dampening the cytokine response during influenza virus infection. Proc Natl Acad Sci USA 2009; 106:1560-5.
4. Nakamura R, Maeda N, Shibata K, Yamada H, Kase T, Yoshikai Y. Interleukin-15 is critical in the pathogenesis of influenza virusinduced acute lung injury. J Virol 2010; 84:5574-82.
5. Rygiel TP, Rijkers ES, de Ruiter T, et al. Lack of CD200 enhances pathological T cell responses during influenza infection. J Immunol 2009; 183:1990-6.
6. Xu L, Yoon H, Zhao MQ, Liu J, Ramana CV, Enelow RI. Cutting edge: pulmonary immunopathology mediated by antigen-specific expression of TNF-alpha by antiviral CD8+ cells. J Immunol 2004; 173:721-5.
7. Crowe CR, Chen K, Pociask DA, et al. Critical role of IL-17RA in immunopathology of influenza infection. J Immunol 2009; 183:5301-10.
8. Sun J, Madan R, Karp CL, Braciale TJ. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat Med 2009; 15:277-84.
9. Seki M, Kohno S, Newstead MW, et al. Critical role of IL-1 receptorassociated kinase-M in regulating chemokine-dependent deleterious inflammation in murine influenza pneumonia. J Immunol 2010; 184:1410-8.
10. Snelgrove RJ, Goulding J, Didierlaurent AM, et al. A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat Immunol 2008; 9:1074-83.
11. Kennedy MK, Glaccum M, Brown SN, et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 2000; 191:771-80.
12. Ashkar AA, Rosenthal KL. Interleukin-15 and natural killer and NKT cells play a critical role in innate protection against genital herpes simplex virus type 2 infection. J Virol 2003; 77:10168-71.
13. Kos FJ, Engleman EG. Requirement for natural killer cells in the induction of cytotoxic T cells. J Immunol 1995; 155:578-84.
14. Burlington DB, Djeu JY, Wells MA, Kiley SC, Quinnan GV Jr Large granular lymphocytes provide an accessory function in the in vitro development of influenza virus-specific cytotoxic T cells. J Immunol 1984; 132:3154-8.
15. Harker JA, Godlee A, Wahlsten JL, et al. Interleukin 18 coexpression during respiratory syncytial virus infection results in enhanced disease mediated by natural killer cells. J Virol 2010; 84:4073-82.
16. Al-Garawi AA, Fattouh R, Walker TD, et al. Acute, but not resolved, influenza A infection enhances susceptibility to house dust mite-induced allergic disease. J Immunol 2009; 182:3095-104.
17. Small CL, Shaler CR, McCormick S, et al. Influenza infection leads to increased susceptibility to subsequent bacterial superinfection by impairing NK cell responses in the lung. J Immunol 2010; 184:2048-56.
18. Crowe SR, Miller SC, Shenyo RM, Woodland DL. Vaccination with an acidic polymerase epitope of influenza virus elicits a potent antiviral T cell response but delayed clearance of an influenza virus challenge. J Immunol 2005; 174:696-701.
19. Crowe SR, Miller SC, Woodland DL. Identification of protective and non-protective T cell epitopes in influenza. Vaccine 2006; 24:452-6.
20. Mian MF, Lauzon NM, Stampfli MR, Mossman KL, Ashkar AA. Impairment of human NK cell cytotoxic activity and cytokine release by cigarette smoke. J Leukoc Biol 2008; 83:774-84.
21. Gaush CR, Smith TF. Replication and plaque assay of influenza virus in an established line of canine kidney cells. Appl Microbiol 1968; 16:588-94.
22. Mocikat R, Braumüller H, Gumy A, et al. Natural killer cells activated by MHC class I(low) targets prime dendritic cells to induce protective CD8 T cell responses. Immunity 2003; 19:561-9.
23. Morandi B, Mortara L, Carrega P, et al. NK cells provide helper signal for CD8+ cells by inducing the expression of membrane-bound IL-15 on DCs. Int Immunol 2009; 21:599-606.
24. Stein-Streilein J, Guffee J. In vivo treatment of mice and hamsters with antibodies to asialo GM1 increases morbidity and mortality to pulmonary influenza infection. J Immunol 1986; 136:1435-41.
25. Brown DM, Roman E, Swain SL. CD4 T cell responses to influenza infection. Semin Immunol 2004; 16:171-7.
26. Lunemann A, Lunemann JD, Munz C. Regulatory NK-cell functions in inflammation and autoimmunity. Mol Med 2009; 15:352-8.
27. Mastroianni CM, d'Ettorre G, Forcina G, et al. Interleukin-15 enhances neutrophil functional activity in patients with human immunodeficiency virus infection. Blood 2000; 96:1979-84.
28. Ohteki T, Tada H, Ishida K, et al. Essential roles of DC-derived IL-15 as a mediator of inflammatory responses in vivo. J Exp Med 2006; 203:2329-38.
29. Schmitz N, Kurrer M, Bachmann MF, Kopf M. Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J Virol 2005; 79:6441-8.
30. Zhao Y, Lu M, Lau LT, et al. Neutrophils may be a vehicle for viral replication and dissemination in human H5N1 avian influenza. Clin Infect Dis 2008; 47:1575-8.
31. Gill N, Ashkar AA. Adaptive immune responses fail to provide protection against genital HSV-2 infection in the absence of IL-15. Eur J Immunol 2007; 37:2529-38.
32. Chen JP, Liao NS, Lai SL, et al. Reduced 2,4-dinitro-1- fluorobenzeneinduced contact hypersensitivity response in IL-15 receptor alphadeficient mice correlates with diminished CCL5/RANTES and CXCL10/IP-10 expression. Eur J Immunol 2005; 35:690-8.
33. Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol 2007; 25:297-336.
34. Nogusa S, Ritz BW, Kassim SH, Jennings SR, Gardner EM. Characterization of age-related changes in natural killer cells during primary influenza infection in mice. Mech Ageing Dev 2008; 129:223-30.
35. Moskophidis D, Kioussis D. Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J Exp Med 1998; 188:223-32.
36. Gazit R, Gruda R, Elboim M, et al. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol 2006; 7:517-23.
37. Kos FJ, Engleman EG. Role of natural killer cells in the generation of influenza virus-specific cytotoxic T cells. Cell Immunol 1996; 173:1-6.
38. Empson VG, McQueen FM, Dalbeth N. The natural killer cell: a further innate mediator of gouty inflammation? Immunol Cell Biol 2010; 88:24-31.
39. Perricone R, Perricone C, De Carolis C, Shoenfeld Y. NK cells in autoimmunity: a two-edg'd weapon of the immune system. Autoimmun Rev 2008; 7:384-90.
40. Goldmann O, Chhatwal GS, Medina E. Contribution of natural killer cells to the pathogenesis of septic shock induced by Streptococcus pyogenes in mice. J Infect Dis 2005; 191:1280-6.
41. Badgwell B, Parihar R, Magro C, Dierksheide J, Russo T, Carson WE 3rd. Natural killer cells contribute to the lethality of a murine model of Escherichia coli infection. Surgery 2002; 132:205-12.
42. Djeu JY, Stocks N, Zoon K, Stanton GJ, Timonen T, Herberman RB. Positive self regulation of cytotoxicity in human natural killer cells by production of interferon upon exposure to influenza and herpes viruses. J Exp Med 1982; 156:1222-34.
43. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 2010; 115:2167-76.
44. Verri WA Jr, Cunha TM, Ferreira SH, et al. IL-15 mediates antigeninduced neutrophil migration by triggering IL-18 production. Eur J Immunol 2007; 37:3373-80.
45. Hashimoto Y, Moki T, Takizawa T, Shiratsuchi A, Nakanishi Y. Evidence for phagocytosis of influenza virus-infected, apoptotic cells by neutrophils and macrophages in mice. J Immunol 2007; 178:2448-57.
46. Wang SZ, Xu H, Wraith A, Bowden JJ, Alpers JH, Forsyth KD. Neutrophils induce damage to respiratory epithelial cells infected with respiratory syncytial virus. Eur Respir J 1998; 12:612-8.
47. Tate MD, Pickett DL, van Rooijen N, Brooks AG, Reading PC. Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J Virol 2010; 84:7569-80.
48. Herold S, Steinmueller M, von Wulffen W, et al. Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J Exp Med 2008; 205:3065-77.
49. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001; 19: 683-765.
50. Graham MB, Braciale VL, Braciale TJ. Influenza virus-specific CD4+ T helper type 2 T lymphocytes do not promote recovery from experimental virus infection. J Exp Med 1994; 180:1273-82.