Towards predicting the lung fibrogenic activity of nanomaterials: Experimental validation of an in vitro fibroblast proliferation assay

Particle and Fibre Toxicology

Volumn 10, Issue 1, 2013, Pages

  Vietti, Giulia ^a   Ibouraadaten, Saloua ^a   Palmai Pallag, Mihaly ^a   Yakoub, Yousof ^a   Bailly, Christian ^a   Fenoglio, Ivana ^b   Marbaix, Etienne ^c   Lison, Dominique ^a   van den Brule, Sybille ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY OF TURIN   (Italy)

^c DE DUVE INSTITUTE   (Belgium)

Author keywords

Asbestos; Carbon nanotubes; CNT; Crocidolite; Dispersion; Lung fibrosis; MLg; WST 1

Indexed keywords

ASBESTOS; BOVINE SERUM ALBUMIN; COLLAGEN; MULTI WALLED NANOTUBE; NANOMATERIAL; OSTEOPONTIN; PLATELET DERIVED GROWTH FACTOR BB; PROPIDIUM IODIDE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPIRATION; CELL ACTIVITY; CELL ASSAY; CELL COUNT; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; CYTOCHEMISTRY; FEMALE; FIBROBLAST; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG FIBROBLAST; LUNG FIBROSIS; LUNG LAVAGE; MOUSE; NONHUMAN; PREDICTION; PREDICTIVE VALUE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; VALIDATION STUDY;

BOVINAE; MUS; RODENTIA;

ANIMALS; ASBESTOS, CROCIDOLITE; BALB 3T3 CELLS; BIOLOGICAL ASSAY; CELL COUNT; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FIBROBLASTS; HUMANS; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, SCANNING; NANOTUBES, CARBON; PARTICLE SIZE; PREDICTIVE VALUE OF TESTS; PULMONARY FIBROSIS; REPRODUCIBILITY OF RESULTS; SURFACE PROPERTIES;

EID: 84885119756     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/1743-8977-10-52     Document Type: Article

References (44)

1. Gorman J. Taming high-tech particles: cautious steps into the nanothech future. Sci News 2002, 161:200-201.
2. Sanchez VC, Pietruska JR, Miselis NR, Hurt RH, Kane AB. Biopersistence and potential adverse health impacts of fibrous nanomaterials: what have we learned from asbestos?. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2009, 1:511-529. 10.1002/wnan.41, 2864601, 20049814.
3. Donaldson K, Aitken R, Tran L, Stone V, Duffin R, Forrest G, Alexander A. Carbon nanotubes: a review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol Sci 2006, 92:5-22. 10.1093/toxsci/kfj130, 16484287.
4. Lam CW, James JT, McCluskey R, Hunter RL. Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol Sci 2004, 77:126-134.
5. Shvedova AA, Kisin ER, Mercer R, Murray AR, Johnson VJ, Potapovich AI, Tyurina YY, Gorelik O, Arepalli S, Schwegler-Berry D, et al. Unusual inflammatory and fibrogenic pulmonary responses to single-walled carbon nanotubes in mice. Am J Physiol Lung Cell Mol Physiol 2005, 289:L698-L708. 10.1152/ajplung.00084.2005, 15951334.
6. Muller J, Huaux F, Moreau N, Misson P, Heilier JF, Delos M, Arras M, Fonseca A, Nagy JB, Lison D. Respiratory toxicity of multi-wall carbon nanotubes. Toxicol Appl Pharmacol 2005, 207:221-231. 10.1016/j.taap.2005.01.008, 16129115.
7. Shvedova AA, Kisin E, Murray AR, Johnson VJ, Gorelik O, Arepalli S, Hubbs AF, Mercer RR, Keohavong P, Sussman N, et al. Inhalation vs. aspiration of single-walled carbon nanotubes in C57BL/6 mice: inflammation, fibrosis, oxidative stress, and mutagenesis. Am J Physiol Lung Cell Mol Physiol 2008, 295:L552-L565. 10.1152/ajplung.90287.2008, 2575941, 18658273.
8. Pauluhn J. Subchronic 13-week inhalation exposure of rats to multiwalled carbon nanotubes: toxic effects are determined by density of agglomerate structures, not fibrillar structures. Toxicol Sci 2010, 113:226-242. 10.1093/toxsci/kfp247, 19822600.
9. Mitchell LA, Gao J, Wal RV, Gigliotti A, Burchiel SW, McDonald JD. Pulmonary and systemic immune response to inhaled multiwalled carbon nanotubes. Toxicol Sci 2007, 100:203-214. 10.1093/toxsci/kfm196, 17660506.
10. Ma-Hock L, Treumann S, Strauss V, Brill S, Luizi F, Mertler M, Wiench K, Gamer AO, van Ravenzwaay B, Landsiedel R. Inhalation toxicity of multiwall carbon nanotubes in rats exposed for 3 months. Toxicol Sci 2009, 112:468-481. 10.1093/toxsci/kfp146, 19584127.
11. Morimoto Y, Hirohashi M, Kobayashi N, Ogami A, Horie M, Oyabu T, Myojo T, Hashiba M, Mizuguchi Y, Kambara T, et al. Pulmonary toxicity of well-dispersed single-wall carbon nanotubes after inhalation. Nanotoxicology 2012, 6:766-775. 10.3109/17435390.2011.620719, 21942532.
12. Wang L, Mercer RR, Rojanasakul Y, Qiu A, Lu Y, Scabilloni JF, Wu N, Castranova V. Direct fibrogenic effects of dispersed single-walled carbon nanotubes on human lung fibroblasts. J Toxicol Environ Health A 2010, 73:410-422. 10.1080/15287390903486550, 20155582.
13. Wang L, Castranova V, Mishra A, Chen B, Mercer RR, Schwegler-Berry D, Rojanasakul Y. Dispersion of single-walled carbon nanotubes by a natural lung surfactant for pulmonary in vitro and in vivo toxicity studies. Part Fibre Toxicol 2010, 7:31. 10.1186/1743-8977-7-31, 2970581, 20958985.
14. Wang X, Xia T, Ntim SA, Ji Z, George S, Meng H, Zhang H, Castranova V, Mitra S, Nel AE. Quantitative techniques for assessing and controlling the dispersion and biological effects of multiwalled carbon nanotubes in mammalian tissue culture cells. ACS Nano 2010, 4:7241-7252. 10.1021/nn102112b, 21067152.
15. Wang X, Xia T, Duch MC, Ji Z, Zhang H, Li R, Sun B, Lin S, Meng H, Liao YP, et al. Pluronic F108 coating decreases the lung fibrosis potential of multiwall carbon nanotubes by reducing lysosomal injury. Nano Lett 2012, 12:3050-3061. 10.1021/nl300895y, 22546002.
16. Wang X, Xia T, Ntim SA, Ji Z, Lin S, Meng H, Chung CH, George S, Zhang H, Wang M, et al. Dispersal state of multiwalled carbon nanotubes elicits profibrogenic cellular responses that correlate with fibrogenesis biomarkers and fibrosis in the murine lung. ACS Nano 2011, 5:9772-9787. 10.1021/nn2033055, 22047207.
17. Crouch E. Pathobiology of pulmonary fibrosis. Am J Physiol 1990, 259:L159-L184.
18. Thannickal VJ, Toews GB, White ES, Lynch JP, Martinez FJ. Mechanisms of pulmonary fibrosis. Annu Rev Med 2004, 55:395-417. 10.1146/annurev.med.55.091902.103810, 14746528.
19. Lu P, Takai K, Weaver VM, Werb Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 2011, 3.
20. Mercer RR, Hubbs AF, Scabilloni JF, Wang L, Battelli LA, Schwegler-Berry D, Castranova V, Porter DW. Distribution and persistence of pleural penetrations by multi-walled carbon nanotubes. Part Fibre Toxicol 2010, 7:28. 10.1186/1743-8977-7-28, 2958975, 20920331.
21. Worle-Knirsch JM, Pulskamp K, Krug HF. Oops they did it again! carbon nanotubes hoax scientists in viability assays. Nano Lett 2006, 6:1261-1268. 10.1021/nl060177c, 16771591.
22. Casey A, Herwog E, Davoren M, Lyng FM, Byrne HJ, Chambers G. Spectroscopic analysis confirms the interactions between single walled carbon nanotubes and various dyes commonly used to assess cytotoxicity. Carbon 2007, 45:1425-1432.
23. Monteiro-Riviere NA, Inman AO, Zhang LW. Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 2009, 234:222-235. 10.1016/j.taap.2008.09.030, 18983864.
24. Muller J, Huaux F, Fonseca A, Nagy JB, Moreau N, Delos M, Raymundo-Pinero E, Beguin F, Kirsch-Volders M, Fenoglio I, et al. Structural defects play a major role in the acute lung toxicity of multiwall carbon nanotubes: toxicological aspects. Chem Res Toxicol 2008, 21:1698-1705. 10.1021/tx800101p, 18636756.
25. Fenoglio I, Greco G, Tomatis M, Muller J, Raymundo-Pinero E, Beguin F, Fonseca A, Nagy JB, Lison D, Fubini B. Structural defects play a major role in the acute lung toxicity of multiwall carbon nanotubes: physicochemical aspects. Chem Res Toxicol 2008, 21:1690-1697. 10.1021/tx800100s, 18636755.
26. Fubini B, Fenoglio I, Tomatis M, Turci F. Effect of chemical composition and state of the surface on the toxic response to high aspect ratio nanomaterials. Nanomedicine (Lond) 2011, 6:899-920.
27. Castranova V, Schulte PA, Zumwalde RD. Occupational nanosafety considerations for carbon nanotubes and carbon nanofibers. Acc Chem Res 2012, 46:642-649.
28. Cesta MF, Ryman-Rasmussen JP, Wallace DG, Masinde T, Hurlburt G, Taylor AJ, Bonner JC. Bacterial lipopolysaccharide enhances PDGF signaling and pulmonary fibrosis in rats exposed to carbon nanotubes. Am J Respir Cell Mol Biol 2010, 43:142-151. 10.1165/rcmb.2009-0113OC, 2937228, 19738159.
29. Li R, Wang X, Ji Z, Sun B, Zhang H, Chang CH, Lin S, Meng H, Liao YP, Wang M, et al. Surface charge and cellular processing of covalently functionalized multiwall carbon nanotubes determine pulmonary toxicity. ACS Nano 2013, 7:2352-2368. 10.1021/nn305567s, 23414138.
30. Wang P, Nie X, Wang Y, Li Y, Ge C, Zhang L, Wang L, Bai R, Chen Z, Zhao Y, Chen C. Multiwall carbon nanotubes mediate macrophage activation and promote pulmonary fibrosis through TGF-beta/smad signaling pathway. Small 2013, doi: 10.1002/smll.201300607. [Epub ahead of print].
31. Zanello LP, Zhao B, Hu H, Haddon RC. Bone cell proliferation on carbon nanotubes. Nano Lett 2006, 6:562-567. 10.1021/nl051861e, 16522063.
32. Bhattacharya M, Wutticharoenmongkol-Thitiwongsawet P, Hamamoto DT, Lee D, Cui T, Prasad HS, Ahmad M. Bone formation on carbon nanotube composite. J Biomed Mater Res A 2011, 96:75-82.
33. Porter DW, Hubbs AF, Mercer RR, Wu N, Wolfarth MG, Sriram K, Leonard S, Battelli L, Schwegler-Berry D, Friend S, et al. Mouse pulmonary dose- and time course-responses induced by exposure to multi-walled carbon nanotubes. Toxicology 2010, 269:136-147. 10.1016/j.tox.2009.10.017, 19857541.
34. Phalen RF. Basic morphology and physiology of the respiratory tract 1984, 33-75. Boca Raton: Inhalation Studies: Foundations and Techniques CRC Press.
35. Han JH, Lee EJ, Lee JH, So KP, Lee YH, Bae GN, Lee SB, Ji JH, Cho MH, Yu IJ. Monitoring multiwalled carbon nanotube exposure in carbon nanotube research facility. Inhal Toxicol 2008, 20:741-749. 10.1080/08958370801942238, 18569096.
36. Galer DM, Leung HW, Sussman RG, Trzos RJ. Scientific and practical considerations for the development of occupational exposure limits (OELs) for chemical substances. Regul Toxicol Pharmacol 1992, 15:291-306. 10.1016/0273-2300(92)90040-G, 1509122.
37. Donaldson K, Murphy FA, Duffin R, Poland CA. 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 2010, 7:5. 10.1186/1743-8977-7-5, 2857820, 20307263.
38. Azad N, Iyer AK, Wang L, Liu Y, Lu Y, Rojanasakul Y. Reactive oxygen species-mediated p38 MAPK regulates carbon nanotube-induced fibrogenic and angiogenic responses. Nanotoxicology 2013, 7:157-168. 10.3109/17435390.2011.647929, 22263913.
39. Blaauboer BJ. The applicability of in vitro-derived data in hazard identification and characterisation of chemicals. Environ Toxicol Pharmacol 2002, 11:213-225. 10.1016/S1382-6689(01)00120-X, 21782605.
40. Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WA, Seaton A, Stone V, Brown S, Macnee W, Donaldson K. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol 2008, 3:423-428. 10.1038/nnano.2008.111, 18654567.
41. Ghiazza M, Vietti G, Fenoglio I. Carbon nanotubes (CNTs): properties, applications and toxicity. Health and environmental risks of nanomaterials UK: Woodhead Publishing, Njuguna J, Pielichowski K, Zhu H, in press.
42. Kermanizadeh A, Pojana G, Gaiser BK, Birkedal R, Bilanicova D, Wallin H, Jensen KA, Sellergren B, Hutchison GR, Marcomini A, Stone V. In vitro assessment of engineered nanomaterials using a hepatocyte cell line: cytotoxicity, pro-inflammatory cytokines and functional markers. Nanotoxicology 2013, 7:301-313. 10.3109/17435390.2011.653416, 22263564.
43. Huaux F, Noel S, Dhooghe B, Panin N, Lo Re S, Lison D, Wallemacq P, Marbaix E, Scholte BJ, Lebecque P, Leal T. Dysregulated proinflammatory and fibrogenic phenotype of fibroblasts in cystic fibrosis. PLoS One 2013, 8:e64341. 10.1371/journal.pone.0064341, 3667188, 23734196.
44. Biondi PA, Chiesa LM, Storelli MR, Renon P. A new procedure for the specific high-performance liquid chromatographic determination of hydroxyproline. J Chromatogr Sci 1997, 35:509-512. 10.1093/chromsci/35.11.509, 9358626.