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Review

An Insight on Bacterial Cellular Targets of Photodynamic Inactivation

Eliana Alves1 Department of Biology & CESAM, University of Aveiro, 3810-193 Aveiro, PortugalView further author information
,
Maria Af Faustino2 Department of Chemistry & QOPNA, University of Aveiro, 3810-193 Aveiro, PortugalView further author information
,
Maria Gpms Neves2 Department of Chemistry & QOPNA, University of Aveiro, 3810-193 Aveiro, PortugalView further author information
,
Angela Cunha1 Department of Biology & CESAM, University of Aveiro, 3810-193 Aveiro, PortugalView further author information
,
Joao Tome2 Department of Chemistry & QOPNA, University of Aveiro, 3810-193 Aveiro, Portugal;3 Department of Organic Chemistry, Ghent University, B-9000Gent, Belgium. [email protected]Correspondence[email protected]
View further author information
&
Adelaide Almeida1 Department of Biology & CESAM, University of Aveiro, 3810-193 Aveiro, PortugalView further author information
Pages 141-164 | Published online: 28 Jan 2014

References

  • World Health Organisation. The evolving threat of antimicrobial resistance: options for action. WHO Press, Geneva, Switzerland (2012).
  • Leung E , WeilDE, RaviglioneM, NakataniH. The WHO policy package to combat antimicrobial resistance.Bull. World Health Organ.89(5), 390–392 (2011).
  • Wang J -F, Chou K-C. Metallo-β-lactamases: structural features, antibiotic recognition, inhibition, and inhibitor design. Curr. Top. Med. Chem.13(10), 1242–1253 (2013).
  • Liu Y , ImlayJA. Cell death from antibiotics without the involvement of reactive oxygen species.Science339(6124), 1210–1213 (2013).
  • Thakor NS , WilsonKS, ScottPG, TaylorDE. An improved procedure for expression and purification of ribosomal protection protein Tet (O) for high-resolution structural studies.Protein Expression Purif.55(2), 388–394 (2007).
  • Witte W , CunyC, KlareI, NübelU, StrommengerB, WernerG. Emergence and spread of antibiotic-resistant Gram-positive bacterial pathogens.Int. J. Med. Microbiol.298(5), 365–377 (2008).
  • Wainwright M , AmaralL. Photobactericides – a local option against multi-drug resistant bacteria.Antibiotics2(2), 182–190 (2013).
  • Foote CS . Definition of type I and type II photosensitized oxidation.Photochem. Photobiol.54(5), 659–659 (1991).
  • Girotti AW . Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms.J. Photochem. Photobiol. B63(1–3), 103–113 (2001).
  • Dai T , Huang Y-Y, Hamblin MR. Photodynamic therapy for localized infections – state of the art. Photodiagn. Photodyn. Ther.6(3), 170–188 (2009).
  • Kharkwal GB , SharmaSK, Huang Y-Y, Dai T, Hamblin MR. Photodynamic therapy for infections: clinical applications. Lasers Surg. Med.43(7), 755–767 (2011).
  • Almeida A , CunhaA, FaustinoM, ToméA, NevesM. Porphyrins as antimicrobial photosensitizing agents. In: Photodynamic Inactivation of Microbial Pathogens: Medical and Environmental Applications. Hamblin M, Jori G (Eds). Royal Society of Chemistry, Cambridge, UK, 83–160 (2011).
  • Wainwright M . Photodynamic medicine and infection control.J. Antimicrob. Chemother.67(4), 787–788 (2012).
  • Huang L , TerakawaM, ZhiyentayevTet al. Innovative cationic fullerenes as broad-spectrum light-activated antimicrobials. Nanomedicine 6(3), 442–452 (2010).
  • Sharma SK , Huang Y-Y, Mroz P, Wharton T, Chiang LY, Hamblin MR. Fullerenes in photodynamic therapy. Nanomedicine (Lond.)6(10), 1813–1825 (2011).
  • Tegos GP , DemidovaTN, Arcila-LopezDet al. Cationic fullerenes are effective and selective antimicrobial photosensitizers. Chem. Biol. 12(10), 1127–1135 (2005).
  • Cieplik F , SpäthA, RegensburgerJet al. Photodynamic biofilm-inactivation by SAPYR–an exclusive singlet oxygen photosensitizer. Free Radic. Biol. Med. 65, 477–487 (2013).
  • Tardivo JP , Del GiglioA, de OliveiraCSet al. Methylene blue in photodynamic therapy: from basic mechanisms to clinical applications. Photodiagnosis Photodyn. Ther.2(3), 175–191 (2005).
  • Tavares A , DiasSRS, CarvalhoCMBet al. Mechanisms of photodynamic inactivation of a Gram-negative recombinant bioluminescent bacterium by cationic porphyrins. Photochem. Photobiol. Sci. 10(10), 1659–1669 (2011).
  • Agostinis P , BergK, CengelKAet al. Photodynamic therapy of cancer: an update. CA Cancer J. Clin. 61(4), 250–281 (2011).
  • Nonell S , GonzalezM, TrullFR. 1H-phenalen-1-one-2-sulfonic acid-an extremely efficient singlet molecular-oxygen sensitizer for aqueous-media.Afinidad50(448), 445–450 (1993).
  • Juzeniene A , NielsenKP, MoanJ. Biophysical aspects of photodynamic therapy.J. Environ. Pathol. Toxicol. Oncol.25(1–2), (2006).
  • Sharman WM , AllenCM, Van Lier JE. Role of activated oxygen species in photodynamic therapy. Methods Enzymol.319, 376–400 (2000).
  • Bronshtein I , AfriM, WeitmanH, FrimerAA, SmithKM, EhrenbergB. Porphyrin depth in lipid bilayers as determined by iodide and parallax fluorescence quenching methods and its effect on photosensitizing efficiency.Biophys. J.87(2), 1155–1164 (2004).
  • Krasnovsky A Jr. Singlet molecular oxygen in photobiochemical systems: IR phosphorescence studies. Membr. Cell Biol.12(5), 665 (1998).
  • Moan J . On the diffusion length of singlet oxygen in cells and tissues.J. Photochem. Photobiol.B6, 343–344 (1990).
  • Ochsner M . Photophysical and photobiological processes in the photodynamic therapy of tumours.J. Photochem. Photobiol. B39(1), 1–18 (1997).
  • Bergamini CM , GambettiS, DondiA, CervellatiC. Oxygen, reactive oxygen species and tissue damage.Curr. Pharm. Des.10(14), 1611–1626 (2004).
  • Plaetzer K , KrammerB, BerlandaJ, BerrF, KiesslichT. Photophysics and photochemistry of photodynamic therapy: fundamental aspects.Lasers Med. Sci.24(2), 259–268 (2009).
  • Pushpan SK , VenkatramanS, AnandVGet al. Porphyrins in photodynamic therapy – a search for ideal photosensitizers. Curr. Med. Chem. Anti-Cancer Agents 2(2), 187–207 (2002).
  • Prasad PN . Introduction to Biophotonics. John Wiley and Sons, NY, USA (2004).
  • Wainwright M , PhoenixD, LaycockS, WareingD, WrightP. Photobactericidal activity of phenothiazinium dyes against methicillin-resistant strains of Staphylococcus aureus. FEMS Microbiol Lett.160(2), 177–181 (1998).
  • Wainwright M , PhoenixD, MarlandJ, WareingD, BoltonF. A study of photobactericidal activity in the phenothiazinium series.FEMS Immunol. Med. Microbiol.19(1), 75–80 (1997).
  • Pereira GF , MaischT. XF drugs: A new family of antibacterials.Drug News Perspect.23(3), 167 (2010).
  • Soukos NS , WilsonM, BurnsT, SpeightPM. Photodynamic effects of toluidine blue on human oral keratinocytes and fibroblasts and Streptococcus sanguis evaluated in vitro. Lasers Surg. Med.18(3), 253–259 (1996).
  • Silhavy TJ , KahneD, WalkerS. The bacterial cell envelope.Cold Spring Harbor Perspect. Biol.2(5), a000414 (2010).
  • Vollmer W , SeligmanSJ. Architecture of peptidoglycan: more data and more models.Trends Microbiol.18(2), 59–66 (2010).
  • St. Denis TG , DaiT, IziksonLet al. All you need is light: antimicrobial photoinactivation as an evolving and emerging discovery strategy against infectious disease. Virulence 2(6), 509–520 (2011).
  • Costa L , Faustino MaF, Neves MGP, Cunha Â, Almeida A. Photodynamic inactivation of mammalian viruses and bacteriophages. Viruses4(7), 1034–1074 (2012).
  • George S , HamblinMR, KishenA. Uptake pathways of anionic and cationic photosensitizers into bacteria.Photochem. Photobiol. Sci.8(6), 788–795 (2009).
  • Nitzan Y , GuttermanM, MalikZ, EhrenbergB. Inactivation of Gram-negative bacteria by photosensitized porphyrins.Photochem. Photobiol.55(1), 89–96 (1992).
  • Minnock A , VernonDI, SchofieldJ, GriffithsJ, ParishJH, BrownSB. Mechanism of uptake of a cationic water-soluble pyridinium zinc phthalocyanine across the outer membrane of Escherichia coli. Antimicrob. Agents Chemother.44(3), 522–527 (2000).
  • Hancock RE . The bacterial outer membrane as a drug barrier.Trends Microbiol.5(1), 37–42 (1997).
  • Rose RK , MatthewsSP, HallRC. Investigation of calcium-binding sites on the surfaces of selected gram-positive oral organisms.Arch. Oral Biol.42(9), 595–599 (1997).
  • Wang X , QuinnPJ. Lipopolysaccharide: biosynthetic pathway and structure modification.Prog. Lipid Res.49(2), 97–107 (2010).
  • Jori G . Photodynamic therapy of microbial infections: state of the art and perspectives.J. Environ. Pathol. Toxicol. Oncol.25(1–2), 505–520 (2006).
  • Usacheva M , TeichertM, UsachevY, SievertC, BielM. Interaction of the photobactericides methylene blue and toluidine blue with a fluorophore in Pseudomonas aeruginosa cells. Lasers Surg. Med.40(1), 55–61 (2008).
  • Usacheva MN , TeichertMC, SievertCE, BielMA. Effect of Ca+ on the photobactericidal efficacy of methylene blue and toluidine blue against Gram-negative bacteria and the dye affinity for lipopolysaccharides.Lasers Med. Sci.38(10), 946–954 (2006).
  • Cronan JE . Bacterial membrane phospholipids: where do we stand?Annu. Rev. Microbiol.57(1), 203–224 (2003).
  • Domingues MM , CastanhoMA, SantosNC. rBPI21 promotes lipopolysaccharide aggregation and exerts its antimicrobial effects by (hemi) fusion of PG-containing membranes.PLoS ONE4(12), e8385 (2009).
  • Shireen T , SinghM, DhawanB, MukhopadhyayK. Characterization of cell membrane parameters of clinical isolates of Staphylococcus aureus with varied susceptibility to α-melanocyte stimulating hormone. Peptides37(2), 334–339 (2012).
  • Epand RM , EpandRF. Lipid domains in bacterial membranes and the action of antimicrobial agents.Biochim. Biophys. Acta Biomembr.1788(1), 289–294 (2009).
  • Cordeiro RM , MiottoR, BaptistaMS. Photodynamic efficiency of cationic meso-porphyrins at lipid bilayers: insights from molecular dynamics simulations.J. Phys. Chem. B116(50), 14618–14627 (2012).
  • de Sousa Neto D , HaweA, TabakM. Interaction of meso-tetrakis (4-N-methylpyridyl) porphyrin in its free base and as a Zn (II) derivative with large unilamellar phospholipid vesicles. Eur. Biophys. J.42, 267–279 (2013).
  • Pashkovskaya A , MaizlishV, ShaposhnikovG, KotovaE, AntonenkoY. Role of electrostatics in the binding of charged metallophthalocyanines to neutral and charged phospholipid membranes.Biochim. Biophys. Acta Biomembr.1778(2), 541–548 (2008).
  • Fiel RJ , Datta-GuptaN, MarkEH, HowardJC. Induction of DNA damage by porphyrin photosensitizers.Cancer Res.41(9 Part 1), 3543–3545 (1981).
  • Lang K , MosingerJ, WagnerováD. Photophysical properties of porphyrinoid sensitizers non-covalently bound to host molecules; models for photodynamic therapy.Coord. Chem. Rev.248(3), 321–350 (2004).
  • Viola G , DallacquaF. Photosensitization of biomolecules by phenothiazine derivatives.Curr. Drug Targets7(9), 1135–1154 (2006).
  • Dutikova I , BorisovaO, ShchelkinaAet al. [5, 10, 15, 20-tetra-(N-methyl-3-pyridyl) porphyrin destabilizes the anti-parallel telomeric quadruplex d (TTAGGG) 4]. Molekuliarnaia biologiia 44(5), 929–937 (2009).
  • Sari MA , BattioniJP, DupréD, MansuyD, le Pecq JB. Interaction of cationic porphyrins with DNA: importance of the number and position of the charges and minimum structural requirements for intercalation. Biochemistry29(17), 4205–4215 (1990).
  • Kovaleva OA , TsvetkovVB, ShchyolkinaAKet al. The role of carboxymethyl substituents in the interaction of tetracationic porphyrins with DNA. Eur. Biophys. J. 41(9), 723–732 (2012).
  • Epe B . DNA damage spectra induced by photosensitization.Photochem. Photobiol. Sci.11(1), 98–106 (2012).
  • Cadet J , DoukiT, BadouardC, FavierA, RavanatJL. Oxidatively generated damage to cellular DNA: mechanistic aspects. In: Oxidative Damage to Nucleic Acids. Evans M, Cooke M (Eds). Springer, NY, USA, 1–13 (2007).
  • Redmond RW , GamlinJN. A compilation of singlet oxygen yields from biologically relevant molecules.Photochem. Photobiol.70(4), 391–475 (1999).
  • Preuss A , ZeugnerL, HackbarthSet al. Photoinactivation of Escherichia coli (SURE2) without intracellular uptake of the photosensitizer. J. Appl. Microbiol. 114(1), 36–43 (2013).
  • Strakhovskaya M , AntonenkoYN, PashkovskayaAet al. Electrostatic binding of substituted metal phthalocyanines to enterobacterial cells: its role in photodynamic inactivation. Biochemistry (Moscow) 74(12), 1305–1314 (2009).
  • Alves E , FaustinoMA, ToméJPet al. Nucleic acid changes during photodynamic inactivation of bacteria by cationic porphyrins. Bioorg. Med. Chem. 21, 4311–4318 (2013).
  • Kato H , KomagoeK, NakanishiY, InoueT, KatsuT. Xanthene dyes induce membrane permeabilization of bacteria and erythrocytes by photoinactivation.Photochem. Photobiol.88(2), 423–431 (2012).
  • Pudziuvyte B , BakieneE, BonnettR, ShatunovPA, MagaraggiaM, JoriG. Alterations of Escherichia coli envelope as a consequence of photosensitization with tetrakis(N-ethylpyridinium-4-yl)porphyrin tetratosylate. Photochem. Photobiol. Sci.10(6), 1046–1055 (2011).
  • Jin H , HuangX, ChenYet al. Photoinactivation effects of hematoporphyrin monomethyl ether on Gram-positive and-negative bacteria detected by atomic force microscopy. Appl. Microbiol. Biotechnol. 88(3), 761–770 (2010).
  • Yow C , TangHM, ChuES, HuangZ. Hypericin-mediated photodynamic antimicrobial effect on clinically isolated pathogens.Photochem. Photobiol.88(3), 626–632 (2012).
  • George S , KishenA. Influence of photosensitizer solvent on the mechanisms of photoactivated killing of Enterococcus faecalis. Photochem. Photobiol.84(3), 734–740 (2008).
  • Caminos DA , SpesiaMB, PonsP, DurantiniEN. Mechanisms of Escherichia coli photodynamic inactivation by an amphiphilic tricationic porphyrin and 5,10,15,20-tetra(4-N,N,N-trimethylammoniumphenyl) porphyrin. Photochem. Photobiol. Sci.7(9), 1071–1078 (2008).
  • Demidova TN , HamblinMR. Effect of cell-photosensitizer binding and cell density on microbial photoinactivation.Antimicrob. Agents Chemother.49(6), 2329–2335 (2005).
  • Ergaieg K , SeuxR. A comparative study of the photoinactivation of bacteria by meso-substituted cationic porphyrin, rose Bengal and methylene blue.Desalination246(1), 353–362 (2009).
  • Gomes MC , SilvaS, FaustinoMAet al. Cationic galactoporphyrin photosensitisers against UV-B resistant bacteria: oxidation of lipids and proteins by 1O2. Photochem. Photobiol. Sci. 12(2), 262–271 (2013).
  • Fresno S , JiménezN, IzquierdoLet al. The ionic interaction of Klebsiella pneumoniae K2 capsule and core lipopolysaccharide. Microbiology 152(6), 1807–1818 (2006).
  • Wiese A , MünstermannM, GutsmannTet al. Molecular mechanisms of polymyxin B-membrane interactions: direct correlation between surface charge density and self-promoted transport. J. Membr. Biol. 162(2), 127–138 (1998).
  • Komagoe K , KatoH, InoueT, KatsuT. Continuous real-time monitoring of cationic porphyrin-induced photodynamic inactivation of bacterial membrane functions using electrochemical sensors.Photochem. Photobiol. Sci.10(7), 1181–1188 (2011).
  • Spesia MB , CaminosDA, PonsP, DurantiniEN. Mechanistic insight of the photodynamic inactivation of Escherichia coli by a tetracationic zinc (II) phthalocyanine derivative. Photodiagn. Photodyn. Ther.6(1), 52–61 (2009).
  • Ragàs X , AgutM, NonellS. Singlet oxygen in Escherichia coli: new insights for antimicrobial photodynamic therapy. Free Radical Biol. Med.49(5), 770–776 (2010).
  • Alves E , CostaL, CarvalhoCet al. Charge effect on the photoinactivation of Gram-negative and Gram-positive bacteria by cationic meso-substituted porphyrins. BMC Microbiol. 9(1), 70 (2009).
  • Nitzan Y , AshkenaziH. Photoinactivation of Acinetobacter baumannii and Escherichia coli B by a cationic hydrophilic porphyrin at various light wavelengths. Curr. Microbiol.42(6), 408–414 (2001).
  • Walther J , BröckerMJ, WätzlichDet al. Protochlorophyllide: a new photosensitizer for the photodynamic inactivation of Gram-positive and Gram-negative bacteria. FEMS Microbiol. Lett. 290(2), 156–163 (2009).
  • Ladan H , NitzanY, MalikZ. The antibacterial activity of haemin compared with cobalt, zinc and magnesium protoporphyrin and its effect on potassium loss and ultrastructure of Staphylococcus aureus. FEMS Microbiol. Lett.112(2), 173–177 (1993).
  • Spesia MB , DurantiniEN. Photodynamic inactivation mechanism of Streptococcus mitis sensitized by zinc (II) 2, 9, 16, 23-tetrakis [2-(N,N,N-trimethylamino) ethoxy] phthalocyanine. J. Photochem. Photobiol. B125, 179–187 (2013).
  • Du W , SunC, LiangZ, HanY, YuJ. Antibacterial activity of hypocrellin A against Staphylococcus aureus. World J. Microbiol. Biotechnol.28(11), 3151–3157 (2012).
  • Webb HK , TruongVK, HasanJ, CrawfordRJ, IvanovaEP. Physico-mechanical characterisation of cells using atomic force microscopy – current research and methodologies.J. Microbiol. Methods86(2), 131–139 (2011).
  • Wright CJ , ShahMK, PowellLC, ArmstrongI. Application of AFM from microbial cell to biofilm.Scanning32(3), 134–149 (2010).
  • Sahu K , BansalH, MukherjeeC, SharmaM, GuptaPK. Atomic force microscopic study on morphological alterations induced by photodynamic action of toluidine blue O in Staphylococcus aureus and Escherichia coli. J. Photochem. Photobiol. B96(1), 9–16 (2009).
  • Lin S -L, Hu J-M, Tang S-S, Wu X-Y, Chen Z-Q, Tang S-Z. Photodynamic inactivation of methylene blue and tungsten-halogen lamp light against food pathogen Listeria monocytogenes. Photochem. Photobiol.88(4), 985–991 (2012).
  • Núñez SC , RibeiroMS, GarcezAS, MiyakawaW. Assessment of photodynamic damage on Escherichia coli via atomic force microscopy. Presented at: SPIE Photonics Europe. Brussels, Belgium, 12–16 April 2010.
  • Boulos L , PrevostM, BarbeauB, CoallierJ, DesjardinsR. LIVE/DEAD® Bac Light™: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J. Microbiol. Methods37(1), 77–86 (1999).
  • Chen CZ , CooperSL. Interactions between dendrimer biocides and bacterial membranes.Biomaterials23(16), 3359–3368 (2002).
  • Romanova NA , BrovkoLY, MooreLet al. Assessment of photodynamic destruction of Escherichia coli O157:H7 and Listeria monocytogenes by using ATP bioluminescence. Appl. Environ. Microbiol. 69(11), 6393–6398 (2003).
  • von Ballmoos C , WiedenmannA, DimrothP. Essentials for ATP synthesis by F1F0 ATP synthases.Annu. Rev. Biochem.78(1), 649–672 (2009).
  • Valduga G , BredaB, GiacomettiGM, JoriG, ReddiE. Photosensitization of wild and mutant strains of Escherichia coli by meso-tetra(N-methyl-4-pyridyl)porphine. Biochem. Biophys. Res. Commun.256(1), 84–88 (1999).
  • Kato H , KomagoeK, InoueT, KatsuT. In situ monitoring of photodynamic inactivation of the membrane functions of bacteria using electrochemical sensors. Anal. Sci.26(10), 1019–1021 (2010).
  • Davies MJ . Singlet oxygen-mediated damage to proteins and its consequences.Biochem. Biophys. Res. Commun.305(3), 761–770 (2003).
  • Pattison DI , RahmantoAS, DaviesMJ. Photo-oxidation of proteins.Photochem. Photobiol. Sci.11(1), 38–53 (2012).
  • Segalla A , BorsarelliCD, BraslavskySEet al. Photophysical, photochemical and antibacterial photosensitizing properties of a novel octacationic Zn(II)-phthalocyanine. Photochem. Photobiol. Sci. 1(9), 641–648 (2002).
  • Dosselli R , MillioniR, PuricelliLet al. Molecular targets of antimicrobial photodynamic therapy identified by a proteomic approach. J. Proteomics 77, 329–343 (2012).
  • Tseng S , TengL, ChenCet al. Toluidine blue O photodynamic inactivation on multidrug-resistant Pseudomonas aeruginosa. Lasers Surg. Med. 41(5), 391–397 (2009).
  • Bertoloni G , LauroFM, CortellaG, MerchatM. Photosensitizing activity of hematoporphyrin on Staphylococcus aureus cells. Biochim. Biophys. Acta1475(2), 169–174 (2000).
  • Stark G . Functional consequences of oxidative membrane damage.J. Membr. Biol.205(1), 1–16 (2005).
  • Imlay JA . Pathways of oxidative damage.Annu. Rev. Microbiol.57(1), 395–418 (2003).
  • Usacheva MN , TeichertMC, BielMA. The interaction of lipopolysaccharides with phenothiazine dyes.Lasers Med. Sci.33(5), 311–319 (2003).
  • Alves E , MeloT, SimõesCet al. Photodynamic oxidation of Staphylococcus warneri membrane phospholipids: new insights based on lipidomics. Rapid Commun. Mass Spectrom. 27(14), 1607–1618 (2013).
  • Alves E , SantosN, MeloTet al. Photodynamic oxidation of Escherichia coli membrane phospholipids: new insights based on lipidomics. Rapid Commun. Mass Spectrom. 27(23), 2717–2728 (2013).
  • Salmon-Divon M , NitzanY, MalikZ. Mechanistic aspects of Escherichia coli photodynamic inactivation by cationic tetra-meso(N-methylpyridyl)porphine. Photochem. Photobiol. Sci.3(5), 423–429 (2004).
  • Ruiz-González R , WhiteJH, AgutM, NonellS, FlorsC. A genetically-encoded photosensitiser demonstrates killing of bacteria by purely endogenous singlet oxygen.Photochem. Photobiol. Sci.11(9), 1411–1413 (2012).
  • Schäfer M , SchmitzC, HorneckG. High sensitivity of Deinococcus radiodurans to photodynamically-produced singlet oxygen. Int. J. Radiat. Biol.74(2), 249–253 (1998).
  • Taraszkiewicz A , FilaG, GrinholcM, NakoniecznaJ. Innovative strategies to overcome biofilm resistance.Biomed Res. Int.2013, 150653 (2013).
  • Kishen A , HaapasaloM. Biofilm models and methods of biofilm assessment.Endodontic Topics22(1), 58–78 (2010).
  • Li X , GuoH, TianQet al. Effects of 5-aminolevulinic acid–mediated photodynamic therapy on antibiotic-resistant staphylococcal biofilm: an in vitro study. J. Surg. Res. 84(2), 1013–1021 (2013).
  • Saino E , SbarraMS, ArciolaCRet al. Photodynamic action of tri-meso (N-methylpyridyl), meso (N-tetradecyl-pyridyl) porphine on Staphylococcus epidermidis biofilms grown on Ti6Al4V alloy. Int. J. Artif. Organs 33(9), 636–645 (2010).
  • Sbarra MS , di PotoA, ArciolaCRet al. Photodynamic action of merocyanine 540 on Staphylococcus epidermidis biofilms. Int. J. Artif. Organs31(9), 848–857 (2008).
  • di Poto A , SbarraMS, ProvenzaG, VisaiL, SpezialeP. The effect of photodynamic treatment combined with antibiotic action or host defence mechanisms on Staphylococcus aureus biofilms. Biomaterials30(18), 3158–3166 (2009).
  • Eick S , MarkauskaiteG, NietzscheS, LaugischO, SalviGE, SculeanA. Effect of photoactivated disinfection with a light-emitting diode on bacterial species and biofilms associated with periodontitis and peri-implantitis.Photodiagn. Photodyn. Ther.10(2), 156–167 (2013).
  • Sharma M , VisaiL, BragheriF, CristianiI, GuptaPK, SpezialeP. Toluidine blue-mediated photodynamic effects on staphylococcal biofilms.Antimicrob. Agents Chemother.52(1), 299–305 (2008).
  • Collins TL , MarkusEA, HassettDJ, RobinsonJB. The effect of a cationic porphyrin on Pseudomonas aeruginosa biofilms. Curr. Microbiol.61(5), 411–416 (2010).
  • Kishen A , UpadyaM, TegosGP, HamblinMR. Efflux pump inhibitor potentiates antimicrobial photodynamic inactivation of Enterococcus faecalis biofilm. Photochem. Photobiol.86(6), 1343–1349 (2010).
  • Fontana C , AbernethyA, SomSet al. The antibacterial effect of photodynamic therapy in dental plaque-derived biofilms. J. Periodontal Res. 44(6), 751–759 (2009).
  • Gad F , ZahraT, HasanT, HamblinMR. Effects of growth phase and extracellular slime on photodynamic inactivation of gram-positive pathogenic bacteria.Antimicrob. Agents Chemother.48(6), 2173–2178 (2004).
  • Lauro FM , PrettoP, CovoloL, JoriG, BertoloniG. Photoinactivation of bacterial strains involved in periodontal diseases sensitized by porphycene–polylysine conjugates.Photochem. Photobiol. Sci.1(7), 468–470 (2002).
  • Pedigo LA , GibbsAJ, ScottRJ, StreetCN. Absence of bacterial resistance following repeat exposure to photodynamic therapy. 73803H–73803H (2009).
  • Tavares A , CarvalhoC, FaustinoMAet al. Antimicrobial photodynamic therapy: study of bacterial recovery viability and potential development of resistance after treatment. Mar. Drugs 8(1), 91–105 (2010).
  • Giuliani F , MartinelliM, CocchiA, ArbiaD, FantettiL, RoncucciG. In vitro resistance selection studies of RLP068/Cl, a new Zn(II) phthalocyanine suitable for antimicrobial photodynamic therapy. Antimicrob. Agents Chemother.54(2), 637–642 (2010).
  • Nitzan Y , AshkenaziH. Photoinactivation of Deinococcus radiodurans: an unusual Gram-positive microorganism. Photochem. Photobiol.69(4), 505–510 (1999).
  • Grinholc M , SzramkaB, KurlendaJ, GraczykA, BielawskiKP. Bactericidal effect of photodynamic inactivation against methicillin-resistant and methicillin-susceptible Staphylococcus aureus is strain-dependent. J. Photochem. Photobiol. B90(1), 57–63 (2008).
  • Nakonieczna J , MichtaE, RybickaM, GrinholcM, Gwizdek-WiśniewskaA, BielawskiK. Superoxide dismutase is upregulated in Staphylococcus aureus following protoporphyrin-mediated photodynamic inactivation and does not directly influence the response to photodynamic treatment. BMC Microbiol.10(1), 323 (2010).
  • Kim SY , KwonOJ, ParkJW. Inactivation of catalase and superoxide dismutase by singlet oxygen derived from photoactivated dye.Biochimie83(5), 437–444 (2001).
  • Kömerik N , WilsonM, PooleS. The effect of photodynamic action on two virulence factors of Gram-negative bacteria.Photochem. Photobiol.72(5), 676–680 (2000).
  • Tubby S , WilsonM, NairS. Inactivation of staphylococcal virulence factors using a light-activated antimicrobial agent.BMC Microbiol.9(1), 211 (2009).
  • Kossakowska M , NakoniecznaJ, KawiakA, KurlendaJ, BielawskiKP, GrinholcM. Discovering the mechanisms of strain-dependent response of Staphylococcus aureus to photoinactivation: oxidative stress toleration, endogenous porphyrin level and strain’s virulence. Photodiagn. Photodyn. Ther.10(4), 348–355 (2013).
  • Bolean M , PaulinoTDP, ThedeiG Jr, Ciancaglini P. Photodynamic therapy with rose bengal induces GroEL expression in Streptococcus mutans. Photomed. Laser Surg.28(S1), S79–S84 (2010).
  • St. Denis TG , HuangL, DaiT, HamblinMR. Analysis of the bacterial heat shock response to photodynamic therapy-mediated oxidative stress.Photochem. Photobiol.87(3), 707–713 (2011).
  • Park HJ , MoonYH, YoonHE, ParkYM, YoonJH, BangIS. Agr function is upregulated by photodynamic therapy (PDT) for Staphylococcus aureus and is related to resistance against PDT. Microbiol. Immunol.57(8), 547–552 (2013).
  • Tegos GP , HamblinMR. Phenothiazinium antimicrobial photosensitizers are substrates of bacterial multidrug resistance pumps.Antimicrob. Agents Chemother.50(1), 196–203 (2006).
  • Tegos GP , MasagoK, AzizF, HigginbothamA, StermitzFR, HamblinMR. Inhibitors of bacterial multidrug efflux pumps potentiate antimicrobial photoinactivation.Antimicrob. Agents Chemother.52(9), 3202–3209 (2008).
  • Philipp-Dormston W , DossM. Comparison of porphyrin and heme biosynthesis in various heterotrophic bacteria.Enzyme16(1), 57 (1973).
  • Ormond AB , FreemanHS. Dye sensitizers for photodynamic therapy.Materials6(3), 817–840 (2013).
  • Hongcharu W , TaylorCR, ChangY, AghassiD, SuthamjariyaK, AndersonRR. Topical ALA-photodynamic therapy for the treatment of acne vulgaris.J. Invest. Dermatol.115(2), 183–192 (2000).
  • Fotinos N , ConvertM, Piffaretti J-C, Gurny R, Lange N. Effects on gram-negative and Gram-positive bacteria mediated by 5-aminolevulinic acid and 5-aminolevulinic acid derivatives. Antimicrob. Agents Chemother.52(4), 1366–1373 (2008).
  • van der Meulen F , IbrahimK, SterenborgH, AlphenL, MaikoeA, DankertJ. Photodynamic destruction of Haemophilus parainfluenzae by endogenously produced porphyrins. J. Photochem. Photobiol. B40(3), 204–208 (1997).
  • Nitzan Y , KauffmanM. Endogenous porphyrin production in bacteria by δ-aminolaevulinic acid and subsequent bacterial photoeradication.Lasers Med. Sci.14(4), 269–277 (1999).
  • Kennedy JC , PottierRH. New trends in photobiology: endogenous protoporphyrin IX, a clinically useful photosensitizer for photodynamic therapy.J. Photochem. Photobiol. B14(4), 275–292 (1992).
  • Szocs K , GaborF, CsikG, FidyJ. δ-aminolaevulinic acid-induced porphyrin synthesis and photodynamic inactivation of Escherichia coli B. J. Photochem. Photobiol. B50(1), 8–17 (1999).
  • Gabor F , SzocsK, MaillardP, CsikG. Photobiological activity of exogenous and endogenous porphyrin derivatives in Escherichia coli and Enterococcus hirae cells. Radiat. Environ. Biophys.40(2), 145–151 (2001).
  • Nitzan Y , Salmon-DivonM, ShporenE, MalikZ. ALA induced photodynamic effects on gram positive and negative bacteria.Photochem. Photobiol. Sci.3(5), 430–435 (2004).
  • Ashkenazi H , MalikZ, HarthY, NitzanY. Eradication of Propionibacterium acnes by its endogenic porphyrins after illumination with high intensity blue light. FEMS Immunol. Med. Microbiol.35(1), 17–24 (2003).
  • Dietel W , BolsenK, DicksonE, FritschC, PottierR, WendenburgR. Formation of water-soluble porphyrins and protoporphyrin IX in 5-aminolevulinic-acid-incubated carcinoma cells.J. Photochem. Photobiol. B33(3), 225–231 (1996).
  • Verkamp E , BackmanV, BjörnssonJ, SöllD, EggertssonG. The periplasmic dipeptide permease system transports 5-aminolevulinic acid in Escherichia coli. J. Bacteriol.175(5), 1452–1456 (1993).
  • Elliott T . Transport of 5-aminolevulinic acid by the dipeptide permease in Salmonella typhimurium. J. Bacteriol.175(2), 325–331 (1993).
  • Daniel H , SpanierB, KottraG, WeitzD. From bacteria to man: archaic proton-dependent peptide transporters at work.Physiology21(2), 93–102 (2006).
  • King ND , O‘brianMR. Identification of the lrp gene in Bradyrhizobium japonicum and its role in regulation of δ-aminolevulinic acid uptake. J. Bacteriol.179(5), 1828–1831 (1997).
  • Harris F , PierpointL. Photodynamic therapy based on 5-aminolevulinic acid and its use as an antimicrobial agent.Med. Res. Rev.32(6), 1292–1327 (2012).
  • Gaullier J -M, Berg K, Peng Q et al. Use of 5-aminolevulinic acid esters to improve photodynamic therapy on cells in culture. Cancer Res.57(8), 1481–1486 (1997).
  • Kloek J , AkkermansW, HenegouwenGM. Derivatives of 5-aminolevulinic acid for photodynamic therapy: enzymatic conversion into protoporphyrin.Photochem. Photobiol.67(1), 150–154 (1998).
  • Luppa P , JacobK, EhretW. The production of porphyrins from δ-aminolaevulinic acid by Haemophilus parainfluenzae. J. Med. Microbiol.39(4), 262–267 (1993).
  • Kjeldstad B , JohnssonA, SandbergS. Influence of pH on porphyrin production in Propionibacterium acnes. Arch. Dermatol. Res.276(6), 396–400 (1984).
  • Nitzan Y , MalikZ, KauffmanM, EhrenbergB. Induction of endogenic porphyrin production in bacteria and subsequent photoinactivation by various light sources. Presented at: BiOS Europe‘97. San Remo, Italy, 4–8 September 1997.
  • Nitzan Y , DrorR, LadanH, MalikZ, KimelS, GottfriedV. Structure-activity relationship of porphines for photoinactivation of bacteria.Photochem. Photobiol.62(2), 342–347 (1995).
  • Ramstad S , le Anh-Vu N, Johnsson A. The temperature dependence of porphyrin production in Propionibacterium acnes after incubation with 5-aminolevulinic acid (ALA) and its methyl ester (m-ALA). Photochem. Photobiol. Sci.5(1), 66–72 (2006).
  • Ramstad S , FutsaetherCM, JohnssonA. Porphyrin sensitization and intracellular calcium changes in the prokaryote Propionibacterium acnes. J. Photochem. Photobiol. B40(2), 141–148 (1997).
  • Luksiene Z , ZukauskasA. Prospects of photosensitization in control of pathogenic and harmful micro-organisms.J. Appl. Microbiol.107(5), 1415–1424 (2009).
  • Grinholc M , SzramkaB, OlenderK, GraczykA. Bactericidal effect of photodynamic therapy against methicillin-resistant Staphylococcus aureus strain with the use of various porphyrin photosensitizers. Acta Biochim. Pol.54(3), 665 (2007).
  • Wainwright M , SmalleyH, FlintC. The use of photosensitisers in acne treatment.J. Photochem. Photobiol. B105(1), 1–5 (2011).
  • Wainwright M . ‘Safe’ photoantimicrobials for skin and soft-tissue infections.Int. J. Antimicrob. Agents36(1), 14–18 (2010).
  • Wainwright M , CrossleyK. Methylene blue – a therapeutic dye for all seasons?J. Chemother.14(5), 431–443 (2002).
  • Brown S . Clinical developments in antimicrobial PDT. Presented at: 12th International Photodynamic Association World Congress Seattle. Seattle, WA, USA, 11–15 June 2009.
  • Mang TS , TayalDP, BaierR. Photodynamic therapy as an alternative treatment for disinfection of bacteria in oral biofilms.Lasers Surg. Med.44(7), 588–596 (2012).
  • Maisch T , WagnerJ, PapastamouVet al. Combination of 10% EDTA, Photosan, and a blue light hand-held photopolymerizer to inactivate leading oral bacteria in dentistry in vitro. J. Appl. Microbiol. 107(5), 1569–1578 (2009).
  • Engelhardt V , KrammerB, PlaetzerK. Antibacterial photodynamic therapy using water-soluble formulations of hypericin or mTHPC is effective in inactivation of Staphylococcus aureus. Photochem. Photobiol. Sci.9(3), 365–369 (2010).
  • Lüthi M , Besic GyengeE, EngstrümMet al. Hypericin- and mTHPC-mediated photodynamic therapy for the treatment of cariogenic bacteria. Med. Laser Appl.24(4), 227–236 (2009).

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