Effects of luteolin and quercetin in combination with some conventional antibiotics against methicillin-resistant Staphylococcus aureus

International Journal of Molecular Sciences

Volumn 17, Issue 11, 2016, Pages

  Amin, Muhammad Usman ^a,e   Khurram, Muhammad ^b   Khan, Taj Ali ^a   Faidah, Hani S ^c   Shah, Zia Ullah ^d   Ur Rahman, Shafiq ^b   Haseeb, Abdul ^c   Ilyas, Muhammad ^d   Ullah, Naseem ^d   Khayam, Sahibzada Muhammad Umar ^d   Iriti, Marcello ^f  

^a KOHAT UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Pakistan)

^b Shaheed Benazir Bhutto University   (Pakistan)

^c UMM AL QURA UNIVERSITY   (Saudi Arabia)

^d Mardan Campus   (Pakistan)

^e KHYBER MEDICAL UNIVERSITY   (Pakistan)

^f UNIVERSITY OF MILAN   (Italy)

Author keywords

Antibiotic resistance; Combination therapy; Flavonoids; MRSA; Phytochemicals; Synergism

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; DRUG COMBINATION; LUTEOLIN; MECA PROTEIN, STAPHYLOCOCCUS AUREUS; PENICILLIN BINDING PROTEIN; QUERCETIN;

DRUG ANTAGONISM; DRUG COMBINATION; DRUG EFFECTS; DRUG POTENTIATION; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; OPEN READING FRAME; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG ANTAGONISM; DRUG COMBINATIONS; DRUG SYNERGISM; GENE EXPRESSION; HUMANS; LUTEOLIN; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; OPEN READING FRAMES; PENICILLIN-BINDING PROTEINS; QUERCETIN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84996536302     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17111947     Document Type: Article

References (41)

1. Morell, E.A.; Balkin, D.M. Methicillin-resistant Staphylococcus aureus: A pervasive pathogen highlights the need for new antimicrobial development. Yale J. Biol. Med. 2010, 83, 223–233.
2. Taj, Y.; Abdullah, F.E.; Kazmi, S.U. Current pattern of antibiotic resistance in Staphylococcus aureus clinical isolates and the emergence of vancomycin resistance. J. Coll. Physicians Surg. Pak. 2010, 20, 728–732.
3. Hafiz, S.; Hafiz, A.N.; Ali, L.; Chughtai, A.S.; Memon, B.; Ahmed, A.; Hussain, S.; Sarwar, G.; Mughal, T.; Awan, A.; et al. Methicillin resistant Staphylococcus aureus: A multicentre study. J. Pak. Med. Assoc. 2002, 52, 312–314.
4. Lin, R.D.; Chin, Y.P.; Lee, M.H. Antimicrobial activity of antibiotics in combination with natural flavonoids against clinical extended-spectrum β-lactamase (ESBL)-producing Klebsiella pneumoniae. Phytother. Res. 2005, 19, 612–617.
5. Moon, S.H.; Lee, K.A.; Park, K.K.; Kim, K.T.; Park, Y.S.; Nah, S.Y.; Mendonca, A.F.; Paik, H.D. Antimicrobial effects of natural flavonoids and a novel flavonoid, 7-O-Butyl Naringenin, on growth of meat-borne Staphylococcus aureus strains. Korean J. Food Sci. Anim. Resour. 2011, 31, 413–419.
6. Darwish, R.M.; Ra’ed, J.; Zarga, M.H.A.; Nazer, I.K. Antibacterial effect of Jordanian propolis and isolated flavonoids against human pathogenic bacteria. Afr. J. Biotechnol. 2011, 9, 5966–5974.
7. Su, Y.; Ma, L.; Wen, Y.; Wang, H.; Zhang, S. Studies of the in vitro antibacterial activities of several polyphenols against clinical isolates of methicillin-resistant Staphylococcus aureus. Molecules 2014, 19, 12630–12639.
8. Idrees, F.; Jabeen, K.; Khan, M.S.; Zafar, A. Antimicrobial resistance profile of methicillin resistant staphylococcal aureus from skin and soft tissue isolates. J. Pak. Med. Assoc. 2009, 59, 266.
9. Liu, H.; Mou, Y.; Zhao, J.; Wang, J.; Zhou, L.; Wang, M.; Wang, D.; Han, J.; Yu, Z.; Yang, F. Flavonoids from Halostachys caspica and their antimicrobial and antioxidant activities. Molecules 2010, 15, 7933–7945.
10. Xu, H.X.; Lee, S.F. Activity of plant flavonoids against antibiotic-resistant bacteria. Phytother. Res. 2001, 15, 39–43.
11. Qiu, J.; Li, H.; Meng, H.; Hu, C.; Li, J.; Luo, M.; Dong, J.; Wang, X.; Wang, J.; Deng, Y.; et al. Impact of luteolin on the production of α-toxin by Staphylococcus aureus. Lett. Appl. Microbiol. 2011, 53, 238–243.
12. Nadia, Z.; Rachid, M. Antioxidant and antibacterial activities of Thymus vulgaris L. Med. Aromat. Plant Res. J. 2013, 1, 5–11.
13. Amin, M.U.; Khurram, M.; Khattak, B.; Khan, J. Antibiotic additive and synergistic action of rutin, morin and quercetin against methicillin resistant Staphylococcus aureus. BMC Complement. Altern. Med. 2015, 15.
14. Stapleton, P.D.; Shah, S.; Anderson, J.C.; Hara, Y.; Hamilton-Miller, J.M.; Taylor, P.W. Modulation of β-lactam resistance in Staphylococcus aureus by catechins and gallates. Int. J. Antimicrob. Agents 2004, 23, 462–467.
15. Shimamura, T.; Zhao, W.H.; Hu, Z.Q. Mechanism of action and potential for use of tea catechin as an anti-infective agent. Antiinfect. Agents Med. Chem. 2007, 6, 57–62.
16. Stapleton, P.D.; Shah, S.; Hara, Y.; Taylor, P.W. Potentiation of catechin gallate-mediated sensitization of Staphylococcus aureus to oxacillin by nongalloylated catechins. Antimicrob. Agents Chemother. 2006, 50, 752–755.
17. Eumkeb, G.; Siriwong, S.; Thumanu, K. Synergistic activity of luteolin and amoxicillin combination against amoxicillin-resistant Escherichia coli and mode of action. J. Photochem. Photobiol. B 2012, 117, 247–253.
18. Caturla, N.; Vera-Samper, E.; Villalaín, J.; Mateo, C.R.; Micol, V. The relationship between the antioxidant and the antibacterial properties of galloylated catechins and the structure of phospholipid model membranes. Free Radic. Biol. Med. 2003, 34, 648–662.
19. Wang, S.Y.; Sun, Z.L.; Liu, T.; Gibbons, S.; Zhang, W.J.; Qing, M. Flavonoids from Sophora moorcroftiana and their synergistic antibacterial effects on MRSA. Phytother. Res. 2014, 28, 1071–1076.
20. Novy, P.; Urban, J.; Leuner, O.; Vadlejch, J.; Kokoska, L. In vitro synergistic effects of baicalin with oxytetracycline and tetracycline against Staphylococcus aureus. J. Antimicrob. Chemother. 2011, 108.
21. Campos, F.M.; Couto, J.A.; Figueiredo, A.R.; Tóth, I.V.; Rangel, A.O.; Hogg, T.A. Cell membrane damage induced by phenolic acids on wine lactic acid bacteria. Int. J. Food Microbiol. 2009, 135, 144–151.
22. Cushnie, T.T.; Lamb, A.J. Antimicrobial activity of flavonoids. Int. J. Antimicrob. Agents 2005, 26, 343–356.
23. Meghashri, S.; Gopal, S. Dihydroxy flavone-induced cytoplasmic membrane damage in Staphylococcus aureus. Int. J. Phytomed. 2012, 4, 150.
24. Kobayashi, N.; Wu, H.; Kojima, K.; Taniguchi, K.; Urasawa, S.; Uehara, N.; Omizu, Y.; Kishi, Y.; Yagihashi, A.; Kurokawa, I. Detection of mecA, femA, and femB genes in clinical strains of staphylococci using polymerase chain reaction. Epidemiol. Infect. 1994, 113, 259–266.
25. Alam, M.M.; Uddin, M.S.; Kobayashi, N.; Ahmed, M.U. Detection of methicillin-resistant Staphylococcus aureus (MRSA) from animal and human origin in Bangladesh by polymerase chain reaction. Bangladesh J. Vet. Med. 2013, 9, 161–166.
26. Goffin, C.; Ghuysen, J.M. Multimodular penicillin-binding proteins: An enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 1998, 62, 1079–1093.
27. Murakami, K.; Fujimura, T.; Doi, M. Nucleotide sequence of the structural gene for the penicillin-binding protein 2 of Staphylococcus aureus and the presence of a homologous gene in other staphylococci. FEMS Microbiol. Lett. 1994, 117, 131–136.
28. Pinho, M.G.; de Lencastre, H.; Tomasz, A. An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci. Proc. Natl. Acad. Sci. USA 2001, 98, 10886–10891.
29. Sato, Y.; Shibata, H.; Arai, T.; Yamamoto, A.; Okimura, Y.; Arakaki, N.; Higuti, T. Variation in synergistic activity by flavone and its related compounds on the increased susceptibility of various strains of methicillin-resistant Staphylococcus aureus to β-lactam antibiotics. Int. J. Antimicrob. Agents 2004, 24, 226–233.
30. Giesbrecht, P.; Kersten, T.; Maidhof, H.; Wecke, J. Staphylococcal cell wall: Morphogenesis and fatal variations in the presence of penicillin. Microbiol. Mol. Biol. Rev. 1998, 62, 1371–1414.
31. Kosmidis, C.; Schindler, B.D.; Jacinto, P.L.; Patel, D.; Bains, K.; Seo, S.M.; Kaatz, G.W. Expression of multidrug resistance efflux pump genes in clinical and environmental isolates of Staphylococcus aureus. Int. J. Antimicrob. Agents 2012, 40, 204–209.
32. Truong-Bolduc, Q.C.; Hooper, D.C. The transcriptional regulators NorG and MgrA modulate resistance to both quinolones and β-lactams in Staphylococcus aureus. J. Bacterial. 2007, 189, 2996–3005.
33. DeMarco, C.E.; Cushing, L.A.; Frempong-Manso, E.; Seo, S.M.; Jaravaza, T.A.; Kaatz, G.W. Efflux-related resistance to norfloxacin, dyes, and biocides in bloodstream isolates of Staphylococcus aureus. Antimicrob. Agents Chemother. 2007, 51, 3235–3239.
34. Gibbons, S.; Moser, E.; Kaatz, G.W. Catechin gallates inhibit multidrug resistance (MDR) in Staphylococcus aureus. Planta Med. 2004, 70, 1240–1242.
35. Qin, R.; Xiao, K.; Li, B.; Jiang, W.; Peng, W.; Zheng, J.; Zhou, H. The combination of catechin and epicatechin gallate from Fructus crataegi potentiates β-lactam antibiotics against methicillin-resistant Staphylococcus aureus (MRSA) in vitro and in vivo. Int. J. Mol. Sci. 2013, 14, 1802–1821.
36. Kateete, D.P.; Kimani, C.N.; Katabazi, F.A.; Okeng, A.; Okee, M.S.; Nanteza, A.; Joloba, M.L.; Najjuka, F.C. Identification of Staphylococcus aureus: DNase and Mannitol salt agar improve the efficiency of the tube coagulase test. Ann. Clin. Microbiol. Antimicrob. 2010, 9.
37. Ergene, A.; Guler, P.; Tan, S.; Mirici, S.; Hamzaoglu, E. Antimicrobial and antifungal activity of Heracleum sphondylium subsp. artivinense. Afr. J. Biotechnol. 2006, 5, 1087–1089.
38. Sakharkar, M.K.; Jayaraman, P.; Soe, W.M.; Chow, V.T.; Sing, L.C.; Sakharkar, K.R. In vitro combinations of antibiotics and phytochemicals against Pseudomonas aeruginosa. J. Microbiol. Immunol. Infect. 2009, 42, 364–370.
39. Arima, H.; Ashida, H.; Danno, G.I. Rutin-enhanced antibacterial activities of flavonoids against Bacillus cereus and Salmonella enteritidis. Biosci. Biotechnol. Biochem. 2002, 66, 1009–1014.
40. European Committee on Antimicrobial Susceptibility Testing. Terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. EUCAST Definitive Document E. Def 1.2. Clin. Microbiol. Infect. 2000, 6, 503–508.
41. Resende, F.A.; Vilegas, W.; Dos Santos, L.C.; Varanda, E.A. Mutagenicity of flavonoids assayed by bacterial reverse mutation (Ames) test. Molecules 2012, 17, 5255–5268.