1,8-Cineol (Eucalyptol) Disrupts Membrane Integrity and Induces Oxidative Stress in Methicillin-Resistant Staphylococcus aureus
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemical and Bacterial Strains
2.2. Antibacterial Activity of 1,8-Cineol
2.3. Effects on Membrane Permeability
2.4. Surface Charge Alteration
2.5. Reactive Oxygen Species Generation
2.6. Lipid Peroxidation
2.7. Antioxidant Enzyme Activity
2.7.1. Measurement of Catalase (CAT) Enzyme Activity
2.7.2. Measurement of Superoxide Dismutase (SOD) Enzyme Activity
2.8. Statistical Analysis
3. Results
3.1. Antibacterial Activity
3.2. Effects on Membrane Permeability
3.3. Surface Charge Alteration
3.4. Generation of Reactive Oxygen Species
3.5. Lipid Peroxidation
3.6. Antioxidant Enzyme Activity
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Diekema, D.J.; Pfaller, M.A.; Schmitz, F.J.; Smayevsky, J.; Bell, J.; Jones, R.N.; Beach, M. SENTRY Partcipants Group. Survey of infections due to Staphylococcus species: Frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997–1999. Clin. Infect. Dis. 2001, 32 (Suppl. S2), S114–S132. [Google Scholar]
- Goss, C.H.; Muhlebach, M.S. Review: Staphylococcus aureus and MRSA in cystic fibrosis. J. Cyst. Fibros. 2011, 10, 298–306. [Google Scholar] [CrossRef] [Green Version]
- Grant, S.S.; Hung, D.T. Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence 2013, 4, 273–283. [Google Scholar] [CrossRef] [Green Version]
- Lakhundi, S.; Zhang, K. Methicillin-Resistant Staphylococcus aureus: Molecular Characterization, Evolution, and Epidemiology. Clin. Microbiol. Rev. 2018, 31, e00020-18. [Google Scholar] [CrossRef] [Green Version]
- Turner, N.A.; Sharma-Kuinkel, B.K.; Maskarinec, S.A.; Eichenberger, E.M.; Shah, P.P.; Carugati, M.; Holland, T.L.; Fowler, V.G., Jr. Methicillin-resistant Staphylococcus aureus: An overview of basic and clinical research. Nat. Rev. Microbiol. 2019, 17, 203–218. [Google Scholar] [CrossRef]
- Deyno, S.; Toma, A.; Worku, M.; Bekele, M. Antimicrobial resistance profile of Staphylococcus aureus isolates isolated from ear discharges of patients at University of Hawassa comprehensive specialized hospital. BMC Pharmacol. Toxicol. 2017, 18, 35. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Foster, T.J. Antibiotic resistance in Staphylococcus aureus. Current status and future prospects. FEMS Microbiol. Rev. 2017, 41, 430–449. [Google Scholar] [CrossRef] [PubMed]
- Cuevas, O.; Cercenado, E.; Vindel, A.; Guinea, J.; Sanchez-Conde, M.; Sanchez-Somolinos, M.; Bouza, E. Evolution of the antimicrobial resistance of Staphylococcus spp. in Spain: Five nationwide prevalence studies, 1986 to 2002. Antimicrob. Agents Chemother. 2004, 48, 4240–4245. [Google Scholar] [CrossRef] [Green Version]
- Moo, C.L.; Osman, M.A.; Yang, S.K.; Yap, W.S.; Ismail, S.; Lim, S.H.; Chong, C.M.; Lai, K.S. Antimicrobial activity and mode of action of 1,8-cineol against carbapenemase-producing Klebsiella pneumoniae. Sci. Rep. 2021, 11, 20824. [Google Scholar] [CrossRef]
- Yang, S.K.; Yusoff, K.; Thomas, W.; Akseer, R.; Alhosani, M.S.; Abushelaibi, A.; Lim, S.H.; Lai, K.S. Lavender essential oil induces oxidative stress which modifies the bacterial membrane permeability of carbapenemase producing Klebsiella pneumoniae. Sci. Rep. 2020, 10, 819. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sousa, V.I.; Parente, J.F.; Marques, J.F.; Forte, M.A.; Tavares, C.J. Microencapsulation of Essential Oils: A Review. Polymers 2022, 14, 1730. [Google Scholar] [CrossRef] [PubMed]
- Bakkali, F.; Averbeck, S.; Averbeck, D.; Idaomar, M. Biological effects of essential oils—A review. Food Chem. Toxicol. 2008, 46, 446–475. [Google Scholar] [CrossRef] [PubMed]
- Zuzarte, M.; Salgueiro, L. Essential Oils Chemistry. In Bioactive Essential Oils and Cancer; De Sousa, D.P., Ed.; Springer: Cham, Switzland, 2015; pp. 19–61. [Google Scholar] [CrossRef]
- Valdivieso-Ugarte, M.; Gomez-Llorente, C.; Plaza-Díaz, J.; Gil, Á. Antimicrobial, Antioxidant, and Immunomodulatory Properties of Essential Oils: A Systematic Review. Nutrients 2019, 11, 2786. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Álvarez-Martínez, F.J.; Barrajón-Catalán, E.; Herranz-López, M.; Micol, V. Antibacterial plant compounds, extracts and essential oils: An updated review on their effects and putative mechanisms of action. Phytomedicine 2021, 90, 153626. [Google Scholar] [CrossRef]
- Guimarães, A.C.; Meireles, L.M.; Lemos, M.F.; Guimarães, M.C.C.; Endringer, D.C.; Fronza, M.; Scherer, R. Antibacterial Activity of Terpenes and Terpenoids Present in Essential Oils. Molecules 2019, 24, 2471. [Google Scholar] [CrossRef] [Green Version]
- Pinto, L.; Tapia-Rodríguez, M.R.; Baruzzi, F.; Ayala-Zavala, J.F. Plant Antimicrobials for Food Quality and Safety: Recent Views and Future Challenges. Foods 2023, 12, 2315. [Google Scholar] [CrossRef]
- Sebei, K.; Sakouhi, F.; Herchi, W.; Khouja, M.L.; Boukhchina, S. Chemical composition and antibacterial activities of seven Eucalyptus species essential oils leaves. Biol. Res. 2015, 48, 7. [Google Scholar] [CrossRef] [Green Version]
- Brown, S.K.; Garver, W.S.; Orlando, R.A. 1,8-cineol: An underappreciated anti-inflammatory therapeutic. J. Biomol. Res. Ther. 2017, 6, 6–11. [Google Scholar] [CrossRef]
- Zacchino, S.A.; Butassi, E.; Cordisco, E.; Svetaz, L.A. Hybrid combinations containing natural products and antimicrobial drugs that interfere with bacterial and fungal biofilms. Phytomedicine 2017, 37, 14–26. [Google Scholar] [CrossRef]
- Zengin, H.; Baysal, A.H. Antibacterial and antioxidant activity of essential oil terpenes against pathogenic and spoilage-forming bacteria and cell structure-activity relationships evaluated by SEM microscopy. Molecules 2014, 19, 17773–17798. [Google Scholar] [CrossRef] [Green Version]
- Merghni, A.; Noumi, E.; Hadded, O.; Dridi, N.; Panwar, H.; Ceylan, O.; Mastouri, M.; Snoussi, M. Assessment of the antibiofilm and antiquorum sensing activities of Eucalyptus globulus essential oil and its main component 1,8-cineol against methicillin-resistant Staphylococcus aureus strains. Microb. Pathog. 2018, 118, 74–80. [Google Scholar] [CrossRef] [PubMed]
- Prakash, A.; Baskaran, R.; Nithyanand, P.; Vadivel, V. Effect of nanoemulsification on the antibacterial and anti-biofilm activities of selected spice essential oils and their major constituents against Salmonella enterica typhimurium. J. Clust. Sci. 2020, 31, 1123–1135. [Google Scholar] [CrossRef]
- Schwarz, S.; Silley, P.; Simjee, S.; Woodford, N.; van Duijkeren, E.; Johnson, A.P.; Gaastra, W. Editorial: Assessing the antimicrobial susceptibility of bacteria obtained from animals. J. Antimicrob. Chemother. 2010, 65, 601–604. [Google Scholar] [CrossRef] [PubMed]
- Lemos, A.S.O.; Campos, L.M.; Melo, L.; Guedes, M.C.M.R.; Oliveira, L.G.; Silva, T.P.; Melo, R.C.N.; Rocha, V.N.; Aguiar, J.A.K.; Apolônio, A.C.M.; et al. Antibacterial and Antibiofilm Activities of Psychorubrin, a Pyranonaphthoquinone Isolated from Mitracarpus frigidus (Rubiaceae). Front. Microbiol. 2018, 9, 724. [Google Scholar] [CrossRef] [Green Version]
- Ferreyra Maillard, A.P.V.; Espeche, J.C.; Maturana, P.; Cutro, A.C.; Hollmann, A. Zeta potential beyond materials science: Applications to bacterial systems and to the development of novel antimicrobials. Biochim. Biophys. Acta Biomembr. 2021, 1863, 183597. [Google Scholar] [CrossRef]
- Espeche, J.C.; Martínez, M.; Maturana, P.; Cutró, A.; Semorile, L.; Maffia, P.C.; Hollmann, A. Unravelling the mechanism of action of “de novo” designed peptide P1 with model membranes and gram-positive and gram-negative bacteria. Arch. Biochem. Biophys. 2020, 693, 108549. [Google Scholar] [CrossRef]
- Han, L.; Patil, S.; Boehm, D.; Milosavljevic, V.; Cullen, P.J.; Bourke, P. Mechanisms of inactivation by high-voltage atmospheric cold plasma differ for Escherichia coli and Staphylococcus aureus. Appl. Environ. Microbiol. 2016, 82, 450–458. [Google Scholar] [CrossRef] [Green Version]
- Hamdi, H.; Ben Salem, I.; Ben Othmène, Y.; Annabi, E.; Abid-Essefi, S. The involvement of ROS generation on Epoxiconazole-induced toxicity in HCT116 cells. Pestic. Biochem. Physiol. 2018, 148, 62–67. [Google Scholar] [CrossRef]
- Ong, K.S.; Cheow, Y.L.; Lee, S.M. The role of reactive oxygen species in the antimicrobial activity of pyochelin. J. Adv. Res. 2017, 8, 393–398. [Google Scholar] [CrossRef]
- Martins, D.; McKay, G.; Sampathkumar, G.; Khakimova, M.; English, A.M.; Nguyen, D. Superoxide dismutase activity confers (p)ppGpp-mediated antibiotic tolerance to stationary-phase Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 2018, 115, 9797–9802. [Google Scholar] [CrossRef] [Green Version]
- Acuña, L.G.; Calderón, I.L.; Elías, A.O.; Castro, M.E.; Vásquez, C.C. Expression of the yggE gene protects Escherichia coli from potassium tellurite-generated oxidative stress. Arch. Microbiol. 2009, 191, 473–476. [Google Scholar] [CrossRef] [PubMed]
- Marklund, S.; Marklund, G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 1974, 47, 469–474. [Google Scholar] [CrossRef] [PubMed]
- Terreni, M.; Taccani, M.; Pregnolato, M. New Antibiotics for Multidrug-Resistant Bacterial Strains: Latest Research Developments and Future Perspectives. Molecules 2021, 26, 2671. [Google Scholar] [CrossRef]
- Kwiatkowski, P.; Łopusiewicz, Ł.; Pruss, A.; Kostek, M.; Sienkiewicz, M.; Bonikowski, R.; Wojciechowska-Koszko, I.; Dołęgowska, B. Antibacterial Activity of Selected Essential Oil Compounds Alone and in Combination with β-Lactam Antibiotics Against MRSA Strains. Int. J. Mol. Sci. 2020, 21, 7106. [Google Scholar] [CrossRef]
- Badawy, M.E.I.; Marei, G.I.K.; Rabea, E.I.; Taktak, N.E.M. Antimicrobial and antioxidant activities of hydrocarbon and oxygenated monoterpenes against some foodborne pathogens through in vitro and in silico studies. Pestic. Biochem. Physiol. 2019, 158, 185–200. [Google Scholar] [CrossRef]
- Farhanghi, A.; Aliakbarlu, J.; Tajik, H.; Mortazavi, N.; Manafi, L.; Jalilzadeh-Amin, G. Antibacterial interactions of pulegone and 1,8-cineol with monolaurin ornisin against Staphylococcus aureus. Food Sci. Nutr. 2022, 10, 2659–2666. [Google Scholar] [CrossRef]
- Kwiatkowski, P.; Pruss, A.; Wojciuk, B.; Dołęgowska, B.; Wajs-Bonikowska, A.; Sienkiewicz, M.; Mężyńska, M.; Łopusiewicz, Ł. The Influence of Essential Oil Compounds on Antibacterial Activity of Mupirocin-Susceptible and Induced Low-Level Mupirocin-Resistant MRSA Strains. Molecules 2019, 24, 3105. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oliveira, G.D.; Rocha, W.R.V.D.; Rodrigues, J.F.B.; Alves, H.D.S. Synergistic and Antibiofilm Effects of the Essential Oil from Croton conduplicatus (Euphorbiaceae) against Methicillin-Resistant Staphylococcus aureus. Pharmaceuticals 2022, 16, 55. [Google Scholar] [CrossRef]
- Mączka, W.; Duda-Madej, A.; Górny, A.; Grabarczyk, M.; Wińska, K. Can Eucalyptol Replace Antibiotics? Molecules 2021, 26, 4933. [Google Scholar] [CrossRef]
- Schürmann, M.; Oppel, F.; Gottschalk, M.; Büker, B.; Jantos, C.A.; Knabbe, C.; Hütten, A.; Kaltschmidt, B.; Kaltschmidt, C.; Sudhoff, H. The Therapeutic Effect of 1,8-Cineol on Pathogenic Bacteria Species Present in Chronic Rhinosinusitis. Front. Microbiol. 2019, 10, 2325. [Google Scholar] [CrossRef] [Green Version]
- Zhou, H.; Fang, J.; Tian, Y.; Lu, X.Y. Mechanisms of nisin resistance in Gram-positive bacteria. Ann. Microbiol. 2014, 64, 413–420. [Google Scholar] [CrossRef]
- Ren, X.; An, P.; Zhai, X.; Wang, S.; Kong, Q. The antibacterial mechanism of pterostilbene derived from xinjiang wine grape: A novel apoptosis inducer in Staphyloccocus aureus and Escherichia coli. LWT 2019, 101, 100–106. [Google Scholar] [CrossRef]
- Gonçalves, F.D.; de Carvalho, C.C. Phenotypic Modifications in Staphylococcus aureus Cells Exposed to High Concentrations of Vancomycin and Teicoplanin. Front. Microbiol. 2016, 7, 13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trombetta, D.; Castelli, F.; Sarpietro, M.G.; Venuti, V.; Cristani, M.; Daniele, C.; Saija, A.; Mazzanti, G.; Bisignano, G. Mechanisms of antibacterial action of three monoterpenes. Antimicrob. Agents Chemother. 2005, 49, 2474–2478. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martinez, R.E.; Pokrovsky, O.S.; Schott, J.; Oelkers, E.H. Surface charge and zeta-potential of metabolically active and dead cyanobacteria. J. Colloid. Interface Sci. 2008, 323, 317–325. [Google Scholar] [CrossRef] [PubMed]
- Bravo-Ferrada, B.M.; Gonçalves, S.; Semorile, L.; Santos, N.C.; Tymczyszyn, E.E.; Hollmann, A. Study of surface damage on cell envelope assessed by AFM and flow cytometry of Lactobacillus plantarum exposed to ethanol and dehydration. J. Appl. Microbiol. 2015, 118, 1409–1417. [Google Scholar] [CrossRef]
- Bravo-Ferrada, B.M.; Gonçalves, S.; Semorile, L.; Santos, N.C.; Brizuela, N.S.; Elizabeth Tymczyszyn, E.; Hollmann, A. Cell surface damage and morphological changes in Oenococcus oeni after freeze-drying and incubation in synthetic wine. Cryobiology 2018, 82, 15–21. [Google Scholar] [CrossRef]
- Bowbe, K.H.; Salah, K.B.H.; Moumni, S.; Ashkan, M.F.; Merghni, A. Anti-Staphylococcal Activities of Rosmarinus officinalis and Myrtus communis Essential Oils through ROS-Mediated Oxidative Stress. Antibiotics 2023, 12, 266. [Google Scholar] [CrossRef]
- Ribeiro-Santos, R.; Carvalho-Costa, D.; Cavaleiro, C.; Costa, H.S.; Albuquerque, T.G.; Castilho, M.C.; Ramos, F.; Melo, N.R.; Sanches-Silva, A. A novel insight on an ancient aromatic plant: The rosemary (Rosmarinus officinalis L.). Trends Food Sci. Technol. 2015, 45, 355–368. [Google Scholar] [CrossRef]
- Yang, S.K.; Yusoff, K.; Ajat, M.; Yap, W.S.; Lim, S.E.; Lai, K.S. Antimicrobial activity and mode of action of terpene linalyl anthranilate against carbapenemase-producing Klebsiella pneumoniae. J. Pharm. Anal. 2021, 11, 210–219. [Google Scholar] [CrossRef]
- Golenia, A.; Leśkiewicz, M.; Regulska, M.; Budziszewska, B.; Szczęsny, E.; Jagiełła, J.; Wnuk, M.; Ostrowska, M.; Lasoń, W.; Basta-Kaim, A.; et al. Catalase activity in blood fractions of patients with sporadic ALS. Pharmacol. Rep. 2014, 66, 704–707. [Google Scholar] [CrossRef] [PubMed]
- Cai, J.Y.; Li, J.; Hou, Y.N.; Ma, K.; Yao, G.D.; Liu, W.W.; Hayashi, T.; Itoh, K.; Tashiro, S.; Onodera, S.; et al. Concentration-dependent dual effects of silibinin on kanamycin-induced cells death in Staphylococcus aureus. Biomed. Pharmacother. 2018, 102, 782–791. [Google Scholar] [CrossRef] [PubMed]
- Sinsinwar, S.; Vadivel, V. Catechin isolated from cashew nut shell exhibits antibacterial activity against clinical isolates of MRSA through ROS-mediated oxidative stress. Appl. Microbiol. Biotechnol. 2020, 104, 8279–8297. [Google Scholar] [CrossRef] [PubMed]
- Hussain, R.M.; Razak, Z.N.R.A.; Saad, W.M.M.; Mustakim, M. Mechanism of antagonistic effects of Andrographis paniculata methanolic extract against Staphylococcus aureus. Asian Pac. J. Trop. Med. 2017, 10, 685–695. [Google Scholar] [CrossRef]
- Nakonieczna, J.; Michta, E.; Rybicka, M.; Grinholc, M.; Gwizdek-Wiśniewska, A.; Bielawski, K.P. Superoxide dismutase is upregulated in Staphylococcus aureus following protoporphyrin-mediated photodynamic inactivation and does not directly influence the response to photodynamic treatment. BMC Microbiol. 2010, 10, 323. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beavers, W.N.; Skaar, E.P. Neutrophil-generated oxidative stress and protein damage in Staphylococcus aureus. Pathog. Dis. 2016, 74, ftw060. [Google Scholar] [CrossRef] [Green Version]
- Gaupp, R.; Ledala, N.; Somerville, G.A. Staphylococcal response to oxidative stress. Front. Cell. Infect. Microbiol. 2012, 2, 33. [Google Scholar] [CrossRef] [Green Version]
MRSA Strain | Analyzed Parameter | Concentration (mg/mL) |
---|---|---|
43300 * | MIC | 7.23 |
MBC | 57.87 | |
MBC/MIC (ratio) | 8 | |
Sa15 ** | MIC | 7.23 |
MBC | 115.75 | |
MBC/MIC (ratio) | 16 |
Strains | Period | Control | MIC/2 | MIC | MIC × 2 | MIC × 4 |
---|---|---|---|---|---|---|
43300 * | 2 h | −18.5 ±0.3 | −27.4 ± 0.7 *** | −27.5 ± 0.7 *** | −27.5 ± 0.5 *** | −27.1 ± 0.4 *** |
24 h | −27.1 ± 1.0 | −27.8 ± 0.3 | −28.1 ± 1.0 | −29.2 ± 0.6 *** | −30.2 ± 0.7 *** | |
Sa15 ** | 2 h | −13.5 ± 3.4 | −28 ± 1.0 *** | −35.9 ± 1.4 *** | −37.0 ± 2.5 *** | −39.5 ± 1.1 *** |
24 h | −21.9 ± 0.8 | −31.8 ± 1.3 *** | −36.7 ± 0.6 *** | −37.4 ± 2.7 *** | −43.5 ± 0.5 *** |
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Merghni, A.; Belmamoun, A.R.; Urcan, A.C.; Bobiş, O.; Lassoued, M.A. 1,8-Cineol (Eucalyptol) Disrupts Membrane Integrity and Induces Oxidative Stress in Methicillin-Resistant Staphylococcus aureus. Antioxidants 2023, 12, 1388. https://doi.org/10.3390/antiox12071388
Merghni A, Belmamoun AR, Urcan AC, Bobiş O, Lassoued MA. 1,8-Cineol (Eucalyptol) Disrupts Membrane Integrity and Induces Oxidative Stress in Methicillin-Resistant Staphylococcus aureus. Antioxidants. 2023; 12(7):1388. https://doi.org/10.3390/antiox12071388
Chicago/Turabian StyleMerghni, Abderrahmen, Ahmed Reda Belmamoun, Adriana Cristina Urcan, Otilia Bobiş, and Mohamed Ali Lassoued. 2023. "1,8-Cineol (Eucalyptol) Disrupts Membrane Integrity and Induces Oxidative Stress in Methicillin-Resistant Staphylococcus aureus" Antioxidants 12, no. 7: 1388. https://doi.org/10.3390/antiox12071388
APA StyleMerghni, A., Belmamoun, A. R., Urcan, A. C., Bobiş, O., & Lassoued, M. A. (2023). 1,8-Cineol (Eucalyptol) Disrupts Membrane Integrity and Induces Oxidative Stress in Methicillin-Resistant Staphylococcus aureus. Antioxidants, 12(7), 1388. https://doi.org/10.3390/antiox12071388