Influence of the protein kinase C activator phorbol myristate acetate on the intracellular activity of antibiotics against hemin- and menadione-auxotrophic small-colony variant mutants of Staphylococcus aureus and their wild-type parental strain in human THP-1 cells

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 12, 2012, Pages 6166-6174

  Garcia, Laetitia G ^a   Lemaire, Sandrine ^a   Kahl, Barbara C ^b   Becker, Karsten ^b   Proctor, Richard A ^c   Tulkens, Paul M ^a   Van Bambekea, Franco̧ise ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; GENTAMICIN; HEMIN; HYDROGEN PEROXIDE; MENADIONE; MOXIFLOXACIN; ORITAVANCIN; OXYTETRACYCLINE; PHORBOL 13 ACETATE 12 MYRISTATE;

ANTIBACTERIAL ACTIVITY; ARTICLE; AUXOTROPHIC MUTANT; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM COLONY; BACTERIUM MUTANT; CELL COUNT; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG POTENCY; HUMAN; HUMAN CELL; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS;

ACETYLCYSTEINE; ANTI-BACTERIAL AGENTS; CELL DIFFERENTIATION; CELL LINE; DRUG RESISTANCE, BACTERIAL; ENZYME ACTIVATORS; GENTAMICINS; HEMIN; HUMANS; HYDROGEN PEROXIDE; MICROBIAL SENSITIVITY TESTS; MONOCYTES; MUTATION; PHAGOCYTOSIS; PROTEIN KINASE C; STAPHYLOCOCCUS AUREUS; TETRADECANOYLPHORBOL ACETATE; VITAMIN K 3;

EID: 84869232768     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01031-12     Document Type: Article

References (55)

1. Allegra L, et al. 2002. Human neutrophil oxidative bursts and their in vitro modulation by different N-acetylcysteine concentrations. Arzneimittelforschung 52:669-676.
2. Ambrose PG, Drusano GL, Craig WA. 2012. In vivo activity of oritavancin in animal infection models and rationale for a new dosing regimen in humans. Clin. Infect. Dis. 54(Suppl 3):S220-S228.
3. Andes D, Craig WA. 2002. Pharmacodynamics of the new fluoroquinolone gatifloxacin in murine thigh and lung infection models. Antimicrob. Agents Chemother. 46:1665-1670.
4. Arhin FF, Sarmiento I, Parr TR, Jr, Moeck G. 2012. Activity of oritavancin and comparators in vitro against standard and high inocula of Staphylococcus aureus. Int. J. Antimicrob. Agents 39:159-162.
5. Baquir B, et al. 2012. Macrophage killing of bacterial and fungal pathogens is not inhibited by intense intracellular accumulation of the lipoglycopeptide antibiotic oritavancin. Clin. Infect. Dis. 54:S230-S232.
6. 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.
7. 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.
8. Baumert N, et al. 2002. Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb. Drug Resist. 8:253-260.
9. Belley A, et al. 2010. Oritavancin disrupts membrane integrity of Staphylococcus aureus and vancomycin-resistant enterococci to effect rapid bacterial killing. Antimicrob. Agents Chemother. 54:5369-5371.
10. Belley A, et al. 2009. Oritavancin kills stationary-phase and biofilm Staphylococcus aureus cells in vitro. Antimicrob. Agents Chemother. 53:918-925.
11. Bergstrand H, et al. 1986. Stimuli-induced superoxide radical generation in vitro by human alveolar macrophages from smokers: modulation by N-acetylcysteine treatment in vivo. J. Free Radic. Biol. Med. 2:119-127.
12. Clinical and Laboratory Standards Institute. 2011. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. M7-A9, 9th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
13. Clinical and Laboratory Standards Institute. 2012. Performance standards for antimicrobial susceptibility testing. Twenty-second informational supplement. MS100-S22. Clinical and Laboratory Standards Institute, Wayne, PA.
14. Daigneault M, Preston JA, Marriott HM, Whyte MK, Dockrell DH. 2010. The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5:e8668. doi:10.1371/journal. pone.0008668.
15. Dwyer DJ, Kohanski MA, Collins JJ. 2009. Role of reactive oxygen species in antibiotic action and resistance. Curr. Opin. Microbiol. 12:482-489.
16. Eng RH, Padberg FT, Smith SM, Tan EN, Cherubin CE. 1991. Bactericidal effects of antibiotics on slowly growing and nongrowing bacteria. Antimicrob. Agents Chemother. 35:1824-1828.
17. Fang FC. 2011. Antimicrobial actions of reactive oxygen species. mBio 2(5):e00141-11. doi:10.1128/mBio.00141-11.
18. Fantin B, Ebert S, Leggett J, Vogelman B, Craig WA. 1991. Factors affecting duration of in-vivo postantibiotic effect for aminoglycosides against gram-negative bacilli. J. Antimicrob. Chemother. 27:829-836.
19. Faull RJ, Kovach NL, Harlan JM, Ginsberg MH. 1994. Stimulation of integrin-mediated adhesion of T lymphocytes and monocytes: two mechanisms with divergent biological consequences. J. Exp. Med. 179:1307-1316.
20. Garcia LG, et al. 2012. 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. Antimicrob. Agents Chemother. 56:3700-3711.
21. Hall IH, Schwab UE, Ward ES, Ives TJ. 2003. Effects of moxifloxacin in zymogen A or S. aureus stimulated human THP-1 monocytes on the inflammatory process and the spread of infection. Life Sci. 73:2675-2685.
22. Hampton MB, Kettle AJ, Winterbourn CC. 1996. Involvement of superoxide and myeloperoxidase in oxygen-dependent killing of Staphylococcus aureus by neutrophils. Infect. Immun. 64:3512-3517.
23. Hauck CR, Ohlsen K. 2006. Sticky connections: extracellular matrix protein recognition and integrin-mediated cellular invasion by Staphylococcus aureus. Curr. Opin. Microbiol. 9:5-11.
24. Hoffmann C, Ohlsen K, Hauck CR. 2011. Integrin-mediated uptake of fibronectin-binding bacteria. Eur. J. Cell Biol. 90:891-896.
25. 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.
26. 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.
27. Khan A, Sarkar S, Sarkar D. 2008. Bactericidal activity of 2-nitroimidazole against the active replicating stage of Mycobacterium bovis BCG and Mycobacterium tuberculosis with intracellular efficacy in THP-1 macrophages. Int. J. Antimicrob. Agents 32:40-45.
28. Kohanski MA, Dwyer DJ, Collins JJ. 2010. How antibiotics kill bacteria: from targets to networks. Nat. Rev. Microbiol. 8:423-435.
29. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797-810.
30. 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.
31. Lee SY, Fan HW, Sutherland C, DeRyke AC, Nicolau DP. 2007. Antibacterial effects of moxifloxacin and levofloxacin simulating epithelial lining fluid concentrations against community-acquired methicillin-resistant Staphylococcus aureus. Drugs R. D. 8:69-77.
32. Lemaire S, et al. 2010. Influence of oritavancin on phagocytosis, generation of reactive oxygen species and killing of intracellular S. aureus in murine and human macrophages and comparison with azithromycin and vancomycin, poster A1-1360. Abstr. 50th Intersci. Conf. Antimicrob. Agents Chemother., Boston, MA. American Society for Microbiology, Washington, DC.
33. 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.
34. 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.
35. Nguyen HA, et al. 2009. Intracellular activity of antibiotics in a model of human THP-1 macrophages infected by a Staphylococcus aureus small-colony variant strain isolated from a cystic fibrosis patient: pharmacodynamic evaluation and comparison with isogenic normalphenotype and revertant strains. Antimicrob. Agents Chemother. 53:1434-1442.
36. Nguyen HA, Grellet J, Dubois V, Saux MC, Quentin C. 2007. Factors compromising the activity of moxifloxacin against intracellular Staphylococcus aureus. J. Antimicrob. Chemother. 59:755-758.
37. Olivier AC, Lemaire S, Van Bambeke F, Tulkens PM, Oldfield E. 2009. Role of rsbU and staphyloxanthin in phagocytosis and intracellular growth of Staphylococcus aureus in human macrophages and endothelial cells. J. Infect. Dis. 200:1367-1370.
38. Ouadrhiri Y, Scorneaux B, Sibille Y, Tulkens PM. 1999. Mechanism of the intracellular killing and modulation of antibiotic susceptibility of Listeria monocytogenes in THP-1 macrophages activated by gamma interferon. Antimicrob. Agents Chemother. 43:1242-1251.
39. Paillard D, Grellet J, Dubois V, Saux MC, Quentin C. 2002. Discrepancy between uptake and intracellular activity of moxifloxacin in a Staphylococcus aureus-human THP-1 monocytic cell model. Antimicrob. Agents Chemother. 46:288-293.
40. 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.
41. 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.
42. Sachse F, Becker K, von Eiff C, Metze D, Rudack C. 2010. Staphylococcus aureus invades the epithelium in nasal polyposis and induces IL-6 in nasal epithelial cells in vitro. Allergy 65:1430-1437.
43. 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.
44. Sinha B, et al. 1999. Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell. Microbiol. 1:101-117.
45. 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.
46. 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.
47. Tsuchiya S, et al. 1980. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26:171-176.
48. 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.
49. Vergison A, et al. 2007. National survey of molecular epidemiology of Staphylococcus aureus colonization in Belgian cystic fibrosis patients. J. Antimicrob. Chemother. 59:893-899.
50. Villagrasa V, et al. 1997. Inhibitory effects of N-acetylcysteine on super-oxide anion generation in human polymorphonuclear leukocytes. J. Pharm. Pharmacol. 49:525-529.
51. 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.
52. 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.
53. von Eiff C, et al. 2006. Phenotype microarray profiling of Staphylococcus aureus menD and hemB mutants with the small-colony-variant phenotype. J. Bacteriol. 188:687-693.
54. Yagci S, Hascelik G, Dogru D, Ozcelik U, Sener B. 28 November 2011. Prevalence and genetic diversity of Staphylococcus aureus small-colony variants in cystic fibrosis patients. Clin. Microbiol. Infect. [Epub ahead of print.] doi:10.1111/j.1469-0691.2011.03742.x.
55. Zhou L, et al. 2010. Retinoid X receptor agonists inhibit phorbol-12-myristate-13-acetate (PMA)-induced differentiation of monocytic THP-1 cells into macrophages. Mol. Cell. Biochem. 335:283-289.