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References

  1. Mathuria JP. 2009. Nanoparticles in tuberculosis diagnosis, treatment and prevention: a hope for the future. Digest J. Nanomater. Biostruct. 4: 309-312.
  2. Kell AJ, Stewart G, Ryan S, Peytavi R, Boissinot M, Huletsky A, et al. 2008. Vancomycin-modified nanoparticles for efficient targeting and preconcentration of gram-positive and gram-negative bacteria. ACS Nano 2: 1777-1788.
    Pubmed CrossRef
  3. Cheon SA, Cho HH, Kim J, Lee J, Kim HJ, Park TJ. 2016. Recent tuberculosis diagnosis toward the end TB strategy. J. Microbiol. Methods 123: 51-61.
    Pubmed CrossRef
  4. Shim BS, Chen W, Doty C, Xu C, Kotov NA. 2008. Smart electronic yarns and wearable fabrics for human biomonitoring made by carbon nanotube coating with polyelectrolytes. Nano Lett. 8: 4151-4157.
    Pubmed CrossRef
  5. Liong M, Lu J, Kovochich M, Xia T, Ruehm SG, Nel AE, et al. 2008. Multifunctional inorganic nanoparticles for imaging, targeting, and drug delivery. ACS Nano 2: 889-896.
    Pubmed PMC CrossRef
  6. Zhou H, Zou F, Koh K, Lee J. 2014. Multifunctional magnetoplasmonic nanomaterials and their biomedical applications. J. Biomed. Nanotechnol. 10: 2921-2949.
    Pubmed CrossRef
  7. Perez JM, Simeone FJ, Saeki Y, Josephson L, Weissleder R. 2003. Viral-induced self-assembly of magnetic nanoparticles allows the detection of viral particles in biological media. J. Am. Chem. Soc. 125: 10192-10193.
    Pubmed CrossRef
  8. Kim JS, Kuk E, Yu KN, Kim J-H, Park SJ, Lee HJ, et al. 2007. Antimicrobial effects of silver nanoparticles. Nanomedicine 3: 95-101.
    Pubmed CrossRef
  9. Anandhakumar S, Raichur AM. 2013. Polyelectrolyte/silver nanocomposite multilayer films as multifunctional thin film platforms for remote activated protein and drug delivery. Acta Biomater. 9: 8864-8874.
    Pubmed CrossRef
  10. Chen X, Schluesener H. 2008. Nanosilver: a nanoproduct in medical application. Toxicol. Lett. 176: 1-12.
    Pubmed CrossRef
  11. Lok C-N, Ho C-M, Chen R, He Q-Y, Yu W-Y, Sun H, et al. 2006. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J. Proteome Res. 5: 916-924.
    Pubmed CrossRef
  12. Wang H, L iu J , Wu X , Tong Z , D eng Z. 2 013. T ailor-made Au@Ag core-shell nanoparticle 2D arrays on protein-coated graphene oxide with assembly enhanced antibacterial activity. Nanotechnology 24: 205102.
    Pubmed CrossRef
  13. Duran N, Marcato PD, De Souza GI, Alves OL, Esposito E. 2007. Antibacterial effect of silver nanoparticles produced by fungal process on textile fabrics and their effluent treatment. J. Biomed. Nanotechnol. 3: 203-208.
    CrossRef
  14. Elechiguerra JL, Burt JL, Morones JR, Camacho-Bragado A, Gao X, Lara HH, et al. 2005. Interaction of silver nanoparticles with HIV-1. J. Nanobiotechnol. 3: 1.
    Pubmed PMC CrossRef
  15. Lee J-S, Lytton-Jean AK, Hurst SJ, Mirkin CA. 2007. Silver nanoparticle-oligonucleotide conjugates based on DNA with triple cyclic disulfide moieties. Nano Lett. 7: 2112-2115.
    Pubmed PMC CrossRef
  16. Thompson DG, Enright A, Faulds K, Smith WE, Graham D. 2008. Ultrasensitive DNA detection using oligonucleotidesilver nanoparticle conjugates. Anal. Chem. 80: 2805-2810.
    Pubmed CrossRef
  17. Ting BP, Zhang J, Gao Z, Ying JY. 2009. A DNA biosensor based on the detection of doxorubicin-conjugated Ag nanoparticle labels using solid-state voltammetry. Biosens. Bioelectron. 25: 282-287.
    Pubmed CrossRef
  18. Ren X, Meng X, Chen D, Tang F, Jiao J. 2005. Using silver nanoparticle to enhance current response of biosensor. Biosens. Bioelectron. 21: 433-437.
    Pubmed CrossRef
  19. Pal S, Tak YK, Song JM. 2007. 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. 73: 1712-1720.
    Pubmed PMC CrossRef
  20. Aymonier C, Schlotterbeck U, Antonietti L, Zacharias P, Thomann R, Tiller JC, et al. 2002. Hybrids of silver nanoparticles with amphiphilic hyperbranched macromolecules exhibiting antimicrobial properties. Chem. Commun. 2002: 3018-3019.
    Pubmed CrossRef
  21. Rubio-Martínez M, Puigmartí-Luis J, Imaz I, Dittrich PS, Maspoch D. 2013. “Dual-template” synthesis of one-dimensional conductive nanoparticle superstructures from coordination metal–peptide polymer crystals. Small 9: 4160-4167.
    Pubmed CrossRef
  22. Maretti L, Billone PS, Liu Y, Scaiano JC. 2009. Facile photochemical synthesis and characterization of highly fluorescent silver nanoparticles. J. Am. Chem. Soc. 131: 13972-13980.
    Pubmed CrossRef
  23. Huang H, Ni X, Loy G, Chew C, Tan K, Loh F, et al. 1996. Photochemical formation of silver nanoparticles in poly (Nvinylpyrrolidone). Langmuir 12: 909-912.
    CrossRef
  24. Yin B, Ma H, Wang S, Chen S. 2003. Electrochemical synthesis of silver nanoparticles under protection of poly (N-vinylpyrrolidone). J. Phys. Chem. B 107: 8898-8904.
    CrossRef
  25. Rodriguez-Sanchez L, Blanco M, Lopez-Quintela M. 2000. Electrochemical synthesis of silver nanoparticles. J. Phys. Chem. B 104: 9683-9688.
    CrossRef
  26. Biswal J, Misra N, Borde LC, Sabharwal S. 2013. Synthesis of silver nanoparticles in methacrylic acid solution by gamma radiolysis and their application for estimation of dopamine at low concentrations. Rad. Phys. Chem. 83: 67-73.
    CrossRef
  27. Hu B, Wang S-B, Wang K, Zhang M, Yu S-H. 2008. Microwave-assisted rapid facile “green” synthesis of uniform silver nanoparticles: self-assembly into multilayered films and their optical properties. J. Phys. Chem C 112: 11169-11174.
    CrossRef
  28. Pillai ZS, Kamat PV. 2004. What factors control the size and shape of silver nanoparticles in the citrate ion reduction method? J. Phys. Chem. B 108: 945-951.
    CrossRef
  29. Turkevich J, Stevenson PC, Hillier J. 1951. A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss. Faraday Soc. 11: 55-75.
    CrossRef
  30. Zhang T, Wang L, Chen Q, Chen C. 2014. Cytotoxic potential of silver nanoparticles. Yonsei Med. J. 55: 283-291.
    Pubmed PMC CrossRef
  31. Burello E, Worth AP. 2011. QSAR modeling of nanomaterials. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 3: 298-306.
    Pubmed CrossRef
  32. Puzyn T, Rasulev B, Gajewicz A, Hu X, Dasari TP, Michalkova A, et al. 2011. Using nano-QSAR to predict the cytotoxicity of metal oxide nanoparticles. Nat. Nanotechnol. 6: 175-178.
    Pubmed CrossRef
  33. Hubbard BK, Walsh CT. 2003. Vancomycin assembly:nature’s way. Angew. Chem. Int. Ed. Engl. 42: 730-765.
    Pubmed CrossRef
  34. Walsh C. 1999. Deconstructing vancomycin. Science 284: 442-443.
    Pubmed CrossRef
  35. Everaerts F, Torrianni M, Hendriks M, Feijen J. 2008. Biomechanical properties of carbodiimide crosslinked collagen:influence of the formation of ester crosslinks. J. Biomed. Mater. Res. A 85: 547-555.
    Pubmed CrossRef
  36. Loveymi BD, Jelvehgari M, Zakeri-Milani P, Valizadeh H. 2012. Design of vancomycin RS-100 nanoparticles in order to increase the intestinal permeability. Adv. Pharm. Bull. 2: 43.
  37. Thottoli AK, Unni AKA. 2013. Effect of trisodium citrate concentration on the particle growth of ZnS nanoparticles. J. Nanostruct. Chem. 3: 1-12.
    CrossRef
  38. Yoo HS, Lee KH, Oh JE, Park TG. 2000. In vitro and in vivo anti-tumor activities of nanoparticles based on doxorubicin–PLGA conjugates. J. Control. Release 68: 419-431.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(8): 1483-1490

Published online August 28, 2017 https://doi.org/10.4014/jmb.1612.12041

Copyright © The Korean Society for Microbiology and Biotechnology.

Enhanced Internalization of Macromolecular Drugs into Mycobacterium smegmatis with the Assistance of Silver Nanoparticles

Fangfang Sun , Sangjin Oh , Jeonghyo Kim , Tatsuya Kato , Hwa-Jung Kim , Jaebeom Lee * and Enoch Y. Park *

Research Institute of Green Science and Technology, Shizuoka University, Suruga-ku, Japan, 1Department of Biomedical Engineering, College of Life Information Science and Instrument Engineering, Hangzhou Dianzi University, P.R. China, 2Department of Cogno-mechatronics Engineering, Pusan National University, Republic of Korea, 3Department of Microbiology and Research Institute for Medical Science, College of Medicine, Chungnam National University, Republic of Korea

Received: January 4, 2017; Accepted: June 8, 2017

Abstract

In this study, silver nanoparticles (AgNPs) were synthesized by the citrate reduction process
and, with the assistance of n-hydroxysuccinimide and 1-ethyl-3-(3-dimethylaminopropyl)
carbodiimide, were successfully loaded with the macromolecular drug vancomycin (VAM) to
form AgNP-VAM bioconjugates. The synthesized AgNPs, VAM, and AgNP-VAM conjugate
were characterized by UV-visible spectroscopy, zeta potential analysis, confocal microscopy,
and transmission electron microscopy. The effect of loading VAM onto AgNPs was
investigated by testing the internalization of the bioconjugate into Mycobacterium smegmatis.
After treatment with the AgNP-VAM conjugate, the bacterial cells showed a significant
decrease in UV absorption, indicating that loading of the VAM on AgNPs had vastly
improved the drug’s internalization compared with that of AgNPs. All the experimental
assessments showed that, compared with free AgNPs and VAM, enhanced internalization had
been successfully achieved with the AgNP-VAM conjugate, thus leading to significantly better
delivery of the macromolecular drug into the M. smegmatis cell. The current research provides
a new potential drug delivery system for the treatment of mycobacterial infections.

Keywords: Mycobacterium smegmatis, silver nanoparticle, internalization, vancomycin, bioconjugate

References

  1. Mathuria JP. 2009. Nanoparticles in tuberculosis diagnosis, treatment and prevention: a hope for the future. Digest J. Nanomater. Biostruct. 4: 309-312.
  2. Kell AJ, Stewart G, Ryan S, Peytavi R, Boissinot M, Huletsky A, et al. 2008. Vancomycin-modified nanoparticles for efficient targeting and preconcentration of gram-positive and gram-negative bacteria. ACS Nano 2: 1777-1788.
    Pubmed CrossRef
  3. Cheon SA, Cho HH, Kim J, Lee J, Kim HJ, Park TJ. 2016. Recent tuberculosis diagnosis toward the end TB strategy. J. Microbiol. Methods 123: 51-61.
    Pubmed CrossRef
  4. Shim BS, Chen W, Doty C, Xu C, Kotov NA. 2008. Smart electronic yarns and wearable fabrics for human biomonitoring made by carbon nanotube coating with polyelectrolytes. Nano Lett. 8: 4151-4157.
    Pubmed CrossRef
  5. Liong M, Lu J, Kovochich M, Xia T, Ruehm SG, Nel AE, et al. 2008. Multifunctional inorganic nanoparticles for imaging, targeting, and drug delivery. ACS Nano 2: 889-896.
    Pubmed KoreaMed CrossRef
  6. Zhou H, Zou F, Koh K, Lee J. 2014. Multifunctional magnetoplasmonic nanomaterials and their biomedical applications. J. Biomed. Nanotechnol. 10: 2921-2949.
    Pubmed CrossRef
  7. Perez JM, Simeone FJ, Saeki Y, Josephson L, Weissleder R. 2003. Viral-induced self-assembly of magnetic nanoparticles allows the detection of viral particles in biological media. J. Am. Chem. Soc. 125: 10192-10193.
    Pubmed CrossRef
  8. Kim JS, Kuk E, Yu KN, Kim J-H, Park SJ, Lee HJ, et al. 2007. Antimicrobial effects of silver nanoparticles. Nanomedicine 3: 95-101.
    Pubmed CrossRef
  9. Anandhakumar S, Raichur AM. 2013. Polyelectrolyte/silver nanocomposite multilayer films as multifunctional thin film platforms for remote activated protein and drug delivery. Acta Biomater. 9: 8864-8874.
    Pubmed CrossRef
  10. Chen X, Schluesener H. 2008. Nanosilver: a nanoproduct in medical application. Toxicol. Lett. 176: 1-12.
    Pubmed CrossRef
  11. Lok C-N, Ho C-M, Chen R, He Q-Y, Yu W-Y, Sun H, et al. 2006. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J. Proteome Res. 5: 916-924.
    Pubmed CrossRef
  12. Wang H, L iu J , Wu X , Tong Z , D eng Z. 2 013. T ailor-made Au@Ag core-shell nanoparticle 2D arrays on protein-coated graphene oxide with assembly enhanced antibacterial activity. Nanotechnology 24: 205102.
    Pubmed CrossRef
  13. Duran N, Marcato PD, De Souza GI, Alves OL, Esposito E. 2007. Antibacterial effect of silver nanoparticles produced by fungal process on textile fabrics and their effluent treatment. J. Biomed. Nanotechnol. 3: 203-208.
    CrossRef
  14. Elechiguerra JL, Burt JL, Morones JR, Camacho-Bragado A, Gao X, Lara HH, et al. 2005. Interaction of silver nanoparticles with HIV-1. J. Nanobiotechnol. 3: 1.
    Pubmed KoreaMed CrossRef
  15. Lee J-S, Lytton-Jean AK, Hurst SJ, Mirkin CA. 2007. Silver nanoparticle-oligonucleotide conjugates based on DNA with triple cyclic disulfide moieties. Nano Lett. 7: 2112-2115.
    Pubmed KoreaMed CrossRef
  16. Thompson DG, Enright A, Faulds K, Smith WE, Graham D. 2008. Ultrasensitive DNA detection using oligonucleotidesilver nanoparticle conjugates. Anal. Chem. 80: 2805-2810.
    Pubmed CrossRef
  17. Ting BP, Zhang J, Gao Z, Ying JY. 2009. A DNA biosensor based on the detection of doxorubicin-conjugated Ag nanoparticle labels using solid-state voltammetry. Biosens. Bioelectron. 25: 282-287.
    Pubmed CrossRef
  18. Ren X, Meng X, Chen D, Tang F, Jiao J. 2005. Using silver nanoparticle to enhance current response of biosensor. Biosens. Bioelectron. 21: 433-437.
    Pubmed CrossRef
  19. Pal S, Tak YK, Song JM. 2007. 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. 73: 1712-1720.
    Pubmed KoreaMed CrossRef
  20. Aymonier C, Schlotterbeck U, Antonietti L, Zacharias P, Thomann R, Tiller JC, et al. 2002. Hybrids of silver nanoparticles with amphiphilic hyperbranched macromolecules exhibiting antimicrobial properties. Chem. Commun. 2002: 3018-3019.
    Pubmed CrossRef
  21. Rubio-Martínez M, Puigmartí-Luis J, Imaz I, Dittrich PS, Maspoch D. 2013. “Dual-template” synthesis of one-dimensional conductive nanoparticle superstructures from coordination metal–peptide polymer crystals. Small 9: 4160-4167.
    Pubmed CrossRef
  22. Maretti L, Billone PS, Liu Y, Scaiano JC. 2009. Facile photochemical synthesis and characterization of highly fluorescent silver nanoparticles. J. Am. Chem. Soc. 131: 13972-13980.
    Pubmed CrossRef
  23. Huang H, Ni X, Loy G, Chew C, Tan K, Loh F, et al. 1996. Photochemical formation of silver nanoparticles in poly (Nvinylpyrrolidone). Langmuir 12: 909-912.
    CrossRef
  24. Yin B, Ma H, Wang S, Chen S. 2003. Electrochemical synthesis of silver nanoparticles under protection of poly (N-vinylpyrrolidone). J. Phys. Chem. B 107: 8898-8904.
    CrossRef
  25. Rodriguez-Sanchez L, Blanco M, Lopez-Quintela M. 2000. Electrochemical synthesis of silver nanoparticles. J. Phys. Chem. B 104: 9683-9688.
    CrossRef
  26. Biswal J, Misra N, Borde LC, Sabharwal S. 2013. Synthesis of silver nanoparticles in methacrylic acid solution by gamma radiolysis and their application for estimation of dopamine at low concentrations. Rad. Phys. Chem. 83: 67-73.
    CrossRef
  27. Hu B, Wang S-B, Wang K, Zhang M, Yu S-H. 2008. Microwave-assisted rapid facile “green” synthesis of uniform silver nanoparticles: self-assembly into multilayered films and their optical properties. J. Phys. Chem C 112: 11169-11174.
    CrossRef
  28. Pillai ZS, Kamat PV. 2004. What factors control the size and shape of silver nanoparticles in the citrate ion reduction method? J. Phys. Chem. B 108: 945-951.
    CrossRef
  29. Turkevich J, Stevenson PC, Hillier J. 1951. A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss. Faraday Soc. 11: 55-75.
    CrossRef
  30. Zhang T, Wang L, Chen Q, Chen C. 2014. Cytotoxic potential of silver nanoparticles. Yonsei Med. J. 55: 283-291.
    Pubmed KoreaMed CrossRef
  31. Burello E, Worth AP. 2011. QSAR modeling of nanomaterials. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 3: 298-306.
    Pubmed CrossRef
  32. Puzyn T, Rasulev B, Gajewicz A, Hu X, Dasari TP, Michalkova A, et al. 2011. Using nano-QSAR to predict the cytotoxicity of metal oxide nanoparticles. Nat. Nanotechnol. 6: 175-178.
    Pubmed CrossRef
  33. Hubbard BK, Walsh CT. 2003. Vancomycin assembly:nature’s way. Angew. Chem. Int. Ed. Engl. 42: 730-765.
    Pubmed CrossRef
  34. Walsh C. 1999. Deconstructing vancomycin. Science 284: 442-443.
    Pubmed CrossRef
  35. Everaerts F, Torrianni M, Hendriks M, Feijen J. 2008. Biomechanical properties of carbodiimide crosslinked collagen:influence of the formation of ester crosslinks. J. Biomed. Mater. Res. A 85: 547-555.
    Pubmed CrossRef
  36. Loveymi BD, Jelvehgari M, Zakeri-Milani P, Valizadeh H. 2012. Design of vancomycin RS-100 nanoparticles in order to increase the intestinal permeability. Adv. Pharm. Bull. 2: 43.
  37. Thottoli AK, Unni AKA. 2013. Effect of trisodium citrate concentration on the particle growth of ZnS nanoparticles. J. Nanostruct. Chem. 3: 1-12.
    CrossRef
  38. Yoo HS, Lee KH, Oh JE, Park TG. 2000. In vitro and in vivo anti-tumor activities of nanoparticles based on doxorubicin–PLGA conjugates. J. Control. Release 68: 419-431.
    CrossRef