Staphylococcus epidermidis biofilms with higher proportions of dormant bacteria induce a lower activation of murine macrophages

Journal of Medical Microbiology

Volumn 60, Issue 12, 2011, Pages 1717-1724

  Cerca, Filipe ^a,b   Andrade, Filipa ^a   França, Ângela ^a,c   Andrade, Elva Bonifácio ^a,b   Ribeiro, Adília ^a   Almeida, Agostinho A ^a   Cerca, Nuno ^c   Pier, Gerald ^d   Azeredo, Joana ^c   Vilanova, Manuel ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF MINHO   (Portugal)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELL SURFACE PROTEIN; GLUCOSE; INTERLEUKIN 1; INTERLEUKIN 6; MAGNESIUM; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN GR1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; BIOFILM; BONE MARROW CELL; CYTOKINE PRODUCTION; DEVICE INFECTION; ENVIRONMENTAL FACTOR; EXTRACELLULAR CALCIUM; GLUCOSE METABOLISM; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INOCULATION; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAPHYLOCOCCUS EPIDERMIDIS;

ANIMALS; BACTERIAL ADHESION; BIOFILMS; BONE MARROW CELLS; CALCIUM; CELL CYCLE PROTEINS; CELLS, CULTURED; GLUCOSE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HYDROGEN-ION CONCENTRATION; INTERLEUKIN-1; INTERLEUKIN-6; MACROPHAGE ACTIVATION; MACROPHAGES; MAGNESIUM; MICE; MICE, INBRED BALB C; STAPHYLOCOCCUS EPIDERMIDIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 81355153709     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.031922-0     Document Type: Article

References (37)

1. Ben-Amor, K., Heilig, H., Smidt, H., Vaughan, E. E., Abee, T. & De Vos, W. M. (2005). Genetic diversity of viable, injured, and dead fecal bacteria assessed by fluorescence-activated cell sorting and 16S rRNA gene analysis. Appl Environ Microbiol 71, 4679-4689.
2. Brown, M. R. W., Allison, D. G. & Gilbert, P. (1988). Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? J Antimicrob Chemother 22, 777-780.
3. Cerca, N., Pier, G. B., Vilanova, M., Oliveira, R. & Azeredo, J. (2004). Influence of batch or fed-batch growth on Staphylococcus epidermidis biofilm formation. Lett Appl Microbiol 39, 420-424.
4. Cook, G. M. & Russell, J. B. (1994). The effect of extracellular pH and lactic acid on pH homeostasis Lactococcus lactis and Streptococcus bovis. Curr Microbiol 28, 165-168.
5. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. (1999). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322.
6. Costerton, W., Veeh, R., Shirtliff, M., Pasmore, M., Post, C. & Ehrlich, G. (2003). The application of biofilm science to the study and control of chronic bacterial infections. J Clin Invest 112, 1466-1477.
7. Croes, S., Deurenberg, R. H., Boumans, M.-L., Beisser, P. S., Neef, C. & Stobberingh, E. E. (2009). Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiol 9, 229.
8. Dasgupta, M. K., Lam, K., Ulan, R. A., Bettcher, K. B., Burns, V., Tyrrell, D. L., Dossetor, J. B. & Costerton, J. W. (1988). An extracorporeal model of biofilm-adherent bacterial microcolony colonization for the study of peritonitis in continuous ambulatory peritoneal dialysis. Am J Nephrol 8, 118-122.
9. Delavechia, C., Hampp, E., Fabra, A. & Castro, S. (2003). Influence of pH and calcium on the growth, polysaccharide production and symbiotic association of Sinorhizobium meliloti SEMIA 116 with alfalfa roots. Biol Fertil Soils 38, 110-114.
10. Ezekowitz, R. A. & Gordon, S. (1982). Down-regulation of mannosyl receptor-mediated endocytosis and antigen F4/80 in Bacillus Calmette-Guérin-activated mouse macrophages. Role of T lymphocytes and lymphokines. J Exp Med 155, 1623-1637.
11. Ezekowitz, R. A., Austyn, J., Stahl, P. D. & Gordon, S. (1981). Surface properties of Bacillus Calmette-Guérin-activated mouse macrophages. Reduced expression of mannose-specific endocytosis, Fc receptors, and antigen F4/80 accompanies induction of Ia. J Exp Med 154, 60-76.
12. Fux, C. A., Costerton, J. W., Stewart, P. S. & Stoodley, P. (2005). Survival strategies of infectious biofilms. Trends Microbiol 13, 34-40.
13. Härtel, C., Osthues, I., Rupp, J., Haase, B., Röder, K., Göpel, W., Herting, E. & Schultz, C. (2008). Characterisation of the host inflammatory response to Staphylococcus epidermidis in neonatal whole blood. Arch Dis Child Fetal Neonatal Ed 93, F140-F145.
14. Kaprelyants, A. S. & Kell, D. B. (1993). Dormancy in stationary-phase cultures of Micrococcus luteus: flow cytometric analysis of starvation and resuscitation. Appl Environ Microbiol 59, 3187-3196.
15. Kaprelyants, A. S., Gottschal, J. C. & Kell, D. B. (1993). Dormancy in nonsporulating bacterial. FEMS Microbiol Rev 104, 271-286.
16. Lemos, J. A. C., Abranches, J. & Burne, R. A. (2005). Responses of cariogenic streptococci to environmental stresses. Curr Issues Mol Biol 7, 95-107.
17. Lewis, K. (2007). Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5, 48-56.
18. Macció, D., Fabra, A. & Castro, S. (2002). Acidity and calcium interaction affect the growth of Bradyrhizobium sp. and the attachment to peanut roots. Soil Biol Biochem 34, 201-208.
19. Mack, D., Siemssen, N. & Laufs, R. (1992). Parallel induction by glucose of adherence and a polysaccharide antigen specific for plasticadherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect Immun 60, 2048-2057.
20. Mayhew, T. M. & Williams, M. A. (1973). The mass and size of normal and activated macrophages-studies with a scanning interferometer. Experientia 29, 80-81.
21. Megyeri, K., Mándi, Y., Degré, M. & Rosztóczy, I. (2002). Induction of cytokine production by different staphylococcal strains. Cytokine 19, 206-212.
22. +- activated macrophages induced during acute toxoplasmosis. J Leukoc Biol 74, 1015-1025.
23. O'Toole, G., Kaplan, H. B. & Kolter, R. (2000). Biofilm formation as microbial development. Annu Rev Microbiol 54, 49-79.
24. 2+ levels. Infect Immun 68, 4518-4522.
25. Qu, Y., Daley, A. J., Istivan, T. S., Rouch, D. A. & Deighton, M. A. (2010). Densely adherent growth mode, rather than extracellular polymer substance matrix build-up ability, contributes to high resistance of Staphylococcus epidermidis biofilms to antibiotics. J Antimicrob Chemother 65, 1405-1411.
26. Renye, J. A., Jr, Piggot, P. J., Daneo-Moore, L. & Buttaro, B. A. (2004). Persistence of Streptococcus mutans in stationary-phase batch cultures and biofilms. Appl Environ Microbiol 70, 6181-6187.
27. Rice, K. C., Nelson, J. B., Patton, T. G., Yang, S.-J. & Bayles, K. W. (2005). Acetic acid induces expression of the Staphylococcus aureus cidABC and lrgAB murein hydrolase regulator operons. J Bacteriol 187, 813-821.
28. Saegeman, V. S. M., De Vos, R., Tebaldi, N. D., Van der Wolf, J. M., Bergervoet, J. H. W., Verhaegen, J., Lismont, D., Verduyckt, B. & Ectors, N. L. (2007). Flow cytometric viability assessment and transmission electron microscopic morphological study of bacteria in glycerol. Microsc Microanal 13, 18-29.
29. Shen, Y., Stojicic, S. & Haapasalo, M. (2010). Bacterial viability in starved and revitalized biofilms: comparison of viability staining and direct culture. J Endod 36, 1820-1823.
30. Shleeva, M. O., Bagramyan, K., Telkov, M. V., Mukamolova, G. V., Young, M., Kell, D. B. & Kaprelyants, A. S. (2002). Formation and resuscitation of "non-culturable" cells of Rhodococcus rhodochrous and Mycobacterium tuberculosis in prolonged stationary phase. Microbiology 148, 1581-1591.
31. Stewart, P. S. & Franklin, M. J. (2008). Physiological heterogeneity in biofilms. Nat Rev Microbiol 6, 199-210.
32. Stuyt, R. J. L., Kim, S.-H., Reznikov, L. L., Fantuzzi, G., Novick, D., Rubinstein, M., Kullberg, B. J., Van der Meer, J. W. M., Dinarello, C. A. & Netea, M. G. (2003). Regulation of Staphylococcus epidermidisinduced IFN-γin whole human blood: the role of endogenous IL-18, IL-12, IL-1, and TNF. Cytokine 21, 65-73.
33. Vuong, C. & Otto, M. (2002). Staphylococcus epidermidis infections. Microbes Infect 4, 481-489.
34. Watkin, E. L. J., O'Hara, G. W. & Glenn, A. R. (1997). Calcium and acid stress interact to affect the growth of Rhizobium leguminosarum bv. trifolii. Soil Biol Biochem 29, 1427-1432.
35. Wijtzes, T., De Wit, J. C., In Huis, Van't, R. & Zwietering, M. H. (1995). Modelling bacterial growth of Lactobacillus curvatus as a function of acidity and temperature. Appl Environ Microbiol 61, 2533-2539.
36. Wolcott, R. D. & Ehrlich, G. D. (2008). Biofilms and chronic infections. JAMA 299, 2682-2684.
37. Yao, Y., Sturdevant, D. E. & Otto, M. (2005). Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenolsoluble modulins in formation of biofilms. J Infect Dis 191, 289-298.