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Respiratory Research
Published in: Respiratory Research 1/2010

Open Access 01-12-2010 | Research

Allergen particle binding by human primary bronchial epithelial cells is modulated by surfactant protein D

Authors: Carsten Schleh, Veit J Erpenbeck, Carla Winkler, Hans D Lauenstein, Matthias Nassimi, Armin Braun, Norbert Krug, Jens M Hohlfeld

Published in: Respiratory Research | Issue 1/2010

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Abstract

Background

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. Our previous work demonstrated that SP-D increases the uptake of SPP by alveolar macrophages. In the present study, we investigated the uptake of SPP in human primary epithelial cells and the potential modulation by SP-D. The patho-physiological consequence was evaluated by measurement of pro-inflammatory mediators.

Methods

SPP were isolated from timothy grass and subsequently fluorescently labelled. Human primary bronchial epithelial cells were incubated with SPP or polystyrene particles (PP) in the presence and absence of surfactant protein D. In addition, different sizes and surface charges of the PP were studied. Particle uptake was evaluated by flow cytometry and confocal microscopy. Soluble mediators were measured by enzyme linked immunosorbent assay or bead array.

Results

SPP were taken up by primary epithelial cells in a dose dependent manner. This uptake was coincided with secretion of Interleukin (IL)-8. SP-D increased the fraction of bronchial epithelial cells that bound SPP but not the fraction of cells that internalized SPP. SPP-induced secretion of IL-8 was further increased by SP-D. PP were bound and internalized by epithelial cells but this was not modulated by SP-D.

Conclusions

Epithelial cells bind and internalize SPP and PP which leads to increased IL-8 secretion. SP-D promotes attachment of SPP to epithelial cells and may thus be involved in the inflammatory response to inhaled allergen.
Literature
1.
D'Amato G, Liccardi G, Frenguelli G: Thunderstorm-asthma and pollen allergy. Allergy 2007,62(1):11–16.CrossRefPubMed
2.
Oberdorster G, Oberdorster E, Oberdorster J: Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 2005,113(7):823–839.CrossRefPubMedPubMedCentral
3.
Schleh C, Hohlfeld JM: Interaction of nanoparticles with the pulmonary surfactant system. InhalToxicol 2009,21(S1):97–103.
4.
Frerking I, Gunther A, Seeger W, Pison U: Pulmonary surfactant: functions, abnormalities and therapeutic options. Intensive Care Med 2001,27(11):1699–1717.CrossRefPubMed
5.
Schurch S, Gehr P, Im Hof V, Geiser M, Green F: Surfactant displaces particles toward the epithelium in airways and alveoli. Respir Physiol 1990,80(1):17–32.CrossRefPubMed
6.
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(12):5273–5281.CrossRefPubMed
7.
Kishore U, Greenhough TJ, Waters P, Shrive AK, Ghai R, Kamran MF, Bernal AL, Reid KB, Madan T, Chakraborty T: Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol Immunol 2006,43(9):1293–1315.CrossRefPubMed
8.
Erpenbeck VJ, Malherbe DC, Sommer S, Schmiedl A, Steinhilber W, Ghio AJ, Krug N, Wright JR, Hohlfeld JM: Surfactant protein D increases phagocytosis and aggregation of pollen-allergen starch granules. Am J Physiol Lung Cell Mol Physiol 2005,288(4):L692-L698.CrossRefPubMed
9.
Restrepo CI, Dong Q, Savov J, Mariencheck WI, Wright JR: Surfactant protein D stimulates phagocytosis of Pseudomonas aeruginosa by alveolar macrophages. Am J Respir Cell Mol Biol 1999,21(5):576–585.CrossRefPubMed
10.
Diamond G, Legarda D, Ryan LK: The innate immune response of the respiratory epithelium. Immunol Rev 2000, 173:27–38.CrossRefPubMed
11.
Hammad H, Chieppa M, Perros F, Willart MA, Germain RN, Lambrecht BN: House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 2009,15(4):410–416.CrossRefPubMedPubMedCentral
12.
Pickett G, Seagrave J, Boggs S, Polzin G, Richter P, Tesfaigzi Y: Effects of 10 cigarette smoke condensates on primary human airway epithelial cells by comparative gene and cytokine expression studies. Toxicol Sci 2010,114(1):79–89.CrossRefPubMed
13.
Salvi S, Semper A, Blomberg A, Holloway J, Jaffar Z, Papi A, Teran L, Polosa R, Kelly F, Sandstrom T, et al.: Interleukin-5 production by human airway epithelial cells. Am J Respir Cell Mol Biol 1999,20(5):984–991.CrossRefPubMed
14.
Park SY, Cho JH, Oh DY, Park JW, Ahn MJ, Han JS, Oh JW: House dust mite allergen Der f 2-induced phospholipase D1 activation is critical for the production of interleukin-13 through activating transcription factor-2 activation in human bronchial epithelial cells. J Biol Chem 2009,284(30):20099–20110.CrossRefPubMedPubMedCentral
15.
Dong Q, Wright JR: Degradation of surfactant protein D by alveolar macrophages. Am J Physiol 1998,274(1 Pt 1):L97–105.PubMed
16.
Erpenbeck VJ, Hagenberg A, Dulkys Y, Elsner J, Balder R, Krentel H, Discher M, Braun A, Krug N, Hohlfeld JM: Natural porcine surfactant augments airway inflammation after allergen challenge in patients with asthma. Am J Respir Crit Care Med 2004,169(5):578–586.CrossRefPubMed
17.
Blank F, Rothen-Rutishauser BM, Schurch S, Gehr P: An optimized in vitro model of the respiratory tract wall to study particle cell interactions. J Aerosol Med 2006,19(3):392–405.CrossRefPubMed
18.
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 FibreToxicol 2007, 4:9.
19.
Blume C, Foerster S, Gilles S, Becker WM, Ring J, Behrendt H, Petersen A, Traidl-Hoffmann C: Human Epithelial Cells of the Respiratory Tract and the Skin Differentially Internalize Grass Pollen Allergens. J Invest Dermatol 2009.
20.
Malhotra R, Haurum J, Thiel S, Jensenius JC, Sim RB: Pollen grains bind to lung alveolar type II cells (A549) via lung surfactant protein A (SP-A). BiosciRep 1993,13(2):79–90.
21.
Geunes-Boyer S, Oliver TN, Janbon G, Lodge JK, Heitman J, Perfect JR, Wright JR: Surfactant Protein D increases phagocytosis of hypocapsular Cryptococcus neoformans by murine macrophages and enhances fungal survival. Infect Immun 2009.
22.
Kudo K, Sano H, Takahashi H, Kuronuma K, Yokota S, Fujii N, Shimada K, Yano I, Kumazawa Y, Voelker DR, et al.: Pulmonary collectins enhance phagocytosis of Mycobacterium avium through increased activity of mannose receptor. J Immunol 2004,172(12):7592–7602.CrossRefPubMed
23.
Wright JR: Immunomodulatory functions of surfactant. Physiol Rev 1997,77(4):931–962.PubMed
24.
Honda Y, Takahashi H, Kuroki Y, Akino T, Abe S: Decreased contents of surfactant proteins A and D in BAL fluids of healthy smokers. Chest 1996,109(4):1006–1009.CrossRefPubMed
25.
Erpenbeck VJ, Schmidt R, Gunther A, Krug N, Hohlfeld JM: Surfactant protein levels in bronchoalveolar lavage after segmental allergen challenge in patients with asthma. Allergy 2006,61(5):598–604.CrossRefPubMed
26.
Geiser M: Update on Macrophage Clearance of Inhaled Micro- and Nanoparticles. J Aerosol Med Pulm Drug Deliv 2010.
27.
Holmskov U, Teisner B, Willis AC, Reid KB, Jensenius JC: Purification and characterization of a bovine serum lectin (CL-43) with structural homology to conglutinin and SP-D and carbohydrate specificity similar to mannan-binding protein. J Biol Chem 1993,268(14):10120–10125.PubMed
28.
Petersen A, Becker WM, Moll H, Blumke M, Schlaak M: Studies on the carbohydrate moieties of the timothy grass pollen allergen Phl p I. Electrophoresis 1995,16(5):869–875.CrossRefPubMed
29.
Gardai SJ, Xiao YQ, Dickinson M, Nick JA, Voelker DR, Greene KE, Henson PM: By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 2003,115(1):13–23.CrossRefPubMed
30.
Bajanowski T, Brinkmann B, Stefanec AM, Barckhaus RH, Fechner G: Detection and analysis of tracers in experimental drowning. Int J Legal Med 1998,111(2):57–61.CrossRefPubMed
31.
Geiser M, Rothen-Rutishauser B, Kapp N, Schurch S, Kreyling W, Schulz H, Semmler M, Im HV, Heyder J, Gehr P: Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and in cultured cells. Environ Health Perspect 2005,113(11):1555–1560.CrossRefPubMedPubMedCentral
32.
Churg A, Stevens B, Wright JL: Comparison of the uptake of fine and ultrafine TiO2 in a tracheal explant system. Am J Physiol 1998,274(1 Pt 1):L81-L86.PubMed
33.
Kreyling WG, Semmler M, Erbe F, Mayer P, Takenaka S, Schulz H, Oberdorster G, Ziesenis A: Translocation of ultrafine insoluble iridium particles from lung epithelium to extrapulmonary organs is size dependent but very low. J Toxicol Environ Health A 2002,65(20):1513–1530.CrossRefPubMed
34.
Semmler-Behnke M, Kreyling WG, Lipka J, Fertsch S, Wenk A, Takenaka S, Schmid G, Brandau W: Biodistribution of 1.4- and 18-nm gold particles in rats. Small 2008,4(12):2108–2111.CrossRefPubMed
35.
36.
Andersson K, Lidholm J: Characteristics and immunobiology of grass pollen allergens. Int Arch Allergy Immunol 2003,130(2):87–107.CrossRefPubMed
37.
Kato T, Yashiro T, Murata Y, Herbert DC, Oshikawa K, Bando M, Ohno S, Sugiyama Y: Evidence that exogenous substances can be phagocytized by alveolar epithelial cells and transported into blood capillaries. Cell Tissue Res 2003,311(1):47–51.CrossRefPubMed
38.
Schins RP, Duffin R, Hohr D, Knaapen AM, Shi T, Weishaupt C, Stone V, Donaldson K, Borm PJ: Surface modification of quartz inhibits toxicity, particle uptake, and oxidative DNA damage in human lung epithelial cells. Chem Res Toxicol 2002,15(9):1166–1173.CrossRefPubMed
39.
Nardone LL, Andrews SB: Cell line A549 as a model of the type II pneumocyte. Phospholipid biosynthesis from native and organometallic precursors. BiochimBiophysActa 1979,573(2):276–295.
40.
Dailey LA, Kleemann E, Merdan T, Petersen H, Schmehl T, Gessler T, Hanze J, Seeger W, Kissel T: Modified polyethylenimines as non viral gene delivery systems for aerosol therapy: effects of nebulization on cellular uptake and transfection efficiency. J Control Release 2004,100(3):425–436.CrossRefPubMed
41.
Foster KA, Yazdanian M, Audus KL: Microparticulate uptake mechanisms of in-vitro cell culture models of the respiratory epithelium. J Pharm Pharmacol 2001,53(1):57–66.CrossRefPubMed
42.
Elfinger M, Maucksch C, Rudolph C: Characterization of lactoferrin as a targeting ligand for nonviral gene delivery to airway epithelial cells. Biomaterials 2007,28(23):3448–3455.CrossRefPubMed
43.
Chiu LL, Perng DW, Yu CH, Su SN, Chow LP: Mold allergen, pen C 13, induces IL-8 expression in human airway epithelial cells by activating protease-activated receptor 1 and 2. J Immunol 2007,178(8):5237–5244.CrossRefPubMed
44.
Nukada Y, Miyazawa M, Kosaka N, Ito Y, Sakaguchi H, Nishiyama N: Production of IL-8 in THP-1 cells following contact allergen stimulation via mitogen-activated protein kinase activation or tumor necrosis factor-alpha production. J Toxicol Sci 2008,33(2):175–185.CrossRefPubMed
45.
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(3):365–371.CrossRefPubMed
46.
Roschmann K, Farhat K, Konig P, Suck R, Ulmer AJ, Petersen A: Timothy grass pollen major allergen Phl p 1 activates respiratory epithelial cells by a non-protease mechanism. Clin Exp Allergy 2009,39(9):1358–1369.CrossRefPubMed
47.
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(3):191–199.CrossRefPubMed
48.
Diabate S, Mulhopt S, Paur HR, Krug HF: The response of a co-culture lung model to fine and ultrafine particles of incinerator fly ash at the air-liquid interface. AlternLab Anim 2008,36(3):285–298.
49.
Alam R, Forsythe PA, Lett-Brown MA, Grant JA: Interleukin-8 and RANTES inhibit basophil histamine release induced with monocyte chemotactic and activating factor/monocyte chemoattractant peptide-1 and histamine releasing factor. Am J Respir Cell Mol Biol 1992,7(4):427–433.CrossRefPubMed
50.
Kimata H, Lindley I, Furusho K: Selective inhibition of spontaneous IgE and IgG4 production by interleukin-8 in atopic patients. Blood 1995,85(11):3191–3198.PubMed
51.
Mahajan L, Madan T, Kamal N, Singh VK, Sim RB, Telang SD, Ramchand CN, Waters P, Kishore U, Sarma PU: Recombinant surfactant protein-D selectively increases apoptosis in eosinophils of allergic asthmatics and enhances uptake of apoptotic eosinophils by macrophages. Int Immunol 2008,20(8):993–1007.CrossRefPubMed
Metadata
Title
Allergen particle binding by human primary bronchial epithelial cells is modulated by surfactant protein D
Authors
Carsten Schleh
Veit J Erpenbeck
Carla Winkler
Hans D Lauenstein
Matthias Nassimi
Armin Braun
Norbert Krug
Jens M Hohlfeld
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2010
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/1465-9921-11-83

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