Possibilities for therapeutic interventions in disrupting Chlamydophila pneumoniae involvement in atherosclerosis

Fundamental and Clinical Pharmacology

Volumn 24, Issue 5, 2010, Pages 607-617

  Deniset, Justin F ^a   Pierce, Grant N ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

atherosclerosis; chlamydophila pneumoniae; drug treatment

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; AMOXICILLIN; ANTIBIOTIC AGENT; AZITHROMYCIN; BACTERIAL PROTEIN; BACTERIAL VACCINE; CLARITHROMYCIN; EFFECTOR CASPASE; GATIFLOXACIN; GLYCOLYTIC ENZYME; HEAT SHOCK PROTEIN 60; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; MACROLIDE; MATRIX METALLOPROTEINASE; MONOCYTE CHEMOTACTIC PROTEIN; NITRIC OXIDE SYNTHASE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN PROTEIN; PATTERN RECOGNITION RECEPTOR; PENTOSE PHOSPHATE; PLACEBO; PLASMINOGEN ACTIVATOR INHIBITOR; PROTEIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; ROXITHROMYCIN; TETRACYCLINE; THROMBOPLASTIN; TOLL LIKE RECEPTOR; UNINDEXED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ACUTE CORONARY SYNDROME; ACUTE HEART INFARCTION; ALTERNATIVE MEDICINE; ARTERIAL WALL THICKENING; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BLOOD VESSEL WALL; CARDIOVASCULAR DISEASE; CARDIOVASCULAR INFECTION; CAROTID ARTERY; CHLAMYDIAL PNEUMONIA; CHLAMYDOPHILA PNEUMONIAE; CLINICAL TRIAL; COMMUNITY ACQUIRED PNEUMONIA; CORONARY ARTERY; CORONARY ARTERY DISEASE; DISEASE ASSOCIATION; DISEASE MODEL; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; EXPERIMENTAL STUDY; FOAM CELL; HEART INFARCTION; HEMATOPOIESIS; HOST CELL; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; INFECTION; ISCHEMIC HEART DISEASE; MACROPHAGE; MYCOPLASMA PNEUMONIAE; NONHUMAN; PERSISTENT INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW; SEROEPIDEMIOLOGY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SODIUM TRANSPORT; T LYMPHOCYTE; TARGET CELL DESTRUCTION; TREATMENT OUTCOME; TYPE III SECRETION SYSTEM; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

ANIMALS; ANTI-BACTERIAL AGENTS; ATHEROSCLEROSIS; CHLAMYDIA INFECTIONS; CHLAMYDOPHILA PNEUMONIAE; CLINICAL TRIALS AS TOPIC; DRUG DELIVERY SYSTEMS; HUMANS;

EID: 77956979450     PISSN: 07673981     EISSN: 14728206     Source Type: Journal    
DOI: 10.1111/j.1472-8206.2010.00863.x     Document Type: Review

References (114)

1. Libby P., Ridker P.M., Hansson G.K. Inflammation in atherosclerosis: from pathophysiology to practice. J. Am. Coll. Cardiol. (2009) 54 2129 2138.
2. Blasi F., Tarsia P., Aliberti S. Chlamydophila pneumoniae. Clin. Microbiol. Infect. (2009) 15 29 35.
3. Saikku P., Leinonen M., Mattila K. et al. Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction. Lancet (1988) 2 983 986.
4. Watson C., Alp N.J. Role of Chlamydia pneumoniae in atherosclerosis. Clin. Sci. (Lond). (2008) 114 509 531.
5. Kuo C.C., Shor A., Campbell L.A., Fukushi H., Patton D.L., Grayston J.T. Demonstration of Chlamydia pneumoniae in atherosclerotic lesions of coronary arteries. J. Infect. Dis. (1993) 167 841 849.
6. Maass M., Bartels C., Engel P.M., Mamat U., Sievers H.H. Endovascular presence of viable Chlamydia pneumoniae is a common phenomenon in coronary artery disease. J. Am. Coll. Cardiol. (1998) 31 827 832. (Pubitemid 28186419)
7. Jackson L.A., Campbell L.A., Schmidt R.A. et al. Specificity of detection of Chlamydia pneumoniae in cardiovascular atheroma: evaluation of the innocent bystander hypothesis. Am. J. Pathol. (1997) 150 1785 1790.
8. Ramirez J.A. Isolation of Chlamydia pneumoniae from the coronary artery of a patient with coronary atherosclerosis. The Chlamydia pneumoniae/ Atherosclerosis Study Group. Ann. Intern. Med. (1996) 125 979 982.
9. Jackson L.A., Campbell L.A., Kuo C.C., Rodriguez D.I., Lee A., Grayston J.T. Isolation of Chlamydia pneumoniae from a carotid endarterectomy specimen. J. Infect. Dis. (1997) 176 292 295.
10. Mosorin M., Surcel H.M., Laurila A. et al. Detection of Chlamydia pneumoniae-reactive T lymphocytes in human atherosclerotic plaques of carotid artery. Arterioscler. Thromb. Vasc. Biol. (2000) 20 1061 1067.
11. Maass M., Gieffers J., Solbach W. Atherogenetically relevant cells support continuous growth of Chlamydia pneumoniae. Herz (2000) 25 68 72.
12. Godzik K.L., O'Brien E.R., Wang S.K., Kuo C.C. In vitro susceptibility of human vascular wall cells to infection with Chlamydia pneumoniae. J. Clin. Microbiol. (1995) 33 2411 2414.
13. Gaydos C.A., Summersgill J.T., Sahney N.N., Ramirez J.A., Quinn T.C. Replication of Chlamydia pneumoniae in vitro in human macrophages, endothelial cells, and aortic artery smooth muscle cells. Infect. Immun. (1996) 64 1614 1620.
14. Gieffers J., van Zandbergen G., Rupp J. et al. Phagocytes transmit Chlamydia pneumoniae from the lungs to the vasculature. Eur. Respir. J. (2004) 23 506 510.
15. Gueinzius K., Magenau A., Erath S. et al. Endothelial cells are protected against phagocyte-transmitted Chlamydophila pneumoniae infections by laminar shear stress Gueinzius: Shear stress protects from C. pneumoniae infection. Atherosclerosis (2008) 198 256 263.
16. Molestina R.E., Miller R.D., Ramirez J.A., Summersgill J.T. Infection of human endothelial cells with Chlamydia pneumoniae stimulates transendothelial migration of neutrophils and monocytes. Infect. Immun. (1999) 67 1323 1330.
17. Kaukoranta-Tolvanen S.S., Ronni T., Leinonen M., Saikku P., Laitinen K. Expression of adhesion molecules on endothelial cells stimulated by Chlamydia pneumoniae. Microb. Pathog. (1996) 21 407 411.
18. Krull M., Klucken A.C., Wuppermann F.N. et al. Signal transduction pathways activated in endothelial cells following infection with Chlamydia pneumoniae. J. Immunol. (1999) 162 4834 4841.
19. Hogdahl M., Soderlund G., Kihlstrom E. Expression of chemokines and adhesion molecules in human coronary artery endothelial cells infected with Chlamydia (Chlamydophila) pneumoniae. APMIS (2008) 116 1082 1088.
20. Yang X., Coriolan D., Schultz K., Golenbock D.T., Beasley D. Toll-like receptor 2 mediates persistent chemokine release by Chlamydia pneumoniae-infected vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. (2005) 25 2308 2314.
21. Chen C., Chai H., Wang X., Lin P.H., Yao Q. Chlamydia heat shock protein 60 decreases expression of endothelial nitric oxide synthase in human and porcine coronary artery endothelial cells. Cardiovasc. Res. (2009) 83 768 777.
22. Netea M.G., Kullberg B.J., Jacobs L.E. et al. Chlamydia pneumoniae stimulates IFN-gamma synthesis through MyD88-dependent, TLR2- and TLR4-independent induction of IL-18 release. J. Immunol. (2004) 173 1477 1482.
23. Mei C.L., He P., Cheng B., Liu W., Wang Y.F., Wan J.J. Chlamydia pneumoniae induces macrophage-derived foam cell formation via PPAR alpha and PPAR gamma-dependent pathways. Cell Biol. Int. (2009) 33 301 308.
24. He P., Mei C., Cheng B., Liu W., Wang Y., Wan J. Chlamydia pneumoniae induces macrophage-derived foam cell formation by up-regulating acyl-coenzyme A: cholesterol acyltransferase 1. Microbes Infect. (2009) 11 157 163.
25. Carratelli C.R., Paolillo R., Rizzo A. Chlamydia pneumoniae stimulates the proliferation of HUVEC through the induction of VEGF by THP-1. Int. Immunopharmacol. (2007) 7 287 294.
26. Kol A., Sukhova G.K., Lichtman A.H., Libby P. Chlamydial heat shock protein 60 localizes in human atheroma and regulates macrophage tumor necrosis factor-alpha and matrix metalloproteinase expression. Circulation (1998) 98 300 307.
27. Nazzal D., Cantero A.V., Therville N. et al. Chlamydia pneumoniae alters mildly oxidized low-density lipoprotein-induced cell death in human endothelial cells, leading to necrosis rather than apoptosis. J. Infect. Dis. (2006) 193 136 145.
28. Dechend R., Gieffers J., Dietz R. et al. Hydroxymethylglutaryl coenzyme A reductase inhibition reduces Chlamydia pneumoniae-induced cell interaction and activation. Circulation (2003) 108 261 265.
29. Schmeck B., Beermann W., N'Guessan P.D. et al. Simvastatin reduces Chlamydophila pneumoniae-mediated histone modifications and gene expression in cultured human endothelial cells. Circ. Res. (2008) 102 888 895.
30. Azenabor A.A., Yang S., Job G., Adedokun O.O. Elicitation of reactive oxygen species in Chlamydia pneumoniae-stimulated macrophages: a Ca2+-dependent process involving simultaneous activation of NADPH oxidase and cytochrome oxidase genes. Med. Microbiol. Immunol. (2005) 194 91 103.
31. Sasu S., LaVerda D., Qureshi N., Golenbock D.T., Beasley D. Chlamydia pneumoniae and chlamydial heat shock protein 60 stimulate proliferation of human vascular smooth muscle cells via toll-like receptor 4 and p44/p42 mitogen-activated protein kinase activation. Circ. Res. (2001) 89 244 250.
32. Hirono S., Dibrov E., Hurtado C., Kostenuk A., Ducas R., Pierce G.N. Chlamydia pneumoniae stimulates proliferation of vascular smooth muscle cells through induction of endogenous heat shock protein 60. Circ. Res. (2003) 93 710 716.
33. Coombes B.K., Mahony J.B. Chlamydia pneumoniae infection of human endothelial cells induces proliferation of smooth muscle cells via an endothelial cell-derived soluble factor(s). Infect. Immun. (1999) 67 2909 2915.
34. Rupp J., Hellwig-Burgel T., Wobbe V., Seitzer U., Brandt E., Maass M. Chlamydia pneumoniae infection promotes a proliferative phenotype in the vasculature through Egr-1 activation in vitro and in vivo. Proc. Natl Acad. Sci. USA (2005) 102 3447 3452.
35. Fryer R.H., Schwobe E.P., Woods M.L., Rodgers G.M. Chlamydia species infect human vascular endothelial cells and induce procoagulant activity. J. Investig. Med. (1997) 45 168 174.
36. Dechend R., Maass M., Gieffers J. et al. Chlamydia pneumoniae infection of vascular smooth muscle and endothelial cells activates NF-kappaB and induces tissue factor and PAI-1 expression: a potential link to accelerated arteriosclerosis. Circulation (1999) 100 1369 1373.
37. Rodel J., Prochnau D., Prager K., Pentcheva E., Hartmann M., Straube E. Increased production of matrix metalloproteinases 1 and 3 by smooth muscle cells upon infection with Chlamydia pneumoniae. FEMS Immunol. Med. Microbiol. (2003) 38 159 164.
38. Fong I.W., Chiu B., Viira E., Fong M.W., Jang D., Mahony J. Rabbit model for Chlamydia pneumoniae infection. J. Clin. Microbiol. (1997) 35 48 52.
39. Fong I.W., Chiu B., Viira E., Jang D., Mahony J.B. De Novo induction of atherosclerosis by Chlamydia pneumoniae in a rabbit model. Infect. Immun. (1999) 67 6048 6055.
40. Muhlestein J.B., Anderson J.L., Hammond E.H. et al. Infection with Chlamydia pneumoniae accelerates the development of atherosclerosis and treatment with azithromycin prevents it in a rabbit model. Circulation (1998) 97 633 636.
41. Hu H., Pierce G.N., Zhong G. The atherogenic effects of chlamydia are dependent on serum cholesterol and specific to Chlamydia pneumoniae. J. Clin. Invest. (1999) 103 747 753.
42. Blessing E., Lin T.M., Campbell L.A., Rosenfeld M.E., Lloyd D., Kuo C. Chlamydia pneumoniae induces inflammatory changes in the heart and aorta of normocholesterolemic C57BL/6J mice. Infect. Immun. (2000) 68 4765 4768.
43. Blessing E., Campbell L.A., Rosenfeld M.E., Chough N., Kuo C.C. Chlamydia pneumoniae infection accelerates hyperlipidemia induced atherosclerotic lesion development in C57BL/6J mice. Atherosclerosis (2001) 158 13 17.
44. Liu L., Hu H., Ji H., Murdin A.D., Pierce G.N., Zhong G. Chlamydia pneumoniae infection significantly exacerbates aortic atherosclerosis in an LDLR-/- mouse model within six months. Mol. Cell. Biochem. (2000) 215 123 128.
45. Blessing E., Campbell L.A., Rosenfeld M.E., Kuo C.C. Chlamydia pneumoniae and hyperlipidemia are co-risk factors for atherosclerosis: infection prior to induction of hyperlipidemia does not accelerate development of atherosclerotic lesions in C57BL/6J mice. Infect. Immun. (2002) 70 5332 5334.
46. Blessing E., Nagano S., Campbell L.A., Rosenfeld M.E., Kuo C.C. Effect of Chlamydia trachomatis infection on atherosclerosis in apolipoprotein E-deficient mice. Infect. Immun. (2000) 68 7195 7197.
47. Liuba P., Karnani P., Pesonen E. et al. Endothelial dysfunction after repeated Chlamydia pneumoniae infection in apolipoprotein E-knockout mice. Circulation (2000) 102 1039 1044.
48. Liuba P., Pesonen E., Paakkari I. et al. Acute Chlamydia pneumoniae infection causes coronary endothelial dysfunction in pigs. Atherosclerosis (2003) 167 215 222.
49. Pislaru S.V., Van Ranst M., Pislaru C. et al. Chlamydia pneumoniae induces neointima formation in coronary arteries of normal pigs. Cardiovasc. Res. (2003) 57 834 842.
50. Deniset J.F., Cheung P.K., Dibrov E., Lee K., Steigerwald S., Pierce G.N. Chlamydophila pneumoniae infection leads to smooth muscle cell proliferation and thickening in the coronary artery without contributions from a host immune response. Am. J. Pathol. (2010) 176 1028 1037.
51. Gieffers J., Solbach W., Maass M. In vitro susceptibilities of Chlamydia pneumoniae strains recovered from atherosclerotic coronary arteries. Antimicrob. Agents Chemother. (1998) 42 2762 2764.
52. Chirgwin K., Roblin P.M., Hammerschlag M.R. In vitro susceptibilities of Chlamydia pneumoniae (Chlamydia sp. strain TWAR). Antimicrob. Agents Chemother. (1989) 33 1634 1635.
53. Schneider C.A., Diedrichs H., Riedel K.D., Zimmermann T., Hopp H.W. In vivo uptake of azithromycin in human coronary plaques. Am. J. Cardiol. (2000) 86 789 791.
54. Fong I.W. Value of animal models for Chlamydia pneumoniae-related atherosclerosis. Am. Heart J. (1999) 138 S512 S513.
55. Meier C.R., Derby L.E., Jick S.S., Vasilakis C., Jick H. Antibiotics and risk of subsequent first-time acute myocardial infarction. JAMA (1999) 281 427 431.
56. Jackson L.A., Smith N.L., Heckbert S.R., Grayston J.T., Siscovick D.S., Psaty B.M. Lack of association between first myocardial infarction and past use of erythromycin, tetracycline, or doxycycline. Emerg. Infect. Dis. (1999) 5 281 284.
57. Gupta S., Leatham E.W., Carrington D., Mendall M.A., Kaski J.C., Camm A.J. Elevated Chlamydia pneumoniae antibodies, cardiovascular events, and azithromycin in male survivors of myocardial infarction. Circulation (1997) 96 404 407. (Pubitemid 27329411)
58. O'Connor C.M., Dunne M.W., Pfeffer M.A. et al. Azithromycin for the secondary prevention of coronary heart disease events: the WIZARD study: a randomized controlled trial. JAMA (2003) 290 1459 1466.
59. Grayston J.T., Kronmal R.A., Jackson L.A. et al. Azithromycin for the secondary prevention of coronary events. N. Engl. J. Med. (2005) 352 1637 1645.
60. Jespersen C.M., Als-Nielsen B., Damgaard M. et al. Randomised placebo controlled multicentre trial to assess short term clarithromycin for patients with stable coronary heart disease: CLARICOR trial. BMJ (2006) 332 22 27.
61. Gurfinkel E., Bozovich G., Beck E., Testa E., Livellara B., Mautner B. Treatment with the antibiotic roxithromycin in patients with acute non-Q-wave coronary syndromes. The final report of the ROXIS Study. Eur. Heart J. (1999) 20 121 127.
62. Sinisalo J., Mattila K., Valtonen V. et al. Effect of 3 months of antimicrobial treatment with clarithromycin in acute non-q-wave coronary syndrome. Circulation (2002) 105 1555 1560.
63. Stone A.F., Mendall M.A., Kaski J.C. et al. Effect of treatment for Chlamydia pneumoniae and Helicobacter pylori on markers of inflammation and cardiac events in patients with acute coronary syndromes: South Thames Trial of Antibiotics in Myocardial Infarction and Unstable Angina (STAMINA). Circulation (2002) 106 1219 1223.
64. Zahn R., Schneider S., Frilling B. et al. Antibiotic therapy after acute myocardial infarction: a prospective randomized study. Circulation (2003) 107 1253 1259.
65. Cercek B., Shah P.K., Noc M. et al. Effect of short-term treatment with azithromycin on recurrent ischaemic events in patients with acute coronary syndrome in the Azithromycin in Acute Coronary Syndrome (AZACS) trial: a randomised controlled trial. Lancet (2003) 361 809 813.
66. Cannon C.P., Braunwald E., McCabe C.H. et al. Antibiotic treatment of Chlamydia pneumoniae after acute coronary syndrome. N. Engl. J. Med. (2005) 352 1646 1654.
67. Coombes B.K., Johnson D.L., Mahony J.B. Strategic targeting of essential host-pathogen interactions in chlamydial disease. Curr. Drug Targets Infect. Disord. (2002) 2 201 216.
68. Gieffers J., Fullgraf H., Jahn J. et al. Chlamydia pneumoniae infection in circulating human monocytes is refractory to antibiotic treatment. Circulation (2001) 103 351 356.
69. Kutlin A., Roblin P.M., Hammerschlag M.R. Effect of prolonged treatment with azithromycin, clarithromycin, or levofloxacin on Chlamydia pneumoniae in a continuous-infection Model. Antimicrob. Agents Chemother. (2002) 46 409 412.
70. Rottenberg M.E., Gigliotti Rothfuchs A.C., Gigliotti D., Svanholm C., Bandholtz L., Wigzell H. Role of innate and adaptive immunity in the outcome of primary infection with Chlamydia pneumoniae, as analyzed in genetically modified mice. J. Immunol. (1999) 162 2829 2836.
71. Penttila J.M., Anttila M., Varkila K. et al. Depletion of CD8+ cells abolishes memory in acquired immunity against Chlamydia pneumoniae in BALB/c mice. Immunology (1999) 97 490 496.
72. Penttila T., Wahlstrom E., Vuola J.M., Sarvas M., Puolakkainen M. Systemic and mucosal antibody response in experimental Chlamydia pneumoniae infection of mice. Comp. Med. (2006) 56 272 278.
73. Rodriguez A., Rottenberg M., Tjarnlund A., Fernandez C. Immunoglobulin A and CD8 T-cell mucosal immune defenses protect against intranasal infection with Chlamydia pneumoniae. Scand. J. Immunol. (2006) 63 177 183.
74. Svanholm C., Bandholtz L., Castanos-Velez E., Wigzell H., Rottenberg M.E. Protective DNA immunization against Chlamydia pneumoniae. Scand. J. Immunol. (2000) 51 345 353.
75. Penttila T., Vuola J.M., Puurula V. et al. Immunity to Chlamydia pneumoniae induced by vaccination with DNA vectors expressing a cytoplasmic protein (Hsp60) or outer membrane proteins (MOMP and Omp2). Vaccine (2000) 19 1256 1265.
76. Penttila T., Tammiruusu A., Liljestrom P. et al. DNA immunization followed by a viral vector booster in a Chlamydia pneumoniae mouse model. Vaccine (2004) 22 3386 3394.
77. Murdin A.D., Dunn P., Sodoyer R. et al. Use of a mouse lung challenge model to identify antigens protective against Chlamydia pneumoniae lung infection. J. Infect. Dis. (2000) 181 (Suppl 3) S544 S551.
78. Pinchuk I., Starcher B.C., Livingston B. et al. A CD8+ T cell heptaepitope minigene vaccine induces protective immunity against Chlamydia pneumoniae. J. Immunol. (2005) 174 5729 5739.
79. Thorpe C., Edwards L., Snelgrove R. et al. Discovery of a vaccine antigen that protects mice from Chlamydia pneumoniae infection. Vaccine (2007) 25 2252 2260.
80. Donnelly J.J., Wahren B., Liu M.A. DNA vaccines: progress and challenges. J. Immunol. (2005) 175 633 639.
81. Mahony J.B. Chlamydiae host cell interactions revealed using DNA microarrays. Ann. N Y Acad. Sci. (2002) 975 192 201.
82. Hammerschlag M.R. The intracellular life of chlamydiae. Semin. Pediatr. Infect. Dis. (2002) 13 239 248.
83. Coombes B.K., Mahony J.B. Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells. Cell Microbiol. (2002) 4 447 460.
84. Shaw E.I., Dooley C.A., Fischer E.R., Scidmore M.A., Fields K.A., Hackstadt T. Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. Mol. Microbiol. (2000) 37 913 925.
85. Valdivia R.H. Chlamydia effector proteins and new insights into chlamydial cellular microbiology. Curr. Opin. Microbiol. (2008) 11 53 59.
86. Mathews S., George C., Flegg C., Stenzel D., Timms P. Differential expression of ompA, ompB, pyk, nlpD and Cpn0585 genes between normal and interferon-gamma treated cultures of Chlamydia pneumoniae. Microb. Pathog. (2001) 30 337 345.
87. Byrne G.I., Ouellette S.P., Wang Z. et al. Chlamydia pneumoniae expresses genes required for DNA replication but not cytokinesis during persistent infection of HEp-2 cells. Infect. Immun. (2001) 69 5423 5429.
88. Nicholson T.L., Olinger L., Chong K., Schoolnik G., Stephens R.S. Global stage-specific gene regulation during the developmental cycle of Chlamydia trachomatis. J. Bacteriol. (2003) 185 3179 3189.
89. Iliffe-Lee E.R., McClarty G. Glucose metabolism in Chlamydia trachomatis: the 'energy parasite' hypothesis revisited. Mol. Microbiol. (1999) 33 177 187.
90. Dibrov P., Dibrov E., Pierce G.N., Galperin M.Y. Salt in the wound: a possible role of Na+ gradient in chlamydial infection. J. Mol. Microbiol. Biotechnol. (2004) 8 1 6.
91. Peters J., Wilson D.P., Myers G., Timms P., Bavoil P.M. Type III secretion a la Chlamydia. Trends Microbiol. (2007) 15 241 251.
92. Heuer D., Brinkmann V., Meyer T.F., Szczepek A.J. Expression and translocation of chlamydial protease during acute and persistent infection of the epithelial HEp-2 cells with Chlamydophila (Chlamydia) pneumoniae. Cell Microbiol. (2003) 5 315 322.
93. Slepenkin A., Motin V., de la Maza L.M., Peterson E.M. Temporal expression of type III secretion genes of Chlamydia pneumoniae. Infect. Immun. (2003) 71 2555 2562.
94. Cortes C., Rzomp K.A., Tvinnereim A., Scidmore M.A., Wizel B. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect. Immun. (2007) 75 5586 5596.
95. Jewett T.J., Fischer E.R., Mead D.J., Hackstadt T. Chlamydial TARP is a bacterial nucleator of actin. Proc. Natl Acad. Sci. USA (2006) 103 15599 15604.
96. Savijoki K., Alvesalo J., Vuorela P., Leinonen M., Kalkkinen N. Proteomic analysis of Chlamydia pneumoniae-infected HL cells reveals extensive degradation of cytoskeletal proteins. FEMS Immunol. Med. Microbiol. (2008) 54 375 384.
97. Rupp J., Gieffers J., Klinger M. et al. Chlamydia pneumoniae directly interferes with HIF-1alpha stabilization in human host cells. Cell Microbiol. (2007) 9 2181 2191.
98. Pirbhai M., Dong F., Zhong Y., Pan K.Z., Zhong G. The secreted protease factor CPAF is responsible for degrading pro-apoptotic BH3-only proteins in Chlamydia trachomatis-infected cells. J. Biol. Chem. (2006) 281 31495 31501.
99. Fischer S.F., Schwarz C., Vier J., Hacker G. Characterization of antiapoptotic activities of Chlamydia pneumoniae in human cells. Infect. Immun. (2001) 69 7121 7129.
100. Airenne S., Surcel H.M., Tuukkanen J., Leinonen M., Saikku P. Chlamydia pneumoniae inhibits apoptosis in human epithelial and monocyte cell lines. Scand. J. Immunol. (2002) 55 390 398.
101. Paland N., Rajalingam K., Machuy N., Szczepek A., Wehrl W., Rudel T. NF-kappaB and inhibitor of apoptosis proteins are required for apoptosis resistance of epithelial cells persistently infected with Chlamydophila pneumoniae. Cell Microbiol. (2006) 8 1643 1655.
102. Ying S., Pettengill M., Latham E.R., Walch A., Ojcius D.M., Hacker G. Premature apoptosis of Chlamydia-infected cells disrupts chlamydial development. J. Infect. Dis. (2008) 198 1536 1544.
103. Costa C.P., Kirschning C.J., Busch D. et al. Role of chlamydial heat shock protein 60 in the stimulation of innate immune cells by Chlamydia pneumoniae. Eur. J. Immunol. (2002) 32 2460 2470.
104. Da Costa C.U., Wantia N., Kirschning C.J. et al. Heat shock protein 60 from Chlamydia pneumoniae elicits an unusual set of inflammatory responses via Toll-like receptor 2 and 4 in vivo. Eur. J. Immunol. (2004) 34 2874 2884.
105. Krull M., Maass M., Suttorp N., Rupp J. Chlamydophila pneumoniae. Mechanisms of target cell infection and activation. Thromb. Haemost. (2005) 94 319 326.
106. Liuba P., Pesonen E., Paakkari I. et al. Co-infection with Chlamydia pneumoniae and Helicobacter pylori results in vascular endothelial dysfunction and enhanced VCAM-1 expression in apoE-knockout mice. J. Vasc. Res. (2003) 40 115 222.
107. Moazed T.C., Campbell L.A., Rosenfeld M.E., Grayston J.T., Kuo C.C. Chlamydia pneumoniae infection accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice. J. Infect. Dis. (1999) 180 238 241.
108. Burnett M.S., Gaydos C.A., Madico G.E. et al. Atherosclerosis in apoE knockout mice infected with multiple pathogens. J. Infect. Dis. (2001) 183 226 231.
109. Caligiuri G., Rottenberg M., Nicoletti A., Wigzell H., Hansson G.K. Chlamydia pneumoniae infection does not induce or modify atherosclerosis in mice. Circulation (2001) 103 2834 2838.
110. Aalto-Setala K., Laitinen K., Erkkila L. et al. Chlamydia pneumoniae does not increase atherosclerosis in the aortic root of apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. (2001) 21 578 584.
111. Ezzahiri R., Stassen F.R., Kurvers H.A., van Pul M.M., Kitslaar P.J., Bruggeman C.A. Chlamydia pneumoniae infection induces an unstable atherosclerotic plaque phenotype in LDL-receptor, ApoE double knockout mice. Eur. J. Vasc. Endovasc. Surg. (2003) 26 88 95.
112. Burian K., Berencsi K., Endresz V. et al. Chlamydia pneumoniae exacerbates aortic inflammatory foci caused by murine cytomegalovirus infection in normocholesterolemic mice. Clin. Diagn. Lab. Immunol. (2001) 8 1263 1266.
113. Liuba P., Pesonen E., Forslid A. et al. Protective effects of simvastatin on coronary artery function in swine with acute infection. Atherosclerosis (2006) 186 331 336.
114. Muhlestein J.B., Anderson J.L., Carlquist J.F. et al. Randomized secondary prevention trial of azithromycin in patients with coronary artery disease: primary clinical results of the ACADEMIC study. Circulation (2000) 102 1755 1760.