Functionalization of Carbon Nanoparticles Modulates Inflammatory Cell Recruitment and NLRP3 Inflammasome Activation
Marie Yang
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
Adjuvant Research Group, School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Search for more papers by this authorKevin Flavin
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
School of Chemistry, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
Search for more papers by this authorIlona Kopf
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
School of Chemistry, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
Search for more papers by this authorGabor Radics
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
School of Chemistry, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
Search for more papers by this authorClaire H. A. Hearnden
Adjuvant Research Group, School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Search for more papers by this authorGavin J. McManus
School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Search for more papers by this authorBarry Moran
School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Search for more papers by this authorAdrian Villalta-Cerdas
Department of Chemistry, University of Texas at El Paso, El Paso, Texas, USA
Search for more papers by this authorLuis A. Echegoyen
Department of Chemistry, University of Texas at El Paso, El Paso, Texas, USA
Search for more papers by this authorCorresponding Author
Silvia Giordani
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
School of Chemistry, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland.Search for more papers by this authorCorresponding Author
Ed C. Lavelle
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
Adjuvant Research Group, School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland.Search for more papers by this authorMarie Yang
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
Adjuvant Research Group, School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Search for more papers by this authorKevin Flavin
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
School of Chemistry, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
Search for more papers by this authorIlona Kopf
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
School of Chemistry, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
Search for more papers by this authorGabor Radics
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
School of Chemistry, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
Search for more papers by this authorClaire H. A. Hearnden
Adjuvant Research Group, School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Search for more papers by this authorGavin J. McManus
School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Search for more papers by this authorBarry Moran
School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Search for more papers by this authorAdrian Villalta-Cerdas
Department of Chemistry, University of Texas at El Paso, El Paso, Texas, USA
Search for more papers by this authorLuis A. Echegoyen
Department of Chemistry, University of Texas at El Paso, El Paso, Texas, USA
Search for more papers by this authorCorresponding Author
Silvia Giordani
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
School of Chemistry, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland.Search for more papers by this authorCorresponding Author
Ed C. Lavelle
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland
Adjuvant Research Group, School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Ireland
Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Trinity College, Dublin 2, Ireland.Search for more papers by this authorAbstract
The inflammatory effects of carbon nanoparticles (NPs) are highly disputed. Here it is demonstrated that endotoxin-free preparations of raw carbon nanotubes (CNTs) are very limited in their capacity to promote inflammatory responses in vitro, as well as in vivo. Upon purification and selective oxidation of raw CNTs, a higher dispersibility is achieved in physiological solutions, but this process also enhances their inflammatory activity. In synergy with toll-like receptor (TLR) ligands, CNTs promote NLRP3 inflammasome activation and it is shown for the first time that this property extends to spherical carbon nano-onions (CNOs) of 6 nm in size. In contrast, the benzoic acid functionalization of purified CNTs and CNOs leads to significantly attenuated inflammatory properties. This is evidenced by a reduced secretion of the inflammatory cytokine IL-1β, and a pronounced decrease in the recruitment of neutrophils and monocytes following injection into mice. Collectively, these results reveal that the inflammatory properties of carbon NPs are highly dependent on their physicochemical characteristics and crucially, that chemical surface functionalization allows significant moderation of these properties.
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References
- 1 S. Iijima, Nature 1991, 354, 56.
- 2 X. Zhao, R. Liu, Environ. Int. 2012, 40, 244.
- 3 N. Sinha, J. T. Yeow, IEEE Trans. Nanobiosci. 2005, 4, 180.
- 4 S. Y. Madani, N. Naderi, O. Dissanayake, A. Tan, A. M. Seifalian, Int. J. Nanomed. 2011, 6, 2963.
- 5 Y. Liu, Y. Zhao, B. Sun, C. Chen, Acc Chem Res 2013, 46, 702.
- 6 S. K. Smart, A. I. Cassady, G. Q. Lu, D. J. Martin, Carbon 2006, 44, 1034.
- 7 L. A. Thomson, F. C. Law, N. Rushton, J. Franks, Biomaterials 1991, 12, 37.
- 8 M. Allen, F. Law, N. Rushton, Clin. Mater. 1994, 17, 1.
- 9 S. Linder, W. Pinkowski, M. Aepfelbacher, Biomaterials 2002, 23, 767.
- 10 T. Thurnherr, C. Brandenberger, K. Fischer, L. Diener, P. Manser, X. Maeder-Althaus, J.-P. Kaiser, H. F. Krug, B. Rothen-Rutishauser, P. Wick, Toxicol. Lett. 2011, 200, 176.
- 11 M. L. Schipper, N. Nakayama-Ratchford, C. R. Davis, N. W. S. Kam, P. Chu, Z. Liu, X. M. Sun, H. J. Dai, S. S. Gambhir, Nat. Nanotechnol. 2008, 3, 2.16.
- 12 D. Urgate, Nature 1992, 359, 707.
- 13 M. Ghosh, S. K. Sonkar, M. Saxena, S. Sarkar, Small 2011, 7, 3170.
- 14 E. L. Chng, M. Pumera, Chemistry 2012, 18, 1401.
- 15 E. Del Canto, K. Flavin, D. Movia, C. Navio, C. Bittencourt, S. Giordani, Chem. Mater. 2011, 23, 67.
- 16 V. E. Kagan, Y. Y. Tyurina, V. A. Tyurin, N. V. Konduru, A. I. Potapovich, A. N. Osipov, E. R. Kisin, D. Schwegler-Berry, R. Mercer, V. Castranova, A. A. Shvedova, Toxicol. Lett. 2006, 165, 88.
- 17 L. G. Delogu, S. M. Stanford, E. Santelli, A. Magrini, A. Bergamaschi, K. Motamedchaboki, N. Rosato, T. Mustelin, N. Bottini, M. Bottini, J. Nanosci. Nanotechnol. 2010, 10.
- 18 K. Pulskamp, S. Diabaté, H. F. Krug, Toxicol. Lett. 2007, 168, 58.
- 19 F. Flavin, I. Kopf, E. Del Canto, C. Navio, C. Bittencourt, S. Giordani, J. Mater. Chem. 2011, 21, 17881.
- 20 G. A. Tynan, A. McNaughton, A. Jarnicki, T. Tsuji, E. C. Lavelle, PloS One 2012, 7, e37261.
- 21 S. L. Hem, H. Hogenesch, Exp. Rev. Vaccines 2007, 6, 685.
- 22 M. W. Munks, A. S. McKee, M. K. MacLeod, R. L. Powell, J. L. Degen, N. A. Reisdorph, J. W. Kappler, P. Marrack, Blood 2010, 116, 5191.
- 23 K. Schroder, J. Tschopp, Cell 2010, 140, 821.
- 24 E. Meunier, A. Coste, D. Olagnier, H. Authier, L. Lefèvre, C. Dardenne, J. Bernad, M. Béraud, E. Flahaut, B. Pipy, Nanomedicine 2012, 8, 987.
- 25 J. Palomäki, E. Välimäki, J. Sund, M. Vippola, P. A. Clausen, K. A. Jensen, K. Savolainen, S. Matikainen, H. Alenius, ACS Nano 2011, 5, 6861.
- 26 A. S. Rettenbacher, B. Elliott, J. S. Hudson, A. Amirkhanian, L. Echegoyen, Chemistry 2005, 12, 376.
- 27 K. Flavin, K. Lawrence, J. Bartelmess, M. Tasior, C. Navio, C. Bittencourt, D. F. O'Shea, D. M. Guldi, S. Giordani, ACS Nano 2011, 5, 1198.
- 28 K. Flavin, N. Chaur, L. Echegoyen, S. Giordani, Org. Lett. 2010, 12, 840.
- 29 M. S. Strano, C. A. Dyke, M. L. Usrey, P. W. Barone, M. J. Allen, H. Shan, C. Kittrell, R. H. Hauge, J. M. Tour, R. E. Smalley, Science 2003, 301, 1519.
- 30 B. Smith, K. Wepasnick, K. E. Schrote, A. R. Bertele, W. P. Ball, C. O'Melia, D. H. Fairbrother, Environ. Sci. Technol. 2009, 43, 819.
- 31 A. Savina, S. Amigorena, Immunol Rev. 2007, 219, 143.
- 32 D. Yang, Y. Zhao, H. Guo, Y. Li, P. Tewary, G. Xing, W. Hou, J. J. Oppenheim, N. Zhang, ACS Nano 2010, 4, 1178.
- 33 K. Inoue, R. Yanagisawa, E. Koike, M. Nishikawa, H. Takano, Free Radical Biol. Med. 2010, 48, 924.
- 34 A. V. Tkach, G. V. Shurin, M. R. Shurin, E. R. Kisin, A. R. Murray, S. H. Young, A. Star, B. Fadeel, V. E. Kagan, A. A. Shvedova, ACS Nano 2011, 5, 5755.
- 35 J. Palomäki, P. Karisola, L. Pylkkänen, K. Savolainen, H. Alenius, Toxicology 2010, 267, 125.
- 36 T. Zhang, M. Tang, L. Kong, H. Li, T. Zhang, S. Zhang, Y. Xue, Y. Pu, J. Hazard Mater. 2012, 219-220, 203.
- 37 D. Crouzier, S. Follot, E. Gentilhomme, E. Flahaut, R. Arnaud, V. Dabouis, C. Castel-larin, J. C. Debouzy, Toxicology 2010, 272, 39.
- 38 A. S. Yazdi, G. Guarda, N. Riteau, S. K. Drexler, A. Tardivel, I. Couillin, J. Tschopp, Proc. Natl. Acad. Sci. USA 2010, 107, 19449.
- 39 H. Li, S. B. Willingham, J. P. Ting, F. Re, J. Immunol. 2008, 181, 17.
- 40 T. Fernandes-Alnemri, J. Wu, J. W. Yu, P. Datta, B. Miller, W. Jankowski, S. Rosenberg, J. Zhang, E. S. Alnemri, Cell Death Differ. 2007, 14, 1590.
- 41 A. Halle, V. Hornung, G. C. Petzold, C. R. Stewart, B. G. Monks, T. Reinheckel, K. A. Fitzgerald, E. Latz, K. J. Moore, D. T. Golenbock, Nat. Immunol. 2008, 9, 857.
- 42 V. Hornung, F. Bauernfeind, A. Halle, E. O. Samstad, H. Kono, K. L. Rock, Nat. Immunol. 2008, 9, 847.
- 43 M. Kool, T. Thomas Soullié, M. van Nimwegen, M. A. M. Willart, F. Muskens, S. Jung, H. C. Hoogsteden, H. Hammad, B. N. Lambrecht, J. Exp. Med. 2008, 205, 869.
- 44 S. Calabro, M. Tortoli, B. C. Baudner, A. Pacitto, M. Cortese, D. T. O'Hagan, E. De Gregorio, A. Seubert, A. Wack, Vaccine 2011, 29, 1812.
- 45 H. Sun, K. G. Pollock, J. M. Brewer, Vaccine 2003, 21, 849.
- 46 A. S. McKee, M. W. Munks, P. Marrack, Immunity 2007, 27, 687.
- 47 L. Yan, F. Zhao, S. Li, Z. Hu, Y. Zhao, Nanoscale 2011, 3, 362.
- 48 M. V. Ivanova, C. Lamprecht, M. J. Loureiro, J. T. Huzil, M. Foldvari, Int. J. Nanomed. 2012, 7, 403.
- 49 R. K. Esch, L. Han, K. K. Foarde, D. S. Ensor, Nanotoxicology 2010, 4, 73.
- 50 F. A. Sharp, D. Ruane, B. Claass, E. Creagh, J. Harris, P. Malyala, M. Singh, D. T. O'Hagan, V. Pétrilli, J. Tschopp, L. A. J. O'Neill, E. C. Lavelle, Proc. Natl. Acad. Sci. USA 2009, 106, 870.
- 51 L. Ding, J. Stilwell, T. Zhang, O. Elboudwarej, H. Jiang, J. P. Selegue, P. A. Cooke, J. W. Gray, F. F. Chen, Nano Lett. 2005, 5, 2448.
- 52 P. Urban, J. J. Valle-Delgado, E. Moles, J. Marques, C. Diez, X. Fernandez-Busquets, Curr. Drug Targets 2012, 13, 1158.
- 53 B. Zhang, C. T. Kwok, J. Mater. Sci. Mater. Med. 2011, 22, 2249.
- 54 Z. Liu, S. Tabakman, K. Welsher, H. Dai, Nano Res. 2009, 2, 85.
- 55 H. L. Karlsson, J. Gustafsson, P. Cronholm, L. Möller, Toxicol. Lett. 2009, 188, 112.
- 56 H. Yang, C. Liu, D. Yang, H. Zhang, Z. Xi, J. Appl. Toxicol. 2009, 29, 69.
- 57 I. Horcas, R. Fernández, J. M. Gómez-Rodríguez, J. Colchero, J. Gómez-Herrero, A. M. Baro, Rev. Sci. Instrum. 2007, 78, 13705.
- 58 F. Martinon, V. Petrilli, A. Mayor, A. Tardivel, J. Tschopp, Nature 2006, 440, 237.
- 59 M. B. Lutz, N. Kukutsch, A. L. Ogilvie, S. Rössner, F. Koch, N. Romani, G. Schuler, J. Immunol. Methods 1999, 223, 77.
- 60 E. A. McNeela, A. Burke, D. R. Neill, C. Baxter, V. E. Fernandes, D. Ferreira, S. Smeaton, R. El-Rachkidy, R. M. McLoughlin, A. Mori, B. Moran, K. A. Fitzgerald, J. Tschopp, V. Pétrilli, P. W. Andrew, A. Kadioglu, E. C. Lavelle, PLoS Pathog. 2010, 6, e 1001191.
- 61 S. L. Doyle, M. Campbell, E. Ozaki, R. G. Salomon, A. Mori, P. F. Kenna, G. J. Farrar, A. S. Kiang, M. M. Humphries, E. C. Lavelle, L. A. O'Neill, J. G. Hollyfield, P. Humphries, Nat. Med. 2012, 18, 791.