Cytotoxicity of single-walled carbon nanotubes on human hepatoma HepG2 cells: An iTRAQ-coupled 2D LC-MS/MS proteome analysis

Toxicology in Vitro

Volumn 25, Issue 8, 2011, Pages 1820-1827

  Yuan, Jifeng ^a   Gao, Hongcai ^a   Sui, Jianjun ^a   Chen, Wei Ning ^a   Ching, Chi Bun ^a  

^a Nanyang Technological University   (Singapore)

Author keywords

Apoptosis; Cellular response; Cytotoxicity; Oxidative stress; Proteome analysis; Single walled carbon nanotubes

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; HEAT SHOCK PROTEIN; SINGLE WALLED NANOTUBE;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CELL GROWTH; CELL METABOLISM; CELL STRAIN HEPG2; CONTROLLED STUDY; CYTOSKELETON; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; ISOBARIC TAGGED RELATIVE AND ABSOLUTE QUANTITATE; LIQUID CHROMATOGRAPHY; LIVER CELL CARCINOMA; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; SIGNAL TRANSDUCTION;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOTOXINS; HEP G2 CELLS; HUMANS; NANOTUBES, CARBON; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY;

MAMMALIA;

EID: 82655173771     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2011.09.022     Document Type: Article

References (48)

1. Benz J., Hofmann A. Annexins: from structure to function. Biological Chemistry 1997, 378:177-183.
2. Cathcart H., Quinn S., Nicolosi V., Kelly J.M., Blau W.J., Coleman J.N. Spontaneous debundling of single-walled carbon nanotubes in DNA-based dispersions. Journal of Physical Chemistry C 2007, 111:66-74.
3. Chakravarty P., Marches R., Zimmerman N.S., Swafford A.D.E., Bajaj P., Musselman I.H., Pantano P., Draper R.K., Vitetta E.S. Thermal ablation of tumor cells with antibody-functionalized single-walled carbon nanotubes. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:8697-8702.
4. Cheng C., Müller K.H., Koziol K.K.K., Skepper J.N., Midgley P.A., Welland M.E., Porter A.E. Toxicity and imaging of multi-walled carbon nanotubes in human macrophage cells. Biomaterials 2009, 30:4152-4160.
5. Chin D., Means A.R. Calmodulin: a prototypical calcium sensor. Trends in Cell Biology 2000, 10:322-328.
6. Cho S.G., Lee Y.H., Park H.S., Ryoo K., Kang K.W., Park J., Eom S.J., Kim M.J., Chang T.S., Choi S.Y., Shim J., Kim Y., Dong M.S., Lee M.J., Kim S.G., Ichijo H., Choi E.J. Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. Journal of Biological Chemistry 2001, 276:12749-12755.
7. Chou C.C., Hsiao H.Y., Hong Q.S., Chen C.H., Peng Y.W., Chen H.W., Yang P.C. Single-walled carbon nanotubes can induce pulmonary injury in mouse model. Nano Letters 2008, 8:437-445.
8. Crabos M., Yamakado T., Heizmann C.W., Cerletti N., Buhler F.R., Erne P. The calcium binding protein tropomyosin in human platelets and cardiac tissue: elevation in hypertensive cardiac hypertrophy. European Journal of Clinical Investigation 1991, 21:472-478.
9. Craig R., Larkin A., Mingo A.M., Thuerauf D.J., Andrews C., McDonough P.M., Glembotski C.C. P38 MAPK and NF-κB collaborate to induce Interleukin-6 Gene expression and release: evidence for a cytoprotective Autocrine signaling pathway in a cardiac myocyte model system. Journal of Biological Chemistry 2000, 275:23814-23824.
10. Ding L., Stilwell J., Zhang T., Elboudwarej O., Jiang H., Selegue J.P., Cooke P.A., Gray J.W., Chen F.F. Molecular characterization of the cytotoxic mechanism of multiwall carbon nanotubes and nano-onions on human skin fibroblast. Nano Letters 2005, 5:2448-2464.
11. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. International Journal of Biochemistry and Cell Biology 2001, 33:637-668.
12. Donato R. Intracellular and extracellular roles of S100 proteins. Microscopy Research and Technique 2003, 60:540-551.
13. Edri E., Regev O. "Shaken, not stable": dispersion mechanism and dynamics of protein-dispersed nanotubes studied via spectroscopy. Langmuir 2009, 25:10459-10465.
14. Fath K.R., Mamajiwalla S.N., Burgess D.R. The cytoskeleton in development of epithelial cell polarity. Journal of Cell Science 1993, 106:65-73.
15. Gary R., Bretscher A. Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Molecular Biology of the Cell 1995, 6:1061-1075.
16. Gigliotti B., Sakizzie B., Bethune D.S., Shelby R.M., Cha J.N. Sequence-independent helical wrapping of single-walled carbon nanotubes by long genomic DNA. Nano Letters 2006, 6:159-164.
17. Gruber C.W., Čemažar M., Heras B., Martin J.L., Craik D.J. Protein disulfide isomerase: the structure of oxidative folding. Trends in Biochemical Sciences 2006, 31:455-464.
18. Herrmann H., Bär H., Kreplak L., Strelkov S.V., Aebi U. Intermediate filaments: from cell architecture to nanomechanics. Nature Reviews Molecular Cell Biology 2007, 8:562-573.
19. Kavanagh K.L., Guo K., Dunford J.E., Wu X., Knapp S., Ebetino F.H., Rogers M.J., Russell R.G.G., Oppermann U. The molecular mechanism of nitrogen-containing bisphosphonates as antiosteoporosis drugs. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:7829-7834.
20. Khan A.P., Poisson L.M., Bhat V.B., Fermin D., Zhao R., Kalyana-Sundaram S., Michailidis G., Nesvizhskii A.I., Omenn G.S., Chinnaiyan A.M., Sreekumar A. Quantitative proteomic profiling of prostate cancer reveals a role for miR-128 in prostate cancer. Molecular and Cellular Proteomics 2010, 9:298-312.
21. Kornberg R.D. Chromatin structure: a repeating unit of histones and DNA. Science 1974, 184:868-871.
22. Laohavisit A., Davies J.M. Annexins. New Phytologist 2011, 189:40-53.
23. Liao J., Omary M.B. 14-3-3 proteins associate with phosphorylated simple epithelial keratins during cell cycle progression and act as a solubility cofactor. Journal of Cell Biology 1996, 133:345-357.
24. Liu Z., Chen K., Davis C., Sherlock S., Cao Q., Chen X., Dai H. Drug delivery with carbon nanotubes for in vivo cancer treatment. Cancer Research 2008, 68:6652-6660.
25. Liu Z., Tabakman S., Welsher K., Dai H. Carbon nanotubes in biology and medicine: in vitro and in vivo detection, imaging and drug delivery. Nano Research 2009, 2:85-120.
26. Mahoney N.M., Janmey P.A., Almo S.C. Structure of the profilin-poly-L-proline complex involved in morphogenesis and cytoskeletal regulation. Nature Structural Biology 1997, 4:953-960.
27. Manna S.K., Sarkar S., Barr J., Wise K., Barrera E.V., Jejelowo O., Rice-Ficht A.C., Ramesh G.T. Single-walled carbon nanotube induces oxidative stress and activates nuclear transcription factor-κB in human keratinocytes. Nano Letters 2005, 5:1676-1684.
28. Monteiro-Riviere N.A., Nemanich R.J., Inman A.O., Wang Y.Y., Riviere J.E. Multi-walled carbon nanotube interactions with human epidermal keratinocytes. Toxicology Letters 2005, 155:377-384.
29. Mu Q., Li Z., Li X., Mishra S.R., Zhang B., Si Z., Yang L., Jiang W., Yan B. Characterization of Protein Clusters of Diverse Magnetic Nanoparticles and Their Dynamic Interactions with Human Cells. Journal of Physical Chemistry C 2009, 113:5390-5395.
30. Nordberg J., Arnér E.S.J. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radical Biology and Medicine 2001, 31:1287-1312.
31. Patskovsky Y.V., Patskovska L.N., Listowsky I. An asparagine-phenylalanine substitution accounts for catalytic differences between hGSTM3-3 and other human class Mu glutathione S-transferases. Biochemistry 1999, 38:16187-16194.
32. Petrash J.M. All in the family: aldose reductase and closely related aldo-keto reductases. Cellular and Molecular Life Sciences 2004, 61:737-749.
33. Porter A.E., Gass M., Bendall J.S., Muller K., Goode A., Skepper J.N., Midgley P.A., Welland M. Uptake of noncytotoxic acid-treated single-walled carbon nanotubes into the cytoplasm of human macrophage cells. ACS Nano 2009, 3:1485-1492.
34. Rajagopalan S., Xu Y., Brenner M.B. Retention of unassembled components of integral membrane proteins by calnexin. Science 1994, 263:387-390.
35. Ross P.L., Huang Y.N., Marchese J.N., Williamson B., Parker K., Hattan S., Khainovski N., Pillai S., Dey S., Daniels S., Purkayastha S., Juhasz P., Martin S., Bartlet-Jones M., He F., Jacobson A., Pappin D.J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Molecular and Cellular Proteomics 2004, 3:1154-1169.
36. Schiessel H. The physics of chromatin. Journal of Physics Condensed Matter 2003, 15:R699-R774.
37. Schlesinger M.J. Heat shock proteins. Journal of Biological Chemistry 1990, 265:12111-12114.
38. Sue G.R., Ho Z.C., Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radical Biology and Medicine 2005, 38:1543-1552.
39. Sui J., Tuan L.T., Zhang J., Chi B.C., Wei N.C. ITRAQ-coupled 2D LC-MS/MS analysis on protein profile in vascular smooth muscle cells incubated with S- and R-enantiomers of propranolol: possible role of metabolic enzymes involved in cellular anabolism and antioxidant activity. Journal of Proteome Research 2007, 6:1643-1651.
40. Wang L., Srinivasan S., Theiss A.L., Merlin D., Sitaraman S.V. Interleukin-6 induces keratin expression in intestinal epithelial cells: potential role of keratin-8 in interleukin-6-induced barrier function alterations. Journal of Biological Chemistry 2007, 282:8219-8227.
41. Wang X., Hinson E.R., Cresswell P. The Interferon-Inducible Protein Viperin Inhibits Influenza Virus Release by Perturbing Lipid Rafts. Cell Host and Microbe 2007, 2:96-105.
42. Xu J., Khiam A.K., Sui J., Zhang J., Tuan L.T., Wei N.C. Comparative proteomics profile of osteoblasts cultured on dissimilar hydroxyapatite biomaterials: an iTRAQ-coupled 2-D LC-MS/MS analysis. Proteomics 2008, 8:4249-4258.
43. Ye S., Zhang H., Wang Y., Jiao F., Lin C., Zhang Q. Carboxylated single-walled carbon nanotubes induce an inflammatory response in human primary monocytes through oxidative stress and NF-κB activation. Journal of Nanoparticle Research 2011, 1:14.
44. Yonemura S., Hirao M., Doi Y., Takahashi N., Kondo T., Tsukita S. Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. Journal of Cell Biology 1998, 140:885-895.
45. Zhang T., Stilwell J.L., Gerion D., Ding L., Elboudwarej O., Cooke P.A., Gray J.W., Alivisatos A.P., Chen F.F. Cellular effect of high doses of silica-coated quantum dot profiled with high throughput gene expression analysis and high content cellomics measurements. Nano Letters 2006, 6:800-808.
46. Zhao W., Gao Y., Brook M.A., Li Y. Wrapping single-walled carbon nanotubes with long single-stranded DNA molecules produced by rolling circle amplification. Chemical Communications 2006, 3582:3584.
47. Zhou H., Mu Q., Gao N., Liu A., Xing Y., Gao S., Zhang Q., Qu G., Chen Y., Liu G., Zhang B., Yan B. A nano-combinatorial library strategy for the discovery of nanotubes with reduced protein-binding, cytotoxicity, and immune response. Nano Letters 2008, 8:859-865.
48. Zimmer D.B., Cornwall E.H., Landar A., Song W. The S100 protein family: history, function, and expression. Brain Research Bulletin 1995, 37:417-429.