Lung exposure of titanium dioxide nanoparticles induces innate immune activation and long-lasting lymphocyte response in the Dark Agouti rat

Journal of Immunotoxicology

Volumn 8, Issue 2, 2011, Pages 111-121

  Gustafsson, Åsa ^a,b   Lindstedt, Elsa ^a,c   Elfsmark, Linda Svensson ^a   Bucht, Anders ^a,b  

^a SWEDISH DEFENCE RESEARCH AGENCY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

dendritic cells; inflammation; lung; Nanoparticles; NK cells; T cells; TiO2

Indexed keywords

CD8 ANTIGEN; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; INTERLEUKIN 6; NANOMATERIAL; NANOPARTICLE; TITANIUM DIOXIDE; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CHRONIC INFLAMMATION; CONTROLLED STUDY; DARK AGOUTI RAT; DENDRITIC CELL; ENVIRONMENTAL EXPOSURE; EOSINOPHIL; HELPER CELL; IMMUNE RESPONSE; IMMUNOSTIMULATION; INFLAMMATION; INHALATION; INNATE IMMUNITY; MALE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RAT; RISK ASSESSMENT; T LYMPHOCYTE ACTIVATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; EOSINOPHILS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; KILLER CELLS, NATURAL; LUNG; MALE; NANOPARTICLES; NEUTROPHIL INFILTRATION; NEUTROPHILS; RATS; TIME FACTORS; TITANIUM;

AGOUTI; RATTUS;

EID: 79955634536     PISSN: 1547691X     EISSN: 1547691X     Source Type: Journal    
DOI: 10.3109/1547691X.2010.546382     Document Type: Article

References (42)

1. Ahn M. H., Kang C. M., Park C. S., Park S. J., Rhim T., Yoon P. O., Chang H. S., Kim S. H., Kyono H., and Kim K. C. 2005. Titanium dioxide particle-induced goblet cell hyperplasia: Association with mast cells and IL-13. Respir. Res. 6:34.
2. Battisto J. R., Smith R. N., Beckman K., Sternlicht M., and Welles W. L. 1982. Susceptibility to adjuvant arthritis in DA and F344 rats. A dominant trait controlled by an autosomal gene locus linked to the major histocompatibility complex. Arthritis Rheum. 25:1194-1200. (Pubitemid 12037827)
3. Bermudez E., Mangum J. B., Wong B. A., Asgharian B., Hext P. M., Warheit D. B., and Everitt J. I. 2004. Pulmonary responses of mice, rats, and hamsters to subchronic inhalation of ultrafne titanium dioxide particles. Toxicol. Sci. 77:347-357. (Pubitemid 38262608)
4. Cambi A., and Figdor C. G. 2003. Dual function of C-type lectin-like receptors in the immune system. Curr. Opin. Cell Biol. 15:539-546. (Pubitemid 37176962)
5. Dieu M. C., Vanbervliet B., Vicari A., Bridon J. M., Oldham E., Aït-Yahia S., Brière F., Zlotnik A., Lebecque S., and Caux C. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in diferent anatomic sites. J. Exp. Med. 188:373-386. (Pubitemid 28357765)
6. Dimitrijevic M., Laban O., Djuric V. J., Stanojevic S., Miletic T., Kovacevic-Jovanovic V., Todorovic C., and Radulovic J. 2001. Behavior and severity of adjuvant arthritis in four rat strains. Brain Behav. Immun. 15:255-265. (Pubitemid 33070958)
7. Eishi Y., and McCullagh P. 1988. PVG rats, resistant to experimental allergic thyroiditis, develop high serum levels of thyroglobulin after sensitization. Clin. Immunol. Immunopathol. 49:101-106.
8. Gasser D. L., Newlin C. M., Palm J., and Gonatas N. K. 1973. Genetic control of susceptibility to experimental allergic encephalomyelitis in rats. Science. 181:872-873.
9. Geijtenbeek T. B., van Vliet S. J., Engering A., 't Hart B. A., and van Kooyk Y. 2004. Self- and nonself-recognition by C-type lectins on dendritic cells. Annu. Rev. Immunol. 22:33-54. (Pubitemid 38680417)
10. Grifths M. M., Eichwald E. J., Martin J. H., Smith C. B., and DeWitt C. W. 1981. Immunogenetic control of experimental Type II collagen-induced arthritis. I. Susceptibility and resistance among inbred strains of rats. Arthritis Rheum. 24:781-789. (Pubitemid 11117266)
11. Gurr J. R., Wang A. S., Chen C. H., and Jan K. Y. 2005. Ultrafne titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicology 213:66-73. (Pubitemid 41191282)
12. Hussain S., Boland S., Baeza-Squiban A., Hamel R., Tomassen L. C., Martens J. A., Billon-Galland M. A., Fleury-Feith J., Moisan F., Pairon J. C., and Marano F. 2009. Oxidative stress and pro-infammatory efects of carbon black and titanium dioxide nanoparticles: Role of particle surface area and internalized amount. Toxicology 260:142-149.
13. Kelly F. J., and Sandström T. 2004. Air pollution, oxidative stress, and allergic response. Lancet 363:95-96. (Pubitemid 38068322)
14. Kheradmand T., Trivedi P. P., Wolf N. A., Roberts P. C., and Swanborg R. H. 2008. Characterization of a subset of bone marrow-derived natural killer cells that regulates T-cell activation in rats. J. Leukoc. Biol. 83:1128-1135. (Pubitemid 351960344)
15. 2 particles of diferent sizes and agglomerations in rats: diferent short- and long-term post-instillation results. Toxicology 264:110-118.
16. Lambrecht B. N., Carro-Muino I., Vermaelen K., and Pauwels R. A. 1999. Allergen-induced changes in bone-marrow progenitor and airway dendritic cells in sensitized rats. Am. J. Respir. Cell Mol. Biol. 20:1165-1174. (Pubitemid 129503234)
17. Lampinen M., Carlson M., Håkansson L. D., and Venge P. 2004. Cytokine-regulated accumulation of eosinophils in infammatory disease. Allergy 59:793-805. (Pubitemid 39005818)
18. Larsen S. T., Roursgaard M., Jensen K. A., and Nielsen G. D. 2010. Nano titanium dioxide particles promote allergic sensitization and lung infammation in mice. Basic Clin. Pharmacol. Toxicol. 106:114-117.
19. Li N., Xia T., and Nel A. E. 2008. Te role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic. Biol. Med. 44:1689-1699.
20. Lorentzen J. C., Andersson M., Issazadeh S., Dahlman I., Luthman H., Weissert R., and Olsson T. 1997. Genetic analysis of infammation, cytokine mRNA expression and disease course of relapsing experimental autoimmune encephalomyelitis in DA rats. J. Neuroimmunol. 80:31-37. (Pubitemid 28015321)
21. Lorentzen J. C., Flornes L., Eklöw C., Bäckdahl L., Ribbhammar U., Guo J. P., Smolnikova M., Dissen E., Seddighzadeh M., Brookes A. J., Alfredsson L., Klareskog L., Padyukov L., and Fossum S. 2007. Association of arthritis with a gene complex encoding C-type lectin-like receptors. Arthritis Rheum. 56:2620-2632. (Pubitemid 47237280)
22. Lundqvist M., Nygren P., Jonsson B. H., and Broo K. 2006. Induction of structure and function in a designed peptide upon adsorption on a silica nanoparticle. Angew. Chem. Int. Ed. Engl. 45:8169-8173. (Pubitemid 44974154)
23. Lundqvist M., Stigler J., Elia G., Lynch I., Cedervall T., and Dawson K. A. 2008. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl. Acad. Sci. USA 105:14265-14270.
24. Ma-Hock L., Burkhardt S., Strauss V., Gamer A. O., Wiench K., van Ravenzwaay B., and Landsiedel R. 2009. Development of a short-term inhalation test in the rat using nano-titanium dioxide as a model substance. Inhal. Toxicol. 21:102-118.
25. 10 and ultrafne particles with special reference to COPD. Eur. Respir. J. Suppl. 40:47s-51s. (Pubitemid 36565582)
26. Maitre B., Boussat S., Jean D., Gouge M., Brochard L., Housset B., Adnot S., and Delclaux C. 2001. Vascular endothelial growth factor synthesis in the acute phase of experimental and clinical lung injury. Eur. Respir. J. 18:100-106. (Pubitemid 32720382)
27. Mills, K. H. 2008. Induction, function, and regulation of IL-17-producing T cells. Eur. J. Immunol. 38:2636-2649.
28. Mills N. L., Törnqvist H., Gonzalez M. C., Vink E., Robinson S. D., Söderberg S., Boon N. A., Donaldson K., Sandström T., Blomberg A., and Newby D. E. 2007. Ischemic and thrombotic efects of dilute diesel-exhaust inhalation in men with coronary heart disease. New Engl. J. Med. 357:1075-1082. (Pubitemid 47443212)
29. Nakagawa H., Komorita N., Shibata F., Ikesue A., Konishi K., Fujioka M., and Kato H. 1994. Identifcation of cytokine-induced neutrophil chemoattractants (CINC), rat GRO/CINC-2 α and CINC-2 β, produced by granulation tissue in culture: Purifcation, complete amino acid sequences, and characterization. Biochem. J. 301 (Pt 2):545-550.
30. Nel A., Xia T., Mädler L., and Li N. 2006. Toxic potential of materials at the nanolevel. Science 311:622-627. (Pubitemid 43191298)
31. NIOSH. 2005. NIOSH Current Intelligence Bulletin: Evaluation of Health Hazard and Recommendations for Occupational Exposure to Titanium Dioxide. Public Review Draft, November 2005. Cincinnati, OH: U.S. Department of Health and Human Services, Public Health Service Centers for Disease Control and Prevention, National Institute for Occupational Safety and Health.
32. Oberdörster G., Ferin J., Gelein R., Soderholm S. C., and Finkelstein J. 1992. Role of the alveolar macrophage in lung injury: Studies with ultrafne particles. Environ. Health Perspect. 97:193-199.
33. Oberdörster G., Ferin J., and Lehnert B. E. 1994. Correlation between particle size, in vivo particle persistence, and lung injury. Environ. Health Perspect. 102 (Suppl 5):173-179. (Pubitemid 24364846)
34. Park E. J., Yoon J., Choi K., Yi J., and Park K. 2009. Induction of chronic infammation in mice treated with titanium dioxide nanoparticles by intratracheal instillation. Toxicology 260:37-46.
35. Renwick L. C., Brown D., Clouter A., and Donaldson K. 2004. Increased infammation and altered macrophage chemotactic responses caused by two ultrafne particle types. Occup. Environ. Med. 61:442-447. (Pubitemid 38655947)
36. Sager T. M., Kommineni C., and Castranova V. 2008. Pulmonary response to intratracheal instillation of ultrafne versus fne titanium dioxide: Role of particle surface area. Part. Fibre Toxicol. 5:17.
37. Sayes C. M., Wahi R., Kurian P. A., Liu Y., West J. L., Ausman K. D., Warheit D. B., and Colvin V. L. 2006. Correlating nanoscale titania structure with toxicity: A cytotoxicity and infammatory response study with human dermal fbroblasts and human lung epithelial cells. Toxicol. Sci. 92:174-185. (Pubitemid 43994876)
38. 2: Role of the specifc surface area and of surface methylation of the particles. Toxicol. Appl. Pharmacol. 222:141-151. (Pubitemid 47094873)
39. Törnqvist H., Mills N. L., Gonzalez M., Miller M. R., Robinson S. D., Megson I. L., Macnee W., Donaldson K., Söderberg S., Newby D. E., Sandström T., and Blomberg A. 2007. Persistent endothelial dysfunction in humans after diesel exhaust inhalation. Am. J. Respir. Crit. Care Med. 176:395-400. (Pubitemid 47267474)
40. Warheit D. B., Hansen J. F., Yuen I. S., Kelly D. P., Snajdr S. I., and Hartsky M. A. 1997. Inhalation of high concentrations of low toxicity dusts in rats results in impaired pulmonary clearance mechanisms and persistent infammation. Toxicol. Appl. Pharmacol. 145:10-22. (Pubitemid 27294765)
41. 2 particles: diferential responses related to surface properties. Toxicology 230:90-104. (Pubitemid 46073330)
42. 2 rods and dots in rats: toxicity is not dependent upon particle size and surface area. Toxicol. Sci. 91:227-236.