journal article·2014-06

Biogenic gold nanoparticles enhance methylene blue-induced phototoxic effect on Staphylococcus epidermidis

Irena Maliszewska, Agata Leśniewska, Joanna Olesiak-Bańska, Katarzyna Matczyszyn, Marek Samoć

Journal of Nanoparticle Research· Volume 16· Issue 6
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Abstract

There is considerable current interest in photodynamic inactivation (PDI) as potential antimicrobial therapy. This study reports successful implementation of PDI of Staphylococcus epidermidis using methylene blue (MB) in combination with biogenic gold nanoparticles (GNP). Monodispersed colloidal GNP were synthesized by reduction of Au+3 in the presence of cell-free filtrate of Trichoderma koningii and were characterized by a number of techniques including UV–Vis and fluorescence spectroscopy, transmission electron microscopy (TEM), and Fourier transform infrared spectroscopy (FTIR) to be 12 ± 3 nm spherical gold particles coated with proteins. Studies on the role of the cell-free filtrate proteins in the synthesis of the GNP indicate that the process is nonenzymatic but involves interactions of various amino acids with gold ions. A Xe lamp (550–780 nm) or a He–Ne laser (632 nm) was used as light sources to study the effect of MB alone, the GNP alone, and the MB–GNP mixture on the viability of bacterial cells. Lethal photosensitization of S. epidermidis with the MB–GNP mixture was achieved after 5 and 10 min exposure to laser or Xe lamp, respectively. It has been found that the MB–GNP mixture exhibits a significant antibacterial activity already in the absence of any light source and gives an enhanced antimicrobial response when using either a laser or a Xe lamp source for photosensitization.
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Research context

OpenAlex topics: Photodynamic Therapy Research Studies · Nanoplatforms for cancer theranostics · Biosensors and Analytical Detection

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References (77)

Show source-provided references
1. Alaaldin M, Alkilany AM, Murphy CJ (2010) Toxicity and cellular uptake of gold nanoparticles: what we have learned so far? J Nanopart Res 12:2313–233310.1007/s11051-010-9911-8 ↗
2. Aromal AS, Philip D (2012) Green synthesis of gold nanoparticles using Trigonella foenum-graecum and its size-dependent catalytic activity. Spectrochim Acta A 97:1–510.1016/j.saa.2012.05.083 ↗
3. Atieh MA (2010) Photodynamic therapy as an adjunctive treatment for chronic periodontitis: a meta-analysis. Lasers Med Sci 25:605–61310.1007/s10103-009-0744-6 ↗
4. Ben Hur E, Moor A (1996) The risk of transfusion-transmitted viral infections. Transfus Med Rev 10:15–2210.1016/S0887-7963(96)80119-2 ↗
5. Choi R, Yang J, Choi J, Lim EK, Kim E, Suh JS, Huh JM, Haam S (2010) Thiolated dextran-coated gold nanorods for photothermal ablation of inflammatory macrophages. Langmuir 26:17520–1752710.1021/la1029728 ↗
6. Dadras S, Mohajerani E, Eftekhar F, Hosseini M (2006) Different photoresponses of Staphylococcus aureus and Pseudomonas aeruginosa to 514, 532, and 633 nm low level lasers in vitro. Curr Microbiol 53:282–28610.1007/s00284-005-0490-3 ↗
7. De Leon SP, Wenzel RP (1984) Hospital-acquired bloodstream infections with Staphylococcus epidermidis: review of cases. Am J Med 77:639–64410.1016/0002-9343(84)90354-1 ↗
8. de Sousa NT, Guirro RR, Santana HF, Silva CC (2012) In vitro analysis of bacterial morphology by atomic force microscopy of low level laser therapy 660, 830 and 904 nm. Photomed Laser Surg 5:281–28510.1089/pho.2011.3160 ↗
9. Donnelly RF, McCarron PA, Tunney MM (2008) Antifungal photodynamic therapy. Microbiol Res 163:1–1210.1016/j.micres.2007.08.001 ↗
10. Enwemeka CS, Williams D, Hollosi S, Yens D, Enwemeka SK (2008) Visible 405 nm SLD light photodestroys methicillin-resistant Staphylococcus aureus (MRSA) in vitro. Lasers Surg Med 40:734–73710.1002/lsm.20724 ↗
11. Enwemeka CS, Williams D, Enwemeka SK, Hollosi S, Yens D (2009) Blue 470-nm light kills methicillin resistant Staphylococcus aureus (MRSA) in vitro. Photomed Laser Surg 27:221–22610.1089/pho.2008.2413 ↗
12. Fu XJ, Fang Y, Yao M (2013) Antimicrobial photodynamic therapy for methicillin-resistant Staphylococcus aureus infection. BioMed Res Int, ID159157. doi: 10.1155/2013/15915710.1155/2013/159157 ↗
13. Gil-Tomás JG, Tubby S, Parkin IP, Narband N, Dekker L, Nair SP, Wilson M, Street C (2007) Lethal photosensitisation of Staphylococcus aureus using a toluidine blue O–tiopronin–gold nanoparticle conjugate. J Mater Chem 17:3739–374610.1039/b706615e ↗
14. Gordel M, Olesiak-Bańska J, Matczyszyn K, Nogues C, Pawlik K, Buckle M, Samoć M (2012) Shape and size separation of gold nanoparticles using glucose gradient density. Proc SPIE 8424 84242F. doi: 10.1117/12.92209710.1117/12.922097 ↗
15. Gordel M, Olesiak-Bańska J, Matczyszyn K, Nogues C, Buckle M, Samoć M (2014) Post-synthesis reshaping of gold nanorods using a femtosecond laser. Phys Chem Chem Phys 16:71–7810.1039/C3CP53457J ↗
16. Grzelczak M, Perez-Juste J, Mulvaney P, Liz-Marzan LM (2008) Shape control in gold nanoparticle synthesis. Chem Soc Rev 37:1783–179110.1039/b711490g ↗
17. Guffey JS, Wilborn J (2006a) Effects of combined 405 nm and 880 nm light on Staphylococcus aureus and Pseudomonas aeruginosa in vitro. Photomed Laser Surg 24:680–68310.1089/pho.2006.24.680 ↗
18. Guffey JS, Wilborn J (2006b) In vitro bactericidal effects of 405 nm and 470 nm blue light. Photomed Laser Surg 24:684–68810.1089/pho.2006.24.684 ↗
19. Guo SE, Wang E (2007) Synthesis and electrochemical applications of gold nanoparticles. Anal Chim Acta 598:181–19210.1016/j.aca.2007.07.054 ↗
20. Harris F, Chatfield LK, Phoenix DA (2005) Phenothiazinium based photosensitisers–photodynamic agents with a multiplicity of cellular targets and clinical applications. Curr Drug Targets 6:615–62710.2174/1389450054545962 ↗
21. Hegge AB, Bruzell E, Kristensen S, Tǿnnesen HH (2012) Photoinactivation of Staphylococcus epidermidis biofilms and suspensions by the hydrophobic photosensitizer curcumin–effect of selected nanocarrier: studies on curcumin and curcuminoides XLVII. Eur J Pharm Sci 47:65–7410.1016/j.ejps.2012.05.002 ↗
22. Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TG (1992) CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgices wound infections. Inf Control Hosp Epidemiol 13:606–60810.2307/30148464 ↗
23. Hu YJ, Zhao RM, Dong JX, Qu SS (2006) Spectroscopic studies on the interaction between methylene blue and bovine serum albumin. J Photochem Photobiol A 179:324–32910.1016/j.jphotochem.2005.08.037 ↗
24. Huang X, Neretina S, El-Sayed MA (2009) Gold nanorods: from synthesis and properties to biological and biomedical applications. Adv Mater 21:4880–491010.1002/adma.200802789 ↗
25. Huang L, Xuan Y, Koide Y, Zhiyentayev T, Tanaka M, Hamblin MR (2012) Type I and type II mechanisms of antimicrobial photodynamic therapy: an in vitro study on gram-negative and gram-positive bacteria. Lasers Surg Med 44:490–49910.1002/lsm.22045 ↗
26. Ingle A, Rai M, Gade G, Manisha Bawaskar M (2009) Fusarium solani: a novel biological agent for the extracellular synthesis of silver nanoparticles. J Nanopart Res 11:2079–208510.1007/s11051-008-9573-y ↗
27. Jori G (2006) Photodynamic therapy of microbial infections: state-of-the-art and perspectives. J Environ Pathol Toxicol Oncol 25:505–51910.1615/JEnvironPatholToxicolOncol.v25.i1-2.320 ↗
28. Jori G, Fabris C, Soncin M, Ferro S, Coppellotti O, Dei D, Fantetti L, Chiti G, Roncucci G (2006) Photodynamic therapy in the treatment of microbial infections: basic principles and perspective applications. Lasers Surg Med 38:468–48110.1002/lsm.20361 ↗
29. Junqueira HC, Severino D, Dias LG, Gugliotti M, Baptista MS (2002) Modulation of methylene blue photochemical properties based on adsorption at aqueous micelle interfaces. Phys Chem Chem Phys 4:2320–232810.1039/b109753a ↗
30. Khan S, Alan F, Azam A, Khan AU (2012) Gold nanoparticles enhance methylene blue-induced photodynamic therapy: a novel therapeutic approach to inhibit Candida albicans biofilm. Int J Nanomed 7:3245–325710.2147/IJN.S31219 ↗
31. Khlebtsov BN, Tuchina ES, Khanadeev VA, Panfilova EV, Petrov PO, Tuchin VV, Khlebtsov NG (2013) Enhanced photoinactivation of Staphylococcus aureus with nanocomposites containing plasmonic particles and hematoporphyrin. J Biophotonics 6:338–35110.1002/jbio.201200079 ↗
32. Klepac-Ceraj V, Patel N, Song X, Holewa C, Patel C, Kent R, Amiji MM, Soukos NS (2011) Photodynamic effects of methylene blue-loaded polymeric nanoparticles on dental plaque bacteria. Lasers Surg Med 43:600–60610.1002/lsm.21069 ↗
33. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–68510.1038/227680a0 ↗
34. Lee KS, El-Sayed MA (2006) Gold and silver nanoparticles in sensing and imaging: sensitivity of plasmon response to size, shape and metal composition. J Phys Chem B 110:19220–1922510.1021/jp062536y ↗
35. Li S, Shen Y, Xie A, Yu X, Zhang X, Yang L, Li C (2007) Rapid room-temperature synthesis of amorphous selenium/protein composites using Capsicum annuum L extract. Nanotechnology 18:40510110.1088/0957-4484/18/40/405101 ↗
36. Lim YT, Cho MY, Choi BS, Noh YW, Chung BH (2008) Diagnosis and therapy of macrophage cells using dextran-coated near-infrared responsive hollow-type gold nanoparticles. Nanotechnology 19:37510510.1088/0957-4484/19/37/375105 ↗
37. Liz-Marzán LM (2006) Tailoring surface plasmons through the morphology and assembly of metal nanoparticles. Langmuir 22:32–4110.1021/la0513353 ↗
38. Malicka J, Gryczynski I, Geddes CD, Lakowicz JR (2003) Metal-enhanced emission from indocyanine green: a new approach to in vivo imaging. J Biomed Opt 8:472–47810.1117/1.1578643 ↗
39. Maliszewska I (2013) Microbial mediated synthesis of gold nanoparticles: preparation, characterization and cytotoxicity studies. Dig J Nano Biostruct 8:1123–1131
40. McCann MT, Gilmore BF, Gorman SP (2008) Staphylococcus epidermidis device-related infections: pathogenesis and clinical management. J Pharm Pharmacol 60:1551–157110.1211/jpp.60.12.0001 ↗
41. Morissey JH (1981) Silver stain for protein in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Chem 117:307–310
42. Naik AJT, Ismailc S, Kayb C, Wilsonc M, Parkina IP (2011) Antimicrobial activity of polyurethane embedded with methylene blue, toluidene blue and gold nanoparticles against Staphylococcus aureus; illuminated with white light. Mater Chem Phys 129:446–45010.1016/j.matchemphys.2011.04.040 ↗
43. Narayanan KB, Sakthivel N (2011) Extracellular synthesis of silver nanoparticles using the leaf extract of Coleus amboinicus Lour. Mater Res Bull 46:1708–171310.1016/j.materresbull.2011.05.041 ↗
44. Nehl CL, Hafner JH (2008) Shape-dependent plasmon resonances of gold nanoparticles. J Mater Chem 18:2415–241910.1039/b714950f ↗
45. Nussbaum EL, Lilge L, Mazzulli T (2002a) Effects of 630-, 660-, 810-, and 905 nm laser irradiation delivering radiant exposure of 1–50 J/cm2 on three species of bacteria in vitro. J Clin Laser Med Surg 20:325–33310.1089/104454702320901116 ↗
46. Nussbaum EL, Lilge L, Mazzulli T (2002b) Effects of 810 nm laser irradiation on in vitro growth of bacteria: comparison of continuous wave and frequency modulated light. Lasers Surg Med 31:343–35110.1002/lsm.10121 ↗
47. Nussbaum EL, Lilge L, Mazzulli T (2003) Effects of low level laser therapy (LLLT) of 810 nm upon in vitro growth of bacteria: relevance of irradiance and radiant exposure. J Clin Laser Med Surg 21:283–29010.1089/104454703322564497 ↗
48. O’Neal DP, Hirsch LR, Halas NJ, Payne JD, West JL (2004) Photo-thermal tumor ablation in mice using near infrared absorbing nanoparticles. Cancer Lett 209:171–17610.1016/j.canlet.2004.02.004 ↗
49. Oleinick NL, Evans HH (1998) The photobiology of photodynamic therapy: cellular targets and mechanisms. Radiat Res 150:146–15610.2307/3579816 ↗
50. Olesiak-Bańska J, Gordel M, Kołkowski R, Matczyszyn K, Samoć M (2012) Third-order nonlinear optical properties of colloidal gold nanorods. J Phys Chem C 116:13731–1373710.1021/jp301821p ↗
51. Paciotti GF, Kingstom DGI, Tamarkin I (2006) Colloidal gold nanoparticles: a novel nanoparticles platform for developing multifunctional tumor-targeted drug delivery vectors. Drug Dev Res 67:47–5410.1002/ddr.20066 ↗
52. Pagonis TC, Chen J, Fontana CR, Devalapally H, Ruggiero K, Song X, Foschi F, Dunham J, Skobe Z, Yamazaki H, Kent R, Tanner ACR, Amiji MM, Soukos NS (2010) Nanoparticle-based endodontic antimicrobial photodynamic therapy. J Endod 36:322–32810.1016/j.joen.2009.10.011 ↗
53. Perni S, Piccirillo C, Pratten J, Prokopovich P, Chrzanowski W, Parkin IP, Wilson M (2009) The antimicrobial properties of light-activated polymers containing methylene blue and gold nanoparticles. Biomaterials 30:89–9310.1016/j.biomaterials.2008.09.020 ↗
54. Perni S, Piccirillo C, Kafizas A, Uppal M, Pratten J, Wilson M, Parkin IP (2010) Antibacterial activity of light-activated silicone containing methylene blue and gold nanoparticles of different sizes. J Clust Sci 21:427–43810.1007/s10876-010-0319-5 ↗
55. Pissuwan D, Valenzuela SM, Miller CM, Cortie MB (2007) A golden bullet? Selective targeting of Toxoplasma gondii tachyzoites using antibody functionalized gold nanorods. Nano Lett 7:3808–3801210.1021/nl072377+ ↗
56. Raab O (1900) The effect of fluorescent substances on infusoria. Z Biol 39:524–526
57. Roy M, Mukherjee P, Mandal BP, Sharma RK, Tyagi AK, Kale SP (2012) Biomimetic synthesis of nanocrystalline silver sol using cysteine: stability aspects and antibacterial activities. RSC Adv 2:6496–650310.1039/c2ra00785a ↗
58. Sadowski Z, Maliszewska I (2011) Applications of gold nanoparticles: current trends and future prospects. In: Rai M, Nelson Duran N (eds) Metal nanoparticles in microbiology. Springer, Heidelberg, 225–24810.1007/978-3-642-18312-6_10 ↗
59. Saino E, Sbarra MS, Arciola CR, Scavone M, Bloise N, Nikolov P, Ricchelli F, Visai L (2010) Photodynamic action of tri-meso(N-methyl-pyridyl), meso(N-tetradecyl-pyridyl) porphine on Staphylococ`cus epidermidis biofilms grown on Ti6Al4 V alloy. Int J Artif Organs 33:636–64510.1177/039139881003300909 ↗
60. Santus R, Grellier P, Schrével J, Mazière JC, Stoltz JF (1998) Photodecontamination of blood components: advantages and drawbacks. Clin Hemorheol Microcirc 18:299–308
61. Sarkar J, Ray S, Chattopadhyay D, Laskar A, Acharya K (2012) Mycogenesis of gold nanoparticles using a phytopathogen Alternaria alternate. Bioprocess Biosyst Eng 35:541–63710.1007/s00449-011-0646-4 ↗
62. Sbarra MS, Di Poto A, Arciola CR, Saino E, Sharma M, Bragheri F, Cristiani I, Speziale P, Visai L (2008) Photodynamic action of merocyanine 540 on Staphylococcus epidermidis biofilms. Int J Artif Organs 31:848–85710.1177/039139880803100914 ↗
63. Sbarra MS, Arciola CR, Di Poto A, Saino E, Rohde H, Speziale P, Visai L (2009) The photodynamic effect of tetra-substituted N-methyl-pyridyl-porphine combined with the action of vancomycin or host defense mechanisms disrupts Staphylococcus epidermidis biofilms. Int J Artif Organs 32:574–58310.1177/039139880903200906 ↗
64. Simpson RJ (2004) Purifying proteins for proteomics: a laboratory manual. Cold Spring Harbor Laboratory Press
65. Singh M, Kumar M, Kalaivani R, Manikandan S, Kumaraguru AK (2013) Metallic silver nanoparticles: a therapeutic agent in combination with antifungal drug against human fungal pathogen. Bioprocess Biosyst Eng 36:407–41510.1007/s00449-012-0797-y ↗
66. Soukos NS, Goodson JM (2011) Photodynamic therapy in the control of oral biofilms. Periodontol 2000 55:143–16610.1111/j.1600-0757.2010.00346.x ↗
67. Tardivo JP, Del Giglio A, Santos de Oliveira C, Gabrielli DS, Junqueira HC, Tada DB, Severino D, Turchiello RF, Baptista MS (2005) Methylene blue in photodynamic therapy: from basic mechanisms to clinical applications. Photodiag Photodyn Ther 2(3):175–19110.1016/S1572-1000(05)00097-9 ↗
68. Valduga G, Bertolini G, Reddi E, Jori G (1993) Effect of extracellalarly generated singlet oxygen on Gram-positive and Gram-negative bacteria. J Photochem Photobiol B 21:81–8610.1016/1011-1344(93)80168-9 ↗
69. Wainwright M (1998) Photodynamic antimicrobial chemotherapy (PACT). J Antimicrob Chemother 42:13–2810.1093/jac/42.1.13 ↗
70. Wainwright M (2010) Safe photoantimicrobials for skin and soft-tissue infections. Int J Antimicrob Agents 36:14–1810.1016/j.ijantimicag.2010.03.002 ↗
71. Wainwright M, Crossley KB (2004) Photosensitising agents-circumventing resistance and breaking down biofilms: a review. Int Biodeter Biodegrad 53:119–12610.1016/j.ibiod.2003.11.006 ↗
72. Wainwright M, Mohr H, Walker WH (2007) Phenothiazinium derivatives for pathogen inactivation in blood products. J Photochem Photobiol B 86:45–5810.1016/j.jphotobiol.2006.07.005 ↗
73. Wang S, Lawson R, Ray PC, Yu H (2011) Toxic effects of gold nanoparticles on Salmonella typhimurim bacteria. Toxicol Ind Health 27:547–55410.1177/0748233710393395 ↗
74. Zhang Z, Jing Wang J, Chunying Chen C (2013) Gold nanorods based platforms for light-mediated theranostics. Theranostics 3:223–23810.7150/thno.5409 ↗
75. Zharov VP, Galitovskaya EN, Jonson C, Thomas K (2005a) Synergistic enhancement of selective nanophotothermolysis with gold nanoclusters: potential for cancer therapy. Laser Surg Med 37:219–22610.1002/lsm.20223 ↗
76. Zharov VP, Letfullin RR, Galitovskaya EN (2005b) Microbubbles-overlapping mode for laser killing of cancer cells with absorbing nanoparticle clusters. J Phys D 38:2571–258110.1088/0022-3727/38/15/007 ↗
77. Zharov VP, Mercer KE, Galitovskaya EN, Smeltzery MS (2006) Photothermal nanotherapeutics and nanodiagnostics for selective killing of bacteria targeted with gold nanoparticles. Biophys J 90:619–62710.1529/biophysj.105.061895 ↗