Anti-proliferative activity of silver nanoparticles

PV AshaRani; M Prakash Hande; Suresh Valiyaveettil

doi:10.1186/1471-2121-10-65

journal article Sep 17, 2009

Anti-proliferative activity of silver nanoparticles

PV AshaRani M Prakash Hande Suresh Valiyaveettil

BMC Cell Biology Vol. 10 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1186/1471-2121-10-65

Abstract

Abstract

Background
Nanoparticles possess exceptional physical and chemical properties which led to rapid commercialisation. Silver nanoparticles (Ag-np) are among the most commercialised nanoparticles due to their antimicrobial potential. Ag-np based cosmetics, therapeutic agents and household products are in wide use, which raised a public concern regarding their safety associated with human and environmental use. No safety regulations are in practice for the use of these nanomaterials. The interactions of nanomaterials with cells, uptake mechanisms, distribution, excretion, toxicological endpoints and mechanism of action remain unanswered.

Results
Normal human lung fibroblasts (IMR-90) and human glioblastoma cells (U251) were exposed to different doses of Ag-nps in vitro. Uptake of Ag-nps occurred mainly through endocytosis (clathrin mediated process and macropinocytosis), accompanied by a time dependent increase in exocytosis rate. The electron micrographs revealed a uniform intracellular distribution of Ag-np both in cytoplasm and nucleus. Ag-np treated cells exhibited chromosome instability and mitotic arrest in human cells. There was efficient recovery from arrest in normal human fibroblasts whereas the cancer cells ceased to proliferate. Toxicity of Ag-np is mediated through intracellular calcium (Ca2+) transients along with significant alterations in cell morphology and spreading and surface ruffling. Down regulation of major actin binding protein, filamin was observed after Ag-np exposure. Ag-np induced stress resulted in the up regulation of metallothionein and heme oxygenase -1 genes.

Conclusion
Here, we demonstrate that uptake of Ag-np occurs mainly through clathrin mediated endocytosis and macropinocytosis. Our results suggest that cancer cells are susceptible to damage with lack of recovery from Ag-np-induced stress. Ag-np is found to be acting through intracellular calcium transients and chromosomal aberrations, either directly or through activation of catabolic enzymes. The signalling cascades are believed to play key roles in cytoskeleton deformations and ultimately to inhibit cell proliferation.

Topics

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References

39

[1]

Percival SL, Bowler PG, Dolman J: Antimicrobial activity of silver-containing dressings on wound microorganisms using an in vitro biofilm model. Int Wound J. 2007, 4: 186-191. 10.1111/j.1742-481X.2007.00296.x. 10.1111/j.1742-481x.2007.00296.x

[2]

Yang P, Wei W, Tao C: Determination of trace thiocyanate with nano-silver coated multi-walled carbon nanotubes modified glassy carbon electrode. Anal Chim Acta. 2007, 585: 331-6. 10.1016/j.aca.2007.01.011. 10.1016/j.aca.2007.01.011

[3]

Kumar C: Nanomaterials- Toxicity, health and Environmental issues. 2006, Wiley- VCH Verlag GmbH & Co, Weinheim

[4]

Zhao Y, Nalwa H: Nanotoxicology - Interactions of Nanomaterials with Biological Systems. 2007, California, USA: American Scienfici Publishers

[5]

Elechiguerra JL, Burt JL, Morones JR, Camacho-Bragado A, Gao X, Lara HH, Yacaman MJ: Interaction of silver nanoparticles with HIV-1. J Nanobiotechnology. 2005, 3: 6-10.1186/1477-3155-3-6. 10.1186/1477-3155-3-6

[6]

Shahverdi AR, Fakhimi A, Shahverdi HR, Minaian S: Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli. Nanomedicine. 2007, 3: 168-71. 10.1016/j.nano.2007.02.001

[7]

Samuel U, Guggenbichler JP: Prevention of catheter-related infections: the potential of a new nano-silver impregnated catheter. Int J Antimicrob Agents. 2004, 23: S75-8. 10.1016/j.ijantimicag.2003.12.004. 10.1016/j.ijantimicag.2003.12.004

[8]

Yang HC, Pon LA: Toxicity of metal ions used in dental alloys: a study in the yeast Saccharomyces cerevisiae. Drug Chem Toxicol. 2003, 26: 75-85. 10.1081/DCT-120020403. 10.1081/dct-120020403

[9]

Hidalgo E, Dominguez C: Study of cytotoxicity mechanisms of silver nitrate in human dermal fibroblasts. Toxicol Lett. 1998, 98: 169-79. 10.1016/S0378-4274(98)00114-3. 10.1016/s0378-4274(98)00114-3

[10]

Naddy RB, Gorsuch JW, Rehner AB, McNerney GR, Bell RA, Kramer JR: Chronic toxicity of silver nitrate to Ceriodaphnia dubia and Daphnia magna, and potential mitigating factors. Aquat Toxicol. 2007, 84: 1-10. 10.1016/j.aquatox.2007.03.022. 10.1016/j.aquatox.2007.03.022

[11]

AshaRani PV, LianWu Y, Gong Z, Valiyaveettil S: Toxicity of silver nanoparticles in zebrafish models. Nanotechnology. 2008, 19: 255102-10.1088/0957-4484/19/25/255102. 10.1088/0957-4484/19/25/255102

[12]

Hussain SM, Hess KL, Gearhart JM, Geiss KT, Schlager JJ: In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol In Vitro. 2005, 19: 975-83. 10.1016/j.tiv.2005.06.034. 10.1016/j.tiv.2005.06.034

[13]

Skebo JE, Grabinski CM, Schrand AM, Schlager JJ, Hussain SM: Assessment of metal nanoparticle agglomeration, uptake, and interaction using high-illuminating system. Int J Toxicol. 2007, 26: 135-41. 10.1080/10915810701226248. 10.1080/10915810701226248

[14]

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: 177-82. 10.1016/j.jcis.2004.02.012. 10.1016/j.jcis.2004.02.012

[15]

Zheng J, Wu X, Wang M, Ran D, Xu W, Yang J: Study on the interaction between silver nanoparticles and nucleic acids in the presence of cetyltrimethylammonium bromide and its analytical application. Talanta. 2008, 74: 526-532. 10.1016/j.talanta.2007.06.014. 10.1016/j.talanta.2007.06.014

[16]

Pal S, Tak YK, Song JM: 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: 1712-20. 10.1128/AEM.02218-06. 10.1128/aem.02218-06

[17]

AshaRani PV, Low Kah MG, Hande MP, Valiyaveettil S: Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS nano. 2009, 3: 279-290. 10.1021/nn800596w. 10.1021/nn800596w

[18]

Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH: Antimicrobial effects of silver nanoparticles. Nanomedicine. 2007, 3: 95-101. 10.1016/j.nano.2006.12.001

[19]

Chithrani BD, Chan WC: Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett. 2007, 7: 1542-1550. 10.1021/nl070363y. 10.1021/nl070363y

[20]

Tsui MT, Wang WX: Biokinetics and tolerance development of toxic metals in Daphnia magna. Environ Toxicol Chem. 2007, 26: 1023-1032. 10.1897/06-430R.1. 10.1897/06-430r.1

[21]

Min KS: [Physiological significance of metallothionein in oxidative stress]. Yakugaku Zasshi. 2007, 127: 695-702. 10.1248/yakushi.127.695. 10.1248/yakushi.127.695

[22]

Woo S, Yum S, Jung JH, Shim WJ, Lee CH, Lee TK: Heavy metal-induced differential gene expression of metallothionein in Javanese medaka, Oryzias javanicus. Mar Biotechnol (NY). 2006, 8: 654-62. 10.1007/s10126-006-6046-0. 10.1007/s10126-006-6046-0

[23]

Clark JE, Foresti R, Green CJ, Motterlini R: Dynamics of haem oxygenase-1 expression and bilirubin production in cellular protection against oxidative stress. Biochem J. 2000, 384: 615-619. 10.1042/0264-6021:3480615. 10.1042/bj3480615

[24]

Elbirt KK, Bonkovsky HL: Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Physicians. 1999, 111: 438-47. 10.1111/paa.1999.111.5.438

[25]

Rahman MF, Wang J, Patterson TA, Saini UT, Robinson BL, Newport GD, Murdock RC, Schlager JJ, Hussain SM, Ali SF: Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol Lett. 2009, 187: 15-21. 10.1016/j.toxlet.2009.01.020. 10.1016/j.toxlet.2009.01.020

[26]

Wang JJ, Sanderson BJ, Wang H: Cyto- and genotoxicity of ultrafine TiO2 particles in cultured human lymphoblastoid cells. Mutat Res. 2007, 628: 99-106. 10.1016/j.mrgentox.2006.12.003

[27]

Lu PJ, Ho IC, Lee TC: Induction of sister chromatid exchanges and micronuclei by titanium dioxide in Chinese hamster ovary-K1 cells. Mutat Res. 1998, 414: 15-20. 10.1016/s1383-5718(98)00034-5

[28]

Mroz RM, Schins RP, Li H, Jimenez LA, Drost EM, Holownia A, MacNee W, Donaldson K: Nanoparticle-driven DNA damage mimics irradiation-related carcinogenesis pathways. Eur Respir J. 2008, 31: 241-251. 10.1183/09031936.00006707. 10.1183/09031936.00006707

[29]

Vevers WF, Jha AN: Genotoxic and cytotoxic potential of titanium dioxide (TiO2) nanoparticles on fish cells in vitro. Ecotoxicology. 2008, 17: 410-420. 10.1007/s10646-008-0226-9. 10.1007/s10646-008-0226-9

[30]

Chinopoulos C, Adam-Vizi V: Calcium, mitochondria and oxidative stress in neuronal pathology. Novel aspects of an enduring theme. Febs J. 2006, 273: 433-450. 10.1111/j.1742-4658.2005.05103.x. 10.1111/j.1742-4658.2005.05103.x

[31]

Moutin MJ, Abramson JJ, Salama G, Dupont Y: Rapid Ag+-induced release of Ca2+ from sarcoplasmic reticulum vesicles of skeletal muscle: a rapid filtration study. Biochim Biophys Acta. 1989, 984: 289-92. 10.1016/0005-2736(89)90295-2. 10.1016/0005-2736(89)90295-2

[32]

Orrenius S, Mccabe MJ, Nicotera P: Ca(2+)-dependent mechanisms of cytotoxicity and programmed cell death. Toxicol Lett. 1992, 64-65: 357-64. 10.1016/0378-4274(92)90208-2. 10.1016/0378-4274(92)90208-2

[33]

Belizario JE, Alves J, Occhiucci JM, Garay-Malpartida M, Sesso A: A mechanistic view of mitochondrial death decision pores. Braz J Med Biol Res. 2007, 40: 1011-24. 10.1590/S0100-879X2006005000109. 10.1590/s0100-879x2006005000109

[34]

Mikhutkina SV, Salmina AB, Sychev AV, Uspenskaya YA, Trufanova LV, Taksanova EI, Olovyannikova RY: Blebbing of thymocyte plasma membrane and apoptosis are related to impairment of capacitance Ca2+ entry into cells. Bull Exp Biol Med. 2004, 137: 551-5. 10.1023/B:BEBM.0000042709.57599.67. 10.1023/b:bebm.0000042709.57599.67

[35]

Cunningham CC, Gorlin JB, Kwiatkowski DJ, Hartwig JH, Janmey PA, Byers HR, Stossel TP: Actin-binding protein requirement for cortical stability and efficient locomotion. Science. 1992, 255: 325-7. 10.1126/science.1549777. 10.1126/science.1549777

[36]

New EJ, Parker D: The mechanism of cell uptake for luminescent lanthanide optical probes: the role of macropinocytosis and the effect of enhanced membrane permeability on compartmentalisation. Org Biomol Chem. 2009, 7: 851-855. 10.1039/b822145f. 10.1039/b822145f

[37]

Suksanpaisan L, Susantad T, Smith DR: Characterization of dengue virus entry into HepG2 cells. J Biomed Sci. 2009, 16: 17-10.1186/1423-0127-16-17. 10.1186/1423-0127-16-17

[38]

Low GK, Fok ED, Ting AP, Hande MP: Oxidative damage induced genotoxic effects in human fibroblasts from Xeroderma Pigmentosum group A patients. Int J Biochem Cell Biol. 2008, 40: 2583-2595. 10.1016/j.biocel.2008.05.009. 10.1016/j.biocel.2008.05.009

[39]

Hande MP, Samper E, Lansdorp P, Blasco MA: Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice. J Cell Biol. 1999, 144: 589-601. 10.1083/jcb.144.4.589. 10.1083/jcb.144.4.589

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Metrics

504

Citations

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References

Details

Published: Sep 17, 2009
Vol/Issue: 10(1)

Authors

Materials Research Laboratory (S5-05-02), Department of Chemistry, National University of Singapore, 3 Science Drive 3, 117543, Singapore

Cite This Article

PV AshaRani, M Prakash Hande, Suresh Valiyaveettil (2009). Anti-proliferative activity of silver nanoparticles. BMC Cell Biology, 10(1). https://doi.org/10.1186/1471-2121-10-65

Anti-proliferative activity of silver nanoparticles

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