Increased uptake and improved intracellular survival of a teicoplanin-resistant mutant of methicillin-resistant staphylococcus aureus in non-professional phagocytes

Chemotherapy

Volumn 55, Issue 3, 2009, Pages 183-188

  Renzoni, Adriana ^a   Huggler, Elzbieta ^a   Kelley, William L ^a   Lew, Daniel ^a   Vaudaux, Pierre ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Endocytic uptake; Human epithelial cells; Intracellular survival; Staphylococcus aureus; Teicoplanin resistance

Indexed keywords

GENTAMICIN; GLYCOPEPTIDE; TEICOPLANIN; VANCOMYCIN;

ARTICLE; BACTERIAL MUTATION; BACTERIUM ISOLATION; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; COLONY FORMING UNIT; CONTROLLED STUDY; EPITHELIUM CELL; GENETIC RESISTANCE; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ANTI-BACTERIAL AGENTS; CELL LINE; DRUG RESISTANCE, BACTERIAL; HUMANS; LYSOSTAPHIN; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MUTATION; PHAGOCYTES; TEICOPLANIN; TIME FACTORS;

EID: 65449145237     PISSN: 00093157     EISSN: None     Source Type: Journal    
DOI: 10.1159/000215304     Document Type: Article

References (44)

1. Lowy FD:Staphylococcus aureus infections. N Engl J Med 1998;339:520-532.
2. Fux CA, Costerton JW, Stewart PS, Stoodley P:Survival strategies of infectious biofilms. Trends Microbiol 2005;13:34-40.
3. Proctor RA, Von Eiff C, Kahl BC, Becker K, McNamara P, Herrmann M, Peters G:Small colony variants:a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 2006;4:295-305.
4. Lowy FD:Is Staphylococcus aureus an intracellular pathogen? Trends Microbiol 2000;8:341-343.
5. Massey RC, Kantzanou MN, Fowler T, Day NP, Schofield K, Wann ER, Berendt AR, Hook M, Peacock SJ:Fibronectin-binding protein A of Staphylococcus aureus has multiple, substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell Microbiol 2001;3:839-851.
6. Fowler T, Johansson S, Wary KK, Hook M:Src kinase has a central role in in vitro cellular internalization of Staphylococcus aureus. Cell Microbiol 2003;5:417-426.
7. Sinha B, Francois PP, Nüsse O, Foti M, Hartford OM, Vaudaux P, Foster TJ, Lew DP, Herrmann M, Krause KH:Fibronectinbinding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol 1999;1:101-118.
8. Agerer F, Michel A, Ohlsen K, Hauck CR:Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J Biol Chem 2003;278:42524-42531.
9. Garzoni C, Kelley WL:Staphylococcus aureus:new evidence for intracellular persistence. Trends Microbiol 2009;17:59-65.
10. Sinha B, Francois P, Que YA, Hussain M, Heilmann C, Moreillon P, Lew D, Krause KH, Peters G, Herrmann M:Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect Immun 2000;68:6871-6878.
11. Agerer F, Lux S, Michel A, Rohde M, Ohlsen K, Hauck CR:Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J Cell Sci 2005;118:2189-2200.
12. Clement S, Vaudaux P, Francois P, Schrenzel J, Huggler E, Kampf S, Chaponnier C, Lew D, Lacroix JS:Evidence of an intracellular reservoir in the nasal mucosa of patients with recurrent Staphylococcus aureus rhinosinusitis. J Infect Dis 2005;192:1023-1028.
13. Plouin-Gaudon I, Clement S, Huggler E, Chaponnier C, Francois P, Lew D, Schrenzel J, Vaudaux P, Lacroix JS:Intracellular residency is frequently associated with recurrent Staphylococcus aureus rhinosinusitis. Rhinolog y 2006;44:249-254.
14. Sendi P, Rohrbach M, Graber P, Frei R, Ochsner PE, Zimmerli W:Staphylococcus aureus small colony variants in prosthetic joint infection. Clin Infect Dis 2006;43:961-967.
15. Liu C, Chambers HF:Staphylococcus aureus with heterogeneous resistance to vancomycin:epidemiology, clinical significance, and critical assessment of diagnostic methods. Antimicrob Agents Chemother 2003;47:3040-3045.
16. Lowy FD:Antimicrobial resistance:the example of Staphylococcus aureus. J Clin Invest 2003;111:1265-1273.
17. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, De Lencastre H, Richardson P, Bruce D, Rubin E, Myers E, Siggia ED, Tomasz A:Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Natl Acad Sci USA 2007;10 4:9451-9456.
18. Cui L, Lian JQ, Neoh HM, Reyes E, Hiramatsu K:DNA microarray-based identification of genes associated with glycopeptide resistance in Staphylococcus aureus. Antimicrob Agents Chemother 2005;49:3404-3413.
19. McAleese F, Wu SW, Sieradzki K, Dunman P, Murphy E, Projan S, Tomasz A:Overexpression of genes of the cell wall stimulon in clinical isolates of Staphylococcus aureus exhibiting vancomycin-intermediate- S. aureus -type resistance to vancomycin. J Bacteriol 2006;188:1120 -1133.
20. Renzoni A, Barras C, Francois P, Charbonnier Y, Huggler E, Garzoni C, Kelley WL, Majcherczyk P, Schrenzel J, Lew DP, Vaudaux P:Transcriptomic and functional analysis of an autolysis-deficient, teicoplanin-re-sistant derivative of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2006;50:3048-3061.
21. Scherl A, Francois P, Charbonnier Y, Deshusses JM, Koessler T, Huyghe A, Bento M, Stahl-Zeng J, Fischer A, Masselot A, Vaezzadeh A, Galle F, Renzoni A, Vaudaux P, Lew D, Zimmermann-Ivol CG, Binz PA, Sanchez JC, Hochstrasser DF, Schrenzel J:Exploring glycopeptide-resistance in Staphylococcus aureus:a combined proteomics and transcriptomics approach for the identification of resistance-related markers. BMC Genomics 2006;7:296.
22. Drummelsmith J, Winstall E, Bergeron MG, Poirier GG, Ouellette M:Comparative proteomics analyses reveal a potential biomarker for the detection of vancomycin-intermediate Staphylococcus aureus strains. J Proteome Res 2007;6:4690-4702.
23. Sieradzki K, Tomasz A:Inhibition of the autolytic system by vancomycin causes mimicry of vancomycin-intermediate Staphylococcus aureus-type resistance, cell concentration dependence of the MIC, and antibiotic tolerance in vancomycin-susceptible S. aureus. Antimicrob Agents Chemother 2006;50:527-533.
24. Renzoni A, Francois P, Li D, Kelley WL, Lew DP, Vaudaux P, Schrenzel J:Modulation of fibronectin adhesins and other virulence factors in a teicoplanin-resistant derivative of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2004;48:2958-2965.
25. Vaudau x P, Francois P, Berger-Bächi B, Lew D:In vivo emergence of subpopulations expressing teicoplanin or vancomycin-resistant phenotypes in a glycopeptide-susceptible, methicillin-resistant strain of Staphylococcus aureus. J Antimicrob Chemother 2001;47:16 3 -17 0 .
26. Lucet JC, Herrmann M, Rohner P, Auckenthaler R, Waldvogel FA, Lew DP:Treatment of experimental foreign body infection caused by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 1990;34:2312-2317.
27. Juuti KM, Sinha B, Werbick C, Peters G, Kuusela PI:Reduced adherence and host cell invasion by methicillin-resistant Staphylococcus aureus expressing the surface protein Pls. J Infect Dis 2004;18 9:1574-1584 .
28. Werbick C, Becker K, Mellmann A, Juuti KM, Von Eiff C, Peters G, Kuusela PI, Friedrich AW, Sinha B:Staphylococcal chromosomal cassette mec type I, spa type, and expression of Pls are determinants of reduced cellular invasiveness of methicillin-resistant Staphylococcus aureus isolates. J Infect Dis 2007;195:1678-1685.
29. Vaudaux P, Waldvogel FA:Gentamicin antibacterial activity in the presence of human polymorphonuclear leukocytes. Antimicrob Agents Chemother 1979;16:743-749.
30. Bernard L, Vaudaux P, Merle C, Stern R, Huggler E, Lew D, Hoffmeyer P:The inhibition of neutrophil antibacterial activity by ultra-high molecular weight polyethylene particles. Biomaterials 2005;26:5552-5557.
31. Vesga O, Groeschel MC, Otten MF, Brar DW, Vann JM, Proctor RA:Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J Infect Dis 1996;173:739-742.
32. Vaud au x P, Fra ncois P, Bisog na no C, Kelley WL, Lew DP, Schrenzel J, Proctor RA, Mc-Namara PJ, Peters G, Von Eiff C:Increased expression of clumping factor and fibronec-tin-binding proteins by hemB mutants of Staphylococcus aureus expressing small colony variant phenotypes. Infect Immun 2002;70:5428-5437.
33. Savolainen K, Paulin L, Westerlund-Wik-ström B, Foster TJ, Korhonen TK, Kuusela P:Expression of pls, a gene closely associated with the mecA gene of methicillin-resistant Staphylococcus aureus, pre vent s bac t e r ia l adhesion in vitro. Infect Immun 2001;69:3013-3020.
34. Huesca M, Peralta R, Sauder DN, Simor AE, McGavin MJ:Adhesion and virulence properties of epidemic Canadian methicillin-re-sistant Staphylococcus aureus strain. 1. identification of novel adhesion functions associated with plasmin-sensitive surface protein. J Infect Dis 2002;185:1285-1296.
35. Vaudaux P, Monzillo V, Francois P, Lew DP, Foster TJ, Berger-Bächi B:Introduction of the mec element (methicillin resistance) into Staphylococcus aureus alters in vitro functional activities of fibrinogen and fibronec-tin adhesins. Antimicrob Agents Chemother 1998;42:564-570.
36. Krut O, Utermohlen O, Schlossherr X, Kronke M:Strain-specific association of cytotoxic activity and virulence of clinical Staphylococcus aureus isolates. Infect Immun 20 03;71:2716-2723.
37. Haslinger-Loffler B, Kahl BC, Grundmeier M, Strangfeld K, Wagner B, Fischer U, Cheung AL, Peters G, Schulze-Osthoff K, Sinha B:Multiple virulence factors are required for Staphylococcus aureus-induced apoptosis in endothelial cells. Cell Microbiol 2005;7:1087-1097.
38. Bayles KW, Wesson CA, Liou LE, Fox LK, Bohach GA, Trumble WR:Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect Immun 1998;66:336 -342 .
39. Wesson CA, Deringer J, Liou LE, Bayles KW, Bohach GA, Trumble WR:Apoptosis induced by Staphylococcus aureus in epithelial cells utilizes a mechanism involving caspases 8 and 3. Infect Immun 200 0;68:2998-3001.
40. Bantel H, Sinha B, Domschke W, Peters G, Schulze-Osthoff K, Janicke RU:Alpha-toxin is a mediator of Staphylococcus aureus-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J Cell Biol 2001;155:637- 648.
41. Schnaith A, Kashkar H, Leggio SA, Addicks K, Kronke M, Krut O:Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J Biol Chem 2007;282:2695-2706.
42. Garzoni C, Francois P, Huyghe A, Couzinet S, Tapparel C, Charbonnier Y, Renzoni A, Lucchini S, Lew DP, Vaudaux P, Kelley WL, Schrenzel J:A global view of Staphylococcus aureus whole genome expression upon internalization in human epithelial cells. BMC Genomics 2007;8:171.
43. Ates-Alagoz Z, Yildiz S, Buyukbingol E:Antimicrobial activities of some tetrahy-dronaphthalene-benzimidazole derivatives. Chemotherapy 2007;53:110-113.
44. Schillaci D, Maggio B, Raffa D, Daidone G, Cascioferro S, Cusimano MG, Raimondi MV:4-Diazopyrazole derivatives as potential new antibiofilm agents. Chemotherapy 2008;54:456-462.