Skip to main content
Top
Published in: Lasers in Medical Science 2/2016

01-02-2016 | Original Article

Photodynamic inactivation of antibiotic-resistant bacteria and biofilms by hematoporphyrin monomethyl ether

Authors: Chengcheng Liu, Min Hu, Dandan Ma, Jin’e Lei, Jiru Xu

Published in: Lasers in Medical Science | Issue 2/2016

Login to get access

Abstract

The worldwide increase in bacterial antibiotic resistance has led to a search for alternative antibacterial therapies. A promising approach to killing antibiotic-resistant bacteria is photodynamic antimicrobial chemotherapy, which uses light in combination with a photosensitizer to induce a phototoxic reaction. We evaluated the photodynamic inactivation (PDI) efficiency of hematoporphyrin monomethyl ether (HMME) on antibiotic-resistant bacteria and biofilms. HMME exhibited no significant dark toxicity and provided dose-dependent inactivation of antibiotic-resistant bacteria and biofilms. After incubation with 100-μM HMME and irradiation with 72-J cm−2 white light, 4.19–7.59 log10 reductions in survival were achieved in planktonic suspension. Antibiotic-resistant strains were as susceptible to PDI in biofilms as in planktonic suspensions, but the inactivation of bacterial cells in biofilms was attenuated. In addition, gram-positive bacterial strains and biofilms were more susceptible than gram-negative strains and biofilms to the PDI effect of HMME. Thus, HMME is a promising photosensitizer for the treatment of infectious diseases caused by antibiotic-resistant bacteria, especially gram-positive bacteria.
Literature
1.
go back to reference Butler MS, Buss AD (2006) Natural products—the future scaffolds for novel antibiotics. Biochem Pharmacol 71(7):919–929CrossRefPubMed Butler MS, Buss AD (2006) Natural products—the future scaffolds for novel antibiotics. Biochem Pharmacol 71(7):919–929CrossRefPubMed
2.
go back to reference Cornaglia G, Giamarellou H, Rossolini GM (2011) Metallo-β-lactamases: a last frontier for β-lactams. Lancet Infect Dis 11(5):381–393CrossRefPubMed Cornaglia G, Giamarellou H, Rossolini GM (2011) Metallo-β-lactamases: a last frontier for β-lactams. Lancet Infect Dis 11(5):381–393CrossRefPubMed
4.
go back to reference Sutherland IW (2001) The biofilm matrix—an immobilized but dynamic microbial environment. Trends Microbiol 9(5):222–227CrossRefPubMed Sutherland IW (2001) The biofilm matrix—an immobilized but dynamic microbial environment. Trends Microbiol 9(5):222–227CrossRefPubMed
5.
go back to reference Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358(9276):135–138CrossRefPubMed Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358(9276):135–138CrossRefPubMed
6.
go back to reference Denis TGS et al (2011) All you need is light: antimicrobial photoinactivation as an evolving and emerging discovery strategy against infectious disease. Virulence 2(6):509–520CrossRef Denis TGS et al (2011) All you need is light: antimicrobial photoinactivation as an evolving and emerging discovery strategy against infectious disease. Virulence 2(6):509–520CrossRef
7.
go back to reference Cassidy CM et al (2009) Drug delivery strategies for photodynamic antimicrobial chemotherapy: from benchtop to clinical practice. J Photochem Photobiol B 95(2):71–80CrossRefPubMed Cassidy CM et al (2009) Drug delivery strategies for photodynamic antimicrobial chemotherapy: from benchtop to clinical practice. J Photochem Photobiol B 95(2):71–80CrossRefPubMed
9.
go back to reference Ferro S et al (2007) Efficient photoinactivation of methicillin-resistant Staphylococcus aureus by a novel porphyrin incorporated into a poly-cationic liposome. Int J Biochem Cell Biol 39(5):1026–1034CrossRefPubMed Ferro S et al (2007) Efficient photoinactivation of methicillin-resistant Staphylococcus aureus by a novel porphyrin incorporated into a poly-cationic liposome. Int J Biochem Cell Biol 39(5):1026–1034CrossRefPubMed
10.
go back to reference Tsai T et al (2009) Improved photodynamic inactivation of Gram-positive bacteria using hematoporphyrin encapsulated in liposomes and micelles. Laser Surg Med 41(4):316–322CrossRef Tsai T et al (2009) Improved photodynamic inactivation of Gram-positive bacteria using hematoporphyrin encapsulated in liposomes and micelles. Laser Surg Med 41(4):316–322CrossRef
11.
go back to reference Jori G et al (2006) Photodynamic therapy in the treatment of microbial infections: basic principles and perspective applications. Laser Surg Med 38(5):468–481CrossRef Jori G et al (2006) Photodynamic therapy in the treatment of microbial infections: basic principles and perspective applications. Laser Surg Med 38(5):468–481CrossRef
12.
go back to reference Pu Y, Chen W, Yue Z (2012) Research progress of Hemoporfin-part one: preclinical study. Photodiagnosis Photodyn Ther 9(2):180–185CrossRefPubMed Pu Y, Chen W, Yue Z (2012) Research progress of Hemoporfin-part one: preclinical study. Photodiagnosis Photodyn Ther 9(2):180–185CrossRefPubMed
13.
go back to reference Li BH et al (2008) Singlet oxygen quantum yields of porphyrin-based photosensitizers for photodynamic therapy. J Innov Opt Health Sci 1(1):141–149CrossRef Li BH et al (2008) Singlet oxygen quantum yields of porphyrin-based photosensitizers for photodynamic therapy. J Innov Opt Health Sci 1(1):141–149CrossRef
14.
go back to reference Song K et al (2005) Phototoxicity of Hemoporfin to ovarian cancer. Biochem Biophys Res Commun 337(1):127–132CrossRefPubMed Song K et al (2005) Phototoxicity of Hemoporfin to ovarian cancer. Biochem Biophys Res Commun 337(1):127–132CrossRefPubMed
15.
go back to reference Cheng JL et al (2010) Hematoporphyrin monomethyl ether-mediated photodynamic effects on THP-1 cell derived macrophages. J Photochem Photobiol B 101(1):9–15CrossRefPubMed Cheng JL et al (2010) Hematoporphyrin monomethyl ether-mediated photodynamic effects on THP-1 cell derived macrophages. J Photochem Photobiol B 101(1):9–15CrossRefPubMed
16.
go back to reference Li BH et al (2010) Differences in sensitivity to HMME-mediated photodynamic therapy between EBV+ C666-1 and EBV-CNE2 cells. Photodiagnosis Photodyn Ther 7(3):204–209CrossRefPubMed Li BH et al (2010) Differences in sensitivity to HMME-mediated photodynamic therapy between EBV+ C666-1 and EBV-CNE2 cells. Photodiagnosis Photodyn Ther 7(3):204–209CrossRefPubMed
17.
go back to reference Peng Z et al (2011) Quaternized chitosan inhibits icaA transcription and biofilm formation by Staphylococcus on a titanium surface. Antimicrob Agents Chemother 55(2):860–866CrossRefPubMedCentralPubMed Peng Z et al (2011) Quaternized chitosan inhibits icaA transcription and biofilm formation by Staphylococcus on a titanium surface. Antimicrob Agents Chemother 55(2):860–866CrossRefPubMedCentralPubMed
18.
go back to reference Tan HL et al (2012) The use of quaternised chitosan-loaded PMMA to inhibit biofilm formation and downregulate the virulence-associated geneexpression of antibiotic-resistant staphylococcus. Biomaterials 33(2):365–377CrossRefPubMed Tan HL et al (2012) The use of quaternised chitosan-loaded PMMA to inhibit biofilm formation and downregulate the virulence-associated geneexpression of antibiotic-resistant staphylococcus. Biomaterials 33(2):365–377CrossRefPubMed
19.
go back to reference Drescher K et al (2013) Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems. Proc Natl Acad Sci U S A 110(11):4345–4350CrossRefPubMedCentralPubMed Drescher K et al (2013) Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems. Proc Natl Acad Sci U S A 110(11):4345–4350CrossRefPubMedCentralPubMed
20.
go back to reference Beirão S et al (2014) Photodynamic inactivation of bacterial and yeast biofilms with a cationic porphyrin. Photochem Photobiol 90(6):1387–1396CrossRefPubMed Beirão S et al (2014) Photodynamic inactivation of bacterial and yeast biofilms with a cationic porphyrin. Photochem Photobiol 90(6):1387–1396CrossRefPubMed
21.
go back to reference Arrojado C et al (2011) Applicability of photodynamic antimicrobial chemotherapy as an alternative to inactivate fish pathogenic bacteria in aquaculture systems. Photochem Photobiol Sci 10(10):1691–1700CrossRefPubMed Arrojado C et al (2011) Applicability of photodynamic antimicrobial chemotherapy as an alternative to inactivate fish pathogenic bacteria in aquaculture systems. Photochem Photobiol Sci 10(10):1691–1700CrossRefPubMed
22.
23.
24.
go back to reference Jori G, Brown SB (2004) Photosensitized inactivation of microorganisms. Photochem Photobiol Sci 3(5):403–405CrossRefPubMed Jori G, Brown SB (2004) Photosensitized inactivation of microorganisms. Photochem Photobiol Sci 3(5):403–405CrossRefPubMed
25.
go back to reference Tsubery H et al (2000) Structure-function studies of polymyxin B nonapeptide: implications to sensitization of gram-negative bacteria. J Med Chem 43(16):3085–3092CrossRefPubMed Tsubery H et al (2000) Structure-function studies of polymyxin B nonapeptide: implications to sensitization of gram-negative bacteria. J Med Chem 43(16):3085–3092CrossRefPubMed
26.
go back to reference Schastak S et al (2010) Efficient photodynamic therapy against gram-positive and gram-negative bacteria using THPTS, a cationic photosensitizer excited by infrared wavelength. Plos One 5(7), e11674CrossRefPubMedCentralPubMed Schastak S et al (2010) Efficient photodynamic therapy against gram-positive and gram-negative bacteria using THPTS, a cationic photosensitizer excited by infrared wavelength. Plos One 5(7), e11674CrossRefPubMedCentralPubMed
27.
go back to reference Costa DCS et al (2012) Comparative photodynamic inactivation of antibiotic resistant bacteria by first and second generation cationic photosensitizers. Photochem Photobiol Sci 11(12):1095–1913 Costa DCS et al (2012) Comparative photodynamic inactivation of antibiotic resistant bacteria by first and second generation cationic photosensitizers. Photochem Photobiol Sci 11(12):1095–1913
28.
go back to reference Demidova T, Hamblin M (2005) Effect of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother 49(6):2329–2335CrossRefPubMedCentralPubMed Demidova T, Hamblin M (2005) Effect of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother 49(6):2329–2335CrossRefPubMedCentralPubMed
29.
go back to reference Cormick MP et al (2009) Photodynamic inactivation of Candida albicans sensitized by tri- and tetra-cationic porphyrin derivatives. Eur J Med Chem 44(4):1592–1599CrossRefPubMed Cormick MP et al (2009) Photodynamic inactivation of Candida albicans sensitized by tri- and tetra-cationic porphyrin derivatives. Eur J Med Chem 44(4):1592–1599CrossRefPubMed
30.
go back to reference Mah TFC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9(1):34–39CrossRefPubMed Mah TFC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9(1):34–39CrossRefPubMed
31.
go back to reference Pereira MA et al (2014) Influence of external bacterial structures in the efficiency of photodynamic inactivation by a cationic porphyrin. Photochem Photobiol Sci 13(4):680–690CrossRefPubMed Pereira MA et al (2014) Influence of external bacterial structures in the efficiency of photodynamic inactivation by a cationic porphyrin. Photochem Photobiol Sci 13(4):680–690CrossRefPubMed
32.
go back to reference Street CN et al (2009) In vitro photodynamic eradication of Pseudomonas aeruginosa in planktonic and biofilm culture. Photochem Photobiol 85(1):137–143CrossRefPubMed Street CN et al (2009) In vitro photodynamic eradication of Pseudomonas aeruginosa in planktonic and biofilm culture. Photochem Photobiol 85(1):137–143CrossRefPubMed
33.
go back to reference Lee CF et al (2004) 5-Aminolaevulinic acid mediated photodynamic antimicrobial chemotherapy on Pseudomonas aeruginosa planktonic and biofilm cultures. J Photochem Photobiol B Biol 75(1–2):21–25CrossRef Lee CF et al (2004) 5-Aminolaevulinic acid mediated photodynamic antimicrobial chemotherapy on Pseudomonas aeruginosa planktonic and biofilm cultures. J Photochem Photobiol B Biol 75(1–2):21–25CrossRef
Metadata
Title
Photodynamic inactivation of antibiotic-resistant bacteria and biofilms by hematoporphyrin monomethyl ether
Authors
Chengcheng Liu
Min Hu
Dandan Ma
Jin’e Lei
Jiru Xu
Publication date
01-02-2016
Publisher
Springer London
Published in
Lasers in Medical Science / Issue 2/2016
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-015-1859-6

Other articles of this Issue 2/2016

Lasers in Medical Science 2/2016 Go to the issue