Surfactant Protein D modulates allergen particle uptake and inflammatory response in a human epithelial airway model
Tóm tắt
Allergen-containing subpollen particles (SPP) are released from whole plant pollen upon contact with water or even high humidity. Because of their size SPP can preferentially reach the lower airways where they come into contact with surfactant protein (SP)-D. The aim of the present study was to investigate the influence of SP-D in a complex three-dimensional human epithelial airway model, which simulates the most important barrier functions of the epithelial airway. The uptake of SPP as well as the secretion of pro-inflammatory cytokines was investigated. SPP were isolated from timothy grass and subsequently fluorescently labeled. A human epithelial airway model was built by using human Type II-pneumocyte like cells (A549 cells), human monocyte derived macrophages as well as human monocyte derived dendritic cells. The epithelial cell model was incubated with SPP in the presence and absence of surfactant protein D. Particle uptake was evaluated by confocal microscopy and advanced computer-controlled analysis. Finally, human primary CD4+ T-Cells were added to the epithelial airway model and soluble mediators were measured by enzyme linked immunosorbent assay or bead array. SPP were taken up by epithelial cells, macrophages, and dendritic cells. This uptake coincided with secretion of pro-inflammatory cytokines and chemokines. SP-D modulated the uptake of SPP in a cell type specific way (e.g. increased number of macrophages and epithelial cells, which participated in allergen particle uptake) and led to a decreased secretion of pro-inflammatory cytokines. These results display a possible mechanism of how SP-D can modulate the inflammatory response to inhaled allergen.
Tài liệu tham khảo
Taylor PE, Jacobson KW, House JM, Glovsky MM: Links between pollen, atopy and the asthma epidemic. Int Arch Allergy Immunol. 2007, 144: 162-170. 10.1159/000103230.
D'Amato G, Liccardi G, Frenguelli G: Thunderstorm-asthma and pollen allergy. Allergy. 2007, 62: 11-16. 10.1111/j.1398-9995.2006.01271.x.
Oberdorster G, Oberdorster E, Oberdorster J: Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect. 2005, 113: 823-839. 10.1289/ehp.7339.
Schurch S, Gehr P, Im H, Geiser M, Green F: Surfactant displaces particles toward the epithelium in airways and alveoli. Respir Physiol. 1990, 80: 17-32. 10.1016/0034-5687(90)90003-H.
Gerber PJ, Lehmann C, Gehr P, Schurch S: Wetting and spreading of a surfactant film on solid particles: influence of sharp edges and surface irregularities. Langmuir. 2006, 22: 5273-5281. 10.1021/la0526683.
Erpenbeck VJ, Malherbe DC, Sommer S, Schmiedl A, Steinhilber W, Ghio AJ, et al: Surfactant protein D increases phagocytosis and aggregation of pollen-allergen starch granules. Am J Physiol Lung Cell Mol Physiol. 2005, 288: L692-L698.
Kishore U, Greenhough TJ, Waters P, Shrive AK, Ghai R, Kamran MF, et al: Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol Immunol. 2006, 43: 1293-1315. 10.1016/j.molimm.2005.08.004.
Guo CJ, Atochina-Vasserman EN, Abramova E, Foley JP, Zaman A, Crouch E, et al: S-nitrosylation of surfactant protein-D controls inflammatory function. PLoS Biol. 2008, 6: e266-10.1371/journal.pbio.0060266.
Schleh C, Erpenbeck VJ, Winkler C, Lauenstein HD, Nassimi M, Braun A, et al: Allergen particle binding by human primary bronchial epithelial cells is modulated by surfactant protein D. Respir Res. 2010, 11: 83-10.1186/1465-9921-11-83.
Lambrecht BN: Dendritic cells and the regulation of the allergic immune response. Allergy. 2005, 60: 271-282. 10.1111/j.1398-9995.2005.00708.x.
Winkler C, Huper K, Wedekind AC, Rochlitzer S, Hartwig C, Muller M, et al: Surfactant protein D modulates pulmonary clearance of pollen starch granules. Exp Lung Res. 2010, 36: 522-530. 10.3109/01902141003790148.
Upham JW, Stick SM: Interactions between airway epithelial cells and dendritic cells: implications for the regulation of airway inflammation. Curr Drug Targets. 2006, 7: 541-545. 10.2174/138945006776818647.
Darveau ME, Jacques E, Rouabhia M, Hamid Q, Chakir J: Increased T-cell survival by structural bronchial cells derived from asthmatic subjects cultured in an engineered human mucosa. J Allergy Clin Immunol. 2008, 121: 692-699. 10.1016/j.jaci.2007.11.023.
Ishii H, Hayashi S, Hogg JC, Fujii T, Goto Y, Sakamoto N, et al: Alveolar macrophage-epithelial cell interaction following exposure to atmospheric particles induces the release of mediators involved in monocyte mobilization and recruitment. Respir Res. 2005, 6: 87-10.1186/1465-9921-6-87.
Boitano S, Safdar Z, Welsh DG, Bhattacharya J, Koval M: Cell-cell interactions in regulating lung function. Am J Physiol Lung Cell Mol Physiol. 2004, 287: L455-L459. 10.1152/ajplung.00172.2004.
Blank F, Rothen-Rutishauser B, Gehr P: Dendritic cells and macrophages form a transepithelial network against foreign particulate antigens. Am J Respir Cell Mol Biol. 2007, 36: 669-677. 10.1165/rcmb.2006-0234OC.
Rothen-Rutishauser B, Mueller L, Blank F, Brandenberger C, Muehlfeld C, Gehr P: A newly developed in vitro model of the human epithelial airway barrier to study the toxic potential of nanoparticles. ALTEX. 2008, 25: 191-196.
Rothen-Rutishauser B, Muhlfeld C, Blank F, Musso C, Gehr P: Translocation of particles and inflammatory responses after exposure to fine particles and nanoparticles in an epithelial airway model. Part Fibre Toxicol. 2007, 4: 9-10.1186/1743-8977-4-9.
Blank F, Wehrli M, Lehmann A, Baum O, Gehr P, von GC, et al: Macrophages and dendritic cells express tight junction proteins and exchange particles in an in vitro model of the human airway wall. Immunobiology. 2011, 216: 86-95. 10.1016/j.imbio.2010.02.006.
Dong Q, Wright JR: Degradation of surfactant protein D by alveolar macrophages. Am J Physiol. 1998, 274: L97-105.
Rothen-Rutishauser B, Muhlfeld C, Blank F, Musso C, Gehr P: Translocation of particles and inflammatory responses after exposure to fine particles and nanoparticles in an epithelial airway model. Part Fibre Toxicol. 2007, 4: 9-10.1186/1743-8977-4-9.
Brandenberger C, Rothen-Rutishauser B, Blank F, Gehr P, Muhlfeld C: Particles induce apical plasma membrane enlargement in epithelial lung cell line depending on particle surface area dose. Respir Res. 2009, 10: 22-10.1186/1465-9921-10-22.
Lehmann AD, Parak WJ, Zhang F, Ali Z, Rocker C, Nienhaus GU, et al: Hybrid nanoparticles: Fluorescent-Magnetic Hybrid Nanoparticles Induce a Dose-Dependent Increase in Proinflammatory Response in Lung Cells in vitro Correlated with Intracellular Localization Small 6/2010. Small. 2010, 6:
Wright JR: Immunoregulatory functions of surfactant proteins. Nat Rev Immunol. 2005, 5: 58-68. 10.1038/nri1528.
Ikegami M, Na CL, Korfhagen TR, Whitsett JA: Surfactant protein D influences surfactant ultrastructure and uptake by alveolar type II cells. Am J Physiol Lung Cell Mol Physiol. 2005, 288: L552-L561. 10.1152/ajplung.00142.2004.
Kato T, Takai T, Fujimura T, Matsuoka H, Ogawa T, Murayama K, et al: Mite serine protease activates protease-activated receptor-2 and induces cytokine release in human keratinocytes. Allergy. 2009
Spiekstra SW, Toebak MJ, Sampat-Sardjoepersad S, van Beek PJ, Boorsma DM, Stoof TJ, et al: Induction of cytokine (interleukin-1alpha and tumor necrosis factor-alpha) and chemokine (CCL20, CCL27, and CXCL8) alarm signals after allergen and irritant exposure. Exp Dermatol. 2005, 14: 109-116. 10.1111/j.0906-6705.2005.00226.x.
Lehto M, Kotovuori A, Palosuo K, Varjonen E, Lehtimaki S, Kalkkinen N, et al: Hev b 6.01 and Hev b 5 induce pro-inflammatory cytokines and chemokines from peripheral blood mononuclear cells in latex allergy. Clin Exp Allergy. 2007, 37: 133-140. 10.1111/j.1365-2222.2006.02622.x.
Maeda S, Maeda S, Shibata S, Chimura N, Fukata T: House dust mite major allergen Der f 1 enhances proinflammatory cytokine and chemokine gene expression in a cell line of canine epidermal keratinocytes. Vet Immunol Immunopathol. 2009
Lee JS, Kim IS, Ryu JS, Yun CY: House dust mite, Dermatophagoides pteronissinus increases expression of MCP-1, IL-6, and IL-8 in human monocytic THP-1 cells. Cytokine. 2008, 42: 365-371. 10.1016/j.cyto.2008.03.010.
Rothen-Rutishauser B, Muhlfeld C, Blank F, Musso C, Gehr P: Translocation of particles and inflammatory responses after exposure to fine particles and nanoparticles in an epithelial airway model. Part Fibre Toxicol. 2007, 4: 9-10.1186/1743-8977-4-9.
Brown DM, Wilson MR, MacNee W, Stone V, Donaldson K: Size-dependent proinflammatory effects of ultrafine polystyrene particles: a role for surface area and oxidative stress in the enhanced activity of ultrafines. Toxicol Appl Pharmacol. 2001, 175: 191-199. 10.1006/taap.2001.9240.
Lehmann AD, Blank F, Baum O, Gehr P, Rothen-Rutishauser BM: Diesel exhaust particles modulate the tight junction protein occludin in lung cells in vitro. Part Fibre Toxicol. 2009, 6: 26-10.1186/1743-8977-6-26.
Muller L, Riediker M, Wick P, Mohr M, Gehr P, Rothen-Rutishauser B: Oxidative stress and inflammation response after nanoparticle exposure: differences between human lung cell monocultures and an advanced three-dimensional model of the human epithelial airways. J R Soc Interface. 2010, 7 (Suppl 1): S27-S40.
Blank F, Rothen-Rutishauser B, Gehr P: Dendritic cells and macrophages form a transepithelial network against foreign particulate antigens. Am J Respir Cell Mol Biol. 2007, 36: 669-677. 10.1165/rcmb.2006-0234OC.
Blank F, Wehrli M, Lehmann A, Baum O, Gehr P, Von GC, et al: Macrophages and dendritic cells express tight junction proteins and exchange particles in an in vitro model of the human airway wall. Immunobiology. 2011, 216: 86-95. 10.1016/j.imbio.2010.02.006.