Macrolide antibiotics improve chemotactic and phagocytic capacity as well as reduce inflammation in sulfur mustard-exposed monocytes

Pulmonary Pharmacology and Therapeutics

Volumn 23, Issue 2, 2010, Pages 97-106

  Gao, Xiugong ^a   Ray, Radharaman ^b   Xiao, Yan ^c   Ishida, Keiko ^a   Ray, Prabhati ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b US ARMY MEDICAL RESEARCH INSTITUTE OF CHEMICAL DEFENSE   (United States)

^c NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

Author keywords

Chemotaxis; Inflammation; Macrolide antibiotic; Monocyte; Phagocytosis; Sulfur mustard

Indexed keywords

AZITHROMYCIN; CLARITHROMYCIN; ERYTHROMYCIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MACROLIDE; MUSTARD GAS; NITRIC OXIDE; ROXITHROMYCIN;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL FUNCTION; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG MECHANISM; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; INFLAMMATION; MONOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTI-BACTERIAL AGENTS; APOPTOSIS; CELL LINE; CHEMICAL WARFARE AGENTS; CHEMOTAXIS; CYTOKINES; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MACROLIDES; MONOCYTES; MUSTARD GAS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHAGOCYTOSIS;

EID: 75749143379     PISSN: 10945539     EISSN: 15229629     Source Type: Journal    
DOI: 10.1016/j.pupt.2009.10.010     Document Type: Article

References (51)

1. Szinicz L. History of chemical and biological warfare agents. Toxicology 214 (2005) 167-181
2. Kehe K., and Szinicz L. Medical aspects of sulphur mustard poisoning. Toxicology 214 (2005) 198-209
3. Amir A., Chapman S., Kadar T., Gozes Y., Sahar R., and Allon N. Sulfur mustard toxicity in macrophages: effect of dexamethasone. J Appl Toxicol 20 (2000) S51-S58
4. Ray R., Keyser B., Benton B., Daher A., Simbulan-Rosenthal C.M., and Rosenthal D.S. Sulfur mustard induces apoptosis in cultured normal human airway epithelial cells: evidence of a dominant caspase-8-mediated pathway and differential cellular responses. Drug Chem Toxicol 31 (2008) 137-148
5. Gao X., Ray R., Xiao Y., Barker P.E., and Ray P. Inhibition of sulfur mustard-induced cytotoxicity and inflammation by the macrolide antibiotic roxithromycin in human respiratory epithelial cells. BMC Cell Biol 8 (2007) 17
6. Eisenmenger W., Drasch G., von Clarmann M., Kretschmer E., and Roider G. Clinical and morphological findings on mustard gas [bis(2-chloroethyl)sulfide] poisoning. J Forensic Sci 36 (1991) 1688-1698
7. Rubin B.K. Immunomodulatory properties of macrolides: overview and historical perspective. Am J Med 117 (2004) 2S-4S
8. Xu G., Fujita J., Negayama K., Yuube K., Hojo S., Yamaji Y., et al. Effect of macrolide antibiotics on macrophage functions. Microbiol Immunol 40 (1996) 473-479
9. Yamaryo T., Oishi K., Yoshimine H., Tsuchihashi Y., Matsushima K., and Nagatake T. Fourteen-member macrolides promote the phosphatidylserine receptor-dependent phagocytosis of apoptotic neutrophils by alveolar macrophages. Antimicrob Agents Chemother 47 (2003) 48-53
10. Hodge S., Hodge G., Brozyna S., Jersmann H., Holmes M., and Reynolds P.N. Azithromycin increases phagocytosis of apoptotic bronchial epithelial cells by alveolar macrophages. Eur Respir J 28 (2006) 486-495
11. Hodge S., Hodge G., Jersmann H., Matthews G., Ahern J., Holmes M., et al. Azithromycin improves macrophage phagocytic function and expression of mannose receptor in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 178 (2008) 139-148
12. Štvrtinová V., Jakubovsky J., and Hulín I. Inflammation and fever (1995), Academic Electronic Press, Bratislava. http://nic.sav.sk/logos/books/scientific/z.html
13. Ray R., Legere R.H., Majerus B.J., and Petrali J.P. Sulfur mustard-induced increase in intracellular free calcium level and arachidonic acid release from cell membrane. Toxicol Appl Pharmacol 131 (1995) 44-52
14. Cory A.H., Owen T.C., Barltrop J.A., and Cory J.G. Use of an aqueous soluble tetrazolium/ formazan assay for cell growth assays in culture. Cancer Commun 3 (1991) 207-212
15. Xiao Y., and Barker P.E. Semiconductor nanocrystal probes for human metaphase chromosomes. Nucleic Acids Res 32 (2004) e28
16. Xiao Y., Telford W.G., Ball J.C., Locascio L.E., and Barker P.E. Semiconductor nanocrystal conjugates, FISH and pH. Nat Methods 2 (2005) 723
17. Gao X., Ray R., Xiao Y., and Ray P. Suppression of inducible nitric oxide synthase expression and nitric oxide production by macrolide antibiotics in sulfur mustard-exposed airway epithelial cells. Basic Clin Pharmacol Toxicol 103 (2008) 255-261
18. Jain R., and Danziger L.H. The macrolide antibiotics: a pharmacokinetic and pharmacodynamic overview. Curr Pharm Des 10 (2004) 3045-3053
19. Steinkamp J.A., Wilson J.S., Saunders G.C., and Stewart C.C. Phagocytosis: flow cytometric quantitation with fluorescent microspheres. Science 215 (1982) 64-66
20. Papirmeister B., Feister A.J., Robinson S.I., and Ford R.D. Medical defense against mustard gas: toxic mechanisms and pharmacological implications (1991), CRC Press, Boca Raton
21. Bosnar M., Kelnerić Z., Munić V., Eraković V., and Parnham M.J. Cellular uptake and efflux of azithromycin, erythromycin, clarithromycin, telithromycin, and cethromycin. Antimicrob Agents Chemother 49 (2005) 2372-2377
22. Knapp S., Leemans J.C., Florquin S., Branger J., Maris N.A., Pater J., et al. Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia. Am J Respir Crit Care Med 167 (2003) 171-179
23. Tamaoki J., Kadota J., and Takizawa H. Clinical implications of the immunomodulatory effects of macrolides. Am J Med 117 (2004) 5S-11S
24. Liles W.C., and Van Voorhis W.C. Review: nomenclature and biologic significance of cytokines involved in inflammation and the host immune response. J Infect Dis 172 (1995) 1573-1580
25. Emad A., and Emad Y. Levels of cytokine in bronchoalveolar lavage (BAL) fluid in patients with pulmonary fibrosis due to sulfur mustard gas inhalation. J Interferon Cytokine Res 27 (2007) 38-43
26. Emad A., and Emad Y. CD4/CD8 ratio and cytokine levels of the BAL fluid in patients with bronchiectasis caused by sulfur mustard gas inhalation. J Inflamm (Lond) 4 (2007) 2
27. Sabourin C.L., Danne M.M., Buxton K.L., Casillas R.P., and Schlager J.J. Cytokine, chemokine, and matrix metalloproteinase response after sulfur mustard injury to weanling pig skin. J Biochem Mol Toxicol 16 (2002) 263-272
28. Ricketts K.M., Santai C.T., France J.A., Graziosi A.M., Doyel T.D., Gazaway M.Y., et al. Inflammatory cytokine response in sulfur mustard-exposed mouse skin. J Appl Toxicol 20 (2000) S73-S76
29. Sabourin C.L., Petrali J.P., and Casillas R.P. Alterations in inflammatory cytokine gene expression in sulfur mustard-exposed mouse skin. J Biochem Mol Toxicol 14 (2000) 291-302
30. Dillman III J.F., McGary K.L., and Schlager J.J. An inhibitor of p38 MAP kinase downregulates cytokine release induced by sulfur mustard exposure in human epidermal keratinocytes. Toxicol In Vitro 18 (2004) 593-599
31. Arroyo C.M., Schafer R.J., Kurt E.M., Broomfield C.A., and Carmichael A.J. Response of normal human keratinocytes to sulfur mustard: cytokine release. J Appl Toxicol 20 (2000) S63-S72
32. Arroyo C.M., Schafer R.J., Kurt E.M., Broomfield C.A., and Carmichael A.J. Response of normal human keratinocytes to sulfur mustard (HD): cytokine release using a non-enzymatic detachment procedure. Hum Exp Toxicol 18 (1999) 1-11
33. Ignarro L.J. Biosynthesis and metabolism of endothelium derived nitric oxide. Annu Rev Pharmacol Toxicol 30 (1990) 535-560
34. Moncada S., Palmer R.M., and Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43 (1991) 109-142
35. Luo J.D., and Chen A.F. Nitric oxide: a newly discovered function on wound healing. Acta Pharmacol Sin 26 (2005) 259-264
36. Grisham M.B., Granger D.N., and Lefer D.J. Modulation of leukocyte-endothelial interactions by reactive metabolites of oxygen and nitrogen: relevance to ischemic heart disease. Free Radic Biol Med 25 (1998) 404-433
37. Hierholzer C., Harbrecht B., Menezes J.M., Kane J., MacMicking J., Nathan C.F., et al. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J Exp Med 187 (1998) 917-928
38. Loscalzo J., and Welch G. Nitric oxide and its role in the cardiovascular system. Prog Cardiovasc Dis 38 (1995) 87-104
39. Nathan C. Inducible nitric oxide synthase: what difference does it make?. J Clin Invest 100 (1997) 2417-2423
40. Palombella V.J., Conner E.M., Fuseler J.W., Destree A., Davis J.M., Laroux F.S., et al. Role of the proteasome and NF-kappaB in streptococcal cell wall-induced polyarthritis. Proc Natl Acad Sci U S A 95 (1998) 15671-15676
41. Gaston B., Drazen J.M., Loscalzo J., and Stamler J.S. The biology of nitrogen oxides in the airways. Am J Respir Crit Care Med 149 (1994) 538-551
42. Stamler J.S., Singel D.J., and Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science 258 (1992) 1898-1902
43. Kooy N.W., Royall J.A., Ye Y.Z., Kelly D.R., and Beckman J.S. Evidence for in vivo peroxynitrite production in human acute lung injury. Am J Respir Crit Care Med 151 (1995) 1250-1254
44. Maziak W., Loukides S., Culpitt S., Sullivan P., Kharitonov S.A., and Barnes P.J. Exhaled nitric oxide in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 157 (1998) 998-1002
45. Kharitonov S.A., Wells A.U., O'Connor B.J., Cole P.J., Hansell D.M., Logan-Sinclair R.B., et al. Elevated levels of exhaled nitric oxide in bronchiectasis. Am J Respir Crit Care Med 151 (1995) 1889-1893
46. Tsai W.C., and Standiford T.J. Immunomodulatory effects of macrolides in the lung: lessons from in-vitro and in-vivo models. Curr Pharm Des 10 (2004) 3081-3093
47. Kohri K., Tamaoki J., Kondo M., Aoshiba K., Tagaya E., and Nagai A. Macrolide antibiotics inhibit nitric oxide generation by rat pulmonary alveolar macrophages. Eur Respir J 15 (2000) 62-67
48. Yang C.M., Hsieh H.L., and Lee C.W. Intracellular signaling mechanisms underlying the expression of pro-inflammatory mediators in airway diseases. Chang Gung Med J 28 (2005) 813-823
49. Ichiyama T., Nishikawa M., Yoshitomi T., Hasegawa S., Matsubara T., Hayashi T., et al. Clarithromycin inhibits NF-kappaB activation in human peripheral blood mononuclear cells and pulmonary epithelial cells. Antimicrob Agents Chemother 45 (2001) 44-47
50. Ianaro A., Ialenti A., Maffia P., Sautebin L., Rombolà L., Carnuccio R., et al. Anti-inflammatory activity of macrolide antibiotics. J Pharmacol Exp Ther 292 (2000) 156-163
51. Straughan D.W., Fentem J.H., and Balls M. Replacement alternative and complementary in vitro methods in pharmaceutical research. In: Castell J.V., and Gómez-Lechón M.J. (Eds). In vitro methods in pharmaceutical research (1997), Academic Press 5-6