Chlamydia pneumoniae induces tissue factor expression in mouse macrophages via activation of Egr-1 and the MEK-ERK1/2 pathway

Circulation Research

Volumn 92, Issue 4, 2003, Pages 394-401

  Bea, Florian ^a   Puolakkainen, Mirja H ^a   McMillen, Timothy ^a   Hudson, Francesca N ^a   Mackman, Nigel ^b   Kuo, Cho Chou ^a   Campbell, Lee Ann ^a   Rosenfeld, Michael E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Arteriosclerosis; Chlamydia pneumoniae; Signal transduction; Tissue factor

Indexed keywords

ANTIBODY; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; NUCLEAR PROTEIN; POLYMYXIN B; PROCOAGULANT; THROMBOPLASTIN; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR EGR 1;

ANIMAL CELL; ARTERIOSCLEROSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; BINDING SITE; CHLAMYDIASIS; CHLAMYDOPHILA PNEUMONIAE; CONSENSUS SEQUENCE; CONTROLLED STUDY; CORONARY ARTERY DISEASE; DNA RESPONSIVE ELEMENT; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC TRANSFECTION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THROMBOGENESIS; THROMBOSIS; TRANSCRIPTION REGULATION;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CELL LINE; CHLAMYDOPHILA PNEUMONIAE; DNA-BINDING PROTEINS; EARLY GROWTH RESPONSE PROTEIN 1; ELECTROPHORETIC MOBILITY SHIFT ASSAY; IMMEDIATE-EARLY PROTEINS; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; NUCLEAR PROTEINS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; THROMBOPLASTIN; TRANSCRIPTION FACTORS;

EID: 0037423893     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000059982.43865.75     Document Type: Article

References (41)

1. Saikku P, Leinonen M, Mattila K, Ekman MR, Nieminen MS, Makela PH, Huttunen JK, Valtonen V. Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction. Lancet. 1998;2:983-986.
2. Kuo CC, Gown AM, Benditt EP, Grayston JT. Detection of Chlamydia pneumoniae in aortic lesions of atherosclerosis by immunocytochemical stain. Arterioscler Thromb. 1993;13:1501-1504.
3. Kuo CC, Shot A, Campbell LA, Fukushi H, Patton DL, Grayston JT. Demonstration of Chlamydia pneumoniae in atherosclerotic lesions of coronary arteries. J Infect Dis. 1993;167:841-849.
4. Moazed TC, Campbell LA, Rosenfeld ME, Grayston JT, Kuo CC. Chlamydia pneumoniae infection accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice. J Infect Dis. 1999;180:238-241.
5. Muhlestein JB, Anderson JL, Hammond EH, Zhao L, Trehan S, Schwobe EP, Carlquist JF. Infection with Chlamydia pneumoniae accelerates the development of atherosclerosis and treatment with azithromycin prevents it in a rabbit model. Circulation. 1998;97:633-636.
6. Hu H, Pierce GN, Zhong G. The atherogenic effects of chlamydia are dependent on serum cholesterol and specific to Chlamydia pneumoniae. J Clin Invest. 1999;103:747-753.
7. Blessing E, Campbell LA, Rosenfeld ME, Chough N, Kuo CC. Chlamydia pneumoniae infection accelerates hyperlipidemia induced atherosclerotic lesion development in C57BL/6J mice. Atherosclerosis. 2001;158:13-17.
8. Shimada K, Mokuno H, Watanabe Y, Sawano M, Daida H, Yamaguchi H. High prevalence of seropositivity for antibodies to Chlamydia-specific lipopolysaccharide in patients with acute coronary syndrome. J Cardiovasc Risk. 2000;7:209-213.
9. de Boer OJ, van der Wal AC, Houtkamp MA, Ossewaarde JM, Teeling P, Becker AE. Unstable atherosclerotic plaques contain T-cells that respond to Chlamydia pneumoniae. Cardiovasc Res. 2000;48:402-408.
10. Moons AH, Levi M, Peters RJ. Tissue factor and coronary artery disease. Cardiovasc Res. 2002;53:313-325.
11. Guha M, O'Connell MA, Pawlinski R, Hollis A, McGovern P, Yan SF, Stern D, Mackman N. Lipopolysaccharide activation of the MEK-ERK1/2 pathway in human monocytic cells mediates tissue factor and tumor necrosis factor a expression by inducing Elk-1 phosphorylation and Egr-1 expression. Blood. 2000;98:1429-1439.
12. Cui MZ, Penn MS, Chisolm GM. Native and oxidized low density lipoprotein induction of tissue factor gene expression in smooth muscle cells is mediated by both Egr-1 and Sp1. J Biol Chem. 1999;274:32795-32802.
13. Houston P, Dickson MC, Ludbrook V, White B, Schwachtgen JL, McVey JH, Mackman N, Reese JM, Gorman DG, Campbell C, Braddock M. Fluid shear stress induction of the tissue factor promoter in vitro and in vivo is mediated by Egr-1. Arterioscler Thromb Vasc Biol. 1999;19:281-289.
14. Bavendiek U, Libby P, Kilbride M, Reynolds R, Mackman N, Schonbeck U. Induction of tissue factor expression in human endothelial cells via CD40 ligand is mediated by AP-1, NF-κB, and Egr-1. J Biol Chem. 2002;277:25032-25039.
15. Dechend R, Maass M, Gieffers J, Dietz R, Scheidereit C, Leutz A, Gulba DC. Chlamydia pneumoniae infection of vascular smooth muscle and endothelial cells activates NF-κB and induces tissue factor and PAI-1 expression: a potential link to accelerated arteriosclerosis. Circulation. 1999;100:1369-1373.
16. Wilcox JN, Smith KM, Schwartz SM, Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. Proc Natl Acad Sci U S A. 1989;86:2839-2843.
17. Landers SC, Gupta M, Lewis JC. Ultrastructural localization of tissue factor on monocyte-derived macrophages and macrophage foam cells associated with atherosclerotic lesions. Virchows Arch. 1994;425:49-54.
18. Muhlfelder TW, Teodorescu V, Rand J, Rosman A, Niemetz J. Human atheromatous plaque extracts induce tissue factor activity (TFa) in monocytes and also express constitutive TFa. Thromb Haemost. 1999;81:146-150.
19. Cui MZ, Parry GC, Oeth P, Larson H, Smith M, Huang RP, Adamson ED, Mackman N. Transcriptional regulation of the tissue factor gene in human epithelial cells is mediated by Sp1 and EGR-1. J Biol Chem. 1996;271:2731-2739.
20. Blessing E, Kuo CC, Lin TM, Campbell LA, Bea F, Chesebro B, Rosenfeld ME. Foam cell formation inhibits growth of Chlamydia pneumoniae but does not attenuate Chlamydia pneumoniae-induced secretion of proinflammatory cytokines. Circulation. 2002;23:1976-1982.
21. Miller SA, Selzman CH, Shames BD, Barton HA, Johnson SM, Harken AH. Chlamydia pneumoniae activates nuclear factor κB and activator protein 1 in human vascular smooth muscle and induces cellular proliferation. J Surg Res. 2000;90:76-81.
22. Hoppe-Seyler F, Butz K, Rittmueller C, von Knebel Doeberitz M. A rapid microscale procedure for the simultaneous preparation of cytoplasmatic RNA, nuclear DNA binding proteins and enzymatically active luciferase extracts. Nucleic Acids Res. 1991;19:5080.
23. Mlot C. Chlamydia linked to atherosclerosis. Science. 1996;272:1422.
24. Capron L. Chlamydia in coronary plaques-hidden culprit or harmless hobo? Nat Med. 1996;2:856-857.
25. Kalayoglu MV, Hoerneman B, LaVerda D, Morrison SG, Morrison RP, Byrne GI. Cellular oxidation of low-density lipoprotein by Chlamydia pneumoniae. J Infect Dis. 1999;180:780-790.
26. Heinemann M, Susa M, Simnacher U, Marre R, Essig A. Growth of Chlamydia pneumoniae induces cytokine production and expression of CD14 in a human monocytic cell line. Infect Immun. 1996;64:4872-4875.
27. Netea MG, Selzman CH, Kullberg BJ, Galama JM, Weinberg A, Stalenhoef AF, Van der Meer JW, Dinarello CA. Acellular components of Chlamydia pneumoniae stimulate cytokine production in human blood mononuclear cells. Eur J Immunol. 2000;30:541-549.
28. Krull M, Klucken AC, Wuppermann FN, Fuhrmann O, Magerl C, Seybold J, Hippenstiel S, Hegemann JH, Jantos CA, Suttorp N. Signal transduction pathways activated in endothelial cells following infection with Chlamydia pneumoniae. J Immunol. 1999;162:4834-4841.
29. Kol A, Sukhova GK, Lichtman AH, Libby P. Chlamydial heat shock protein 60 localizes in human atheroma and regulates macrophage tumor necrosis factor-α and matrix metalloproteinase expression. Circulation. 1998;98:300-307.
30. Libby P. Current concepts of the pathogenesis of the acute coronary syndromes. Circulation. 2001;104:365-372.
31. Moll T, Czyz M, Holzmuller H, Hofer-Warbinek R, Wagner E, Winkler H, Bach FH, Hofer E. Regulation of the tissue factor promoter in endothelial cells: binding of NF κB-, AP-1-, and Sp1-like transcription factors. J Biol Chem. 1995;270:3849-3857.
32. Mackman N. Regulation of the tissue factor gene. Thromb Haemost. 1997;78:747-754.
33. Yan SF, Zou YS, Gao Y, Zhai C, Mackman N, Lee SL, Milbrandt J, Pinsky D, Kisiel W, Stem D. Tissue factor transcription driven by Egr-1 is a critical mechanism of murine pulmonary fibrin deposition in hypoxia. Proc Natl Acad Sci U S A. 1999;95:9299-9303.
34. McCaffrey TA, Fu C, Du B, Eksinar S, Kent KC, Bush H Jr, Kreiger K, Rosengart T, Cybulsky MI, Silverman ES, Collins T. High-level expression of Egr-1 and Egr-1-inducible genes in mouse and human atherosclerosis. J Clin Invest. 2000;105:653-662.
35. Du B, Fu C, Kent KC, Bush H Jr, Schulick AH, Kreiger K, Collins T, McCaffrey TA. Elevated Egr-1 in human atherosclerotic cells transcriptionally represses the transforming growth factor-β type II receptor. J Biol Chem. 2000;275:39039-39047.
36. Kaisho T, Hoshino K, Iwabe T, Takeuchi O, Yasui T, Akira S. Endotoxin can induce MyD88-deficient dendritic cells to support T(h)2 cell differentiation. Int Immunol. 2002;14:695-700.
37. Sasu S, LaVerda D, Qureshi N, Golenbock DT, 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.
38. Kalayoglu MV, Indrawati, Morrison RP, Morrison SG, Yuan Y, Byrne GI. Chlamydial virulence determinants in atherogenesis: the role of chlamydial lipopolysaccharide and heat shock protein 60 in macrophagelipoprotein interactions. J Infect Dis. 2000;181:S483-S489.
39. Bulut Y, Faure E, Thomas L, Karahashi H, Michelsen KS, Equils O, Morrison SG, Morrison RP, Arditi M. Chlamydial heat shock protein 60 activates macrophages and endothelial cells through Toll-like receptor 4 and MD2 in a MyD88-dependent pathway. J Immunol. 2002;168:1435-1440.
40. Netea MG, Kullberg BJ, Galama JM, Stalenhoef AF, Dinarello CA, Van der Meer JW. Non-LPS components of Chlamydia pneumoniae stimulate cytokine production through Toll-like receptor 2-dependent pathways. Eur J Immunol. 2002;32:1188-1195.
41. Prebeck S, Kirschning C, Durr S, da Costa C, Donath B, Brand K, Redecke V, Wagner H, Miethke T. Predominant role of toll-like receptor 2 versus 4 in Chlamydia pneumoniae-induced activation of dendritic cells. J Immunol. 2001;167:3316-3323.