Diesel exhaust particles modify natural killer cell function and cytokine release
Tóm tắt
Natural killer (NK) cells are an important lymphocyte population in the nasal mucosa and play important roles in linking the innate and the adaptive immune response. Their two main functions are direct cell-mediated cytotoxicity and the release of cytokines. They are important during viral infections and cancer. Due to their location in the nasal mucosa, NK cells are likely exposed to inhaled pollutants, such as diesel exhaust. Whether and how exposure to diesel exhaust particles (DEP) affects NK cell function in the context of viral infections has not been investigated. NK cells were isolated from peripheral blood obtained from normal healthy volunteers and subsequently stimulated with the viral mimetic polyinosinic:polycytidylic acid (pI:C), DEP, or pI:C+DEP for 18 hours. NK cells were subsequently analyzed for changes in surface marker expression, cytokine production, gene expression changes, and cytotoxic function using flow cytometry, ELISA, qRT-PCR, and cell-mediated cytotoxicity assay, respectively. Stimulation of NK cells with pI:C and pI:C+DEP, but not DEP alone, increased the release of IL-1β, IL-2, IL-4, IL-8, IL-10, IL-12p70, IFN-γ and TNF-α. As compared to pI:C alone or pI:C+DEP, the release of IL-1β, IL-8 and TNF-α was significantly lower after DEP stimulation alone. Stimulation with pI:C alone increased the gene and protein expression of granzyme B and perforin, which was completely blunted by adding DEP. Addition of DEP further reduced CD16 expression in pI:C stimulated cells. Similarly, cell-mediated cytotoxicity was significantly reduced by the addition of DEP. In the context of viral infection, DEP potentially reduces NK cells' ability to kill virus-infected host cells, in spite of normal cytokine levels, and this may increase susceptibility to viral infections . This reduction in the potential ability of NK cells to kill virus-infected host cells may increase the susceptibility to viral infections after DEP exposure.
Tài liệu tham khảo
Culley FJ: Natural killer cells in infection and inflammation of the lung. Immunology 2009, 128: 151–163. 10.1111/j.1365-2567.2009.03167.x
Horvath KM, Herbst M, Zhou H, Zhang H, Noah TL, Jaspers I: Nasal lavage natural killer cell function is suppressed in smokers after live attenuated influenza virus. Respir Res 2011, 12: 102. 10.1186/1465-9921-12-102
Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S: Innate or adaptive immunity? The example of natural killer cells. Science 2011, 331: 44–49. 10.1126/science.1198687
Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S: Functions of natural killer cells. Nat Immunol 2008, 9: 503–510.
Farag SS, Caligiuri MA: Human natural killer cell development and biology. Blood Rev 2006, 20: 123–137. 10.1016/j.blre.2005.10.001
Robertson MJ: Role of chemokines in the biology of natural killer cells. J Leukoc Biol 2002, 71: 173–183.
Lanier LL: Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 2008, 9: 495–502.
Marcenaro E, Carlomagno S, Pesce S, Della Chiesa M, Parolini S, Moretta A, Sivori S: NK cells and their receptors during viral infections. Immunotherapy 2011,3(9):1075–86. 10.2217/imt.11.99
Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, Davis DM, Strominger JL, Yewdell JW, Porgador A: Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 2001, 409: 1055–1060. 10.1038/35059110
Pessino A, Sivori S, Bottino C, Malaspina A, Morelli L, Moretta L, Biassoni R, Moretta A: Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med 1998, 188: 953–960. 10.1084/jem.188.5.953
Williams LA, Ulrich CM, Larson T, Wener MH, Wood B, Campbell PT, Potter JD, McTiernan A, De Roos AJ: Proximity to traffic, inflammation, and immune function among women in the Seattle, Washington, area. Environ Health Perspect 2009, 117: 373–378.
Finkelman FD, Yang M, Orekhova T, Clyne E, Bernstein J, Whitekus M, Diaz-Sanchez D, Morris SC: Diesel exhaust particles suppress in vivo IFN-gamma production by inhibiting cytokine effects on NK and NKT cells. J Immunol 2004, 172: 3808–3813.
Muller L, Brighton LE, Ilona J: Ozone exposure of epithelial cells shifts co-cultured natural killer cells towards the produc-tion of type 2 cytokines. Am J Physiol-Lung C 2013,304(5):L332–41. 10.1152/ajplung.00256.2012
Van Loveren H, Krajnc EI, Rombout PJ, Blommaert FA, Vos JG: Effects of ozone, hexachlorobenzene, and bis(tri-n-butyltin)oxide on natural killer activity in the rat lung. Toxicol Appl Pharmacol 1990, 102: 21–33. 10.1016/0041-008X(90)90080-E
Ciencewicki J, Jaspers I: Air pollution and respiratory viral infection. Inhal Toxicol 2007, 19: 1135–1146. 10.1080/08958370701665434
Harrod KS, Jaramillo RJ, Rosenberger CL, Wang SZ, Berger JA, McDonald JD, Reed MD: Increased susceptibility to RSV infection by exposure to inhaled diesel engine emissions. Am J Resp Cell Mol 2003, 28: 451–463. 10.1165/rcmb.2002-0100OC
Hahon N, Booth JA, Green F, Lewis TR: Influenza virus infection in mice after exposure to coal dust and diesel engine emissions. Environ Res 1985, 37: 44–60. 10.1016/0013-9351(85)90048-9
Jaspers I, Ciencewicki JM, Zhang W, Brighton LE, Carson JL, Beck MA, Madden MC: Diesel exhaust enhances influenza virus infections in respiratory epithelial cells. Toxicol Sci 2005, 85: 990–1002. 10.1093/toxsci/kfi141
O'Connor GM, Hart OM, Gardiner CM: Putting the natural killer cell in its place. Immunology 2006, 117: 1–10. 10.1111/j.1365-2567.2005.02256.x
Brunekreef B, Holgate ST: Air pollution and health. Lancet 2002, 360: 1233–1242. 10.1016/S0140-6736(02)11274-8
Pope CA, Burnett RT, Thurston GD, Thun MJ, Calle EE, Krewski D, Godleski JJ: Cardiovascular mortality and long-term exposure to particulate air pollution: epidemiological evidence of general pathophysiological pathways of disease. Circulation 2004, 109: 71–77.
Noah TL, Zhou H, Monaco J, Horvath K, Herbst M, Jaspers I: Tobacco smoke exposure and altered nasal responses to live attenuated influenza virus. Environ Health Perspect 2011, 119: 78–83.
Noah TL, Zhou H, Zhang H, Horvath K, Robinette C, Kesic M, Meyer M, Diaz-Sanchez D, Jaspers I: Diesel exhaust exposure and nasal response to attenuated influenza in normal and allergic volunteers. Am J Respir Crit Care Med 2012, 185: 179–185. 10.1164/rccm.201103-0465OC
Chavez-Galan L, Arenas-Del Angel MC, Zenteno E, Chavez R, Lascurain R: Cell death mechanisms induced by cytotoxic lymphocytes. Cell Mol Immunol 2009, 6: 15–25. 10.1038/cmi.2009.3
Wargnier A, Legrosmaida S, Bosselut R, Bourge JF, Lafaurie C, Ghysdael J, Sasportes M, Paul P: Identification of human granzyme-B promoter regulatory elements interacting with activated T-cell-specific proteins - implication of ikaros and Cbf binding-sites in promoter activation. Proc Natl Acad Sci U S A 1995, 92: 6930–6934. 10.1073/pnas.92.15.6930
Huang C, Bi E, Hu Y, Deng W, Tian Z, Dong C, Sun B: A novel NF-kappaB binding site controls human granzyme B gene transcription. J Immunol 2006, 176: 4173–4181.
Rousalova I, Krepela E: Granzyme B-induced apoptosis in cancer cells and its regulation (Review). Int J Oncol 2010, 37: 1361–1378.
Cao D, Tal TL, Graves LM, Gilmour I, Linak W, Reed W, Bromberg PA, Samet JM: Diesel exhaust particulate-induced activation of Stat3 requires activities of EGFR and Src in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2007, 292: L422-L429.
Tal TL, Simmons SO, Silbajoris R, Dailey L, Cho SH, Ramabhadran R, Linak W, Reed W, Bromberg PA, Samet JM: Differential transcriptional regulation of IL-8 expression by human airway epithelial cells exposed to diesel exhaust particles. Toxicol Appl Pharmacol 2010, 243: 46–54. 10.1016/j.taap.2009.11.011
Jiang K, Zhong B, Gilvary DL, Corliss BC, Hong-Geller E, Wei S, Djeu JY: Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat Immunol 2000, 1: 419–425. 10.1038/80859
Ma CL, Wang J, Luo J: Activation of nuclear factor kappa B by diesel exhaust particles in mouse epidermal cells through phosphatidylinositol 3-kinase/Akt signaling pathway. Biochem Pharmacol 2004, 67: 1975–1983. 10.1016/j.bcp.2004.01.023
Aktas E, Akdis M, Bilgic S, Disch R, Falk CS, Blaser K, Akdis C, Deniz G: Different natural killer (NK) receptor expression and immunoglobulin E (IgE) regulation by NK1 and NK2 cells. Clin Exp Immunol 2005, 140: 301–309. 10.1111/j.1365-2249.2005.02777.x
Biron CA, Brossay L: NK cells and NKT cells in innate defense against viral infections. Curr Opin Immunol 2001, 13: 458–464. 10.1016/S0952-7915(00)00241-7
Walzer T, Dalod M, Robbins SH, Zitvogel L, Vivier E: Natural-killer cells and dendritic cells: "l'union fait la force". Blood 2005, 106: 2252–2258. 10.1182/blood-2005-03-1154
Bratke K, Bottcher B, Leeder K, Schmidt S, Kupper M, Virchow JC Jr, Luttmann W: Increase in granzyme B+ lymphocytes and soluble granzyme B in bronchoalveolar lavage of allergen challenged patients with atopic asthma. Clin Exp Immunol 2004, 136: 542–548. 10.1111/j.1365-2249.2004.02468.x
Moretta A: The dialogue between human natural killer cells and dendritic cells. Curr Opin Immunol 2005, 17: 306–311. 10.1016/j.coi.2005.03.004
Moretta A, Marcenaro E, Sivori S, Della Chiesa M, Vitale M, Moretta L: Early liaisons between cells of the innate immune system in inflamed peripheral tissues. Trends Immunol 2005, 26: 668–675. 10.1016/j.it.2005.09.008
Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, Sallusto F: Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 2004, 5: 1260–1265. 10.1038/ni1138
Walzer T, Vivier E: G-protein-coupled receptors in control of natural killer cell migration. Trends Immunol 2011, 32: 486–492. 10.1016/j.it.2011.05.002
Siren J, Sareneva T, Pirhonen J, Strengell M, Veckman V, Julkunen I, Matikainen S: Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J Gen Virol 2004, 85: 2357–2364. 10.1099/vir.0.80105-0
Sanders CJ, Doherty PC, Thomas PG: Respiratory epithelial cells in innate immunity to influenza virus infection. Cell Tissue Res 2011, 343: 13–21. 10.1007/s00441-010-1043-z
Borchers MT, Harris NL, Wesselkamper SC, Vitucci M, Cosman D: NKG2D ligands are expressed on stressed human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006, 291: L222-L231. 10.1152/ajplung.00327.2005
Cooper MA, Fehniger TA, Caligiuri MA: The biology of human natural killer-cell subsets. Trends Immunol 2001, 22: 633–640. 10.1016/S1471-4906(01)02060-9
Brady J, Carotta S, Thong RP, Chan CJ, Hayakawa Y, Smyth MJ, Nutt SL: The interactions of multiple cytokines control NK cell maturation. J Immunol 2010, 185: 6679–6688. 10.4049/jimmunol.0903354
Brady J, Hayakawa Y, Smyth MJ, Nutt SL: IL-21 induces the functional maturation of murine NK cells. J Immunol 2004, 172: 2048–2058.
Walzer T, Dalod M, Vivier E, Zitvogel L: Natural killer cell-dendritic cell crosstalk in the initiation of immune responses. Expert Opin Biol Ther 2005,5(Suppl 1):S49-S59.
Jacobs BL, Langland JO: When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 1996, 219: 339–349. 10.1006/viro.1996.0259
Borchers MT, Harris NL, Wesselkamper SC, Zhang S, Chen Y, Young L, Lau GW: The NKG2D-activating receptor mediates pulmonary clearance of Pseudomonas aeruginosa. Infect Immun 2006, 74: 2578–2586. 10.1128/IAI.74.5.2578-2586.2006
Harrod KS, Jaramillo RJ, Berger JA, Gigliotti AP, Seilkop SK, Reed MD: Inhaled diesel engine emissions reduce bacterial clearance and exacerbate lung disease to Pseudomonas aeruginosa infection in vivo. Toxicol Sci 2005, 83: 155–165.
Saxena RK, Saxena QB, Weissman DN, Simpson JP, Bledsoe TA, Lewis DM: Effect of diesel exhaust particulate on bacillus Calmette-Guerin lung infection in mice and attendant changes in lung interstitial lymphoid subpopulations and IFNgamma response. Toxicol Sci 2003, 73: 66–71. 10.1093/toxsci/kfg048
Jaspers I, Sheridan PA, Zhang W, Brighton LE, Chason KD, Hua X, Tilley SL: Exacerbation of allergic inflammation in mice exposed to diesel exhaust particles prior to viral infection. Part Fibre Toxicol 2009, 6: 22. 10.1186/1743-8977-6-22
Bauer RN, Brighton LE, Mueller L, Xiang Z, Rager JE, Fry RC, Peden DB, Jaspers I: Influenza enhances caspase-1 in bronchial epithelial cells from asthmatic volunteers and is associated with pathogenesis. J Allergy Clin Immunol 2012, 130: 958–967. e914 10.1016/j.jaci.2012.07.013