Effects of subchronic exposure of silver nanoparticles on intestinal microbiota and gut-associated immune responses in the ileum of Sprague-Dawley rats

Nanotoxicology

Volumn 9, Issue 3, 2015, Pages 279-289

  Williams, Katherine ^a   Milner, Jessica ^a   Boudreau, Mary D ^a   Gokulan, Kuppan ^a   Cerniglia, Carl E ^a   Khare, Sangeeta ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Bacteria; Microbiome; Mucosal immunity

Indexed keywords

ANTIBIOTIC AGENT; CASPASE RECRUITMENT DOMAIN PROTEIN 15; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 43; INTERLEUKIN 10; MUCIN 2; MUCIN 3; SILVER ACETATE; SILVER NANOPARTICLE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; METAL NANOPARTICLE; SILVER;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIUM IDENTIFICATION; BACTEROIDES; BACTEROIDETES; BIFIDOBACTERIUM; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; ENTEROBACTERIACEAE; ESCHERICHIA COLI; FEMALE; FIRMICUTES; GENE EXPRESSION; IMMUNE RESPONSE; INTESTINE FLORA; INTESTINE FUNCTION; KLEBSIELLA; LACTOBACILLUS; LONG TERM EXPOSURE; MALE; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA; SHIGELLA; SPRAGUE DAWLEY RAT; YERSINIA PESTIS; ANIMAL; CHEMISTRY; DRUG EFFECTS; ILEUM; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA;

FIRMICUTES; LACTOBACILLUS; NEGIBACTERIA; RATTUS;

ANIMALS; FEMALE; GENE EXPRESSION; ILEUM; MALE; METAL NANOPARTICLES; MICROBIOTA; RATS; RATS, SPRAGUE-DAWLEY; SILVER;

EID: 84929675174     PISSN: 17435390     EISSN: 17435404     Source Type: Journal    
DOI: 10.3109/17435390.2014.921346     Document Type: Article

References (39)

1. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Hostbacterial mutualism in the human intestine. Science 307:1915-20.
2. Beer C, Foldbjerg R, Hayashi Y, Sutherland DS, Autrup H. 2012. Toxicity of silver nanoparticles-nanoparticle or silver ion? Toxicol Lett 208: 286-92.
3. Boczkowski J, Hoet P. 2010. What's new in nanotoxicology? Implications for public health from a brief review of the 2008 literature. Nanotoxicology 4:1-14.
4. Bugla-Ploskonska G, Leszkiewicz A, Borak B, Jasiorski M, Drulis-Kawa Z, Baszczuk A, et al. 2007. Bactericidal properties of silica particles with silver islands located on the surface. Int J Antimicrob Agents 29: 746-8.
5. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. 2005. Diversity of the human intestinal microbial flora. Science 308:1635-8.
6. Genter MB, Newman NC, Shertzer HG, Ali SF, Bolon B. 2012. Distribution and systemic effects of intranasally administered 25 nm silver nanoparticles in adult mice. Toxicol Pathol 40:1004-13.
7. Goodman AL, Mcnulty NP, Zhao Y, Leip D, Mitra RD, Lozupone CA, et al. 2009. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6:279-89.
8. Hadrup N, Lam HR. 2014. Oral toxicity of silver ions, silver nanoparticles and colloidal silver-a review. Regul Toxicol Pharmacol 68:1-7.
9. Ikeda H, Sasaki M, Ishikawa A, Sato Y, Harada K, Zen Y, et al. 2007. Interaction of Toll-like receptors with bacterial components induces expression of CDX2 and MUC2 in rat biliary epithelium in vivo and in culture. Lab Invest 87:559-71.
10. Isaacson R, Kim HB. 2012. The intestinal microbiome of the pig. Anim Health Res Rev 13:100-9.
11. Ishikawa E, Matsuki T, Kubota H, Makino H, Sakai T, Oishi K, et al. 2013. Ethnic diversity of gut microbiota: species characterization of Bacteroides fragilis group and genus Bifidobacterium in healthy Belgian adults, and comparison with data from Japanese subjects. J Biosci Bioeng 116:265-70.
12. Khare S, Ficht TA, Santos RL, Romano J, Ficht AR, Zhang S, et al. 2004. Rapid and sensitive detection of Mycobacterium avium subsp. paratuberculosis in bovine milk and feces by a combination of immunomagnetic bead separation-conventional PCR and real-time PCR. J Clin Microbiol 42:1075-81.
13. Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, et al. 2008. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague-Dawley rats. Inhal Toxicol 20:575-83.
14. Lee JH, Kim YS, Song KS, Ryu HR, Sung JH, Park JD, et al. 2013. Biopersistence of silver nanoparticles in tissues from Sprague-Dawley rats. Part Fibre Toxicol 10:36-49.
15. Li J, Rong K, Zhao H, Li F, Lu Z, Chen R. 2013. Highly selective antibacterial activities of silver nanoparticles against Bacillus subtilis. J Nanosci Nanotechnol 13:6806-13.
16. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-8.
17. Loeschner K, Hadrup N, Qvortrup K, Larsen A, Gao X, Vogel U, et al. 2011. Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part Fibre Toxicol 8:18-31.
18. Macia L, Thorburn AN, Binge LC, Marino E, Rogers KE, Maslowski KM, et al. 2012. Microbial influences on epithelial integrity and immune function as a basis for inflammatory diseases. Immunol Rev 245:164-76.
19. Mariat D, Firmesse O, Levenez F, Guimaraes V, Sokol H, Dore J, et al. 2009. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9:123.
20. Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, et al. 2013. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339: 1084-8.
21. Mcguckin MA, Lindén SK, Sutton P, Florin TH. 2011. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265-78.
22. Merrifield DL, Shaw BJ, Harper GM, Saoud IP, Davies SJ, Handy RD, Henry TB. 2013. Ingestion of metal-nanoparticle contaminated food disrupts endogenous microbiota in zebrafish (Danio rerio). Environ Pollut 174:157-63.
23. NTP. 2002. TER20001. Final study report on the developmental toxicity evaluation for silver acetate (CAS No. 563-63-3) administered by gavage to Sprague Dawley (CDR) rats on gestational days 6-19.
24. In: Price CJ, George JD, eds. NTIS #PB2002-109208. Springfield, Virginia: National Technical Information Services. Available from: http://ntp.niehs.nih.gov/index.cfmobjectid=072FB691-B130-5E1A-3FF5EE8FEEAE9329#.U3PimVe9HuE [last accessed 21 May 2014].
25. Petnicki-Ocwieja T, Hrncir T, Liu YJ, Biswas A, Hudcovic T, Tlaskalova-Hogenova H, Kobayashi KS. 2009. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci USA 106:15813-18.
26. Powell JJ, Faria N, Thomas-Mckay E, Pele LC. 2010. Origin and fate of dietary nanoparticles and microparticles in the gastrointestinal tract. J Autoimmun 34:J226-33.
27. Powers KW, Brown SC, Krishna VB, Wasdo SC, Moudgil BM, Roberts SM. 2006. Research strategies for safety evaluation of nanomaterials. Part VI. Characterization of nanoscale particles for toxicological evaluation. Toxicol Sci 90:296-303.
28. Reikvam DH, Erofeev A, Sandvik A, Grcic V, Jahnsen FL, Gaustad P, et al. 2011. Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. PLoS One 6: e17996.
29. Robles Alonso V, Guarner F. 2013. Linking the gut microbiota to human health. Br J Nutr 109(Suppl 2):S21-6.
30. Sawosz E, Binek M, Grodzik M, Zielinska M, Sysa P, Szmidt M, et al. 2007. Influence of hydrocolloidal silver nanoparticles on gastrointestinal microflora and morphology of enterocytes of quails. Arch Anim Nutr 61:444-51.
31. Sharma VK, Siskova KM, Zboril R, Gardea-Torresdey JL. 2014. Organic-coated silver nanoparticles in biological and environmental conditions: fate, stability and toxicity. Adv Colloid Interface Sci 204: 15-34.
32. Silver S. 2003. Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341-53.
33. Sintubin L, De Gusseme B, Van der Meeren P, Pycke BF, Verstraete W, Boon N. 2011. The antibacterial activity of biogenic silver and its mode of action. Appl Microbiol Biotechnol 91:153-62.
34. Tang J, Xiong L, Wang S, Wang J, Liu L, Li J, et al. 2009. Distribution, translocation and accumulation of silver nanoparticles in rats. J Nanosci Nanotechnol 9:4924-32.
35. Van der Zande M, Vandebriel RJ, Van Doren E, Kramer E, Herrera Rivera Z, Serrano-Rojero CS, et al. 2012. Distribution, elimination, and toxicity of silver nanoparticles and silver ions in rats after 28-day oral exposure. ACS Nano 6:7427-42.
36. Wang JH, Doyle M, Manning BJ, Di Wu Q, Blankson S, Redmond HP. 2002. Induction of bacterial lipoprotein tolerance is associated with suppression of toll-like receptor 2 expression. J Biol Chem 277: 36068-75.
37. Winter SE, Lopez CA, Baumler AJ. 2013. The dynamics of gutassociated microbial communities during inflammation. EMBO Rep 14:319-27.
38. Xue Y, Zhang S, Huang Y, Zhang T, Liu X, Hu Y, et al. 2012. Acute toxic effects and gender-related biokinetics of silver nanoparticles following an intravenous injection in mice. J Appl Toxicol 32:890-9.
39. Zhang H, Dibaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, et al. 2009. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 106:2365-70.