journal article·2010-05Open access

Carbon nanotubes degraded by neutrophil myeloperoxidase induce less pulmonary inflammation

Valerian E. Kagan, Nagarjun V. Konduru, Weihong Feng, Brett L. Allen, Jennifer Conroy, Yuri Volkov, Irina I. Vlasova, Natalia A. Belikova, Naveena Yanamala, Alexander Kapralov, Yulia Y. Tyurina, Jingwen Shi, Elena R. Kisin, Ashley R. Murray, Jonathan Franks, Donna Stolz, Pingping Gou, Judith Klein-Seetharaman, Bengt Fadeel, Alexander Star, Anna A. Shvedova

Nature Nanotechnology· Volume 5· Issue 5

Abstract

We have shown previously that single-walled carbon nanotubes can be catalytically biodegraded over several weeks by the plant-derived enzyme, horseradish peroxidase. However, whether peroxidase intermediates generated inside human cells or biofluids are involved in the biodegradation of carbon nanotubes has not been explored. Here, we show that hypochlorite and reactive radical intermediates of the human neutrophil enzyme myeloperoxidase catalyse the biodegradation of single-walled carbon nanotubes in vitro, in neutrophils and to a lesser degree in macrophages. Molecular modelling suggests that interactions of basic amino acids of the enzyme with the carboxyls on the carbon nanotubes position the nanotubes near the catalytic site. Importantly, the biodegraded nanotubes do not generate an inflammatory response when aspirated into the lungs of mice. Our findings suggest that the extent to which carbon nanotubes are biodegraded may be a major determinant of the scale and severity of the associated inflammatory responses in exposed individuals.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Nanoparticles: synthesis and applications · Medical and Biological Ozone Research · Heavy Metal Exposure and Toxicity

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (30)

Show source-provided references
1. Allen, B. L. et al. Biodegradation of single-walled carbon nanotubes through enzymatic catalysis. Nano Lett. 8, 3899–3903 (2008).10.1021/nl802315h ↗
2. Maynard, A. D. et al. Safe handling of nanotechnology. Nature 444, 267–269 (2006).10.1038/444267a ↗
3. Shvedova, A. A. et al. Mechanisms of pulmonary toxicity and medical applications of carbon nanotubes: two faces of Janus? Pharmacol. Ther. 121, 192–204 (2009).10.1016/j.pharmthera.2008.10.009 ↗
4. Jia, G. et al. Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube and fullerene. Environ. Sci. Technol. 39, 1378–1383 (2005).10.1021/es048729l ↗
5. Kagan, V. E. et al. Direct and indirect effects of single walled carbon nanotubes on RAW 264.7 macrophages: role of iron. Toxicol. Lett. 165, 88–100 (2006).10.1016/j.toxlet.2006.02.001 ↗
6. Kisin, E. R. et al. Single-walled carbon nanotubes: geno- and cytotoxic effects in lung fibroblast V79 cells. J. Toxicol. Environ. Health. A 70, 2071–2079 (2007).10.1080/15287390701601251 ↗
7. Shvedova, A. A. et al. Unusual inflammatory and fibrogenic pulmonary responses to single-walled carbon nanotubes in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L698–L708 (2005).10.1152/ajplung.00084.2005 ↗
8. Shvedova, A. A. 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. 295, L552–L565 (2008).10.1152/ajplung.90287.2008 ↗
9. Muller, J. et al. Structural defects play a major role in the acute lung toxicity of multiwall carbon nanotubes: toxicological aspects. Chem. Res. Toxicol. 21, 1698–1705 (2008).10.1021/tx800101p ↗
10. Poland, C. A. et al. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nature Nanotech. 3, 423–428 (2008).10.1038/nnano.2008.111 ↗
11. Wei, Z., Kondratenko, M., Dao, L. H. & Perepichka, D. F. Rectifying diodes from asymmetrically functionalized single-wall carbon nanotubes. J. Am. Chem. Soc. 128, 3134–3135 (2006).10.1021/ja053950z ↗
12. Yoon, S. M. et al. Selective oxidation on metallic carbon nanotubes by halogen oxoanions. J. Am. Chem. Soc. 130, 2610–2616 (2008).10.1021/ja077449d ↗
13. Wu, C.-H. Studies of the equilibrium and thermodynamics of the absorption of Cu2+ onto as-produced and modified carbon nanotubes. J. Colloid Interface Sci. 311, 338–346 (2007).10.1016/j.jcis.2007.02.077 ↗
14. Hampton, M. B., Kettle, A. J. & Winterbourn, C. C. Inside the neutrophil phagosome: oxidants, myeloperoxidase and bacterial killing. Blood 92, 3007–3017 (1998).10.1182/blood.V92.9.3007 ↗
15. Sutherland, K., Mahoney, J. R., II, Coury, A. J. & Eaton, J. W. Degradation of biomaterials by phagocyte-derived oxidants. J. Clin. Invest. 92, 2360–2367 (1993).10.1172/JCI116841 ↗
16. Kuznetsova, A. et al. Oxygen-containing functional groups on single-wall carbon nanotubes: NEXAFS and vibrational spectroscopic studies. J. Am. Chem. Soc. 123, 10699–10704 (2001).10.1021/ja011021b ↗
17. Panasenko, O. M. et al. Generation of free radicals during decomposition of hydroperoxide in the presence of myeloperoxidase or activated neutrophils. Biochemistry (Mosc) 70, 998–1004 (2005).10.1007/s10541-005-0215-z ↗
18. Kearns, S. & Dawson, R., Jr. Cytoprotective effect of taurine against hypochlorous acid toxicity to PC12 cells. Adv. Exp. Med. Biol. 483, 563–570 (2000).10.1007/0-306-46838-7_60 ↗
19. Lessig, J. et al. Myeloperoxidase binds to non-vital spermatozoa on phosphatidylserine epitopes. Apoptosis 12, 1803–1812 (2007).10.1007/s10495-007-0113-5 ↗
20. Olivier, M. L. & Paul, R. O. EPR spin-trapping of a myeloperoxidase protein radical. Biochem. Biophys. Res. Commun. 1, 199–202 (2000).
21. Kam, N. & Dai, H. Single walled carbon nantoubes for transport and delivery of biological cargos. Phys. Stat. Sol. 243, 3561–3566 (2006).10.1002/pssb.200669226 ↗
22. Zipfel, M., Carmine, T. C., Gerber, C., Niethammer, D. & Bruchelt, G. Evidence for the activation of myeloperoxidase by f-Meth-Leu-Phe prior to its release from neutrophil granulocytes. Biochem. Biophys. Res. Commun. 232, 209–212 (1997).10.1006/bbrc.1997.6257 ↗
23. McKenzie, S. E. & Schreiber, A. D. Fc gamma receptors in phagocytes. Curr. Opin. Hematol. 5, 16–21 (1998).10.1097/00062752-199801000-00003 ↗
24. Kettle, A. J., Gedye, C. A. & Winterbourn, C. C. Mechanism of inactivation of myeloperoxidase by 4-aminobenzoic acid hydrazide. Biochem. J. 321, 503–508 (1997).10.1042/bj3210503 ↗
25. Touyz, R. M. Apocynin, NADPH oxidase and vascular cells: a complex matter. Hypertension 51, 172–174 (2008).10.1161/HYPERTENSIONAHA.107.103200 ↗
26. Batrakova, E. V. et al. A macrophage–nanozyme delivery system for Parkinson's disease. Bioconjug. Chem. 18, 1498–1506 (2007).10.1021/bc700184b ↗
27. Dou, H. et al. Development of a macrophage-based nanoparticle platform for antiretroviral drug delivery. Blood 108, 2827–2835 (2006).10.1182/blood-2006-03-012534 ↗
28. Konduru, N. V. et al. Phosphatidylserine targets single-walled carbon nanotubes to professional phagocytes in vitro and in vivo. PLoS One 4, e4398 (2009).10.1371/journal.pone.0004398 ↗
29. DeLano, W. L. The PyMOL Molecular Graphics System (DeLano Scientific, 2002).
30. Yanamala, N., Tirupula, K. C. & Klein-Seetharaman, J. Preferential binding of allosteric modulators to active and inactive conformational states of metabotropic glutamate receptors. BMC Bioinformatics 9(Suppl 1), S16 (2008).10.1186/1471-2105-9-S1-S16 ↗