Killing of Staphylococcus aureus in murine macrophages by chloroquine used alone and in combination with ciprofloxacin or azithromycin

Journal of Inflammation Research

Volumn 8, Issue , 2015, Pages 29-47

  Dey, Somrita ^a   Bishayi, Biswadev ^a  

^a UNIVERSITY OF CALCUTTA   (India)

Author keywords

Azithromycin; Ciprofloxacin; Intracellular survival

Indexed keywords

AZITHROMYCIN; CATALASE; CHLOROQUINE; CIPROFLOXACIN; CYTOKINE; SUPEROXIDE;

ANIMAL CELL; ARTICLE; BACTERICIDAL ACTIVITY; BACTERIUM IDENTIFICATION; BLOOD LEVEL; CELL ACTIVITY; CELL ASSAY; CELL LYSATE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DRUG CYTOTOXICITY; DRUG DETERMINATION; DRUG EFFICACY; ENZYME ACTIVITY; GROWTH INHIBITION; GROWTH RATE; IMMUNE RESPONSE; MALE; MONOTHERAPY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PERITONEUM MACROPHAGE; STAPHYLOCOCCUS AUREUS;

EID: 84923353948     PISSN: None     EISSN: 11787031     Source Type: Journal    
DOI: 10.2147/JIR.S76045     Document Type: Article

References (103)

1. Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339(8): 520–532.
2. Brouillette E, Grondin G, Shkreta L, Lacasse P, Talbot BG. In vivo and in vitro demonstration that Staphylococcus aureus is an intracellular pathogen in the presence or absence of fibronectin-binding proteins. Microb Pathog. 2003;35(4):159–168.
3. Gordon RJ, Lowy FD. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis. 2008;46 Suppl 5: S350–S359.
4. Carryn S, Chanteux H, Seral C, Mingeot-Leclercq MP, Van Bambeke F, Tulkens PM. Intracellular pharmacodynamics of antibiotics. Infect Dis Clin North Am. 2003;17(3):615–634.
5. van den Broek PJ. Antimicrobial drugs, microorganisms, and phagocytes. Rev Infect Dis. 1989;11(2):213–245.
6. Krut O, Sommer H, Krönke M. Antibiotic-induced persistence of cytotoxic Staphylococcus aureus in non-phagocytic cells. J Antimicrob Chemother. 2004;53(2):167–173.
7. Al-Nawas B, Shah PM. Intracellular activity of ciprofloxacin and moxifloxacin, a new 8-methoxyquinolone, against methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother. 1998;41(6): 655–658.
8. Foster TJ. Immune evasion by staphylococci. Nat Rev Microbiol. 2005; 3(12):948–958.
9. Zetola N, Francis JS, Nuermberger EL, Bishai WR. Community-acquired meticillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis. 2005;5(5):275–286.
10. Hiramatsu K. Vancomycin-resistant Staphylococcus aureus: a new model of antibiotic resistance. Lancet Infect Dis. 2001;1(3):147–155.
11. Gresham HD, Lowrance JH, Caver TE, Wilson BS, Cheung AL, Lindberg FP. Survival of Staphylococcus aureus inside neutrophils contributes to infection. J Immunol. 2000;164(7):3713–3722.
12. Hudson MC, Ramp WK, Nicholson NC, Williams AS, Nousiainen MT. Internalization of Staphylococcus aureus by cultured osteoblasts. Microb Pathog. 1995;19(6):409–419.
13. 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(1):336–342.
14. Menzies BE, Kourteva I. Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect Immun. 1998;66(12): 5994–5998.
15. Das D, Saha SS, Bishayi B. Intracellular survival of Staphylococcus aureus: correlating production of catalase and superoxide dismutase with levels of inflammatory cytokines. Inflamm Res. 2008;57(7):340–349.
16. Das D, Bishayi B. Staphylococcal catalase protects intracellularly survived bacteria by destroying H2O2 produced by the murine peritoneal macrophages. Microb Pathog. 2009;47(2):57–67.
17. Das D, Bishayi B. Contribution of Catalase and Superoxide Dismutase to the Intracellular Survival of Clinical Isolates of Staphylococcus aureus in Murine Macrophages. Indian J Microbiol. 2010;50(4):375–384.
18. Lowy FD. Is Staphylococcus aureus an intracellular pathogen? Trends Microbiol. 2000;8(8):341–343.
19. Hamza T, Li B. Differential responses of osteoblasts and mac­rophages upon Staphylococcus aureus infection. BMC Microbiol. 2014;14:207.
20. Mal P, Dutta K, Bandyopadhyay D, Basu A, Khan R, Bishayi B. Azithromycin in combination with riboflavin decreases the severity of Staphylococcus aureus infection induced septic arthritis by modulating the production of free radicals and endogenous cytokines. Inflamm Res. 2013;62(3):259–274.
21. Mal P, Dutta S, Bandyopadhyay D, Dutta K, Basu A, Bishayi B. Gentamicin in combination with ascorbic acid regulates the severity of Staphylococcus aureus infection-induced septic arthritis in mice. Scand J Immunol. 2012;76(6):528–540.
22. Mal P, Ghosh D, Bandyopadhyay D, Dutta K, Bishayi B. Ampicillin alone and in combination with riboflavin modulates Staphylococcus aureus infection induced septic arthritis in mice. Indian J Exp Biol. 2012;50(10):677–689.
23. Rogers DE, Tompsett R. The survival of staphylococci within human leukocytes. J Exp Med. 1952;95(2):209–230.
24. Underhill DM, Goodridge H. Information processing during phagocytosis. Nat Rev Immunol. 2012;12(7):492–502.
25. Pechère JC. The activity of azithromycin in animal models of infection. Eur J Clin Microbiol Infect Dis. 1991;10(10):821–827.
26. van den Broek PJ. Activity of antibiotics against microorganisms ingested by mononuclear phagocytes. Eur J Clin Microbiol Infect Dis. 1991;10(2):114–118.
27. Tulkens PM. Intracellular distribution and activity of antibiotics. Eur J Clin Microbiol Infect Dis. 1991;10(2):100–106.
28. Seral C, Barcia-Macay M, Mingeot-Leclercq MP, Tulkens PM, Van Bambeke F. Comparative activity of quinolones (ciprofloxacin, levofloxacin, moxifloxacin and garenoxacin) against extracellular and intracellular infection by Listeria monocytogenes and Staphy­lococcus aureus in J774 macrophages. J Antimicrob Chemother. 2005;55(4):511–517.
29. Nguyen HA, Grellet J, Paillard D, Dubois V, Quentin C, Saux MC. Factors influencing the intracellular activity of fluoroquinolones: a study using levofloxacin in a Staphylococcus aureus THP-1 monocyte model. J Antimicrob Chemother. 2006;57(5):883–890.
30. Hall IH, Schwab UE, Ward ES, Ives T. Disposition and intracellular levels of moxifloxacin in human THP-1 monocytes in unstimulated and stimulated conditions. Int J Antimicrob Agents. 2003;22(6):579–587.
31. Labro MT. Immunomodulatory action of antibacterial agents. Clinical Immunotherapy. 1996;6(6):454–464.
32. Labro MT. Intraphagocytic penetration of macrolide antibiotics. In: Bryskier AJ, Butzler JP, Neu HC, Tulkens PM, editors. Macrolides: Chemistry, Pharmacology and Clinical Use. Paris: Arnette Blackwell; 1993:379–388.
33. Vergne I, Constant P, Lanéelle G. Phagosomal pH determination by dual fluorescence flow cytometry. Anal Biochem. 1998;255(1):127–132.
34. Poole B, Ohkuma S. Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J Cell Biol. 1981;90(3):665–669.
35. Chakravortty D, Hensel M. Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microbes Infect. 2005;5:621–627.
36. Pollock JD, Williams DA, Gifford MA, et al. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte super­oxide production. Nat. Genet. 1995;9:202–209.
37. van Sorge NM, Beasley FC, Gusarov I, et al. Methicillin-resistant Staphylococcus aureus bacterial nitric-oxide synthase affects antibi­otic sensitivity and skin abscess development. J Biol Chem. Mar 1, 2013;288(9):6417–6426.
38. Carlier MB, Garcia-Luque I, Montenez JP, Tulkens PM, Piret J. Accumulation, release and subcellular localization of azithromycin in phagocytic and non-phagocytic cells in culture. Int J Tissue React. 1994;16(5–6):211–220.
39. Miossec-Bartoli C, Pilatre L, Peyron P, et al. The new ketolide HMR3647 accumulates in the azurophil granules of human polymorphonuclear cells. Anitmicrob Agents Chemother. 1999;43(10):2457–2462.
40. Carlier MB, Scorneaux B, Zenebergh A, Desnottes JF, Tulkens PM. Animal model pharmacokinetics and pharmacodynamics: a critical review. J Anitmicrob Agents Chemother. 1990;26 Suppl B:27–39.
41. Andes D, Craig WA. Animal model pharmacokinetics and pharmacodynamics: a critical review. Int J Antimicrob Agents. 2002; 19(4):261–268.
42. Maurin M, Raoult D. Phagolysosomal alkalinization and intracellular killing of Staphylococcus aureus by amikacin. J Infect Dis. 1994;169(2): 330–336.
43. Seral C, Van Bambeke F, Tulkens PM. Quantitative analysis of gentamicin, azithromycin, telithromycin, ciprofloxacin, moxifloxacin, and oritavancin (LY333328) activities against intracellular Staphylococcus aureus in mouse J774 macrophages. Antimicrob Agents Chemother. 2003;47(7):2283–2292.
44. Levitz SM, Nong SH, Seetoo KF, et al. Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect Immun. 1999;67(2):885–890.
45. Augustijns P, Geusens P, Verbeke N. Chloroquine levels in blood dur­ing chronic treatment of patients with rheumatoid arthritis. Eur J Clin Pharmacol. 1992;42(4):429–433.
46. Newman SL, Gootee L, Brunner G, Deepe GS Jr. Chloroquine induces human macrophage killing of Histoplasma capsulatum by limiting the availability of intracellular iron and is therapeutic in a murine model of histoplasmosis. J Clin Invest. 1994;93(4):1422–1429.
47. Picot S, Peyron F, Vuillez JP, Polack B, Ambroise-Thomas P. Chloroquine inhibits tumor necrosis factor production by human macrophages in vitro. J Infect Dis. 1991;164(4):830.
48. Yasuda H, Leelahavanichkul A, Tsunoda S, et al. Chloroquine and inhi­bition of Toll-like receptor 9 protect from sepsis-induced acute kidney injury. Am J Physiol Renal Physiol. 2008;294(5):F1050–F1058.
49. Thomé R, Moraes AS, Bombeiro AL, et al. Chloroquine treatment enhances regulatory T cells and reduces the severity of experimental autoimmune encephalomyelitis. Plos One. 2013;8(6):e65913.
50. Cooper RG, Magwere T. Chloroquine: novel uses and manifestations. Indian J Med Res. 2008;127(4):305–316.
51. Leigh PC, Van Furth R, Van Zwet TL. In vitro determination of phagocytosis and intracellular killing by polymorphonuclear and mononuclear phagocytes. In: Weir DM, editor. Handbook of Experimental Immunology. 4th ed. Oxford: Blackwell Scientific; 1986:1–46.
52. Absolom DR. Basic methods for the study of phagocytosis. Methods Enzymol. 1986;132:95–180.
53. Nandi D, Mishra MK, Basu A, Bishayi B. Protective effects of interleukin-6 in lipopolysaccharide (LPS)-induced experimental endotoxemia are linked to alteration in hepatic anti-oxidant enzymes and endogenous cytokines. Immunobiology. 2010;215(6):443–451.
54. Avci E, Akarslan ZZ, Erten H, Coskun-Cevher S. Oxidative stress and cellular immunity in patients with recurrent aphthous ulcers. Braz J Med Biol Res. 2014;47(5):355–360.
55. Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem. 1968;25(1):192–205.
56. Colowick SP, Kaplan NO, Absolom DR. Basic methods for the study of phagocytosis. In: Sabato GD, Everse J, editors. Methods in Enzymology. Vol 132, Immunochemical techniques part J: phago­cytosis and cell-mediated cytotoxicity. New York: Academic Press; 1986:160.
57. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254.
58. Bishayi B, Bandyopadhyay D, Majhi A, Adhikary R. Possible role of Toll-like receptor-2 in the intracellular survival of Staphylococcus aureus in murine peritoneal macrophages: involvement of cytok­ines and anti-oxidant enzymes. Scand J Immunol. 2014;80(2):127–143.
59. Bishayi B, Bandyopadhyay D, Majhi A, Adhikary R. Expression of CXCR1 (Interleukin-8 Receptor) in Murine Macrophages After Staphylococcus aureus Infection and its Possible Implication on Intracellular Survival Correlating with Cytokines and Bacterial Anti-Oxidant Enzymes. Inflammation. Epub August 17, 2014. Avail­able from: http://www.ncbi.nlm.nih.gov/pubmed/25129059. Accessed August 17, 2014.
60. Ignatowski TA, Bidlack JM. Differential kappa-opioid receptor expression on mouse lymphocytes at varying stages of maturation and on mouse macrophages after selective elicitation. J Pharmacol Exp Ther. 1999;290(2):863–870.
61. Polliack A, Gordon S. Scanning electron microscopy of murine macrophages. Surface characteristics during maturation, activation, and phagocytosis. Lab Invest. 1975;33(5):469–477.
62. Weber SM, Levitz SM. Chloroquine interferes with lipopolysaccharide-induced TNF-alpha gene expression by a nonlysosomotropic mechanism. J Immunol. 2000;165(3):1534–1540.
63. Ohkuma S, Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A. 1978;75(7):3327–3331.
64. Lee Hand W, Debra L Hand. Characteristics and mechanisms of azithromycin accumulation and efflux in human polymorphonu­clear leukocytes. International Journal of Antimicrobial Agents. 2001;18:419–425.
65. Hand WL, King-Thompson NL, Holman JW. Entry of roxithromycin (RU 965), imipenem, cefotaxime, trimethoprim, and metronidazole into human polymorphonuclear leukocytes. Anitmicrob Agents Chemother. 1987;31(10):1553–1557.
66. Levitz SM, Harrison TS, Tabuni A, Liu X. Chloroquine induces human mononuclear phagocytes to inhibit and kill Cryptococcus neoformans by a mechanism independent of iron deprivation. J Clin Invest. 1997;100(6):1640–1646.
67. Levitz SM1, Nong SH, Seetoo KF, Harrison TS, Speizer RA, Simons ER. Cryptococcus neoformans resides in an acidic phago­lysosome of human macrophages. Infect Immun. 1999;672(2):885–890.
68. Fox RI. Mechanism of action of hydroxychloroquine as an antirheumatic drug. Semin Arthritis Rheum. 1993;23(2 Suppl 1):82–91.
69. Geisow MJ, D’Arcy Hart P, Young MR. Temporal changes of lysosome and phagosome pH during phagolysosome formation in macrophages: studies by fluorescence spectroscopy. J Cell Biol. 1981;89(3):645–652.
70. Steinberg TH, Hand WL. Effect of phagocyte membrane stimulation on antibiotic uptake and intracellular bactericidal activity. Antimicrob Agents Chemother. 1987;31(4):660–662.
71. Leiper K, Morris AI, Rhodes JM. Open label trial of oral clarithromycin in active Crohn’s disease. Aliment Pharmacol Ther. 2000;14(6): 801–806.
72. Flanagan PK, Campbell BJ, Rhodes JM. OC-140 Hydroxychloroquine as a treatment for crohn’s disease: enhancing antibiotic efficacy and macrophage killing of E coli. Gut. 2012;61:A60–A61.
73. Oliphant CM, Green GM. Quinolones: a comprehensive review. Am Fam Physician. 2002;65(3):455–464.
74. Ilo CE, Ilondu NA, Okwoli N, et al. Effect of chloroquine on the bioavailability of ciprofloxacin in humans. Am J Ther. 2006;13(5):432–435.
75. Vrančić M, Banjanac M, Nujić K, et al. Azithromycin distinctive­lymodulates classical activation of human monocytes in vitro. Br J Pharmacol. 2012;165(5):1348–1360.
76. Munić V, Banjanac M, Koštrun S, et al. Intensity of macrolide anti-inflam­matory activity in J774A.1 cells positively correlates with cellular accu­mulation and phospholipidosis. Pharmacol Res. 2011;64(3):298–307.
77. Crosbie PA, Woodhead MA. Long-term macrolide therapy in chronic inflammatory airway diseases. Eur Respir J. 2009;33(1):171–181.
78. Anderson R, Jooné GK. In vitro investigation of the intraphagocytic bio­activities of ciprofloxacin and the new fluoroquinolone agents, clinaflox­acin (CI-960) and PD 131628. Chemotherapy. 1993;39(6):424–431.
79. Boya P, Andreau K, Poncet D, et al. Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J Exp Med. 2003;197(10):1323–1334.
80. Kazzim OJ, Adegbolagun OM, Osho O, Anumudu CI. Additive effects of ciprofloxacin on the in-vitro activity of chloroquine against a clinical isolate of Plasmodium falciparum. Ann Trop Med Parasitol. 2006;100(7):579–584.
81. Abrantes P, Dimopoulos G, Grosso AR, do Rosário VE, Silveira H. Chloroquine mediated modulation of Anopheles gambiae gene expression. PLoS One. 2008;3(7):e2587.
82. Kanoh S, Rubin BK. Mechanisms of action and clinical application of macrolides as immunomodulatory medications. Clin Microbiol Rev. 2010;23(3):590–615.
83. Murata Y, Shimamura T, Hamuro J. The polarization of T(h)1/T(h)2 balance is dependent on the intracellular thiol redox status of macrophages due to the distinctive cytokine production. Int Immunol. 2002;14(2):201–212.
84. Elia AC, Prearo M, Pacini N, Dörr AJ, Abete MC. Effects of selenium diets on growth, accumulation and antioxidant response in juvenile carp. Ecotoxicol Environ Saf. 2011;74(2):166–173.
85. Cheeseman KH, Slater TF. An introduction to free radical biochemistry. Br Med Bull. 1993;49:481–493.
86. Wolin MS, Gupte SA, Oeckler RA. Superoxide in the vascular system. J Vasc Res. 2002;39(3):191–207.
87. Muro S, Cui X, Gajewski C, Murciano JC, Muzykantov VR, Koval M. Slow intracellular trafficking of catalase nanoparticles targeted to ICAM-1 protects endothelial cells from oxidative stress. Am J Physiol Cell Physiol. 2003;285(5):C1339–C1347.
88. Iyawe HO, Onigbinde AO, Aina OO. Effect of chloroquine and ascorbic acid interaction on the oxidative stress status of Plasmodium berghei infested mice. Int J Pharmacol. 2006;2(1):1–4.
89. Sacre K, Criswell LA, McCune JM. Hydroxychloroquine is associated with impaired interferon-alpha and tumor necrosis factor-alpha production by plasmacytoid dendritic cells in systemic lupus erythematosus. Arthritis Res Ther. 2012;14(3):R155.
90. Ouyang Q, Huang Z, Wang Z, Chen X, Ni J, Lin L. Effects of pristane alone or combined with chloroquine on macrophage activation, oxidative stress, and Th1/Th2 skewness. J Immunol Res. 2014;2014(2014):Article ID 613136.
91. Jeong JY, Jue DM. Chloroquine inhibits processing of tumor necrosis factor in lipopolysaccharide-stimulated RAW 264.7 macrophages. J Immunol. 1997;158(10):4901–4907.
92. Vazifeh D, Bryskier A, Labro MT. Effect of proinflammatory cytokines on theinterplay between roxithromycin, HMR 3647, or HMR 3004 and human polymorphonuclear neutrophils. Antimicrob Agents Chemother. 2000;44(3):511–521.
93. Kollias G, Douni E, Kassiotis G, Kontoyiannis D. The function of tumour necrosis factor and receptors in models of multi-organ inflam­mation, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease. Ann Rheum Dis. 1999;58(1):132–139.
94. Schulte W, Bernhagen J, Bucala R. Cytokines in sepsis: potent immunoregulators and potential therapeutic targets–an updated view. Mediators Inflamm. 2013;2013:165974.
95. Mosser DM, Zhang X. Activation of murine macrophages. Curr Protoc Immunol. 2008;14:14.2.
96. Furst DE. Pharmacokinetics of hydroxychloroquine and chloro­quine during treatment of rheumatic diseases. Lupus. 1996;5 Suppl 1:S11–S15.
97. Nujić K, Banjanac M, Munić V, Polančec D, Eraković Haber V. Impairment of lysosomal functions by azithromycin and chloroquine contributes to anti-inflammatory phenotype. Cellular Immunol. 2012;279(1):78–86.
98. Park YC, Pae HO, Yoo JC, Choi BM, Jue DM, Chung HT. Chloroquine inhibits inducible nitric oxide synthase expression in murine peritoneal macrophages. Pharmacol Toxicol. 1999;85(4):188–191.
99. Tamaoki J, Kondo M, Kohri K, Aoshiba K, Tagaya E, Nagai A. Macrolide antibiotics protect against immune complex-induced lung injury in rats: role of nitric oxide from alveolar macrophages. J Immunol. 1999;163(5):2909–2915.
100. Rutz M, Metzger J, Gellert T, et al. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur J Immunol. 2004;34(9):2541–2550.
101. Blasius AL, Beutler B. Intracellular toll-like receptors. Immunity. 2010;32(3):305–315.
102. Kuznik A, Bencina M, Svajger U, Jeras M, Rozman B, Jerala R. Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines. J Immunol. 2011;186(8):4794–4804.
103. Wallace DJ, Gudsoorkar VS, Weisman MH, Venuturupalli SR. New insights into mechanisms of therapeutic effects of antimalarial agents in SLE. Nat Rev Rheumatol. 2012;8(9):522–533.