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Research article
Bioactive Compounds and Chemical Biology
Lycopene-induced hydroxyl radical causes oxidative DNA damage in Escherichia coli
School of Life Sciences, BK 21 Plus KNU Creative BioResearch Group, College of Natural Sciences, Kyungpook National University, Daegu 702-701, Republic of Korea
Received: June 3, 2014; Accepted: July 10, 2014
J. Microbiol. Biotechnol. 2014; 24(9): 1232-1237
Published September 28, 2014 https://doi.org/10.4014/jmb.1406.06009
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
Lycopene, which is a well-known red carotenoid pigment, has been drawing scientific interest
because of its potential biological functions. The current study reports that lycopene acts as a
bactericidal agent by inducing reactive oxygen species (ROS)-mediated DNA damage in
Escherichia coli. Lycopene treatment elevated the level of ROS—in particular, hydroxyl radicals
(•OH) —which can damage DNA in E. coli. Lycopene-induced DNA damage in bacteria was
confirmed and we also observed cell filamentation caused by cell division arrest, an indirect
marker of the DNA damage repair system, in lycopene-treated E. coli. Increased RecA
expression was observed, indicating activation of the DNA repair system (SOS response). To
summarize, lycopene exerts its antibacterial effects by inducing •OH -mediated DNA damage
that cannot be ameliorated by the SOS response. Lycopene may be a clinically useful adjuvant
for current antimicrobial therapies.
Keywords
Lycopene, hydroxyl radical, DNA damage, oxidative stress, Escherichia coli
References
- Arias CA, Murray BE. 2009. Antibiotic-resistant bugs in the 21st century - a clinical super-challenge. N. Engl. J. Med. 360: 439-443.
- Basu A, Imrhan V. 2007. Tomatoes versus lycopene in oxidative stress and carcinogenesis: conclusions from clinical trials. Eur. J. Clin. Nutr. 61: 295-303.
- Brynildsen MP, Winkler JA, Spina CS, MacDonald IS, Collins JJ. 2013. Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production. Nat. Biotechnol. 31: 160-165.
- Chandra RV, Prabhuji ML, Roopa DA, Ravirajan S, Kishore HC. 2008. Efficacy of lycopene in the treatment of gingivitis:a randomized, placebo-controlled clinical trial. J. Nutr. 138:49-53.
- Chen J, Jin K, Chen M, Pei W, Kawaguchi K, Greenberg DA, Simon RP. 1997. Early detection of DNA strand breaks in the brain after transient focal ischemia: implications for the role of DNA damage in apoptosis and neuronal cell death. J. Neurochem. 69: 232-245.
- Costa V, Moradas-Ferreira P. 2001. Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights in to aging, apoptosis and disease. Mol. Aspects Med. 22: 217-246.
- Cozzi R, Ricordy R, Aglitti T, Gatta V, Perticone P, De Salvia R. 1997. Ascorbic acid and beta-carotene as modulators of oxidative damage Carcinogenesis 18: 223-228.
- Cui J, Holmes EH, Greene TG, Liu PK. 2000. Oxidative DNA damage precedes DNA fragmentation after experimental stroke in rat brain. FASEB J. 14: 955-967.
- Daniel B, DeCoster MA. 2004. Quantification of sPSA-2 ind uced early a nd late apoptosis c hanges i n neuronal c ell cultures using combined TUNEL and DAPI staining. Brain Res. Protoc. 13: 144-150.
- Ferullo DJ, Lovett ST. 2008. The stringent response and cell cycle arrest in Escherichia coli. PLoS Genet. 4: e1000300.
- Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC. 2012. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 334: 315-319.
- Furuya EY, Lowy FD. 2006. Antimicrobial-resistant bacteria in the community setting. Nat. Rev. Microbiol. 4: 36-45.
- Han CH, Yang CH, Sohn DW, Kim SW, Kang SH, Cho YH. 2008. Synergistic effect between lycopene and ciprofloxacin on a chronic bacterial prostatitis rat model. Int. J. Antimicrob. Agents 31: 102-107.
- Huang D, Shenoy A, Cui JK, Huang W, Liu PK. 2000. In situ detection of AP sites and DNA strand breaks with 3’phosphate ends in ischemic mouse brain. FASEB J. 14: 407417.
- Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140.
- Kaufmann WK, Paules RS. 1996. DNA damage and cell cycle checkpoints. FASEB J. 10: 238-347.
- Klepser ME, Ernst EJ, Lewis RE, Ernst ME, Pfaller MA. 1998. Influence of test conditions on antifungal time-kill curve results: proposal for standardized methods. Antimicrob. Agents Chemother. 42: 1207-1212.
- Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797-810.
- Lowe GM, Booth LA, Young AJ, Bilton RF. 1999. Lycopene and beta-carotene protect against oxidative damage in HT29 cells at low concentrations but rapidly lose this capacity at higher doses. Free Radic. Res. 30: 141-151.
- Madeo F, Fröhlich E, Fröhlich KU. 1997. A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol. 139: 729-734.
- Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, Cohen SN. 2004. SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305:1629-1631.
- Phillips AJ, Sudbery I, Ramsdale M. 2003. Apoptosis induced by environmental stresses and amphothericin B in Candida albicans. Proc. Natl. Acad. Sci. USA 100: 14327-14332.
- Sanchez L. 2001. TCA protein precipitation. Protocols on line.
- Sharma V, Sakai Y, Smythe KA, Yokobayashi Y. 2012. Knockdown of recA gene expression by artificial small RNAs in Escherichia coli. Biochem. Biophys. Res. Commun. 430:256-259.
- Shkilnyj P, Koudelka MP, Koudelka GB. 2013. Bacteriophage 434 Hex protein prevents RecA-mediated repressor autocleavage. Viruses 5: 111-126.
- Sung WS, Lee IS, Lee DG. 2007. Damage to the cytoplasmic membrane a nd cell death c aused b y lycopene i n Candida albicans. J. Microbiol. Biotechnol. 17: 1797-1804.
- Tzur A, Kafri R, LeBleu VS, Lahav G, Kirschner MW. 2009. Cell growth and size homeostasis in proliferating animal cells. Science 325: 167-171.
- Zelezetsky I, Pacor S, Pag U, Papo N, Shai Y, Sahl HG, Tossi A. 2005. Controlled alteration of the shape and conformational stability of alpha-helical cell-lytic peptides:effect on mode of action and cell specificity. Biochem. J. 390:177-188.
- Zunino SJ, Ducore JM, Storms DH. 2007. Parthenolide induces significant apoptosis and production of reactive oxygen species in high-risk pre-B leukemia cells. Cancer Lett. 254:119-127.
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Research article
J. Microbiol. Biotechnol. 2014; 24(9): 1232-1237
Published online September 28, 2014 https://doi.org/10.4014/jmb.1406.06009
Copyright © The Korean Society for Microbiology and Biotechnology.
Lycopene-induced hydroxyl radical causes oxidative DNA damage in Escherichia coli
Wonyoung Lee 1 and Dong Gun Lee 1*
School of Life Sciences, BK 21 Plus KNU Creative BioResearch Group, College of Natural Sciences, Kyungpook National University, Daegu 702-701, Republic of Korea
Received: June 3, 2014; Accepted: July 10, 2014
Abstract
Lycopene, which is a well-known red carotenoid pigment, has been drawing scientific interest
because of its potential biological functions. The current study reports that lycopene acts as a
bactericidal agent by inducing reactive oxygen species (ROS)-mediated DNA damage in
Escherichia coli. Lycopene treatment elevated the level of ROS—in particular, hydroxyl radicals
(•OH) —which can damage DNA in E. coli. Lycopene-induced DNA damage in bacteria was
confirmed and we also observed cell filamentation caused by cell division arrest, an indirect
marker of the DNA damage repair system, in lycopene-treated E. coli. Increased RecA
expression was observed, indicating activation of the DNA repair system (SOS response). To
summarize, lycopene exerts its antibacterial effects by inducing •OH -mediated DNA damage
that cannot be ameliorated by the SOS response. Lycopene may be a clinically useful adjuvant
for current antimicrobial therapies.
Keywords: Lycopene, hydroxyl radical, DNA damage, oxidative stress, Escherichia coli
References
- Arias CA, Murray BE. 2009. Antibiotic-resistant bugs in the 21st century - a clinical super-challenge. N. Engl. J. Med. 360: 439-443.
- Basu A, Imrhan V. 2007. Tomatoes versus lycopene in oxidative stress and carcinogenesis: conclusions from clinical trials. Eur. J. Clin. Nutr. 61: 295-303.
- Brynildsen MP, Winkler JA, Spina CS, MacDonald IS, Collins JJ. 2013. Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production. Nat. Biotechnol. 31: 160-165.
- Chandra RV, Prabhuji ML, Roopa DA, Ravirajan S, Kishore HC. 2008. Efficacy of lycopene in the treatment of gingivitis:a randomized, placebo-controlled clinical trial. J. Nutr. 138:49-53.
- Chen J, Jin K, Chen M, Pei W, Kawaguchi K, Greenberg DA, Simon RP. 1997. Early detection of DNA strand breaks in the brain after transient focal ischemia: implications for the role of DNA damage in apoptosis and neuronal cell death. J. Neurochem. 69: 232-245.
- Costa V, Moradas-Ferreira P. 2001. Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights in to aging, apoptosis and disease. Mol. Aspects Med. 22: 217-246.
- Cozzi R, Ricordy R, Aglitti T, Gatta V, Perticone P, De Salvia R. 1997. Ascorbic acid and beta-carotene as modulators of oxidative damage Carcinogenesis 18: 223-228.
- Cui J, Holmes EH, Greene TG, Liu PK. 2000. Oxidative DNA damage precedes DNA fragmentation after experimental stroke in rat brain. FASEB J. 14: 955-967.
- Daniel B, DeCoster MA. 2004. Quantification of sPSA-2 ind uced early a nd late apoptosis c hanges i n neuronal c ell cultures using combined TUNEL and DAPI staining. Brain Res. Protoc. 13: 144-150.
- Ferullo DJ, Lovett ST. 2008. The stringent response and cell cycle arrest in Escherichia coli. PLoS Genet. 4: e1000300.
- Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC. 2012. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 334: 315-319.
- Furuya EY, Lowy FD. 2006. Antimicrobial-resistant bacteria in the community setting. Nat. Rev. Microbiol. 4: 36-45.
- Han CH, Yang CH, Sohn DW, Kim SW, Kang SH, Cho YH. 2008. Synergistic effect between lycopene and ciprofloxacin on a chronic bacterial prostatitis rat model. Int. J. Antimicrob. Agents 31: 102-107.
- Huang D, Shenoy A, Cui JK, Huang W, Liu PK. 2000. In situ detection of AP sites and DNA strand breaks with 3’phosphate ends in ischemic mouse brain. FASEB J. 14: 407417.
- Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140.
- Kaufmann WK, Paules RS. 1996. DNA damage and cell cycle checkpoints. FASEB J. 10: 238-347.
- Klepser ME, Ernst EJ, Lewis RE, Ernst ME, Pfaller MA. 1998. Influence of test conditions on antifungal time-kill curve results: proposal for standardized methods. Antimicrob. Agents Chemother. 42: 1207-1212.
- Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797-810.
- Lowe GM, Booth LA, Young AJ, Bilton RF. 1999. Lycopene and beta-carotene protect against oxidative damage in HT29 cells at low concentrations but rapidly lose this capacity at higher doses. Free Radic. Res. 30: 141-151.
- Madeo F, Fröhlich E, Fröhlich KU. 1997. A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol. 139: 729-734.
- Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, Cohen SN. 2004. SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305:1629-1631.
- Phillips AJ, Sudbery I, Ramsdale M. 2003. Apoptosis induced by environmental stresses and amphothericin B in Candida albicans. Proc. Natl. Acad. Sci. USA 100: 14327-14332.
- Sanchez L. 2001. TCA protein precipitation. Protocols on line.
- Sharma V, Sakai Y, Smythe KA, Yokobayashi Y. 2012. Knockdown of recA gene expression by artificial small RNAs in Escherichia coli. Biochem. Biophys. Res. Commun. 430:256-259.
- Shkilnyj P, Koudelka MP, Koudelka GB. 2013. Bacteriophage 434 Hex protein prevents RecA-mediated repressor autocleavage. Viruses 5: 111-126.
- Sung WS, Lee IS, Lee DG. 2007. Damage to the cytoplasmic membrane a nd cell death c aused b y lycopene i n Candida albicans. J. Microbiol. Biotechnol. 17: 1797-1804.
- Tzur A, Kafri R, LeBleu VS, Lahav G, Kirschner MW. 2009. Cell growth and size homeostasis in proliferating animal cells. Science 325: 167-171.
- Zelezetsky I, Pacor S, Pag U, Papo N, Shai Y, Sahl HG, Tossi A. 2005. Controlled alteration of the shape and conformational stability of alpha-helical cell-lytic peptides:effect on mode of action and cell specificity. Biochem. J. 390:177-188.
- Zunino SJ, Ducore JM, Storms DH. 2007. Parthenolide induces significant apoptosis and production of reactive oxygen species in high-risk pre-B leukemia cells. Cancer Lett. 254:119-127.
