Apoptotic, inflammatory, and fibrogenic effects of two different types of multi-walled carbon nanotubes in mouse lung

Archives of Toxicology

Volumn 88, Issue 9, 2014, Pages 1725-1737

  Van Berlo, D ^a,b   Wilhelmi, V ^a   Boots, A W ^a,c   Hullmann, M ^a   Kuhlbusch, T A J ^d,e   Bast, A ^c   Schins, R P F ^a   Albrecht, C ^a,b  

^a IUF LEIBNIZ RESEARCH INSTITUTE FOR ENVIRONMENTAL MEDICINE   (Germany)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d Air Quality and Sustainable Nanotechnology   (Germany)

^e UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Apoptosis; Fibrosis; Inflammation; Lung; Macrophage; Multi walled carbon nanotubes

Indexed keywords

CASPASE 3; HEME OXYGENASE 1; HYDROGEN PEROXIDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MULTI WALLED NANOTUBE; NEUTROPHIL COLLAGENASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; BIOLOGICAL MARKER; CARBON NANOTUBE; PARTICULATE MATTER; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL HYPERPLASIA; CHEMICAL COMPOSITION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; FIBROGENESIS; GENE EXPRESSION; HISTIOCYTOSIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; LUNG FIBROSIS; LUNG GRANULOMA; LUNG TOXICITY; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ADMINISTRATION AND DOSAGE; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; COMPARATIVE STUDY; DRUG EFFECTS; FIBROSIS; GERMFREE ANIMAL; IMMUNOLOGY; INHALATIONAL DRUG ADMINISTRATION; LUNG; MACROPHAGE ACTIVATION; METABOLISM; PARTICLE SIZE; PARTICULATE MATTER; PATHOLOGY; PNEUMONIA; RESPIRATORY TRACT MUCOSA; SCANNING ELECTRON MICROSCOPY; TOXICITY; TRANSFORMED CELL LINE; ULTRASTRUCTURE;

MUS;

ADMINISTRATION, INHALATION; ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CELL LINE, TRANSFORMED; FEMALE; FIBROSIS; HYDROGEN PEROXIDE; LUNG; MACROPHAGE ACTIVATION; MACROPHAGES; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, SCANNING; NANOTUBES, CARBON; PARTICLE SIZE; PARTICULATE MATTER; PNEUMONIA; REACTIVE OXYGEN SPECIES; RESPIRATORY MUCOSA; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 84906216751     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1220-z     Document Type: Article

References (65)

1. Beamer CA, Holian A (2007) Antigen-presenting cell population dynamics during murine silicosis. Am J Respir Cell Mol Biol 37:729-738 (Pubitemid 350211643)
2. Cho HY, Reddy SP, Kleeberger SR (2006) Nrf2 defends the lung from oxidative stress. Antioxid Redox Signal 8:76-87 (Pubitemid 43324533)
3. Clift MJ, Endes C, Vanhecke D, Wick P, Gehr P, Schins RP, Petri-Fink A, Rothen-Rutishauser B (2014) A comparative study of different in vitro lung cell culture systems to assess the most beneficial tool for screening the potential adverse effects of carbon nanotubes. Toxicol Sci 137:55-64
4. Davis JM, Ramakrishnan L (2009) The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136:37-49
5. De Volder MF, Tawfick SH, Baughman RH, Hart AJ (2013) Carbon nanotubes: present and future commercial applications. Science 339:535-539
6. Di Giorgio ML, Di Bucchianico S, Ragnelli AM, Aimola P, Santucci S, Poma A (2011) Effects of single and multi walled carbon nanotubes on macrophages: cyto and genotoxicity and electron microscopy. Mutat Res 722:20-31
7. Doll NJ, Stankus RP, Barkman HW (1983) Immunopathogenesis of asbestosis, silicosis, and coal workers' pneumoconiosis. Clin Chest Med 4:3-14 (Pubitemid 13095102)
8. Donaldson K (2000) Nonneoplastic lung responses induced in experimental animals by exposure to poorly soluble nonfibrous particles. Inhal Toxicol 12:121-139
9. Donaldson K, Aitken R, Tran L, Stone V, Duffin R, Forrest G, Alexander A (2006) Carbon nanotubes: a review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol Sci 92:5-22 (Pubitemid 43985785)
10. Donaldson K, Murphy FA, Duffin R, Poland CA (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. Particle Fibre Toxicol 7:5
11. Driscoll KE, Lindenschmidt RC, Maurer JK, Higgins JM, Ridder G (1990) Pulmonary response to silica or titanium dioxide: inflammatory cells, alveolar macrophage-derived cytokines, and histopathology. Am J Respir Cell Mol Biol 2:381-390
12. Elgrabli D, Abella-Gallart S, Robidel F, Rogerieux F, Boczkowski J, Lacroix G (2008) Induction of apoptosis and absence of inflammation in rat lung after intratracheal instillation of multiwalled carbon nanotubes. Toxicology 253:131-136
13. Fairbairn IP (2004) Macrophage apoptosis in host immunity to mycobacterial infections. Biochem Soc Trans 32:496-498
14. Gasser M, Wick P, Clift MJ, Blank F, Diener L, Yan B, Gehr P, Krug HF, Rothen-Rutishauser B (2012) Pulmonary surfactant coating of multi-walled carbon nanotubes (MWCNTs) influences their oxidative and pro-inflammatory potential in vitro. Part Fibre Toxicol 9:17
15. Hansen K, Mossman BT (1987) Generation of superoxide (O2-.) from alveolar macrophages exposed to asbestiform and nonfibrous particles. Cancer Res 47:1681-1686 (Pubitemid 17044503)
16. Hirano S, Kanno S, Furuyama A (2008) Multi-walled carbon nanotubes injure the plasma membrane of macrophages. Toxicol Appl Pharmacol 232:244-251
17. Jaurand MC, Renier A, Daubriac J (2009) Mesothelioma: do asbestos and carbon nanotubes pose the same health risk? Part Fibre Toxicol 6:16
18. Kane AB, MacDonald JL, Moalli PA (1986) Acute injury and regeneration of mesothelial cells produced by crocidolite asbestos fibers. Am Rev Respir Dis 133:A198
19. Kato T, Totsuka Y, Ishino K, Matsumoto Y, Tada Y, Nakae D, Goto S, Masuda S, Ogo S, Kawanishi M, Yagi T, Matsuda T, Watanabe M, Wakabayashi K (2013) Genotoxicity of multi-walled carbon nanotubes in both in vitro and in vivo assay systems. Nanotoxicology 7:452-461
20. Kermanizadeh A, Pojana G, Gaiser BK, Birkedal R, Bilanicova D, Wallin H, Jensen KA, Sellergren B, Hutchison GR, Marcomini A, Stone V (2013) In vitro assessment of engineered nanomaterials using a hepatocyte cell line: cytotoxicity, pro-inflammatory cytokines and functional markers. Nanotoxicology 7:301-313
21. Kim JE, Lim HT, Minai-Tehrani A, Kwon JT, Shin JY, Woo CG, Choi M, Baek J, Jeong DH, Ha YC, Chae CH, Song KS, Ahn KH, Lee JH, Sung HJ, Yu IJ, Beck GR Jr, Cho MH (2010) Toxicity and clearance of intratracheally administered multiwalled carbon nanotubes from murine lung. J Toxicol Environ Health A 73:1530-1543
22. Kisin ER, Murray AR, Sargent L, Lowry D, Chirila M, Siegrist KJ, Schwegler-Berry D, Leonard S, Castranova V, Fadeel B, Kagan VE, Shvedova AA (2011) Genotoxicity of carbon nanofibers: are they potentially more or less dangerous than carbon nanotubes or asbestos? Toxicol Appl Pharmacol 252:1-10
23. Kobayashi N, Naya M, Ema M, Endoh S, Maru J, Mizuno K, Nakanishi J (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
24. Koerten HK, Hazekamp J, Kroon M, Daems WT (1990) Asbestos body formation and iron accumulation in mouse peritoneal granulomas after the introduction of crocidolite asbestos fibers. Am J Pathol 136:141-157 (Pubitemid 20034961)
25. Kuwano K, Miyazaki H, Hagimoto N, Kawasaki M, Fujita M, Kunitake R, Kaneko Y, Hara N (1999) The involvement of Fas-Fas ligand pathway in fibrosing lung diseases. Am J Respir Cell Mol Biol 20:53-60 (Pubitemid 129504842)
26. Leigh J, Wang H, Bonin A, Peters M, Ruan X (1997) Silica-induced apoptosis in alveolar and granulomatous cells in vivo. Environ Health Perspect 105(Suppl 5):1241-1245
27. Li JG, Li WX, Xu JY, Cai XQ, Liu RL, Li YJ, Zhao QF, Li QN (2007a) Comparative study of pathological lesions induced by multiwalled carbon nanotubes in lungs of mice by intratracheal instillation and inhalation. Environ Toxicol 22:415-421
28. Li Z, Hulderman T, Salmen R, Chapman R, Leonard S, Young SH, Shvedova A, Luster MI, Simeonova PP (2007b) Cardiovascular effects of pulmonary exposure to single-wall carbon nanotubes. Environ Health Perspect 115:377-382 (Pubitemid 46554435)
29. Liang J, Jung Y, Tighe RM, Xie T, Liu N, Leonard M, Gunn MD, Jiang D, Noble PW (2012) A macrophage subpopulation recruited by C chemokine ligand-2 clears apoptotic cells in noninfectious lung injury. Am J Physiol Lung Cell Mol Physiol 302:L933-L940
30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408 (Pubitemid 34164012)
31. Luo M, Deng X, Shen X, Dong L, Liu Y (2012) Comparison of cytotoxicity of pristine and covalently functionalized multi-walled carbon nanotubes in RAW 264.7 macrophages. J Nanosci Nanotechnol 12:274-283
32. Mariani TJ, Roby JD, Mecham RP, Parks WC, Crouch E, Pierce RA (1996) Localization of type I procollagen gene expression in sil-ica- induced granulomatous lung disease and implication of transforming growth factor-beta as a mediator of fibrosis. Am J Pathol 148:151-164 (Pubitemid 26019653)
33. Mercer R, Hubbs AF, Scabilloni JF, Wang L, Battelli LA, Friend S, Castranova V, Porter DW (2011) Pulmonary fibrotic response to aspiration of multi-walled carbon nanotubes. Particle Fibre Toxicol 8:21
34. Miller BG, Searl A, Davis JM, Donaldson K, Cullen RT, Bolton RE, Buchanan D, Soutar CA (1999) Influence of fibre length, dissolution and biopersistence on the production of mesothelioma in the rat peritoneal cavity. Ann Occup Hyg 43:155-166 (Pubitemid 29225213)
35. Mitchell LA, Gao J, Wal RV, Gigliotti A, Burchiel SW, McDonald JD (2007) Pulmonary and systemic immune response to inhaled multiwalled carbon nanotubes. Toxicol Sci 100:203-214 (Pubitemid 47617817)
36. Moolgavkar SH, Brown RC, Turim J (2001) Biopersistence, fiber length, and cancer risk assessment for inhaled fibers. Inhal Toxicol 13:755-772 (Pubitemid 32929240)
37. Mossman BT (2000) Mechanisms of action of poorly soluble particulates in overload-related lung pathology. Inhal Toxicol 12:141-148
38. Muhlfeld C, Poland CA, Duffin R, Brandenberger C, Murphy FA, Rothen-Rutishauser B, Gehr P, Donaldson K (2012) Differential effects of long and short carbon nanotubes on the gas-exchange region of the mouse lung. Nanotoxicology 6:867-879
39. Muller J, Huaux F, Moreau N, Misson P, Heilier JF, Delos M, Arras M, Fonseca A, Nagy JB, Lison D (2005) Respiratory toxicity of multi-wall carbon nanotubes. Toxicol Appl Pharmacol 207:221-231 (Pubitemid 41207915)
40. Murphy FA, Schinwald A, Poland CA, Donaldson K (2012) The mechanism of pleural inflammation by long carbon nanotubes: interaction of long fibres with macrophages stimulates them to amplify pro-inflammatory responses in mesothelial cells. Part Fibre Toxicol 9:8
41. Nagatomo H, Morimoto Y, Oyabu T, Hirohashi M, Ogami A, Yamato H, Kuroda K, Higashi T, Tanaka I (2005) Expression of heme oxygenase-1 in the lungs of rats exposed to crocidolite asbestos. Inhal Toxicol 17:293-296 (Pubitemid 40563311)
42. Niu J, Kolattukudy PE (2009) Role of MCP-1 in cardiovascular disease: molecular mechanisms and clinical implications. Clin Sci 117:95-109
43. Oberdorster G (1996) Evaluation and use of animal models to assess mechanisms of fibre carcinogenicity. IARC Sci Publ 140:107-125
44. Osmond-McLeod MJ, Poland CA, Murphy F, Waddington L, Morris H, Hawkins SC, Clark S, Aitken R, McCall MJ, Donaldson K (2011) Durability and inflammogenic impact of carbon nanotubes compared with asbestos fibres. Parti Fibre Toxicol 8:15
45. Pacurari M, Qian Y, Fu W, Schwegler-Berry D, Ding M, Castranova V, Guo NL (2012) Cell permeability, migration, and reactive oxygen species induced by multiwalled carbon nanotubes in human microvascular endothelial cells. J Toxicol Environ Health A 75:129-147
46. Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WA, Seaton A, Stone V, Brown S, Macnee W, Donaldson K (2008) Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol 3:423-428
47. Porter DW, Ramsey D, Hubbs AF, Battelli L, Ma J, Barger M, Landsittel D, Robinson VA, McLaurin J, Khan A, Jones W, Teass A, Castranova V (2001) Time course of pulmonary response of rats to inhalation of crystalline silica: histological results and biochemical indices of damage, lipidosis, and fibrosis. J Environ Pathol Toxicol Oncol 20(Suppl 1):1-14 (Pubitemid 32879947)
48. Roda E, Coccini T, Acerbi D, Barni S, Vaccarone R, Manzo L (2011) Comparative pulmonary toxicity assessment of pristine and functionalized multi-walled carbon nanotubes intratracheally instilled in rats: morphohistochemical evaluations. Histol Histopathol 26:357-367
49. Sabo-Attwood T, Ramos-Nino M, Bond J, Butnor KJ, Heintz N, Gruber AD, Steele C, Taatjes DJ, Vacek P, Mossman BT (2005) Gene expression profiles reveal increased mClca3 (Gob5) expression and mucin production in a murine model of asbestos-induced fibrogenesis. Am J Pathol 167:1243-1256 (Pubitemid 41541411)
50. Sato T, Takeno M, Honma K, Yamauchi H, Saito Y, Sasaki T, Morikubo H, Nagashima Y, Takagi S, Yamanaka K, Kaneko T, Ishigatsubo Y (2006) Heme oxygenase-1, a potential biomarker of chronic silicosis, attenuates silica-induced lung injury. Am J Respir Crit Care Med 174:906-914 (Pubitemid 44564791)
51. Schinwald A, Chernova T, Donaldson K (2012a) Use of silver nanowires to determine thresholds for fibre length-dependent pulmonary inflammation and inhibition of macrophage migration in vitro. Part Fibre Toxicol 9:47
52. Schinwald A, Murphy FA, Prina-Mello A, Poland CA, Byrne F, Movia D, Glass JR, Dickerson JC, Schultz DA, Jeffree CE, Macnee W, Donaldson K (2012b) The threshold length for fiber-induced acute pleural inflammation: shedding light on the early events in asbestos-induced mesothelioma. Toxicol Sci 128:461-470
53. Sohaebuddin SK, Thevenot PT, Baker D, Eaton JW, Tang L (2010) Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol 7:22
54. Stone V, Johnston H, Schins RP (2009) Development of in vitro systems for nanotoxicology: methodological considerations. Crit Rev Toxicol 39:613-626
55. Suga M, Iyonaga K, Ichiyasu H, Saita N, Yamasaki H, Ando M (1999) Clinical significance of MCP-1 levels in BALF and serum in patients with interstitial lung diseases. Eur Respir J 14:376-382 (Pubitemid 29461305)
56. Takaya M, Serita F, Yamazaki K, Aiso S, Kubota H, Asakura M, Ikawa N, Nagano K, Arito H, Fukushima S (2010) Characteristics of multiwall carbon nanotubes for an intratracheal instillation study with rats. Ind Health 48:452-459
57. Tanaka T, Terada M, Ariyoshi K, Morimoto K (2010) Monocyte chemoattractant protein-1/C chemokine ligand 2 enhances apoptotic cell removal by macrophages through Rac1 activation. Biochem Biophys Res Commun 399:677-682
58. van Berlo D, Wessels A, Boots AW, Wilhelmi V, Scherbart AM, Gerloff K, van Schooten FJ, Albrecht C, Schins RP (2010) Neutro-phil- derived ROS contribute to oxidative DNA damage induction by quartz particles. Free Radic Biol Med 49:1685-1693
59. van Berlo D, Clift MJ, Albrecht C, Schins RP (2012) Carbon nanotubes: an insight into the mechanisms of their potential genotoxicity. Swiss Med Wkly 142:w13698
60. Vietti G, Ibouraadaten S, Palmai-Pallag M, Yakoub Y, Bailly C, Fenoglio I, Marbaix E, Lison D, van den Brule S (2013) Towards predicting the lung fibrogenic activity of nanomaterials: experimental validation of an in vitro fibroblast proliferation assay. Part Fibre Toxicol 10:52
61. Wang X, Jia G, Wang H, Nie H, Yan L, Deng XY, Wang S (2009) Diameter effects on cytotoxicity of multi-walled carbon nanotubes. J Nanosci Nanotechnol 9:3025-3033
62. Wang X, Katwa P, Podila R, Chen P, Ke PC, Rao AM, Walters DM, Wingard CJ, Brown JM (2011) Multi-walled carbon nanotube instillation impairs pulmonary function in C57BL/6 mice. Part Fibre Toxicol 8:24
63. Wang X, Guo J, Chen T, Nie H, Wang H, Zang J, Cui X, Jia G (2012) Multi-walled carbon nanotubes induce apoptosis via mitochondrial pathway and scavenger receptor. Toxicol In Vitro 26:799-806
64. Wilhelmi V, Fischer U, van Berlo D, Schulze-Osthoff K, Schins RP, Albrecht C (2012) Evaluation of apoptosis induced by nanoparticles and fine particles in RAW 264.7 macrophages: facts and artefacts. Toxicol In Vitro 26:323-334
65. Yao SQ, Rojanasakul LW, Chen ZY, Xu YJ, Bai YP, Chen G, Zhang XY, Zhang CM, Yu YQ, Shen FH, Yuan JX, Chen J, He QC (2011) Fas/FasL pathway-mediated alveolar macrophage apoptosis involved in human silicosis. Apoptosis 16:1195-1204