Inert 50-nm polystyrene nanoparticles that modify pulmonary dendritic cell function and inhibit allergic airway inflammation

Journal of Immunology

Volumn 188, Issue 3, 2012, Pages 1431-1441

  Hardy, Charles L ^a,b,c   LeMasurier, Jeanne S ^a,b,c   Belz, Gabrielle T ^d   Scalzo Inguanti, Karen ^a   Yao, Jun ^a,b,c   Xiang, Sue D ^a   Kanellakis, Peter ^e   Bobik, Alex ^e   Strickland, Deborah H ^f,g   Rolland, Jennifer M ^a,b,c   O'Hehir, Robyn E ^a,b,c   Plebanski, Magdalena ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b ALFRED HOSPITAL   (Australia)

^c Cooperative Research Center for Asthma and Airways ^*  (Australia)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^g UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; AMINO ACID; IMMUNOGLOBULIN E; NANOPARTICLE; POLYSTYRENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; FLOW CYTOMETRY; IMMUNOMODULATION; LIPID PEROXIDATION; LUNG PARENCHYMA; MOUSE; NONHUMAN; OXIDATIVE STRESS; PNEUMONIA; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DENDRITIC CELLS; LUNG; MICE; NANOSTRUCTURES; OXIDATIVE STRESS; PNEUMONIA; POLYSTYRENES;

EID: 84856562857     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100156     Document Type: Article

References (56)

1. Oberdörster, G., E. Oberdörster, and J. Oberdörster. 2005. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 113: 823-839. (Pubitemid 40984181)
2. Brunekreef, B., and S. T. Holgate. 2002. Air pollution and health. Lancet 360: 1233-1242. (Pubitemid 35232725)
3. Nel, A. 2005. Atmosphere. Air pollution-related illness: effects of particles. Science 308: 804-806. (Pubitemid 40629248)
4. Umetsu, D. T., J. J. McIntire, O. Akbari, C. Macaubas, and R. H. DeKruyff. 2002. Asthma: an epidemic of dysregulated immunity. Nat. Immunol. 3: 715-720.
5. Ichinose, T., H. Takano, Y. Miyabara, R. Yanagisawa, and M. Sagai. 1997. Murine strain differences in allergic airway inflammation and immunoglobulin production by a combination of antigen and diesel exhaust particles. Toxicology 122: 183-192. (Pubitemid 27390690)
6. Løvik, M., A. K. Høgseth, P. I. Gaarder, R. Hagemann, and I. Eide. 1997. Diesel exhaust particles and carbon black have adjuvant activity on the local lymph node response and systemic IgE production to ovalbumin. Toxicology 121: 165-178. (Pubitemid 27273790)
7. Nel, A. E., D. Diaz-Sanchez, D. Ng, T. Hiura, and A. Saxon. 1998. Enhancement of allergic inflammation by the interaction between diesel exhaust particles and the immune system. J. Allergy Clin. Immunol. 102: 539-554.
8. Hao, M., S. Comier, M. Wang, J. J. Lee, and A. Nel. 2003. Diesel exhaust particles exert acute effects on airway inflammation and function in murine allergen provocation models. J. Allergy Clin. Immunol. 112: 905-914. (Pubitemid 37412058)
9. Alessandrini, F., H. Schulz, S. Takenaka, B. Lentner, E. Karg, H. Behrendt, and T. Jakob. 2006. Effects of ultrafine carbon particle inhalation on allergic inflammation of the lung. J. Allergy Clin. Immunol. 117: 824-830.
10. de Haar, C., I. Hassing, M. Bol, R. Bleumink, and R. Pieters. 2006. Ultrafine but not fine particulate matter causes airway inflammation and allergic airway sensitization to co-administered antigen in mice. Clin. Exp. Allergy 36: 1469-1479. (Pubitemid 44674132)
11. de Haar, C., M. Kool, I. Hassing, M. Bol, B. N. Lambrecht, and R. Pieters. 2008. Lung dendritic cells are stimulated by ultrafine particles and play a key role in particle adjuvant activity. J. Allergy Clin. Immunol. 121: 1246-1254.
12. Larsen, S. T., M. Roursgaard, K. A. Jensen, and G. D. Nielsen. 2010. Nano titanium dioxide particles promote allergic sensitization and lung inflammation in mice. Basic Clin. Pharmacol. Toxicol. 106: 114-117.
13. Inoue, K., R. Yanagisawa, E. Koike, M. Nishikawa, and H. Takano. 2010. Repeated pulmonary exposure to single-walled carbon nanotubes exacerbates allergic inflammation of the airway: Possible role of oxidative stress. Free Radic. Biol. Med. 48: 924-934.
14. Inoue, K., E. Koike, R. Yanagisawa, S. Hirano, M. Nishikawa, and H. Takano. 2009. Effects of multi-walled carbon nanotubes on a murine allergic airway inflammation model. Toxicol. Appl. Pharmacol. 237: 306-316.
15. Ghio, A. J., and R. B. Devlin. 2001. Inflammatory lung injury after bronchial instillation of air pollution particles. Am. J. Respir. Crit. Care Med. 164: 704-708. (Pubitemid 32801680)
16. Huang, Y. C., A. J. Ghio, J. Stonehuerner, J. McGee, J. D. Carter, S. C. Grambow, and R. B. Devlin. 2003. The role of soluble components in ambient fine particles-induced changes in human lungs and blood. Inhal. Toxicol. 15: 327-342. (Pubitemid 36458883)
17. Inoue, K., H. Takano, K. Hiyoshi, T. Ichinose, K. Sadakane, R. Yanagisawa, S. Tomura, and Y. Kumagai. 2007. Naphthoquinone enhances antigen-related airway inflammation in mice. Eur. Respir. J. 29: 259-267. (Pubitemid 46231902)
18. Xu, J., M. Futakuchi, M. Iigo, K. Fukamachi, D. B. Alexander, H. Shimizu, Y. Sakai, S. Tamano, F. Furukawa, T. Uchino, et al. 2010. Involvement of macrophage inflammatory protein 1alpha (MIP1alpha) in promotion of rat lung and mammary carcinogenic activity of nanoscale titanium dioxide particles administered by intra-pulmonary spraying. Carcinogenesis 31: 927-935.
19. Li, N., M. Wang, L. A. Bramble, D. A. Schmitz, J. J. Schauer, C. Sioutas, J. R. Harkema, and A. E. Nel. 2009. The adjuvant effect of ambient particulate matter is closely reflected by the particulate oxidant potential. Environ. Health Perspect. 117: 1116-1123.
20. Reddy, S. T., M. A. Swartz, and J. A. Hubbell. 2006. Targeting dendritic cells with biomaterials: developing the next generation of vaccines. Trends Immunol. 27: 573-579. (Pubitemid 44708833)
21. Xiang, S. D., A. Scholzen, G. Minigo, C. David, V. Apostolopoulos, P. L. Mottram, and M. Plebanski. 2006. Pathogen recognition and development of particulate vaccines: does size matter? Methods 40: 1-9. (Pubitemid 44415493)
22. Fifis, T., A. Gamvrellis, B. Crimeen-Irwin, G. A. Pietersz, J. Li, P. L. Mottram, I. F. McKenzie, and M. Plebanski. 2004. Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. J. Immunol. 173: 3148-3154. (Pubitemid 39142021)
23. Reddy, S. T., A. J. van der Vlies, E. Simeoni, V. Angeli, G. J. Randolph, C. P. O'Neil, L. K. Lee, M. A. Swartz, and J. A. Hubbell. 2007. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat. Biotechnol. 25: 1159-1164. (Pubitemid 47538111)
24. Hardy, C. L., L. Kenins, A. C. Drew, J. M. Rolland, and R. E. O'Hehir. 2003. Characterization of a mouse model of allergy to a major occupational latex glove allergen Hev b 5. Am. J. Respir. Crit. Care Med. 167: 1393-1399. (Pubitemid 36609725)
25. Vremec, D., M. Zorbas, R. Scollay, D. J. Saunders, C. F. Ardavin, L. Wu, and K. Shortman. 1992. The surface phenotype of dendritic cells purified from mouse thymus and spleen: investigation of the CD8 expression by a subpopulation of dendritic cells. J. Exp. Med. 176: 47-58.
26. Weckmann, M., A. Collison, J. L. Simpson, M. V. Kopp, P. A. Wark, M. J. Smyth, H. Yagita, K. I. Matthaei, N. Hansbro, B. Whitehead, et al. 2007. Critical link between TRAIL and CCL20 for the activation of TH2 cells and the expression of allergic airway disease. Nat. Med. 13: 1308-1315. (Pubitemid 350073595)
27. Belz, G. T., S. Bedoui, F. Kupresanin, F. R. Carbone, and W. R. Heath. 2007. Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat. Immunol. 8: 1060-1066. (Pubitemid 47423753)
28. Kanellakis, P., N. J. Slater, X. J. Du, A. Bobik, and D. J. Curtis. 2006. Granulocyte colony-stimulating factor and stem cell factor improve endogenous repair after myocardial infarction. Cardiovasc. Res. 70: 117-125.
29. Belz, G. T., C. M. Smith, L. Kleinert, P. Reading, A. Brooks, K. Shortman, F. R. Carbone, and W. R. Heath. 2004. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. USA 101: 8670-8675. (Pubitemid 38745829)
30. Smith, C. M., G. T. Belz, N. S. Wilson, J. A. Villadangos, K. Shortman, F. R. Carbone, and W. R. Heath. 2003. Cutting edge: conventional CD8 alpha+ dendritic cells are preferentially involved in CTL priming after footpad infection with herpes simplex virus-1. J. Immunol. 170: 4437-4440. (Pubitemid 36519947)
31. Hardy, C. L., A. E. O'Connor, J. Yao, K. Sebire, D. M. de Kretser, J. M. Rolland, G. P. Anderson, D. J. Phillips, and R. E. O'Hehir. 2006. Follistatin is a candidate endogenous negative regulator of activin A in experimental allergic asthma. Clin. Exp. Allergy 36: 941-950. (Pubitemid 43972961)
32. van Rijt, L. S., H. Kuipers, N. Vos, D. Hijdra, H. C. Hoogsteden, and B. N. Lambrecht. 2004. A rapid flow cytometric method for determining the cellular composition of bronchoalveolar lavage fluid cells in mouse models of asthma. J. Immunol. Methods 288: 111-121. (Pubitemid 38739257)
33. Beaty, S. R., C. E. Rose, Jr., and S. S. Sung. 2007. Diverse and potent chemokine production by lung CD11bhigh dendritic cells in homeostasis and in allergic lung inflammation. J. Immunol. 178: 1882-1895. (Pubitemid 46154661)
34. von Garnier, C., L. Filgueira, M. Wikstrom, M. Smith, J. A. Thomas, D. H. Strickland, P. G. Holt, and P. A. Stumbles. 2005. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J. Immunol. 175: 1609-1618. (Pubitemid 41023063)
35. Huang, T. J., P. A. MacAry, P. Eynott, A. Moussavi, K. C. Daniel, P. W. Askenase, D. M. Kemeny, and K. F. Chung. 2001. Allergen-specific Th1 cells counteract efferent Th2 cell-dependent bronchial hyperresponsiveness and eosinophilic inflammation partly via IFN-gamma. J. Immunol. 166: 207-217. (Pubitemid 32038434)
36. Greenwood, D. L., K. Dynon, M. Kalkanidis, S. Xiang, M. Plebanski, and J. P. Scheerlinck. 2008. Vaccination against foot-and-mouth disease virus using peptides conjugated to nano-beads. Vaccine 26: 2706-2713.
37. Mottram, P. L., D. Leong, B. Crimeen-Irwin, S. Gloster, S. D. Xiang, J. Meanger, R. Ghildyal, N. Vardaxis, and M. Plebanski. 2007. Type 1 and 2 immunity following vaccination is influenced by nanoparticle size: formulation of a model vaccine for respiratory syncytial virus. Mol. Pharm. 4: 73-84.
38. Scheerlinck, J. P., S. Gloster, A. Gamvrellis, P. L. Mottram, and M. Plebanski. 2006. Systemic immune responses in sheep, induced by a novel nano-bead adjuvant. Vaccine 24: 1124-1131. (Pubitemid 43202258)
39. Xia, T., M. Kovochich, J. Brant, M. Hotze, J. Sempf, T. Oberley, C. Sioutas, J. I. Yeh, M. R. Wiesner, and A. E. Nel. 2006. Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett. 6: 1794-1807. (Pubitemid 44327550)
40. Hammad, H., and B. N. Lambrecht. 2008. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat. Rev. Immunol. 8: 193-204. (Pubitemid 351323293)
41. Vermaelen, K. Y., I. Carro-Muino, B. N. Lambrecht, and R. A. Pauwels. 2001. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J. Exp. Med. 193: 51-60. (Pubitemid 32060697)
42. Lebman, D. A., and R. L. Coffman. 1988. Interleukin 4 causes isotype switching to IgE in T cell-stimulated clonal B cell cultures. J. Exp. Med. 168: 853-862.
43. Grünig, G., M. Warnock, A. E. Wakil, R. Venkayya, F. Brombacher, D. M. Rennick, D. Sheppard, M. Mohrs, D. D. Donaldson, R. M. Locksley, and D. B. Corry. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282: 2261-2263. (Pubitemid 29004075)
44. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science 282: 2258-2261. (Pubitemid 29004074)
45. Kuperman, D. A., X. Huang, L. L. Koth, G. H. Chang, G. M. Dolganov, Z. Zhu, J. A. Elias, D. Sheppard, and D. J. Erle. 2002. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8: 885-889.
46. Foster, P. S., S. P. Hogan, A. J. Ramsay, K. I. Matthaei, and I. G. Young. 1996. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J. Exp. Med. 183: 195-201. (Pubitemid 26028759)
47. Hogan, S. P., A. Koskinen, K. I. Matthaei, I. G. Young, and P. S. Foster. 1998. Interleukin-5-producing CD4+ T cells play a pivotal role in aeroallergen-induced eosinophilia, bronchial hyperreactivity, and lung damage in mice. Am. J. Respir. Crit. Care Med. 157: 210-218. (Pubitemid 28071285)
48. Yamaguchi, Y., T. Suda, J. Suda, M. Eguchi, Y. Miura, N. Harada, A. Tominaga, and K. Takatsu. 1988. Purified interleukin 5 supports the terminal differentiation and proliferation of murine eosinophilic precursors. J. Exp. Med. 167: 43-56. (Pubitemid 18093692)
49. Yang, M., S. P. Hogan, S. Mahalingam, S. M. Pope, N. Zimmermann, P. Fulkerson, L. A. Dent, I. G. Young, K. I. Matthaei, M. E. Rothenberg, and P. S. Foster. 2003. Eotaxin-2 and IL-5 cooperate in the lung to regulate IL-13 production and airway eosinophilia and hyperreactivity. J. Allergy Clin. Immunol. 112: 935-943. (Pubitemid 37412062)
50. Vermaelen, K., and R. Pauwels. 2003. Accelerated airway dendritic cell maturation, trafficking, and elimination in a mouse model of asthma. Am. J. Respir. Cell Mol. Biol. 29: 405-409. (Pubitemid 37094000)
51. Robays, L. J., T. Maes, S. Lebecque, S. A. Lira, W. A. Kuziel, G. G. Brusselle, G. F. Joos, and K. V. Vermaelen. 2007. Chemokine receptor CCR2 but not CCR5 or CCR6 mediates the increase in pulmonary dendritic cells during allergic airway inflammation. J. Immunol. 178: 5305-5311. (Pubitemid 46595316)
52. Sung, S. S., S. M. Fu, C. E. Rose, Jr., F. Gaskin, S. T. Ju, and S. R. Beaty. 2006. A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J. Immunol. 176: 2161-2172. (Pubitemid 43201663)
53. Stumbles, P. A., D. H. Strickland, C. L. Pimm, S. F. Proksch, A. M. Marsh, A. S. McWilliam, A. Bosco, I. Tobagus, J. A. Thomas, S. Napoli, et al. 2001. Regulation of dendritic cell recruitment into resting and inflamed airway epithelium: use of alternative chemokine receptors as a function of inducing stimulus. J. Immunol. 167: 228-234. (Pubitemid 32567782)
54. Stumbles, P. A., J. A. Thomas, C. L. Pimm, P. T. Lee, T. J. Venaille, S. Proksch, and P. G. Holt. 1998. Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity. J. Exp. Med. 188: 2019-2031. (Pubitemid 28562519)
55. Jakubzick, C., M. Bogunovic, A. J. Bonito, E. L. Kuan, M. Merad, and G. J. Randolph. 2008. Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes. J. Exp. Med. 205: 2839-2850.
56. del Rio, M. L., J. I. Rodriguez-Barbosa, E. Kremmer, and R. Förster. 2007. CD103- and CD103+ bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4+ and CD8+ T cells. J. Immunol. 178: 6861-6866. (Pubitemid 46847411)