Gene expression profile of human lung epithelial cells chronically exposed to single-walled carbon nanotubes

Nanoscale Research Letters

Volumn 10, Issue 1, 2015, Pages 1-12

  Chen, Dongquan ^a   Stueckle, Todd A ^b   Luanpitpong, Sudjit ^c   Rojanasakul, Yon ^c   Lu, Yongju ^d   Wang, Liying ^b  

^a University of Alabama at Birmingham   (United States)

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

^c WEST VIRGINIA UNIVERSITY   (United States)

^d WAYNE STATE UNIVERSITY   (United States)

Author keywords

Gene expression; Lung; Microarray; p53; Pathways; Single walled carbon nanotubes

Indexed keywords

ASBESTOS; BIOASSAY; BIOLOGICAL ORGANS; CELL DEATH; CELL SIGNALING; GENE EXPRESSION; MAMMALS; MICROARRAYS; NANOTUBES; RESPIRATORY SYSTEM;

CARCINOGENIC POTENTIAL; DIFFERENTIALLY EXPRESSED GENE; ENGINEERED NANOMATERIALS; GENE EXPRESSION PROFILES; LUNG; MALIGNANT TRANSFORMATIONS; PATHWAYS; SINGLEWALLED CARBON NANOTUBE (SWCNT);

SINGLE-WALLED CARBON NANOTUBES (SWCN);

ASBESTOS; BIOTECHNOLOGY; CARBON FIBERS; CELLS; GENES;

ANIMALIA; MUS;

EID: 84961289516     PISSN: 19317573     EISSN: 1556276X     Source Type: Journal    
DOI: 10.1186/s11671-014-0707-0     Document Type: Article

References (61)

1. Zhang Z, Yang X, Zhang Y, Zeng B, Wang S, Zhu T, et al. Delivery of telomerase reverse transcriptase small interfering RNA in complex with positively charged single-walled carbon nanotubes suppresses tumor growth. Clin cancer Res. 2006;12:4933–9.
2. Roco MC. Environmentally responsible development of nanotechnology. Environ Sci Technol. 2005;39:106A–12.
3. Helland A, Wick P, Koehler A, Schmid K, Som C. Reviewing the environmental and human health knowledge base of carbon nanotubes. Environ Health Perspect. 2007;115:1125–31.
4. Jaurand MC, Renier A, Daubriac J. Mesothelioma: Do asbestos and carbon nanotubes pose the same health risk? Part Fibre Toxicol. 2009;6:16.
5. Manning CB, Vallyathan V, Mossman BT. Diseases caused by asbestos: mechanisms of injury and disease development. Int Immunopharmacol. 2002;2:191–200.
6. Song Y, Li X, Wang L, Rojanasakul Y, Castranova V, Li H, et al. Nanomaterials in humans: identification, characteristics, and potential damage. Toxicol Pathol. 2011;39:841–9.
7. Mercer RR, Hubbs AF, Scabilloni JF, Wang L, Battelli LA, Schwegler-Berry D, et al. Distribution and persistence of pleural penetrations by multi-walled carbon nanotubes. Part Fibre Toxicol. 2010;7:28.
8. Mercer RR, Scabilloni J, Wang L, Kisin E, Murray AR, Schwegler-Berry D, et al. 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:L87–97.
9. Shvedova AA, Kisin E, Murray AR, Johnson VJ, Gorelik O, Arepalli S, 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:L552–65.
10. Wang L, Mercer RR, Rojanasakul Y, Qiu A, Lu Y, Scabilloni JF, et al. Direct fibrogenic effects of dispersed single-walled carbon nanotubes on human lung fibroblasts. J Toxic Environ Health A. 2010;73:410–22.
11. Sargent LM, Porter DW, Staska LM, Hubbs AF, Lowry DT, Battelli L, et al. Promotion of lung adenocarcinoma following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol. 2014;11:3.
12. Sargent LM, Hubbs AF, Young SH, Kashon ML, Dinu CZ, Salisbury JL, et al. Single-walled carbon nanotube-induced mitotic disruption. Mutat Res. 2012;745:28–37.
13. Wang L, Luanpitpong S, Castranova V, Tse W, Lu Y, Pongrakhananon V, et al. Carbon nanotubes induce malignant transformation and tumorigenesis of human lung epithelial cells. Nano Lett. 2011;11:2796–803.
14. Folkmann JK, Risom L, Jacobsen NR, Wallin H, Loft S, Moller P. Oxidatively damaged DNA in rats exposed by oral gavage to C60 fullerenes and single-walled carbon nanotubes. Environ Health Perspect. 2009;117:703–8.
15. Lindberg HK, Falck GC, Suhonen S, Vippola M, Vanhala E, Catalan J, et al. Genotoxicity of nanomaterials: DNA damage and micronuclei induced by carbon nanotubes and graphite nanofibres in human bronchial epithelial cells in vitro. Toxicol Lett. 2009;186:166–73.
16. Yamashita K, Yoshioka Y, Higashisaka K, Morishita Y, Yoshida T, Fujimura M, et al. Carbon nanotubes elicit DNA damage and inflammatory response relative to their size and shape. Inflammation. 2010;33:276–80.
17. Pacurari M, Yin XJ, Zhao J, Ding M, Leonard SS, Schwegler-Berry D, et al. 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. 2008;116:1211–7.
18. Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WA, Seaton A, et al. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol. 2008;3:423–8.
19. Takagi A, Hirose A, Nishimura T, Fukumori N, Ogata A, Ohashi N, et al. Induction of mesothelioma in p53+/− mouse by intraperitoneal application of multi-wall carbon nanotube. J Toxicol Sci. 2008;33:105–16.
20. Sargent LM, Shvedova AA, Hubbs AF, Salisbury JL, Benkovic SA, Kashon ML, et al. Induction of aneuploidy by single-walled carbon nanotubes. Environ Mol Mutagen. 2009;50:708–17.
21. Azad N, Iyer AK, Wang L, Liu Y, Lu Y, Rojanasakul Y. Reactive oxygen species-mediated p38 MAPK regulates carbon nanotube-induced fibrogenic and angiogenic responses. Nanotoxicology. 2013;7:157–68.
22. Park EJ, Roh J, Kim SN, Kang MS, Lee BS, Kim Y, et al. Biological toxicity and inflammatory response of semi-single-walled carbon nanotubes. PLoS One. 2011;6:e25892.
23. Snyder-Talkington BN, Pacurari M, Dong C, Leonard SS, Schwegler-Berry D, Castranova V, et al. Systematic analysis of multiwalled carbon nanotube-induced cellular signaling and gene expression in human small airway epithelial cells. Toxicol Sci. 2013;133:79–89.
24. Lohcharoenkal W, Wang L, Stueckle TA, Dinu CZ, Castranova V, Liu Y, et al. Chronic exposure to carbon nanotubes induces invasion of human mesothelial cells through matrix metalloproteinase-2. ACS Nano. 2013;7:7711–23.
25. Nagai H, Okazaki Y, Chew SH, Misawa N, Yamashita Y, Akatsuka S, et al. Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. Proc Natl Acad Sci U S A. 2011;108:E1330–8.
26. Shvedova AA, Yanamala N, Kisin ER, Tkach AV, Murray AR, Hubbs A, et al. Long-term effects of carbon containing engineered nanomaterials and asbestos in the lung: one year postexposure comparisons. Am J Physiol Lung Cell Mol Physiol. 2014;306:L170–82.
27. Wang L, Stueckle TA, Mishra A, Derk R, Meighan T, Castranova V, et al. Neoplastic-like transformation effect of single-walled and multi-walled carbon nanotubes compared to asbestos on human lung small airway epithelial cells. Nanotoxicology. 2014;8:485–507.
28. Teeguarden JG, Webb-Robertson BJ, Waters KM, Murray AR, Kisin ER, Varnum SM, et al. Comparative proteomics and pulmonary toxicity of instilled single-walled carbon nanotubes, crocidolite asbestos, and ultrafine carbon black in mice. Toxicol Sci. 2011;120:123–35.
29. Pacurari M, Qian Y, Porter DW, Wolfarth M, Wan Y, Luo D, et al. Multi-walled carbon nanotube-induced gene expression in the mouse lung: association with lung pathology. Toxicol Appl Pharmacol. 2011;255:18–31.
30. Wu P, Yuan SS, Ho CC, Hsieh WY, Hong QS, Yu SL, et al. Focal amplification of HOXD-harboring chromosome region is implicated in multiple-walled carbon nanotubes-induced carcinogenicity. Nano Lett. 2013;13:4632–41.
31. 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. Toxicol Sci. 2010;7:5.
32. She QB, Chen N, Dong Z. ERKs and p38 kinase phosphorylate p53 protein at serine 15 in response to UV radiation. J Biol Chem. 2000;275:20444–9.
33. Appella E, Anderson CW. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem. 2001;268:2764–72.
34. Gerwin BI, Spillare E, Forrester K, Lehman TA, Kispert J, Welsh JA, et al. Mutant p53 can induce tumorigenic conversion of human bronchial epithelial cells and reduce their responsiveness to a negative growth factor, transforming growth factor beta 1. Proc Natl Acad Sci U S A. 1992;89:2759–63.
35. Unger T, Sionov RV, Moallem E, Yee CL, Howley PM, Oren M, et al. Mutations in serines 15 and 20 of human p53 impair its apoptotic activity. Oncogene. 1999;18:3205–12.
36. Hussain SP, Amstad P, Raja K, Sawyer M, Hofseth L, Shields PG, et al. Mutability of p53 hotspot codons to benzo(a)pyrene diol epoxide (BPDE) and the frequency of p53 mutations in nontumorous human lung. Cancer Res. 2001;61:6350–5.
37. 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;6:235–43.
38. Liao WT, Lin P, Cheng TS, Yu HS, Chang LW. Arsenic promotes centrosome abnormalities and cell colony formation in p53 compromised human lung cells. Toxicol Appl Pharmacol. 2007;225:162–70.
39. Stueckle TA, Lu Y, Davis ME, Wang L, Jiang BH, Holaskova I, et al. Chronic occupational exposure to arsenic induces carcinogenic gene signaling networks and neoplastic transformation in human lung epithelial cells. Toxicol Appl Pharmacol. 2012;261:204–16.
40. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med. 1990;9:811–8.
41. Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–5.
42. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–82.
43. Harris CC. p53 tumor suppressor gene: at the crossroads of molecular carcinogenesis, molecular epidemiology, and cancer risk assessment. Environ Health Perspect. 1996;104 Suppl 3:435–9.
44. Lehman TA, Modali R, Boukamp P, Stanek J, Bennett WP, Welsh JA, et al. p53 mutations in human immortalized epithelial cell lines. Carcinogenesis. 1993;14:833–9.
45. Herzog E, Byrne HJ, Casey A, Davoren M, Lenz AG, Maier KL, et al. SWCNT suppress inflammatory mediator responses in human lung epithelium in vitro. Toxicol Appl Pharmacol. 2009;234:378–90.
46. Turabekova M, Rasulev B, Theodore M, Jackman J, Leszczynska D, Leszczynski J. Immunotoxicity of nanoparticles: a computational study suggests that CNTs and C60 fullerenes might be recognized as pathogens by Toll-like receptors. Nanoscale. 2014;6:3488–95.
47. Sargent LM, Reynolds SH, Castranova V. Potential pulmonary effects of engineered carbon nanotubes: in vitro genotoxic effects. Nanotoxicology. 2010;4:396–408.
48. Shivapurkar N, Reddy J, Chaudhary PM, Gazdar AF. Apoptosis and lung cancer: a review. J Cell Biochem. 2003;88:885–98.
49. Gatenby RA, Gillies RJ. A microenvironmental model of carcinogenesis. Nat Rev Cancer. 2008;8:56–61.
50. Park EJ, Zahari NE, Lee EW, Song J, Lee JH, Cho MH, et al. SWCNTs induced autophagic cell death in human bronchial epithelial cells. Toxicol In Vitro. 2014;28:442–50.
51. Zhang T, Qi Y, Liao M, Xu M, Bower KA, Frank JA, et al. Autophagy is a cell self-protective mechanism against arsenic-induced cell transformation. Toxicol Sci. 2012;130:298–308.
52. Behrens J. Control of beta-catenin signaling in tumor development. Ann N Y Acad Sci. 2000;910:21–33. discussion 33–25.
53. Cox ML, Meek DW. Phosphorylation of serine 392 in p53 is a common and integral event during p53 induction by diverse stimuli. Cell Signal. 2010;22:564–71.
54. Ghosh JC, Dohi T, Kang BH, Altieri DC. Hsp60 regulation of tumor cell apoptosis. J Biol Chem. 2008;283:5188–94.
55. 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. author reply 386–388.
56. Nagai H, Toyokuni S. Differences and similarities between carbon nanotubes and asbestos fibers during mesothelial carcinogenesis: shedding light on fiber entry mechanism. Cancer Sci. 2012;103:1378–90.
57. Huang X, Zhang F, Sun X, Choi KY, Niu G, Zhang G, et al. The genotype-dependent influence of functionalized multiwalled carbon nanotubes on fetal development. Biomaterials. 2014;35:856–65.
58. Zhang L, Gallup M, Zlock L, Finkbeiner WE, McNamara NA. Rac1 and Cdc42 differentially modulate cigarette smoke-induced airway cell migration through p120-catenin-dependent and -independent pathways. Am J Pathol. 2013;182:1986–95.
59. Pez F, Lopez A, Kim M, Wands JR, Caron de Fromentel C, Merle P. Wnt signaling and hepatocarcinogenesis: molecular targets for the development of innovative anticancer drugs. J Hepatol. 2013;59:1107–17.
60. Licciulli S, Avila JL, Hanlon L, Troutman S, Cesaroni M, Kota S, et al. Notch1 is required for Kras-induced lung adenocarcinoma and controls tumor cell survival via p53. Cancer Res. 2013;73:5974–84.
61. Fuchs SY, Adler V, Pincus MR, Ronai Z. MEKK1/JNK signaling stabilizes and activates p53. Proc Natl Acad Sci U S A. 1998;95:10541–6.