MyD88-dependent pro-interleukin-1β induction in dendritic cells exposed to food-grade synthetic amorphous silica

Particle and Fibre Toxicology

Volumn 14, Issue 1, 2017, Pages

  Winkler, Hans Christian ^a,c   Kornprobst, Julian ^a   Wick, Peter ^b   van Moos, Lea Maria ^c   Trantakis, Ioannis ^c   Schraner, Elisabeth Maria ^a   Bathke, Barbara ^d   Hochrein, Hubertus ^d   Suter, Mark ^a   Naegeli, Hanspeter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b SWISS FEDERAL LABORATORIES FOR MATERIALS SCIENCE AND TECHNOLOGY   (Switzerland)

^c ETH ZURICH   (Switzerland)

^d Bavarian Nordic GmbH   (Germany)

Author keywords

E 551; Food additive; Food toxicology; Gut associated lymphoid tissue; Inflammatory bowel disease; Nanomaterial; Silicon dioxide; Synthetic amorphous silica

Indexed keywords

CD40 ANTIGEN; CD69 ANTIGEN; CD86 ANTIGEN; FLT3 LIGAND; INTERLEUKIN 1BETA; IRON PHOSPHORUS OXIDE NANOPARTICLE; L SELECTIN; MYELOID DIFFERENTIATION FACTOR 88; NANOMATERIAL; NANOPARTICLE; SILICON DIOXIDE; TITANIUM DIOXIDE NANOPARTICLE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; FOOD ADDITIVE; IL1B PROTEIN, MOUSE; INFLAMMASOME; MYD88 PROTEIN, MOUSE; PATTERN RECOGNITION RECEPTOR; PROTEIN PRECURSOR; TOLL LIKE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL LYSATE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DENDRITIC CELL; ENDOSOME; ENZYME ACTIVATION; INCUBATION TIME; MOUSE; NONHUMAN; PHYSICAL CHEMISTRY; PHYSICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; DEFICIENCY; DOSE RESPONSE; DRUG EFFECTS; ENDOCYTOSIS; FOOD SAFETY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PROTEIN PROCESSING; RISK ASSESSMENT; SYNTHESIS; TIME FACTOR; ULTRASTRUCTURE; UPREGULATION;

ANIMALS; CELLS, CULTURED; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; ENDOSOMES; FOOD ADDITIVES; FOOD SAFETY; INFLAMMASOMES; INTERLEUKIN-1BETA; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NANOPARTICLES; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, PATTERN RECOGNITION; RISK ASSESSMENT; SIGNAL TRANSDUCTION; SILICON DIOXIDE; TIME FACTORS; TOLL-LIKE RECEPTORS; UP-REGULATION;

EID: 85021216334     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/s12989-017-0202-8     Document Type: Article

References (51)

1. Watowich SS, Liu Y-J. Mechanisms regulating dendritic cell specification and development. Immunol Rev. 2010;238:76-92.
2. Shortman K, Naik SH. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol England. 2007;7:19-30.
3. Bogunovic M, Ginhoux F, Helft J, Shang L, Hashimoto D, Greter M, et al. Origin of the lamina propria dendritic cell network. Immunity. 2009;31:513-25.
4. Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 2009;31:502-12.
5. Pandey S, Kawai T, Akira S. Microbial sensing by Toll-like receptors and intracellular nucleic acid sensors. Cold Spring Harb Perspect Biol. 2015;7:a016246.
6. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol. 2003;21:335-76.
7. Deguine J, Barton GM. MyD88: a central player in innate immune signaling. F1000Prime Rep. 2014;6:97.
8. Warheit DB, Donner EM. Risk assessment strategies for nanoscale and fine-sized titanium dioxide particles: recognizing hazard and exposure issues. Food Chem Toxicol. 2015;85:138-47.
9. Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I, et al. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1α and IL-1β. Proc Natl Acad Sci U S A. 2010;107:19449-54.
10. Evans SM, Ashwood P, Warley A, Berisha F, Thompson RPH, Powell JJ. The role of dietary microparticles and calcium in apoptosis and interleukin-1β release of intestinal macrophages. Gastroenterology. 2002;123:1543-53.
11. Lomer MCE, Thompson RPH, Powell JJ. Fine and ultrafine particles of the diet: influence on the mucosal immune response and association with Crohn's disease. Proc Nutr Soc. 2002;61:123-30.
12. Winter M, Beer H-D, Hornung V, Krämer U, Schins RPF, Förster I. Activation of the inflammasome by amorphous silica and TiO2 nanoparticles in murine dendritic cells. Nanotoxicology. 2011;5:326-40.
13. Yada RY, Buck N, Canady R, DeMerlis C, Duncan T, Janer G, et al. Engineered nanoscale food ingredients: evaluation of current knowledge on material characteristics relevant to uptake from the gastrointestinal tract. Compr Rev Food Sci Food Saf. 2014;13:730-44.
14. Yang Y, Faust JJ, Schoepf J, Hristovski K, Capco DG, Herckes P, et al. Survey of food-grade silica dioxide nanomaterial occurrence, characterization, human gut impacts and fate across its lifecycle. Sci Total Environ. 2016;565:902-12.
15. Dekkers S, Krystek P, Peters RJB, Lankveld DPK, Bokkers BGH, van Hoeven-Arentzen PH, et al. Presence and risks of nanosilica in food products. Nanotoxicology. 2011;5:393-405.
16. Peters R, Kramer E, Oomen AG, Herrera Rivera ZE, Oegema G, Tromp PC, et al. Presence of nano-sized silica during in vitro digestion of foods containing silica as a food additive. ACS Nano. 2012;6:2441-51.
17. Weir A, Westerhoff P, Fabricius L, Hristovski K, von Goetz N. Titanium dioxide nanoparticles in food and personal care products. Environ Sci Technol. 2012;46:2242-50.
18. Hilty FM, Arnold M, Hilbe M, Teleki A, Knijnenburg JTN, Ehrensperger F, et al. Iron from nanocompounds containing iron and zinc is highly bioavailable in rats without tissue accumulation. Nat Nanotechnol. 2010;5:374-80.
19. Rohner F, Ernst FO, Arnold M, Hilbe M, Biebinger R, Ehrensperger F, et al. Synthesis, characterization, and bioavailability in rats of ferric phosphate nanoparticles. J Nutr. 2007;137:614-9.
20. Guo J, Gu N, Chen J, Shi T, Zhou Y, Rong Y, et al. Neutralization of interleukin-1 beta attenuates silica-induced lung inflammation and fibrosis in C57BL/6 mice. Arch Toxicol. 2013;87:1963-73.
21. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science. 2008;320:674-7.
22. Tsugita M, Morimoto N, Nakayama M. SiO2 and TiO2 nanoparticles synergistically trigger macrophage inflammatory responses. Part Fibre Toxicol. 2017;14:11.
23. Netea MG, van de Veerdonk FL, van der Meer JWM, Dinarello CA, Joosten LAB. Inflammasome-independent regulation of IL-1-family cytokines. Annu Rev Immunol. 2015;33:49-77.
24. Gross O, Thomas CJ, Guarda G, Tschopp J. The inflammasome: an integrated view. Immunol Rev. 2011;243:136-51.
25. Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood. 2011;117:3720-32.
26. Rabolli V, Badissi AA, Devosse R, Uwambayinema F, Yakoub Y, Palmai-Pallag M, et al. The alarmin IL-1α is a master cytokine in acute lung inflammation induced by silica micro- and nanoparticles. Part Fibre Toxicol. 2014;11:69.
27. Franchi L, Eigenbrod T, Nunez G. Cutting edge: TNF-alpha mediates sensitization to ATP and silica via the NLRP3 inflammasome in the absence of microbial stimulation. J Immunol. 2009;183:792-6.
28. Hummel TZ, Kindermann A, Stokkers PCF, Benninga MA, ten Kate FJW. Exogenous pigment in Peyer patches of children suspected of having IBD. J Pediatr Gastroenterol Nutr. 2014;58:477-80.
29. Shepherd NA, Crocker PR, Smith AP, Levison DA. Exogenous pigment in Peyer's patches. Hum Pathol. 1987;18:50-4.
30. Powell JJ, Ainley CC, Harvey RS, Mason IM, Kendall MD, Sankey EA, et al. Characterisation of inorganic microparticles in pigment cells of human gut associated lymphoid tissue. Gut. 1996;38:390-5.
31. van der Zande M, Vandebriel RJ, Groot MJ, Kramer E, Herrera Rivera ZE, Rasmussen K, et al. Sub-chronic toxicity study in rats orally exposed to nanostructured silica. Part Fibre Toxicol. 2014;11:8.
32. Xu Y, Zhan Y, Lew AM, Naik SH, Kershaw MH. Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J Immunol. 2007;179:7577-84.
33. Naik SH, O'Keeffe M, Proietto A, Shortman K, Wu L. CD8+, CD8-, and plasmacytoid dendritic cell generation in vitro using flt3 ligand. Methods Mol Biol. 2010;595:167-76.
34. Zucker RM, Massaro EJ, Sanders KM, Degn LL, Boyes WK. Detection of TiO2 nanoparticles in cells by flow cytometry. Cytometry A. 2010;77:677-85.
35. Wang X, Mansukhani ND, Guiney LM, Lee J-H, Li R, Sun B, et al. Toxicological profiling of highly purified metallic and semiconducting single-walled carbon nanotubes in the rodent lung and E. coli. ACS Nano. 2016;10:6008-19.
36. Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med. 1995;182:389-400.
37. Sarkar K, Kruhlak MJ, Erlandsen SL, Shaw S. Selective inhibition by rottlerin of macropinocytosis in monocyte-derived dendritic cells. Immunology. 2005;116:513-24.
38. Rutz M, Metzger J, Gellert T, Luppa P, Lipford GB, Wagner H, et al. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur J Immunol. 2004;34:2541-50.
39. Dalod M, Chelbi R, Malissen B, Lawrence T. Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. EMBO J England. 2014;33:1104-16.
40. Lo RS, Giordano G, Yakoub Y, Devosse R, Uwambayinema F, Couillin I, et al. Uncoupling between inflammatory and fibrotic responses to silica: evidence from MyD88 knockout mice. PLoS One. 2014;9:e99383.
41. Cheers C, Haigh AM, Kelso A, Metcalf D, Stanley ER, Young AM. Production of colony-stimulating factors (CSFs) during infection: separate determinations of macrophage-, granulocyte-, granulocyte-macrophage-, and multi-CSFs. Infect Immun. 1988;56:247-51.
42. Cohen JM, Teeguarden JG, Demokritou P. An integrated approach for the in vitro dosimetry of engineered nanomaterials. Part Fibre Toxicol. 2014;11:20.
43. Hinderliter PM, Minard KR, Orr G, Chrisler WB, Thrall BD, Pounds JG, et al. ISDD: a computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies. Part Fibre Toxicol. 2010;7:36.
44. Zhang HY, Dunphy DR, Jiang XM, Meng H, Sun BB, Tarn D, et al. Processing pathway dependence of amorphous silica nanoparticle toxicity: colloidal vs pyrolytic. J Am Chem Soc. 2012;134:15790-804.
45. Sun B, Pokhrel S, Dunphy DR, Zhang H, Ji Z, Wang X, et al. Reduction of acute inflammatory effects of Fumed silica Nanoparticles in the lung by adjusting Silanol display through Calcination and metal doping. ACS Nano. 2015;9:9357-72.
46. Cohen JM, DeLoid GM, Demokritou P. A critical review of in vitro dosimetry for engineered nanomaterials. Nanomedicine (Lond). 2015;10:3015-32.
47. Winkler HC, Suter M, Naegeli H. Critical review of the safety assessment of nano-structured silica additives in food. J Nanobiotechnol. 2016;14:44.
48. Sepeur S, Laryea N, Goedicke S, Groß F. Nanotechnology: technical basics and applications. Vincentz Network: Hannover; 2008.
49. Smulders S, Kaiser J-P, Zuin S, Van Landuyt KL, Golanski L, Vanoirbeek J, et al. Contamination of nanoparticles by endotoxin: evaluation of different test methods. Part Fibre Toxicol. 2012;9:41.
50. Hochrein H, Schlatter B, O'Keeffe M, Wagner C, Schmitz F, Schiemann M, et al. Herpes simplex virus type-1 induces IFN-alpha production via Toll-like receptor 9-dependent and -independent pathways. Proc Natl Acad Sci U S A. 2004;101:11416-21.
51. Roberts IM. Iso-butanol saturated water: a simple procedure for increasing staining intensity of resin sections for light and electron microscopy. J Microsc. 2002;207:97-107.