Lung macrophages Digest carbon nanotubes using a superoxide/peroxynitrite oxidative pathway

ACS Nano

Volumn 8, Issue 6, 2014, Pages 5610-5621

  Kagan, Valerian E ^a   Kapralov, Alexandr A ^a   St Croix, Claudette M ^a   Watkins, Simon C ^a   Kisin, Elena R ^a   Kotchey, Gregg P ^b   Balasubramanian, Krishnakumar ^a   Vlasova, Irina I ^a,c   Yu, Jaesok ^d   Kim, Kang ^d   Seo, Wanji ^e   Mallampalli, Rama K ^d,f   Star, Alexander ^e   Shvedova, Anna A ^a  

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

^b Department of Environmental and Occupational Health Health Effects Lab Division National Institute for Occupational Safety and Health ^*  (United States)

^c FEDERAL RESEARCH AND CLINICAL CENTER OF PHYSICAL CHEMICAL MEDICINE OF FEDERAL MEDICAL BIOLOGICAL AGENCY   (Russian Federation)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f Acute Lung Injury Center of Excellence   (United States)

Author keywords

biodegradation; lung; peroxynitrite; single walled carbon nanotubes

Indexed keywords

BIODEGRADATION; BIOLOGICAL ORGANS; MICROBIOLOGY; NANOPARTICLES; SINGLE-WALLED CARBON NANOTUBES (SWCN);

ACTIVATED MACROPHAGES; ANIMAL MODEL; BACTERIAL PATHOGENS; CARBONACEOUS NANOPARTICLES; FUNCTIONALIZED; LUNG; OXIDATIVE PATHWAYS; PEROXYNITRITES;

MACROPHAGES;

BIOMATERIAL; CARBON; CARBON NANOTUBE; NITRIC OXIDE; OXYGEN; PEROXYNITROUS ACID; SUPEROXIDE;

ACOUSTICS; ANIMAL; C57BL MOUSE; CHEMISTRY; DRUG EFFECTS; HUMAN; INFLAMMATION; LUNG; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MACROPHAGE; METABOLISM; MOUSE; NANOTECHNOLOGY; NEUTROPHIL; PATHOLOGY; PROCEDURES; RAT;

ACOUSTICS; ANIMALS; BIOCOMPATIBLE MATERIALS; BRONCHOALVEOLAR LAVAGE; CARBON; HUMANS; INFLAMMATION; LUNG; MACROPHAGES; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; NANOTECHNOLOGY; NANOTUBES, CARBON; NEUTROPHILS; NITRIC OXIDE; OXYGEN; PEROXYNITROUS ACID; RATS; SUPEROXIDES;

EID: 84903434034     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn406484b     Document Type: Article

References (50)

1. Sanchez, V. C.; Pietruska, J. R.; Miselis, N. R.; Hurt, R. H.; Kane, A. B. Biopersistence and Potential Adverse Health Impacts of Fibrous Nanomaterials: What Have We Learned from Asbestos? Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2009, 1 (5) 511-529
2. Xia, T.; Li, N.; Nel, A. E. Potential Health Impact of Nanoparticles Annu. Rev. Public Health 2009, 30, 137-150
3. Ishimatsu, S.; Hori, H.; Kasai, T.; Ogami, A.; Morimoto, Y.; Oyabu, T.; Tanaka, I. Biological Effect of Carbon Graphite Whisker in Rat Lung by Long-Term Inhalation Inhal. Toxicol. 2009, 21, 668-673
4. Shvedova, A. A.; Kagan, V. E. The Role of Nanotoxicology in Realizing the 'Helping Without Harm' Paradigm of Nanomedicine: Lessons from Studies of Pulmonary Effects of Single-Walled Carbon Nanotubes J. Int. Med. 2010, 267, 106-118
5. Jain, S.; Thakare, V. S.; Das, M.; Godugu, C.; Jain, A. K.; Mathur, R.; Chuttani, K.; Mishra, A. K. Toxicity of Multiwalled Carbon Nanotubes with End Defects Critically Depends on Their Functionalization Density Chem. Res. Toxicol. 2011, 24, 2028-2039
6. Kolosnjaj-Tabi, J.; Hartman, K. B.; Boudjemaa, S.; Ananta, J. S.; Morgant, G.; Szwarc, H.; Wilson, L. J.; Moussa, F. In Vivo Behavior of Large Doses of Ultrashort and Full-Length Single-Walled Carbon Nanotubes after Oral and Intraperitoneal Administration to Swiss Mice ACS Nano 2010, 4, 1481-1492
7. 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
8. Wei, Z. H.; Wang, H.; Chen, X. Y.; Wang, B. S.; Rong, Z. X.; Wang, B. S.; Su, B. H.; Chen, H. Z. Time-and Dose-Dependent Effect of Psyllium on Serum Lipids in Mild-To-Moderate Hypercholesterolemia: A Meta-Analysis Of Controlled Clinical Trials Eur. J. Clin. Nutr. 2009, 63, 821-827
9. Allen, B. L.; Kotchey, G. P.; Chen, Y.; Yanamala, N. V.; Klein-Seetharaman, J.; Kagan, V. E.; Star, A. Mechanistic Investigations Of Horseradish Peroxidase-Catalyzed Degradation of Single-Walled Carbon Nanotubes J. Am. Chem. Soc. 2009, 131, 17194-17205
10. Naqui, A.; Chance, B.; Cadenas, E. Reactive Oxygen Intermediates in Biochemistry Annu. Rev. Biochem. 1986, 55, 137-166 (Pubitemid 16070766)
11. Kotchey, G. P.; Hasan, S. A.; Kapralov, A. A.; Ha, S. H.; Kim, K.; Shvedova, A. A.; Kagan, V. E.; Star, A. A Natural Vanishing Act: The Enzyme-Catalyzed Degradation of Carbon Nanomaterials Acc. Chem. Res. 2012, 45, 1770-1781
12. Russier, J.; Menard-Moyon, C.; Venturelli, E.; Gravel, E.; Marcolongo, G.; Meneghetti, M.; Doris, E.; Bianco, A. Oxidative Biodegradation of Single- and Multi-Walled Carbon Nanotubes Nanoscale 2011, 3, 893-896
13. Kagan, V. E.; Konduru, N. V.; Feng, W.; Allen, B. L.; Conroy, J.; Volkov, Y.; Vlasova, I. I.; Belikova, N. A.; Yanamala, N.; Kapralov, A. et al. Carbon Nanotubes Degraded by Neutrophil Myeloperoxidase Induce Less Pulmonary Inflammation Nat. Nanotechnol. 2010, 5, 354-359
14. Shvedova, A. A.; Kapralov, A. A.; Feng, W. H.; Kisin, E. R.; Murray, A. R.; Mercer, R. R.; St Croix, C. M.; Lang, M. A.; Watkins, S. C.; Konduru, N. V. et al. Impaired Clearance and Enhanced Pulmonary Inflammatory/Fibrotic Response to Carbon Nanotubes in Myeloperoxidase-Deficient Mice PloS One 2012, 7, e30923
15. Furtmuller, P. G.; Zederbauer, M.; Jantschko, W.; Helm, J.; Bogner, M.; Jakopitsch, C.; Obinger, C. Active Site Structure and Catalytic Mechanisms of Human Peroxidases Arch. Biochem. Biophys. 2006, 445, 199-213 (Pubitemid 43082213)
16. Arnhold, J.; Flemmig, J. Human Myeloperoxidase in Innate and Acquired Immunity Arch. Biochem. Biophys. 2010, 500, 92-106
17. Yoon, S. M.; Kim, S. J.; Shin, H. J.; Benayad, A.; Choi, S. J.; Kim, K. K.; Kim, S. M.; Park, Y. J.; Kim, G.; Choi, J. Y. et al. Selective Oxidation on Metallic Carbon Nanotubes by Halogen Oxoanions J. Am. Chem. Soc. 2008, 130 (8) 2610-2616 (Pubitemid 351304776)
18. Zhang, L.; Petersen, E. J.; Habteselassie, M. Y.; Mao, L.; Huang, Q. Degradation of Multiwall Carbon Nanotubes by Bacteria Environ. Pollut. 2013, 181, 335-339
19. Soehnlein, O.; Lindbom, L.; Weber, C. Mechanisms Underlying Neutrophil-Mediated Monocyte Recruitment Blood 2009, 114 (21) 4613-4623
20. Shvedova, A. A.; Kisin, E.; Murray, A. R.; Johnson, V. J.; Gorelik, O.; Arepalli, S.; Hubbs, A. F.; Mercer, R. R.; Keohavong, P.; Sussman, N. 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. 2008, 295, L552-L565
21. Dale, D. C.; Boxer, L.; Liles, W. C. The Phagocytes: Neutrophils and Monocytes Blood 2008, 112, 935-945
22. Linares, E.; Giorgio, S.; Mortara, R. A.; Santos, C. X.; Yamada, A. T.; Augusto, O. Role of Peroxynitrite in Macrophage Microbicidal Mechanisms in Vivo Revealed by Protein Nitration and Hydroxylation Free Radical Biol. Med. 2001, 30, 1234-1242 (Pubitemid 32463934)
23. Forman, H. J.; Torres, M. Redox Signaling in Macrophages Mol. Aspects Med. 2001, 22, 189-216 (Pubitemid 33000522)
24. Szabo, C.; Ischiropoulos, H.; Radi, R. Peroxynitrite: Biochemistry, Pathophysiology and Development of Therapeutics Nat. Rev. Drug Discovery 2007, 6, 662-680 (Pubitemid 47207751)
25. Pacher, P.; Beckman, J. S.; Liaudet, L. Nitric Oxide and Peroxynitrite in Health and Disease Physiol. Rev. 2007, 87, 315-424 (Pubitemid 46217686)
26. Shvedova, A. A.; Kisin, E. R.; Murray, A. R.; Kommineni, C.; Castranova, V.; Fadeel, B.; Kagan, V. E. Increased Accumulation of Neutrophils and Decreased Fibrosis in the Lung of NADPH Oxidase-Deficient C57BL/6 Mice Exposed to Carbon Nanotubes Toxicol. Appl. Pharmacol. 2008, 231, 235-240
27. Badireddy, A. R.; Wiesner, M. R.; Liu, J. Detection, Characterization, and Abundance of Engineered Nanoparticles in Complex Waters by Hyperspectral Imagery with Enhanced Darkfield Microscopy Environ. Sci. Technol. 2012, 46, 10081-10088
28. Weinkauf, H.; Brehm-Stecher, B. F. Enhanced Dark Field Microscopy for Rapid Artifact-Free Detection of Nanoparticle Binding to Candida Albicans Cells and Hyphae Biotechnol. J. 2009, 4, 871-879
29. Koppenol, W. H.; Moreno, J. J.; Pryor, W. A.; Ischiropoulos, H.; Beckman, J. S. Peroxynitrite, a Cloaked Oxidant Formed by Nitric Oxide and Superoxide Chem. Res. Toxicol. 1992, 5, 834-842 (Pubitemid 23004874)
30. Kim K, H. S. W.; Ashkenazi, S.; O'Donnell, M.; Agarwal, A.; Kotov, N. A.; Denny, M. F.; Kaplan, M.J. Photoacoustic Imaging of Early Inflammatory Response Using Gold Nanorods Appl. Phys. Lett. 2007, 90, 223901-223903
31. 2 Radicals in Aqueous Solution J. Phys. Chem. Ref. Data 1985, 14, 1041-1110
32. Qin, Z. The Use Of THP-1 Cells as a Model for Mimicking the Function and Regulation of Monocytes and Macrophages in the Vasculature Atherosclerosis 2012, 221, 2-11
33. Wardman, P. Fluorescent and Luminescent Probes for Measurement of Oxidative and Nitrosative Species in Cells and Tissues: Progress, Pitfalls, and Prospects Free Radical Biol. Med. 2007, 43, 995-1022 (Pubitemid 47302656)
34. Shvedova, A. A.; Pietroiusti, A.; Fadeel, B.; Kagan, V. E. Mechanisms of Carbon Nanotube-Induced Toxicity: Focus on Oxidative Stress Toxicol. Appl. Pharmacol. 2012, 261 (2) 121-133
35. Oberdorster, G. Nanotoxicology: In Vitro-in Vivo Dosimetry Environ. Health Perspect. 2012, 120, A13 author reply A13
36. Shvedova, A. A.; Kisin, E. R.; Mercer, R.; Murray, A. R.; Johnson, V. J.; Potapovich, A. I.; Tyurina, Y. Y.; Gorelik, O.; Arepalli, S.; Schwegler-Berry, D. et al. Unusual Inflammatory and Fibrogenic Pulmonary Responses to Single-Walled Carbon Nanotubes in Mice Am. J. Physiol. Lung Cell. Mol. Physiol. 2005, 289, L698-L708 (Pubitemid 41504399)
37. Bussy, C.; Cambedouzou, J.; Lanone, S.; Leccia, E.; Heresanu, V.; Pinault, M.; Mayne-L'hermite, M.; Brun, N.; Mory, C.; Cotte, M. et al. Carbon Nanotubes in Macrophages: Imaging and Chemical Analysis by X-Ray Fluorescence Microscopy Nano Lett. 2008, 8, 2659-2663
38. Murphy, F. A.; Schinwald, A.; Poland, C. A.; Donaldson, K. The Mechanism of Pleural Inflammation by Long Carbon Nanotubes: Interaction of Long Fibres with Macrophages Stimulates Them to Amplify Pro-Inflammatory Responses in Mesothelial Cells Part. Fibre Toxicol. 2012, 9, 8
39. Hickman-Davis, J. M.; O'Reilly, P.; Davis, I. C.; Peti-Peterdi, J.; Davis, G.; Young, K. R.; Devlin, R. B.; Matalon, S. Killing of Klebsiella Pneumoniae by Human Alveolar Macrophages Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 282, L944-L956 (Pubitemid 34654610)
40. Darrah, P. A.; Hondalus, M. K.; Chen, Q.; Ischiropoulos, H.; Mosser, D. M. Cooperation Between Reactive Oxygen and Nitrogen Intermediates in Killing of Rhodococcus Equi by Activated Macrophages Infect. Immun. 2000, 68, 3587-3593 (Pubitemid 30340462)
41. Ischiropoulos, H.; Zhu, L.; Beckman, J. S. Peroxynitrite Formation from Macrophage-Derived Nitric Oxide Arch. Biochem. Biophys. 1992, 298, 446-451
42. Cox, G.; Crossley, J.; Xing, Z. Macrophage Engulfment of Apoptotic Neutrophils Contributes to the Resolution of Acute Pulmonary Inflammation in Vivo Am. J. Respir. Cell Mol. Biol. 1995, 12, 232-237
43. Choi, H. C.; Shim, M.; Bangsaruntip, S.; Dai, H. Spontaneous Reduction of Metal Ions on the Sidewalls of Carbon Nanotubes J. Am. Chem. Soc. 2002, 124, 9058-9059 (Pubitemid 34847660)
44. Andon, F. T.; Kapralov, A. A.; Yanamala, N.; Feng, W.; Baygan, A.; Chambers, B. J.; Hultenby, K.; Ye, F.; Toprak, M. S.; Brandner, B. D. et al. Biodegradation of Single-Walled Carbon Nanotubes by Eosinophil Peroxidase Small 2013, 9, 2721-2729
45. Konduru, N. V.; Tyurina, Y. Y.; Feng, W.; Basova, L. V.; Belikova, N. A.; Bayir, H.; Clark, K.; Rubin, M.; Stolz, D.; Vallhov, H. et al. Phosphatidylserine Targets Single-Walled Carbon Nanotubes to Professional Phagocytes in Vitro and in Vivo PloS One 2009, 4, e4398
46. Rodriguez, P. L.; Harada, T.; Christian, D. A.; Pantano, D. A.; Tsai, R. K.; Discher, D. E. Minimal Self Peptides that Inhibit Phagocytic Clearance and Enhance Delivery of Nanoparticles Science 2013, 339, 971-975
47. Shvedova, A. A.; Kisin, E. R.; Porter, D.; Schulte, P.; Kagan, V. E.; Fadeel, B.; Castranova, V. Mechanisms of Pulmonary Toxicity and Medical Applications of Carbon Nanotubes: Two Faces of Janus? Pharmacol. Ther. 2009, 121, 192-204
48. Donaldson, K.; P, C.; Murphy, F. A.; Macfarlane, M.; Chernova, T.; Schinwald, A. Pulmonary Toxicity of Carbon Nanotubes and Asbestos-Similarities and Differences Adv. Drug Delivery Rev. 2013, 65, 2078-2086
49. Occupational Exposure to Carbon Nanotubes and Nanofibers. NIOSH Current Intelligence Bulletin No. 65, available online at http://www.cdc.gov/niosh/docs/ 2013-145/pdfs/2013-145.pdf, 2013.
50. von der Kammer, F.; Ferguson, P. L.; Holden, P. A.; Masion, A.; Rogers, K. R.; Klaine, S. J.; Koelmans, A. A.; Horne, N.; Unrine, J. M. Analysis of Engineered Nanomaterials in Complex Matrices (Environment and Biota): General Considerations and Conceptual Case Studies Environ. Toxicol. Chem. 2012, 31, 32-49