Advances in mechanisms and signaling pathways of carbon nanotube toxicity

Nanotoxicology

Volumn 9, Issue 5, 2015, Pages 658-676

  Dong, Jie ^a   Ma, Qiang ^a  

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

Author keywords

Carbon nanotubes; Fiber toxicity; Mechanism; Nanotoxicology; Signaling pathway

Indexed keywords

CARBON NANOTUBE; CRYOPYRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P53; TRANSFORMING GROWTH FACTOR BETA1;

CARCINOGENICITY; CELL PROLIFERATION; CYTOTOXICITY; FIBROSIS; GENOTOXICITY; HUMAN; IMMUNE SYSTEM; IMMUNOTOXICITY; INFLAMMATION; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; NANOTECHNOLOGY; NANOTOXICOLOGY; NONHUMAN; OXIDATIVE STRESS; PATHOGENICITY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; RIGIDITY; RISK ASSESSMENT; SIGNAL TRANSDUCTION; SOLUBILITY; SURFACE AREA; ADVERSE EFFECTS; ANIMAL; CHEMISTRY; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; PARTICLE SIZE; PROCEDURES; STANDARDS; SURFACE PROPERTY; TRENDS;

MAMMALIA;

ANIMALS; CELL PROLIFERATION; ENVIRONMENTAL EXPOSURE; HUMANS; INFLAMMATION; NANOTECHNOLOGY; NANOTUBES, CARBON; OXIDATIVE STRESS; PARTICLE SIZE; RISK ASSESSMENT; SIGNAL TRANSDUCTION; SOLUBILITY; SURFACE PROPERTIES;

EID: 84937864661     PISSN: 17435390     EISSN: 17435404     Source Type: Journal    
DOI: 10.3109/17435390.2015.1009187     Document Type: Review

References (162)

1. Adamson IY, Bakowska J, Bowden DH. 1993. Mesothelial cell proliferation after instillation of long or short asbestos fibers into mouse lung. Am J Pathol 142:1209-16.
2. Aiso S, Yamazaki K, Umeda Y, Asakura M, Kasai T, Takaya M, et al. 2010. Pulmonary toxicity of intratracheally instilled multiwall carbon nanotubes in male Fischer 344 rats. Ind Health 48:783-95.
3. Alarifi S, Ali D, Verma A, Almajhdi FN, Al-Qahtani AA. 2014. Singlewalled carbon nanotubes induce cytotoxicity and DNA damage via reactive oxygen species in human hepatocarcinoma cells. In Vitro Cell Dev Biol Anim 50:714-22.
4. Arthur JS, Ley SC. 2013. Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol 13:679-92.
5. Azad N, Iyer AK, Wang L, Liu Y, Lu Y, Rojanasakul Y. 2013. Reactive oxygen species-mediated p38 MAPK regulates carbon nanotubeinduced fibrogenic and angiogenic responses. Nanotoxicology 7: 157-68.
6. Bergsbaken T, Fink SL, Cookson BT. 2009. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7:99-109.
7. Borm PJ, Schins RP, Albrecht C. 2004. Inhaled particles and lung cancer, part B: paradigms and risk assessment. Int J Cancer, 110:3-14.
8. Bottini M, Bruckner S, Nika K, Bottini N, Bellucci S, Magrini A, et al. 2006. Multi-walled carbon nanotubes induce T lymphocyte apoptosis. Toxicol Lett 160:121-6.
9. Brown DM, Dickson C, Duncan P, Al-Attili F, Stone V. 2010. Interaction between nanoparticles and cytokine proteins: impact on protein and particle functionality. Nanotechnology 21:215104.
10. Brown DM, Kinloch IA, Bangert U, Windle AH, Walters DM, Walker GS, et al. 2007. An in vitro study of the potential of carbon nanotubes and nanofibres to induce inflammation mediators and frustrated phagocytosis. Carbon 45:1743-56.
11. Carrero-Sanchez JC, Elias AL, Mancilla R, Arrellin G, Terrones H, Laclette JP, et al. 2006. Biocompatibility and toxicological studies of carbon nanotubes doped with nitrogen. Nano Lett 6:1609-16.
12. Case BW, Abraham JL, Meeker G, Pooley FD, Pinkerton KE. 2011. Applying definitions of ''asbestos'' to environmental and ''low-dose'' exposure levels and health effects, particularly malignant mesothelioma. J Toxicol Environ Health B Crit Rev 14:3-39.
13. Cassel SL, Eisenbarth SC, Iyer SS, Sadler JJ, Colegio OR, Tephly LA, et al. 2008. The Nalp3 inflammasome is essential for the development of silicosis. Proc Natl Acad Sci USA 105:9035-40.
14. Chang CC, Tsai ML, Huang HC, Chen CY, Dai SX. 2012. Epithelialmesenchymal transition contributes to SWCNT-induced pulmonary fibrosis. Nanotoxicology 6:600-10.
15. Chaudhury A, Howe PH. 2009. The tale of transforming growth factor-beta (TGFbeta) signaling: A soigne enigma. IUBMB Life 61: 929-39.
16. Chen T, Nie H, Gao X, Yang J, Pu J, Chen Z, et al. 2014. Epithelialmesenchymal transition involved in pulmonary fibrosis induced by multi-walled carbon nanotubes via TGF-beta/Smad signaling pathway. Toxicol Lett 226:150-62.
17. Cheng WW, Lin ZQ, Wei BF, Zeng Q, Han B, Wei CX, et al. 2011. Single-walled carbon nanotube induction of rat aortic endothelial cell apoptosis: reactive oxygen species are involved in the mitochondrial pathway. Int J Biochem Cell Biol 43:564-72.
18. Chou CC, Hsiao HY, Hong QS, Chen CH, Peng YW, Chen HW, et al. 2008. Single-walled carbon nanotubes can induce pulmonary injury in mouse model. Nano Lett 8:437-45.
19. Council NR. 2012. A Research Strategy for Environmental, Health, and Safety Aspects of Engineered Nanomaterials. Washington, DC: The National Academic Press.
20. Davis JM, Addison J, Bolton RE, Donaldson K, Jones AD, Smith T. 1986. The pathogenicity of long versus short fibre samples of amosite asbestos administered to rats by inhalation and intraperitoneal injection. Br J Exp Pathol 67:415-30.
21. De Volder MF, Tawfick SH, Baughman RH, Hart AJ. 2013. Carbon nanotubes: present and future commercial applications. Science 339: 535-9.
22. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G. 1993. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 122:103-11.
23. Dickinson BC, Chang CJ. 2011. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 7: 504-11.
24. Ding L, Stilwell J, Zhang T, Elboudwarej O, Jiang H, Selegue JP, et al. 2005. Molecular characterization of the cytotoxic mechanism of multiwall carbon nanotubes and nano-onions on human skin fibroblast. Nano Lett 5:2448-64.
25. Donaldson K, Aitken R, Tran L, Stone V, Duffin R, Forrest G, et al. 2006. Carbon nanotubes: A review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol Sci 92:5-22.
26. 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. Part Fibre Toxicol 7:5.
27. Dong J, Porter DW, Battelli LA, Wolfarth MG, Richardson DL, Ma Q. 2014. Pathologic and molecular profiling of rapid-onset fibrosis and inflammation induced by multi-walled carbon nanotubes. Arch Toxicol [Epub ahead of print]. DOI: 10. 1007/s00204-014-1428-y.
28. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. 2008. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320:674-7.
29. Fernandez IE, Eickelberg O. 2012. The impact of TGF-beta on lung fibrosis: from targeting to biomarkers. Proc Am Thorac Soc 9:111-6.
30. Finkel T. 2005. Radical medicine: treating ageing to cure disease. Nat Rev Mol Cell Biol 6:971-6.
31. Finkel T. 2011. Signal transduction by reactive oxygen species. J Cell Biol 194:7-15.
32. Gebel T, Foth H, Damm G, Freyberger A, Kramer PJ, LilienblumW, et al. 2014. Manufactured nanomaterials: categorization and approaches to hazard assessment. Arch Toxicol 88:2191-211.
33. Hamilton Jr RF, Xiang C, Li M, Ka I, Yang F, Ma D, et al. 2013. Purification and sidewall functionalization of multiwalled carbon nanotubes and resulting bioactivity in two macrophage models. Inhal Toxicol 25:199-210.
34. Han SG, Andrews R, Gairola CG. 2010. Acute pulmonary response of mice to multi-wall carbon nanotubes. Inhal Toxicol 22:340-7.
35. Han YG, Xu J, Li ZG, Ren GG, Yang Z. 2012. In vitro toxicity of multiwalled carbon nanotubes in C6 rat glioma cells. Neurotoxicology 33: 1128-34.
36. Hansen G, Mcintire JJ, Yeung VP, Berry G, Thorbecke GJ, Chen L, et al. 2000. CD4(+) T helper cells engineered to produce latent TGF-beta1 reverse allergen-induced airway hyperreactivity and inflammation. J Clin Invest 105:61-70.
37. He X, Young SH, Ferback JE, Ma Q. 2012. Single-walled carbon nanotubes induce fibrogenic effect by disturbing mitochondrial oxidative stress and activating NF-kB signaling. J Clin Toxicol S5:005.
38. He X, Young SH, Schwegler-Berry D, Chisholm WP, Fernback JE, Ma Q. 2011. Multiwalled carbon nanotubes induce a fibrogenic response by stimulating reactive oxygen species production, activating NF-kappaB signaling, and promoting fibroblast-to-myofibroblast transformation. Chem Res Toxicol 24:2237-48.
39. Hirano S, Fujitani Y, Furuyama A, Kanno S. 2010. Uptake and cytotoxic effects of multi-walled carbon nanotubes in human bronchial epithelial cells. Toxicol Appl Pharmacol 249:8-15.
40. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, et al. 2008. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9: 847-56.
41. Hsieh WY, Chou CC, Ho CC, Yu SL, Chen HY, Chou HY, et al. 2012. Single-walled carbon nanotubes induce airway hyperreactivity and parenchymal injury in mice. Am J Respir Cell Mol Biol 46:257-67.
42. Huang X, Zhang F, Sun X, Choi KY, Niu G, Zhang G, et al. 2014. The genotype-dependent influence of functionalized multiwalled carbon nanotubes on fetal development. Biomaterials 35:856-65.
43. Hussain S, Sangtian S, Anderson SM, Snyder RJ, Marshburn JD, Rice AB, 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.
44. Inoue K, Koike E, Yanagisawa R, Hirano S, Nishikawa M, Takano H. 2009. Effects of multi-walled carbon nanotubes on a murine allergic airway inflammation model. Toxicol Appl Pharmacol 237: 306-16.
45. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG. 2002. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110:341-50.
46. IWGN. 1999. Nanotechnology Research Directions: IWGN Workshopreport. Vision for Nanotechnology R&D in the Next Decade. Washington, DC: National Science and Technology Council Committee on Technology Interagency Working Group on Nanoscience, Engineering and Technology (IWGN).
47. Jeffrey KL, Camps M, Rommel C, Mackay CR. 2007. Targeting dualspecificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat Rev Drug Discov 6:391-403.
48. Jia G, Wang H, Yan L, Wang X, Pei R, Yan T, et al. 2005. Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ Sci Technol 39:1378-83.
49. Johnston HJ, Hutchison GR, Christensen FM, Peters S, Hankin S, Aschberger K, et al. 2010. 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 4:207-46.
50. Kagan VE, Konduru NV, Feng W, Allen BL, Conroy J, Volkov Y, et al. 2010. Carbon nanotubes degraded by neutrophil myeloperoxidase induce less pulmonary inflammation. Nat Nanotechnol 5:354-9.
51. Kagan VE, Tyurina YY, Tyurin VA, Konduru NV, Potapovich AI, Osipov AN, et al. 2006. Direct and indirect effects of single walled carbon nanotubes on RAW 264. 7 macrophages: role of iron. Toxicol Lett 165: 88-100.
52. Kalluri R, Neilson EG. 2003. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112:1776-84.
53. Kang JL, Lee K, Castranova V. 2000. Nitric oxide up-regulates DNAbinding activity of nuclear factor-kappaB in macrophages stimulated with silica and inflammatory stimulants. Mol Cell Biochem 215:1-9.
54. Kanno S, Hirano S, Chiba S, Takeshita H, Nagai T, Takada M, et al. 2014. The role of Rho-kinases in IL-1beta release through phagocytosis of fibrous particles in human monocytes. Arch Toxicol 89:73-85.
55. Kato T, Totsuka Y, Ishino K, Matsumoto Y, Tada Y, Nakae D, et al. 2013. Genotoxicity of multi-walled carbon nanotubes in both in vitro and in vivo assay systems. Nanotoxicology 7:452-61.
56. Kitani A, Fuss I, Nakamura K, Kumaki F, Usui T, Strober W. 2003. Transforming growth factor (TGF)-beta1-producing regulatory T cells induce Smad-mediated interleukin 10 secretion that facilitates coordinated immunoregulatory activity and amelioration of TGFbeta1-mediated fibrosis. J Exp Med 198:1179-88.
57. Kool M, Petrilli V, De Smedt T, Rolaz A, Hammad H, Van Nimwegen M, et al. 2008. Cutting edge: Alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J Immunol 181:3755-9.
58. Lacerda L, Ali-Boucetta H, Herrero MA, Pastorin G, Bianco A, Prato M, et al. 2008. Tissue histology and physiology following intravenous administration of different types of functionalized multiwalled carbon nanotubes. Nanomedicine (London) 3:149-61.
59. Lam CW, James JT, Mccluskey R, Hunter RL. 2004. Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol Sci 77:126-34.
60. Lamkanfi M, Dixit VM. 2014. Mechanisms and functions of inflammasomes. Cell 157:1013-22.
61. Lee JK, Sayers BC, Chun KS, Lao HC, Shipley-Phillips JK, Bonner JC, et al. 2012. Multi-walled carbon nanotubes induce COX-2 and iNOS expression via MAP kinase-dependent and-independent mechanisms in mouse RAW264. 7 macrophages. Part Fibre Toxicol 9:14.
62. Liu Y, Zhao Y, Sun B, Chen C. 2013. Understanding the toxicity of carbon nanotubes. Acc Chem Res 46:702-13.
63. Liu Z, Chen K, Davis C, Sherlock S, Cao Q, Chen X, et al. 2008. Drug delivery with carbon nanotubes for in vivo cancer treatment. Cancer Res 68:6652-60.
64. Lohcharoenkal W, Wang L, Stueckle TA, Park J, Tse W, Dinu CZ, et al. 2014. Role of H-Ras/ERK signaling in carbon nanotube-induced neoplastic-like transformation of human mesothelial cells. Front Physiol 5:222.
65. Luanpitpong S, Wang L, Stueckle TA, Tse W, Chen YC, Rojanasakul Y. 2014. Caveolin-1 regulates lung cancer stem-like cell induction and p53 inactivation in carbon nanotube-driven tumorigenesis. Oncotarget 5:3541-54.
66. Ma Q. 2010. Transcriptional responses to oxidative stress: pathological and toxicological implications. Pharmacol Ther 125:376-93.
67. Ma Q. 2013. Role of Nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 53:401-26.
68. Mangum JB, Turpin EA, Antao-Menezes A, Cesta MF, Bermudez E, Bonner JC. 2006. 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 3:15.
69. Manke A, Luanpitpong S, Dong C, Wang L, He X, Battelli L, et al. 2014. Effect of fiber length on carbon nanotube-induced fibrogenesis. Int J Mol Sci 15:7444-61.
70. Manna SK, Sarkar S, Barr J, Wise K, Barrera EV, Jejelowo O, et al. 2005. Single-walled carbon nanotube induces oxidative stress and activates nuclear transcription factor-kappaB in human keratinocytes. Nano Lett 5:1676-84.
71. Maynard AD, Kuempel ED. 2005. Airborne nanostructured particles and occupational health. J Nanopart Res 7:587-614.
72. Maynard AD, Warheit DB, Philbert MA. 2011. The new toxicology of sophisticated materials: nanotoxicology and beyond. Toxicol Sci 120: S109-29.
73. Mercer RR, Hubbs AF, Scabilloni JF, Wang L, Battelli LA, Friend S, et al. 2011. Pulmonary fibrotic response to aspiration of multi-walled carbon nanotubes. Part Fibre Toxicol 8:21.
74. Mercer RR, Scabilloni J, Wang L, Kisin E, Murray AR, Schwegler-Berry D, et al. 2008. 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 294: L87-97.
75. Mercer RR, Scabilloni JF, Hubbs AF, Battelli LA, Mckinney W, Friend S, et al. 2013a. Distribution and fibrotic response following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol 10:33.
76. Mercer RR, Scabilloni JF, Hubbs AF, Wang L, Battelli LA, Mckinney W, et al. 2013b. Extrapulmonary transport of MWCNT following inhalation exposure. Part Fibre Toxicol 10:38.
77. Meunier E, Coste A, Olagnier D, Authier H, Lefevre L, Dardenne C, et al. 2012. Double-walled carbon nanotubes trigger IL-1beta release in human monocytes through Nlrp3 inflammasome activation. Nanomedicine 8:987-95.
78. 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 100:203-14.
79. Mitchell LA, Lauer FT, Burchiel SW, Mcdonald JD. 2009. Mechanisms for how inhaled multiwalled carbon nanotubes suppress systemic immune function in mice. Nat Nanotechnol 4:451-6.
80. Morgan W. K. C., Gee J. B. L. 1995. Asbestos-related diseases. In: Morgan W. K. C., Seaton A, eds. Occupational Lung Diseases, 3rd ed. Philadelphia: W. B. Saunders Company.
81. Muller J, Decordier I, Hoet PH, Lombaert N, Thomassen L, Huaux F, et al. 2008. Clastogenic and aneugenic effects of multi-wall carbon nanotubes in epithelial cells. Carcinogenesis 29:427-33.
82. Muller J, Delos M, Panin N, Rabolli V, Huaux F, Lison D. 2009. Absence of carcinogenic response to multiwall carbon nanotubes in a 2-year bioassay in the peritoneal cavity of the rat. Toxicol Sci 110:442-8.
83. Muller J, Huaux F, Moreau N, Misson P, Heilier JF, Delos M, et al. 2005. Respiratory toxicity of multi-wall carbon nanotubes. Toxicol Appl Pharmacol 207:221-31.
84. Munshi A, Ramesh R. 2013. Mitogen-activated protein kinases and their role in radiation response. Genes Cancer 4:401-8.
85. Murphy FA, Poland CA, Duffin R, Al-Jamal KT, Ali-Boucetta H, Nunes A, et al. 2011. 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 178:2587-600.
86. Murray AR, Kisin E, Leonard SS, Young SH, Kommineni C, Kagan VE, et al. 2009. Oxidative stress and inflammatory response in dermal toxicity of single-walled carbon nanotubes. Toxicology 257: 161-71.
87. Nagai H, Okazaki Y, Chew SH, Misawa N, Yamashita Y, Akatsuka S, et al. 2011. Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. Proc Natl Acad Sci USA 108:E1330-8.
88. Nakao A, Miike S, Hatano M, Okumura K, Tokuhisa T, Ra C, et al. 2000. Blockade of transforming growth factor beta/Smad signaling in T cells by overexpression of Smad7 enhances antigen-induced airway inflammation and airway reactivity. J Exp Med 192:151-8.
89. Nerl HC, Cheng C, Goode AE, Bergin SD, Lich B, Gass M, et al. 2011. Imaging methods for determining uptake and toxicity of carbon nanotubes in vitro and in vivo. Nanomedicine (London) 6:849-65.
90. NIOSH. 2013a. Current Intelligence Bulletin 65: occupational exposure to carbon naotubes and nanofibers.
91. NIOSH. 2013b. Current Strategies for Engineering Controls in Nanomaterial Production and Downstream Handling Processes. Cincinnati: Department of Health and Human Services, Centers for Disease Control and Prevention, National Institute for Occupational Safety and Health.
92. NSF. 2011. Nanotechnology research directions for societal needs in 2020: retrospective and outlook summary. National Science Foundation. In: Roco M, Mirkin C, Hersan M, eds. Science Policy Reports. New York: Springer.
93. Pacher P, Beckman JS, Liaudet L. 2007. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315-424.
94. PacurariM, Yin XJ, Zhao J, Ding M, Leonard SS, Schwegler-Berry D, et al. 2008. Raw single-wall carbon nanotubes induce oxidative stress and activate MAPKs, AP-1, NF-kappaB, and Akt in normal and malignant human mesothelial cells. Environ Health Perspect 116:1211-17.
95. Palomaki J, Valimaki E, Sund J, Vippola M, Clausen PA, Jensen KA, et al. 2011. Long, needle-like carbon nanotubes and asbestos activate the NLRP3 inflammasome through a similar mechanism. ACS Nano 5: 6861-70.
96. Park EJ, Cho WS, Jeong J, Yi J, Choi K, Park K. 2009. Pro-inflammatory and potential allergic responses resulting from B cell activation in mice treated with multi-walled carbon nanotubes by intratracheal instillation. Toxicology 259:113-21.
97. Park EJ, Roh J, Kim SN, Kang MS, Han YA, Kim Y, et al. 2011. A single intratracheal instillation of single-walled carbon nanotubes induced early lung fibrosis and subchronic tissue damage in mice. Arch Toxicol 85:1121-31.
98. Park EJ, Zahari NE, Lee EW, Song J, Lee JH, Cho MH, et al. 2014. SWCNTs induced autophagic cell death in human bronchial epithelial cells. Toxicol In Vitro 28:442-50.
99. Patlolla AK, Hussain SM, Schlager JJ, Patlolla S, Tchounwou PB. 2010. Comparative study of the clastogenicity of functionalized and nonfunctionalized multiwalled carbon nanotubes in bone marrow cells of Swiss-Webster mice. Environ Toxicol 25:608-21.
100. Peeters PM, Perkins TN, Wouters EF, Mossman BT, Reynaert NL. 2013. Silica induces NLRP3 inflammasome activation in human lung epithelial cells. Part Fibre Toxicol 10:3.
101. Poland CA, Duffin R, Kinloch I, Maynard A, WallaceWA, Seaton A, et al. 2008. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol 3: 423-8.
102. Porter DW, Hubbs AF, Chen BT, Mckinney W, Mercer RR, Wolfarth MG, et al. 2013. Acute pulmonary dose-responses to inhaled multi-walled carbon nanotubes. Nanotoxicology 7:1179-94.
103. Porter DW, Hubbs AF, Mercer RR, Wu N, Wolfarth MG, Sriram K, et al. 2010. Mouse pulmonary dose-and time course-responses induced by exposure to multi-walled carbon nanotubes. Toxicology 269:136-47.
104. Pulskamp K, Diabate S, Krug HF. 2007. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol Lett 168:58-74.
105. Ravichandran P, Baluchamy S, Sadanandan B, Gopikrishnan R, Biradar S, Ramesh V, et al. 2010. Multiwalled carbon nanotubes activate NF-kappaB and AP-1 signaling pathways to induce apoptosis in rat lung epithelial cells. Apoptosis 15:1507-16.
106. Reddy AR, Reddy YN, Krishna DR, Himabindu V. 2012. Pulmonary toxicity assessment of multiwalled carbon nanotubes in rats following intratracheal instillation. Environ Toxicol 27:211-19.
107. Rose BA, Force T, Wang Y. 2010. Mitogen-activated protein kinase signaling in the heart: Angels versus demons in a heart-breaking tale. Physiol Rev 90:1507-46.
108. Rothen-Rutishauser B, Brown DM, Piallier-Boyles M, Kinloch IA, Windle AH, Gehr P, et al. 2010. Relating the physicochemical characteristics and dispersion of multiwalled carbon nanotubes in different suspension media to their oxidative reactivity in vitro and inflammation in vivo. Nanotoxicology 4:331-42.
109. Ryman-Rasmussen JP, Cesta MF, Brody AR, Shipley-Phillips JK, Everitt JI, Tewksbury EW, et al. 2009a. Inhaled carbon nanotubes reach the subpleural tissue in mice. Nat Nanotechnol 4:747-51.
110. Ryman-Rasmussen JP, Tewksbury EW, Moss OR, Cesta MF, Wong BA, Bonner JC. 2009b. Inhaled multiwalled carbon nanotubes potentiate airway fibrosis in murine allergic asthma. Am J Respir Cell Mol Biol 40:349-58.
111. Sager TM, Wolfarth MW, Andrew M, Hubbs A, Friend S, Chen TH, et al. 2014. Effect of multi-walled carbon nanotube surface modification on bioactivity in the C57BL/6 mouse model. Nanotoxicology 8:317-27.
112. Sakamoto Y, Nakae D, Fukumori N, Tayama K, Maekawa A, Imai K, et al. 2009. Induction of mesothelioma by a single intrascrotal administration of multi-wall carbon nanotube in intact male Fischer 344 rats. J Toxicol Sci 34:65-76.
113. Sargent LM, Hubbs AF, Young SH, Kashon ML, Dinu CZ, Salisbury JL, et al. 2012. Single-walled carbon nanotube-induced mitotic disruption. Mutat Res 745:28-37.
114. Sargent LM, Porter DW, Staska LM, Hubbs AF, Lowry DT, Battelli L, et al. 2014. Promotion of lung adenocarcinoma following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol 11:3.
115. Sargent LM, Reynolds SH, Castranova V. 2010. Potential pulmonary effects of engineered carbon nanotubes: in vitro genotoxic effects. Nanotoxicology 4:396-408.
116. Sayers BC, Taylor AJ, Glista-Baker EE, Shipley-Phillips JK, Dackor RT, Edin ML, et al. 2013. Role of cyclooxygenase-2 in exacerbation of allergen-induced airway remodeling by multiwalled carbon nanotubes. Am J Respir Cell Mol Biol 49:525-35.
117. Schins RP, Knaapen AM. 2007. Genotoxicity of poorly soluble particles. Inhal Toxicol 19:189-98.
118. Schmierer B, Hill CS. 2007. TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8:970-82.
119. Schroder K, Tschopp J. 2010. The inflammasomes. Cell 140:821-32.
120. Seaton A, Tran L, Aitken R, Donaldson K. 2010. Nanoparticles, human health hazard and regulation. J R Soc Interface 7:S119-29.
121. Shvedova AA, Kapralov AA, Feng WH, Kisin ER, Murray AR, Mercer RR, et al. 2012a. Impaired clearance and enhanced pulmonary inflammatory/fibrotic response to carbon nanotubes in myeloperoxidase-deficient mice. PLoS One 7:e30923.
122. ShvedovaAA, Kisin E, Murray AR, Johnson VJ, Gorelik O, Arepalli S, et al. 2008a. 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 295:L552-65.
123. Shvedova AA, Kisin ER, Mercer R, Murray AR, Johnson VJ, Potapovich AI, et al. 2005. Unusual inflammatory and fibrogenic pulmonary responses to single-walled carbon nanotubes in mice. Am J Physiol Lung Cell Mol Physiol 289:L698-708.
124. Shvedova AA, Kisin ER, Murray AR, Gorelik O, Arepalli S, Castranova V, et al. 2007. Vitamin E deficiency enhances pulmonary inflammatory response and oxidative stress induced by singlewalled carbon nanotubes in C57BL/6 mice. Toxicol Appl Pharmacol 221:339-48.
125. Shvedova AA, Kisin ER, Murray AR, Kommineni C, Castranova V, Fadeel B, et al. 2008b. Increased accumulation of neutrophils and decreased fibrosis in the lung of NADPH oxidase-deficient C57BL/6 mice exposed to carbon nanotubes. Toxicol Appl Pharmacol 231: 235-40.
126. Shvedova AA, Pietroiusti A, Fadeel B, Kagan VE. 2012b. Mechanisms of carbon nanotube-induced toxicity: focus on oxidative stress. Toxicol Appl Pharmacol 261:121-33.
127. Siegrist KJ, Reynolds SH, Kashon ML, Lowry DT, Dong C, Hubbs AF, et al. 2014. Genotoxicity of multi-walled carbon nanotubes at occupationally relevant doses. Part Fibre Toxicol 11:6.
128. Sime PJ, Xing Z, Graham FL, Csaky KG, Gauldie J. 1997. Adenovectormediated gene transfer of active transforming growth factor-beta1 induces prolonged severe fibrosis in rat lung. J Clin Invest 100:768-76.
129. Snyder-Talkington BN, Schwegler-Berry D, Castranova V, Qian Y, Guo NL. 2013. Multi-walled carbon nanotubes induce human microvascular endothelial cellular effects in an alveolar-capillary co-culture with small airway epithelial cells. Part Fibre Toxicol 10:35.
130. Stanton MF. 1973. Some etiological considerations of fibre carcinogenesis. In: Bogovski P, Gilson JC, Timbrell V, Wagner JC, eds. Biological Effects of Asbestos. Lyon, France: WHO IARC.
131. Stone V, Donaldson K. 2006. Nanotoxicology: signs of stress. Nat Nanotechnol 1:23-4.
132. Subramanian V, Youtie J, Porter AL, Shapira P. 2010. Is there a shift to ''active nanostructures"? J Nanopart Res 12:1-10.
133. Sutterwala FS, Haasken S, Cassel SL. 2014. Mechanism of NLRP3 inflammasome activation. Ann N Y Acad Sci 1319:82-95.
134. Takagi A, Hirose A, Futakuchi M, Tsuda H, Kanno J. 2012. Dosedependent mesothelioma induction by intraperitoneal administration of multi-wall carbon nanotubes in p53 heterozygous mice. Cancer Sci 103:1440-4.
135. Takagi A, Hirose A, Nishimura T, Fukumori N, Ogata A, Ohashi N, et al. 2008. Induction of mesothelioma in p53+/- mouse by intraperitoneal application of multi-wall carbon nanotube. J Toxicol Sci 33:105-16.
136. Taylor AJ, Mcclure CD, Shipkowski KA, Thompson EA, Hussain S, Garantziotis S, 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:e106870.
137. Thurnherr T, Brandenberger C, Fischer K, Diener L, Manser P, Maeder-Althaus X, et al. 2011. A comparison of acute and long-term effects of industrial multiwalled carbon nanotubes on human lung and immune cells in vitro. Toxicol Lett 200:176-86.
138. Tschopp J, Schroder K. 2010. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat Rev Immunol 10:210-15.
139. Ursini CL, Cavallo D, Fresegna AM, Ciervo A, Maiello R, Buresti G, et al. 2014. Differences in cytotoxic, genotoxic, and inflammatory response of bronchial and alveolar human lung epithelial cells to pristine and COOH-functionalized multiwalled carbon nanotubes. Biomed Res Int 2014:359506.
140. 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.
141. Vietti G, Ibouraadaten S, Palmai-Pallag M, Yakoub Y, Bailly C, Fenoglio I, 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.
142. Wagner EF, Nebreda AR. 2009. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9:537-49.
143. Wang J, Sun P, Bao Y, Liu J, An L. 2011a. Cytotoxicity of single-walled carbon nanotubes on PC12 cells. Toxicol In Vitro 25:242-50.
144. Wang L, Luanpitpong S, Castranova V, Tse W, Lu Y, Pongrakhananon V, et al. 2011b. Carbon nanotubes induce malignant transformation and tumorigenesis of human lung epithelial cells. Nano Lett 11:2796-803.
145. Wang L, Mercer RR, Rojanasakul Y, Qiu A, Lu Y, Scabilloni JF, et al. 2010a. Direct fibrogenic effects of dispersed single-walled carbon nanotubes on human lung fibroblasts. J Toxicol Environ Health A 73: 410-22.
146. Wang P, Nie X, Wang Y, Li Y, Ge C, Zhang L, et al. 2013. Multiwall carbon nanotubes mediate macrophage activation and promote pulmonary fibrosis through TGF-beta/Smad signaling pathway. Small 9:3799-811.
147. Wang X, Xia T, Ntim SA, Ji Z, George S, Meng H, et al. 2010b. Quantitative techniques for assessing and controlling the dispersion and biological effects of multiwalled carbon nanotubes in mammalian tissue culture cells. ACS Nano 4:7241-52.
148. Warheit DB, Laurence BR, Reed KL, Roach DH, Reynolds GA, Webb TR. 2004. Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats. Toxicol Sci 77:117-25.
149. Wick P, Manser P, Limbach LK, Dettlaff-Weglikowska U, Krumeich F, Roth S, et al. 2007. The degree and kind of agglomeration affect carbon nanotube cytotoxicity. Toxicol Lett 168:121-31.
150. Winter M, Beer HD, Hornung V, Kramer U, Schins RP, Forster I. 2011. Activation of the inflammasome by amorphous silica and TiO2 nanoparticles in murine dendritic cells. Nanotoxicology 5:326-40.
151. Wu L, Zhang Y, Zhang C, Cui X, Zhai S, Liu Y, et al. 2014. Tuning cell autophagy by diversifying carbon nanotube surface chemistry. ACS Nano 8:2087-99.
152. Wu W, Li R, Bian X, Zhu Z, Ding D, Li X, et al. 2009. Covalently combining carbon nanotubes with anticancer agent: preparation and antitumor activity. ACS Nano 3:2740-50.
153. Wynn TA. 2011. Integrating mechanisms of pulmonary fibrosis. J Exp Med 208:1339-50.
154. Xu J, Futakuchi M, Shimizu H, Alexander DB, Yanagihara K, Fukamachi K, et al. 2012. Multi-walled carbon nanotubes translocate into the pleural cavity and induce visceral mesothelial proliferation in rats. Cancer Sci 103:2045-50.
155. Yamaguchi A, Fujitani T, Ohyama K, Nakae D, Hirose A, Nishimura T, et al. 2012. Effects of sustained stimulation with multi-wall carbon nanotubes on immune and inflammatory responses in mice. J Toxicol Sci 37:177-89.
156. Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I, et al. 2010. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1alpha and IL-1beta. Proc Natl Acad Sci USA 107: 19449-54.
157. Ye S, Jiang Y, Zhang H, Wang Y, Wu Y, Hou Z, et al. 2012. Multi-walled carbon nanotubes induce apoptosis in RAW 264. 7 cell-derived osteoclasts through mitochondria-mediated death pathway. J Nanosci Nanotechnol 12:2101-12.
158. Ye SF, Wu YH, Hou ZQ, Zhang QQ. 2009. ROS and NF-kappaB are involved in upregulation of IL-8 in A549 cells exposed to multi-walled carbon nanotubes. Biochem Biophys Res Commun 379:643-8.
159. Zhang Q, Huang JQ, Qian WZ, Zhang YY, Wei F. 2013. The road for nanomaterials industry: A review of carbon nanotube production, posttreatment, and bulk applications for composites and energy storage. Small 9:1237-65.
160. Zhang YE. 2009. Non-Smad pathways in TGF-beta signaling. Cell Res 19:128-39.
161. Zhao X, Liu R. 2012. Recent progress and perspectives on the toxicity of carbon nanotubes at organism, organ, cell, and biomacromolecule levels. Environ Int 40:244-55.
162. Zhiqing L, Zhuge X, Fuhuan C, Danfeng Y, Huashan Z, Bencheng L, et al. 2010. ICAM-1 and VCAM-1 expression in rat aortic endothelial cells after single-walled carbon nanotube exposure. J Nanosci Nanotechnol 10:8562-74.