DOI QR코드

DOI QR Code

Lycopene-Induced Hydroxyl Radical Causes Oxidative DNA Damage in Escherichia coli

  • Lee, Wonyoung (School of Life Sciences, BK 21 Plus KNU Creative BioResearch Group, College of Natural Sciences, Kyungpook National University) ;
  • Lee, Dong Gun (School of Life Sciences, BK 21 Plus KNU Creative BioResearch Group, College of Natural Sciences, Kyungpook National University)
  • Received : 2014.06.03
  • Accepted : 2014.07.10
  • Published : 2014.09.28

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

References

  1. Arias CA, Murray BE. 2009. Antibiotic-resistant bugs in the 21st century - a clinical super-challenge. N. Engl. J. Med. 360: 439-443. https://doi.org/10.1056/NEJMp0804651
  2. Basu A, Imrhan V. 2007. Tomatoes versus lycopene in oxidative stress and carcinogenesis: conclusions from clinical trials. Eur. J. Clin. Nutr. 61: 295-303.
  3. 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. https://doi.org/10.1038/nbt.2458
  4. 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. https://doi.org/10.1093/jn/138.1.49
  5. 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.
  6. 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. https://doi.org/10.1016/S0098-2997(01)00012-7
  7. 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. https://doi.org/10.1093/carcin/18.1.223
  8. 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. https://doi.org/10.1096/fasebj.14.7.955
  9. Daniel B, DeCoster MA. 2004. Quantification of sPSA-2 induced early and late apoptosis changes in neuronal cell cultures using combined TUNEL and DAPI staining. Brain Res. Protoc. 13: 144-150. https://doi.org/10.1016/j.brainresprot.2004.04.001
  10. Ferullo DJ, Lovett ST. 2008. The stringent response and cell cycle arrest in Escherichia coli. PLoS Genet. 4: e1000300. https://doi.org/10.1371/journal.pgen.1000300
  11. 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.
  12. Furuya EY, Lowy FD. 2006. Antimicrobial-resistant bacteria in the community setting. Nat. Rev. Microbiol. 4: 36-45. https://doi.org/10.1038/nrmicro1325
  13. 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. https://doi.org/10.1016/j.ijantimicag.2007.07.016
  14. 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: 407-417. https://doi.org/10.1096/fasebj.14.2.407
  15. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140. https://doi.org/10.1038/nrmicro818
  16. Kaufmann WK, Paules RS. 1996. DNA damage and cell cycle checkpoints. FASEB J. 10: 238-347. https://doi.org/10.1096/fasebj.10.2.8641557
  17. 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.
  18. 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. https://doi.org/10.1016/j.cell.2007.06.049
  19. 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. https://doi.org/10.1080/10715769900300151
  20. Madeo F, Fröhlich E, Fröhlich KU. 1997. A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol. 139: 729-734. https://doi.org/10.1083/jcb.139.3.729
  21. 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. https://doi.org/10.1126/science.1101630
  22. 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. https://doi.org/10.1073/pnas.2332326100
  23. Sanchez L. 2001. TCA protein precipitation. Protocols on line.
  24. 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.
  25. Shkilnyj P, Koudelka MP, Koudelka GB. 2013. Bacteriophage 434 Hex protein prevents RecA-mediated repressor autocleavage. Viruses 5: 111-126. https://doi.org/10.3390/v5010111
  26. Sung WS, Lee IS, Lee DG. 2007. Damage to the cytoplasmic membrane and cell death caused by lycopene in Candida albicans. J. Microbiol. Biotechnol. 17: 1797-1804.
  27. Tzur A, Kafri R, LeBleu VS, Lahav G, Kirschner MW. 2009. Cell growth and size homeostasis in proliferating animal cells. Science 325: 167-171. https://doi.org/10.1126/science.1174294
  28. 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. https://doi.org/10.1042/BJ20042138
  29. 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. https://doi.org/10.1016/j.canlet.2007.03.002

Cited by

  1. Cinnamon Oil Inhibits Shiga Toxin Type 2 Phage Induction and Shiga Toxin Type 2 Production in Escherichia coli O157:H7 vol.82, pp.22, 2014, https://doi.org/10.1128/aem.01702-16
  2. Phytol has antibacterial property by inducing oxidative stress response in Pseudomonas aeruginosa vol.50, pp.12, 2014, https://doi.org/10.1080/10715762.2016.1241395
  3. Kocuria gwangalliensis 유래 phytoene desaturase 유전자의 cloning과 특성 연구 vol.45, pp.3, 2014, https://doi.org/10.4014/mbl.1704.04003
  4. Molecular Cloning and Overexpression of Phytoene Desaturase (CrtI) from Paracoccus haeundaensis vol.46, pp.2, 2014, https://doi.org/10.4014/mbl.1802.02013
  5. Alternative Therapeutic Interventions: Antimicrobial Peptides and Small Molecules to Treat Microbial Keratitis vol.9, pp.None, 2014, https://doi.org/10.3389/fchem.2021.694998
  6. Silver nanoparticles-induced H2O2 triggers apoptosis-like death and is associated with dinF in Escherichia coli vol.55, pp.2, 2014, https://doi.org/10.1080/10715762.2020.1866178
  7. Periplanetasin-2 Enhances the Antibacterial Properties of Vancomycin or Chloramphenicol in Escherichia coli vol.31, pp.2, 2014, https://doi.org/10.4014/jmb.2010.10058
  8. Acetylated cashew gum and fucan for incorporation of lycopene rich extract from red guava (Psidium guajava L.) in nanostructured systems: Antioxidant and antitumor capacity vol.191, pp.None, 2014, https://doi.org/10.1016/j.ijbiomac.2021.09.116
  9. Lycopene attenuates Staphylococcus aureus-induced inflammation via inhibiting α-hemolysin expression vol.23, pp.9, 2021, https://doi.org/10.1016/j.micinf.2021.104853
  10. Tomato Seed Mucilage as a New Source of Biodegradable Film-Forming Material: Effect of Glycerol and Cellulose Nanofibers on the Characteristics of Resultant Films vol.14, pp.12, 2021, https://doi.org/10.1007/s11947-021-02734-8
  11. Lycopene: From tomato to its nutraceutical use and its association with nanotechnology vol.118, pp.no.pa, 2021, https://doi.org/10.1016/j.tifs.2021.10.015