Bioactivity of nanosilver in Caenorhabditis elegans: Effects of size, coat, and shape

Toxicology Reports

Volumn 1, Issue , 2014, Pages 923-944

  Hunt, Piper Reid ^a   Keltner, Zachary ^a   Gao, Xiugong ^a   Oldenburg, Steven J ^b   Bushana, Priyanka ^a   Olejnik, Nicholas ^a   Sprando, Robert L ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b NanoComposix Inc   (United States)

Author keywords

Alternative toxicity model; Growth assay; Ionic silver; Nanosilver; Physico chemical properties; Silver uptake

Indexed keywords

CITRIC ACID; MACROGOL; POLYETHYLENEIMINE; POVIDONE; SILVER NANOPARTICLE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION; GENE REGULATORY NETWORK; IMMUNE RESPONSE; LIGHT SCATTERING; MASS SPECTROMETRY; MICROARRAY ANALYSIS; MICROBIAL GROWTH; NONHUMAN; PARTICLE SIZE; TOXICITY TESTING; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROSCOPY; UPREGULATION; ZETA POTENTIAL;

EID: 84922738274     PISSN: 22147500     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxrep.2014.10.020     Document Type: Article

References (90)

1. Watson J.D., Crick F.H. Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 1953, 171(4356):737-738.
2. Abrahams J.P., Leslie A.G., et al. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 1994, 370(6491):621-628.
3. Dittman J., Ryan T.A. Molecular circuitry of endocytosis at nerve terminals. Annu. Rev. Cell Dev. Biol. 2009, 25:133-160.
4. McNeil S.E. Nanotechnology for the biologist. J. Leukoc. Biol. 2005, 78(3):585-594.
5. Chau C.-F., Wu S.-H., et al. The development of regulations for food nanotechnology. Trends Food Sci. Technol. 2007, 18(5):269-280.
6. Project-on-Emerging-Technologies Nanotechnology-based consumer products analysis. Consumer Products 2013, March 10, 2011, http://www.nanotechproject.org/inventories/consumer/analysis_draft/ (retrieved 22.10.13).
7. Xia T., Li N., et al. Potential health impact of nanoparticles. Annu. Rev. Public Health 2009, 30:137-150.
8. Sondi I., Salopek-Sondi B. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J. Colloid Interface Sci. 2004, 275(1):177-182.
9. Elechiguerra J.L., Burt J.L., et al. Interaction of silver nanoparticles with HIV-1. J. Nanobiotechnol. 2005, 3:6.
10. Lara H.H., Ayala-Nunez N.V., et al. Mode of antiviral action of silver nanoparticles against HIV-1. J. Nanobiotechnol. 2010, 8:1.
11. Martinez-Gutierrez F., Olive P.L., et al. Synthesis, characterization, and evaluation of antimicrobial and cytotoxic effect of silver and titanium nanoparticles. Nanomedicine 2010, 6(5):681-688.
12. Martinez-Gutierrez F., Thi E.P., et al. Antibacterial activity, inflammatory response, coagulation and cytotoxicity effects of silver nanoparticles. Nanomedicine 2012, 8(3):328-336.
13. Nowack B., Krug H.F., et al. 120 years of nanosilver history: implications for policy makers. Environ. Sci. Technol. 2011, 45(4):1177-1183.
14. Card J.W., Jonaitis T.S., et al. An appraisal of the published literature on the safety and toxicity of food-related nanomaterials. Crit. Rev. Toxicol. 2011, 41(1):22-49.
15. Kittler S., Greulich C., et al. Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chem. Mater. 2010, 22(16):4548-4554.
16. van der Zande M., Vandebriel R.J., et al. Distribution, elimination, and toxicity of silver nanoparticles and silver ions in rats after 28-day oral exposure. ACS Nano 2012, 6(8):7427-7442.
17. Morones J.R., Elechiguerra J.L., et al. The bactericidal effect of silver nanoparticles. Nanotechnology 2005, 16(10):2346-2353.
18. Kim K.-T., Truong L., et al. Silver nanoparticle toxicity in the embryonic zebrafish is governed by particle dispersion and ionic environment. Nanotechnology 2013, 24:1-8.
19. Park M.V., Neigh A.M., et al. The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. Biomaterials 2011, 32(36):9810-9817.
20. Homan K.A., Souza M., et al. Silver nanoplate contrast agents for in vivo molecular photoacoustic imaging. ACS Nano 2012, 6(1):641-650.
21. Pal S., Tak Y.K., et al. Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. Appl. Environ. Microbiol. 2007, 73(6):1712-1720.
22. George S., Lin S., et al. Surface defects on plate-shaped silver nanoparticles contribute to its hazard potential in a fish gill cell line and zebrafish embryos. ACS Nano 2012, 6(5):3745-3759.
23. Tolaymat T.M., El Badawy A.M., et al. An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: a systematic review and critical appraisal of peer-reviewed scientific papers. Sci. Total Environ. 2010, 408(5):999-1006.
24. El Badawy A.M., Luxton T.P., et al. Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions. Environ. Sci. Technol. 2010, 44(4):1260-1266.
25. 3 in branched polyethyleneimine/HEPES solutions. Langmuir 2007, 23(19):9836-9843.
26. 2 nanoparticles. Nanomedicine 2008, 4(3):226-236.
27. Eck W., Craig G., et al. PEGylated gold nanoparticles conjugated to monoclonal F19 antibodies as targeted labeling agents for human pancreatic carcinoma tissue. ACS Nano 2008, 2(11):2263-2272.
28. Dobrovolskaia M.A., McNeil S.E. Immunological properties of engineered nanomaterials. Nat. Nanotechnol. 2007, 2(8):469-478.
29. Costanza J., El Badawy A.M., et al. Comment on 120 Years of nanosilver history: implications for policy makers. Environ. Sci. Technol. 2011, 45(17):7591-7592. author reply 7593-7595.
30. Hunt P.R., Marquis B.J., et al. Nanosilver suppresses growth and induces oxidative damage to DNA in Caenorhabditis elegans. J. Appl. Toxicol. 2013, 33(10):1131-1142.
31. Oberdorster G. Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J. Intern. Med. 2010, 267(1):89-105.
32. Sayes C.M., Reed K.L., et al. Assessing toxicity of fine and nanoparticles: comparing in vitro measurements to in vivo pulmonary toxicity profiles. Toxicol. Sci. 2007, 97(1):163-180.
33. Betts K.S. Tox21 to date: steps toward modernizing human hazard characterization. Environ. Health Perspect. 2013, 121(7):a228.
34. Sprando R.L., Olejnik N., et al. A method to rank order water soluble compounds according to their toxicity using Caenorhabditis elegans, a complex object parametric analyzer and sorter, and axenic liquid media. Food Chem. Toxicol. 2009, 47(4):722-728.
35. Boyd W.A., McBride S.J., et al. A high-throughput method for assessing chemical toxicity using a Caenorhabditis elegans reproduction assay. Toxicol. Appl. Pharmacol. 2010, 245(2):153-159.
36. Hunt P.R., Olejnik N., et al. Toxicity ranking of heavy metals with screening method using adult Caenorhabditis elegans and propidium iodide replicates toxicity ranking in rat. Food Chem. Toxicol. 2012, 50(9):3280-3290.
37. nanoComposix Guidelines for Nanotoxicology Researchers Using nanoComposix Materials. v1.1 2012, September, http://cdn.shopify.com/s/files/1/0257/8237/files/nanoComposix_Guidelines_for_Nanotox_Researchers.pdf?13692 (retrieved 09.07.14).
38. Tong W., Cao X., et al. ArrayTrack - supporting toxicogenomic research at the U.S. Food and Drug Administration National Center for Toxicological Research. Environ. Health Perspect. 2003, 111(15):1819-1826.
39. Irizarry R.A., Hobbs B., et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4(2):249-264.
40. Hochreiter S., Clevert D.A., et al. A new summarization method for Affymetrix probe level data. Bioinformatics 2006, 22(8):943-949.
41. Kelly K.L., Coronado E., et al. The optical properties of metal nanoparticles: the influence of size, shape, and dielectric environment. J. Phys. Chem. B 2003, 107(3):668-677.
42. Hadrup N., Loeschner K., et al. Subacute oral toxicity investigation of nanoparticulate and ionic silver in rats. Arch. Toxicol. 2012, 86(4):543-551.
43. Pujol N., Zugasti O., et al. Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog. 2008, 4(7):e1000105.
44. WormBase (2014). (retrieved 30.05.14). http://www.wormbase.org/.
45. Friling R.S., Bensimon A., et al. Xenobiotic-inducible expression of murine glutathione S-transferase Ya subunit gene is controlled by an electrophile-responsive element. Proc. Natl. Acad. Sci. U. S. A. 1990, 87(16):6258-6262.
46. Fisher M.B., Paine M.F., et al. The role of hepatic and extrahepatic UDP-glucuronosyltransferases in human drug metabolism. Drug Metab. Rev. 2001, 33(3-4):273-297.
47. Huang da W., Sherman B.T., et al. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37(1):1-13.
48. Huang da W., Sherman B.T., et al. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4(1):44-57.
49. OMIM Online Mendelian Inheritance in Man 2014, http://omim.org (retrieved 30.05.14).
50. Google Scholar, 2014, http:scholar.google.com (retrieved 30.05.14).
51. O'Rourke D., Baban D., et al. Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res. 2006, 16(8):1005-1016.
52. Shapira M., Hamlin B.J., et al. A conserved role for a GATA transcription factor in regulating epithelial innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(38):14086-14091.
53. Troemel E.R., Chu S.W., et al. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2006, 2(11):e183.
54. Muir R.E., Tan M.W. Virulence of Leucobacter chromiireducens subsp. solipictus to Caenorhabditis elegans: characterization of a novel host-pathogen interaction. Appl. Environ. Microbiol. 2008, 74(13):4185-4198.
55. Pukkila-Worley R., Ausubel F.M., et al. Candida albicans infection of Caenorhabditis elegans induces antifungal immune defenses. PLoS Pathog. 2011, 7(6):e1002074.
56. Sahu S.N., Lewis J., et al. Genomic analysis of immune response against Vibrio cholerae hemolysin in Caenorhabditis elegans. PLoS ONE 2012, 7(5):e38200.
57. Wong D., Bazopoulou D., et al. Genome-wide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection. Genome Biol. 2007, 8(9):R194.
58. McElwee M.K., Ho L.A., et al. Comparative toxicogenomic responses of mercuric and methyl-mercury. BMC Genomics 2013, 14:698.
59. Roh J.-Y., Park S.-Y., et al. Cadmium toxicity monitoring using stress related gene expressions in Caenorhabditis elegans. Mol. Cell. Toxicol. 2006, 2(1):54-59.
60. Cui Y., McBride S.J., et al. Toxicogenomic analysis of Caenorhabditis elegans reveals novel genes and pathways involved in the resistance to cadmium toxicity. Genome Biol. 2007, 8(6):R122.
61. Sahu S.N., Lewis J., et al. Genomic analysis of stress response against arsenic in Caenorhabditis elegans. PLOS ONE 2013, 8(7):e66431.
62. Lewis J.A., Gehman E.A., et al. Alterations in gene expression in Caenorhabditis elegans associated with organophosphate pesticide intoxication and recovery. BMC Genomics 2013, 14:291.
63. Przybysz A.J., Choe K.P., et al. Increased age reduces DAF-16 and SKN-1 signaling and the hormetic response of Caenorhabditis elegans to the xenobiotic juglone. Mech. Ageing Dev. 2009, 130(6):357-369.
64. Shin H., Lee H., et al. Gene expression profiling of oxidative stress response of C. elegans aging defective AMPK mutants using massively parallel transcriptome sequencing. BMC Res. Notes 2011, 4:34.
65. Dawe A.S., Bodhicharla R.K., et al. Low-intensity microwave irradiation does not substantially alter gene expression in late larval and adult Caenorhabditis elegans. Bioelectromagnetics 2009, 30(8):602-612.
66. Kwon J.Y., Hong M., et al. Ethanol-response genes and their regulation analyzed by a microarray and comparative genomic approach in the nematode Caenorhabditis elegans. Genomics 2004, 83(4):600-614.
67. Roh J.Y., Jung I.H., et al. Toxic effects of di(2-ethylhexyl)phthalate on mortality, growth, reproduction and stress-related gene expression in the soil nematode Caenorhabditis elegans. Toxicology 2007, 237(1-3):126-133.
68. Lewis J.A., Szilagyi M., et al. Distinct patterns of gene and protein expression elicited by organophosphorus pesticides in Caenorhabditis elegans. BMC Genomics 2009, 10:202.
69. Vinuela A., Snoek L.B., et al. Genome-wide gene expression analysis in response to organophosphorus pesticide chlorpyrifos and diazinon in C. elegans. PLoS ONE 2010, 5(8):e12145.
70. Reichert K., Menzel R. Expression profiling of five different xenobiotics using a Caenorhabditis elegans whole genome microarray. Chemosphere 2005, 61(2):229-237.
71. Hasegawa K., Miwa S., et al. Acrylamide-responsive genes in the nematode Caenorhabditis elegans. Toxicol. Sci. 2008, 101(2):215-225.
72. Lee S.J., Murphy C.T., et al. Glucose shortens the life span of C. elegans by downregulating DAF-16/FOXO activity and aquaporin gene expression. Cell Metab. 2009, 10(5):379-391.
73. Schwerdt C.E., Schaffer F.L. Some physical and chemical properties of purified poliomyelitis virus preparations. Ann. N. Y. Acad. Sci. 1955, 61(4):740-750. discussion 750-743.
74. Stuart D.C. Virology 1961, 13(2):177-190.
75. Wallis C., Melnick J.L. Virus aggregation as the cause of the non-neutralizable persistent fraction. J. Virol. 1967, 1(3):478-488.
76. Fifis T., Gamvrellis A., et al. Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. J. Immunol. 2004, 173(5):3148-3154.
77. Matuk Y., Ghosh M., et al. Distribution of silver in the eyes and plasma proteins of the albino rat. Can. J. Ophthalmol. 1981, 16(3):145-150.
78. Kim Y.S., Song M.Y., et al. Subchronic oral toxicity of silver nanoparticles. Part. Fibre Toxicol. 2010, 7:20.
79. Loeschner K., Hadrup N., et al. Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part. Fibre Toxicol. 2011, 8:18.
80. Park E.J., Bae E., et al. Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ. Toxicol. Pharmacol. 2010, 30(2):162-168.
81. Roh J.Y., Sim S.J., et al. Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics. Environ. Sci. Technol. 2009, 43(10):3933-3940.
82. Sifri C.D., Begun J., et al. The worm has turned - microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol. 2005, 13(3):119-127.
83. Irazoqui J.E., Ng A., et al. Role for beta-catenin and HOX transcription factors in Caenorhabditis elegans and mammalian host epithelial-pathogen interactions. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(45):17469-17474.
84. De Jong W.H., Van Der Ven L.T., et al. Systemic and immunotoxicity of silver nanoparticles in an intravenous 28 days repeated dose toxicity study in rats. Biomaterials 2013, 34(33):8333-8343.
85. Harper S.L., Carriere J.L., et al. Systematic evaluation of nanomaterial toxicity: utility of standardized materials and rapid assays. ACS Nano 2011, 5(6):4688-4697.
86. Goodman C.M., McCusker C.D., et al. Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjug. Chem. 2004, 15(4):897-900.
87. He C., Hu Y., et al. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 2010, 31(13):3657-3666.
88. Verma A., Stellacci F. Effect of surface properties on nanoparticle-cell interactions. Small 2010, 6(1):12-21.
89. Lee O., Jeong S.H., et al. Influence of surface charge of gold nanorods on skin penetration. Skin Res. Technol. 2013, 19(1):e390-e396.
90. McGhee J.D. The C. elegans intestine. WormBook 2007, The C. elegans Research Community. 10.1895/wormbook.1.133.1.