Sputum containing zinc enhances carbapenem resistance, biofilm formation and virulence of Pseudomonas aeruginosa

Microbial Pathogenesis

Volumn 77, Issue , 2014, Pages 36-41

  Marguerettaz, Mélanie ^a   Dieppois, Guennaëlle ^a   Que, Yok Ai ^b   Ducret, Véréna ^a   Zuchuat, Sandrine ^a   Perron, Karl ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Biofilm; Carbapenem; Cystic fibrosis; Pseudomonas aeruginosa; Sputum; Virulence; Zinc

Indexed keywords

CADMIUM; CARBAPENEM; ELASTASE; MESSENGER RNA; PORIN; RHAMNOLIPID; ZINC; ANTIINFECTIVE AGENT; CARBAPENEM DERIVATIVE; CARRIER PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BIOFILM; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYSTIC FIBROSIS; DISEASE EXACERBATION; GENE EXPRESSION REGULATION; LASB GENE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OPRD GENE; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RHLA GENE; SPUTUM ANALYSIS; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPUTUM; VIRULENCE;

ANTI-BACTERIAL AGENTS; BIOFILMS; CARBAPENEMS; DRUG RESISTANCE, BACTERIAL; HUMANS; MEMBRANE TRANSPORT PROTEINS; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; SPUTUM; VIRULENCE; ZINC;

EID: 84908577450     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2014.10.011     Document Type: Article

References (57)

1. Formigari A., Irato P., Santon A. Zinc, antioxidant systems and metallothionein in metal mediated-apoptosis: biochemical and cytochemical aspects. Comp. Biochem. Physiology Toxicol. Pharmacol. CBP 2007, 146(4):443-459.
2. Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283(2-3):65-87.
3. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39(1):44-84.
4. Berger M.M., Cavadini C., Bart A., Mansourian R., Guinchard S., Bartholdi I., Vandervale A., Krupp S., Chiolero R., Freeman J., et al. Cutaneous copper and zinc losses in burns. Burns 1992, 18(5):373-380.
5. Gray R.D., Duncan A., Noble D., Imrie M., O'Reilly D.S., Innes J.A., Porteous D.J., Greening A.P., Boyd A.C. Sputum trace metals are biomarkers of inflammatory and suppurative lung disease. Chest 2010, 137(3):635-641.
6. Smith D.J., Anderson G.J., Bell S.C., Reid D.W. Elevated metal concentrations in the CF airway correlate with cellular injury and disease severity. J. Cyst. Fibros. Official J. Eur. Cyst. Fibros. Soc. 2014, 13(3):289-295.
7. Latunde-Dada G.O. Iron metabolism: microbes, mouse, and man. BioEssays news Rev. Mol. Cell. Dev. Biol. 2009, 31(12):1309-1317.
8. Weinberg E.D. Iron availability and infection. Biochim. Biophys. Acta 2009, 1790(7):600-605.
9. Hodgkinson V., Petris M.J. Copper homeostasis at the host-pathogen interface. J. Biol. Chem. 2012, 287(17):13549-13555.
10. Samanovic M.I., Ding C., Thiele D.J., Darwin K.H. Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe 2012, 11(2):106-115.
11. Benoit S.L., Miller E.F., Maier R.J. Helicobacter pylori stores nickel to aid its host colonization. Infect Immun. 2013, 81(2):580-584.
12. Fones H., Preston G.M. The impact of transition metals on bacterial plant disease. FEMS Microbiol. Rev. 2013, 37(4):495-519.
13. Reva O., Bezuidt O. Distribution of horizontally transferred heavy metal resistance operons in recent outbreak bacteria. Mob. Genet. Elem. 2012, 2(2):96-100.
14. Caille O., Rossier C., Perron K. Acopper-activated two-component system interacts with zinc and imipenem resistance in Pseudomonas aeruginosa. J. Bacteriol. 2007, 189(13):4561-4568.
15. Perron K., Caille O., Rossier C., Van Delden C., Dumas J.L., Kohler T. CzcR-CzcS, a two-component system involved in heavy metal and carbapenem resistance in Pseudomonas aeruginosa. J. Biol. Chem. 2004, 279(10):8761-8768.
16. Dieppois G., Ducret V., Caille O., Perron K. The transcriptional regulator CzcR modulates antibiotic resistance and quorum sensing in Pseudomonas aeruginosa. PLoS One 2012, 7(5). e38148.
17. Rosenfeld M., Ramsey B.W., Gibson R.L. Pseudomonas acquisition in young patients with cystic fibrosis: pathophysiology, diagnosis, and management. Curr. Opin. Pulm. Med. 2003, 9(6):492-497.
18. Juhas M., Eberl L., Tummler B. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ. Microbiol. 2005, 7(4):459-471.
19. Trias J., Nikaido H. Protein D2 channel of the Pseudomonas aeruginosa outer membrane has a binding site for basic amino acids and peptides. J. Biol. Chem. 1990, 265(26):15680-15684.
20. Trias J., Nikaido H. Outer membrane protein D2 catalyzes facilitated diffusion of carbapenems and penems through the outer membrane of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1990, 34(1):52-57.
21. Sriramulu D.D., Lunsdorf H., Lam J.S., Romling U. Microcolony formation: a novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung. J. Med. Microbiol. 2005, 54(Pt. 7):667-676.
22. Fung C., Naughton S., Turnbull L., Tingpej P., Rose B., Arthur J., Hu H., Harmer C., Harbour C., Hassett D.J., et al. Gene expression of Pseudomonas aeruginosa in a mucin-containing synthetic growth medium mimicking cystic fibrosis lung sputum. J. Med. Microbiol. 2010, 59(Pt 9):1089-1100.
23. Versieck J. Trace elements in human body fluids and tissues. Crit. Rev. Clin. Lab. Sci. 1985, 22(2):97-184.
24. Abrantes M.C., Lopes Mde F. Kok J: Impact of manganese, copper and zinc ions on the transcriptome of the nosocomial pathogen Enterococcus faecalis V583. PLoS One 2011, 6(10). e26519.
25. Wiegand I., Hilpert K., Hancock R.E. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 2008, 3(2):163-175.
26. EloffJ.N. Asensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta. Med. 1998, 64(8):711-713.
27. Studier F.W., Rosenberg A.H., Dunn J.J., DubendorffJ.W. Use of T7 RNA polymerase to direct expression of cloned genes. Meth. Enzym. 1990, 185:60-89.
28. PfafflM.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic. Acids Res. 2002, 30(9). e36.
29. Moreau-Marquis S., Stanton B.A., O'Toole G.A. Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm. Pharmacol. Ther. 2008, 21(4):595-599.
30. Sutherland I.W. The biofilm matrix-an immobilized but dynamic microbial environment. Trends. Microbiol. 2001, 9(5):222-227.
31. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284(5418):1318-1322.
32. Singh P.K., Schaefer A.L., Parsek M.R., Moninger T.O., Welsh M.J., Greenberg E.P. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 2000, 407(6805):762-764.
33. Hoiby N., Krogh Johansen H., Moser C., Song Z., Ciofu O., Kharazmi A. Pseudomonas aeruginosa and the invitro and invivo biofilm mode of growth. Microbes. Infect. 2001, 3(1):23-35.
34. Worlitzsch D., Tarran R., Ulrich M., Schwab U., Cekici A., Meyer K.C., Birrer P., Bellon G., Berger J., Weiss T., et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 2002, 109(3):317-325.
35. Kirchner S., Fothergill J.L., Wright E.A., James C.E., Mowat E., Winstanley C. Use of artificial sputum medium to test antibiotic efficacy against Pseudomonas aeruginosa in conditions more relevant to the cystic fibrosis lung. J. Vis. Exp. 2012, (64). e3857.
36. Folkesson A., Jelsbak L., Yang L., Johansen H.K., Ciofu O., Hoiby N., Molin S. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat. Rev. Microbiol. 2012, 10(12):841-851.
37. Yang L., Jelsbak L., Molin S. Microbial ecology and adaptation in cystic fibrosis airways. Environ. Microbiol. 2011, 13(7):1682-1689.
38. Martin D.W., Schurr M.J., Mudd M.H., Govan J.R., Holloway B.W., Deretic V. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. U S A 1993, 90(18):8377-8381.
39. Smith E.E., Buckley D.G., Wu Z., Saenphimmachak C., Hoffman L.R., D'Argenio D.A., Miller S.I., Ramsey B.W., Speert D.P., Moskowitz S.M., et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. U S A 2006, 103(22):8487-8492.
40. Hogardt M., Heesemann J. Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. Int. J. Med. Microbiol. 2010, 300(8):557-562.
41. Li H., Luo Y.F., Williams B.J., Blackwell T.S., Xie C.M. Structure and function of OprD protein in Pseudomonas aeruginosa: from antibiotic resistance to novel therapies. Int. J. Med. Microbiol. 2012, 302(2):63-68.
42. Lister P.D., Wolter D.J., Hanson N.D. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin. Microbiol. Rev. 2009, 22(4):582-610.
43. Muller C., Plesiat P., Jeannot K. Atwo-component regulatory system interconnects resistance to polymyxins, aminoglycosides, fluoroquinolones, and beta-lactams in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2011, 55(3):1211-1221.
44. Ochs M.M., McCusker M.P., Bains M., Hancock R.E. Negative regulation of the Pseudomonas aeruginosa outer membrane porin OprD selective for imipenem and basic amino acids. Antimicrob. Agents Chemother. 1999, 43(5):1085-1090.
45. Kohler T., Epp S.F., Curty L.K., Pechere J.C. Characterization of MexT, the regulator of the MexE-MexF-OprN multidrug efflux system of Pseudomonas aeruginosa. J. Bacteriol. 1999, 181(20):6300-6305.
46. Booth S.C., Workentine M.L., Wen J., Shaykhutdinov R., Vogel H.J., Ceri H., Turner R.J., Weljie A.M. Differences in metabolism between the biofilm and planktonic response to metal stress. J. Proteome Res. 2011, 10(7):3190-3199.
47. Davies D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2003, 2(2):114-122.
48. Workentine M.L., Sibley C.D., Glezerson B., Purighalla S., Norgaard-Gron J.C., Parkins M.D., Rabin H.R., Surette M.G. Phenotypic heterogeneity of Pseudomonas aeruginosa populations in a cystic fibrosis patient. PLoS One 2013, 8(4). e60225.
49. Conrady D.G., Brescia C.C., Horii K., Weiss A.A., Hassett D.J., Herr A.B. Azinc-dependent adhesion module is responsible for intercellular adhesion in staphylococcal biofilms. Proc. Natl. Acad. Sci. U S A 2008, 105(49):19456-19461.
50. Conrady D.G., Wilson J.J., Herr A.B. Structural basis for Zn2+-dependent intercellular adhesion in staphylococcal biofilms. Proc. Natl. Acad. Sci. U S A 2013, 110(3):E202-E211.
51. Banin E., Brady K.M., Greenberg E.P. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl. Environ. Microbiol. 2006, 72(3):2064-2069.
52. Singh P.K., Parsek M.R., Greenberg E.P., Welsh M.J. Acomponent of innate immunity prevents bacterial biofilm development. Nature 2002, 417(6888):552-555.
53. Sobke A., Klinger M., Hermann B., Sachse S., Nietzsche S., Makarewicz O., Keller P.M., Pfister W., Straube E. The urinary antibiotic 5-nitro-8-hydroxyquinoline (Nitroxoline) reduces the formation and induces the dispersal of Pseudomonas aeruginosa biofilms by chelation of iron and zinc. Antimicrob. Agents Chemother. 2012, 56(11):6021-6025.
54. Berger M.M., Chiolero R. Relations between copper, zinc and selenium intakes and malondialdehyde excretion after major burns. Burns 1995, 21(7):507-512.
55. Voruganti V.S., Klein G.L., Lu H.X., Thomas S., Freeland-Graves J.H., Herndon D.N. Impaired zinc and copper status in children with burn injuries: need to reassess nutritional requirements. Burns 2005, 31(6):711-716.
56. Dardenne M. Zinc and immune function. Eur. J. Clin. Nutr 2002, 56(Suppl.3):S20-S23.
57. Berger M.M. Antioxidant micronutrients in major trauma and burns: evidence and practice. Nutr. Clin. Pract. Official Publ. Am. Soc. Parenter. Enter. Nutr. 2006, 21(5):438-449.