An in vitro alveolar macrophage assay for predicting the short-term inhalation toxicity of nanomaterials

Wiemann, Martin; Vennemann, Antje; Sauer, Ursula G.; Wiench, Karin; Ma-Hock, Lan; Landsiedel, Robert

doi:10.1186/s12951-016-0164-2

Cited by 152Nanoparticles: synthesis and applicationsOccupational and environmental lung diseasesImmunotoxicology and immune responses

An in vitro alveolar macrophage assay for predicting the short-term inhalation toxicity of nanomaterials

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Wiemann, Martin, Vennemann, Antje, Sauer, Ursula G., Wiench, Karin, Ma-Hock, Lan, Landsiedel, Robert·2016·Journal of Nanobiotechnology

DOI 10.1186/s12951-016-0164-2PMC PMC4779246

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Abstract

BACKGROUND: Most in vitro studies investigating nanomaterial pulmonary toxicity poorly correlate to in vivo inhalation studies. Alveolar macrophages (AMs) play an outstanding role during inhalation exposure since they effectively clear the alveoli from particles. This study addresses the applicability of an in vitro alveolar macrophage assay to distinguish biologically active from passive nanomaterials. METHODS: Rat NR8383 alveolar macrophages were exposed to 18 inorganic nanomaterials, covering AlOOH, BaSO4, CeO2, Fe2O3, TiO2, ZrO2, and ZnO NMs, amorphous SiO2 and graphite nanoplatelets, and two nanosized organic pigments. ZrO2 and amorphous SiO2 were tested without and with surface functionalization. Non-nanosized quartz DQ12 and corundum were used as positive and negative controls, respectively. The test materials were incubated with the cells in protein-free culture medium. Lactate dehydrogenase, glucuronidase, and tumour necrosis factor alpha were assessed after 16 h. In parallel, H2O2 was assessed after 1.5 h. Using the no-observed-adverse-effect concentrations (NOAECs) from available rat short-term inhalation studies (STIS), the test materials were categorized as active (NOAEC < 10 mg/m(3)) or passive. RESULTS: In vitro data reflected the STIS categorization if a particle surface area-based threshold of <6000 mm(2)/mL was used to determine the biological relevance of the lowest observed significant in vitro effects. Significant effects that were recorded above this threshold were assessed as resulting from test material-unspecific cellular 'overload'. Test materials were assessed as active if ≥2 of the 4 in vitro parameters undercut this threshold. They were assessed as passive if 0 or 1 parameter was altered. An overall assay accuracy of 95 % was achieved. CONCLUSIONS: The in vitro NR8383 alveolar macrophage assay allows distinguishing active from passive nanomaterials. Thereby, it allows determining whether in vivo short-term inhalation testing is necessary for hazard assessment. Results may also be used to group nanomaterials by biological activity. Further work should aim at validating the assay.

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The biological responses of NR8383 cells to nanomaterials are well documented and correlate with in vivo outcomes, supporting their use as a predictive model.
“The biological responses of NR8383 cells to nanomaterials are well documented and have been shown to correlate with in vivo outcomes [28]. This supports their use as a predictive model and contributes to the reduction and refinement of animal experiments.”
From Macrophages bend long fibres with flexural rigidity lower than 3 mN·nm2 to avoid frustrated phagocytosis (2026) · cites this paper as [28]
Human alveolar macrophages are larger than rat alveolar macrophages, with mean diameters of approximately 21.2 ± 0.3 μm and 13.1 ± 2.5 μm, respectively.
“On average, human alveolar macrophages are larger than rat alveolar macrophages, with mean diameters of approximately 21.2 ± 0.3 μm and 13.1 ± 2.5 μm, respectively [28, 45].”
From Macrophages bend long fibres with flexural rigidity lower than 3 mN·nm2 to avoid frustrated phagocytosis (2026) · cites this paper as [28]
At the stalled stage, the internalized portion of the fibre measured ca. 26 μm, roughly twice the size of a typical NR8383 macrophage in its detached and rounded state (12.5-12.8 μm).
“At this stage, the internalized portion of the fibre measured ca. 26 μm, which is roughly twice the size of a typical NR8383 macrophage in its detached and rounded state (12.5 –12.8 μm) [28].”
From Macrophages bend long fibres with flexural rigidity lower than 3 mN·nm2 to avoid frustrated phagocytosis (2026) · cites this paper as [28]

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[1]Regulation (EC) No 1907/2006 of the European Parliament and of the Council of 18 December 2006 concerning the Registration, Evaluation, Authorisation and Restriction of Chemicals (REACH), establishing a European Chemicals Agency, amending Directive 1999/45/EC and repealing Council Regulation (EEC) No 793/93 and Commission Regulation (EC) No 1488/94 as well as Council Directive 76/769/EEC and Commission Directives 91/155/EEC, 93/67/EEC, 93/105/EC and 2000/21/EC. OJ L. 2006;396:1.
[2]EU Commission recommendation on the definition of nanomaterial. OJ L 2011;275:38.
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[91]Schippritt D Lipinski HG Wiemann M Wohlleben W Kuhlbusch T Schnekenburger J Lehr C-M Measurement of nanoparticle uptake by alveolar macrophages: A new approach based on quantitative image analysis Nanomaterials Throughout their Lifecycles: Safety 2014 Boca Raton Human Hazard and Exposure. Taylor & Francis
[114]Landsiedel R, Schnekenburger J, Alessandrini F, Buesen R, Haase A, Luch A, Ma-Hock L, Wiemann M. nanoGEM final project report (Gemeinsamer Abschlussbericht nanoGEM). Chapter 6. Work package 4 (AP4): Nanoparticle toxicology: Material properties and effects. 2014. doi:10.2314/GBV:82774322X(project report in German). · DOI

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A multi-omics approach reveals mechanisms of nanomaterial toxicity and structure–activity relationships in alveolar macrophages
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Toxicity assessment of metal oxide nanomaterials using in vitro screening and murine acute inhalation studies
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Perilous paradigm of graphene oxide and its derivatives in biomedical applications: Insight to immunocompatibility
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Nanomaterial categorization by surface reactivity: A case study comparing 35 materials with four different test methods
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Review of New Approach Methodologies for Application in Risk Assessment of Nanoparticles in the Food and Feed Sector: Status and Challenges
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Subtoxic cell responses to silica particles with different size and shape
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An inter-laboratory effort to harmonize the cell-delivered in vitro dose of aerosolized materials
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Methodological considerations when conducting in vitro , air–liquid interface exposures to engineered nanoparticle aerosols
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Pulmonary toxicity in rats following inhalation exposure to poorly soluble particles: The issue of impaired clearance and the relevance for human health hazard and risk assessment
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Surface reactivity measurements as required for grouping and read-across: An advanced FRAS protocol
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Refining in vitro models for nanomaterial exposure to cells and tissues
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Toxicity mechanism of engineered nanomaterials: Focus on mitochondria
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Parametric Optimization of an Air–Liquid Interface System for Flow-Through Inhalation Exposure to Nanoparticles: Assessing Dosimetry and Intracellular Uptake of CeO2 Nanoparticles
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Comparison of quantitation methods in proteomics to define relevant toxicological information on AhR activation of HepG2 cells by BaP
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The Use of Nanomaterial In Vivo Organ Burden Data for In Vitro Dose Setting
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Assessing the in vitro toxicity of airborne (nano)particles to the human respiratory system: from basic to advanced models
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Revisiting the stress paradigm for silica nanoparticles: decoupling of the anti-oxidative defense, pro-inflammatory response and cytotoxicity
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An in-depth multi-omics analysis in RLE-6TN rat alveolar epithelial cells allows for nanomaterial categorization
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A quantitative framework to group nanoscale and microscale particles by hazard potency to derive occupational exposure limits: Proof of concept evaluation
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In Vitro and In Vivo Short-Term Pulmonary Toxicity of Differently Sized Colloidal Amorphous SiO2
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Effects of Ultrasonic Dispersion Energy on the Preparation of Amorphous SiO2 Nanomaterials for In Vitro Toxicity Testing
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Nanomaterials induce different levels of oxidative stress, depending on the used model system: Comparison of in vitro and in vivo effects
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Barium sulfate micro- and nanoparticles as bioinert reference material in particle toxicology
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Comparing α-Quartz-Induced Cytotoxicity and Interleukin-8 Release in Pulmonary Mono- and Co-Cultures Exposed under Submerged and Air-Liquid Interface Conditions
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Differences in the toxicity of cerium dioxide nanomaterials after inhalation can be explained by lung deposition, animal species and nanoforms
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Rationale and decision rules behind the ECETOC NanoApp to support registration of sets of similar nanoforms within REACH
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Systematic Review of Multi-Omics Approaches to Investigate Toxicological Effects in Macrophages
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Protein and lipid homeostasis altered in rat macrophages after exposure to metallic oxide nanoparticles
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Combined In Vitro and In Vivo Approaches to Propose a Putative Adverse Outcome Pathway for Acute Lung Inflammation Induced by Nanoparticles: A Study on Carbon Dots
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Differential Effects of Surface-Functionalized Zirconium Oxide Nanoparticles on Alveolar Macrophages, Rat Lung, and a Mouse Allergy Model
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A cross-species and model comparison of the acute toxicity of nanoparticles used in the pigment and ink industries
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Genes expression profiling of alveolar macrophages exposed to non-functionalized, anionic and cationic multi-walled carbon nanotubes shows three different mechanisms of toxicity
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Kinetics of chemotaxis, cytokine, and chemokine release of NR8383 macrophages after exposure to inflammatory and inert granular insoluble particles
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Time-resolved characterization of the mechanisms of toxicity induced by silica and amino-modified polystyrene on alveolar-like macrophages
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Graphite particles induce ROS formation in cell free systems and human cells
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Specific Surface Modifications of Silica Nanoparticles Diminish Inflammasome Activation and In Vivo Expression of Selected Inflammatory Genes
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Silica Nanoparticles Provoke Cell Death Independent of p53 and BAX in Human Colon Cancer Cells
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Use of Cause-and-Effect Analysis to Optimize the Reliability of In Vitro Inhalation Toxicity Measurements Using an Air–Liquid Interface
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Interaction of rat alveolar macrophages with dental composite dust
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Lung Toxicity Analysis of Nano-Sized Kaolin and Bentonite: Missing Indications for a Common Grouping
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Revealing Silver Nanoparticle Uptake by Macrophages Using SR-μXRF and LA-ICP-MS
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Multi-walled carbon nanotubes induce stronger migration of inflammatory cells in vitro than asbestos or granular particles but a similar pattern of inflammatory mediators
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Toxicity of TiO2 Nanoparticles: Validation of Alternative Models
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Evaluation of the NLRP3 Inflammasome Activating Effects of a Large Panel of TiO2 Nanomaterials in Macrophages
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Aerogels are not regulated as nanomaterials, but can be assessed by tiered testing and grouping strategies for nanomaterials
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A Low-Serum Culture System for Prolonged in Vitro Toxicology Experiments on a Macrophage System
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Immediate and Sustained Effects of Cobalt and Zinc-Containing Pigments on Macrophages
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Predicting nanomaterials pulmonary toxicity in animals by cell culture models: Achievements and perspectives
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Phosphonate coating of SiO2 nanoparticles abrogates inflammatory effects and local changes of the lipid composition in the rat lung: a complementary bioimaging study
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The influence of exposure approaches to in vitro lung epithelial barrier models to assess engineered nanomaterial hazard
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Morphometric Characterization of Rat and Human Alveolar Macrophage Cell Models and their Response to Amiodarone using High Content Image Analysis
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Genotoxicity and Gene Expression in the Rat Lung Tissue following Instillation and Inhalation of Different Variants of Amorphous Silica Nanomaterials (aSiO2 NM)
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Carbon nanotubes: A review on risks assessment, mechanism of toxicity and future directives to prevent health implication
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Resolution of MoS 2 Nanosheets‐Induced Pulmonary Inflammation Driven by Nanoscale Intracellular Transformation and Extracellular‐Vesicle Shuttles
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Pro-inflammatory and genotoxic responses by metal oxide nanomaterials in alveolar epithelial cells and macrophages in submerged condition and air-liquid interface: An in vitro-in vivo correlation study
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Classes of organic pigments meet tentative PSLT criteria and lack toxicity in short-term inhalation studies
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Use of new approach methodologies (NAMs) to meet regulatory requirements for the assessment of tobacco and other nicotine-containing products
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Cell-Biological Response and Sub-Toxic Inflammatory Effects of Titanium Dioxide Particles with Defined Polymorphic Phase, Size, and Shape
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Possibilities to group nanomaterials across different substances – A case study on organic pigments
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LA-ICP-MS and Immunohistochemical Staining with Lanthanide-Labeled Antibodies to Study the Uptake of CeO2 Nanoparticles by Macrophages in Tissue Sections
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Updated Aspects of Safety Regulations for Biomedical Applications of Aerogel Compounds—Compendia-Like Evaluation
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Risk Assessment and Risk Management
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Assessing biological oxidative damage induced by graphene-based materials: An asset for grouping approaches using the FRAS assay
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Serum Lowers Bioactivity and Uptake of Synthetic Amorphous Silica by Alveolar Macrophages in a Particle Specific Manner
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Application of Cell Membrane-Coated Nanomaterials for Tumor Treatment
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PLATOX: Integrated In Vitro/In Vivo Approach for Screening of Adverse Lung Effects of Graphene-Related 2D Nanomaterials
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Towards characterization of cell culture conditions for reliable proteomic analysis: in vitro studies on A549, differentiated THP-1, and NR8383 cell lines
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Key Role of Choline Head Groups in Large Unilamellar Phospholipid Vesicles for the Interaction with and Rupture by Silica Nanoparticles
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Wiemann, M., Vennemann, A., Sauer, U., Wiench, K., Ma‐Hock, L., & Landsiedel, R. (2016) · Figshare · doi:10.6084/m9.figshare.c.3613751_d1
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Authors: Wiemann, M., Vennemann, A., Sauer, U. G., Wiench, K., Ma-Hock, L., & Landsiedel, R.
Affiliations: BASF (Germany) (DE)
Corresponding author: Wiemann, Martin
ORCID: Wiemann, Martin
Vennemann, Antje
Sauer, Ursula G.
Wiench, Karin
Landsiedel, Robert
Venue: Journal of Nanobiotechnology
Publisher: Springer Science and Business Media LLC
Published: 2016-03-05
Volume: 14
Issue: 1
Pages: 16-16
ISSN: 1477-3155 (ISSN-L)
DOI: 10.1186/s12951-016-0164-2
PMC: PMC4779246
OpenAlex: W2290248210
Cited by: 152
References: 120
Citations by year: 2026: 6 · 2025: 13 · 2024: 12 · 2023: 12 · 2022: 18 · 2021: 14 · 2020: 18 · 2019: 18 · 2018: 17 · 2017: 18 · 2016: 6
FWCI: 8.76
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Journal of Nanobiotechnology (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: Bundesministerium für Bildung und Forschung (03X0105, 0315483A)
Topics: Physical Sciences › Materials Science › Materials Chemistry › Nanoparticles: synthesis and applications
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Occupational and environmental lung diseases
Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
Keywords: alveolar macrophages, NR8383 cells, in vitro-in vivo correlation, zirconia nanoparticles, amorphous silica nanoparticles, surface functionalization, hazard assessment, cytotoxicity, oxidative stress
MeSH terms: Animals, Cell Line, Ferric Compounds, Graphite, Hydrogen Peroxide, Lung, Particle Size, Silicon Dioxide, Titanium, Macrophages, Alveolar, Inhalation Exposure, Nanostructures, Rats

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An in vitro alveolar macrophage assay for predicting the short-term inhalation toxicity of nanomaterials

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