Cell permeability, migration, and reactive oxygen species induced by multiwalled carbon nanotubes in human microvascular endothelial cells

Journal of Toxicology and Environmental Health - Part A: Current Issues

Volumn 75, Issue 3, 2012, Pages 129-147

  Pacurari, M ^a   Qian, Y ^b   Fu, W ^a   Schwegler Berry, D ^b   Ding, M ^b   Castranova, V ^a,b   Guo, N L ^a,c  

^a WEST VIRGINIA UNIVERSITY   (United States)

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

^c WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; MULTI WALLED NANOTUBE; REACTIVE OXYGEN METABOLITE;

ACTIN FILAMENT; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL PERMEABILIZATION; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG TARGETING; HUMAN; HUMAN CELL; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL;

ACTIN CYTOSKELETON; CELL MEMBRANE PERMEABILITY; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CCL2; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; NANOTUBES, CARBON; REACTIVE OXYGEN SPECIES;

ANIMALIA;

EID: 84856818978     PISSN: 15287394     EISSN: 10872620     Source Type: Journal    
DOI: 10.1080/15287394.2012.625549     Document Type: Article

References (67)

1. Aghajanian, A., Wittchen, E. S., Allingham, M. J., Garrett, T. A., and, Burridge, K. 2008. Endothelial cell junctions and the regulation of vascular permeability and leukocyte transmigration. J. Thromb. Haemost., 6: 1453-60.
2. Aiso, S., Yamazaki, K., Umeda, Y., Asakura, M., Kasai, T., Takaya, M., Toya, T., Koda, S., Nagano, K., Arito, H., and, Fukushima, S. 2010. Pulmonary toxicity of intratracheally instilled multiwall carbon nanotubes in male Fischer 344 rats. Ind. Health, 48: 783-95.
3. Aiso, S., Kubota, H., Umeda, Y., Kasai, T., Takaya, M., Yamazaki, K., Nagano, K., Sakai, T., Koda, S., and, Fukushima, S. 2011. Translocation of intratracheally instilled multiwall carbon nanotubes to lung-associated lymph nodes in rats. Ind. Health, 49: 215-20.
4. Apopa, P. L., Qian, Y., Shao, R., Guo, N. L., Schwegler-Berry, D., Pacurari, M., Porter, D., Shi, X., Vallyathan, V., Castranova, V., and, Flynn, D. C. 2009. Iron oxide nanoparticles induce human microvascular endothelial cell permeability through reactive oxygen species production and microtubule remodeling. Part. Fibre Toxicol., 6: 1
5. Asakura, M., Sasaki, T., Sugiyama, T., Takaya, M., Koda, S., Nagano, K., Arito, H., and, Fukushima, S. 2010. Genotoxicity and cytotoxicity of multi-wall carbon nanotubes in cultured Chinese hamster lung cells in comparison with chrysotile A fibers. J. Occup. Health, 52: 155-66.
6. Aschberger, K., Johnston, H. J., Stone, V., Aitken, R. J., Hankin, S. M., Peters, S. A., Tran, C. L., and, Christensen, F. M. 2010. Review of carbon nanotubes toxicity and exposure-Appraisal of human health risk assessment based on open literature. Crit. Rev. Toxicol., 40: 759-90.
7. Banerjee, A. K., Weiner, B. B., Fairhurst, D., and, Tscharnuter, W. W. 1996. Light scattering for measuring electrophoretic mobility in concentrated colloidal suspensions. Abstr. Am. Chem. Soc., 212: 42
8. Barchowsky, A., Lannon, B. M., Elmore, L. C., and, Treadwell, M. D. 1997. Increased focal adhesion kinase-and urokinase-type plasminogen activator receptor-associated cell signaling in endothelial cells exposed to asbestos. Environ. Health Perspect., 105 (suppl. 5): 1131-37.
9. Barchowsky, A., Roussel, R. R., Krieser, R. J., Mossman, B. T., and, Treadwell, M. D. 1998. Expression and activity of urokinase and its receptor in endothelial and pulmonary epithelial cells exposed to asbestos. Toxicol. Appl. Pharmacol., 152: 388-96. (Pubitemid 28492280)
10. Bianco, A., Kostarelos, K., Partidos, C.D., and, Prato, M. 2005. Biomedical applications of functionalised carbon nanotubes. Chem. Commun., 5: 571-77. (Pubitemid 40299037)
11. Branchaud, R. M., MacDonald, J. L., and, Kane, A. B. 1989. Induction of angiogenesis by intraperitoneal injection of asbestos fibers. FASEB J., 3: 1747-52. (Pubitemid 19104829)
12. Burke, A., Ding, X., Singh, R., Kraft, R.A., Levi-Polyachenko, N., Rylander, M. N., Szot, C., Buchanan, C., Whitney, J., Fisher, J., Hatcher, H. C., D'Agostino, R. Jr., Kock, N. D., Ajayan, P. M., Carroll, D. L., Akman, S., Torti, F. M., and, Torti, S. V. 2009. Long-term survival following a single treatment of kidney tumors with multiwalled carbon nanotubes and near-infrared radiation. Proc. Natl. Acad. Sci. USA, 106: 12897-902.
13. Chen, L. M., Kuo, C. H., Lai, T. Y., Lin, Y. M., Su, C. C., Hsu, H. H., Tsai, F. J., Tsai, C. H., Huang, C. Y., and, Tang, C. H. 2011. RANKL increases migration of human lung cancer cells through intercellular adhesion molecule-1 up-regulation. J. Cell. Biochem., 112: 933-41.
14. Christenson, E. M., Anseth, K. S., van den Beucken, J. J., Chan, C. K., Ercan, B., Jansen, J. A., Laurencin, C. T., Li, W. J., Murugan, R., Nair, L. S., Ramakrishna, S., Tuan, R. S., Webster, T. J., and, Mikos, A. G. 2007. Nanobiomaterial applications in orthopedics. J. Orthop. Res., 25: 11-22. (Pubitemid 46070727)
15. Davis, J. M., Addison, J., Bolton, R. E., Donaldson, K., Jones, A. D., and, Smith, T. 1986. The pathogenicity of long versus short fibre samples of amosite asbestos administered to rats by inhalation and intraperitoneal injection. Br. J. Exp. Pathol., 67: 415-30. (Pubitemid 16059890)
16. Davis, J. M., and, Jones, A. D. 1988. Comparisons of the pathogenicity of long and short fibres of chrysotile asbestos in rats. Br. J. Exp. Pathol., 69: 717-37.
17. Deng, X., Jia, G., Wang, H., Sun, H., Wang, X., Yang, S., Wang, T., and, Liu, Y. 2007. Translocation and fate of multi-walled carbon nanotubes in vivo. Carbon, 45: 1419-24. (Pubitemid 46829028)
18. Ding, L., Stilwell, J., Zhang, T., Elboudwarej, O., Jiang, H., Selegue, J. P., Cooke, P. A., Gray, J. W., and, Chen, F. F. 2005. Molecular characterization of the cytotoxic mechanism of multiwall carbon nanotubes and nano-onions on human skin fibroblast. Nano Lett., 5: 2448-64. (Pubitemid 43090840)
19. Donaldson, K., Aitken, R., Tran, L., Stone, V., Duffin, R., Forrest, G., and, Alexander, A. 2006. Carbon nanotubes: A review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol. Sci., 92: 5-22. (Pubitemid 43985785)
20. Dudek, S. M., and, Garcia, J. G. 2001. Cytoskeletal regulation of pulmonary vascular permeability. J. Appl. Physiol., 91: 1487-500. (Pubitemid 32900340)
21. Fang, J., Nakamura, H., and, Maeda, H. 2011. The EPR effect: Unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev., 63: 136-51.
22. Garcia, J. G., Dodson, R. F., and, Callahan, K. S. 1989. Effect of environmental particulates on cultured human and bovine endothelium. Cellular injury via an oxidant-dependent pathway. Lab. Invest., 61: 53-61. (Pubitemid 19203853)
23. Gerszten, R. E., Garcia-Zepeda, E. A., Lim, Y. C., Yoshida, M., Ding, H. A., Gimbrone, M. A. Jr., Luster, A. D., Luscinskas, F. W., and, Rosenzweig, A. 1999. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature, 398: 718-23.
24. Gotlieb, A. I. 1990. The endothelial cytoskeleton: Organization in normal and regenerating endothelium. Toxicol. Pathol., 18: 603-17.
25. Guo, J., Zhang, X., Li, Q., and, Li, W. 2007. Biodistribution of functionalized multiwall carbon nanotubes in mice. Nucl. Med. Biol., 34: 579-83. (Pubitemid 46963011)
26. Gwinn, M. R., and, Vallyathan, V. 2006. Nanoparticles: Health effects-Pros and cons. Environ. Health Perspect., 114: 1818-25.
27. Hamilton, J. A. 1983. Asbestos fibers, plasma and inflammation. Environ. Health Perspect., 51: 281-85. (Pubitemid 14240832)
28. Hassoun, P. M., Mouthon, L., Barbera, J. A., Eddahibi, S., Flores, S.C., Grimminger, F., Jones, P. L., Maitland, M. L., Michelakis, E. D., Morrell, N. W., Newman, J. H., Rabinovitch, M., Schermuly, R., Stenmark, K. R., Voelkel, N. F., Yuan, J. X., and, Humbert, M. 2009. Inflammation, growth factors, and pulmonary vascular remodeling. J. Am. Coll. Cardiol., 54: S10-S19.
29. Hirata, E., Uo, M., Takita, H., Akasaka, T., Watari, F., and, Yokoyama, A. 2009. Development of a 3D collagen scaffold coated with multiwalled carbon nanotubes. J. Biomed. Mater. Res. B Appl. Biomater., 90: 629-34.
30. Houle, F., and, Huot, J. 2006. Dysregulation of the endothelial cellular response to oxidative stress in cancer. Mol. Carcinogen., 45: 362-67. (Pubitemid 43865842)
31. Iijima, S. 1991. Helical microtubules of graphitic carbon. Nature, 354: 56-58. (Pubitemid 21896780)
32. Jin, H., Heller, D. A., and, Strano, M. S. 2008. Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells. Nano Lett., 8: 1577-85.
33. Johnston, H. J., Hutchison, G. R., Christensen, F. M., Peters, S., Hankin, S., Aschberger, K., and, Stone, V. 2010. A critical review of the biological mechanisms underlying the in vivo and in vitro toxicity of carbon nanotubes: The contribution of physico-chemical characteristics. Nanotoxicology, 4: 207-46.
34. Kane, A. B. 1996. Mechanisms of mineral fibre carcinogenesis. IARC Sci. Publ., 140: 11-34.
35. Kane, A. B., and, Hurt, R. H. 2008. Nanotoxicology: The asbestos analogy revisited. Nat. Nanotechnol., 3: 378-79. (Pubitemid 351948250)
36. Kis, A., and, Zettl, A. 2008. Nanomechanics of carbon nanotubes. Philos. Trans. A Math. Phys. Eng. Sci., 366: 1591-611. (Pubitemid 351445688)
37. Kostarelos, K., Bianco, A., and, Prato, M. 2009. Promises, facts and challenges for carbon nanotubes in imaging and therapeutics. Nat. Nanotechnol., 4: 627-33.
38. Lacerda, L., Soundararajan, A., Singh, R., Pastorin, G., Al-Jamal, K. T., Turton, J., Frederik, P., Herrero, M. A., Bao, S. L. A., Emfietzoglou, D., Mather, S., Phillips, W. T., Prato, M., Bianco, A., Goins, B., and, Kostarelos, K. 2008. Dynamic Imaging of functionalized multi-walled carbon nanotube systemic circulation and urinary excretion. Adv. Mater., 20: 225-30. (Pubitemid 351205693)
39. Lee, J. S. Y., and, Gotlieb, A. I. 2003. Understanding the role of the cytoskeleton in the complex regulation of the endothelial repair. Histol. Histopathol., 18: 879-87. (Pubitemid 36773232)
40. Li, X., Gao, H., Uo, M., Sato, Y., Akasaka, T., Abe, S., Feng, Q., Cui, F., and, Watari, F. 2009. Maturation of osteoblast-like SaoS2 induced by carbon nanotubes. Biomed. Mater., 4: 015005
41. Lum, H., and, Roebuck, K. A. 2001. Oxidant stress and endothelial cell dysfunction. Am. J. Physiol. Cell Physiol., 280: C719-41.
42. Mehta, D., and, Malik, A. B. 2006. Signaling mechanisms regulating endothelial permeability. Physiol. Rev., 86: 279-367.
43. Misra, S. K., Ansari, T., Mohn, D., Valappil, S. P., Brunner, T. J., Stark, W. J., Roy, I., Knowles, J. C., Sibbons, P. D., Jones, E. V., Boccaccini, A. R., and, Salih, V. 2010. Effect of nanoparticulate bioactive glass particles on bioactivity and cytocompatibility of poly(3-hydroxybutyrate) composites. J. R. Soc. Interface, 7: 453-65.
44. Monteiro-Riviere, N. A., Nemanich, R. J., Inman, A. O., Wang, Y. Y., and, Riviere, J. E. 2005. Multi-walled carbon nanotube interactions with human epidermal keratinocytes. Toxicol. Lett., 155: 377-84. (Pubitemid 40093001)
45. Nel, A., Xia, T., Madler, L., and, Li, N. 2006. Toxic potential of materials at the nanolevel. Science, 311: 622-27. (Pubitemid 43191298)
46. Pacurari, M., Castranova, V., and, Vallyathan, V. 2010. Single-and multi-wall carbon nanotubes versus asbestos: Are the carbon nanotubes a new health risk to humans?. J. Toxicol. Environ. Health A, 73: 378-95.
47. Pantarotto, D., Briand, J. P., Prato, M., and, Bianco, A. 2004. Translocation of bioactive peptides across cell membranes by carbon nanotubes. Chem. Commun., 1: 16-17. (Pubitemid 38121939)
48. Patlolla, A., Knighten, B., and, Tchounwou, P. 2010. Multi-walled carbon nanotubes induce cytotoxicity, genotoxicity and apoptosis in normal human dermal fibroblast cells. Ethnicity Dis., 20 (S1): 65-72.
49. Podesta, J. E., Al-Jamal, K. T., Herrero, M. A., Tian, B., Ali-Boucetta, H., Hegde, V., Bianco, A., Prato, M., and, Kostarelos, K. 2009. Antitumor activity and prolonged survival by carbon-nanotube-mediated therapeutic siRNA silencing in a human lung xenograft model. Small, 5: 1176-85.
50. Poland, C. A., Duffin, R., Kinloch, I., Maynard, A., Wallace, W. A., Seaton, A., Stone, V., Brown, S., Macnee, W., and, Donaldson, K. 2008. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat. Nanotechnol., 3: 423-28.
51. Porter, D., Sriram, K., Wolfarth, M., Jefferson, A., Schwegler-Berry, D., Andrew, M., and, Castranova, V. 2008. A biocompatible medium for nanoparticle dispersion. Nanotoxicology, 2: 144-54.
52. Porter, D. W., Hubbs, A. F., Mercer, R. R., Wu, N., Wolfarth, M. G., Sriram, K., Leonard, S., Battelli, L., Schwegler-Berry, D., Friend, S., Andrew, M., Chen, B. T., Tsuruoka, S., Endo, M., and, Castranova, V. 2010. Mouse pulmonary dose-and time course-responses induced by exposure to multi-walled carbon nanotubes. Toxicology, 269: 136-47.
53. Qian, Y., Ducatman, A., Ward, R., Leonard, S., Bukowski, V., Lan Guo, N., Shi, X., Vallyathan, V., and, Castranova, V. 2010. Perfluorooctane sulfonate (PFOS) induces reactive oxygen species (ROS) production in human microvascular endothelial cells: Role in endothelial permeability. J. Toxicol. Environ. Health A, 73: 819-36.
54. Qian, Y., Liu, K. J., Chen, Y., Flynn, D. C., Castranova, V., and, Shi, X. 2005. Cdc42 regulates arsenic-induced NADPH oxidase activation and cell migration through actin filament reorganization. J. Biol. Chem., 280: 3875-84. (Pubitemid 40223857)
55. Raffa, V., Vittorio, O., Ciofani, G., Pensabene, V., and, Cuschieri, A. 2009. Cell creeping and controlled migration by magnetic carbon nanotubes. Nanoscale Res. Lett., 5: 257-62.
56. Ruggiero, A., Villa, C.H., Bander, E., Rey, D. A., Bergkvist, M., Batt, C. A., Manova-Todorova, K., Deen, W. M., Scheinberg, D. A., and, McDevitt, M. R. 2010a. Paradoxical glomerular filtration of carbon nanotubes. Proc. Natl. Acad. Sci. USA, 107: 12369-74.
57. Ruggiero, A., Villa, C. H., Holland, J. P., Sprinkle, S. R., May, C., Lewis, J. S., Scheinberg, D. A., and, McDevitt, M. R. 2010b. Imaging and treating tumor vasculature with targeted radiolabeled carbon nanotubes. Int. J. Nanomed., 5: 783-802.
58. Shao, R., and, Guo, X. 2004. Human microvascular endothelial cells immortalized with human telomerase catalytic protein: A model for the study of in vitro angiogenesis. Biochem. Biophys. Res. Commun., 321: 788-94. (Pubitemid 39044379)
59. Shasby, D. M., Shasby, S. S., Sullivan, J. M., and, Peach, M. J. 1982. Role of endothelial cell cytoskeleton in control of endothelial permeability. Circ. Res., 51: 657-61. (Pubitemid 13236152)
60. Singh, R., Pantarotto, D., Lacerda, L., Pastorin, G., Klumpp, C., Prato, M., Bianco, A., and, Kostarelos, K. 2006. Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. Proc. Natl. Acad. Sci. USA, 103: 3357-62. (Pubitemid 43346474)
61. Strieter, R. M., and, Mehrad, B. 2009. New mechanisms of pulmonary fibrosis. Chest, 136: 1364-70.
62. Takagi, A., Hirose, A., Nishimura, T., Fukumori, N., Ogata, A., Ohashi, N., Kitajima, S., and, Kanno, J. 2008. Induction of mesothelioma in p53+/mouse by intraperitoneal application of multi-wall carbon nanotube. J. Toxicol. Sci., 33: 105-16. (Pubitemid 351340768)
63. Wallace, W. A., Fitch, P. M., Simpson, A. J., and, Howie, S. E. 2007. Inflammation-associated remodelling and fibrosis in the lung-A process and an end point. Int. J. Exp. Pathol., 88: 103-10. (Pubitemid 46570076)
64. Wang, W., Watari, F., Omori, M., Liao, S., Zhu, Y., Yokoyama, A., Uo, M., Kimura, H., and, Ohkubo, A. 2007. Mechanical properties and biological behavior of carbon nanotube/polycarbosilane composites for implant materials. J. Biomed. Mater. Res. B Appl. Biomater., 82: 223-30. (Pubitemid 47015372)
65. Wang, X., Xia, T., Ntim, S. A., Ji, Z., George, S., Meng, H., Zhang, H., Castranova, V., Mitra, S., and, Nel, A. E. 2010. Quantitative techniques for assessing and controlling the dispersion and biological effects of multiwalled carbon nanotubes in mammalian tissue culture cells. ACS Nano, 4: 7241-52.
66. Weber, K. S., Nelson, P. J., Grone, H. J., and, Weber, C. 1999. Expression of CCR2 by endothelial cells: Implications for MCP-1 mediated wound injury repair and In vivo inflammatory activation of endothelium. Arterioscler. Thromb. Vasc. Biol., 19: 2085-93. (Pubitemid 29422239)
67. Yadav, S. K., Bera, T., Saxena, P. S., Maurya, A. K., Garbyal, R. S., Vajtai, R., Ramachandrarao, P., and, Srivastava, A. 2010. MWCNTs as reinforcing agent to the hap-gel nanocomposite for artificial bone grafting. J. Biomed. Mater. Res. A, 93: 886-96.