GroEL1, a heat shock protein 60 of chlamydia pneumoniae, induces lectin-like oxidized low-density lipoprotein receptor 1 expression in endothelial cells and enhances atherogenesis in hypercholesterolemic rabbits

Journal of Immunology

Volumn 186, Issue 7, 2011, Pages 4405-4414

  Lin, Feng Yen ^a,b   Lin, Yi Wen ^a,b   Huang, Chun Yao ^a,b   Chang, Yu Jia ^b   Tsao, Nai Wen ^a   Chang, Nen Chung ^a,b   Ou, Keng Liang ^b   Chen, Ta Liang ^a,c   Shih, Chun Ming ^a,b   Chen, Yung Hsiang ^d  

^a TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c School of Medicine   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

APOCYNIN; C REACTIVE PROTEIN; DIPHENYLIODONIUM SALT; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEAT SHOCK PROTEIN 60; MACROGOL; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN GROEL1; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CELL INFILTRATION; CHLAMYDOPHILA PNEUMONIAE; CONTROLLED STUDY; CORONARY ARTERY; CYTOTOXICITY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ERYTHROCYTE SEDIMENTATION RATE; GENE; HUMAN; HUMAN CELL; HYPERCHOLESTEROLEMIA; IN VITRO STUDY; MACROPHAGE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; RAC1 GENE; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ADULT; ANIMALS; ATHEROSCLEROSIS; CELL LINE, TUMOR; CHAPERONIN 60; CHLAMYDOPHILA INFECTIONS; CHLAMYDOPHILA PNEUMONIAE; CORONARY VESSELS; ENDOTHELIUM, VASCULAR; HELA CELLS; HUMANS; HYPERCHOLESTEROLEMIA; INFLAMMATION MEDIATORS; MALE; RABBITS; SCAVENGER RECEPTORS, CLASS E; TOLL-LIKE RECEPTOR 4; UP-REGULATION;

EID: 79955029534     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003116     Document Type: Article

References (47)

1. Xu, Q. 2003. Infections, heat shock proteins, and atherosclerosis. Curr. Opin. Cardiol. 18: 245-252. (Pubitemid 37041042)
2. Volanen, I., M. J. Järvisalo, R. Vainionpää, M. Arffman, K. Kallio, S. Anglé, T. Rönnemaa, J. Viikari, J. Marniemi, O. T. Raitakari, and O. Simell. 2006. Increased aortic intima-media thickness in 11-year-old healthy children with persistent Chlamydia pneumoniae seropositivity. Arterioscler. Thromb. Vasc. Biol. 26: 649-655.
3. Blessing, E., L. A. Campbell, M. E. Rosenfeld, N. Chough, and C. C. Kuo. 2001. Chlamydia pneumoniae infection accelerates hyperlipidemia induced atherosclerotic lesion development in C57BL/6J mice. Atherosclerosis 158: 13-17. (Pubitemid 32735462)
4. Ezzahiri, R., H. J. Nelissen-Vrancken, H. A. Kurvers, F. R. Stassen, I. Vliegen, G. E. Grauls, M. M. van Pul, P. J. Kitslaar, and C. A. Bruggeman. 2002. Chlamydophila pneumoniae (Chlamydia pneumoniae) accelerates the formation of complex atherosclerotic lesions in Apo E3-Leiden mice. Cardiovasc. Res. 56: 269-276. (Pubitemid 35223497)
5. Kalayoglu, M. V., and G. I. Byrne. 1998. Induction of macrophage foam cell formation by Chlamydia pneumoniae. J. Infect. Dis. 177: 725-729. (Pubitemid 28099889)
6. Kalayoglu, M. V., B. Hoerneman, D. LaVerda, S. G. Morrison, R. P. Morrison, and G. I. Byrne. 1999. Cellular oxidation of low-density lipoprotein by Chlamydia pneumoniae. J. Infect. Dis. 180: 780-790. (Pubitemid 29411365)
7. Hybiske,K.,andR.S.Stephens.2007. Mechanismsofhostcellexitbytheintracellular bacteriumChlamydia.Proc.Natl.Acad. Sci.USA104:11430-11435. (Pubitemid 47175157)
8. Zügel, U., and S. H. Kaufmann. 1999. Role of heat shock proteins in protection from and pathogenesis of infectious diseases. Clin. Microbiol. Rev. 12: 19-39. (Pubitemid 29055952)
9. Borel, N., J. T. Summersgill, S. Mukhopadhyay, R. D. Miller, J. A. Ramirez, and A. Pospischil. 2008. Evidence for persistent Chlamydia pneumoniae infection of human coronary atheromas. Atherosclerosis 199: 154-161. (Pubitemid 351842691)
10. Kol, A., T. Bourcier, A. H. Lichtman, and P. Libby. 1999. Chlamydial and human heat shock protein 60s activate human vascular endothelium, smooth muscle cells, and macrophages. J. Clin. Invest. 103: 571-577. (Pubitemid 29094058)
11. Krüll, M., A. C. Klucken, F. N. Wuppermann, O. Fuhrmann, C. Magerl, J. Seybold, S. Hippenstiel, J. H. Hegemann, C. A. Jantos, and N. Suttorp. 1999. Signal transduction pathways activated in endothelial cells following infection with Chlamydia pneumoniae. J. Immunol. 162: 4834-4841. (Pubitemid 29314887)
12. Sasu, S., D. LaVerda, N. Qureshi, D. T. Golenbock, and D. Beasley. 2001. 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. 89: 244-250. (Pubitemid 34132682)
13. Yoshida, T., N. Koide, I. Mori, H. Ito, and T. Yokochi. 2006. Chlamydia pneumoniae infection enhances lectin-like oxidized low-density lipoprotein receptor (LOX-1) expression on human endothelial cells. FEMS Microbiol. Lett. 260: 17-22. (Pubitemid 43873567)
14. Winocour, P. H., P. N. Durrington, D. Bhatnagar, M. Ishola, S. Arrol, and M. Mackness. 1992. Abnormalities of VLDL, IDL, and LDL characterize insulin-dependent diabetes mellitus. Arterioscler. Thromb. 12: 920-928.
15. Steinbrecher, U. P., S. Parthasarathy, D. S. Leake, J. L. Witztum, and D. Steinberg. 1984. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc. Natl. Acad. Sci. USA 81: 3883-3887. (Pubitemid 14087823)
16. Hatch, F. T. 1968. Practical methods for plasma lipoprotein analysis. Adv. Lipid Res. 6: 1-68.
17. Oriol, A., J. M. Ribera, J. Arnal, F. Milla, M. Batlle, and E. Feliu. 1993. Saccharomyces cerevisiae septicemia in a patient with myelodysplastic syndrome. Am. J. Hematol. 43: 325-326. (Pubitemid 23205222)
18. Smith, K. R., L. R. Klei, and A. Barchowsky. 2001. Arsenite stimulates plasma membrane NADPH oxidase in vascular endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 280: L442-L449.
19. Costa, C. P., C. J. Kirschning, D. Busch, S. Dürr, L. Jennen, U. Heinzmann, S. Prebeck, H. Wagner, and T. Miethke. 2002. Role of chlamydial heat shock protein 60 in the stimulation of innate immune cells by Chlamydia pneumoniae. Eur. J. Immunol. 32: 2460-2470.
20. Yokoyama, M., N. Inoue, and S. Kawashima. 2000. Role of the vascular NADH/ NADPH oxidase system in atherosclerosis. Ann. N. Y. Acad. Sci. 902: 241-247, discussion 247-248.
21. Belland, R. J., S. P. Ouellette, J. Gieffers, and G. I. Byrne. 2004. Chlamydia pneumoniae and atherosclerosis. Cell. Microbiol. 6: 117-127. (Pubitemid 38111593)
22. Grayston, J. T. 2000. Background and current knowledge of Chlamydia pneumoniae and atherosclerosis. J. Infect. Dis. 181(Suppl. 3): S402-S410. (Pubitemid 30416105)
23. Ieven, M. M., andV.Y. Hoymans. 2005. Involvement of Chlamydia pneumoniae in atherosclerosis: More evidence for lack of evidence. J. Clin.Microbiol. 43: 19-24. (Pubitemid 40096274)
24. Kalayoglu, M. V., P. Libby, and G. I. Byrne. 2002. Chlamydia pneumoniae as an emerging risk factor in cardiovascular disease. JAMA 288: 2724-2731. (Pubitemid 35403786)
25. Wells, B. J., A. G. Mainous, III, and L. M. Dickerson. 2004. Antibiotics for the secondary prevention of ischemic heart disease: A meta-analysis of randomized controlled trials. Arch. Intern. Med. 164: 2156-2161. (Pubitemid 39410806)
26. Illoh, K. O., O. C. Illoh, H. B. Feseha, and J. M. Hallenbeck. 2005. Antibiotics for vascular diseases: A meta-analysis of randomized controlled trials. Atherosclerosis 179: 403-412. (Pubitemid 40364637)
27. Saikku, P., M. Leinonen, L. Tenkanen, E. Linnanmäki, M. R. Ekman, V. Manninen, M. Mänttäri, M. H. Frick, and J. K. Huttunen. 1992. Chronic Chlamydia pneumoniae infection as a risk factor for coronary heart disease in the Helsinki Heart Study. Ann. Intern. Med. 116: 273-278.
28. Chen, S., R. Sorrentino, K. Shimada, Y. Bulut, T. M. Doherty, T. R. Crother, and M. Arditi. 2008. Chlamydia pneumoniae-induced foam cell formation requires MyD88-dependent and -independent signaling and is reciprocally modulated by liver X receptor activation. J. Immunol. 181: 7186-7193.
29. Naiki, Y., R. Sorrentino, M. H. Wong, K. S. Michelsen, K. Shimada, S. Chen, A. Yilmaz, A. Slepenkin, N. W. Schröder, T. R. Crother, et al. 2008. TLR/ MyD88 and liver X receptor alpha signaling pathways reciprocally control Chlamydia pneumoniae-induced acceleration of atherosclerosis. J. Immunol. 181: 7176-7185.
30. Wick, G., H. Perschinka, and Q. Xu. 1999. Autoimmunity and atherosclerosis. Am. Heart J. 138: S444-S449. (Pubitemid 29523230)
31. Kol, A., G. K. Sukhova, A. H. Lichtman, and P. Libby. 1998. Chlamydial heat shock protein 60 localizes in human atheroma and regulates macrophage tumor necrosis factor-alpha and matrix metalloproteinase expression. Circulation 98: 300-307. (Pubitemid 28348051)
32. Belay, T., F. O. Eko, G. A. Ananaba, S. Bowers, T. Moore, D. Lyn, and J. U. Igietseme. 2002. Chemokine and chemokine receptor dynamics during genital chlamydial infection. Infect. Immun. 70: 844-850. (Pubitemid 34083848)
33. Fong, I. W., B. Chiu, E. Viira, D. Jang, and J. B. Mahony. 1999. De novo induction of atherosclerosis by Chlamydia pneumoniae in a rabbit model. Infect. Immun. 67: 6048-6055. (Pubitemid 29508136)
34. Muhlestein, J. B., J. L. Anderson, E. H. Hammond, L. Zhao, S. Trehan, E. P. Schwobe, and J. F. Carlquist. 1998. Infection with Chlamydia pneumoniae accelerates the development of atherosclerosis and treatment with azithromycin prevents it in a rabbit model. Circulation 97: 633-636. (Pubitemid 28090954)
35. Jackson, D. J., J. P. Rakwar, B. Chohan, K. Mandaliya, J. J. Bwayo, J. O. Ndinya- Achola, N. J. Nagelkerke, J. K. Kreiss, and S. Moses. 1997. Urethral infection in a workplace population of East African men: Evaluation of strategies for screening and management. J. Infect. Dis. 175: 833-838. (Pubitemid 27142956)
36. Hu, H., G. N. Pierce, and G. Zhong. 1999. The atherogenic effects of chlamydia are dependent on serum cholesterol and specific to Chlamydia pneumoniae. J. Clin. Invest. 103: 747-753. (Pubitemid 29122429)
37. Moazed, T. C., L. A. Campbell, M. E. Rosenfeld, J. T. Grayston, and C. C. Kuo. 1999. Chlamydia pneumoniae infection accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice. J. Infect. Dis. 180: 238-241. (Pubitemid 29293945)
38. Tsukamoto, K., M. Kinoshita, K. Kojima, Y. Mikuni, M. Kudo, M. Mori, M. Fujita, E. Horie, N. Shimazu, and T. Teramoto. 2002. Synergically increased expression of CD36, CLA-1 and CD68, but not of SR-A and LOX-1, with the progression to foam cells from macrophages. J. Atheroscler. Thromb. 9: 57-64.
39. Boullier, A., D. A. Bird, M. K. Chang, E. A. Dennis, P. Friedman, K. Gillotre- Taylor, S. Horkko,W. Palinski, O. Quehenberger, P. Shaw, et al. 2001. Scavenger receptors, oxidized LDL, and atherosclerosis. Ann. N. Y. Acad. Sci. 947: 214- 222, discussion 222-213.
40. Faure, E., L. Thomas, H. Xu, A. Medvedev, O. Equils, and M. Arditi. 2001. Bacterial lipopolysaccharide and IFN-gamma induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: Role of NF-kappa B activation. J. Immunol. 166: 2018-2024. (Pubitemid 32114690)
41. Sakurai, K., and T. Sawamura. 2003. Stress and vascular responses: Endothelial dysfunction via lectin-like oxidized low-density lipoprotein receptor-1: Close relationships with oxidative stress. J. Pharmacol. Sci. 91: 182-186. (Pubitemid 36575574)
42. Cominacini, L., A. F. Pasini, U. Garbin, A. Davoli, M. L. Tosetti, M. Campagnola, A. Rigoni, A. M. Pastorino, V. Lo Cascio, and T. Sawamura. 2000. Oxidized low density lipoprotein (ox-LDL) binding to ox-LDL receptor-1 in endothelial cells induces the activation of NF-kappaB through an increased production of intracellular reactive oxygen species. J. Biol. Chem. 275: 12633-12638. (Pubitemid 30241412)
43. Cominacini, L., A. Rigoni, A. F. Pasini, U. Garbin, A. Davoli, M. Campagnola, A. M. Pastorino, V. Lo Cascio, and T. Sawamura. 2001. The binding of oxidized low density lipoprotein (ox-LDL) to ox-LDL receptor-1 reduces the intracellular concentration of nitric oxide in endothelial cells through an increased production of superoxide. J. Biol. Chem. 276: 13750-13755.
44. Li, D. Y., H. J. Chen, and J. L. Mehta. 2001. Statins inhibit oxidized-LDLmediated LOX-1 expression, uptake of oxidized-LDL and reduction in PKB phosphorylation. Cardiovasc. Res. 52: 130-135. (Pubitemid 32835246)
45. Vergnani, L., S. Hatrik, F. Ricci, A. Passaro, N. Manzoli, G. Zuliani, V. Brovkovych, R. Fellin, and T. Malinski. 2000. Effect of native and oxidized low-density lipoprotein on endothelial nitric oxide and superoxide production: Key role of L-arginine availability. Circulation 101: 1261-1266. (Pubitemid 30158613)
46. Nagase, M., K. Ando, T. Nagase, S. Kaname, T. Sawamura, and T. Fujita. 2001. Redox-sensitive regulation of lox-1 gene expression in vascular endothelium. Biochem. Biophys. Res. Commun. 281: 720-725. (Pubitemid 32917860)
47. Li, L., T. Sawamura, and G. Renier. 2004. Glucose enhances human macrophage LOX-1 expression: Role for LOX-1 in glucose-induced macrophage foam cell formation. Circ. Res. 94: 892-901. (Pubitemid 38490066)