Carvacrol Induces Heat Shock Protein 60 and Inhibits Synthesis of Flagellin in Escherichia coli O157:H7
Open accessAbstract
The essential oils of oregano and thyme are active against a number of food-borne pathogens, such as Escherichia coli O157:H7. Carvacrol is one of the major antibacterial components of these oils, and p-cymene is thought to be its precursor in the plant. The effects of carvacrol and p-cymene on protein synthesis in E. coli O157:H7 ATCC 43895 cells were investigated. Bacteria were grown overnight in Mueller-Hinton broth with a sublethal concentration of carvacrol or p-cymene, and their protein compositions were analyzed by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and confirmed by Western blotting. The presence of 1 mM carvacrol during overnight incubation caused E. coli O157:H7 to produce significant amounts of heat shock protein 60 (HSP60) (GroEL) (P < 0.05) and inhibited the synthesis of flagellin highly significantly (P < 0.001), causing cells to be aflagellate and therefore nonmotile. The amounts of HSP70 (DnaK) were not significantly affected. p-Cymene at 1 mM or 10 mM did not induce HSP60 or HSP70 in significant amounts and did not have a significant effect on flagellar synthesis. Neither carvacrol (0.3, 0.5, 0.8, or 1 mM) nor p-cymene (0.3, 0.5, or 0.8 mM) treatment of cells in the mid-exponential growth phase induced significant amounts of HSP60 or HSP70 within 3 h, although numerical increases of HSP60 were observed. Motility decreased with increasing concentrations of both compounds, but existing flagella were not shed. This study is the first to demonstrate that essential oil components induce HSP60 in bacteria and that overnight incubation with carvacrol prevents the development of flagella in E. coli O157:H7.
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In many conditions, such as in the presence of sub-lethal concentrations of essential oils or other antimicrobial compounds, microorganisms react by increasing their expression of stress-response proteins to repair damaged proteins.
“In many conditions, such as in the presence of sub-lethal concentrations of EOs or other antimicrobial compounds, microorganisms react by increasing their expression of the stress-response proteins [25] to repair the damaged proteins [20].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [25]
Cites
Essential oils: Their antibacterial properties and potential applications in foods—A review
Burt, S. (2004) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.03.022 · Cited by 10,488 · see citing works
Self-citationEscherichia coli and Salmonella :cellular and molecular biology
Neidhardt, F. C. (1996) · ASM Press eBooks · Cited by 8,230 · see citing works
Antimicrobial agents from plants: Antibacterial activity of plant volatile oils
Dorman, H. J. D., & Deans, S. G. (2000) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2000.00969.x · Cited by 4,334 · see citing works
Escherichia Coli and Salmonella: Typhimurium Cellular and Molecular Biology
Neidhardt, F. C., & Ingraham, J. L. (1987) · Medical Entomology and Zoology · Cited by 4,089 · see citing works
The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5
Hayashi, F., Smith, K. D., Ozinsky, A., Hawn, T. R., Yi, E. C., Goodlett, D. R., Eng, J. K., Akira, S., Underhill, D. M., & Aderem, A. A. (2001) · Nature · doi:10.1038/35074106 · Cited by 3,605 · see citing works
Molecular Chaperones in the Cytosol: from Nascent Chain to Folded Protein
Hartl, F. U., & Hayer-Hartl, M. K. (2002) · Science · doi:10.1126/science.1068408 · Cited by 3,335 · see citing works
Characterization of the action of selected essential oil components on Gram-negative bacteria
Helander, I. M., Alakomi, H.-L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., Gorris, L. G. M., & von Wright, A. (1998) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf980154m · Cited by 1,664 · see citing works
Ultee, A., Bennik, M. H. J., & Moezelaar, R. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.4.1561-1568.2002 · Cited by 1,602 · see citing works
Mead, P. S., & Griffin, P. M. (1998) · The Lancet · doi:10.1016/s0140-6736(98)01267-7 · Cited by 1,031 · see citing works
Mechanisms of Action of Carvacrol on the Food-Borne Pathogen <i>Bacillus cereus</i>
Ultee, A., Kets, E. P. W., & Smid, E. J. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.10.4606-4610.1999 · Cited by 781 · see citing works
Gill, A. O., & Holley, R. A. (2006) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2005.10.009 · Cited by 541 · see citing works
Flagellin-Deficient Legionella Mutants Evade Caspase-1- and Naip5-Mediated Macrophage Immunity
Ren, T., Zamboni, D. S., Roy, C. R., Dietrich, W. F., & Vance, R. E. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020018 · Cited by 536 · see citing works
Pasqua, R. D., Hoskins, N., Betts, G., & Mauriello, G. (2006) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf052722l · Cited by 503 · see citing works
Wendakoon, C. N., & Sakaguchi, M. (1995) · Journal of Food Protection · doi:10.4315/0362-028x-58.3.280 · Cited by 377 · cited 1× · see citing works
“There are also indications for the inhibition of other enzymes (39).”
BackgroundThe flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells
Girón, J. A., Torres, A. G., Freer, E., et al. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02899.x · Cited by 363 · see citing works
Antimicrobial Activity of Carvacrol toward Bacillus cereus on Rice
Ultee, A., Slump, R. A., Steging, G., & Smid, E. J. (2000) · Journal of Food Protection · doi:10.4315/0362-028x-63.5.620 · Cited by 350 · see citing works
Jamroz, D., Wertelecki, T., Houszka, M., & Kamel, C. (2006) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/j.1439-0396.2005.00603.x · Cited by 330 · see citing works
Si, W., Gong, J., Tsao, R., Zhou, T., Yu, H., Poppe, C., Johnson, R. P., & Du, Z. (2005) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2005.02789.x · Cited by 321 · see citing works
Foodborne Disease Significance of Escherichia coli O157:H7 and Other Enterohemorrhagic E. coli
Buchanan, R. L., & Doyle, M. P. (1997) · Food technology · Cited by 272 · see citing works
Skandamis, P. N., & Nychas, G. E. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.4.1646-1653.2000 · Cited by 232 · see citing works
Gill, A. O., & Holley, R. A. (2006) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2006.04.046 · Cited by 226 · see citing works
Burt, S. A., Vlielander, R., Haagsman, H. P., & Veldhuizen, E. J. A. (2005) · Journal of Food Protection · doi:10.4315/0362-028x-68.5.919 · Cited by 226 · see citing works
Self-citationThe speed of the flagellar rotary motor of Escherichia coli varies linearly with protonmotive force
Gabel, C. V., & Berg, H. C. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1533395100 · Cited by 204 · see citing works
Boog, C. J. P., de Graeff-Meeder, E. R., Lucassen, M. A., et al. (1992) · The Journal of Experimental Medicine · doi:10.1084/jem.175.6.1805 · Cited by 202 · see citing works
Juliano, C. C. A., Mattana, A., & Usaï, M. (2000) · Journal of Essential Oil Research · doi:10.1080/10412905.2000.9699578 · Cited by 175 · see citing works
Shen, A., & Higgins, D. E. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020030 · Cited by 124 · see citing works
Inhibition of oregano essential oil and EDTA on Escherichia coli O157:H7
Skandamis, P. N., Koutsoumanis, K., Fasseas, K., & Nychas, G. E. (2001) · Italian Journal of Food Science · Cited by 123 · see citing works
Adverse conditions which cause lack of flagella in Escherichia coli
Li, C., Louise, C. J., Shi, W., et al. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.8.2229-2235.1993 · Cited by 102 · see citing works
MENDOZA‐YEPES, M. J., SANCHEZ‐HIDALGO, L. E., MAERTENS, G., & Marín‐Iniesta, F. (1997) · Journal of Food Safety · doi:10.1111/j.1745-4565.1997.tb00175.x · Cited by 77 · see citing works
Best, A., Ragione, R. M. L., Sayers, A. R., et al. (2005) · Infection and Immunity · doi:10.1128/iai.73.3.1836-1846.2005 · Cited by 49 · see citing works
Caillet, S., Shareck, F., & Lacroix, M. (2005) · Journal of Food Protection · doi:10.4315/0362-028x-68.12.2571 · Cited by 47 · see citing works
Kunin, C. M., Hua, T., & Bakaletz, L. O. (1995) · Infection and Immunity · doi:10.1128/iai.63.5.1796-1799.1995 · Cited by 43 · see citing works
Lipolytic Effects of Citrus Peel Oils and Their Components
Choi, H. (2006) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf052409j · Cited by 42 · see citing works
Mason, C. A., Dünner, J., Indra, P., et al. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.8.3433-3440.1999 · Cited by 33 · see citing works
Hagmüller, W., Jugl-Chizzola, M., Zitterl‐Eglseer, K., et al. (2006) · PubMed · Cited by 29 · see citing works
Best, A., Ragione, R. M. L., Clifford, D., et al. (2005) · Veterinary Microbiology · doi:10.1016/j.vetmic.2005.10.033 · Cited by 15 · see citing works
Ropadiar as alternative for anti microbial growth promoter in diets of weanling pigs
van Krimpen, M. M., & Binnendijk, G. P. (2001) · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Hyldgaard, M., Mygind, T., & Meyer, R. L. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00012 · Cited by 2,191 · see citing works
Effect of essential oils on pathogenic bacteria
Nazzaro, F., Fratianni, F., De Martino, L., Coppola, R., & De Feo, V. (2013) · Pharmaceuticals · doi:10.3390/ph6121451 · Cited by 2,186 · see citing works
Phytochemicals as antibiotic alternatives to promote growth and enhance host health
Lillehoj, H., Liu, Y., Calsamiglia, S., Fernandez-Miyakawa, M. E., Chi, F., Cravens, R. L., Oh, S., & Gay, C. G. (2018) · Veterinary Research · doi:10.1186/s13567-018-0562-6 · Cited by 515 · see citing works
Di Pasqua, R., Mamone, G., Ferranti, P., Ercolini, D., & Mauriello, G. (2010) · PROTEOMICS · doi:10.1002/pmic.200900568 · Cited by 171 · see citing works
La Storia, A., Ercolini, D., Marinello, F., Di Pasqua, R., Villani, F., & Mauriello, G. (2011) · Research in Microbiology · doi:10.1016/j.resmic.2010.11.006 · Cited by 156 · see citing works
In vitro activity of carvacrol against staphylococcal preformed biofilm by liquid and vapour contact
Nostro, A., Marino, A., Blanco, A. R., Cellini, L., Di Giulio, M., Pizzimenti, F., Roccaro, A. S., & Bisignano, G. (2009) · Journal of Medical Microbiology · doi:10.1099/jmm.0.009274-0 · Cited by 99 · see citing works
- Authors
- Burt, S. A., van der Zee, R., Koets, A. P., de Graaff, A. M., van Knapen, F., Gaastra, W., Haagsman, H. P., & Veldhuizen, E. J. A.
- Affiliations
- Institute for Risk Assessment Sciences, Division of Veterinary Public Health
- Department of Infectious Diseases and Immunology
- Centre for Cell Imaging, Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
- Corresponding author
- Burt, Sara A.
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2007-07-15
- Volume
- 73
- Issue
- 14
- Pages
- 4484-4490
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC1932834
- OpenAlex
- W2167358281
- Cited by
- 280
- References
- 37
- Citations by year
- 2026: 6 · 2025: 17 · 2024: 17 · 2023: 11 · 2022: 24 · 2021: 11 · 2020: 25 · 2019: 17 · 2018: 19 · 2017: 20 · 2016: 24 · 2015: 13 · 2014: 11 · 2013: 19 · 2012: 17
- FWCI
- 11.94
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Essential Oils and Antimicrobial Activity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Keywords
- carvacrol, p-cymene, Escherichia coli O157:H7, heat shock protein 60, GroEL, bacterial motility, HSP70, DnaK, essential oils, oregano, thyme, foodborne pathogens, antibacterial activity, protein synthesis
- MeSH terms
- Cymenes, Anti-Bacterial Agents, Electrophoresis, Polyacrylamide Gel, Flagella, Flagellin, Locomotion, Microscopy, Interference, Blotting, Western, Chaperonin 60, HSP70 Heat-Shock Proteins, Escherichia coli O157, Proteome, Escherichia coli Proteins, Monoterpenes
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