Mechanism of antibacterial activity of copper nanoparticles

In a previous communication, we reported a new method of synthesis of stable metallic copper nanoparticles (Cu-NPs), which had high potency for bacterial cell filamentation and cell killing. The present study deals with the mechanism of filament formation and antibacterial roles of Cu-NPs in E. coli cells. Our results demonstrate that NP-mediated dissipation of cell membrane potential was the probable reason for the formation of cell filaments. On the other hand, Cu-NPs were found to cause multiple toxic effects such as generation of reactive oxygen species, lipid peroxidation, protein oxidation and DNA degradation in E. coli cells. In vitro interaction between plasmid pUC19 DNA and Cu-NPs showed that the degradation of DNA was highly inhibited in the presence of the divalent metal ion chelator EDTA, which indicated a positive role of Cu(2+) ions in the degradation process. Moreover, the fast destabilization, i.e. the reduction in size, of NPs in the presence of EDTA led us to propose that the nascent Cu ions liberated from the NP surface were responsible for higher reactivity of the Cu-NPs than the equivalent amount of its precursor CuCl2; the nascent ions were generated from the oxidation of metallic NPs when they were in the vicinity of agents, namely cells, biomolecules or medium components, to be reduced simultaneously.

[1]  B. Ninham,et al.  Synthesis of Copper Nanosize Particles in Anionic Reverse Micelles: Effect of the Addition of a Cationic Surfactant on the Size of the Crystallites , 1995 .

[2]  O. A. Bogoslovskaya,et al.  Wound-healing properties of copper nanoparticles as a function of physicochemical parameters , 2010 .

[3]  K. Zavitz,et al.  Inactivation of the Escherichia coli priA DNA replication protein induces the SOS response , 1991, Journal of bacteriology.

[4]  Chi-Ming Che,et al.  Proteomic analysis of the mode of antibacterial action of silver nanoparticles. , 2006, Journal of proteome research.

[5]  E. Bi,et al.  FtsZ ring structure associated with division in Escherichia coli , 1991, Nature.

[6]  S. Haram,et al.  Synthesis and Characterization of Copper Sulfide Nanoparticles in Triton-X 100 Water-in-Oil Microemulsions , 1996 .

[7]  Zhiqiang Hu,et al.  Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. , 2008, Environmental science & technology.

[8]  R. Fischer,et al.  A non-aqueous organometallic route to highly monodispersed copper nanoparticles using [Cu(OCH(Me)CH2NMe2)2]. , 2002, Chemical communications.

[9]  G. Walker,et al.  The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. , 2000, Annual review of genetics.

[10]  K. Feris,et al.  Selective toxicity of zinc oxide nanoparticles to prokaryotic and eukaryotic systems. , 2007, Applied physics letters.

[11]  I. Sondi,et al.  Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. , 2004, Journal of colloid and interface science.

[12]  Wei Jiang,et al.  Bacterial toxicity comparison between nano- and micro-scaled oxide particles. , 2009, Environmental pollution.

[13]  Thomas J Webster,et al.  Bactericidal effect of iron oxide nanoparticles on Staphylococcus aureus , 2010, International journal of nanomedicine.

[14]  E. Stadtman,et al.  Protein Oxidation in Aging, Disease, and Oxidative Stress* , 1997, The Journal of Biological Chemistry.

[15]  Mechanism of protonophores-mediated induction of heat-shock response in Escherichia coli , 2009, BMC Microbiology.

[16]  W. Stark,et al.  Large-scale production of carbon-coated copper nanoparticles for sensor applications , 2006, Nanotechnology.

[17]  V. Iyer,et al.  Radiation induced synthesis and characterization of copper nanoparticles , 1998 .

[18]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[19]  J. Lutkenhaus,et al.  Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Mark R Wiesner,et al.  Effect of a fullerene water suspension on bacterial phospholipids and membrane phase behavior. , 2007, Environmental science & technology.

[21]  Y. Kang,et al.  Synthesis of oleate capped Cu nanoparticles by thermal decomposition , 2006 .

[22]  G. Bertani,et al.  HOST CONTROLLED VARIATION IN BACTERIAL VIRUSES , 1953, Journal of bacteriology.

[23]  J. Courcelle,et al.  Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. , 2001, Genetics.

[24]  Jeen-Woo Park,et al.  Control of singlet oxygen-induced oxidative damage in Escherichia coli. , 2002, Journal of biochemistry and molecular biology.

[25]  L. Kotra,et al.  High-Resolution Atomic Force Microscopy Studies of the Escherichia coli Outer Membrane: Structural Basis for Permeability , 2000 .

[26]  C. Swenberg,et al.  Differences in unwinding of supercoiled DNA induced by the two enantiomers of anti-benzo[a]pyrene diol epoxide. , 1992, Nucleic acids research.

[27]  U. Keyser,et al.  Indole prevents Escherichia coli cell division by modulating membrane potential , 2012, Biochimica et biophysica acta.

[28]  Lei Chen,et al.  The use of CTAB to control the size of copper nanoparticles and the concentration of alkylthiols on their surfaces , 2006 .

[29]  Abdul Hameed,et al.  Investigations into the antibacterial behavior of copper nanoparticles against Escherichia coli , 2010, Annals of Microbiology.

[30]  Siddhartha P Duttagupta,et al.  Strain specificity in antimicrobial activity of silver and copper nanoparticles. , 2008, Acta biomaterialia.

[31]  H. Sies Damage to plasmid DNA by singlet oxygen and its protection. , 1993, Mutation research.

[32]  D. Janero,et al.  Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. , 1990, Free radical biology & medicine.

[33]  C. Rock,et al.  Membrane lipid homeostasis in bacteria , 2008, Nature Reviews Microbiology.

[34]  N. W. Davis,et al.  The complete genome sequence of Escherichia coli K-12. , 1997, Science.

[35]  A. Gedanken,et al.  Pulsed sonoelectrochemical synthesis of size-controlled copper nanoparticles stabilized by poly(N-vinylpyrrolidone). , 2006, The journal of physical chemistry. B.

[36]  S. Saha,et al.  Role of membrane potential on artificial transformation of E. coli with plasmid DNA. , 2006, Journal of biotechnology.

[37]  Ruchira Chakraborty,et al.  A simple robust method for synthesis of metallic copper nanoparticles of high antibacterial potency against E. coli , 2012, Nanotechnology.

[38]  F. Neidhardt,et al.  Preparation of Escherichia coli samples for 2-D gel analysis. , 1999, Methods in molecular biology.

[39]  Yoon-Sik Lee,et al.  Corrigendum to "Antimicrobial effects of silver nanoparticles" (Nanomed Nanotechnol Biol Med. 2007;1:95-101) , 2014 .

[40]  The two inducible responses, SOS and heat-shock, in Escherichia coli act synergistically during Weigle reactivation of the bacteriophage ϕX174 , 2007, International journal of radiation biology.

[41]  Anjali A. Athawale,et al.  Synthesis of CTAB–IPA reduced copper nanoparticles , 2005 .

[42]  Kirk J. Ziegler,et al.  Synthesis of organic monolayer-stabilized copper nanocrystals in supercritical water. , 2001, Journal of the American Chemical Society.

[43]  Jungho Hwang,et al.  Susceptibility constants of Escherichia coli and Bacillus subtilis to silver and copper nanoparticles. , 2007, The Science of the total environment.

[44]  B. Jana,et al.  In vitro interaction between calf thymus DNA and Escherichia coli LPS in the presence of divalent cation Ca2+. , 2008, Biopolymers.

[45]  G. Borkow,et al.  Copper, An Ancient Remedy Returning to Fight Microbial, Fungal and Viral Infections , 2009 .

[46]  Scott J. Hultgren,et al.  Morphological plasticity as a bacterial survival strategy , 2008, Nature Reviews Microbiology.

[47]  A. Gedanken,et al.  Understanding the antibacterial mechanism of CuO nanoparticles: revealing the route of induced oxidative stress. , 2012, Small.

[48]  Ke Karlovu,et al.  The bactericidal effect of silver nanoparticles , 2010 .

[49]  Ameer Azam,et al.  Size-dependent antimicrobial properties of CuO nanoparticles against Gram-positive and -negative bacterial strains , 2012, International journal of nanomedicine.

[50]  L. Hamoen,et al.  Membrane potential is important for bacterial cell division , 2010, Proceedings of the National Academy of Sciences.

[51]  C. Yeh,et al.  Formation and Characteristics of Cu Colloids from CuO Powder by Laser Irradiation in 2-Propanol , 1999 .

[52]  Changsheng Liu,et al.  Antibacterial properties of mesoporous copper-doped silica xerogels , 2009, Biomedical materials.

[53]  M. Cronin,et al.  Metals, toxicity and oxidative stress. , 2005, Current medicinal chemistry.

[54]  E. Cabiscol,et al.  Oxidative stress in bacteria and protein damage by reactive oxygen species. , 2000, International microbiology : the official journal of the Spanish Society for Microbiology.

[55]  D. Bramhill,et al.  Bacterial SOS Checkpoint Protein SulA Inhibits Polymerization of Purified FtsZ Cell Division Protein , 1998, Journal of bacteriology.

[56]  S. Surzycki Preparation of Genomic DNA from Bacteria , 2000 .

[57]  K. Klabunde,et al.  Chemical and catalytic activity of copper nanoparticles prepared via metal vapor synthesis , 2005 .

[58]  Dae Hong Jeong,et al.  Antimicrobial effects of silver nanoparticles. , 2007, Nanomedicine : nanotechnology, biology, and medicine.