Time-Dependent subcellular distribution and effects of carbon nanotubes in lungs of mice

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Købler, Carsten ^a   Poulsen, Sarah S ^b,c   Saber, Anne T ^b   Jacobsen, Nicklas R ^b   Wallin, Håkan ^b,d   Yauk, Carole L ^e   Halappanavar, Sabina ^e   Vogel, Ulla ^a,b   Qvortrup, Klaus ^d   Mølhave, Kristian ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b NATIONAL RESEARCH CENTRE FOR THE WORKING ENVIRONMENT   (Denmark)

^c ROSKILDE UNIVERSITY   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e Environmental and Radiation Health Sciences Direct Health Canada   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON NANOTUBE; EOTAXIN; EOTAXIN 2; MESSENGER RNA; MULTI WALLED NANOTUBE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COMPOSITION; CELL INTERACTION; CONTROLLED STUDY; CYTOSOL; ELECTRON MICROSCOPY; ENDOCYTOSIS; EOSINOPHIL; EOSINOPHIL COUNT; EOSINOPHILIC CRYSTALLINE PNEUMONIA; FEMALE; GENE EXPRESSION; INFLAMMATORY CELL; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; LUNG PARENCHYMA; LUNG TOXICITY; MACROPHAGE; MEMBRANE DAMAGE; MOUSE; NONHUMAN; PARTICLE RESUSPENSION; PNEUMONIA; REPRODUCIBILITY; TRANSMISSION ELECTRON MICROSCOPY; ULTRAMICROTOMY; ANIMAL; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; LOEFFLER PNEUMONIA; LUNG; PARTICLE SIZE; PROCEDURES; TIME FACTOR; ULTRASTRUCTURE;

MUS;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; FEMALE; LUNG; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; NANOTUBES, CARBON; PARTICLE SIZE; PULMONARY EOSINOPHILIA; TIME FACTORS;

EID: 84921769966     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116481     Document Type: Article

References (57)

1. Monthioux M, Kuznetsov VL (2006) Who should be given the credit for the discovery of carbon nanotubes? Carbon 44: 1621-1623. doi: 10.1016/j.carbon.2006.03.019.
2. Donaldson K, Poland CA, Murphy FA, MacFarlane M, Chernova T, et al. (2013) Pulmonary toxicity of carbon nanotubes and asbestos-Similarities and differences. Advanced Drug Delivery Reviews 65: 2078-2086. doi: 10.1016/j.addr.2013.07.014 PMID: 23899865
3. Pauluhn J (2009) Subchronic 13-week inhalation exposure of rats to multiwalled carbon nanotubes:Toxic effects are determined by density of agglomerate structures, not fibrillar structures. Toxicological Sciences 113: 226-242. doi: 10.1093/toxsci/kfp247 PMID: 19822600
4. Aschberger K, Johnston HJ, Stone V, Aitken RJ, Hankin SM, et al. (2010) Review of carbon nanotubes toxicity and exposure-Appraisal of human health risk assessment based on open literature. Critical Reviews in Toxicology 40: 759-790. doi: 10.3109/10408444.2010.506638 PMID: 20860524
5. Porter DW, Hubbs AF, Mercer RR, Wu N, Wolfarth MG, et al. (2010) Mouse pulmonary dose-and time course-responses induced by exposure to multi-walled carbon nanotubes. Toxicology 269: 136-147. doi: 10.1016/j.tox.2009.10.017 PMID: 19857541
6. Hamilton RF, Wu Z, Mitra S, Shaw PK, Holian A (2013) Effect of MWCNT size, carboxylation, and purification on in vitro and in vivo toxicity, inflammation and lung pathology. Particle and Fibre Toxicology 10: 57. doi: 10.1186/1743-8977-10-57 PMID: 24225053
7. Nagai H, Okazaki Y, Chew SH, Misawa N, Yamashita Y, et al. (2011) Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. Proceedings of the National Academy of Sciences 108: E1330-E1338. doi: 10.1073/pnas.1110013108 PMID: 22084097
8. Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WAH, et al. (2008) Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nature Nanotech 3: 423-428. doi: 10.1038/nnano.2008.111 PMID: 18654567
9. Muller J, Huaux F, Fonseca A, Nagy JB, Moreau N, et al. (2008) Structural defects play a major role in the acute lung toxicity of multiwall carbon nanotubes: Toxicological aspects. Chemical Research in Toxicology 21: 1698-1705. doi: 10.1021/tx800101p PMID: 18636756
10. Wang X, Xia T, Addo Ntim S, Ji Z, Lin S, 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: 9772-9787. doi: 10.1021/nn2033055 PMID: 22047207
11. Ali-Boucetta H, Nunes A, Sainz R, Herrero MA, Tian B, et al. (2013) Asbestos-like pathogenicity of long carbon nanotubes alleviated by chemical functionalization. Angewandte Chemie 125: 2330-2334. doi: 10.1002/ange.201207664.
12. Lacerda L, Russier J, Pastorin G, Herrero MA, Venturelli E, et al. (2012) Translocation mechanisms of chemically functionalised carbon nanotubes across plasma membranes. Biomaterials 33: 3334-3343. doi: 10.1016/j.biomaterials.2012.01.024 PMID: 22289266
13. Sager TM, Wolfarth MW, Andrew M, Hubbs A, Friend S, et al. (2014) Effect of multi-walled carbon nanotube surface modification on bioactivity in the C57BL/6 mouse model. Nanotoxicology 8: 317-327. doi: 10.3109/17435390.2013.779757 PMID: 23432020
14. Kapralov AA, Feng WH, Amoscato AA, Yanamala N, Balasubramanian K, et al. (2012) Adsorption of surfactant lipids by single-walled carbon nanotubes in mouse lung upon pharyngeal aspiration. ACS Nano 6: 4147-4156. doi: 10.1021/nn300626q PMID: 22463369
15. Ma-Hock L, Treumann S, Strauss V, Brill S, Luizi F, et al. (2009) Inhalation toxicity of multiwall carbon nanotubes in rats exposed for 3 months. Toxicological Sciences 112: 468-481. doi: 10.1093/toxsci/ kfp146 PMID: 19584127
16. Poulsen SS, Jacobsen NR, Labib S, Wu D, Husain M, et al. (2013) Transcriptomic analysis reveals novel mechanistic insight into murine biological responses to multi-walled carbon nanotubes in lungs and cultured lung epithelial cells. PLoS ONE 8: e80452. doi: 10.1371/journal.pone.0080452 PMID: 24260392
17. Erdely A, Liston A, Salmen-Muniz R, Hulderman T, Young S-H, et al. (2011) Identification of systemic markers from a pulmonary carbon nanotube exposure: Journal of Occupational and Environmental Medicine 53: S80-S86. doi: 10.1097/JOM.0b013e31821ad724 PMID: 21654424
18. Girtsman TA, Beamer CA, Wu N, Buford M, Holian A (2014) IL-1R signalling is critical for regulation of multi-walled carbon nanotubes-induced acute lung inflammation in C57Bl/6 mice. Nanotoxicology 8: 17-27. doi: 10.3109/17435390.2012.744110 PMID: 23094697
19. Muller J, Huaux F, Moreau N, Misson P, Heilier J-F, et al. (2005) Respiratory toxicity of multi-wall carbon nanotubes. Toxicology and Applied Pharmacology 207: 221-231. doi: 10.1016/j.taap.2005.01.008 PMID: 16129115
20. Ronzani C, Spiegelhalter C, Vonesch J-L, Lebeau L, Pons F (2012) Lung deposition and toxicological responses evoked by multi-walled carbon nanotubes dispersed in a synthetic lung surfactant in the mouse. Archives of Toxicology 86: 137-149. doi: 10.1007/s00204-011-0741-y PMID: 21805258
21. Ryman-Rasmussen JP, Cesta MF, Brody AR, Shipley-Phillips JK, Everitt JI, et al. (2009) Inhaled carbon nanotubes reach the subpleural tissue in mice. Nature Nanotechnology 4: 747-751. doi: 10.1038/ nnano.2009.305 PMID: 19893520
22. Kobayashi N, Naya M, Ema M, Endoh S, Maru J, et al. (2010) Biological response and morphological assessment of individually dispersed multi-wall carbon nanotubes in the lung after intratracheal instillation in rats. Toxicology 276: 143-153. doi: 10.1016/j.tox.2010.07.021 PMID: 20696199
23. Al-Jamal KT, Nerl H, Müller KH, Ali-Boucetta H, Li S, et al. (2011) Cellular uptake mechanisms of functionalised multi-walled carbon nanotubes by 3D electron tomography imaging. Nanoscale 3: 2627.doi: 10.1039/c1nr10080g PMID: 21603701
24. Mu Q, Broughton DL, Yan B (2009) Endosomal leakage and nuclear translocation of multiwalled carbon nanotubes: Developing a model for cell uptake. Nano Letters 9: 4370-4375. doi: 10.1021/nl902647x PMID: 19902917
25. Pantarotto D, Singh R, McCarthy D, Erhardt M, Briand J-P, et al. (2004) Functionalized carbon nanotubes for plasmid DNA gene delivery. Angewandte Chemie International Edition 43: 5242-5246. doi: 10.1002/anie.200460437 PMID: 15455428
26. Marangon I, Boggetto N, Ménard-Moyon C, Venturelli E, Béoutis M-L, et al. (2012) Intercellular carbon nanotube translocation assessed by flow cytometry imaging. Nano Letters 12: 4830-4837. doi: 10. 1021/nl302273p PMID: 22928721
27. Købler C, Saber AT, Jacobsen NR, Wallin H, Vogel U, et al. (2014) FIB-SEM imaging of carbon nanotubes in mouse lung tissue. Analytical and Bioanalytical Chemistry. Available: http://link.springer.com/ 10.1007/s00216-013-7566-x. Accessed 2014 Feb 26.
28. Nanogenotox (2013) Towards a method for detecting the potential genotoxicity of nanomaterials. Available: www.nanogenotox.eu. Accessed 2014 Apr 28.
29. Porter DW, Hubbs AF, Chen BT, McKinneyW, Mercer RR, et al. (2013) Acute pulmonary dose- responses to inhaled multi-walled carbon nanotubes. Nanotoxicology 7: 1179-1194. doi: 10.3109/ 17435390.2012.719649 PMID: 22881873
30. Bhattacharya K, Andón FT, El-Sayed R, Fadeel B (2013) Mechanisms of carbon nanotube-induced toxicity: Focus on pulmonary inflammation. Advanced Drug Delivery Reviews 65: 2087-2097. doi: 10. 1016/j.addr.2013.05.012 PMID: 23751779
31. Ross MH (2011) Histology: a text and atlas: with correlated cell and molecular biology. 6th ed. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health. 974 p.
32. Persson H, Købler C, Mølhave K, Samuelson L, Tegenfeldt JO, et al. (2013) Fibroblasts cultured on nanowires exhibit low motility, impaired cell Division, and DNA Damage. Small 9: 4006-4016. doi: 10. 1002/smll.201300644 PMID: 23813871
33. Wierzbicki R, Købler C, Jensen MRB,Łopaciñska J, Schmidt MS, et al. (2013) Mapping the complex morphology of cell interactions with nanowire substrates using FIB-SEM. PLoS ONE 8: e53307. doi: 10.1371/journal.pone.0053307 PMID: 23326412
34. Elmore SA, Berridge BR, Boyle MC, Cora MC, Hoenerhoff MJ, et al. (2012) Proceedings of the 2012 national toxicology program satellite symposium. Toxicologic Pathology 41: 151-180. doi: 10.1177/ 0192623312467102 PMID: 23262640
35. Feldmesser M, Kress Y, Casadevall A (2001) Intracellular crystal formation as a mechanism of cytotoxicity in murine pulmonary Cryptococcus neoformans infection. Infection and Immunity 69: 2723-2727. doi: 10.1128/IAI.69.4.2723-2727.2001 PMID: 11254641
36. Guo L (2000) Biochemical characterization of endogenously formed eosinophilic crystals in the lungs of mice. Journal of Biological Chemistry 275: 8032-8037. doi: 10.1074/jbc.275.11.8032 PMID: 10713123 37.
37. Murray AB, Luz A (1990) Acidophilic macrophage pneumonia in laboratory mice. Vet Pathol 27: 274- 281. PMID: 2169666
38. Hoenerhoff MJ, StarostMF,Ward JM(2006) Eosinophilic crystalline pneumonia as amajor cause of death in 129S4/SvJaemice. Veterinary Pathology 43: 682-688. doi: 10.1354/vp.43-5-682 PMID: 16966445
39. Bourdon JA, Saber AT, Jacobsen NR, Jensen KA, Madsen AM, et al. (2012) Carbon black nanoparticle instillation induces sustained inflammation and genotoxicity in mouse lung and liver. Particle and Fibre Toxicology 9: 5. doi: 10.1186/1743-8977-9-5 PMID: 22300514
40. Saber AT, Lamson JS, Jacobsen NR, Ravn-Haren G, Hougaard KS, et al. (2013) Particle-induced pulmonary acute phase response correlates with neutrophil influx linking inhaled particles and cardiovascular risk. PLoS ONE 8: e69020. doi: 10.1371/journal.pone.0069020 PMID: 23894396
41. Nio J, Fujimoto W, Konno A, Kon Y, Owhashi M, et al. (2004) Cellular expression of murine Ym1 and Ym2, chitinase family proteins, as revealed by in situ hybridization and immunohistochemistry. Histochemistry and Cell Biology 121. Available: http://link.springer.com/10.1007/s00418-004-0654-4. Accessed 2013 Oct 4.
42. Waern I, Jia J, Pejler G, Zcharia E, Vlodavsky I, et al. (2010) Accumulation of Ym1 and formation of intracellular crystalline bodies in alveolar macrophages lacking heparanase. Molecular Immunology 47: 1467-1475. doi: 10.1016/j.molimm.2010.02.004 PMID: 20226534
43. Humbles AA, Lu B, Friend DS, Okinaga S, Lora J, et al. (2002) The murine CCR3 receptor regulates both the role of eosinophils and mast cells in allergen-induced airway inflammation and hyperresponsiveness. Proceedings of the National Academy of Sciences 99: 1479-1484. doi: 10.1073/pnas. 261462598 PMID: 11830666
44. Guo R-F, Lentsch AB, Warner RL, Huber-Lang M, Sarma JV, et al. (2001) Regulatory effects of eotaxin on acute lung inflammatory injury. The Journal of Immunology 166: 5208-5218. PMID: 11290805
45. Heath H, Qin S, Rao P, Wu L, LaRosa G, et al. (1997) Chemokine receptor usage by human eosinophils. The importance of CCR3 demonstrated using an antagonistic monoclonal antibody. Journal of Clinical Investigation 99: 178-184. doi: 10.1172/JCI119145 PMID: 9005985
46. Ben-Yehuda C, Bader R, Puxeddu I, Levi-Schaffer F, Breuer R, et al. (2008) Airway eosinophil accumulation and eotaxin-2/CCL24 expression following allergen challenge in BALB/c mice. Experimental Lung Research 34: 467-479. doi: 10.1080/01902140802220625 PMID: 18850374
47. Canton I, Battaglia G (2012) Endocytosis at the nanoscale. Chemical Society Reviews 41: 2718. doi: 10.1039/c2cs15309b PMID: 22389111
48. Wang X, Zang JJ, Wang H, Nie H, Wang TC, et al. (2010) Pulmonary toxicity in mice exposed to low and medium doses of water-soluble multi-walled carbon nanotubes. Journal of Nanoscience and Nanotechnology 10: 8516-8526. doi: 10.1166/jnn.2010.2688 PMID: 21121361
49. Treumann S, Ma-Hock L, Groters S, Landsiedel R, van Ravenzwaay B (2013) Additional histopathologic examination of the lungs from a 3-month inhalation toxicity study with multiwall carbon nanotubes in rats. Toxicological Sciences 134: 103-110. doi: 10.1093/toxsci/kft089 PMID: 23570993
50. Van Zweiten M., Zurcher C, Solleveld HA, Hollander CF (1981) Immunological techniques applied to aging research. Boca Raton, Fla: CRC Press. 236 p.
51. Teeguarden JG,Webb-Robertson B-J, Waters KM,Murray AR, Kisin ER, et al. (2010) Comparative proteomics and pulmonary toxicity of instilled single-walled carbon nanotubes, crocidolite asbestos, and ultrafine carbon black inmice. Toxicological Sciences 120: 123-135. doi: 10.1093/toxsci/kfq363 PMID: 21135415
52. Nygaard UC, Hansen JS, Samuelsen M, Alberg T, Marioara CD, et al. (2009) Single-walled and multiwalled carbon nanotubes promote allergic immune responses in mice. Toxicological Sciences 109: 113-123. doi: 10.1093/toxsci/kfp057 PMID: 19293371
53. PMID: 22300483Saber AT, Jacobsen N, Mortensen A, Szarek J, Jackson P, et al. (2012) Nanotitanium dioxide toxicity in mouse lung is reduced in sanding dust from paint. Particle and Fibre Toxicology 9: 4. doi: 10.1186/ 1743-8977-9-4 PMID: 22300483
54. Saber AT, Jensen KA, Jacobsen NR, Birkedal R, Mikkelsen L, et al. (2012) Inflammatory and genotoxic effects of nanoparticles designed for inclusion in paints and lacquers. Nanotoxicology 6: 453-471. doi: 10.3109/17435390.2011.587900 PMID: 21649461
55. Beamer CA, Girtsman TA, Seaver BP, Finsaas KJ,Migliaccio CT, et al. (2013) IL-33mediatesmulti-walled carbon nanotube (MWCNT)-induced airway hyper-reactivity via themobilization of innate helper cells in the lung. Nanotoxicology 7: 1070-1081. doi: 10.3109/17435390.2012.702230 PMID: 22686327
56. Inoue K, Koike E, Yanagisawa R, Hirano S, Nishikawa M, et al. (2009) Effects of multi-walled carbon nanotubes on a murine allergic airway inflammation model. Toxicology and Applied Pharmacology 237: 306-316. doi: 10.1016/j.taap.2009.04.003 PMID: 19371758
57. Andón FT, Kapralov AA, Yanamala N, Feng W, Baygan A, et al. (2013) Biodegradation of single-walled carbon nanotubes by eosinophil peroxidase. Small 9: 2721-2729. doi: 10.1002/smll.201202508 PMID: 23447468