Azithromycin reduces Chlamydia pneumoniae-induced attenuation of eNOS and cGMP production by endothelial cells

European Journal of Clinical Investigation

Volumn 35, Issue 9, 2005, Pages 573-582

  Bouwman, John J M ^a   Visseren, F L J ^b   Bevers, L M ^b   Van Der Vlist, W E ^a   Bouter, K P ^c   Diepersloot, R J A ^a  

^a DEPARTMENT OF SURGERY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c JEROEN BOSCH HOSPITAL   (Netherlands)

Author keywords

Chlamydia pneumoniae; Cyclic guanosine monophosphate; Cytomegalovirus; Endothelial dysfunction; Endothelial nitric oxide synthase; Reactive oxygen species

Indexed keywords

AZITHROMYCIN; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL CULTURE; CHLAMYDOPHILA PNEUMONIAE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOTOXICITY; DOSE RESPONSE; DRUG ACCUMULATION; DRUG ACTIVITY; ENDOTHELIUM CELL; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; IMMUNOASSAY; MINIMUM INHIBITORY CONCENTRATION; PRIORITY JOURNAL; STATISTICAL ANALYSIS; UMBILICAL VEIN;

ANTI-BACTERIAL AGENTS; AZITHROMYCIN; CELL SURVIVAL; CELLS, CULTURED; CHLAMYDOPHILA INFECTIONS; CHLAMYDOPHILA PNEUMONIAE; CYCLIC GMP; CYTOMEGALOVIRUS INFECTIONS; ENDOTHELIAL CELLS; HUMANS; NITRIC OXIDE SYNTHASE TYPE III; REACTIVE OXYGEN SPECIES;

EID: 24144454632     PISSN: 00142972     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2362.2005.01541.x     Document Type: Article

References (66)

1. Blum A, Peleg A, Weinberg M. Anti-cytomegalovirus (CMV) IgG antibody titer in patients with risk factors to atherosclerosis. Clin Exp Med 2003;3 (3):157-60.
2. Campbell LA, Kuo CC. Chlamydia pneumoniae and atherosclerosis. Semin Respir Infect 2003;18 (1):48-54.
3. Kalayoglu MV, Libby P, Byrne GI. Chlamydia pneumoniae as an emerging risk factor in cardiovascular disease. JAMA 2002;288 (21):2724-31.
4. Muhlestein JB, Anderson JL. Chronic infection and coronary artery disease. Cardio Clin 2003;21 (3):333-62.
5. Becker AE, de Boer OJ, van der Wal AC. The role of inflammation and infection in coronary artery disease. Ann Rev Med 2001;52:289-97.
6. Saikku P, Leinonen M, Mattila K, Ekman MR, Nieminen MS, Makela PH et al. Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction. Lancet 1988;2 (8618):983-6.
7. Kuo CC, Shor A, Campbell LA, Fukushi H, Patton DL, Grayston JT. Demonstration of Chlamydia pneumoniae in atherosclerotic lesions of coronary arteries. J Infect Dis 1993;4:841-9.
8. Muhlestein JB, Hammond EH, Carlquist JF, Radicke E, Thomson MJ, Karagounis LA et al. Increased incidence of Chlamydia species within the coronary arteries of patients with symptomatic atherosclerotic versus other forms of cardiovascular disease. J Am Coll Cardiol 1996;7:1555-61.
9. Jackson LA, Campbell LA, Kuo CC, Rodriguez DI, Lee A, Grayston JT. Isolation of Chlamydia pneumoniae from a carotid endarterectomy specimen. J Infec Dis 1997;176 (1):292-5.
10. Ramirez JA. Isolation of Chlamydia pneumoniae from the coronary artery of a patient with coronary atherosclerosis. The Chlamydia pneumoniae/ Atherosclerosis Study Group. Ann Intern Med 1996;125 (12):979-82.
11. Boman J, Hammerschlag MR. Chlamydia pneumoniae and atherosclerosis: critical assessment of diagnostic methods and relevance to treatment studies. Clin Microbiol Rev 2002;15 (1):1-20.
12. Dowell SF, Peeling RW, Boman J, Carlone GM, Fields BS, Guarner J et al. Standardizing Chlamydia pneumoniae assays: recommendations from the Centers for Disease Control and Prevention (USA) and the Laboratory Centre for Disease Control (Canada). Clin Infect Dis 2001;33 (4):492-503. Epub.
13. Ieven MM, Hoymans VY. Involvement of Chlamydia pneumoniae in atherosclerosis: more evidence for lack of evidence. J Clin Microbiol 2005;43 (1):19-24.
14. Adam E, Melnick JL, Probtsfield JL, Petrie BL, Burek J, Bailey KR et al. High levels of cytomegalovirus antibody in patients requiring vascular surgery for atherosclerosis. Lancet 1987;2 (8554):291-3.
15. Blum A, Giladi M, Weinberg M, Kaplan G, Pasternack H, Laniado S et al. High anti-cytomegalovirus (CMV) IgG antibody titer is associated with coronary artery disease and may predict post-coronary balloon angioplasty restenosis. Am J Cardiol 1998;81 (7):866-8.
16. Nieto FJ, Adam E, Sorlie P, Farzadegan H, Melnick JL, Comstock GW et al. Cohort study of cytomegalovirus infection as a risk factor for carotid intimal-medial thickening, a measure of subclinical atherosclerosis. Circulation 1996;94 (5):922-7.
17. Grahame-Clarke C, Chan NN, Andrew D, Ridgway GL, Betteridge DJ, Emery V et al. Human cytomegalovirus seropositivity is associated with impaired vascular function. Circulation 2003;108 (6):678-83. Epub. 2003.
18. Melnick JL, Hu C, Burek J, Adam E, DeBakey ME. Cytomegalovirus DNA in arterial walls of patients with atherosclerosis. J Med Virol 1994;42 (2):170-4.
19. Muhlestein JB, Horne BD, Carlquist JF, Madsen TE, Bair TL, Pearson RR et al. Cytomegalovirus seropositivity and C-reactive protein have independent and combined predictive value for mortality in patients with angiographically demonstrated coronary artery disease. Circulation 2000;102 (16):1917-23.
20. Blankenberg S, Rupprecht HJ, Bickel C, Espinola-Klein C, Rippin G, Hafner G et al. Cytomegalovirus infection with interleukin-6 response predicts cardiac mortality in patients with coronary artery disease. Circulation 2001;103 (24):2915-21.
21. Clarkson P, Celermajer DS, Powe AJ, Donald AE, Henry RM, Deanfield JE. Endothelium-dependent dilatation is impaired in young healthy subjects with a family history of premature coronary disease. Circulation 1997;96 (10):3378-83.
22. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993;329 (27):2002-12.
23. Lum H, Roebuck KA. Oxidant stress and endothelial cell dysfunction. Am J Physiol Cell Physiol 2001;280 (4):C719-41.
24. Reed LJ, Muench MJ. A simple method of estimating fifty percent endpoints. Am J Hyg 1938;27:493.
25. Suchland RJ, Geisler WM, Stamm WE. Methodologies and cell lines used for antimicrobial susceptibility testing of Chlamydia spp. Antimicrob Agents Chemother 2003;47 (2):636-42.
26. Foulds G, Shepard RM, Johnson RB. The pharmacokinetics of azithromycin in human serum and tissues. J Antimicrob Chemother 1990;25 (Suppl A):73-82.
27. Baldwin DR, Wise R, Andrews JM, Ashby JP, Honeybourne D. Azithromycin concentrations at the sites of pulmonary infection. Eur Respir J 1990;3 (8):886-90.
28. Schneider CA, Diedrichs H, Riedel KD, Zimmermann T, Hopp HW. In vivo uptake of azithromycin in human coronary plaques. Am J Cardiol 2000;86 (7):789-91.
29. Reveneau N, Crane DD, Fischer E, Caldwell HD. Bactericidal activity of first-choice antibiotics against gamma interferon-induced persistent infection of human epithelial cells by Chlamydia trachomatis. Antimicrob Agents Chemother 2005;49 (5):1787-93.
30. Chirgwin K, Roblin PM, Hammerschlag MR. In vitro susceptibilities of Chlamydia pneumoniae (Chlamydia sp. strain TWAR). Antimicrob Agents Chemother 1989;33 (9):1634-5.
31. Agacfidan A, Moncada J, Schachter J. In vitro activity of azithromycin (CP-62,993) against Chlamydia trachomatis and Chlamydia pneumoniae. Antimicrob Agents Chemother 1993;37 (9):1746-8.
32. Donati M, Rodriguez FM, Olmo A, D'Apote L, Cevenini R. Comparative in-vitro activity of moxifloxacin, minocycline and azithromycin against Chlamydia spp. J Antimicrob Chemother 1999;43 (6):825-7.
33. High KP. Atherosclerosis and infection due to Chlamydia pneumoniae or cytomegalovirus: weighing the evidence. Clin Infect Dis 1999;28 (4):746-9.
34. Spence JD, Norris J. Infection, inflammation, and atherosclerosis. Stroke 2003;34 (2):333-4.
35. Leinenen M, Saikku P. Evidence for infectious agents in cardiovascular disease and atherosclerosis. Lancet Infect Dis 2002;2 (1):11-7.
36. Hippenstiel S, Suttorp N. Interaction of pathogens with the endothelium. Thromb Haemost 2003;89 (1):18-24.
37. Keller TT, Mairuhu AT, de Kruif MD, Klein SK, Gerdes VE, ten Cate XX et al. Infections and endothelial cells. Cardiovasc Res 2003;60 (1):40-8.
38. Cardaropoli S, Silvagno F, Morra E, Pescarmona GP, Todros T. Infectious and inflammatory stimuli decrease endothelial nitric oxide synthase activity in vitro. J Hypertens 2003;21 (11):2103-10.
39. Nerheim PL, Meier JL, Vasef MA, Li WG, Hu L, Rice JB et al. Enhanced cytomegalovirus infection in atherosclerotic human blood vessels. Am J Pathol 2004;164 (2):589-600.
40. Prasad A, Zhu J, Halcox JP, Waclawiw MA, Epstein SE, Quyyumi AA. Predisposition to atherosclerosis by infections: role of endothelial dysfunction. Circulation 2002;106 (2):184-90.
41. Caligiuri G, Rottenberg M, Nicoletti A, Wigzell H, Hansson GK. Chlamydia pneumoniae infection does not induce or modify atherosclerosis in mice. Circulation 2001;103 (23):2834-8.
42. Epstein SE, Zhou YF, Zhu J. Infection and atherosclerosis: emerging mechanistic paradigms. Circulation 1999;100 (4): e20-8.
43. Khairy P, Rinfret S, Tardif JC, Marchand R, Shapiro S, Brophy J et al. Absence of association between infectious agents and endothelial function in healthy young men. Circulation 2003;107 (15):1966-71.Epub.
44. Visseren FL, Verkerk MS, Bouter KP, Diepersloot RJ, Erkelens DW. Interleukin-6 production by endothelial cells after infection with influenza virus and cytomegalovirus. J Lab Clin Med 1999;134 (6):623-30.
45. Bouwman JJ, Visseren FL, Bosch MC, Bouter KP, Diepersloot RJ. Procoagulant and inflammatory response of virus-infected monocytes. Eur J Clin Invest 2002;32 (10):759-66.
46. Knight DA, Waldman WJ, Sedmak DD. Cytomegalovirus-mediated modulation of adhesion molecule expression by human arterial and microvascular endothelial cells. Transplantation 1999;68 (11):1814-8.
47. Zhu J, Quyyumi AA, Norman JE, Csako G, Epstein SE. Cytomegalovirus in the pathogenesis of atherosclerosis: the role of inflammation as reflected by elevated C-reactive protein levels. J Am Coll Cardiol 1999;34 (6):1738-43.
48. Kawashima S. The two faces of endothelial nitric oxide synthase in the pathophysiology of atherosclerosis. Endothelium 2004; 11 (2):99-107.
49. Visseren FL, Verkerk MS, van der Bruggen T, Marx JJ, van Asbeck BS, Diepersloot RJ. Iron chelation and hydroxyl radical scavenging reduce the inflammatory response of endothelial cells after infection with Chlamydia pneumoniae or influenza A. Eur J Clin Invest 2002;32 (Suppl 1):84-90.
50. Thomas SR, Chen K, Keaney JF Jr. Oxidative stress and endothelial nitric oxide bioactivity. Antioxid Redox Signal 2003;5 (2):18-94.
51. Fichtischerer S, Zeiher AM. Endothelial dysfunction in acute coronary syndromes: association with elevated C-reactive protein levels. Ann Med 2000;32 (8):515-8.
52. Fichtischerer S, Breuer S, Schachinger V, Dimmeler S, Zeiher AM. C-reactive protein levels determine systemic nitric oxide bioavailability in patients with coronary artery disease. Eur Heart J 2004;25 (16):1412-8.
53. Parchure N, Zouridakis EG, Kaski JC. Effect of azithromycin treatment on endothelial function in patients with coronary artery disease and evidence of Chlamydia pneumoniae infection. Circulation 2002;105 (11):1298-303.
54. Wiesli P, Czerwenka W, Meniconi A, Maly FE, Hoffmann U, Vetter W et al. Roxithromycin treatment prevents progression of peripheral arterial occlusive disease in Chlamydia pneumoniae seropositive men: a randomized, double-blind, placebo-controlled trial. Circulation 2002;105 (22):2646-52.
55. Ballou DP, Zhao Y, Brandish PE, Marletta MA. Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase: the simple NO-binding model is incorrect. Proc Natl Acad Sci USA 2002;99 (19):12097-101. Epub.
56. Muhlestein JB. Antibiotic treatment of atherosclerosis. Curr Opin Lipido 2003;14 (6):605-14.
57. Sander D, Winbeck K, Klingelhofer J, Etgen T, Conrad B. Reduced progression of early carotid atherosclerosis after antibiotic treatment and Chlamydia pneumoniae seropositivity. Circulation 2002;106 (19):2428-33.
58. Wells BJ, Mainous AGI, Dickerson LM. Antibiotics for the secondary prevention of ischemic heart disease: a meta-analysis of randomized controlled trials. Arch Intern Med 2004;164 (19):2156-61.
59. Grayston JT. Antibiotic treatment of atherosclerotic cardiovascular disease. Circulation 2003;107 (9):1228-30.
60. Cleland JG, Huan LP, Freemantle N, Clark AL, Coletta AP. Clinical trials update from the European Society of Cardiology: SENIORS, ACES, PROVE-IT, ACTION, and the HF-ACTION trial. Eur J Heart Fail 2004;6 (6):787-91.
61. O'Connor CM, Dunne MW, Pfeffer MA, Muhlestein JB, Yao L, Gupta S et al. Azithromycin for the secondary prevention of coronary heart disease events: the WIZARD study: a randomized controlled trial. JAMA 2003;290 (11):1459-66.
62. Gieffers J, Fullgraf H, Jahn J, Klinger M, Dalhoff K, Katus HA et al. Chlamydia pneumoniae infection in circulating human monocytes is refractory to antibiotic treatment. Circulation 2001;103 (3):351-6.
63. Hoymans VY, Bosmans JM, Leven M, Vrints CJ. Chlamydia pneumoniae and atherosclerosis. Acta Chir Belg 2002; 102 (5):317-22.
64. Kuvin JT, Gokce N, Holbrook M, Hunter LM, Patel AR, Sliney KA et al. Effect of short-term antibiotic treatment on Chlamydia pneumoniae and peripheral endothelial function. Am J Cardiol 2003;91 (6):732-5.
65. SoRelle R. Treatment with azithromycin improves endothelial function. Circulation 2002;105 (11):e9083-4.
66. Bouwman JJ, Visseren FL, Bouter PK, Diepersloot RJ. Azithromycin inhibits interleukin-6 but not fibrinogen production in hepatocytes infected with cytomegalovirus and Chlamydia pneumoniae. J Lab Clin Med 2004;144 (1):18-26.