ZnO nanoparticles induced adjuvant effect via toll-like receptors and Src signaling in Balb/c mice

Toxicology Letters

Volumn 230, Issue 3, 2014, Pages 421-433

  Roy, Ruchi ^a,b   Kumar, Dinesh ^a   Sharma, Akanksha ^a,b   Gupta, Parul ^a   Chaudhari, Bhushan P ^a   Tripathi, Anurag ^a   Das, Mukul ^a,b   Dwivedi, Premendra D ^a,b  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

^b ACADEMY OF SCIENTIFIC AND INNOVATIVE RESEARCH ACSIR   (India)

Author keywords

Adjuvant; Src signaling; Toll like receptors; Zinc oxide nanoparticles

Indexed keywords

CYCLOOXYGENASE 2; GELATINASE B; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; OVALBUMIN; PROSTAGLANDIN E2; PROTEIN TYROSINE KINASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; ZINC OXIDE NANOPARTICLE; ICAM1 PROTEIN, MOUSE; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; IRAK1 PROTEIN, MOUSE; LYN PROTEIN-TYROSINE KINASE; MYD88 PROTEIN, MOUSE; NANOPARTICLE; PTGS2 PROTEIN, MOUSE; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TLR6 PROTEIN, MOUSE; TOLL LIKE RECEPTOR; ZINC OXIDE;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFECT; FEMALE; GENE EXPRESSION; HOUSEKEEPING GENE; MACROPHAGE; MORPHOMETRICS; MOUSE; NONHUMAN; PEYER PATCH; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECONDARY IMMUNE RESPONSE; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; DRUG EFFECTS; IMMUNOLOGY; INFLAMMATION; INTESTINE; METABOLISM;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CASPASE 1; CYCLOOXYGENASE 2; FEMALE; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-1BETA; INTESTINES; MACROPHAGES; MICE; MICE, INBRED BALB C; MYELOID DIFFERENTIATION FACTOR 88; NANOPARTICLES; OVALBUMIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TNF RECEPTOR-ASSOCIATED FACTOR 6; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 6; TOLL-LIKE RECEPTORS; ZINC OXIDE;

EID: 84910071417     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.08.008     Document Type: Article

References (57)

1. Aydin Sevinc B., Hanley L. Antibacterial activity of dental composites containing zinc oxide nanoparticles. J. Biomed. Mater. Res. B Appl. Biomater. 2010, 94:22-31.
2. Barton G.M., Kagan J.C. A cell biological view of toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 2009, 9:535-542.
3. Boggon T.J., Eck M.J. Structure and regulation of Src family kinases. Oncogene 2004, 23:7918-7927.
4. Bondarenko O., Juganson K., Ivask A., Kasemets K., Mortimer M., Kahru A. Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch. Toxicol. 2013, 87:1181-1200.
5. Byeon S.E., Yi Y.S., Oh J., Yoo B.C., Hong S., Cho J.Y. The role of Src kinase in macrophage-mediated inflammatory responses. Mediators Inflamm. 2012, 2012:512926.
6. Chang C. The immune effects of naturally occurring and synthetic nanoparticles. J. Autoimmun. 2010, 34:J234-J246.
7. Collins T. Endothelial nuclear factor-κ B and the initiation of the atherosclerotic lesion. Lab. Invest. 1993, 68:499-508.
8. Da Silva C.A., Pochard P., Lee C.G., Elias J.A. Chitin particles are multifaceted immune adjuvants. Am. J. Respir. Crit. Care Med. 2010, 182:1482-1491.
9. Fabricius D., Neubauer M., Mandel B., Schütz C., Viardot A., Vollmer A., Jahrsdörfer B., Debatin K.M. Prostaglandin E2 inhibits IFN-alpha secretion and Th1 costimulation by human plasmacytoid dendritic cells via E-prostanoid 2 and E-prostanoid 4 receptor engagement. J. Immunol. 2010, 184:677-684.
10. Diaz-Sanchez D., Tsien A., Fleming J., Saxon A. Combined diesel exhaust particulate and ragweed allergen challenge markedly enhances in vivo nasal ragweed-specific IgE and shows cytokine production to a Th2-type pattern. J. Immunol. 1997, 158:2406.
11. Fujimaki H., Saneyoshi K., Shiraishi F., Imai T., Endo T. Inhalation of diesel exhaust enhances antigen-specific IgE antibody production in mice. Toxicology 1997, 116:227.
12. Geiser M., Kreyling W.G. Deposition and biokinetics of inhaled nanoparticles. Part. Fibre Toxicol. 2010, 7:2.
13. Glass C.K., Witztum J.L. Atherosclerosis. The road ahead. Cell 2001, 104:503-516.
14. Grandoch M., Roscioni S.S., Schmidt M. The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br. J. Pharmacol. 2010, 159:265-284.
15. He L., Liu Y., Mustapha A., Lin M. Antifungal activity of zinc oxide nanoparticles against Botrytis cinerea and Penicillium expansum. Microbiol. Res. 2011, 166:207-215.
16. Houslay M.D. Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem. Sci. 2010, 35:91-100.
17. Ichinose T., Takano H., Miyabara Y., Yanagisawa R., Sagai M. Murine strain differences in allergic airway inflammation and immunoglobulin production by a combination of antigen and diesel exhaust particles. Toxicology 1997, 122:183-192.
18. Ingley E., Schneider J.R., Payne C.J., McCarthy D.J., Harder K.W., Hibbs M.L., Klinken S.P. Csk-binding protein mediates sequential enzymatic down-regulation and degradation of Lyn in erythropoietin-stimulated cells. J. Biol. Chem. 2006, 281:31920-31929.
19. Kim S.R., Rhee Y.K. Overlap between asthma and COPD: where the two diseases converge. Allergy Asthma Immunol. Res. 2010, 2:209-214.
20. Kim M.H., Seo J.H., Kim H.M., Jeong H.J. Zinc oxide nanoparticles, a novel candidate for the treatment of allergic inflammatory diseases. Eur. J. Pharmacol. 2014, 738:31-39.
21. Koga K., Takaesu G., Yoshida R., Nakaya M., Kobayashi T., Kinjyo I., Yoshimura A. Cyclic adenosine monophosphate suppresses the transcription of proinflammatory cytokines via the phosphorylated c-Fos protein. Immunity 2009, 30:372-383.
22. Kool M., Willart M.A., van Nimwegen M., Bergen I., Pouliot P., Virchow J.C., Rogers N., Osorio F., Reis e Sousa C., Hammad H., Lambrecht B.N. An unexpected role for uric acid as an inducer of T helper 2 cell immunity to inhaled antigens and inflammatory mediator of allergic asthma. Immunity 2011, 34:527-540.
23. Kuroda E., Coban C., Ishii K.J. Particulate adjuvant and innate immunity: past achievements, present findings, and future prospects. Int. Rev. Immunol. 2013, 32:209-220.
24. Kuroda E., Ishii K.J., Uematsu S., Ohata K., Coban C., Akira S., Aritake K., Urade Y., Morimoto Y. Silica crystals and aluminum salts regulate the production of prostaglandin in macrophages via NALP3 inflammasome-independent mechanisms. Immunity 2011, 34:514-526.
25. Kuroda E., Yamashita U. Mechanisms of enhanced macrophage-mediated prostaglandin E2 production and its suppressive role in Th1 activation in Th2-dominant BALB/c mice. J. Immunol. 2003, 170:757-764.
26. Lee S., Yun H.-S., Kim S.-H. The comparative effects of mesoporous silica nanoparticles and colloidal silica on inflammation and apoptosis. Biomaterials 2011, 32:9434-9443.
27. Li N., Harkema J.R., Lewandowski R.P., Wang M., Bramble L.A., Gookin G.R., Ning Z., Kleinman M.T., Sioutas C., Nel E. Ambient ultrafine particles provide a strong adjuvant effect in the secondary immune response: implication for traffic-related asthma flares. Am. J. Physiol. Lung Cell. Mol. Physiol. 2010, 299(3):L374-L383.
28. Lipovsky A., Nitzan Y., Gedanken A., Lubart R. Antifungal activity of ZnO nanoparticles - the role of ROS mediated cell injury. Nanotechnology 2011, 22:105101.
29. Løvik M., Høgseth A.K., Gaarder P.I., Hagemann R., Eide I. Diesel exhaust particles and carbon black have adjuvant activity on the local lymph node response and systemic IgE production to ovalbumin. Toxicology 1997, 121:165-178.
30. Majori M., Vachier I., Godard P., Farce M., Bousquet J., Chanez P. Superoxide anion production by monocytes of corticosteroid-treated asthmatic patients. Eur. Respir. J. 1998, 11:133.
31. Matsumura M., Nagata M., Nakamura K., Kawai M., Baba T., Yamaki K., Yoshino S. Adjuvant effect of zinc oxide on Th2 but not Th1 immune responses in mice. Immunopharmacol. Immunotoxicol. 2010, 32:56-62.
32. 2) at rest or in lungs primed with lipopolysaccharide. J. Toxicol. Environ. Health 2010, 73:396-409. A.
33. Nohynek G.J., Dufour E.K., Roberts M.S. Nanotechnology, cosmetics and the skin: is there a health risk?. Skin Pharmacol. Physiol. 2008, 21:136-149.
34. O'Neill L.A. When signaling pathways collide: positive and negative regulation of toll-like receptor signal transduction. Immunity 2008, 29:12-20.
35. Ohta K., Yamashita N., Tajima M., Miyasaka T., Nakano J., Nakajima M., Ishii A., Horiuchi T., Mano K., Miyamoto T. Diesel exhaust particulate induces airway hyperresponsiveness in a murine model: essential role of GM-CSF. J. Allergy Clin. Immunol. 1999, 104:1024.
36. + T cells. J. Immunol. 1997, 159:591-598.
37. Park J., Lim D.-H Lim H.-J., Kwon T., Choi J.-S., Jeong S., Choi I.-H., Cheon J. Size dependent macrophage responses and toxicological effects of Ag nanoparticles. Chem. Commun. 2011, 47:4382-4384.
38. Parker C.W., Smith J.W. Alterations in cyclic adenosine monophosphate metabolism in human bronchial asthma. Leukocyte responsiveness to -adrenergic agents. J. Clin. Invest. 1973, 52:48-59.
39. Pavlovic S., Du B., Sakamoto K., Khan K.M., Natarajan C., Breyer R.M., Dannenberg A.J., Falcone D.J. Targeting prostaglandin E2 receptors as an alternative strategy to block cyclooxygenase-2-dependent extracellular matrix-induced matrix metalloproteinase-9 expression by macrophages. J. Biol. Chem. 2006, 281:3321-3328.
40. Petrilli V., Dostert C., Mayor A., Martinon F., Tschopp J. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Diff. 2007, 14:1583-1589.
41. Price N.M., Gilman R.H., Uddin J., Recavarren S., Friedland J.S. Unopposed matrix metalloproteinase-9 expression in human tuberculous granuloma and the role of TNF-alpha-dependent monocyte networks. J. Immunol. 2003, 171:5579-5586.
42. Reed S.G., Pihl D.L., Conlon P.J., Grabstein K.H. IL-1 as adjuvant: role of T cells in the augmentation of specific antibody production by recombinant human IL-1α. J. Immunol. 1989, 142:3129-3133.
43. Roy R., Kumar S., Verma A.K., Sharma A., Chaudhari B.P., Tripathi A., Das M., Dwivedi P.D. Zinc oxide nanoparticles provide an adjuvant effect to ovalbumin via Th2 response in Balb/c mice. Int. Immunol. 2014, 26:159-172.
44. Roy R., Parashar V., Chauhan L.K., Shanker R., Das M., Tripathi A., Dwivedi P.D. Mechanism of uptake of ZnO nanoparticles and inflammatory responses in macrophages require PI3K mediated MAPKs signaling. Toxicol. In Vitro 2014, 28:457-467.
45. Roy R., Singh S.K., Das M., Tripathi A., Dwivedi P.D. Toll-like receptor 6 mediated inflammatory and functional responses of zinc oxide nanoparticles primed macrophages. Immunology 2014, 10.1111/imm.12276.
46. Schipper M.L., Cheng Z., Bentolila Lee S., Iyer L.A., G Rao J., Chen X., Wu A.M., Weiss S., Gambhir S.S. microPET-based biodistribution of quantum dots in living mice. J. Nucl. Med. 2007, 48:1511-1518.
47. Shi Y., Mucsi A.D., Ng G. Monosodium urate crystals in inflammation and immunity. Immunol. Rev. 2010, 233:203-217.
48. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
49. Tsou T.C., Yeh C., Tsai F.Y., Lin J., Cheng T.J., Chao H.R., Tai A. Zinc oxide particles induce inflammatory responses in vascular endothelial cells via NF-kappaB signaling. J. Hazard. Mater. 2010, 183:182-188.
50. Tsou T.C., Liou S.H., Yeh S.C., Tsai F.Y., Chao H.R. Crucial role of Toll-like receptors in the zinc/nickel-induced inflammatory response in vascular endothelial cells. Toxicol. Appl. Pharmacol 2013, 273:492-499.
51. Tripathy N., Hong T.-K., Ha K.-T., Jeong H.-S., Hahn Y.-B. Effect of ZnO nanoparticles aggregation on the toxicity in RAW 264.7 murine macrophage. J. Hazard. Mater. 2014, 270:110-117.
52. Uematsu S., Matsumoto M., Takeda K., Akira S. Lipopolysaccharide-dependent prostaglandin E(2) production is regulated by the glutathione-dependent prostaglandin E(2) synthase gene induced by the toll-like receptor 4/MyD88/NF-IL6 pathway. J. Immunol. 2002, 168:5811-5816.
53. Vargas L., Patino P.J., Montoya F., Vanegas A.C., Echavarria A., Garcia de Olarte D. A study of granulocyte respiratory burst in patients with allergic bronchial asthma. Inflammation 1998, 22:45.
54. Whitekus M.J., Li N., Zhang M., Wang M., Horwitz M.A., Nelson S.K., Horwitz L.D., Brechun N., Diaz-Sanchez D., Nel E. Thiol antioxidants inhibit the adjuvant effects of aerosolized diesel exhaust particles in a murine model for ovalbumin sensitization. J. Immunol. 2002, 168:2560-2567.
55. Wilhelmi V., Fischer U., Weighardt H., Schulze-Osthoff K., Nickel C., Stahlmecke B., Kuhlbusch T.A., Scherbart A.M., Esser C., Schins R.P., Albrecht C. Zinc oxide nanoparticles induce necrosis and apoptosis in macrophages in a p47phox- and Nrf2-independent manner. PLoS One 2013, 8:e65704.
56. Xu Y., Tang H., J- H., Wang H., Liu Y. Evaluation of the adjuvant effect of silver nanoparticles both in vitro and in vivo. Tox. Lett. 2013, 219:42-48.
57. Yang L., Froio R.M., Sciuto T.E., Dvorak A.M., Alon R., Luscinskas F.W. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-α-activated vascular endothelium under flow. Blood 2005, 106:584-592.