Pharmacodynamic evaluation of the activity of antibiotics against hemin- and menadione-dependent small-colony variants of Staphylococcus aureus in models of extracellular (broth) and intracellular (THP-1 monocytes) infections

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 7, 2012, Pages 3700-3711

  Garcia, L G ^a   Lemaire, S ^a   Kahl, B C ^b   Becker, K ^b   Proctor, R A ^c   Denis, O ^d   Tulkens, P M ^a   Van Bambeke, F ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DAPTOMYCIN; GENTAMICIN; HEMIN; MENADIONE; MOXIFLOXACIN; ORITAVANCIN; RIFAMPICIN; VANCOMYCIN;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; HUMAN; HUMAN CELL; MAXIMUM PLASMA CONCENTRATION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SINGLE DRUG DOSE; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; CELL LINE; DAPTOMYCIN; GENTAMICINS; GLYCOPEPTIDES; HEMIN; HUMANS; MICROBIAL SENSITIVITY TESTS; MONOCYTES; RIFAMPIN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VANCOMYCIN; VITAMIN K 3;

EID: 84862530787     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00285-12     Document Type: Article

References (69)

1. Arhin FF, et al. 2008. Effect of polysorbate 80 on oritavancin binding to plastic surfaces: implications for susceptibility testing. Antimicrob. Agents Chemother. 52:1597-1603.
2. Atalla H, Gyles C, Mallard B. 2010. Persistence of a Staphylococcus aureus small colony variants (S. aureus SCV) within bovine mammary epithelial cells. Vet. Microbiol. 143:319-328.
3. Baba-Moussa L, et al. 2008. Virulence factors produced by strains of Staphylococcus aureus isolated from urinary tract infections. J. Hosp. Infect. 68:32-38.
4. Baltch AL, Ritz WJ, Bopp LH, Michelsen P, Smith RP. 2008. Activities of daptomycin and comparative antimicrobials, singly and in combination, against extracellular and intracellular Staphylococcus aureus and its stable small-colony variant in human monocyte-derived macrophages and in broth. Antimicrob. Agents Chemother. 52:1829-1833.
5. Balwit JM, van Langevelde P, Vann JM, Proctor RA. 1994. Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J. Infect. Dis. 170:1033-1037.
6. Barcia-Macay M, Lemaire S, Mingeot-Leclercq MP, Tulkens PM, Van Bambeke F. 2006. Evaluation of the extracellular and intracellular activities (human THP-1 macrophages) of telavancin versus vancomycin against methicillin- susceptible, methicillin-resistant, vancomycin-intermediate and vancomycin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 58:1177-1184.
7. Barcia-Macay M, Seral C, Mingeot-Leclercq MP, Tulkens PM, Van Bambeke F. 2006. Pharmacodynamic evaluation of the intracellular activities of antibiotics against Staphylococcus aureus in a model of THP-1 macrophages. Antimicrob. Agents Chemother. 50:841-851.
8. Barza M. 1994. Challenges to antibiotic activity in tissue. Clin. Infect. Dis. 19:910-915.
9. Bates DM, et al. 2003. Staphylococcus aureus menD and hemB mutants are as infective as the parent strains, but the menadione biosynthetic mutant persists within the kidney. J. Infect. Dis. 187:1654-1661.
10. Belley A, et al. 2011. Comparison of a single dose of oritavancin to daily dosing regimens of daptomycin or vancomycin against methicillin-resistant Staphylococcus aureus in an in vitro pharmacokinetic/pharmacodynamic model, poster A1-021. Abstr. 51th Intersci. Conf. Antimicrob. Agents Chemother., Chicago, IL.
11. Belley A, et al. 2009. Oritavancin kills stationary-phase and biofilm Staphylococcus aureus cells in vitro. Antimicrob. Agents Chemother. 53:918-925.
12. Besier S, et al. 2007. Prevalence and clinical significance of Staphylococcus aureus small-colony variants in cystic fibrosis lung disease. J. Clin. Microbiol. 45:168-172.
13. Clinical and Laboratory Standards Institute. 2010. Performance standards for antimicrobial susceptibility testing. Twentieth informational supplement (MS100-S20) (29). Clinical and Laboratory Standards Institute, Wayne, PA.
14. Dyke KG. 1969. Penicillinase production and intrinsic resistance to penicillins in methicillin-resistant cultures of Staphylococcus aureus. J. Med. Microbiol. 2:261-278.
15. Eisenberg ES, Mandel LJ, Kaback HR, Miller MH. 1984. Quantitative association between electrical potential across the cytoplasmic membrane and early gentamicin uptake and killing in Staphylococcus aureus. J. Bacteriol. 157:863-867.
16. Fuchs PC, Barry AL, Brown SD. 2000. Daptomycin susceptibility tests: interpretive criteria, quality control, and effect of calcium on in vitro tests. Diagn. Microbiol. Infect. Dis. 38:51-58.
17. Ghigo E, et al. 2002. Coxiella burnetii survival in THP-1 monocytes involves the impairment of phagosome maturation: IFN-gamma mediates its restoration and bacterial killing. J. Immunol. 169:4488-4495.
18. Gilligan PH, Gage PA, Welch DF, Muszynski MJ, Wait KR. 1987. Prevalence of thymidine-dependent Staphylococcus aureus in patients with cystic fibrosis. J. Clin. Microbiol. 25:1258-1261.
19. Idelevich EA, et al. 2011. Comparative in vitro activity of finafloxacin against staphylococci displaying normal and small colony variant phenotypes. J. Antimicrob. Chemother. 66:2809-2813.
20. Jiang M, et al. 2007. Menaquinone biosynthesis in Escherichia coli: identification of 2-succinyl-5-enolpyruvyl-6-hydroxy-3-cyclohexene-1-carboxylate as a novel intermediate and re-evaluation of MenD activity. Biochemistry 46:10979-10989.
21. Kahl B, et al. 1998. Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J. Infect. Dis. 177:1023-1029.
22. Kahl BC, et al. 2003. Population dynamics of persistent Staphylococcus aureus isolated from the airways of cystic fibrosis patients during a 6-year prospective study. J. Clin. Microbiol. 41:4424-4427.
23. Karauzum H, et al. 2008. Comparison of adhesion and virulence of two predominant hospital-acquired methicillin-resistant Staphylococcus aureus clones and clonal methicillin-susceptible S. aureus isolates. Infect. Immun. 76:5133-5138.
24. Kohler C, et al. 2008. A defect in menadione biosynthesis induces global changes in gene expression in Staphylococcus aureus. J. Bacteriol. 190:6351-6364.
25. Lannergard J, et al. 2008. Identification of the genetic basis for clinical menadione-auxotrophic small-colony variant isolates of Staphylococcus aureus. Antimicrob. Agents Chemother. 52:4017-4022.
26. Lecaroz C, Blanco-Prieto MJ, Burrell MA, Gamazo C. 2006. Intracellular killing of Brucella melitensis in human macrophages with microsphere- encapsulated gentamicin. J. Antimicrob. Chemother. 58:549-556.
27. Lemaire S, et al. 2009. Activities of ceftobiprole and other cephalosporins against extracellular and intracellular (THP-1 macrophages and keratinocytes) forms of methicillin-susceptible and methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 53:2289-2297.
28. Lemaire S, et al. 2011. Activity of moxifloxacin against intracellular community-acquired methicillin-resistant Staphylococcus aureus: comparison with clindamycin, linezolid and co-trimoxazole and attempt at defining an intracellular susceptibility breakpoint. J. Antimicrob. Chemother. 66:596-607.
29. Lemaire S, et al. 2010. Cellular pharmacodynamics of the novel biaryloxazolidinone radezolid: studies with infected phagocytic and nonphagocytic cells, using Staphylococcus aureus, Staphylococcus epidermidis, Listeria monocytogenes, and Legionella pneumophila. Antimicrob. Agents Chemother. 54:2549-2559.
30. Lemaire S, Tulkens PM, Van Bambeke F. 2011. Contrasting effects of acidic pH on the extracellular and intracellular activities of the anti-gram-positive fluoroquinolones moxifloxacin and delafloxacin against Staphylococcus aureus. Antimicrob. Agents Chemother. 55:649-658.
31. Lemaire S, Van Bambeke F, Tulkens PM. 2011. Activity of finafloxacin, a novel fluoroquinolone with increased activity at acid pH, towards extracellular and intracellular Staphylococcus aureus, Listeria monocytogenes and Legionella pneumophila. Int. J. Antimicrob. Agents 38:52-59.
32. Liu C, et al. 2011. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children: executive summary. Clin. Infect. Dis. 52:285-292.
33. Mascio CT, Alder JD, Silverman JA. 2007. Bactericidal action of daptomycin against stationary-phase and nondividing Staphylococcus aureus cells. Antimicrob. Agents Chemother. 51:4255-4260.
34. Mates SM, et al. 1982. Membrane potential and gentamicin uptake in Staphylococcus aureus. Proc. Natl. Acad. Sci. U. S. A. 79:6693-6697.
35. McNamara PJ, Proctor RA. 2000. Staphylococcus aureus small colony variants, electron transport and persistent infections. Int. J. Antimicrob. Agents 14:117-122.
36. Miller MH, Edberg SC, Mandel LJ, Behar CF, Steigbigel NH. 1980. Gentamicin uptake in wild-type and aminoglycoside-resistant smallcolony mutants of Staphylococcus aureus. Antimicrob. Agents Chemother. 18:722-729.
37. Murillo O, et al. 2006. Efficacy of high doses of levofloxacin in experimental foreign-body infection by methicillin-susceptible Staphylococcus aureus. Antimicrob. Agents Chemother. 50:4011-4017.
38. Nguyen HA, et al. 2009. Intracellular activity of antibiotics in a model of human THP-1 macrophages infected by a Staphylococcus aureus smallcolony variant strain isolated from a cystic fibrosis patient: pharmacodynamic evaluation and comparison with isogenic normal-phenotype and revertant strains. Antimicrob. Agents Chemother. 53:1434-1442.
39. Nguyen HA, et al. 2009. Intracellular activity of antibiotics in a model of human THP-1 macrophages infected by a Staphylococcus aureus smallcolony variant strain isolated from a cystic fibrosis patient: study of antibiotic combinations. Antimicrob. Agents Chemother. 53:1443-1449.
40. Proctor RA, et al. 1998. Staphylococcal small colony variants have novel mechanisms for antibiotic resistance. Clin. Infect. Dis. 27(Suppl 1):S68-S74.
41. Proctor RA, van Langevelde P, Kristjansson M, Maslow JN, Arbeit RD. 1995. Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin. Infect. Dis. 20:95-102.
42. Proctor RA, et al. 2006. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol. 4:295-305.
43. Rubino CM, et al. 2009. Oritavancin population pharmacokinetics in healthy subjects and patients with complicated skin and skin structure infections or bacteremia. Antimicrob. Agents Chemother. 53:4422-4428.
44. Sabath LD, Wallace SJ, Gerstein DA. 1972. Suppression of intrinsic resistance to methicillin and other penicillins in Staphylococcus aureus. Antimicrob. Agents Chemother. 2:350-355.
45. Sadowska B, et al. 2002. Characteristics of Staphylococcus aureus, isolated from airways of cystic fibrosis patients, and their small colony variants. FEMS Immunol. Med. Microbiol. 32:191-197.
46. Sandberg A, et al. 2011. Intra-and extracellular activities of dicloxacillin and linezolid against a clinical Staphylococcus aureus strain with a small-colony-variant phenotype in an in vitro model of THP-1 macrophages and an in vivo mouse peritonitis model. Antimicrob. Agents Chemother. 55:1443-1452.
47. Schwende H, Fitzke E, Ambs P, Dieter P. 1996. Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1,25-dihydroxyvitamin D3. J. Leukoc. Biol. 59:555-561.
48. Scorneaux B, Ouadrhiri Y, Anzalone G, Tulkens PM. 1996. Effect of recombinant human gamma interferon on intracellular activities of antibiotics against Listeria monocytogenes in the human macrophage cell line THP-1. Antimicrob. Agents Chemother. 40:1225-1230.
49. Seidl K, et al. 2011. Combinatorial phenotypic signatures distinguish persistent from resolving methicillin-resistant Staphylococcus aureus bacteremia isolates. Antimicrob. Agents Chemother. 55:575-582.
50. Sendi P, Proctor RA. 2009. Staphylococcus aureus as an intracellular pathogen: the role of small colony variants. Trends Microbiol. 17:54-58.
51. Seral C, Van Bambeke F, Tulkens PM. 2003. Quantitative analysis of gentamicin, azithromycin, telithromycin, ciprofloxacin, moxifloxacin, and oritavancin (LY333328) activities against intracellular Staphylococcus aureus in mouse J774 macrophages. Antimicrob. Agents Chemother. 47:2283-2292.
52. Stokes RW, Doxsee D. 1999. The receptor-mediated uptake, survival, replication, and drug sensitivity of Mycobacterium tuberculosis within the macrophage-like cell line THP-1: a comparison with human monocyte- derived macrophages. Cell. Immunol. 197:1-9.
53. Takemura H, et al. 2000. Evaluation of a human monocytic cell line THP-1 model for assay of the intracellular activities of antimicrobial agents against Legionella pneumophila. J. Antimicrob. Chemother. 46:589-594.
54. Trampuz A, et al. 2007. Efficacy of a novel rifamycin derivative, ABI- 0043, against Staphylococcus aureus in an experimental model of foreignbody infection. Antimicrob. Agents Chemother. 51:2540-2545.
55. Tsuchiya S, et al. 1980. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26:171-176.
56. Tuchscherr L, et al. 2011. Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol. Med. 3:129-141.
57. Tuomanen E, Cozens R, Tosch W, Zak O, Tomasz A. 1986. The rate of killing of Escherichia coli by beta-lactam antibiotics is strictly proportional to the rate of bacterial growth. J. Gen. Microbiol. 132:1297-1304.
58. Uhlemann AC, et al. 2012. Identification of a highly transmissible animal- independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. mBio 3(2):e00027-12. doi:10.1128/mBio.00027-12.
59. Van Bambeke F, Barcia-Macay M, Lemaire S, Tulkens PM. 2006. Cellular pharmacodynamics and pharmacokinetics of antibiotics: current views and perspectives. Curr. Opin. Drug Discov. Dev. 9:218-230.
60. Van Bambeke F, Mingeot-Leclercq MP, Struelens MJ, Tulkens PM. 2008. The bacterial envelope as a target for novel anti-MRSA antibiotics. Trends Pharmacol. Sci. 29:124-134.
61. Van Bambeke F, Van Laethem Y, Courvalin P, Tulkens PM. 2004. Glycopeptide antibiotics: from conventional molecules to new derivatives. Drugs 64:913-936.
62. Vaudaux P, et al. 2002. Increased expression of clumping factor and fibronectin-binding proteins by hemB mutants of Staphylococcus aureus expressing small colony variant phenotypes. Infect. Immun. 70:5428-5437.
63. Vesga O, et al. 1996. Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J. Infect. Dis. 173:739-742.
64. von Eiff C. 2008. Staphylococcus aureus small colony variants: a challenge to microbiologists and clinicians. Int. J. Antimicrob. Agents 31:507-510.
65. von Eiff C, et al. 2001. Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with Darier's disease. Clin. Infect. Dis. 32:1643-1647.
66. von Eiff C, et al. 1997. A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J. Bacteriol. 179:4706-4712.
67. Wendte JM, Ponnusamy D, Reiber D, Blair JL, Clinkenbeard KD. 2011. In vitro efficacy of antibiotics commonly used to treat human plague against intracellular Yersinia pestis. Antimicrob. Agents Chemother. 55:3752-3757.
68. Yamaguchi H, et al. 2002. A Chlamydia pneumoniae infection model using established human lymphocyte cell lines. FEMS Microbiol. Lett. 216:229-234.
69. Zhou H, et al. 2012. Genome-wide RNAi screen in IFN-gamma-treated human macrophages identifies genes mediating resistance to the intracellular pathogen Francisella tularensis. PLoS One 7:e31752. doi:10.1371/journal.pone.0031752.