Expert consensus on an in vitro approach to assess pulmonary fibrogenic potential of aerosolized nanomaterials

Archives of Toxicology

Volumn 90, Issue 7, 2016, Pages 1769-1783

  Clippinger, Amy J ^a   Ahluwalia, Arti ^b   Allen, David ^c   Bonner, James C ^d   Casey, Warren ^e   Castranova, Vincent ^f   David, Raymond M ^g   Halappanavar, Sabina ^h   Hotchkiss, Jon A ⁱ   Jarabek, Annie M ^j   Maier, Monika ^k   Polk, William ^c   Rothen Rutishauser, Barbara ^l   Sayes, Christie M ^m   Sayre, Phil ⁿ   Sharma, Monita ^a   Stone, Vicki ^o  

^a PETA International Science Consortium Ltd   (United Kingdom)

^b UNIVERSITY OF PISA   (Italy)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e NTP Interagency Center for the Evaluation of Alternative Toxicological Methods   (United States)

^f WEST VIRGINIA UNIVERSITY   (United States)

^g BASF CORPORATION   (United States)

^h HEALTH CANADA   (Canada)

ⁱ DOW CHEMICAL COMPANY   (United States)

^j U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^k EVONIK INDUSTRIES AG   (Germany)

^l UNIVERSITY OF FRIBOURG   (Switzerland)

^m BAYLOR UNIVERSITY   (United States)

ⁿ nanoRisk Analytics   (United States)

^o HERIOT WATT UNIVERSITY   (United Kingdom)

more..

Author keywords

In vitro testing strategies; Inhalation toxicity; Multi walled carbon nanotubes; MWCNTs; Pulmonary fibrosis; Regulatory risk assessment

Indexed keywords

CYTOKINE; GROWTH FACTOR; MULTI WALLED NANOTUBE; NANOMATERIAL; AEROSOL;

ADVERSE OUTCOME; AEROSOL; ARTICLE; COCULTURE; CONSENSUS; EXPOSURE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INHALATION TEST; LUNG FIBROSIS; LUNG TOXICITY; NANOTOXICOLOGY; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; ADVERSE EFFECTS; ANIMAL; ANIMAL TESTING ALTERNATIVE; BIOLOGICAL MODEL; CELL CULTURE; CELL CULTURE TECHNIQUE; CHEMICALLY INDUCED; CYTOLOGY; DEVICES; DRUG EFFECTS; EQUIPMENT DESIGN; LUNG; PROCEDURES; TOXICITY TESTING;

AEROSOLS; ANIMAL USE ALTERNATIVES; ANIMALS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; EQUIPMENT DESIGN; HUMANS; INHALATION EXPOSURE; LUNG; MODELS, BIOLOGICAL; NANOSTRUCTURES; PULMONARY FIBROSIS; TOXICITY TESTS;

EID: 84975321420     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-016-1717-8     Document Type: Article

References (96)

1. Alfaro-Moreno E, Nawrot TS et al (2008) Co-cultures of multiple cell types mimic pulmonary cell communication in response to urban PM10. Eur Respir J 32(5):1184–1194
2. Anjilvel S, Asgharian B (1995) A multiple-path model of particle deposition in the rat lung. Fundam Appl Toxicol 28(1):41–50
3. Ankley GT, Bennett RS et al (2010) Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29(3):730–741
4. Asgharian B, Price OT et al (2014) Computational modeling of nanoscale and microscale particle deposition, retention and dosimetry in the mouse respiratory tract. Inhal Toxicol 26(14):829–842
5. Banga A, Witzmann FA et al (2012) Functional effects of nanoparticle exposure on Calu-3 airway epithelial cells. Cell Physiol Biochem 29(1–2):197–212
6. Bellmann B, Muhle H et al (2001) Effects of nonfibrous particles on ceramic fiber (RCF1) toxicity in rats. Inhal Toxicol 13(10):877–901
7. Bhattacharya K, Andón FT et al (2013) Mechanisms of carbon nanotube-induced toxicity: focus on pulmonary inflammation. Adv Drug Deliv Rev 65(15):2087–2097
8. Bouwmeester H, Lynch I et al (2011) Minimal analytical characterization of engineered nanomaterials needed for hazard assessment in biological matrices. Nanotoxicology 5(1):1–11
9. Bove PF, Dang H et al (2013) Breaking the in vitro alveolar type II cell proliferation barrier while retaining ion transport properties. Am J Respir Cell Mol Biol 50(4):767–776
10. Carterson AJ, Honer zu Bentrup K et al (2005) A549 lung epithelial cells grown as three-dimensional aggregates: alternative tissue culture model for Pseudomonas aeruginosa pathogenesis. Infect Immun 73(2):1129–1140
11. Cei D, Ahluwalia A et al (2014) Development of a dynamic model of the alveolar interface for the study of aerosol deposition. In: Proceedings of the XIX international conference on mechanics in medicine and biology, 2–5 September 2014, Bologna, Italy
12. Cheng Y-S (1986) Bivariate lognormal distribution for characterizing asbestos fiber aerosols. Aerosol Sci Technol 5(3):359–368
13. Chortarea S, Clift MJ et al (2015) Repeated exposure to carbon nanotube-based aerosols does not affect the functional properties of a 3D human epithelial airway model. Nanotoxicology 9(8):983–993
14. Coecke S, Balls M et al (2005) Guidance on good cell culture practice. a report of the second ECVAM task force on good cell culture practice. Altern Lab Anim 33(3):261–287
15. DeLoid G, Cohen JM et al (2014) Estimating the effective density of engineered nanomaterials for in vitro dosimetry. Nat Commun 5:3514
16. Donaldson K, Murphy F et al (2010) Asbestos, carbon nanotubes and the pleural mesothelium: a review of the hypothesis regarding the role of long fibre retention in the parietal pleura, inflammation and mesothelioma. Part Fibre Toxicol 7(1):5
17. Dong X, Liu L et al (2015) Effects of carboxylated multiwalled carbon nanotubes on the function of macrophages. J Nanomater 2015:638760-1–638760-8
18. ESAC (2008) ESAC statement on the use of FCS and other animal-derived supplements. http://eurl-ecvam.jrc.ec.europa.eu/about-ecvam/archive-publications/publication/ESAC28_statement_FCS_20080508.pdf
19. Fedan J, Thompson J et al (2014) Inhalation of multi-walled carbon nanotubes affects lung resistance and compliance and evokes airway hyperreactivity to methacholine in rats (660.1). FASEB J 28(1 Supplement)
20. Foucaud L, Wilson MR et al (2007) Measurement of reactive species production by nanoparticles prepared in biologically relevant media. Toxicol Lett 174(1–3):1–9
21. Foucaud L, Goulaouic S et al (2010) Oxidative stress induction by nanoparticles in THP-1 cells with 4-HNE production: stress biomarker or oxidative stress signalling molecule? Toxicol In Vitro 24(6):1512–1520
22. Francis AP, Ganapathy S et al (2015) One time nose-only inhalation of MWCNTs: exploring the mechanism of toxicity by intermittent sacrifice in Wistar rats. Toxicol Rep 2:111–120
23. Gangwal S, Brown JS et al (2011) Informing selection of nanomaterial concentrations for ToxCast in vitro testing based on occupational exposure potential. Environ Health Perspect 119(11):1539–1546
24. Gliga AR, Skoglund S et al (2014) Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release. Part Fibre Toxicol 11:11
25. Godwin H, Nameth C et al (2015) Nanomaterial categorization for assessing risk potential to facilitate regulatory decision-making. ACS Nano 9(4):3409–3417
26. Hanes J, Schaffitzel C et al (2000) Picomolar affinity antibodies from a fully synthetic naive library selected and evolved by ribosome display. Nat Biotechnol 18(12):1287–1292
27. Haniu H, Saito N et al (2014) Biological responses according to the shape and size of carbon nanotubes in BEAS-2B and MESO-1 cells. Int J Nanomed 9:1979–1990
28. Hartung T, Balls M et al (2002) Good cell culture practice. ECVAM good cell culture practice task force report 1. Altern Lab Anim 30(4):407–414
29. Hermanns MI, Unger RE et al (2004) Lung epithelial cell lines in coculture with human pulmonary microvascular endothelial cells: development of an alveolo-capillary barrier in vitro. Lab Invest 84(6):736–752
30. Herzog F, Clift MJ et al (2013) Exposure of silver-nanoparticles and silver–ions to lung cells in vitro at the air–liquid interface. Part Fibre Toxicol 10(1):11
31. Herzog F, Loza K et al (2014) Mimicking exposures to acute and lifetime concentrations of inhaled silver nanoparticles by two different in vitro approaches. Beilstein J Nanotechnol 5:1357–1370
32. Hinderliter PM, Minard KR et al (2010) ISDD: a computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies. Part Fibre Toxicol 7(1):36
33. Holsapple MP, Farland WH et al (2005) Research strategies for safety evaluation of nanomaterials, part II: toxicological and safety evaluation of nanomaterials, current challenges and data needs. Toxicol Sci 88(1):12–17
34. Horvath L, Umehara Y et al (2015) Engineering an in vitro air–blood barrier by 3D bioprinting. Sci Rep 5:7974
35. Huh D, Matthews BD et al (2010) Reconstituting organ-level lung functions on a chip. Science 328(5986):1662–1668
36. Hussain S, Sangtian S et al (2014) Inflammasome activation in airway epithelial cells after multi-walled carbon nanotube exposure mediates a profibrotic response in lung fibroblasts. Part Fibre Toxicol 11:28
37. InLiveTox (2012) Development and evaluation of a novel tool for physiologically accurate data generation. http://www.inlivetox.eu/fileadmin/user/pdf/InLiveTox-Final_publishable_report.pdf
38. Jackson G, Mankus C et al (2013) A triple cell co-culture model of the air–blood barrier reconstructed from primary human cells. Toxicol Lett 221. doi:10.1016/j.toxlet.2013.05.270
39. Jarabek AM, Asgharian B et al (2005) Dosimetric adjustments for interspecies extrapolation of inhaled poorly soluble particles (PSP). Inhal Toxicol 17(7–8):317–334
40. JRC (2014) Multi-walled carbon nanotubes, NM-400, NM-401, NM-402, NM-403: characterisation and physico-chemical properties. http://publications.jrc.ec.europa.eu/repository/bitstream/JRC91205/mwcnt-online.pdf
41. Jud C, Clift MJ et al (2013) Nanomaterials and the human lung: what is known and what must be deciphered to realise their potential advantages? Swiss Med Wkly 143:w13758
42. Kim JS, Sung JH et al (2014) In vivo genotoxicity evaluation of lung cells from Fischer 344 rats following 28 days of inhalation exposure to MWCNTs, plus 28 days and 90 days post-exposure. Inhal Toxicol 26(4):222–234
43. Klein CL, Wiench K et al (2012) Hazard identification of inhaled nanomaterials: making use of short-term inhalation studies. Arch Toxicol 86(7):1137–1151
44. Klein SG, Serchi T et al (2013) An improved 3D tetraculture system mimicking the cellular organisation at the alveolar barrier to study the potential toxic effects of particles on the lung. Part Fibre Toxicol 10:31
45. Labib S, Williams A et al (2016) Nano-risk science: application of toxicogenomics in an adverse outcome pathway framework for risk assessment of multi-walled carbon nanotubes. Part Fibre Toxicol 13(1):1–17
46. Lehman JH, Terrones M et al (2011) Evaluating the characteristics of multiwall carbon nanotubes. Carbon 49(8):2581–2602
47. Lehr C-M (2002) Cell culture models of biological barriers: in vitro test systems for drug absorption and delivery. Taylor & Francis, London
48. Lenz AG, Karg E et al (2009) A dose-controlled system for air–liquid interface cell exposure and application to zinc oxide nanoparticles. Part Fibre Toxicol 6:32
49. Li R, Wang X et al (2013) Surface charge and cellular processing of covalently functionalized multiwall carbon nanotubes determine pulmonary toxicity. ACS Nano 7(3):2352–2368
50. Ma-Hock L, Treumann S et al (2009) Inhalation toxicity of multiwall carbon nanotubes in rats exposed for 3 months. Toxicol Sci 112(2):468–481
51. Mast RW, Hesterberg TW et al (1994) Chronic inhalation and biopersistence of refractory ceramic fiber in rats and hamsters. Environ Health Perspect 102(Suppl 5):207–209
52. McCarthy J, Gong X et al (2011) Polystyrene nanoparticles activate ion transport in human airway epithelial cells. Int J Nanomed 6:1343–1356
53. Mishra A, Rojanasakul Y et al (2012) Assessment of pulmonary fibrogenic potential of multiwalled carbon nanotubes in human lung cells. J Nanomater 2012:930931-1–930931-11
54. Mishra A, Stueckle TA et al (2015) Identification of TGF-Beta Receptor-1 as a key regulator of carbon nanotube-induced fibrogenesis. Am J Physiol Lung Cell Mol Physiol 309(8):821–833
55. Moss OR, Wong BA, Asgharian B (1994) Bimodal, bivariate, log-normal distribution in the application of inhalation toxicology specific to the measurement of fiber and particle dosimetry. In: Dungworth DL et al (eds) Toxic and carcinogenic effects of solid particles in the respiratory tract, ILSI Press, Washington, DC, pp 623–628
56. Mudway IS, Stenfors N et al (2004) An in vitro and in vivo investigation of the effects of diesel exhaust on human airway lining fluid antioxidants. Arch Biochem Biophys 423(1):200–212
57. Nel A, Xia T et al (2012) Nanomaterial toxicity testing in the 21st century: use of a predictive toxicological approach and high-throughput screening. Acc Chem Res 46(3):607–621
58. NIOSH (2013) Current Intelligence Bulletin 65: Occupational exposure to carbon nanotubes and nanofibers. http://www.cdc.gov/niosh/docs/2013-145/pdfs/2013-145.pdf
59. NRC (2007) Toxicity testing in the twenty-first century: a vision and a strategy. Washington, DC, p 146
60. Nymark P, Catalán J et al (2013) Genotoxicity of polyvinylpyrrolidone-coated silver nanoparticles in BEAS 2B cells. Toxicology 313(1):38–48
61. Oberdorster G, Maynard A et al (2005) Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy. Part Fibre Toxicol 2:8
62. OECD (2005) Guidance document on the validation and international acceptance of new or updated test methods for hazard assessment. http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?doclanguage=en&cote=env/jm/mono%282005%2914
63. OECD (2009) Test No. 413: subchronic inhalation toxicity: 90-day study. OECD Publishing
64. OECD (2012a) Important issues on risk assessment of manufactured nanomaterials. http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2012)8&doclanguage=en
65. OECD (2012b) Guidance on sample preparation and dosimetry for the safety testing of manufactured nanomaterials. Series on the Safety of Manufactured Nanomaterials No. 36. http://search.oecd.org/officialdocuments/displaydocumentpdf/?cote=env/jm/mono(2012)40&doclanguage=en
66. Oomen AG, Bos PM et al (2014) Concern-driven integrated approaches to nanomaterial testing and assessment-report of the NanoSafety Cluster Working Group 10. Nanotoxicology 8(3):334–348
67. Palecanda A, Kobzik L (2001) Receptors for unopsonized particles: the role of alveolar macrophage scavenger receptors. Curr Mol Med 1(5):589–595
68. Poland CA, Duffin R et al (2008) Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol 3(7):423–428
69. Poulsen SS, Saber AT et al (2015) MWCNTs of different physicochemical properties cause similar inflammatory responses, but differences in transcriptional and histological markers of fibrosis in mouse lungs. Toxicol Appl Pharmacol 284(1):16–32
70. RIVM (2002) Multiple Path Particle Dosimetry Model (MPPD v 1.0): a model for human and rat airway particle dosimetry. Model available online at: http://www.ara.com/products/mppd.htm. National Institute for Public Health and the Environment, Bilthoven
71. Rothen-Rutishauser BM, Kiama SG et al (2005) A three-dimensional cellular model of the human respiratory tract to study the interaction with particles. Am J Respir Cell Mol Biol 32(4):281–289
72. Rothen-Rutishauser B, Blank F et al (2008) In vitro models of the human epithelial airway barrier to study the toxic potential of particulate matter. Expert Opin Drug Metab Toxicol 4(8):1075–1089
73. Rotoli BM, Bussolati O et al (2008) Non-functionalized multi-walled carbon nanotubes alter the paracellular permeability of human airway epithelial cells. Toxicol Lett 178(2):95–102
74. Sanchez VC, Weston P et al (2011) A 3-dimensional in vitro model of epithelioid granulomas induced by high aspect ratio nanomaterials. Part Fibre Toxicol 8:17
75. Sargent LM, Porter DW et al (2014) Promotion of lung adenocarcinoma following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol 11:3
76. Schurch D, Vanhecke D et al (2014) Modeling nanoparticle-alveolar epithelial cell interactions under breathing conditions using captive bubble surfactometry. Langmuir 30(17):4924–4932
77. Scott-Fordsmand JJ, Pozzi-Mucelli S et al (2014) A unified framework for nanosafety is needed. Nano Today 9(5):546–549
78. SOR/2005-247 (2005) New substances notification regulations (chemicals and polymers). http://laws-lois.justice.gc.ca/eng/regulations/SOR-2005-247/page-1.html
79. Steimer A, Haltner E et al (2005) Cell culture models of the respiratory tract relevant to pulmonary drug delivery. J Aerosol Med 18(2):137–182
80. Stöber W (1972) Dynamic shape factors of nonspherical aerosol particles. In: Mercer TT, Morrow PE, Stöber W (eds) Assessment of airborne particles, Charles C Thomas, Springfield, IL, pp 249–289
81. Stone V, Pozzi-Mucelli S et al (2014) ITS-NANO—prioritising nanosafety research to develop a stakeholder driven intelligent testing strategy. Part Fibre Toxicol 11:9
82. Sturm R (2009) A theoretical approach to the deposition of cancer-inducing asbestos fibers in the human respiratory tract. Open Lung Cancer J 2:1–11
83. Sturm R (2011) A computer model for the simulation of fiber-cell interaction in the alveolar region of the respiratory tract. Comput Biol Med 41(7):565–573
84. Sturm R, Hofmann W (2006) A computer program for the simulation of fiber deposition in the human respiratory tract. Comput Biol Med 36(11):1252–1267
85. Sturm R, Hofmann W (2009) A theoretical approach to the deposition and clearance of fibers with variable size in the human respiratory tract. J Hazard Mater 170(1):210–218
86. Taquahashi Y, Ogawa Y et al (2013) Improved dispersion method of multi-wall carbon nanotube for inhalation toxicity studies of experimental animals. J Toxicol Sci 38(4):619–628
87. Taylor AJ, McClure CD et al (2014) Atomic layer deposition coating of carbon nanotubes with aluminum oxide alters pro-fibrogenic cytokine expression by human mononuclear phagocytes in vitro and reduces lung fibrosis in mice in vivo. PLoS One 9(9):e106870
88. Teeguarden JG, Hinderliter PM et al (2007) Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments. Toxicol Sci 95(2):300–312
89. US EPA (2015) Control of Nanoscale Materials under the Toxic Substances Control Act. http://www.epa.gov/reviewing-new-chemicals-under-toxic-substances-control-act-tsca/control-nanoscale-materials-under. Accessed 5 Dec 2015
90. van Berlo D, Wilhelmi V et al (2014) Apoptotic, inflammatory, and fibrogenic effects of two different types of multi-walled carbon nanotubes in mouse lung. Arch Toxicol 88(9):1725–1737
91. Vance ME, Kuiken T et al (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–1780
92. Vietti G, Ibouraadaten S et al (2013) Towards predicting the lung fibrogenic activity of nanomaterials: experimental validation of an in vitro fibroblast proliferation assay. Part Fibre Toxicol 10:52
93. Vincent JH (2005) Health-related aerosol measurement: a review of existing sampling criteria and proposals for new ones. J Environ Monit 7(11):1037–1053
94. Wang X, Xia T et al (2011) Dispersal state of multiwalled carbon nanotubes elicits profibrogenic cellular responses that correlate with fibrogenesis biomarkers and fibrosis in the murine lung. ACS Nano 5(12):9772–9787
95. Winkler DA, Mombelli E et al (2012) Applying quantitative structure-activity relationship approaches to nanotoxicology: current status and future potential. Toxicology 313(1):15–23
96. Zielinski H, Mudway IS et al (1999) Modeling the interactions of particulates with epithelial lining fluid antioxidants. Am J Physiol Lung Cell Mol Physiol 277(4):L719–L726