Extensive temporal transcriptome and microRNA analyses identify molecular mechanisms underlying mitochondrial dysfunction induced by multi-walled carbon nanotubes in human lung cells

References

• Antico Arciuch VG, Elguero ME, Poderoso JJ, Carreras MC. 2012. Mitochondrial regulation of cell cycle and proliferation. Antioxid Redox Signal 16:1150–80
   PubMed Web of Science ®Google Scholar
• Assaily W, Rubinger D, Wheaton K, Lin Y, Ma W, Xuan W, et al. 2011. Ros-mediated p53 induction of lpin1 regulates fatty acid oxidation in response to nutritional stress. Mol Cell 44:491–501
   Google Scholar
• Attene-Ramos M, Huang R, Michael S, Witt K, Richard A, Tice R, et al. 2014. Profiling of the tox21 chemical collection for mitochondrial function to identify compounds that acutely decrease mitochondrial membrane potential. Environ Health Perspect 123:49–56
   Google Scholar
• Bienertova-Vasku J, Sana J, Slaby O. 2013. The role of micrornas in mitochondria in cancer. Cancer Lett 336:1–7
   Google Scholar
• Cavill R, Kleinjans J, Briedé J-J. 2013. Dtw4omics: comparing patterns in biological time series. PLoS ONE 8:e71823
   PubMed Web of Science ®Google Scholar
• Chen R, Huo L, Shi X, Bai R, Zhang Z, Zhao Y, et al. 2014. Endoplasmic reticulum stress induced by zinc oxide nanoparticles is an earlier biomarker for nanotoxicological evaluation. ACS Nano 8:2562–74
   PubMed Web of Science ®Google Scholar
• Courcot E, Leclerc J, Lafitte J-J, Mensier E, Jaillard S, Gosset P, et al. 2012. Xenobiotic metabolism and disposition in human lung cell models: comparison with in vivo expression profiles. Drug Metab Dispos 40:1953–65
   PubMed Web of Science ®Google Scholar
• Cveticanin J, Joksic G, Leskovac A, Petrovic S, Sobot A, Neskovic O. 2010. Using carbon nanotubes to induce micronuclei and double strand breaks of the DNA in human cells. Nanotechnology 21:015102
   PubMed Web of Science ®Google Scholar
• Dai M, Wang P, Boyd AD, Kostov G, Athey B, Jones EG, et al. 2005. Evolving gene/transcript definitions significantly alter the interpretation of genechip data. Nucl Acid Res 33:e175
   PubMed Web of Science ®Google Scholar
• De Volder MFL, Tawfick SH, Baughman RH, Hart AJ. 2013. Carbon nanotubes: present and future commercial applications. Science 339:535–9
   PubMed Web of Science ®Google Scholar
• Deferme L, Briedé JJ, Claessen SMH, Jennen DGJ, Cavill R, Kleinjans JCS. 2013. Time series analysis of oxidative stress response patterns in hepg2: a toxicogenomics approach. Toxicology 306:24–34
   Google Scholar
• Di Giorgio ML, Bucchianico SD, 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 Genet Toxicol Environ Mutagen 722:20–31
   PubMed Web of Science ®Google Scholar
• Donaldson K, Murphy F, Duffin R, Poland C. 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
   PubMed Web of Science ®Google Scholar
• Dörger M, Münzing S, Allmeling A, Krombach F. 2000. Comparison of the phagocytic response of rat and hamster alveolar macrophages to man-made vitreous fibers in vitro. Hum Exp Toxicol 19:635–40
   PubMed Web of Science ®Google Scholar
• Eijssen LMT, Jaillard M, Adriaens ME, Gaj S, De Groot PJ, Müller M, Evelo CT. 2013. User-friendly solutions for microarray quality control and pre-processing on arrayanalysis.Org. Nucl Acid Res 41:W71–6
   PubMed Web of Science ®Google Scholar
• Ernst J, Bar-Joseph Z. 2006. Stem: a tool for the analysis of short time series gene expression data. BMC Bioinformat 7:191
   PubMed Web of Science ®Google Scholar
• Garcia-Canton C, Minet E, Anadon A, Meredith C. 2013. Metabolic characterization of cell systems used in in vitro toxicology testing: lung cell system beas-2b as a working example. Toxicol Vitro 27:1719–27
   PubMed Web of Science ®Google Scholar
• Geiser M, Matter M, Maye I, Im Hof V, Gehr P, Schürch S. 2003. Influence of airspace geometry and surfactant on the retention of man-made vitreous fibers (mmvf 10a). Environ Health Perspect 111:895–901
   PubMed Web of Science ®Google Scholar
• Gilmour PS, Brown DM, Beswick PH, Macnee W, Rahman I, Donaldson K. 1997. Free radical activity of industrial fibers: role of iron in oxidative stress and activation of transcription factors. Environ Health Perspect 105:1313–17
   PubMed Web of Science ®Google Scholar
• Giorgi C, Agnoletto C, Bononi A, Bonora M, De Marchi E, Marchi S, et al. 2012. Mitochondrial calcium homeostasis as potential target for mitochondrial medicine. Mitochondrion 12:77–85
   Google Scholar
• Grosse Y, Loomis D, Guyton KZ, Lauby-Secretan B, El Ghissassi F, Bouvard V, et al. 2014. Carcinogenicity of fluoro-edenite, silicon carbide fibres and whiskers, and carbon nanotubes. Lancet Oncol 15:1427–8
   PubMed Web of Science ®Google Scholar
• Haniu H, Saito N, Matsuda Y, Kim Y-A, Park K, Tsukahara T, et al. 2011. Elucidation mechanism of different biological responses to multi-walled carbon nanotubes using four cell lines. Int J Nanomed. 6:3487–97
   Web of Science ®Google Scholar
• Hebels D Ga J, Briedé JJ, Khampang R, Kleinjans JCS, De Kok TMCM. 2010. Radical mechanisms in nitrosamine- and nitrosamide-induced whole-genome gene expression modulations in caco-2 cells. Toxicol Sci 116:194–205
   Google Scholar
• Hesterberg TW, Axten C, Mcconnell EE, Oberdörster G, Everitt J, Miiller WC, et al. 1997. Chronic inhalation study of fiber glass and amosite asbestos in hamsters: Twelve-month preliminary results. Environ Health Perspect 105:1223–9
   PubMed Web of Science ®Google Scholar
• Hesterberg TW, Miiller WC, Mcconnell EE, Chevalier J, Hadley JG, Bernstein DM, et al. 1993. Chronic inhalation toxicity of size-separated glass fibers in fischer 344 rats. Toxicol Sci 20:464–76
   Google Scholar
• Huang DW, Sherman BT, Lempicki RA. 2008. Systematic and integrative analysis of large gene lists using david bioinformatics resources. Nat Protocols 4:44–57
   PubMed Web of Science ®Google Scholar
• Huang S, Partridge M, Ghandhi S, Davidson M, Amundson S, Hei T. 2012. Mitochondria-derived reactive intermediate species mediate asbestos-induced genotoxicity and oxidative stress–responsive signaling pathways. Environ Health Perspect 120:840–7
   Google Scholar
• IARC. 2002. Man-Made Vitreous Fibres. IARC Monographs. France: IARC
   Google Scholar
• Jensen CG, Watson M. 1999. Inhibition of cytokinesis by asbestos and synthetic fibres. Cell Biol Int 23:829–40
   PubMed Web of Science ®Google Scholar
• Jensen KA. 2013. Deliverable 4.1: Summary report on primary physicochemical properties of manufactured nanomaterials used in NANOGENOTOX. Available at: http://www.nanogenotox.eu/files/PDF/Deliverables/d4.1_summary%20report.pdf . Accessed on 1st August 2014
   Google Scholar
• Kamburov A, Stelzl U, Lehrach H, Herwig R. 2013. The consensuspathdb interaction database: 2013 update. Nucl Acid Res 41:D793–800
   PubMed Web of Science ®Google Scholar
• Katsushima K, Shinjo K, Natsume A, Ohka F, Fujii M, Osada H, et al. 2012. Contribution of microrna-1275 to claudin11 protein suppression via a polycomb-mediated silencing mechanism in human glioma stem-like cells. J Biol Chem 287:27396–406
   PubMed Web of Science ®Google Scholar
• Kinnula VL, Yankaskas JR, Chang L, Virtanen I, Linnala A, Kang BH, Crapo JD. 1994. Primary and immortalized (beas 2b) human bronchial epithelial cells have significant antioxidative capacity in vitro. Am J Resp Cell Mol Biol 11:568–76
   PubMedGoogle Scholar
• Krewski D, Acosta D, Andersen M, Anderson H, Bailar JC, Boekelheide K, et al., Staff of Committee on Toxicity T & Assessment of Environmental A. 2010. Toxicity testing in the 21st century: a vision and a strategy. J Toxicol Environ Health, Part B 13:51–138
   PubMed Web of Science ®Google Scholar
• Leithner K, Hrzenjak A, Trotzmuller M, Moustafa T, Kofeler HC, Wohlkoenig C, et al. 2014. Pck2 activation mediates an adaptive response to glucose depletion in lung cancer. Oncogene 34:1044–50
   Google Scholar
• Lindberg HK, Falck GCM, Singh R, Suhonen S, Järventaus H, Vanhala E, et al. 2013. Genotoxicity of short single-wall and multi-wall carbon nanotubes in human bronchial epithelial and mesothelial cells in vitro. Toxicology 313:24–37
   PubMed Web of Science ®Google Scholar
• Liu G, Cheresh P, Kamp DW. 2013. Molecular basis of asbestos-induced lung disease. Annu Rev Pathol: Mech Dis 8:161–87
   Google Scholar
• Liu G, Kamp DW. 2011. Mitochondrial DNA damage: role of ogg1 and aconitase. In: Kruman I, ed. DNA Repair. Rijeka, Croatia: InTech, 85–102
   Google Scholar
• Lopez-Romero P. 2011. Pre-processing and differential expression analysis of agilent microrna arrays using the agimicrorna bioconductor library. BMC Genom 12:64
   PubMed Web of Science ®Google Scholar
• Mao P, Reddy PH. 2011. Aging and amyloid beta-induced oxidative DNA damage and mitochondrial dysfunction in alzheimer’s disease: implications for early intervention and therapeutics. Biochim Biophys Acta 1812:1359–70
   PubMed Web of Science ®Google Scholar
• Mcconnell E, Axten C, Hesterberg T, Chevalier J, Miiller W, Everitt J, et al. 1999. Studies on the inhalation toxicology of two fiberglasses and amosite asbestos in the syrian golden hamster. Part ii. Results of chronic exposure. Inhal Toxicol 11:785–835
   PubMed Web of Science ®Google Scholar
• Misawa T, Takahama M, Kozaki T, Lee H, Zou J, Saitoh T, Akira S. 2013. Microtubule-driven spatial arrangement of mitochondria promotes activation of the nlrp3 inflammasome. Nat Immunol 14:454–60
   PubMed Web of Science ®Google Scholar
• Mishra A, Rojanasakul Y, Chen BT, Castranova V, Mercer RR, Wang L. 2012. Assessment of pulmonary fibrogenic potential of multiwalled carbon nanotubes in human lung cells. J Nanomat 2012:930931
   Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Murray A, Kisin E, Tkach A, Yanamala N, Mercer R, Young S-H, et al. 2012. Factoring-in agglomeration of carbon nanotubes and nanofibers for better prediction of their toxicity versus asbestos. Part Fibre Toxicol 9:10
   PubMed Web of Science ®Google Scholar
• Nabben M, Hoeks J, Moonen-Kornips E, Van Beurden D, Briedé JJ, Hesselink MKC, et al. 2011. Significance of uncoupling protein 3 in mitochondrial function upon mid- and long-term dietary high-fat exposure. FEBS Lett 585:4010–17
   Google Scholar
• Nymark P, Jensen K, Suhonen S, Kembouche Y, Vippola M, Kleinjans J, et al. 2014. Free radical scavenging and formation by multi-walled carbon nanotubes in cell free conditions and in human bronchial epithelial cells. Partic Fibre Toxicol 11:4
   PubMed Web of Science ®Google Scholar
• Nymark P, Lindholm P, Korpela M, Lahti L, Ruosaari S, Kaski S, et al. 2007. Gene expression profiles in asbestos-exposed epithelial and mesothelial lung cell lines. BMC Genom 8:62
   PubMed Web of Science ®Google Scholar
• Nymark P, Wikman H, Hienonen-Kempas T, Anttila S. 2008. Molecular and genetic changes in asbestos-related lung cancer. Cancer Lett 265:1–15
   PubMed Web of Science ®Google Scholar
• Nymark P, Wikman H, Ruosaari S, Hollmén J, Vanhala E, Karjalainen A, et al. 2006. Identification of specific gene copy number changes in asbestos-related lung cancer. Cancer Res 66:5737–43
   PubMed Web of Science ®Google Scholar
• Oliveros J. 2007. An interactive tool for comparing lists with venn diagrams. Available at: http://bioinfogp.Cnb.Csic.Es/tools/venny/index.html . Accessed on 15th January 2015
   Google Scholar
• Osmond-Mcleod M, Poland C, Murphy F, Waddington L, Morris H, Hawkins S, et al. 2011. Durability and inflammogenic impact of carbon nanotubes compared with asbestos fibres. Part Fibre Toxicol 8:15
   PubMed Web of Science ®Google Scholar
• Palomäki J, Sund J, Vippola M, Kinaret P, Greco D, Savolainen K, et al. 2015. A secretomics analysis reveals major differences in the macrophage responses towards different types of carbon nanotubes. Nanotoxicology [ Epub ahead of print]: 1–10. doi: 10.3109/17435390.2014.969346
   Google Scholar
• Palomäki J, Välimäki 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
   PubMed Web of Science ®Google Scholar
• Panduri V, Weitzman SA, Chandel N, Kamp DW. 2003. The mitochondria-regulated death pathway mediates asbestos-induced alveolar epithelial cell apoptosis. Am J Resp Cell Mol Biol 28:241–8
   PubMed Web of Science ®Google Scholar
• Panduri V, Weitzman SA, Chandel NS, Kamp DW. 2004. Mitochondrial-derived free radicals mediate asbestos-induced alveolar epithelial cell apoptosis. Am J Physiol – Lung Cell Mol Physiol 286:L1220–7
   PubMed Web of Science ®Google Scholar
• Piskernik C, Haindl S, Behling T, Gerald Z, Kehrer I, Redl H, Kozlov AV. 2008. Antimycin a and lipopolysaccharide cause the leakage of superoxide radicals from rat liver mitochondria. Biochim Biophys Acta – Molecular Basis of Disease 1782:280–5
   Google Scholar
• Pociask DA, Sime PJ, Brody AR. 2004. Asbestos-derived reactive oxygen species activate tgf-[beta]1. Lab Invest 84:1013–23
   PubMed Web of Science ®Google Scholar
• Poland CA, Duffin R, Kinloch I, Maynard A, Wallace Wa H, Seaton A, et al. 2008. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nano 3:423–8
   PubMed Web of Science ®Google Scholar
• Poulsen SS, Jacobsen NR, Labib S, Wu D, Husain M, Williams A, et al. 2013. Transcriptomic analysis reveals novel mechanistic insight into murine biological responses to multi-walled carbon nanotubes in lungs and cultured lung epithelial cells. PLoS ONE 8:e80452
   PubMed Web of Science ®Google Scholar
• Poulsen SS, Saber AT, Williams A, Andersen O, Købler C, Atluri R, et al. 2015. MWCNTs of different physicochemical properties cause similar inflammatory responses, but differences in transcriptional and histological markers of fibrosis in mouse lungs. Toxicol Appl Pharmacol 284:16–32
   PubMed Web of Science ®Google Scholar
• Prokisch H, Andreoli C, Ahting U, Heiss K, Ruepp A, Scharfe C, Meitinger T. 2006. Mitop2: the mitochondrial proteome database—now including mouse data. Nucl Acid Res 34:D705–11
   PubMed Web of Science ®Google Scholar
• Pulskamp K, Diabaté 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
   PubMed Web of Science ®Google Scholar
• R Core team. 2014. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing
   Google Scholar
• Ramzan R, Staniek K, Kadenbach B, Vogt S. 2010. Mitochondrial respiration and membrane potential are regulated by the allosteric atp-inhibition of cytochrome c oxidase. Biochim Biophys Acta – Bioenergetics 1797:1672–80
   PubMedGoogle Scholar
• Reddel RR, Ke Y, Gerwin BI, Mcmenamin MG, Lechner JF, Su RT, et al. 1988. Transformation of human bronchial epithelial cells by infection with sv40 or adenovirus-12 sv40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing sv40 early region genes. Cancer Res 48:1904–9
   PubMed Web of Science ®Google Scholar
• Ryman-Rasmussen JP, Tewksbury EW, Moss OR, Cesta MF, Wong BA, Bonner JC. 2009. Inhaled multiwalled carbon nanotubes potentiate airway fibrosis in murine allergic asthma. Am J Resp Cell Mol Biol 40:349–58
   PubMed Web of Science ®Google Scholar
• Sargent L, Porter D, Staska L, Hubbs A, Lowry D, Battelli L, et al. 2014. Promotion of lung adenocarcinoma following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol 11:3
   PubMed Web of Science ®Google Scholar
• Searl A, Buchanan D, Cullen RT, Jones AD, Miller BG, Soutar CA. 1999. Biopersistence and durability of nine mineral fibre types in rat lungs over 12 months. Ann Occup Hyg 43:143–53
   PubMed Web of Science ®Google Scholar
• Siegrist K, Reynolds S, Kashon M, Lowry D, Dong C, Hubbs A, et al. 2014. Genotoxicity of multi-walled carbon nanotubes at occupationally relevant doses. Part Fibre Toxicol 11:6
   PubMed Web of Science ®Google Scholar
• Smyth GK, Michaud J, Scott HS. 2005. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21:2067–75
   PubMed Web of Science ®Google Scholar
• Snyder-Talkington B, Dymacek J, Porter D, Wolfarth M, Mercer R, Pacurari M, et al. 2013. System-based identification of toxicity pathways associated with multi-walled carbon nanotube-induced pathological responses. Toxicol Appl Pharmacol 272:476–89
   PubMed Web of Science ®Google Scholar
• Sohn EJ, Kim J, Hwang Y, Im S, Moon Y, Kang DM. 2012. Tgf-beta suppresses the expression of genes related to mitochondrial function in a549 cells. Cell Mol Biol (Noisy-le-grand) 58:OL1763–7
   Google Scholar
• Sriram K, Porter D, Jefferson A, Lin G, Wolfarth M, Chen B, et al. 2009. Neuroinflammation and blood-brain barrier changes following exposure to engineered nanomaterials. Toxicologist 108:458
   Google Scholar
• Takagi A, Hirose A, Futakuchi M, Tsuda H, Kanno J. 2012. Dose-dependent mesothelioma induction by intraperitoneal administration of multi-wall carbon nanotubes in p53 heterozygous mice. Cancer Sci 103:1440–4
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Tomasetti M, Neuzil J, Dong L. 2014. Micrornas as regulators of mitochondrial function: role in cancer suppression. Biochim Biophys Acta – General Subjects 1840:1441–53
   Google Scholar
• Topinka J, Loli P, Dušinská M, Hurbánková M, Kováčiková Z, Volkovová K, et al. 2006. Mutagenesis by man-made mineral fibres in the lung of rats. Mutat Res Fundam Mol Mech Mutagen 595:174–83
   PubMed Web of Science ®Google Scholar
• Toyokuni S. 2013. Genotoxicity and carcinogenicity risk of carbon nanotubes. Adv Drug Deliv Rev 65:2098–110
   PubMed Web of Science ®Google Scholar
• Tran CL, Jones AD, Donaldson K. 1996. Evidence of overload, dissolution and breakage of mmvf10 fibres in the rcc chronic inhalation study. Exp Toxicol Pathol 48:500–4
   PubMedGoogle Scholar
• Van Den Hof WFPM, Van Summeren A, Lommen A, Coonen MLJ, Brauers K, Van Herwijnen M, et al. 2014. Integrative cross-omics analysis in primary mouse hepatocytes unravels mechanisms of cyclosporin a-induced hepatotoxicity. Toxicology 324:18–26
   PubMed Web of Science ®Google Scholar
• Wang L, Stueckle TA, Mishra A, Derk R, Meighan T, Castranova V, Rojanasakul Y. 2014. Neoplastic-like transformation effect of single-walled and multi-walled carbon nanotubes compared to asbestos on human lung small airway epithelial cells. Nanotoxicology 8:485–507
   PubMed Web of Science ®Google Scholar
• 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 Vitro 26:799–806
   PubMed Web of Science ®Google Scholar
• Wright GL, Maroulakou IG, Eldridge J, Liby TL, Sridharan V, Tsichlis PN, Muise-Helmericks RC. 2008. Vegf stimulation of mitochondrial biogenesis: requirement of akt3 kinase. FASEB 22:3264–75
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Horiba M, Buescher JL, Huang D, Gendelman HE, Ransohoff RM, Ikezu T. 2005. Overexpression of monocyte chemotactic protein-1/ccl2 in β-amyloid precursor protein transgenic mice show accelerated diffuse β-amyloid deposition. Am J Pathol 166:1475–85
   Google Scholar