Antibiofilm action of a toluidine blue O-silver nanoparticle conjugate on Streptococcus mutans: a mechanism of type I photodynamic therapy

Biofouling

Volumn 32, Issue 3, 2016, Pages 313-328

  Misba, Lama ^a   Kulshrestha, Shatavari ^a   Khan, Asad U ^a  

^a ALIGARH MUSLIM UNIVERSITY   (India)

Author keywords

Biofilm; gene expression; photodynamic therapy; toluidine blue O silver nanoparticle conjugate; type I

Indexed keywords

BACTERIUM; BIOASSAY; BIOFILM; DYE; GENE EXPRESSION; NANOPARTICLE; OXYGEN; SECONDARY METABOLITE; SILVER; TOXICITY; VIABILITY;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS MUTANS;

ANTIINFECTIVE AGENT; METAL NANOPARTICLE; PHOTOSENSITIZING AGENT; SILVER; TOLONIUM CHLORIDE;

BIOFILM; DENTAL CARIES; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; PHOTOCHEMOTHERAPY; PHYSIOLOGY; PROCEDURES; SCANNING ELECTRON MICROSCOPY; STREPTOCOCCUS MUTANS;

ANTI-BACTERIAL AGENTS; BIOFILMS; DENTAL CARIES; HUMANS; METAL NANOPARTICLES; MICROSCOPY, ELECTRON, SCANNING; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; SILVER; STREPTOCOCCUS MUTANS; TOLONIUM CHLORIDE;

EID: 84959348277     PISSN: 08927014     EISSN: 10292454     Source Type: Journal    
DOI: 10.1080/08927014.2016.1141899     Document Type: Article

References (55)

1. J.Abranches, J.H.Miller, A.R.Martinez, P.J.Simpson-Haidaris, R.A.Burne, J.A.Lemos. 2011. The collagen-binding protein cnm is required for Streptococcus mutans adherence to and intracellular invasion of human coronary artery endothelial cells. Infect Immune. 79:2277–2284. doi: 10.1128/IAI.00767-10.10.1128/IAI.00767-10
2. A.Al-Ahmad, C.Tennert, L.Karygianni, K.T.Wrbas, E.Hellwig, M.J.Altenburger. 2013. Antimicrobial photodynamic therapy using visible light plus water-filtered infrared-A (wIRA). J Med Microbiol. 62:467–473. doi: 10.1099/jmm.0.048843-0.10.1099/jmm.0.048843-0
3. V.Alt, T.Bechert, P.Steinrucke, M.Wagener, P.Seidel, A.Dingeldein, E.Domann, R.Schnettler. 2004. An in vitro assessment of the antibacterial properties and cytotoxicity of nanoparticulate silver bone cement. Biomaterials. 25:4383–4391. doi: 10.1016/j.biomaterials.2003.10.078.10.1016/j.biomaterials.2003.10.078
4. K.P.Bankura, D.Maity, M.M.R.Mollick, D.Mondal, B.Bhowmick, M.K.Bain, A.Chakraborty, J.Sarkar, K.Acharya, D.Chattopadhyay. 2012. Synthesis, characterization and antimicrobial activity of dextran stabilized silver nanoparticles in aqueous medium. Carbohyd Polym. 89:1159–1165. doi: 10.1016/j.carbpol.2012.03.089.10.1016/j.carbpol.2012.03.089
5. R.Bryaskova, D.Pencheva, S.Nikolov, T.Kantardjiev. 2011. Synthesis and comparative study on the antimicrobial activity of hybrid materials based on silver nanoparticles (AgNps) stabilized by polyvinylpyrrolidone (PVP). J Chem Biol. 4:185–191. doi: 10.1007/s12154-011-0063-9.10.1007/s12154-011-0063-9
6. J.N.Cai, M.A.Kim, J.E.Jung, S.Pandit, K.Y.Song, J.G.Jeon. 2015. Effect of combined oleic acid and fluoride at sub-MIC levels on EPS formation and viability of Streptococcus mutans UA159 biofilms. Biofouling. 31:555–563. doi: 10.1080/08927014.2015.1076799.10.1080/08927014.2015.1076799
7. B.L.Carpenter, X.Situ, F.Scholle, J.Bartelmess, W.W.Weare, R.A.Ghiladi. 2015. Antiviral, antifungal and antibacterial activities of a BODIPY-based photose. Molecules. 20:10604–10621. doi: 10.3390/molecules200610604.10.3390/molecules200610604
8. L.Costa, M.A.F.Faustino, J.P.C.Tomé, M.G.P.S.Neves, A.C.Tome, J.A.S.Cavaleiro, A.Cunha, A.Almeida. 2013. Involvement of type I and type II mechanisms on the photoinactivation of non-enveloped DNA and RNA bacteriophages. J Photochem Photobiol B. 120:10–16. doi: 10.1016/j.jphotobiol.2013.01.005.10.1016/j.jphotobiol.2013.01.005
9. T.N.Demidova, M.R.Hamblin. 2005. Effect of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother. 49:2329–2335. doi: 10.1128/AAC.49.6.2329-2335.2005.10.1128/AAC.49.6.2329-2335.2005
10. R.S.Diggikar, R.H.Patil, S.B.Kale, D.K.Thombre, W.N.Gade, M.V.Kulkarni, B.B.Kale. 2013. Silver-decorated orthorhombic nanotubes of lithium vanadium oxide: an impeder of bacterial growth and biofilm. Appl Microbiol Biot. 97:8283–8290. doi: 10.1007/s00253-013-5096-2.10.1007/s00253-013-5096-2
11. R.M.Donlan. 2002. Biofilms: microbial life on surfaces. Emerge Infect Dis. 8:881–890. doi: 10.3201/eid0809.020063.10.3201/eid0809.020063
12. C.A.Fux, P.A.Stoodly, L.Hall-Stoodly, J.W.Costerton. 2003. Bacterial biofilm: a diagnostic and therapeutic challenge. Expert Rev Anti-infect. 1:667–683. doi: 10.1586/14787210.1.4.667.10.1586/14787210.1.4.667
13. C.A.Fux, J.W.Costerton, P.S.Stewart, P.Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13:34–40. doi: 10.1016/j.tim.2004.11.010.10.1016/j.tim.2004.11.010
14. D.P.Gnanadhas, M.B.Thomas, R.Thomas, A.M.Raichur, D.Chakravortty. 2013. Interaction of silver nanoparticles with serum proteins affects their antimicrobial activity in vivo. Antimicrob Agents Chemother. 57:4945–4955. doi: 10.1128/AAC.00152-13.10.1128/AAC.00152-13
15. M.R.Hamblin, T.Hasan. 2004. Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem Photobiol. 3:436–450. doi: 10.1039/b311900a.10.1039/b311900a
16. S.Hasan, M.Danishuddin, M.Adil, K.Singh, P.K.Verma, A.U.Khan. 2012. Efficacy of E. officinalis on the cariogenic properties of Streptococcus mutans: a novel and alternative approach to suppress quorum-sensing mechanism. PLoS one. 7:e40319. doi: 10.1371/journal.pone.0040319.10.1371/journal.pone.0040319
17. S.Hasan, K.Singh, M.Danisuddin, P.K.Verma, A.U.Khan. 2014. Inhibition of major virulence pathways of Streptococcus mutans by quercitrin and deoxynojirimycin: a synergistic approach of infection control. PLoS one. 9:e91736. doi: 10.1371/journal.pone.0091736.10.1371/journal.pone.0091736
18. J.F.Hernández-Sierra, F.Ruiz, D.C.Cruz Pena. 2008. The antimicrobial sensitivity of Streptococcus mutans to nanoparticles of silver, zinc oxide, and gold. Nanomedicine. 4:237–240. doi: 10.1016/j.nano.2008.04.005.10.1016/j.nano.2008.04.005
19. L.Huang, T.G.St.Denis, Y.Xuan. 2012. Paradoxical potentiation of methylene blue-mediated antimicrobial photodynamic inactivation by sodium azide: role of ambient oxygen and azide radicals. Free Radical Bio Med. 53:2062–2071. doi: 10.1016/j.freeradbiomed.2012.09.006.10.1016/j.freeradbiomed.2012.09.006
20. A.Ichinose-Tsuno, A.Aoki, Y.Takeuchi. 2014. Antimicrobial photodynamic therapy suppressesdental plaque formation in healthy adults: a randomized controlled clinical trial. BMC Oral Health. 14:152–161. doi: 10.1186/1472-6831-14-152.10.1186/1472-6831-14-152
21. B.Islam, S.N.Khan, I.Haque, M.Alam, M.Mushfiq, A.U.Khan. 2008. Novel anti-adherence activity of mulberry leaves: inhibition of Streptococcus mutans biofilm by 1-deoxynojirimycin isolated from Morus alba. J Antimicrob Chemother. 62:751–757. doi: 10.1093/jac/dkn253.10.1093/jac/dkn253
22. S.Jaiswa, B.Duffy, A.K.Jaiswa, N.Stobie, P.McHale. 2010. Enhancement of the antibacterial properties of silver nanoparticles using-cyclodextrin as a capping agent. Int J Antimicrob Agents. 36:280–283. doi: 10.1016/j.ijantimicag.2010.05.006.10.1016/j.ijantimicag.2010.05.006
23. N.Kashef, G.R.S.Abadi, G.E.Djavid. 2012. Photodynamic inactivation of primary human fibroblasts by methylene blue and toluidine blue O. Photodiag Photodyn Ther. 9:355–358. doi: 10.1016/j.pdpdt.2012.05.001.10.1016/j.pdpdt.2012.05.001
24. K.R.Kasimova, M.Sadasivam, G.Landi, T.Sarnaf, M.R.Hamblin. 2014. Potentiation of photoinactivation of Gram-positive and Gram-negative bacteria mediated by six phenothiazinium dyes by addition of azide ion. Photochem Photobiol Sci. 13:1541–1548. doi: 10.1039/C4PP00021H.10.1039/C4PP00021H
25. M.K.Khaing Oo, Y.Yang, Y.Hu, M.Gomez, H.Du, H.Wang. 2012. Gold nanoparticle-enhanced and size-dependent generation of reactive oxygen species from protoporphyrin IX. ACS NANO. 6:1939–1947. doi: 10.1021/nn300327c.10.1021/nn300327c
26. S.Khan, F.Alam, A.Azam, A.U.Khan. 2012. Gold nanoparticles enhance methylene blue–induced photodynamic therapy: a novel therapeutic approach to inhibit Candida albicans biofilm. Int J Nanomedicine. 7:3245–3257. doi: 10.2147/IJN.10.2147/IJN
27. J.E.Krol, S.Biswas, C.King, I.Biswas. 2014. SMU.746-SMU.747 a putative membrane permease complex is involved in aciduricity acidogenesis and biofilm formation in Streptococcus mutans. J Bacteriol. 196:129–139. doi: 10.1128/JB.00960-13.10.1128/JB.00960-13
28. S.Kulshrestha, S.Khan, R.Meena, A.U.Khan. 2014. A graphene/zinc oxide nanocomposite film protects dental implant surfaces against cariogenic Streptococcus mutans. Biofouling. 30:1281–1294. doi: 10.1080/08927014.2014.983093.10.1080/08927014.2014.983093
29. W.T.Li. 2009. Nanotechology-based strategies to enhance the efficacy of photodynamic therapy for cancer. Current Drug Metabolism. 10:851–860. doi: 10.2174/138920009790274559.10.2174/138920009790274559
30. Y.H.Li, N.Tang, M.B.Aspiras, P.C.Y.Lau, J.H.Lee, R.P.Ellen, D.G.Cvitcovitch. 2002. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol. 184:2699–2708. doi: 10.1128/JB.184.10.2699-2708.2002.10.1128/JB.184.10.2699-2708.2002
31. W.J.Loesche. 1986. Role of Streptococcus mutans in human dental decay. Microbiol Rev. 50:353–380.
32. C.Y.Loo, D.A.Corliss, N.Ganeshkumar. 2000. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol. 182:1374–1382. doi: 10.1128/JB.182.5.1374-1382.2000.10.1128/JB.182.5.1374-1382.2000
33. M.Merchat, J.D.Spikes, G.Bertoloni, G.Jori. 1996. Studies on the mechanism of bacteria photosensitization by meso-substituted cationic porphyrins. J Photochem Photobiol B. 35:149–157. doi: 10.1016/S1011-1344(96)07321-6.10.1016/S1011-1344(96)07321-6
34. K.H.Metwalli, S.A.Khan, B.P.Krom, M.A.Jabra-Rizk. 2013. Streptococcus mutans, Candida albicans, and the human mouth: a sticky situation. PLoS Pathog. 9:e100361.
35. D.R.Monteiro, L.F.Gorup, A.S.Takamiya, A.C.Ruvollo-Filho, E.R.de Camargo, D.B.Barbosa. 2009. The growing importance of materials that prevent microbial adhesion: antimicrobial effect of medical devices containing silver. Int J Antimicrob Agents. 34:103–110. doi: 10.1016/j.ijantimicag.2009.01.017.10.1016/j.ijantimicag.2009.01.017
36. J.R.Morones, J.L.Elechiguerra, A.Camacho, K.Holt, J.B.Kouri, J.T.Rameίrez, M.J.Yacaman. 2005. The bactericidal effect of silver nanoparticles. Nanotechnology. 16:2346–2353. doi: 10.1088/0957-4484/16/10/059.10.1088/0957-4484/16/10/059
37. J.Nakonieczna, A.Rapacka-Zdonczyk, A.Kawiak, K.P.Bielawski, M.Grinholc. 2013. Sub-lethal photodynamic inactivation renders Staphylococcus aureus susceptible to silver nanoparticles. Photochem Photobiol Sci. 12:1622–1627. doi: 10.1039/c3pp50039j.10.1039/c3pp50039j
38. O.Oluola, L.Kong, L.Fein, L.E.Weisman. 2007. Lysostaphin in treatment of neonatal Staphylococcus aureus infection. Antimicrob Agents Chemother. 51:2198–2200. doi: 10.1128/AAC.00506-06.10.1128/AAC.00506-06
39. S.Perni, P.Prokopovich, J.Pratten, I.P.Parkin, M.Wilson. 2011. Nanoparticles: their potential use in antibacterial photodynamic therapy. Photochem Photobiol. 10:712–720. doi: 10.1039/c0pp00360c.10.1039/c0pp00360c
40. J.P.M.L.Rolim, M.A.S.de-Melo, S.F.Guedes, F.B.Albuquerque-Filho, J.R.de Souza, N.A.P.Nogueira, I.C.J.Zanin, L.K.A.Rodrigues. 2012. The antimicrobial activity of photodynamic therapy against Streptococcus mutans using different photosensitizers. J Photochem Photobiol B. 106:40–46. doi: 10.1016/j.jphotobiol.2011.10.001.10.1016/j.jphotobiol.2011.10.001
41. J.C.Scaiano, K.Stamplecoskie. 2013. Can surface plasmon fields provide a new way to photosensitize organic photoreactions? From designer nanoparticles to custom applications. J Phys Chem Lett. 4:1177–1187. doi: 10.1021/jz400002a.10.1021/jz400002a
42. M.Sharma, L.Visai, F.Bragheri, I.Cristiani, P.K.Gupta, P.Speziale. 2008. Toluidine blue-mediated photodynamic effects on staphylococcal biofilms. Antimicrob Agents Chemother. 52:299–305. doi: 10.1128/AAC.00988-07.10.1128/AAC.00988-07
43. A.Shrestha, M.R.Hamblin, A.Kishen. 2014. Photoactivated rose bengal functionalized chitosan nanoparticles produce antibacterial/biofilm activity and stabilize dentin-collagen. Nanomedicine. 10:491–501. doi: 10.1016/j.nano.2013.10.010.10.1016/j.nano.2013.10.010
44. D.Steinberg, D.Moreinos, J.Featherstone, M.Shemesh, O.Feuerstein. 2008. Genetic and physiological effects of noncoherent visible light combined with hydrogen peroxide on Streptococcus mutans in biofilm. Antimicrob Agents Chemother. 52:2626–2631. doi: 10.1128/AAC.01666-07.10.1128/AAC.01666-07
45. S.Y.E.Tan, S.C.Chew, S.Y.Y.Tan, M.Givskov, L.Yang. 2014. Emerging frontiers in detection and control of bacterial biofilms. Curr Opin Biotechnol. 26:1–6. doi: 10.1016/j.copbio.2013.08.002.10.1016/j.copbio.2013.08.002
46. M.Tanaka, M.Kinoshita, Y.Yoshihara, N.Shinomiya, S.Seki, K.Nemoto, T.Hirayama, T.Dai, L.Huang, M.R.Hamblin, Y.Morimoto. 2012. Optimal photosensitizers for photodynamic therapy of infections should kill bacteria but spare neutrophils. Photochem Photobiol. 88:227–232. doi: 10.1111/php.2011.88.issue-1.10.1111/php.2011.88.issue-1
47. A.Taraszkiewicz, G.Fila, M.Grinholc, J.Nakonieczna. 2013. Innovative stategies to overcome biofilm resistance. BioMed Research International. ID:150653.
48. A.Tavares, C.M.B.Carvalho, M.A.Faustino. 2010. Antimicrobial photodynamic therapy: study of bacterial recovery viability and potential development of resistance after treatment. Mar Drugs. 8:91–105. doi: 10.3390/md8010091.10.3390/md8010091
49. Q.H.Tran, V.Q.Nguyen, A.T.Le. 2013. Silver nanoparticles: synthesis, properties, toxicology, applications and perspectives. Adv Nat Sci. 4:033001.
50. J.Turkevich, P.C.Stevenson, J.Hillier. 1951. A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss Faraday Soc. 11:55–75. doi: 10.1039/df9511100055.10.1039/df9511100055
51. F.Vatansever, W.C.M.A.de Melo, P.Avci, D.Vecchio, M.Sadasivam, A.Gupta, R.Chandran, M.Karimi, N.A.Parizott, R.Yin,. 2013. Antimicrobial strategies centered around reactive oxygen species – bactericidal antibiotics, photodynamic therapy and beyond. FEMS Microbiol Rev. 37:955–989. doi: 10.1111/1574-6976.12026.10.1111/1574-6976.12026
52. M.Wainwright. 1998. Photodynamic antimicrobial chemotherapy (PACT). J Antimicrob Chemother. 42:13–28. doi: 10.1093/jac/42.1.13.10.1093/jac/42.1.13
53. S.Wood, B.Nattress, J.Kirkham, R.Shore, S.Brookes, J.Griffiths, C.Robinson. 1999. An in vitro study of the use of photodynamic therapy for the treatment of natural oral plaque biofilms formed in vivo. J Photochem Photobiol B. 50:1–7. doi: 10.1016/S1011-1344(99)00056-1.10.1016/S1011-1344(99)00056-1
54. I.C.J.Zanin, R.B.Goncalves, A.B.Junior, C.K.Hope, J.Pratten. 2005. Susceptibility of Streptococcus mutans biofilms to photodynamic therapy: an in vitro study. J Antimicrob Chemother. 56:324–330. doi: 10.1093/jac/dki232.10.1093/jac/dki232
55. B.Zeina, J.Greenman, Corry, W.M.Purcell. 2003. Antimicrobial photodynamic therapy: assessment of genotoxic effects on keratinocytes in vitro. Br J Derm. 148:229–232. doi: 10.1046/j.1365-2133.2003.05091.x.10.1046/j.1365-2133.2003.05091.x