A systems toxicology approach on the mechanism of uptake and toxicity of MWCNT in Caenorhabditis elegans

Chemico-Biological Interactions

Volumn 239, Issue , 2015, Pages 153-163

  Eom, Hyun Jeong ^a   Roca, Carlos P ^b   Roh, Ji Yeon ^a   Chatterjee, Nivedita ^a   Jeong, Jae Seong ^a   Shim, Ilseob ^c   Kim, Hyun Mi ^c   Kim, Phil Je ^c   Choi, Kyunghee ^c   Giralt, Francesc ^b   Choi, Jinhee ^a  

^a University of Seoul   (South Korea)

^b UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^c National Institute of Environmental Research   (South Korea)

Author keywords

Adverse outcome pathway; Caenorhabditis elegans; Multiwall carbon nanotubes; Phagocytosis; Systems toxicology

Indexed keywords

4 AMINOBUTYRATE AMINOTRANSFERASE; ACTIN; ACTIN 2; ACTIN 3; ACTIN 4; ACTIN 5; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE SUBUNIT H28O16 1 PROTEIN; ASPARTIC PROTEINASE; ASPARTYL PROTEASE 1; EUKARYOTIC INITIATION FACTOR 4; EXTRACELLULAR SUPEROXIDE DISMUTASE; GABA TRANSAMINASE 1; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 4; HEAT SHOCK PROTEIN 70; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR; INITIATION FACTOR 2; INITIATION FACTOR 3; MALATE DEHYDROGENASE; MALATE DEHYDROGENASE 1; MAMMALIAN TARGET OF RAPAMYCIN; METHYLTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; MULTI WALLED NANOTUBE; PHOSPHOETHANOLAMINE METHYLTRANSFERASE 2; PROTEIN KINASE B; TRANSCRIPTION FACTOR DAF 16; UNCLASSIFIED DRUG; CARBON NANOTUBE;

ACT 2 GENE; ACT 3 GENE; ACT 4 GENE; ACT 5 GENE; ADULT; ARTICLE; ASP 1 GENE; BIOINFORMATICS; CAENORHABDITIS ELEGANS; CED 10 GENE; CEP 1 GENE; CITRIC ACID CYCLE; CONTROLLED STUDY; CTL 2 GENE; DAF 16 GENE; DOWN REGULATION; DYN 1 GENE; ENDOCYTOSIS; ENDOPLASMIC RETICULUM STRESS; ENZYME SUBUNIT; FATTY ACID METABOLISM; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENOME ANALYSIS; GTA 1 GENE; HSP 4 GENE; HSP 70 GENE; INGESTION; LONG TERM EXPOSURE; MDH 1 GENE; MICROARRAY ANALYSIS; MORTALITY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PHAGOCYTOSIS; PHAGOSOME; PMK 1 GENE; PMT 2 GENE; PROTEIN EXPRESSION; PROTEOMICS; RAB 7 GENE; REPRODUCTION; REPRODUCTIVE TOXICITY; RME 1 GENE; RME 2 GENE; RME 8 GENE; SOD 3 GENE; SYSTEMS TOXICOLOGY; TOXICOLOGY; TRANSCRIPTOMICS; UPREGULATION; XENOBIOTIC METABOLISM; YOUNG ADULT; ANIMAL; DRUG EFFECTS; GENETICS; METABOLISM; MUTATION; PROCEDURES; REPRODUCIBILITY; TOXICITY TESTING;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; ENDOCYTOSIS; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; MICROARRAY ANALYSIS; MUTATION; NANOTUBES, CARBON; OXIDATIVE STRESS; PHAGOCYTOSIS; PROTEOMICS; REPRODUCIBILITY OF RESULTS; TOXICITY TESTS;

EID: 84937622188     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2015.06.031     Document Type: Article

References (75)

1. M.H. Gass, K.K.K. Koziol, A.H. Windle, and P.A. Midgley Four-dimensional spectral tomography of carbonaceous nanocomposites Nano Lett. 6 2006 376 379
2. J.M. Schnorr, and T.M. Swager Emerging applications of carbon nanotubes Chem. Mater. 23 2011 646 657
3. J. Du, S. Wang, H. You, and X. Zhao Understanding the toxicity of carbon nanotubes in the environment is crucial to the control of nanomaterials in producing and processing and the assessment of health risk for human: a review Environ. Toxicol. Pharmacol. 36 2 2013 451 462
4. C. Ma, W. Zhang, Y. Zhu, L. Ji, R. Zhang, N. Koratkar, and J. Liang Alignment and dispersion of functionalized carbon nanotubes in polymer composites induced by an electric field Carbon 46 2008 706 720
5. X. Zhao, and R. Liu Recent progress and perspectives on the toxicity of carbon nanotubes at organism, organ, cell, and biomacromolecule levels Environ. Int. 40 2012 244 255
6. K. Donaldson, F.A. Murphy, R. Duffin, and C.A. Poland 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 2010 5
7. K. Donaldson, C.A. Poland, F.A. Murphy, M. MacFarlane, T. Chernova, and A. Schinwald Pulmonary toxicity of carbon nanotubes and asbestos - similarities and differences Adv. Drug Deliv. Rev. 65 15 2013 2078 2086
8. C.A. Poland, R. Duffin, I. Kinloch, A. Maynard, W.A. Wallace, A. Seaton, V. Stone, S. Brown, W. Macnee, and K. Donaldson Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study Nat. Nanotechnol. 3 7 2008 423 428
9. A.R. Reddy, D.R. Krishna, Y.N. Reddy, and V. Himabindu 6504 Toxicol. Mech. Methods 20 2010 267 272
10. T. Galloway, C. Lewis, I. Dolciotti, B.D. Johnston, J. Moger, and F. Regoli Sublethal toxicity of nano-titanium dioxide and carbon nanotubes in a sediment dwelling marine polychaete Environ. Pollut. 158 5 2010 1748 1755
11. F. Mouchet, P. Landois, P. Puech, E. Pinelli, E. Flahaut, and L. Gauthier Carbon nanotube ecotoxicity in amphibians: assessment of multiwalled carbon nanotubes and comparison with double-walled carbon nanotubes Nanomedicine 5 6 2010 963 974
12. J. Cheng, E. Flahaut, and S.H. Cheng Effect of carbon nanotubes on developing zebrafish embryos Environ. Toxicol. Chem. 26 4 2007 708 716
13. Y. Zhao, Q. Wu, Y. Li, A. Nouara, R. Jia, and D. Wang In vivo translocation and toxicity of multi-walled carbon nanotubes are regulated by microRNAs Nanoscale 6 8 2014 4275 4284
14. R. Klaper, D. Arndt, K. Setyowati, J. Chen, and F. Goetz Functionalization impacts the effects of carbon nanotubes on the immune system of rainbow trout, Oncorhynchus mykiss Aquat Toxicol. 100 2 2010 211 217
15. M.C. Leung, J.V. Goldstone, W.A. Boyd, J.H. Freedman, and J.N. Meyer Caenorhabditis elegans generates biologically relevant levels of genotoxic metabolites from aflatoxin B1 but not benzo[a]pyrene in vivo Toxicol. Sci. 118 2 2010 444 453
16. J. Choi, O.V. Tsyusko, J.M. Unrine, N. Chatterjee, J.M. Ahn, X. Yang, L.B. Thornton, I.T. Ryde, D. Starnes, and J.N. Meyer A micro-sized model for the in vivo studies of nanoparticle toxicity: what has Caenorhabditis elegans taught us? Environ. Chem. 11 3 2014 227 246
17. G.T. Ankley, R.S. Bennett, R.J. Erickson, D.J. Hoff, M.W. Hornung, R.D. Johnson, D.R. Mount, J.W. Nichols, C.L. Russom, P.K. Schmieder, J.A. Serrrano, J.E. Tietge, and D.L. Villeneuve Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment Environ. Toxicol. Chem. 29 3 2010 730 741
18. H.C. Wu, X.L. Chang, L. Liu, F. Zhao, and Y.L. Zhao Chemistry of carbon nanotubes in biomedical applications J. Mater. Chem. 20 2010 1036 1052
19. D. Tasis, N. Tagmatarchis, A. Bianco, and M. Prato Chemistry of carbon nanotubes Chem. Rev. 106 2006 1105 1136
20. S. Vardharajula, S.Z. Ali, P.M. Tiwari, E. Eroʇlu, K. Vig, V.A. Dennis, and S.R. Singh Functionalized carbon nanotubes: biomedical applications Int. J. Nanomed. 7 2012 361 5374
21. K.K. Jain Advances in use of functionalized carbon nanotubes for drug design and discovery Expert Opin. Drug Discov. 7 11 2012 1029 1037
22. J.Y. Roh, S.J. Sim, J. Yi, K. Park, K.H. Chung, D.Y. Ryu, and J. Choi Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics Environ. Sci. Technol. 43 10 2009 3933 3940
23. L. Shi, L.H. Reid, W.D. Jones, R. Shippy, J.A. Warrington, S.C. Baker, P.J. Collins, F. de Longueville, and et al. The microarray quality control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements Nat. Biotechnol. 24 9 2006 1151 1161
24. P.H. Chen, K.M. Hsiao, and C.C. Chou Molecular characterization of toxicity mechanism of single-walled carbon nanotubes Biomaterials 34 2013 5661 5669
25. S. Pillai, R. Behra, H. Nestler, M.J. Suter, L. Sigg, and K. Schirmer Linking toxicity and adaptive responses across the transcriptome, proteome, and phenotype of Chlamydomonas reinhardtii exposed to silver Proc. Natl. Acad. Sci. U.S.A. 111 9 2014 3490 3495
26. J.E. Irazoqui, J.M. Urbach, and F.M. Ausubel Evolution of host innate defence. Insights from Caenorhabditis elegans and primitive invertebrates Nat. Rev. Immunol. 10 2010 47 58
27. X.W. Wang, N.S. Tan, B. Ho, and J.L. Ding Evidence for the ancient origin of the NF-kappaB/IkappaB cascade: its archaic role in pathogen infection and immunity Proc. Natl. Acad. Sci. U.S.A. 103 2006 4204 4209
28. N. Azad, A.K. Iyer, L. Wang, Y. Liu, Y. Lu, and Y. Rojanasakul Reactive oxygen species-mediated p38 MAPK regulates carbon nanotube-induced fibrogenic and angiogenic responses Nanotoxicology 7 2013 157 168
29. W.Y. Hsieh, C.C. Chou, C.C. Ho, S.L. Yu, H.Y. Chen, H.Y. Chou, J.J. Chen, H.W. Chen, and P.C. Yang Single-walled carbon nanotubes induce airway hyper reactivity and parenchymal injury in mice Am. J. Respir. Cell Mol. Biol. 46 2012 257 267
30. Z. Sun, Z. Liu, J. Meng, J. Meng, J. Duan, S. Xie, X. Lu, Z. Zhu, C. Wang, S. Chen, H. Xu, and X.D. Yang Carbon nanotubes enhance cytotoxicity mediated by human lymphocytes in vitro PLoS ONE 6 2011 e21073
31. T. Kaletta, and M.O. Hengartner Finding function in novel targets: C. elegans as a model organism Nat. Rev. Drug Discovery 5 2006 387 398
32. B. Lant, and K.B. Storey An overview of stress response and hypometabolic strategies in Caenorhabditis elegans: conserved and contrasting signals with the mammalian system Int. J. Biol. Sci. 6 2010 9 50
33. U. Taylor, A. Barchanski, S. Petersen, W.A. Kues, U. Baulain, L. Gamrad, L. Sajti, S. Barcikowski, and D. Rath Gold nanoparticles interfere with sperm functionality by membrane adsorption without penetration Nanotoxicology 8 2014 118 127
34. U. Taylor, A. Barchanski, W. Garrels, S. Klein, W. Kues, S. Barcikowski, and D. Rath Toxicity of gold nanoparticles on somatic and reproductive cells Adv. Exp. Med. Biol. 733 2012 125 133
35. D. Tiedemann, U. Taylor, C. Rehbock, J. Jakobi, S. Klein, W.A. Kues, S. Barcikowski, and D. Rath Reprotoxicity of gold, silver, and gold-silver alloy nanoparticles on mammalian gametes Analyst 139 2014 931 942
36. T. Kirkegaard, A.G. Roth, N.H. Petersen, A.K. Mahalka, O.D. Olsen, I. Moilanen, A. Zylicz, J. Knudsen, K. Sandhoff, C. Arenz, P.K. Kinnunen, J. Nylandsted, and M. Jäättelä Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology Nature 463 2010 549 553
37. S.S. Mambula, and S.K. Calderwood Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes J. Immunol. 177 2006 7849 7857
38. B.S. Polla, F. Gabert, B.M. Peyrusse, and M.R. Jacquier-Sarlin Increased proteolysis of diphtheria toxin by human monocytes after heat shock: a subsidiary role for heat-shock protein 70 in antigen processing Immunology 120 2007 230 241
39. P.S. Hegde, I.R. White, and C. Debouck Interplay of transcriptomics and proteomics Curr. Opin. Biotechnol. 14 2003 647 651
40. C. Núñez, A. Esteve-Núñez, C. Giometti, S. Tollaksen, T. Khare, W. Lin, D. Lovley, and R.B.A. Methé DNA microarray and proteomic analyses of the RpoS regulon in Geobacter sulfurreducens J. Bacteriol. 188 2006 2792 2800
41. H. Ali-Boucetta, A. Nunes, R. Sainz, M.A. Herrero, B. Tian, M. Prato, A. Bianco, and K. Kostarelos Asbestos-like pathogenicity of long carbon nanotubes alleviated by chemical functionalization Angew. Chem. Int. Ed. Engl. 52 8 2013 2274 2278
42. K.M. Pondman, M. Sobik, A. Nayak, A.G. Tsolaki, A. Jäkel, E. Flahaut, S. Hampel, B. Ten Haken, R.B. Sim, and U. Kishore Complement activation by carbon nanotubes and its influence on the phagocytosis and cytokine response by macrophages Nanomedicine 10 6 2014 1287 1299
43. R. Li, X. Wang, Z. Ji, B. Sun, H. Zhang, C.H. Chang, S. Lin, H. Meng, Y.P. Liao, M. Wang, Z. Li, A.A. Hwang, T.B. Song, R. Xu, Y. Yang, J.I. Zink, A.E. Nel, and T. Xia Surface charge and cellular processing of covalently functionalized multiwall carbon nanotubes determine pulmonary toxicity ACS Nano 7 2013 2352 2368
44. X. Li, L. Wang, Y. Fan, Q. Feng, and F. Cui Biocompatibility and toxicity of nanoparticles and nanotubes J. Nanomater. 548389 2012 19
45. X. Zhang, Y. Zhu, J. Li, Z. Zhu, J. Li, W. Li, and Q. Huang Tuning the cellular uptake and cytotoxicity of carbon nanotubes by surface hydroxylation J. Nanopart. Res. 13 12 2011 6941 6952
46. Y. Zhao, Q. Wu, Y. Li, and D. Wang Translocation, transfer, and in vivo safety evaluation of engineered nanomaterials in the non-mammalian alternative toxicity assay model of nematode Caenorhabditis elegans RSC Adv. 3 2013 5741
47. A. Albini, V. Mussi, A. Parodi, A. Ventura, E. Principi, S. Tegami, M. Rocchia, E. Francheschi, I. Sogno, R. Cammarota, G. Finzi, F. Sessa, D.M. Noonan, and U. Valbusa Interactions of single-wall carbon nanotubes with endothelial cells Nanomedicine 6 2010 277 288
48. P. Cherukuri, S.M. Bachilo, S.H. Litovsky, and R.B. Weisman Near-infrared fluorescence microscopy of single-walled carbon nanotubes in phagocytic cells J. Am. Chem. Soc. 126 2004 15638 15639
49. H. Jin, D.A. Heller, and M.S. Strano Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells Nano Lett. 8 2008 1577 1585
50. N.W.S. Kam, and H. Dai Carbon nanotubes as intracellular protein transporters: generality and biological functionality J. Am. Chem. Soc. 127 2005 6021 6026
51. N.W.S. Kam, T.C. Jessop, P.A. Wender, and H. Dai Nanotube molecular transporters: internalization of carbon nanotube-protein conjugates into mammalian cells J. Am. Chem. Soc. 126 2004 6850 6851
52. D. Cai, J.M. Mataraza, Z.H. Qin, Z. Huang, J. Huang, T.C. Chiles, D. Carnahan, K. Kempa, and Z. Ren Highly efficient molecular delivery into mammalian cells using carbon nanotube spearing Nat. Methods 2 2005 449 454
53. K. Kostarelos, L. Lacerda, G. Pastorin, W. Wu, S. Wieckowski, J. Luangsivilay, S. Godefroy, D. Pantarotto, J.P. Briand, S. Muller, M. Prato, and A. Bianco Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type Nat. Nanotechnol. 2 2007 108 113
54. X. Wang, Y.C. Wu, V.A. Fadok, M.C. Lee, K. Gengyo-Ando, L.C. Cheng, D. Ledwich, P.K. Hsu, J.Y. Chen, B.K. Chou, P. Henson, S. Mitani, and D. Xue Cell corpse engulfment mediated by C. elegans phosphatidylserine receptor through CED-5 and CED-12 Science 302 2003 1563 1566
55. P.W. Reddien, and H.R. Horvitz CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans Nat. Cell Biol. 2 2000 131 136
56. Y.C. Wu, and H.R. Horvitz C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180 Nature 392 1998 501 504
57. Y.C. Wu, M.C. Tsai, L.C. Cheng, C.J. Chou, and N.Y. Weng C. elegans CED-12 acts in the conserved crkII/DOCK180/Rac pathway to control cell migration and cell corpse engulfment Dev. Cell 1 2001 491 502
58. J.O. Agola, L. Hong, Z. Surviladze, O. Ursu, A. Waller, J.J. Strouse, D.S. Simpson, C.E. Schroeder, T.I. Oprea, J.E. Golden, J. Aubé, T. Buranda, L.A. Sklar, and A. Wandinger-Ness A competitive nucleotide binding inhibitor: in vitro characterization of Rab7 GTPase inhibition ACS Chem. Biol. 7 6 2012 1095 1108
59. S.L. Schwartz, C. Cao, O. Pylypenko, A. Rak, and A. Wandinger-Ness Rab GTPases at a glance J. Cell Sci. 120 Pt 22 2007 3905 3910
60. X. Yu, S. Odera, C.H. Chuang, N. Lu, and Z. Zhou C. elegans dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells Dev. Cell 10 6 2006 743 757
61. X. Yu, N. Lu, and Z. Zhou Phagocytic receptor CED-1 initiates a signaling pathway for degrading engulfed apoptotic cells PLoS Biol. 6 3 2008 e61
62. K. Peynshaert, B.B. Manshian, F. Joris, K. Braeckmans, S.C. De Smedt, J. Demeester, and S.J. Soenen Exploiting intrinsic nanoparticle toxicity: the pros and cons of nanoparticle-induced autophagy in biomedical research Chem. Rev. 114 15 2014 7581 7609
63. B. Grant, Y. Zhang, M.C. Paupard, S.X. Lin, D.H. Hall, and D. Hirsh Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling Nat. Cell Biol. 3 2001 573 579
64. B. Grant, and D. Hirsh Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte Mol. Biol. Cell 10 1999 4311 4326
65. Y. Zhang, B. Grant, and D. Hirsh RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans Mol. Biol. Cell 12 2001 2011 2021
66. B.K. Choi, D.J. Chitwood, and Y.K. Paik Proteomic changes during disturbance of cholesterol metabolism by azacoprostane treatment in Caenorhabditis elegans Mol. Cell. Proteomics 2 2003 1086 1095
67. R. Zhang, M.J. Piao, K.C. Kim, A.D. Kim, J.Y. Choi, J. Choi, and J.W. Hyun Endoplasmic reticulum stress signaling is involved in silver nanoparticles-induced apoptosis Int. J. Biochem. Cell Biol. 44 1 2012 224 232
68. O.V. Tsyusko, J.M. Unrine, D. Spurgeon, E. Blalock, D. Starnes, M. Tseng, G. Joice, and P.M. Bertsch Toxicogenomic responses of the model organism Caenorhabditis elegans to gold nanoparticles Environ. Sci. Technol. 46 2012 4115 4124
69. Z. Kostova, and D.H. Wolf For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection EMBO J. 22 2003 2309 2317
70. C. Koumenis ER stress, hypoxia tolerance and tumor progression Curr. Mol. Med. 6 2006 55 69
71. J. Guo, H.Y. Nie, H.F. Wang, and G. Jia The cytotoxicity and expression changes of endoplasmic reticulum related genes induced by MWCNTs with different surface modifications Beijing Da Xue Xue Bao 43 2011 342 347
72. X. Wang, J. Guo, T. Chen, H. Nie, H. Wang, J. Zang, X. Cui, and G. Jia Multi-walled carbon nanotubes induce apoptosis via mitochondrial pathway and scavenger receptor Toxicol. In Vitro 26 2012 799 806
73. X. He, S.H. Young, D. Schwegler-Berry, W.P. Chisholm, J.E. Fernback, and Q. Ma Multiwalled carbon nanotubes induce a fibrogenic response by stimulating reactive oxygen species production, activating NF-κB signaling, and promoting fibroblast-to-myofibroblast transformation Chem. Res. Toxicol. 24 2011 2237 2248
74. R.K. Srivastava, A.B. Pant, M.P. Kashyap, V. Kumar, M. Lohani, L. Jonas, and Q. Rahman Multi-walled carbon nanotubes induce oxidative stress and apoptosis in human lung cancer cell line-A549 Nanotoxicology 5 2011 195 207
75. S.F. Ye, Y.H. Wu, Z.Q. Hou, and Q.Q. Zhang 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 2009 643 648