Effect of fiber length on carbon nanotube-induced fibrogenesis

International Journal of Molecular Sciences

Volumn 15, Issue 5, 2014, Pages 7444-7461

  Manke, Amruta ^a   Luanpitpong, Sudjit ^a   Dong, Chenbo ^b   Wang, Liying ^c   He, Xiaoqing ^a   Battelli, Lori ^c   Derk, Raymond ^c   Stueckle, Todd A ^c   Porter, Dale W ^c   Sager, Tina ^c   Gou, Honglei ^b   Dinu, Cerasela Zoica ^b   Wu, Nianqiang ^b   Mercer, Robert R ^c   Rojanasakul, Yon ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b West Virginia University   (United States)

^c NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

Author keywords

Carbon nanotubes; Fiber length; Lung fibrosis; ROS; TGF ; Type I collagen

Indexed keywords

CARBON NANOTUBE; COLLAGEN TYPE 1; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA; CYTOTOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; ATOMIC FORCE MICROSCOPY; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY ASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBER LENGTH; FIBROGENESIS; FLUOROMETRY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; LUNG FIBROSIS; MALE; NONHUMAN; OXIDATIVE STRESS; PHYSICAL PARAMETERS; PROTEIN EXPRESSION; ROENTGEN SPECTROSCOPY; SCANNING ELECTRON MICROSCOPE; SIRCOL ASSAY; WESTERN BLOTTING; WST-1 ASSAY; CELL CULTURE; CELL SURVIVAL; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; FIBROBLAST; METABOLISM; PATHOLOGY; TOXICITY;

CELL SURVIVAL; CELLS, CULTURED; COLLAGEN TYPE I; CYTOTOXINS; FIBROBLASTS; HUMANS; NANOTUBES, CARBON; OXIDATIVE STRESS; PULMONARY FIBROSIS; REACTIVE OXYGEN SPECIES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84899756674     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15057444     Document Type: Article

References (42)

1. 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.
2. Oberdörster, G.; Maynard, A.; Donaldson, K.; Castranova, V.; Fitzpatrick, J.; Ausman, K.; Carter, J.; Karn, B.; Kreyling, W.; Lai, D.; et al. Principles for characterizing the potential human health effects from exposure to nanomaterials: Elements of a screening strategy. Part. Fibre Toxicol. 2005, 2, 8.
3. Lam, C.; James, J. T.; McCluskey, R.; Hunter, R. L. Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol. Sci. 2004, 77, 126-134.
4. Kolosnjaj, J.; Szwarc, H.; Moussa, F. Toxicity studies of carbon nanotubes. Adv. Exp. Med. Biol. 2007, 620, 181-204.
5. Jaurand, M. F.; Renier, A.; Daubriac, J. Mesothelioma: Do asbestos and carbon nanotubes pose the same health risk? Part. Fibre Toxicol. 2009, 6, 16.
6. Stella, G. M. Carbon nanotubes and pleural damage: Perspectives of nanosafety in the light of asbestos experience. Biointerphases 2011, 6, P1-P17.
7. Shvedova, A. A.; Kisin, E. R.; Mercer, R.; Murray, A. R.; Johnson, V. J.; Potapovich, A. I.; Tyurina, Y. Y.; 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.
8. Shvedova, A. A.; Kisin, E.; Murray, A. R.; Johnson, V. J.; Gorelik, O.; Arepalli, S.; Hubbs, A. F.; Mercer, R. R.; 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.
9. Mercer, R. R.; Scabilloni, J.; Wang, L.; Kisin, E.; Murray, A. R.; Schwegler-Berry, D.; Shvedova, A. A.; Castranova, V. Alteration of deposition pattern and pulmonary response as a result of improved dispersion of aspirated single-walled carbon nanotubes in a mouse model. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294, L87-L97.
10. Park, E.; Roh, J.; Kim, S.; Kang, M.; Han, Y.; Kim, Y.; Hong, J. T.; Choi, K. A single intratracheal instillation of single-walled carbon nanotubes induced early lung fibrosis and subchronic tissue damage in mice. Arch. Toxicol. 2011, 85, 1121-1131.
11. Poland, C. A.; Duffin, R.; Kinloch, I.; Maynard, A.; Wallace, W. A. H.; 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.
12. Murphy, F. A.; Poland, C. A.; Duffin, R.; Al-Jamal, K.; Ali-Boucetta, H.; Nunes, A.; Byrne, F.; Prina-Mello, A.; Volkov, Y.; Li, S.; et al. Length-dependent retention of carbon nanotubes in the pleural space of mice initiates sustained inflammation and progressive fibrosis on the parietal pleura. Am. J. Pathol. 2011, 178, 2587-2600.
13. Liu, J.; Legros, S.; Ma, G.; Veinot, J. G. C.; von, D. K.; Hofmann, T. Influence of surface functionalization and particle size on the aggregation kinetics of engineered nanoparticles. Chemosphere 2012, 87, 918-924.
14. Palomäki, J.; Välimäki, E.; Sund, J.; Vippola, M.; Clausen, P. A.; Jensen, K. A.; Savolainen, K.; Matikainen, S.; Alenius, H. Long, needle-like carbon nanotubes and asbestos activate the nlrp3 inflammasome through a similar mechanism. ACS Nano 2011, 5, 6861-6870.
15. Vietti, G.; Ibouraadaten, S.; Palmai-Pallag, M.; Yakoub, Y.; Bailly, C.; Fenoglio, I.; Marbaix, E.; Lison, D.; van den Brule, S. Towards predicting the lung fibrogenic activity of nanomaterials: Experimental validation of an in vitro fibroblast proliferation assay. Part. Fibre Toxicol. 2013, 10, 52.
16. Wang, L.; Castranova, V.; Mishra, A.; Chen, B.; Mercer, R. R.; 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.
17. Wang, L.; Mercer, R. R.; Rojanasakul, Y.; Qiu, A.; Lu, Y.; Scabilloni, J. F.; 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.
18. Murray, A. R.; Kisin, E. R.; Tkach, A. V.; Yanamala, N.; Mercer, R.; Young, S.; Fadeel, B.; Kagan, V. E.; Shvedova, A. A. Factoring-in agglomeration of carbon nanotubes and nanofibers for better prediction of their toxicity versus asbestos. Part. Fibre Toxicol. 2012, 9, 10.
19. Leask, A.; Abraham, D. J. TGF-β signaling and the fibrotic response. FASEB J. 2004, 18, 816-827.
20. Rhyu, D. Y.; Yang, Y.; Ha, H.; Lee, G. T.; Song, J. S.; Uh, S.; Lee, H. B. Role of reactive oxygen species in TGF-β1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J. Am. Soc. Nephrol. 2005, 16, 667-675.
21. Porter, D. W.; Hubbs, A. F.; Mercer, R. R.; Wu, N.; Wolfarth, M. G.; 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.
22. Mercer, R. R.; Hubbs, A. F.; Scabilloni, J. F.; Wang, L.; Battelli, L. A.; Friend, S.; Castranova, V.; Porter, D. W. Pulmonary fibrotic response to aspiration of multi-walled carbon nanotubes. Part. Fibre Toxicol. 2011, 8, 21.
23. Shvedova, A. A.; Kapralov, A. A.; Feng, W. H.; Kisin, E. R.; Murray, A. R.; Mercer, R. R.; St Croix, C. M.; Lang, M. A.; Watkins, S. C.; Konduru, N. V.; et al. Impaired clearance and enhanced pulmonary inflammatory/fibrotic response to carbon nanotubes in myeloperoxidase-deficient mice. PLoS One 2012, 7, e30923.
24. Johnston, H. J.; Hutchison, G. R.; Christensen, F. M.; Peters, S.; Hankin, S.; Aschberger, K.; Stone, V. A critical review of the biological mechanisms underlying the in vivo and in vitro toxicity of carbon nanotubes: The contribution of physico-chemical characteristics. Nanotoxicology 2010, 4, 207-246.
25. Chang, C.; Tsai, M.; Huang, H.; Chen, C.; Dai, S. Epithelial-mesenchymal transition contributes to SWCNT-induced pulmonary fibrosis. Nanotoxicology 2012, 6, 600-610.
26. Mangum, J. B.; Turpin, E. A.; Antao-Menezes, A.; Cesta, M. F.; Bermudez, E.; Bonner, J. C. Single-walled carbon nanotube (SWCNT)-induced interstitial fibrosis in the lungs of rats is associated with increased levels of PDGF mRNA and the formation of unique intercellular carbon structures that bridge alveolar macrophages in situ. Part. Fibre Toxicol. 2006, 3, 15.
27. He, X.; Young, S. H.; Fernback, J. E.; Ma, Q. Single-walled carbon nanotubes induce fibrogenic effect by disturbing mitochondrial oxidative stress and activating NF-κb signaling. J. Clin. Toxicol. 2012, 2012, doi: 10. 4172/2161-0495. S5-005.
28. Sharma, C. S.; Sarkar, S.; Periyakaruppan, A.; Barr, J.; Wise, K.; Thomas, R.; Wilson, B. L.; Ramesh, G. T. Single-walled carbon nanotubes induces oxidative stress in rat lung epithelial cells. J. Nanosci. Nanotechnol. 2007, 7, 2466-2472.
29. Kagan, V. E.; Tyurina, Y. Y.; Tyurin, V. A.; Konduru, N. V.; Potapovich, A. I.; Osipov, A. N.; Kisin, E. R.; Schwegler-Berry, D.; Mercer, R.; Castranova, V.; et al. Direct and indirect effects of single walled carbon nanotubes on RAW 264. 7 macrophages: Role of iron. Toxicol. Lett. 2006, 165, 88-100.
30. Pacurari, M.; Yin, X. J.; Zhao, J.; Ding, M.; Leonard, S. S.; Schwegler-Berry, D.; Ducatman, B. S.; Sbarra, D.; Hoover, M. D.; Castranova, V.; et al. Raw single-wall carbon nanotubes induce oxidative stress and activate MAPKs, AP-1, NF-κB, and Akt in normal and malignant human mesothelial cells. Environ. Health Perspect. 2008, 116, 1211-1217.
31. Azad, N.; Iyer, A. K. V.; 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.
32. Bonner, J. C. Lung fibrotic responses to particle exposure. Toxicol. Pathol. 2007, 35, 148-153.
33. Shvedova, A. A.; Castranova, V.; Kisin, E. R.; Schwegler-Berry, D.; Murray, A. R.; Gandelsman, V. Z.; Maynard, A.; Baron, P. Exposure to carbon nanotube material: Sssessment of nanotube cytotoxicity using human keratinocyte cells. J. Toxicol. Environ. Health A 2003, 66, 1909-1926.
34. Liu, D.; Wang, L.; Wang, Z.; Cuschieri, A. Different cellular response mechanisms contribute to the length-dependent cytotoxicity of multi-walled carbon nanotubes. Nanoscale Res. Lett. 2012, 7, 361-361.
35. Tabet, L.; Bussy, C.; Amara, N.; Setyan, A.; Grodet, A.; Rossi, M. J.; Pairon, J. C.; Boczkowski, J.; Lanone, S. Adverse effects of industrial multiwalled carbon nanotubes on human pulmonary cells. J. Toxicol. Environ. Health A 2009, 72, 60-73.
36. Ding, L.; Stilwell, J.; Zhang, T.; Elboudwarej, O.; Jiang, H.; Selegue, J. P.; Cooke, P. A.; Gray, J. W.; Chen, F. F. Molecular characterization of the cytotoxic mechanism of multiwall carbon nanotubes and nano-onions on human skin fibroblast. Nano Lett. 2005, 5, 2448-2464.
37. 2-generating NADH oxidase in human lung fibroblasts by transforming growth factor beta 1. J. Biol. Chem. 1995, 270, 30334-30338.
38. Fernandez, I. E.; Eickelberg, O. The impact of TGF-β on lung fibrosis: From targeting to biomarkers. Proc. Am. Thorac. Soc. 2012, 9, 111-116.
39. Wang, P.; Nie, X.; Wang, Y.; Li, Y.; Ge, C.; Zhang, L.; Wang, L.; Bai, R.; Chen, Z.; Zhao, Y.; et al. Multiwall carbon nanotubes mediate macrophage activation and promote pulmonary fibrosis through TGF-β/Smad signaling pathway. Small 2013, 9, 3799-3811.
40. Yu, Q.; Stamenkovic, I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-β and promotes tumor invasion and angiogenesis. Genes Dev. 2000, 14, 163-176.
41. Muller, J.; Huaux, F.; Moreau, N.; Misson, P.; Heilier, J.-F.; Delos, M.; Arras, M.; Fonseca, A.; Nagy, J. B.; Lison, D. Respiratory toxicity of multi-wall carbon nanotubes. Toxicol. Appl. Pharmacol. 2005, 207, 221-231.
42. Mercer, R. R.; Scabilloni, J. F.; Hubbs, A. F.; Battelli, L. A.; McKinney, W.; Friend, S.; Wolfarth, M. G.; Andrew, M.; Castranova, V.; Porter, D. W. Distribution and fibrotic response following inhalation exposure to multi-walled carbon nanotubes. Part. Fibre Toxicol. 2013, 10, 33.