Human lysozyme synergistically enhances bactericidal dynamics and lowers the resistant mutant prevention concentration for metronidazole to helicobacter pylori by increasing cell permeability

Molecules

Volumn 21, Issue 11, 2016, Pages

  Zhang, Xiaolin ^a   Jiang, Anmin ^b   Yu, Hao ^a   Xiong, Youyi ^a   Zhou, Guoliang ^a   Qin, Meisong ^a   Dou, Jinfeng ^a   Wang, Jianfei ^a,c  

^a ANHUI SCIENCE AND TECHNOLOGY UNIVERSITY   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

Author keywords

Bactericidal dynamics; H. Pylori; Human lysozyme; Metronidazole; Mutant prevention concentration

Indexed keywords

1 NAPHTHYLAMINE; ASPARTATE AMINOTRANSFERASE; LYSOZYME; LYSOZYME C, HUMAN; METRONIDAZOLE; N-PHENYL-1-NAPHTHYLAMINE;

ANALOGS AND DERIVATIVES; ANTIBIOTIC RESISTANCE; CELL WALL; DRUG EFFECTS; DRUG POTENTIATION; GENETICS; HELICOBACTER PYLORI; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; MUTATION;

1-NAPHTHYLAMINE; ASPARTATE AMINOTRANSFERASES; CELL WALL; DRUG RESISTANCE, BACTERIAL; DRUG SYNERGISM; HELICOBACTER PYLORI; HUMANS; METRONIDAZOLE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MURAMIDASE; MUTATION;

EID: 84993993161     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules21111435     Document Type: Article

References (39)

1. Moayyedi, P.; Hunt, R.H. Helicobacter pylori public health implications. Helicobacter 2004, 9, 67-72. [CrossRef] [PubMed]
2. Malfertheiner, P.; Chan, F.K.; McColl, K.E. Peptic ulcer disease. Lancet 2009, 374, 1449-1461. [CrossRef]
3. Kuipers, E.J. H. Pylori and the risk and management of associated diseases: Gastritis, ulcer disease, atrophic gastritis and gastric cancer. Aliment. Pharmacol. Ther. 1997, 11, 71-88. [CrossRef] [PubMed]
4. Wang, J.; Chen, R.C.; Zheng, Y.X.; Zhao, S.S.; Li, N.; Zhou, R.R.; Huang, Y.; Huang, Z.B.; Fan, X.G. Helicobacter pylori infection may increase the risk of progression of chronic hepatitis B disease among the Chinese population: A meta-analysis. Int. J. Infect. Dis. 2016, 50, 30-37. [CrossRef] [PubMed]
5. Zhao, B.; Zhao, J.; Cheng, W.F.; Shi, W.J.; Liu, W.; Pan, X.L.; Zhang, G.X. Efficacy of H. Pylori eradication therapy on functional dyspepsia: A meta-analysis of randomized controlled studies with 12-month follow-up. J. Clin. Gastroenterol. 2014, 48, 241-247. [CrossRef] [PubMed]
6. Guo, Q.; Guo, S.; Zhang, Y. Treatment of gastric MALT lymphoma with a focus on H. Pylori eradication. Int. J. Hematol. 2013, 97, 735-742. [CrossRef] [PubMed]
7. Shiotani, A.; Cen, P.; Graham, D.Y. Eradication of gastric cancer is now both possible and practical. Semin. Cancer Biol. 2013, 23, 492-501. [CrossRef] [PubMed]
8. Malfertheiner, P.; Megraud, F.; O'Morain, C.A.; Atherton, J.; Axon, A.T.; Bazzoli, F.; Gensini, G.F.; Gisbert, J.P.; Graham, D.Y.; Rokkas, T.; et al. Management of H. Pylori infection-the Maastricht IV/Florence Consensus Report. Gut 2012, 61, 646-664. [CrossRef] [PubMed]
9. Banić, M.; Franceschi, F.; Babić, Z.; Gasbarrini, A. Extragastric manifestations of H. Pylori infection. Helicobacter 2012, 17, 49-55.
10. Georgopoulos, S.D.; Polymeros, D.; Triantafyllou, K.; Spiliadi, C.; Mentis, A.; Karamanolis, D.G.; Ladas, S.D. Hypergastrinemia is associated with increased risk of distal colon adenomas. Digestion 2006, 74, 42-46. [CrossRef] [PubMed]
11. Houben, M.H.; van de Beek, D.; Hensen, E.F.; de Craen, A.J.; Rauws, E.A.; Tytgat, G.N. A systematic review of H. Pylori eradication therapy-the impact of antimicrobial resistance on eradication rates. Aliment. Pharmacol. Ther. 1999, 13, 1047-1055. [CrossRef] [PubMed]
12. Graham, D.Y.; Qureshi, W.A. Antibiotic-resistant H. Pylori infection and its treatment. Curr. Pharm. Des. 2000, 6, 1537-1544. [PubMed]
13. Zhao, X.; Drlica, K. Restricting the selection of antibiotic-resistant mutants: A general strategy derived from fluoroquinolone studies. Clin. Infect. Dis. 2001, 33, S147-S156. [CrossRef] [PubMed]
14. Olofsson, S.K.; Cars, O. Optimizing drug exposure to minimize selection of antibiotic resistance. Clin. Infect. Dis. 2007, 45, S129-S136. [CrossRef] [PubMed]
15. Drlica, K. The mutant selection window and antimicrobial resistance. J. Antimicrob. Chemother. 2003, 52, 11-17. [CrossRef] [PubMed]
16. Drlica, K.; Zhao, X. Mutant selection window hypothesis updated. Clin. Infect. Dis. 2007, 44, 681-688. [CrossRef] [PubMed]
17. Akinbi, H.T.; Epaud, R.; Bhatt, H.;Weaver, T.E. Bacterial killing is enhanced by expression of lysozyme in the lungs of transgenic mice. J. Immunol. 2000, 165, 5760-5766. [CrossRef] [PubMed]
18. Markart, P.; Korfhagen, T.R.; Weaver, T.E.; Akinbi, H.T. Mouse lysozyme M is important in pulmonary host defense against Klebsiella pneumoniae infection. Am. J. Respir. Crit. Care Med. 2004, 169, 454-458. [CrossRef] [PubMed]
19. Martinez, J.G.; Waldon, M.; Huang, Q.; Alvarez, S.; Oren, A.; Sandoval, N.; Du, M.; Zhou, F.; Zenz, A.; Lohner, K.; et al. Membrane-targeted synergistic activity of docosahexaenoic acid and lysozyme against Pseudomonas aeruginosa. Biochem. J. 2009, 419, 193-200. [CrossRef] [PubMed]
20. Koch, A.L. Bacterial wall as target for attack: Past, present, and future research. Clin. Microbiol. Rev. 2003, 16, 673-687. [CrossRef] [PubMed]
21. Ibrahim, H.R.; Matsuzaki, T.; Aoki, T. Genetic evidence that antibacterial activity of lysozyme is independent of its catalytic function. FEBS Lett. 2001, 506, 27-32. [CrossRef]
22. Nash, J.A.; Ballard, T.N.;Weaver, T.E.; Akinbi, H.T. The peptidoglycan degrading property of lysozyme is not required for bactericidal activity in vivo. J. Immunol. 2006, 177, 519-526. [CrossRef] [PubMed]
23. Wang, G.; Lo, L.F.; Forsberg, L.S.; Maier, R.J. Helicobacter pylori peptidoglycan modifications confer lysozyme resistance and contribute to survival in the host. MBio 2012, 3, e00409-12. [CrossRef] [PubMed]
24. Helander, I.M.; Mattila-Sandholm, T. Fluorometric assessment of gram-negative bacterial permeabilization. J. Appl. Microbiol. 2000, 88, 213-219. [CrossRef] [PubMed]
25. Loh, B.; Grant, C.; Hancock, R.E. Use of the fluorescent probe 1-N-Phenylnaphthyl-amine to study the interactions of aminoglycoside antibiotics with the outer membrane of pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1984, 26, 546-551. [CrossRef] [PubMed]
26. Nicoletti, I.; Migliorati, G.; Pagliacci, M.C.; Grignani, F.; Riccardi, C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 1991, 139, 271-279. [CrossRef]
27. Zhang, X.L.; Jiang, A.M.; Ma, Z.Y.; Li, X.B.; Xiong, Y.Y.; Dou, J.F.; Wang, J.F. The synthetic antimicrobial peptide Pexiganan and its nanoparticles (PNPs) exhibit the anti-H. Pylori activity in vitro and in vivo. Molecules 2015, 20, 3972-3985. [CrossRef] [PubMed]
28. De Francesco, V.; Giorgio, F.; Hassan, C.; Manes, G.; Vannella, L.; Panella, C.; Ierardi, E.; Zullo, A.Worldwide H. Pylori antibiotic resistance: A systematic review. J. Gastrointest. Liver Dis. 2010, 19, 409-414.
29. Mégraud, F. H. Pylori antibiotic resistance: Prevalence, importance, and advances in testing. Gut 2004, 53, 1374-1384.
30. Gao, W.; Cheng, H.; Hu, F.; Li, J.; Wang, L.; Yang, G.; Xu, L.; Zheng, X. The evolution of H. Pylori antibiotics resistance over 10 years in Beijing, China. Helicobacter 2010, 15, 460-466. [CrossRef] [PubMed]
31. Borody, T.J.; Carrick, J.; Hazell, S.L. Symptoms improve after the eradication of gastric Campylobacter pyloridis. Med. J. Aust. 1987, 146, 450-451. [PubMed]
32. Kuo, C.H.; Hsu, P.I.; Kuo, F.C.; Wang, S.S.; Hu, H.M.; Liu, C.J.; Chuah, S.K.; Chen, Y.H.; Hsieh, M.C.; Wu, D.C.; et al. Comparison of 10 day bismuth quadruple therapy with high-dose metronidazole or levofloxacin for second-line H. Pylori therapy: A randomized controlled trial. J. Antimicrob. Chemother. 2013, 68, 222-228. [CrossRef] [PubMed]
33. Liang, X.; Xu, X.; Zheng, Q.; Zhang, W.; Sun, Q.; Liu, W.; Xiao, S.; Lu, H. Efficacy of bismuth-containing quadruple therapies for clarithromycin-, metronidazole-, and fluoroquinolone-resistant H. Pylori infections in a prospective study. Clin. Gastroenterol. Hepatol. 2013, 11, 802-807. [CrossRef] [PubMed]
34. Jeong, J.Y.; Mukhopadhyay, A.K.; Dailidiene, D.; Wang, Y.; Velapatiño, B.; Gilman, R.H.; Parkinson, A.J.; Nair, G.B.; Wong, B.C.; Lam, S.K.; et al. Sequential inactivation of rdxA (HP0954) and frxA (HP0642) nitroreductase genes causes moderate and high-level metronidazole resistance in Helicobacter pylori. J. Bacteriol. 2000, 182, 5082-5090. [CrossRef] [PubMed]
35. Goodwin, A.; Kersulyte, D.; Sisson, G.; Veldhuyzen van Zanten, S.J.O.; Berg, D.E.; Hoffman, P.S. Metronidazole resistance in Helicobacter pylori is due to null mutations in a gene (rdxA) that encodes an oxygen-insensitive NADPH nitroreductase. Mol. Microbiol. 1998, 28, 383-393. [CrossRef] [PubMed]
36. Binh, T.T.; Suzuki, R.; Trang, T.T.; Kwon, D.H.; Yamaoka, Y. Search for novel candidate mutations for metronidazole resistance in Helicobacter pylori using next-generation sequencing. Antimicrob. Agents Chemother. 2015, 59, 2343-2348. [CrossRef] [PubMed]
37. Ward, D.E.; de Vos, W.M.; van der Oost, J. Molecular analysis of the role of two aromatic aminotrans-ferases and a broad-specificity aspartate aminotransferase in the aromatic amino acid metabolism of Pyrococcus furiosus. Archaea 2002, 1, 133-141. [CrossRef] [PubMed]
38. Zhao, X.; Drlica, K. Restricting the selection of antibiotic-resistant mutant bacteria: Measurement and potential use of the mutant selection window. J. Infect. Dis. 2002, 185, 561-565. [CrossRef] [PubMed]
39. Blondeau, J.M.; Zhao, X.; Hansen, G.; Drlica, K. Mutant prevention concentration of fluoroquinolones for clinical isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2001, 45, 433-438. [CrossRef] [PubMed]