Genotoxicity of multi-walled carbon nanotubes at occupationally relevant doses

Particle and Fibre Toxicology

Volumn 11, Issue 1, 2014, Pages

  Siegrist, Katelyn J ^a   Reynolds, Steven H ^a   Kashon, Michael L ^a   Lowry, David T ^a   Dong, Chenbo ^b   Hubbs, Ann F ^a   Young, Shih Houng ^a   Salisbury, Jeffrey L ^c   Porter, Dale W ^a   Benkovic, Stanley A ^a   McCawley, Michael ^d   Keane, Michael J ^a   Mastovich, John T ^e   Bunker, Kristin L ^e   Cena, Lorenzo G ^a   Sparrow, Mark C ^e   Sturgeon, Jacqueline L ^e   Dinu, Cerasela Z ^b   Sargent, Linda M ^a  

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

^b West Virginia University   (United States)

^c MAYO CLINIC   (United States)

^d WEST VIRGINIA UNIVERSITY   (United States)

^e RJ LEE GROUP   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MULTI WALLED NANOTUBE;

ANEUPLOIDY; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CENTROSOME; CHROMOSOME NUMBER; CONCENTRATION RESPONSE; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENOTOXICITY; HUMAN; HUMAN CELL; MICROTUBULE; MITOSIS SPINDLE; NANOTOXICOLOGY; OCCUPATIONAL EXPOSURE; PRIORITY JOURNAL;

APOPTOSIS; CELL CYCLE; CELL SURVIVAL; CELLS, CULTURED; CHROMOSOMES; DNA DAMAGE; ENVIRONMENTAL MONITORING; EPITHELIAL CELLS; FLOW CYTOMETRY; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICROSCOPY, ATOMIC FORCE; MITOSIS; MUTAGENS; NANOTUBES, CARBON; OCCUPATIONAL EXPOSURE; SPECTROMETRY, X-RAY EMISSION; SPECTRUM ANALYSIS, RAMAN; SPINDLE APPARATUS; STEM CELLS;

EID: 84893186344     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/1743-8977-11-6     Document Type: Article

References (105)

1. De Volder MF, Tawfick SH, Baughman RH, Hart AJ. Carbon nanotubes: present and future commercial applications. Science 2013, 339:535-539. 10.1126/science.1222453, 23372006.
2. Liu J, Rinzler AG, Dai HJ, Hafner JH, Bradley RK, Boul PJ, Lu A, Iverson T, Shelimov K, Huffman CB, et al. Fullerene pipes. Science 1998, 280:1253-1256. 10.1126/science.280.5367.1253, 9596576.
3. McAllister K, Sazani P, Adam M, Cho MJ, Rubinstein M, Samulski RJ, DeSimone JM. Polymeric nanogels produced via inverse microemulsion polymerization as potential gene and antisense delivery agents. J Am Chem Soc 2002, 124:15198-15207. 10.1021/ja027759q, 12487595.
4. Bradley J, Nordan MM, Tassinari O. The Recession's Ripple Effect on Nanotech 2009, Boston, MA: Lux Research, Inc, Book The Recession's Ripple Effect on Nanotech.
5. Erdely A, Dahm M, Chen BT, Zeidler-Erdely PC, Fernback JE, Birch ME, Evans DE, Kashon ML, Deddens JA, Hulderman T, et al. Carbon nanotube dosimetry: from workplace exposure assessment to inhalation toxicology. Part Fibre Toxicol 2013, 10:53. 10.1186/1743-8977-10-53, 24144386.
6. 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.
7. Maynard AD, Baron PA, Foley M, Shvedova AA, Kisin ER, Castranova V. Exposure to carbon nanotube material: aerosol release during the handling of unrefined single-walled carbon nanotube material. J Toxicol Environ Health A 2004, 67:87-107. 10.1080/15287390490253688, 14668113.
8. Yeganeh B, Kull CM, Hull MS, Marr LC. Characterization of airborne particles during production of carbonaceous nanomaterials. Environ Sci Technol 2008, 42:4600-4606. 10.1021/es703043c, 18605593.
9. 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 -, 7:5. 2857820, 20307263.
10. Oberdorster G. Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J Intern Med 2010, 267:89-105. 10.1111/j.1365-2796.2009.02187.x, 20059646.
11. Kato T, Totsuka Y, Ishino K, Matsumoto Y, Tada Y, Nakae D, Goto S, Masuda S, Ogo S, Kawanishi M, et al. Genotoxicity of multi-walled carbon nanotubes in both in vitro and in vivo assay systems. Nanotoxicology 2013, 7:452-461. 10.3109/17435390.2012.674571, 22397533.
12. Monteiro-Riviere NA, Nemanich RJ, Inman AO, Wang YY, Riviere JE. Multi-walled carbon nanotube interactions with human epidermal keratinocytes. Toxicol Lett 2005, 155:377-384. 10.1016/j.toxlet.2004.11.004, 15649621.
13. Muller J, Decordier I, Hoet PH, Lombaert N, Thomassen L, Huaux F, Lison D, Kirsch-Volders M. Clastogenic and aneugenic effects of multi-wall carbon nanotubes in epithelial cells. Carcinogenesis 2008, 29:427-433. 10.1093/carcin/bgm243, 18174261.
14. Ponti J, Broggi F, Mariani V, De Marzi L, Colognato R, Marmorato P, Gioria S, Gilliland D, Pascual Garcia C, Meschini S, et al. Morphological transformation induced by multiwall carbon nanotubes on Balb/3 T3 cell model as an in vitro end point of carcinogenic potential. Nanotoxicology 2013, 7:221-233. 10.3109/17435390.2011.652681, 22279961.
15. Tavares AM, Louro H, Antunes S, Quarre S, Simar S, De Temmerman PJ, Verleysen E, Mast J, Jensen KA, Norppa H, et al. Genotoxicity evaluation of nanosized titanium dioxide, synthetic amorphous silica and multi-walled carbon nanotubes in human lymphocytes. Toxicol In Vitro 2014, 28:60-69. 10.1016/j.tiv.2013.06.009, 23811260.
16. Di Giorgio ML, Di Bucchianico S, Ragnelli AM, Aimola P, Santucci S, Poma A. Effects of single and multi walled carbon nanotubes on macrophages: cyto and genotoxicity and electron microscopy. Mutat Res 2011, 722:20-31. 10.1016/j.mrgentox.2011.02.008, 21382506.
17. Li X, Peng Y, Qu X. Carbon nanotubes selective destabilization of duplex and triplex DNA and inducing B-A transition in solution. Nucleic Acids Res 2006, 34:3670-3676. 10.1093/nar/gkl513, 1540735, 16885240.
18. Li X, Peng Y, Ren J, Qu X. Carboxyl-modified single-walled carbon nanotubes selectively induce human telomeric i-motif formation. Proc Natl Acad Sci USA 2006, 103:19658-19663. 10.1073/pnas.0607245103, 1750900, 17167055.
19. Sargent LM, Hubbs AF, Young SH, Kashon ML, Dinu CZ, Salisbury JL, Benkovic SA, Lowry DT, Murray AR, Kisin ER, et al. Single-walled carbon nanotube-induced mitotic disruption. Mutat Res 2012, 745:28-37. 10.1016/j.mrgentox.2011.11.017, 22178868.
20. Rodriguez-Fernandez L, Valiente R, Gonzalez J, Villegas JC, Fanarraga ML. Multiwalled carbon nanotubes display microtubule biomimetic properties in vivo, enhancing microtubule assembly and stabilization. ACS Nano 2012, 6:6614-6625. 10.1021/nn302222m, 22769231.
21. Cortez BA, Machado-Santelli GM. Chrysotile effects on human lung cell carcinoma in culture: 3-D reconstruction and DNA quantification by image analysis. BMC Cancer 2008, 8:181. 10.1186/1471-2407-8-181, 2464777, 18588678.
22. Cortez BD, Quassollo G, Caceres A, Machado-Santelli GM. The fate of chrysotile-induced multipolar mitosis and aneuploid population in cultured lung cancer cells. PLoS One 2011, 6:1860.
23. Ramirez P, Eastmond DA, Laclette JP, Ostrosky-Wegman P. Disruption of microtubule assembly and spindle formation as a mechanism for the induction of aneuploid cells by sodium arsenite and vanadium pentoxide. Mutat Res 1997, 386:291-298. 10.1016/S1383-5742(97)00018-5, 9219566.
24. Sargent LM, Shvedova AA, Hubbs AF, Salisbury JL, Benkovic SA, Kashon ML, Lowry DT, Murray AR, Kisin ER, Friend S, et al. Induction of aneuploidy by single-walled carbon nanotubes. Environ Mol Mutagen 2009, 50:708-717. 10.1002/em.20529, 19774611.
25. Ehrlich VA, Nersesyan AK, Hoelzi C, Ferk F, Bichler J, Valic E, Schaffer A, Schulte-Hermann R, Fenech M, Wagner KH, Knasmuller S. Inhalative exposure to vanadium pentoxide causes DNA damage in workers: results of a multiple end point study. Environ Health Perspect 2008, 116:1689-1693. 10.1289/ehp.11438, 2599764, 19079721.
26. Ress NB, Chou BJ, Renne RA, Dill JA, Miller RA, Roycroft JH, Hailey JR, Haseman JK, Bucher JR. Carcinogenicity of inhaled vanadium pentoxide in F344/N rats and B6C3F1 mice. Toxicol Sci 2003, 74:287-296. 10.1093/toxsci/kfg136, 12773761.
27. Yegles M, Janson X, Dong HY, Renier A, Jaurand MC. Role of fibre characteristics on cytotoxicity and induction of anaphase/telophase aberrations in rat pleural mesothelial cells in vitro: correlations with in vivo animal findings. Carcinogenesis 1995, 16:2751-2758. 10.1093/carcin/16.11.2751, 7586195.
28. Yegles M, Saint-Etienne L, Renier A, Janson X, Jaurand MC. Induction of metaphase and anaphase/telophase abnormalities by asbestos fibers in rat pleural mesothelial cells in vitro. Am J Respir Cell Mol Biol 1993, 9:186-191. 10.1165/ajrcmb/9.2.186, 8393329.
29. Hubbs A, Castranova V, Chen BT, Frazer DG, McKinney W, Mercer RR, Kashon ML, Battelli LA, Willard P, Porter DW. Pulmonary inflammation, epithelial hyperplasia, and lymph node translocation after multi-walled carbon nanotube inhalation. Washington DC. Toxicol Sci 2011, 120:11.
30. 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.
31. 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.
32. 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.
33. Porter DW, Hubbs AF, Chen TB, McKinney W, Mercer RR, Wolfarth MG, Battelli L, Wu N, Sriram K, Leonard S, et al. Acute pulmonary dose-responses to inhaled multi-walled carbon nanotubes. Nanotoxicology 2012, 269:136-147.
34. Bauer AK, Dwyer-Nield LD, Hankin JA, Murphy RC, Malkinson AM. The lung tumor promoter, butylated hydroxytoluene (BHT), causes chronic inflammation in promotion-sensitive BALB/cByJ mice but not in promotion-resistant CXB4 mice. Toxicology 2001, 169:1-15. 10.1016/S0300-483X(01)00475-9, 11696405.
35. Bauer AK, Dwyer-Nield LD, Keil K, Koski K, Malkinson AM. Butylated hydroxytoluene (BHT) induction of pulmonary inflammation: a role in tumor promotion. Exp Lung Res 2001, 27:197-216. 10.1080/019021401300053948, 11293324.
36. Bauer AK, Rondini EA. REVIEW PAPER: the role of inflammation in mouse pulmonary neoplasia. Vet Pathol 2009, 46:369-390. 10.1354/vp.08-VP-0217-B-REV, 19176494.
37. Hussain SP, Harris CC. Inflammation and cancer: an ancient link with novel potentials. Int J Cancer 2007, 121:2373-2380. 10.1002/ijc.23173, 17893866.
38. Malkinson AM. Role of inflammation in mouse lung tumorigenesis: a review. Exp Lung Res 2005, 31:57-82.
39. Pitot HC. Endogenous carcinogenesis - the role of tumor promotion. Proc Soc Exp Biol Med 1991, 198:661-666.
40. Pitot HC. Multistage carcinogenesis - genetic and epigenetic mechanisms in relation to cancer prevention. Cancer Detect Prev 1993, 17:567-573.
41. Markowitz SB, Levin SM, Miller A, Morabia A. Asbestos 2013, Am J Respir Crit Care Med: Asbestosis, Smoking and Lung Cancer: New Findings from the North American Insulator Cohort.
42. Naimi AI, Cole SR, Hudgens MG, Brookhart MA, Richardson DB. Assessing the component associations of the healthy worker survivor bias: occupational asbestos exposure and lung cancer mortality. Ann Epidemiol 2013, 23:334-341. 10.1016/j.annepidem.2013.03.013, 23683709.
43. Mercer R, Hubbs A, Scabilloni J, Wang L, Battelli L, Schwegler-Berry D, Castranova V, Porter D. Distribution and persistence of pleural penetrations by multi-walled carbon nanotubes. Part Fibre Toxicol 2013, 7:28.
44. Ryman-Rasmussen JP, Cesta MF, Brody AR, Shipley-Phillips JK, Everitt JI, Tewksbury EW, Moss OR, Wong BA, Dodd DE, Andersen ME, Bonner JC. Inhaled carbon nanotubes reach the subpleural tissue in mice. Nat Nanotechnol 2009, 4:747-751. 10.1038/nnano.2009.305, 2783215, 19893520.
45. Sargent LM, Reynolds SH, Lowry D, Kashon ML, Benkovic SA, Salisbury JL, Hubbs AF, Keane MJ, Mastovich J, Bunker KL, et al. Genotoxicity of multi-walled carbon nanotubes at occupationally relevant doses. Proc Am Assoc Cancer Res 2012, 53:1320. Abstract #5464.
46. Stone KC, Mercer RR, Gehr P, Stockstill B, Crapo JD. Allometric relationships of cell numbers and size in the mammalian lung. Am J Respir Cell Mol Biol 1992, 6:235-243. 10.1165/ajrcmb/6.2.235, 1540387.
47. Hubbs A, Greskevitch M, Kuempel E, Suarez F, Toraason M. Abrasive blasting agents: designing studies to evaluate relative risk. J Toxicol Environ Health A 2005, 68:999-1016. 10.1080/15287390590912612, 16020188.
48. 29 CFR-Occupational Safety and Health Regulations (OSHA Standards). https://www.osha.gov/pls/oshaweb/owadisp.show_document?p_table=standards&p_id=9992.
49. Health NIOSH. Current Intelligence Bulletin 65: Occupational Exposure to Carbon Nanotubes and Nanofibers 2013,
50. Lee JH, Lee SB, Bae GN, Jeon KS, Yoon JU, Ji JH, Sung JH, Lee BG, Lee JH, Yang JS, et al. Exposure assessment of carbon nanotube manufacturing workplaces. Inhal Toxicol 2010, 22:369-381. 10.3109/08958370903367359, 20121582.
51. Maynard AD, Aitken RJ. Assessing exposure to airborne nanomaterials: current abilities and future requirements. Nanotoxicology 2007, 1:26-41.
52. Methner M, Hodson L, Dames A, Geraci C. Nanoparticle Emission Assessment Technique (NEAT) for the identification and measurement of potential inhalation exposure to engineered nanomaterials-Part B: Results from 12 field studies. J Occup Environ Hyg 2010, 7:163-176.
53. British Standards Institution Nanoparticle - Vocabulary 2011, Grimsby, UK: Castle PRess, Book Nanoparticle - Vocabulary, British Standards Institution.
54. Porter AE, Gass M, Bendall JS, Muller K, Goode A, Skepper JN, Midgley PA, Welland M. Uptake of noncytotoxic acid-treated single-walled carbon nanotubes into the cytoplasm of human macrophage cells. ACS Nano 2009, 3:1485-1492. 10.1021/nn900416z, 19459622.
55. Marcolongo G, Ruaro G, Gobbo M, Meneghetti M. Amino acid functionalization of double-wall carbon nanotubes studied by Raman spectroscopy. Chem Commun (Camb) 2007, 5:4925-4927.
56. Datsyuk V, Kalyva M, Papagelis K, Parthenios J, Tasis D, Siokou A, Kallitsis I, Galiotis C. Chemical oxidation of multiwalled carbon nanotubes. Carbon 2008, 46:833-840.
57. Underhill DM, Goodridge HS. Information processing during phagocytosis. Nat Rev Immunol 2012, 12:492-502. 10.1038/nri3244, 22699831.
58. Dinu CZ, Zhu G, Bale SS, Anand G, Reeder PJ, Sanford K, Whited G, Kane RS, Dordick JS. Enzyme-based nanoscale composites for Use as active decontamination surfaces. Adv Funct Mater 2010, 20:392-398.
59. Wiktor AE, Van Dyke DL, Stupca PJ, Ketterling RP, Thorland EC, Shearer BM, Fink SR, Stockero KJ, Majorowicz JR, Dewald GW. Preclinical validation of fluorescence in situ hybridization assays for clinical practice. Genet Med 2006, 8:16-23. 10.1097/01.gim.0000195645.00446.61, 16418595.
60. Yurov YB, Iourov IY, Monakhov VV, Soloviev IV, Vostrikov VM, Vorsanova SG. The variation of aneuploidy frequency in the developing and adult human brain revealed by an interphase FISH study. J Histochem Cytochem 2005, 53:385-390. 10.1369/jhc.4A6430.2005, 15750026.
61. Iijima S. Helical microtubules of graphitic carbon. Nature 1991, 354:56-58.
62. Chiu JC, Chang CM, Hsieh BZ, Lin SC, Yeh CY, Lin GR, Lee CK, Lin JJ, Cheng WH. Pulse shortening mode-locked fiber laser by thickness and concentration product of carbon nanotube based saturable absorber. Opt Express 2011, 19:4036-4041. 10.1364/OE.19.004036, 21369231.
63. Yang WR, Thordarson P, Gooding JJ, Ringer SP, Braet F. Carbon nanotubes for biological and biomedical applications. Nanotechnology 2007, 18:412001.
64. Bonner JC, Silva RM, Taylor A, Brown JM, Hilderbrand SC, Castranova V, Porter DW, Elder A, Oberdörster G, Harkema JR, Bramble LA, Kavanagh TJ, Botta D, Nel A, Pinkerton KE. Interlaboratory Evaluation of Rodent Pulmonary Responses to Engineered Nanomaterials: The NIEHS Nano GO Consortium. Environ Health Perspect 2013, 121:676-682. 10.1289/ehp.1205693, 3672912, 23649427.
65. Oberdorster G, Stone V, Donaldson K. Toxicology of nanoparticles: a historical perspective. Nanotoxicology 2007, 1:2-25.
66. Pitot HC, Campbell HA, Maronpot R, Bawa N, Rizvi TA, Xu YH, Sargent L, Dragan Y, Pyron M. Critical parameters in the quantitation of the stages of initiation, promotion, and progression in one model of hepatocarcinogenesis in the rat. Toxicol Pathol 1989, 17:594-611.
67. D'Assoro AB, Busby R, Suino K, Delva E, Almodovar-Mercado GJ, Johnson H, Folk C, Farrugia DJ, Vasile V, Stivala F, Salisbury JL. Genotoxic stress leads to centrosome amplification in breast cancer cell lines that have an inactive G1/S cell cycle checkpoint. Oncogene 2004, 23:4068-4075. 10.1038/sj.onc.1207568, 15064746.
68. Lingle WL, Lukasiewicz K, Salisbury JL. Deregulation of the centrosome cycle and the origin of chromosomal instability in cancer. Adv Exp Med Biol 2005, 570:393-421. 10.1007/1-4020-3764-3_14, 18727509.
69. Lingle WL, Salisbury JL. Methods for the analysis of centrosome reproduction in cancer cells. Methods Cell Biol 2001, 67:325-336.
70. Dinu CZ, Bale SS, Zhu GY, Dordick JS. Tubulin encapsulation of carbon nanotubes into functional hybrid assemblies. Small 2009, 5:310-315. 10.1002/smll.200801434, 19148890.
71. Canman JC, Cameron LA, Maddox PS, Straight A, Tirnauer JS, Mitchison TJ, Fang GW, Kapoor TM, Salmon ED. Determining the position of the cell division plane. Nature 2003, 424:1074-1078. 10.1038/nature01860, 12904818.
72. Chial HJ, Giddings TH, Siewert EA, Hoyt MA, Winey M. Altered dosage of the Saccharomyces cerevisiae spindle pole body duplication gene, NDC1, leads to aneuploidy and polyploidy. Proc Natl Acad Sci USA 1999, 96:10200-10205. 10.1073/pnas.96.18.10200, 17866, 10468586.
73. Hong KU, Park YS, Seong YS, Kang DM, Bae CD, Park J. Functional importance of the anaphase-promoting complex-Cdh1-mediated degradation of TMAP/CKAP2 in regulation of spindle function and cytokinesis. Mol Cell Biol 2007, 27:3667-3681. 10.1128/MCB.01386-06, 1900002, 17339342.
74. Asakura M, Sasaki T, Sugiyama T, Takaya M, Koda S, Nagano K, Arito H, Fukushima S. Genotoxicity and cytotoxicity of multi-wall carbon nanotubes in cultured Chinese hamster lung cells in comparison with chrysotile A fibers. J Occup Health 2010, 52:155-166. 10.1539/joh.L9150, 20379079.
75. Mangum JB, Turpin EA, Antao-Menezes A, Cesta MF, Bermudez E, Bonner JC. 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. 10.1186/1743-8977-3-15, 1693565, 17134509.
76. Mardin BR, Schiebel E. Breaking the ties that bind: new advances in centrosome biology. J Cell Biol 2012, 197:11-18. 10.1083/jcb.201108006, 3317805, 22472437.
77. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 2002, 21:4896-4905. 10.1093/emboj/cdf503, 126299, 12234929.
78. Nieznanska H, Dudek E, Zajkowski T, Szczesna E, Kasprzak AA, Nieznanski K. Prion protein impairs kinesin-driven transport. Biochem Biophys Res Commun 2012, 425:788-793. 10.1016/j.bbrc.2012.07.153, 22885185.
79. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E. Tau and MAP2 inhibit attachment of kinesin: single-molecule assay of motility in the presence of MAPs. Biophys J 2002, 82:63a-63a.
80. Thies E, Biernat J, Mandelkow EM. MARK/Par1 kinase is a regulator of microtubule-dependent transport in axons by phosphorylating tau protein. Neurobiol Aging 2004, 25:S427-S427.
81. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature 1998, 396:643-649. 10.1038/25292, 9872311.
82. Rangaswami H, Bulbule A, Kundu GC. Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol 2006, 16:79-87. 10.1016/j.tcb.2005.12.005, 16406521.
83. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, Haack H, Nardone J, Lee K, Reeves C, Li Y, et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131:1190-1203. 10.1016/j.cell.2007.11.025, 18083107.
84. Pampaloni F, Florin EL. Microtubule architecture: inspiration for novel carbon nanotube-based biomimetic materials. Trends Biotechnol 2008, 26:302-310. 10.1016/j.tibtech.2008.03.002, 18433902.
85. Shimamoto Y, Maeda YT, Ishiwata S, Libchaber AJ, Kapoor TM. Insights into the micromechanical properties of the metaphase spindle. Cell 2011, 145:1062-1074. 10.1016/j.cell.2011.05.038, 3124677, 21703450.
86. 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.
87. Donaldson K, Stone V, Seaton A, Tran L, Aitken R, Poland C. Re: Induction of mesothelioma in p53 mouse by intraperitoneal application of multi-wall carbon nanotube. J Toxicol Sci 2008, 33:385-388. 10.2131/jts.33.385, 18670173.
88. Mercer RR, Hubbs AF, Scabilloni JF, Wang L, Battelli LA, Friend S, Castranova V, Porter DW. Pulmonary fibrotic response to aspiration of multi-walled carbon nanotubes. Part Fibre Toxicol 2011, 8:21. 10.1186/1743-8977-8-21, 3152886, 21781304.
89. Mercer RR, Scabilloni JF, Hubbs AF, Battelli LA, McKinney W, Friend S, Wolfarth MG, Andrew M, Castranova V, Porter DW. Distribution and fibrotic response following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol 2013, 10.
90. Frost G, Darnton A, Harding AH. The effect of smoking on the risk of lung cancer mortality for asbestos workers in Great Britain (1971-2005). Ann Occup Hyg 2011, 55:239-247. 10.1093/annhyg/meq089, 21252055.
91. Frost G, Harding AH, Darnton A, McElvenny D, Morgan D. Occupational exposure to asbestos and mortality among asbestos removal workers: a Poisson regression analysis. Br J Cancer 2008, 99:822-829. 10.1038/sj.bjc.6604564, 2528146, 18728672.
92. Kane AB. Animal models of malignant mesothelioma. Inhal Toxicol 2006, 18:1001-1004. 10.1080/08958370600835393, 16920675.
93. Metintas S, Metintas M, Ak G, Kalyoncu C. Environmental asbestos exposure in rural Turkey and risk of lung cancer. Int J Environ Health Res 2012, 22:468-479. 10.1080/09603123.2011.654330, 22300246.
94. Takagi A, Hirose A, Nishimura T, Fukumori N, Ogata A, Ohashi N, Kitajima S, Kanno J. Induction of mesothelioma in p53+/- mouse by intraperitoneal application of multi-wall carbon nanotube. J Toxicol Sci 2008, 33:105-116. 10.2131/jts.33.105, 18303189.
95. Takagi A, Hirose A, Futakuchi M, Tsuda H, Kanno J. Dose-dependent mesothelioma induction by intraperitoneal administration of multi-wall carbon nanotubes in p53 heterozygous mice. Cancer Sci 2012, 103:1440-1444. 10.1111/j.1349-7006.2012.02318.x, 3569866, 22537085.
96. Nagai H, Okazaki Y, Chew SH, Misawa N, Yamashita Y, Akatsuka S, Ishihara T, Yamashita K, Yoshikawa Y, Yasui H, et al. Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. Proc Natl Acad Sci USA 2011, 108:E1330-E1338. 10.1073/pnas.1110013108, 3241783, 22084097.
97. Sargent LM, Porter DW, LM S, AF H, Lowry DT LB, KJ S, ML K, RR M, AK B, et al. Promotion of lung adenocarcinoma following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol in press.
98. Devereux TR, Anderson MW, Belinsky SA. Role of Ras protooncogene activation in the formation of spontaneous and nitrosamine-induced lung-tumors in the resistant C3h mouse. Carcinogenesis 1991, 12:299-303. 10.1093/carcin/12.2.299, 1995195.
99. Malkinson AM. The genetic-basis of susceptibility to lung-tumors in mice. Toxicology 1989, 54:241-271. 10.1016/0300-483X(89)90062-0, 2650016.
100. Chen CY, Ge CC, Lao F, Li W, Li YF, Qiu Y, Mao XY, Li B, Chai ZF, Zhao YL. Quantitative analysis of metal impurities in carbon nanotubes: efficacy of different pretreatment protocols for ICPMS spectroscopy. Anal Chem 2008, 80:9426-9434. 10.1021/ac801469b, 18998708.
101. Food and Drug Administration Guidance for industry: assessing the effects of significant manufacturing process changes, including emerging technologies, on teh safety and regulatory status of food ingredients and food contact substances, including food ingredients that are color additives - draft guidance. Book Guidance for Industry: Assessing the Effects of Significant Manufacturing Process Changes, Including Emerging Technologies, on teh Safety and Regulatory Status of Food Ingredients and Food Contact SUbstances, Including Food Ingredients that are Color Additives - Draft Guidance 2012, Rockville, MD: Food and Drug Administration, Food and Drug Administration.
102. Oxford Dictionaries Online http://oxforddictionaries.com/.
103. Salisbury JL, D'Assoro AB, Lingle WL. Centrosome amplification and the origin of chromosomal instability in breast cancer. J Mammary Gland Biol Neoplasia 2004, 9:275-283.
104. Haas A, Fischer MS. Three-dimensional reconstruction of histological sections using modern product-design software. Anat Rec 1997, 249:510-516. 10.1002/(SICI)1097-0185(199712)249:4<510::AID-AR11>3.0.CO;2-R, 9415459.
105. ACMG Standards and guidelines for clinical genetics laboratories, in: documentation of FISH results 2006, Bethesda, MD: American College of Medical Genetics, ACMG.