Lack of PD-L1 Expression by iNKT Cells Improves the Course of Influenza A Infection

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Maazi, Hadi ^a   Singh, Abinav K ^a   Speak, Anneliese O ^a   Lombardi, Vincent ^a   Lam, Jonathan ^a   Khoo, Bryant ^a   Inn, Kyung Soo ^a   Sharpe, Arlene H ^b   Jung, Jae U ^a   Akbari, Omid ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 4; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; PROGRAMMED DEATH 1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL STIMULATION; CELL TRANSFER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE COURSE; FEMALE; HISTOPATHOLOGY; IMMUNE RESPONSE; INFECTION SENSITIVITY; INFLUENZA A; LYMPHOCYTE FUNCTION; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PNEUMONIA; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; WEIGHT REDUCTION; WILD TYPE;

ANIMALS; ANTIGENS, CD274; CYTOKINES; DENDRITIC CELLS; FEMALE; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; INFLUENZA A VIRUS, H1N1 SUBTYPE; LUNG; MICE; MICE, INBRED BALB C; NATURAL KILLER T-CELLS; ORTHOMYXOVIRIDAE INFECTIONS; PROGRAMMED CELL DEATH 1 LIGAND 2 PROTEIN;

EID: 84875023175     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059599     Document Type: Article

References (62)

1. Barker WH, Mullooly JP, (1980) Impact of epidemic type A influenza in a defined adult population. Am J Epidemiol 112: 798-811.
2. Barker WH, Mullooly JP, (1982) Pneumonia and influenza deaths during epidemics: implications for prevention. Arch Intern Med 142: 85-89.
3. Thompson WW, Comanor L, Shay DK, (2006) Epidemiology of seasonal influenza: use of surveillance data and statistical models to estimate the burden of disease. J Infect Dis 194 (Suppl 2): S82-91.
4. Clements ML, Betts RF, Tierney EL, Murphy BR, (1986) Serum and nasal wash antibodies associated with resistance to experimental challenge with influenza A wild-type virus. J Clin Microbiol 24: 157-160.
5. Clements ML, Murphy BR, (1986) Development and persistence of local and systemic antibody responses in adults given live attenuated or inactivated influenza A virus vaccine. J Clin Microbiol 23: 66-72.
6. Murphy BR, Baron S, Chalhub EG, Uhlendorf CP, Chanock RM, (1973) Temperature-sensitive mutants of influenza virus. IV. Induction of interferon in the nasopharynx by wild-type and a temperature-sensitive recombinant virus. J Infect Dis 128: 488-493.
7. Droebner K, Haasbach E, Fuchs C, Weinzierl AO, Stevanovic S, et al. (2008) Antibodies and CD4(+) T-cells mediate cross-protection against H5N1 influenza virus infection in mice after vaccination with a low pathogenic H5N2 strain. Vaccine 26: 6965-6974.
8. La Gruta NL, Kedzierska K, Stambas J, Doherty PC, (2007) A question of self-preservation: immunopathology in influenza virus infection. Immunol Cell Biol 85: 85-92.
9. Lawrence CW, Ream RM, Braciale TJ, (2005) Frequency, specificity, and sites of expansion of CD8+ T cells during primary pulmonary influenza virus infection. J Immunol 174: 5332-5340.
10. De Santo C, Salio M, Masri SH, Lee LY, Dong T, et al. (2008) Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloid-derived suppressor cells in mice and humans. J Clin Invest 118: 4036-4048.
11. Paget C, Ivanov S, Fontaine J, Blanc F, Pichavant M, et al. (2011) Potential role of invariant NKT cells in the control of pulmonary inflammation and CD8+ T cell response during acute influenza A virus H3N2 pneumonia. J Immunol 186: 5590-5602.
12. Akbari O, Stock P, Meyer E, Kronenberg M, Sidobre S, et al. (2003) Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat Med 9: 582-588.
13. Akbari O, Stock P, Singh AK, Lombardi V, Lee WL, et al. (2010) PD-L1 and PD-L2 modulate airway inflammation and iNKT-cell-dependent airway hyperreactivity in opposing directions. Mucosal Immunol 3: 81-91.
14. Barral DC, Brenner MB, (2007) CD1 antigen presentation: how it works. Nat Rev Immunol 7: 929-941.
15. Bendelac A, Savage PB, Teyton L, (2007) The biology of NKT cells. Annu Rev Immunol 25: 297-336.
16. Godfrey DI, Kronenberg M, (2004) Going both ways: immune regulation via CD1d-dependent NKT cells. J Clin Invest 114: 1379-1388.
17. Tessmer MS, Fatima A, Paget C, Trottein F, Brossay L, (2009) NKT cell immune responses to viral infection. Expert Opin Ther Targets 13: 153-162.
18. Cerundolo V, Silk JD, Masri SH, Salio M, (2009) Harnessing invariant NKT cells in vaccination strategies. Nat Rev Immunol 9: 28-38.
19. Diana J, Brezar V, Beaudoin L, Dalod M, Mellor A, et al. (2011) Viral infection prevents diabetes by inducing regulatory T cells through NKT cell-plasmacytoid dendritic cell interplay. J Exp Med 208: 729-745.
20. Terabe M, Berzofsky JA, (2007) NKT cells in immunoregulation of tumor immunity: a new immunoregulatory axis. Trends Immunol 28: 491-496.
21. Dong H, Zhu G, Tamada K, Chen L, (1999) B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 5: 1365-1369.
22. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, et al. (2000) Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 192: 1027-1034.
23. Yamazaki T, Akiba H, Iwai H, Matsuda H, Aoki M, et al. (2002) Expression of programmed death 1 ligands by murine T cells and APC. J Immunol 169: 5538-5545.
24. Kerzerho J, Maazi H, Speak AO, Szely N, Lombardi V, et al. (2012) Programmed cell death ligand 2 regulates T(H)9 differentiation and induction of chronic airway hyperreactivity. J Allergy Clin Immunol.
25. Eppihimer MJ, Gunn J, Freeman GJ, Greenfield EA, Chernova T, et al. (2002) Expression and regulation of the PD-L1 immunoinhibitory molecule on microvascular endothelial cells. Microcirculation 9: 133-145.
26. Rodig N, Ryan T, Allen JA, Pang H, Grabie N, et al. (2003) Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+ T cell activation and cytolysis. Eur J Immunol 33: 3117-3126.
27. Liang SC, Greenwald RJ, Latchman YE, Rosas L, Satoskar A, et al. (2006) PD-L1 and PD-L2 have distinct roles in regulating host immunity to cutaneous leishmaniasis. Eur J Immunol 36: 58-64.
28. Maier H, Isogawa M, Freeman GJ, Chisari FV, (2007) PD-1: PD-L1 interactions contribute to the functional suppression of virus-specific CD8+ T lymphocytes in the liver. J Immunol 178: 2714-2720.
29. Cui J, Shin T, Kawano T, Sato H, Kondo E, et al. (1997) Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 278: 1623-1626.
30. Keir ME, Liang SC, Guleria I, Latchman YE, Qipo A, et al. (2006) Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med 203: 883-895.
31. Talon J, Salvatore M, O'Neill RE, Nakaya Y, Zheng H, et al. (2000) Influenza A and B viruses expressing altered NS1 proteins: A vaccine approach. Proc Natl Acad Sci U S A 97: 4309-4314.
32. Lombardi V, Stock P, Singh AK, Kerzerho J, Yang W, et al. (2010) A CD1d-dependent antagonist inhibits the activation of invariant NKT cells and prevents development of allergen-induced airway hyperreactivity. J Immunol 184: 2107-2115.
33. Latchman YE, Liang SC, Wu Y, Chernova T, Sobel RA, et al. (2004) PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc Natl Acad Sci U S A 101: 10691-10696.
34. Zhang Y, Chung Y, Bishop C, Daugherty B, Chute H, et al. (2006) Regulation of T cell activation and tolerance by PDL2. Proc Natl Acad Sci U S A 103: 11695-11700.
35. Chang YJ, Kim HY, Albacker LA, Lee HH, Baumgarth N, et al. (2011) Influenza infection in suckling mice expands an NKT cell subset that protects against airway hyperreactivity. J Clin Invest 121: 57-69.
36. Coquet JM, Chakravarti S, Kyparissoudis K, McNab FW, Pitt LA, et al. (2008) Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc Natl Acad Sci U S A 105: 11287-11292.
37. Durante-Mangoni E, Wang R, Shaulov A, He Q, Nasser I, et al. (2004) Hepatic CD1d expression in hepatitis C virus infection and recognition by resident proinflammatory CD1d-reactive T cells. J Immunol 173: 2159-2166.
38. Kakimi K, Guidotti LG, Koezuka Y, Chisari FV, (2000) Natural killer T cell activation inhibits hepatitis B virus replication in vivo. J Exp Med 192: 921-930.
39. Johnson TR, Hong S, Van Kaer L, Koezuka Y, Graham BS, (2002) NK T cells contribute to expansion of CD8(+) T cells and amplification of antiviral immune responses to respiratory syncytial virus. J Virol 76: 4294-4303.
40. Ashkar AA, Rosenthal KL, (2003) 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 77: 10168-10171.
41. Grubor-Bauk B, Simmons A, Mayrhofer G, Speck PG, (2003) Impaired clearance of herpes simplex virus type 1 from mice lacking CD1d or NKT cells expressing the semivariant V alpha 14-J alpha 281 TCR. J Immunol 170: 1430-1434.
42. Motsinger A, Haas DW, Stanic AK, Van Kaer L, Joyce S, et al. (2002) CD1d-restricted human natural killer T cells are highly susceptible to human immunodeficiency virus 1 infection. J Exp Med 195: 869-879.
43. Ho LP, Denney L, Luhn K, Teoh D, Clelland C, et al. (2008) Activation of invariant NKT cells enhances the innate immune response and improves the disease course in influenza A virus infection. Eur J Immunol 38: 1913-1922.
44. Van Dommelen SL, Degli-Esposti MA, (2004) NKT cells and viral immunity. Immunol Cell Biol 82: 332-341.
45. Liu TY, Uemura Y, Suzuki M, Narita Y, Hirata S, et al. (2008) Distinct subsets of human invariant NKT cells differentially regulate T helper responses via dendritic cells. Eur J Immunol 38: 1012-1023.
46. Hatta Y, Hershberger K, Shinya K, Proll SC, Dubielzig RR, et al. (2010) Viral replication rate regulates clinical outcome and CD8 T cell responses during highly pathogenic H5N1 influenza virus infection in mice. PLoS Pathog 6.
47. Hufford MM, Kim TS, Sun J, Braciale TJ, (2011) Antiviral CD8+ T cell effector activities in situ are regulated by target cell type. J Exp Med 208: 167-180.
48. Kishimoto K, Sandner S, Imitola J, Sho M, Li Y, et al. (2002) Th1 cytokines, programmed cell death, and alloreactive T cell clone size in transplant tolerance. J Clin Invest 109: 1471-1479.
49. Wood KJ, Sawitzki B, (2006) Interferon gamma: a crucial role in the function of induced regulatory T cells in vivo. Trends Immunol 27: 183-187.
50. Bocek P Jr, Foucras G, Paul WE, (2004) Interferon gamma enhances both in vitro and in vivo priming of CD4+ T cells for IL-4 production. J Exp Med 199: 1619-1630.
51. Moran TM, Isobe H, Fernandez-Sesma A, Schulman JL, (1996) Interleukin-4 causes delayed virus clearance in influenza virus-infected mice. J Virol 70: 5230-5235.
52. Chang YJ, Kim HY, Albacker LA, Baumgarth N, McKenzie AN, et al. (2011) Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol 12: 631-638.
53. Garcia-Sastre A, Durbin RK, Zheng H, Palese P, Gertner R, et al. (1998) The role of interferon in influenza virus tissue tropism. J Virol 72: 8550-8558.
54. Ronni T, Matikainen S, Sareneva T, Melen K, Pirhonen J, et al. (1997) Regulation of IFN-alpha/beta, MxA, 2′,5′-oligoadenylate synthetase, and HLA gene expression in influenza A-infected human lung epithelial cells. J Immunol 158: 2363-2374.
55. Sareneva T, Matikainen S, Kurimoto M, Julkunen I, (1998) Influenza A virus-induced IFN-alpha/beta and IL-18 synergistically enhance IFN-gamma gene expression in human T cells. J Immunol 160: 6032-6038.
56. Singh AK, Stock P, Akbari O, (2011) Role of PD-L1 and PD-L2 in allergic diseases and asthma. Allergy 66: 155-162.
57. Curran MA, Montalvo W, Yagita H, Allison JP, (2010) PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A 107: 4275-4280.
58. Dulgerian LR, Garrido VV, Stempin CC, Cerban FM, (2011) Programmed death ligand 2 regulates arginase induction and modifies Trypanosoma cruzi survival in macrophages during murine experimental infection. Immunology 133: 29-40.
59. Guleria I, Khosroshahi A, Ansari MJ, Habicht A, Azuma M, et al. (2005) A critical role for the programmed death ligand 1 in fetomaternal tolerance. J Exp Med 202: 231-237.
60. Paterson AM, Brown KE, Keir ME, Vanguri VK, Riella LV, et al. (2011) The programmed death-1 ligand 1: b7-1 pathway restrains diabetogenic effector T cells in vivo. J Immunol 187: 1097-1105.
61. Matsumoto K, Inoue H, Nakano T, Tsuda M, Yoshiura Y, et al. (2004) B7-DC regulates asthmatic response by an IFN-gamma-dependent mechanism. J Immunol 172: 2530-2541.
62. Erickson JJ, Gilchuk P, Hastings AK, Tollefson SJ, Johnson M, et al. (2012) Viral acute lower respiratory infections impair CD8+ T cells through PD-1. J Clin Invest 122: 2967-2982.