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Titanium Dioxide Nanoparticles Exacerbate DSS-Induced Colitis

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Titanium Dioxide Nanoparticles Exacerbate DSS-Induced Colitis Inflammatory bowel disease ORIGINAL ARTICLE Gut: first published as 10.1136/gutjnl-2015-310297 on 4 February 2016. Downloaded from Titanium dioxide nanoparticles exacerbate DSS-induced colitis: role of the NLRP3 inflammasome Pedro A Ruiz,1 Belen Morón,1 Helen M Becker,1 Silvia Lang,1 Kirstin Atrott,1 Marianne R Spalinger,1 Michael Scharl,1,2 Kacper A Wojtal,1 Anne Fischbeck-Terhalle,1 Isabelle Frey-Wagner,1 Martin Hausmann,1 Thomas Kraemer,3 Gerhard Rogler1,2 ► Additional material is ABSTRACT published online only. To view Objective Western lifestyle and diet are major Significance of this study please visit the journal online environmental factors playing a role in the development (http://dx.doi.org/10.1136/ gutjnl-2015-310297). of IBD. Titanium dioxide (TiO2) nanoparticles are widely 1 used as food additives or in pharmaceutical formulations What is already known on this subject? Division of Gastroenterology and are consumed by millions of people on a daily basis. ▸ and Hepatology, University of Titanium dioxide induces reactive oxygen Zurich, Zurich, Switzerland We investigated the effects of TiO2 in the development species (ROS) formation as well as 2Zurich Center for Integrative of colitis and the role of the nucleotide-binding inflammation in vitro and in vivo. Human Physiology, University of oligomerisation domain receptor, pyrin domain ▸ The nucleotide-binding oligomerisation domain Zurich, Zurich, Switzerland fl 3 containing (NLRP)3 in ammasome. receptor, pyrin domain containing (NLRP)3 Department of Forensic fi fl Pharmacology and Toxicology, Design Wild-type and NLRP3-de cient mice with in ammasome is activated in the presence of Institute of Forensic Medicine, dextran sodium sulfate-induced colitis were orally titanium dioxide. University of Zurich, Zurich, administered with TiO2 nanoparticles. The ▸ Polymorphisms in the Nlrp3 gene have been Switzerland fl proin ammatory effects of TiO2 particles in cultured linked to the development of Crohn’s Disease. human intestinal epithelial cells (IECs) and macrophages Correspondence to were also studied, as well as the ability of TiO crystals What are the new findings? Professor Dr Gerhard Rogler, 2 to traverse IEC monolayers and accumulate in the blood ▸ Oral administration of titanium dioxide Division of Gastroenterology fl and Hepatology, University of of patients with IBD using inductively coupled plasma nanoparticles worsens intestinal in ammation Zurich, Raemistrasse 100, Zurich in the dextran sodium sulfate (DSS) mouse mass spectrometry. http://gut.bmj.com/ 8091, Switzerland; model of colitis. Results Oral administration of TiO2 nanoparticles [email protected] worsened acute colitis through a mechanism involving ▸ Titanium dioxide crystals accumulate in the fl spleen of DSS-treated mice following oral PAR, BM and HMB have the NLRP3 in ammasome. Importantly, crystals were gavage. contributed equally found to accumulate in spleen of TiO2-administered ▸ Titanium dioxide particles accumulate and mice. In vitro, TiO2 particles were taken up by IECs and Received 6 July 2015 macrophages and triggered NLRP3-ASC-caspase-1 activate the NLRP3 inflammasome in human Revised 19 January 2016 intestinal epithelial cells and macrophages. on September 25, 2021 by guest. Protected copyright. Accepted 20 January 2016 assembly, caspase-1 cleavage and the release of NLRP3- β ▸ Levels of titanium are increased in the blood of Published Online First associated interleukin (IL)-1 and IL-18. TiO2 also 16 March 2016 induced reactive oxygen species generation and patients with IBD. increased epithelial permeability in IEC monolayers. How might it impact on clinical practice in Increased levels of titanium were found in blood of the foreseeable future? patients with UC having active disease. ▸ fl fi Components of the in ammasome may Conclusion These ndings indicate that individuals represent novel therapeutic targets for the with a defective intestinal barrier function and pre- fl treatment of IBD. existing in ammatory condition, such as IBD, might be ▸ Our results suggest a cautionary use of negatively impacted by the use of TiO2 nanoparticles. titanium dioxide in pharmaceutical formulations and support a therapeutic benefitfromlow inorganic particle diet in patients with IBD. INTRODUCTION The aetiology of IBD remains only partially under- stood; however, it is now accepted that both triggers are the increased hygiene and ‘Western Crohn’s disease (CD) and UC are caused by inter- diet’, which includes ingestion of nanoparticles.56 play of genetic and environmental factors that Inorganic nanoparticles and microparticles are trigger an inappropriate immune response.12The used as additives to influence the appearance of a incidence of IBD is increasing in many nations dietary product. The most commonly used addi- To cite: Ruiz PA, Morón B, undergoing ‘westernisation’, supporting an import- tives are submicron-sized (100–1000 nm diameter) Becker HM, et al. Gut ant role of environmental factors during IBD particles of titanium dioxide (TiO2, E171) and alu- 2017;66:1216–1224. pathogenesis.34Among those environmental minium silicate (E559). Food and pharma grade 1216 Ruiz PA, et al. Gut 2017;66:1216–1224. doi:10.1136/gutjnl-2015-310297 Inflammatory bowel disease TiO2 is found both in its bulk form and as nanoparticle. In fact, suggesting that TiO2 nanoparticles could pose a specific risk to at least 36% of the TiO2 particles present in food consists of patients with IBD. Gut: first published as 10.1136/gutjnl-2015-310297 on 4 February 2016. Downloaded from nanoparticles with a particle diameter less than 100 nm.7 The daily intake of TiO2 was estimated by the European Food Safety MATERIAL AND METHODS Authorities in 2004 to be 1.28 mg/kg bodyweight.8 Further to Mouse experiments this, in a dietary study assessing the TiO2 consumption of Acute colitis was induced in female WT (C57BL/6J) and − − patients with CD and healthy volunteers Lomer et al9 estimated Nlrp3 / mice between 12 and 14 weeks of age by oral adminis- 30 that the median individual TiO2 intake in both groups was tration of 1.5% DSS (MP Biomedicals) in drinking water ad 2.5 mg/day. A later study estimated a daily intake of TiO2 food libitum for 7 days. A suspension of TiO2 nanoparticles (rutile, 7 grade of 0.2–2 mg/kg bodyweight, evidencing that TiO2 is 30–50 nm, IoLiTec) in drinking water was administered daily by ingested in substantial amounts on a daily basis. To date, no oral gavage. WT mice were divided in three groups of 12 mice restrictions for the use of TiO2 are enforced by food safety each, and received water, 50 or 500 mg TiO2/day/kg body- −/− authorities and only good manufacturing practice guidelines weight. Nlrp3 mice received water (n=10) or 500 mg TiO2/ limit the use of these compounds.10 11 An increasing body of lit- day/kg bodyweight (n=10). On day 8, colitis was assessed by erature has revealed that exposure to TiO2 can cause adverse endoscopy and mice were sacrificed for sample collection. All effects, including the production of reactive oxygen species the animal experiments were approved by the veterinary author- (ROS),12 inflammatory responses and tumour formation.13 In ities of Zurich, Switzerland. mice, TiO2 nanoparticles cause genotoxic effects in blood cells, bone marrow and liver, and DNA deletions in the offspring.14 Colonoscopy and determination of histological score Cytotoxic effects resulting from TiO2-induced production of Animals were anaesthetised intraperitoneally with a mixture of ROS were observed in human lymphoblastoid cells,15 fibro- ketamine 90–120 mg/kg bodyweight (Vétoquinol) and xylazine blasts, bronchial epithelial cells16 and alveolar macrophages,17 8 mg/kg bodyweight (Bayer), and colonoscopy was performed 31 which led to the classification of TiO2 as ‘possibly carcinogenic as described previously. Animals were sacrificed and colon for humans’. Nanoparticles can accumulate in several organs, length was measured. About 1 cm of tissue was removed from such as kidney, lung, brain, liver and spleen.18 19 In intestinal the distal third of the colon and fixed in 4% formalin overnight. biopsies, dark aggregates of TiO2 were detected in M-cells of H&E stained sections of the paraffin-embedded tissue were Peyer’s patches and in underlying macrophages.20 Interestingly, used for histological analysis. Histological score was determined 32 33 these sites of TiO2 uptake correspond to regions where first as described previously by two independent, blinded signs of inflammation in patients with CD manifest.21 investigators. Nucleotide-binding oligomerisation domain receptor, pyrin domain containing (NLRP)3 is a member of the Nod-like recep- Western blotting and co-immunoprecipitation tor (NLR) family that regulates the activation of caspase-1 by Total protein from cell monolayers was harvested into M-PER forming signalling complexes called ‘inflammasomes’. On acti- lysis buffer (Thermo Fisher Scientific) and western blotting was vation, NLRP3 binds to the apoptosis-associated speck-like performed to determine the expression of NLRP3 (Enzo life protein containing a caspase recruitment domain (ASC) adapter sciences), caspase-1, ASC, IL-1β (Cell Signaling Technologies) http://gut.bmj.com/ protein, which in turn recruits and activates caspase-1. Activated and IL-18 (MBL). Co-immunoprecipitation (Co-IP) was caspase-1 cleaves pro-interleukin (IL)-1β and pro-IL-18 into performed overnight at 4°C using NLRP3 antibody. their biologically active forms.22 23 Single nucleotide poly- Immunocomplexes were collected with Protein G Sepharose morphisms in the Nlrp3 gene have been linked to the develop- beads (GE Healthcare) for 1 h at 4°C prior to western blotting. ment of CD.24 NLRP3 has been shown to be activated by a wide range of pathogens and intrinsic danger signals like ATP,25 Microscopy of spleen cryosections and Caco-2 monolayers ROS, crystalline monosodium urate,26 cholesterol crystals27 and Confocal reflection microscopy was combined with fluorescence on September 25, 2021 by guest. Protected copyright. inorganic materials like aluminium salts,28 asbestos and silica microscopy in a Leica SP8 laser scanning confocal microscope, as 29 28 crystals.
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