Anti-inflammatory effects of tobramycin and a copper-tobramycin complex with superoxide dismutase-like activity

British Journal of Pharmacology

Volumn 168, Issue 5, 2013, Pages 1165-1181

  Gziut, M ^a   MacGregor, H ^a   Nevell, T ^a   Mason, T ^a   Laight, D ^a   Shute, J K ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

aminoglycoside antibiotic; anti inflammatory therapy; copper chelation; endothelium; IL 8; neutrophil; neutrophil elastase; platelet; reactive oxygen species (ROS); T cell

Indexed keywords

ALPHA 1 ANTITRYPSIN; COPPER COMPLEX; DICHLORODIHYDROFLUORESCEIN DIACETATE; HEPARAN SULFATE; HYDROGEN PEROXIDE; LEUKOCYTE ELASTASE; PENICILLAMINE; RANTES; SUPEROXIDE; SUPEROXIDE DISMUTASE; THROMBIN; TOBRAMYCIN; TOBRAMYCIN COPPER COMPLEX; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; LEUKOCYTE ACTIVATION; LUNG ENDOTHELIUM; LYMPHOCYTE MIGRATION; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; THROMBOCYTE ACTIVATION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

ANTI-INFLAMMATORY AGENTS; BLOOD PLATELETS; CATALASE; CELL LINE; CELLS, CULTURED; CHEMOKINE CCL5; COPPER; ENDOTHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; LEUKOCYTE ELASTASE; NEUTROPHILS; SUPEROXIDE DISMUTASE; SUPEROXIDES; T-LYMPHOCYTES; TOBRAMYCIN; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84874263897     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12018     Document Type: Article

References (60)

1. Alcock NW, (1987). A hydrogen peroxide digestion system for tissue trace metal analysis. Biol Trace Elem Res 13: 363-370.
2. Baltus T, von Hundelshausen P, Mause SF, Buhre W, Rossaint R, Weber C, (2008). Differential and additive effects of platelet-derived chemokines on monocyte arrest on inflamed endothelium under flow conditions. J Leuk Biol 78: 435-441.
3. Bar-Or D, Thomas GW, Yuki RL, Rael LT, Shimonkevitz RP, Curtis CG, et al. (2003). Copper stimulates the synthesis and release of interleukin-8 in human endothelial cells: a possible early role in systemic inflammatory responses. Shock 20: 154-158.
4. Boueiz A, Hassoun PM, (2009). Regulation of endothelial barrier function by reactive oxygen and nitrogen species. Microvasc Res 77: 26-34.
5. Brewer GJ, (2008). The risks of free copper in the body and the development of useful anticopper drugs. Curr Opin Clin Nutr Metab Care 11: 727-732.
6. Camakaris J, Voskoboinik I, Mercer JF, (1999). Molecular mechanisms of copper homeostasis. Biochem Biophys Res Commun 261: 225-232.
7. Campbell EJ, Owen CA, (2007). The sulfate groups of chondrotin sulfate and heparan sulfate-containing proteoglycans in neutrophil plasma membranes are novel binding sites for human leukocyte elastase and cathepsin G. J Biol Chem 282: 14645-14654.
8. Cantin A, Woods DE, (1993). Protection by antibiotics against myeloperoxidase-dependent cytotoxicity to lung epithelial cells in vitro. J Clin Invest 91: 38-45.
9. Cook-Mills JM, (2006). Hydrogen peroxide activation of endothelial cell-associated MMPs during VCAM-1-dependent leukocyte migration. Cell Mol Biol (Noisy-Le-Grand) 52: 8-16.
10. Doring G, (2010). Prevention of Pseudomonas aeruginosa infection in cystic fibrosis patients. Int J Med Microbiol 300: 573-577.
11. Elizur A, Cannon C, Ferkol TW, (2008). Airway inflammation in cystic fibrosis. Chest 133: 489-495.
12. Elson-Schwab L, Garner OB, Schuksz M. Crawford BE, Esko JD, Tor Y, (2007). Guanindinylated neomycin delivers large, bioactive cargo into cells through a heparan sulfate-dependent pathway. J Biol Chem 282: 13585-13591.
13. Ewing JF, Janero DR, (1995). Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal Biochem 232: 243-248.
14. Freitas M, Lima JLFC, Fernandes E, (2009). Optical probes for detection and quantification of neutrophils oxidative burst. A review. Anal Chim Acta 649: 8-23.
15. Geller DE, Pitlick WH, Nardella PA, Tracewell WG, Ramsey BW, (2002). Pharmacokinetics and bioavailability of aerosolised tobramycin in cystic fibrosis. Chest 122: 219-226.
16. Gokhale N, Patwardhan A, Cowan JA, (2007). Metalloaminoglycosides: chemistry and biological relevance. In:, Arya DP, (ed.). Aminoglycoside Antibiotics: From Chemical Biology to Drug Discovery. John Wiley and Sons: Hoboken, NJ, pp. 235-254.
17. Gray RD, Duncan A, Noble D, Imrie M, O'Reilly DSJ, Innes JA, et al. (2010). Sputum trace metals are biomarkers of inflammatory and suppurative lung disease. Chest 137: 635-641.
18. Hattori H, Subramanian KK, Sakai J, Jia Y, Li Y, Porter TF, et al. (2010). Small-molecule screen identifies reactive oxygen species as key regulators of neutrophil chemotaxis. Proc Natl Acad Sci U S A 107: 3546-3551.
19. Hu G-F, (1998). Copper stimulates proliferation of human endothelial cells under culture. J Cell Biochem 69: 326-335.
20. Hubeau C, Lorenzato M, Couetil JP, Hubert D, Dusser D, Puchelle E, et al. (2001). Quantitative anaysis of inflammatory cells infiltrating the cystic fibrosis airway mucosa. Clin Exp Immunol 124: 69-76.
21. Huber AR, Weiss SJ, (1989). Disruption of the subendothelial basement membrane during neutrophil diapedesis in an in vitro construct of a blood vessel wall. J Clin Invest 83: 1122-1136.
22. von Hundelhausen CW, (2007). Platelets as immune cells bridging inflammation and cardiovascular disease. Circ Res 100: 27-40.
23. Jezowska-Bojczuk M, Karaczyn A, Kozlowski H, (1998). Copper (II) binding to tobramycin: potentiometric and spectroscopic studies. Carbohydr Res 313: 265-269.
24. Kameyoshi Y, Dorschner A, Mallet AI, Christophers E, Schroder J-M, (1992). Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human eosinophils. J Exp Med 176: 587-592.
25. Kawai T, Seki M, Hiromatsu K, Eastcott JW, Watts GFM, Sugai M, et al. (1999). Selective diapedesis of Th1 cells induced by endothelial cell RANTES. J Immunol 163: 3269-3278.
26. 2+ interactions with peptides and aminoglycosides. Coord Chem Rev 249: 2323-2334.
27. Laurila JP, Laatikainen LE, Castellone MD, Laukkanen MO, (2009). SOD3 reduces inflammatory cell migration by regulating adhesion molecule and cytokine expression. PLoS ONE 4: e5786.
28. Lengfelder E, Fuchs C, Younes M, Weser U, (1979). Functional aspects of the superoxide dismutative action of Cu-penicillamine. Biochim Biophys Acta 567: 492-502.
29. Liochev SI, Fridovich I, (2007). The effects of superoxide dismutase on H2O2 formation. Free Rad Biol Med 42: 1465-1469.
30. Loetscher P, Seitz M, Baggiolini M, Moser B, (1996). Interleukin-2 regulates CC chemokine receptor expression and chemotactic responsiveness in T lymphocytes. J Exp Med 184: 569-577.
31. MacGregor HJ, Kato Y, Marshall LJ, Nevell TG, Shute JK, (2011). A copper-hydrogen peroxide redox system induces dityrosine cross-links and chemokine oligomerisation. Cytokine 56: 669-675.
32. Mattoscio D, Evangelista V, De Cristofaro R, Recchiuti A, Pandolfi A, Di Silvetsre S, et al. (2010). Cystic fibrosis transmembrane conductance regulator (CFTR) expression in human platelets: impact on mediators and mechanisms of the inflammatory response. FASEB J 24: 3970-3980.
33. Milanino R, Buchner V, (2006). Copper: role of the 'endogenous' and 'exogenous' metal on the development and control of inflammatory processes. Rev Environ Health 21: 153-214.
34. Mizuguchi S, Stephen J, Bihari R, Markovic N, Suehiro S, Capretta A, et al. (2009). CORM-3-derived CO modulates polymorphonuclear leukocyte migration across the vascular endothelium by reducing levels of cell surface-bound elastase. Am J Physiol Heart Circ Physiol 297: H920-H929.
35. Muller WA, (2011). Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol Mech Dis 6: 323-344.
36. Muscoli C, Cuzzocrea S, Riley DP, Zweier JL, Thiemermann C, Wang Z-Q SD, (2003). On the selectivity of superoxide dismutase mimetics and its importance in pharmacological studies. Br J Pharmacol 140: 445-460.
37. Nakagawara A, Nathan CF, Cohn ZA, (1981). Hydrogen peroxide metabolism in human monocytes during differentiation in vitro. J Clin Invest 68: 1243-1252.
38. Nakamura S, Yanagihara K, Araki N, Yamada K, Morinaga Y, Izumikawa K, et al. (2011). High-dose tobramycin inhibits lipopolysaccharide-induced MUC5AC production in human lung epithelial cells. Eur J Pharmacol 659: 67-71.
39. O'Sullivan BP, Michelson AD, (2006). The inflammatory role of platelets in cystic fibrosis. Am J Respir Crit Care Med 173: 483-490.
40. Paakko P, Kirby M, do Bois RM, Gillissen A, Ferrans VJ, Crystal RG, (1996). Activated neutrophils secrete stored α1-antitrypsin. Am J Respir Crit Care Med 154: 1829-1833.
41. Percival SS, Kauwell GPA, Bowser E, Wagner M, (1999). Altered copper status in adult men with cystic fibrosis. J Am Coll Nutr 18: 614-619.
42. Persichini T, Percario Z, Mazzon E, Colasanti M, Cuzzocrea S, Musci G, (2006). Copper activates the NF-κB pathway in vivo. Antioxid Redox Signal 8: 1897-1904.
43. Petreccia DC, Nauseef WM, Clark RA, (1987). Respiratory burst of normal human eosinophils. J Leuk Biol 41: 283-288.
44. Pitchford SC, (2007). Novel uses for anti-platelet agents as anti-inflammatory drugs. Br J Pharmacol 152: 987-1002.
45. Pitchford SC, Momi S, Baglioni S, Casali L, Giannini S, Rossi R, et al. (2008). Allergen induces the migration of platelets to lung tissue in allergic asthma. Am J Respir Crit Care Med 177: 604-612.
46. Proudfoot AEI, Handel TM, Johnson Z, Lau EK, LiWang P, Clark-Lewis I, et al. (2002). Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci U S A 100: 1885-1890.
47. Ramsey BW, Pepe MS, Quan JM, Otto KL, Montgomery AB, Williams-Warren J, et al. (1999). Intermittent administration of inhaled tobramycin in patients with cystic fibrosis. N Engl J Med 340: 23-30.
48. Ratjen F, Brockhaus F, Angyalosi G, (2009). Aminoglycoside therapy against Pseudomonas aeruginosa in cystic fibrosis: a review. J Cyst Fibros 8: 361-369.
49. Romagni S, (1994). Lymphokine production by human T cells in disease states. Annu Rev Immunol 12: 227-257.
50. Rottner M, Freyssinet J-M, Martinez MC, (2009). Mechanisms of the noxious inflammatory cycle in cystic fibrosis. Respir Res 10: 23.
51. Rottner M, Tual-Chalot S, Mostefai HA, Andriantsitohaina R, Freyssinet J-M, Martinez MC, (2011). Increased oxidative stress induces apoptosis in human cystic fibrosis cells. PLoS ONE 6: e24880.
52. Rowe RG, Weiss SJ, (2008). Breaching the basement membrane: who, when and how? Trends Cell Biol 18: 560-574.
53. Sallusto F, Lanzavecchia A, Mackay CR, (1998). Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunol Today 18: 568-574.
54. Schmitt Y, (1997). Copper and zinc determination in plasma and corpuscular components of peripheral blood of patients with preterminal and terminal renal failure. J Trace Elements Med Biol 11: 210-214.
55. Solic N, Wilson J, Wilson SJ, Shute JK, (2005). Endothelial activation and increased heparan sulphate expression in cystic fibrosis. Am J Respir Crit Care Med 172: 892-898.
56. Spisni E, Valerii MC, Manerba M, Strillacci A, Polazzi E, Mattia T, et al. (2009). Effect of copper on extracellular levels of ket pro-inflammatory molecules in hypothalamic GN11 and primary neurons. Neurotoxicology 30: 605-612.
57. Sreedhara A, Freed JD, Cowan JA, (2000). Efficient inorganic deoxyribonucleases. Greater than 50-million-fold rate enhancement in enzyme-like DNA cleavage. J Am Chem Soc 122: 8814-8824.
58. Tapeiro H, Townsend DM, Tew KD, (2003). Trace elements in human physiology and pathology. Copper Biomed Pharmacother 57: 386-398.
59. Weder JE, Dillon CT, Hambley TW, Kennedy BJ, Lay PA, Biffin JR, et al. (2002). Copper complexes of non-steroidal anti-inflammatory drugs: an opportunity yet to be realized. Coord Chem Rev 232: 95-126.
60. Witko-Sarsat V, Descamps-Latscha B, (1994). Neutrophil derived oxidants and proteinases as immunomodulatory mediators in inflammation. Mediators Inflamm 3: 257-273.