Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice

Circulation

Volumn 109, Issue 22, 2004, Pages 2801-2806

  Gibson III, Frank C ^a   Hong, Charlie ^b   Chou, Hsin Hua ^a,c   Yumoto, Hiromichi ^a   Chen, Jiqiu ^d   Lien, Egil ^e,f   Wong, Jodie ^b   Genco, Caroline Attardo ^a,b,g,h  

^a BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^b BOSTON UNIVERSITY   (United States)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^f UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^g BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h EBRC   (United States)

Author keywords

Atherosclerosis; Endothelium; Infection; Inflammation; Receptors

Indexed keywords

APOLIPOPROTEIN E; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN RECOGNITION; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR DISEASE; CHRONIC INFLAMMATION; CONTROLLED STUDY; DISEASE ACTIVITY; FIMBRIA; IMMUNE RESPONSE; IMMUNIZATION; MOUSE; NONHUMAN; PERIODONTAL DISEASE; POLYMERASE CHAIN REACTION; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL;

ANIMALS; APOLIPOPROTEINS E; ARTERIOSCLEROSIS; BACTEROIDACEAE INFECTIONS; CELLS, CULTURED; FIMBRIAE, BACTERIAL; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RECEPTORS, CELL SURFACE; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS; UP-REGULATION;

EID: 2942544238     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000129769.17895.F0     Document Type: Article

References (49)

1. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
2. Libby P. What have we learned about the biology of atherosclerosis? The role of inflammation. Am J Cardiol. 2001;88:3J-6J.
3. Zhang SH, Reddick RL, Piedrahita JA, et al. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 1992;258:468-471.
4. Plump AS, Smith JD, Hayek T, et al. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343-353.
5. Mach F, Sauty A, Iarossi AS, et al. Differential expression of three T lymphocyte-activating CXC chemokines by human atheroma-associated cells. J Clin Invest. 1999;104:1041-1050.
6. Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem. 1997;272:20963-20966.
7. Gupta S, Pablo AM, Jiang X, et al. IFN-gamma potentiates atherosclerosis in apoE knock-out mice. J Clin Invest. 1997;99:2752-2761.
8. Liuzzo G, Biasucci LM, Gallimore JR, et al. The prognostic value of C-reactive protein and serum amyloid a protein in severe unstable angina. N Engl J Med. 1994;331:417-424.
9. Cybulsky MI, Iiyama K, Li H, et al. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest. 2001;107:1255-1262.
10. Xu XH, Shah PK, Faure E, et al. Toll-like receptor-4 is expressed by macrophages in murine and human lipid-rich atherosclerotic plaques and upregulated by oxidized LDL. Circulation. 2001;104:3103-3108.
11. Lien E, Ingalls RR. Toll-like receptors. Crit Care Med. 2002;30:S1-S11.
12. Shuto T, Imasato A, Jono H, et al. Glucocorticoids synergistically enhance nontypeable Haemophilus influenzae-induced Toll-like receptor 2 expression via a negative cross-talk with p38 MAP kinase. J Biol Chem. 2002;277:17263-17270.
13. Wang T, Lafuse WP, Zwilling BS. Regulation of toll-like receptor 2 expression by macrophages following Mycobacterium avium infection. J Immunol. 2000;165:6308-6313.
14. Hansson GK, Libby P, Schonbeck U, et al. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ Res. 2002;91:281-291.
15. Epstein SE, Zhou YF, Zhu J. Potential role of cytomegalovirus in the pathogenesis of restenosis and atherosclerosis. Am Heart J. 1999;138:S476-S478.
16. Mach F, Sukhova GK, Michetti M, et al. Influence of Helicobacter pylori infection during atherogenesis in vivo in mice. Circ Res. 2002;90:E1-E4.
17. Beck JD, Elter JR, Heiss G, et al. Relationship of periodontal disease to carotid artery intima-media wall thickness: the atherosclerosis risk in communities (ARIC) study. Arterioscler Thromb Vasc Biol. 2001;21:1816-1822.
18. Wu T, Trevisan M, Genco RJ, et al. Periodontal disease and risk of cerebrovascular disease: the first National Health and Nutrition Examination Survey and its follow-up study. Arch Intern Med. 2000;160:2749-2755.
19. Wright SD, Burton C, Hernandez M, et al. Infectious agents are not necessary for murine atherogenesis. J Exp Med. 2000;191:1437-1442.
20. Hujoel PP, Drangsholt M, Spiekerman C, et al. Periodontal disease and coronary heart disease risk. JAMA. 2000;284:1406-1410.
21. Beck JD, Offenbacher S, Williams R, et al. Periodontitis: a risk factor for coronary heart disease? Ann Periodontol. 1998;3:127-141.
22. Armitage GC. Periodontal diseases: diagnosis. Ann Periodontol. 1996;1:37-215.
23. Oliver RC, Brown LJ, Loe H. Periodontal diseases in the United States population. J Periodontol. 1998;69:269-278.
24. Holt SC, Ebersole J, Felton J, et al. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science. 1988;239:55-57.
25. Griffen AL, Becker MR, Lyons SR, et al. Prevalence of Porphyromonas gingivalis and periodontal health status. J Clin Microbiol. 1998;36:3239-3242.
26. Haraszthy VI, Zambon JJ, Trevisan M, et al. Identification of periodontal pathogens in atheromatous plaques. J Periodontol. 2000;71:1554-1560.
27. Messini M, Skourti I, Markopulos E, et al. Bacteremia after dental treatment in mentally handicapped people. J Clin Periodontol. 1999;26:469-473.
28. Lee SC, Fung CP, Lin CC, et al. Porphyromonas gingivalis bacteremia and subhepatic abscess after renal transplantation: a case report. J Microbiol Immunol Infect. 1999;32:213-216.
29. Li L, Messas E, Batista EL Jr, et al. Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation. 2002;105:861-867.
30. Lalla E, Lamster IB, Hofmann MA, et al. Oral infection with a periodontal pathogen accelerates early atherosclerosis in apolipoprotein E-null mice. Arterioscler Thromb Vasc Biol. 2003;23:1405-1411.
31. Holt SC, Kesavalu L, Walker S, et al. Virulence factors of Porphyromonas gingivalis. Periodontology. 2000;20:168-238.
32. Deshpande RG, Khan MB, Genco CA. Invasion of aortic and heart endothelial cells by Porphyromonas gingivalis. Infect Immun. 1998;66:5337-5343.
33. Khlgatian M, Nassar H, Chou HH, et al. Fimbria-dependent activation of cell adhesion molecule expression in Porphyromonas gingivalis-infected endothelial cells. Infect Immun. 2002;70:257-267.
34. Nassar H, Chou HH, Khlgatian M, et al. Role for fimbriae and lysine-specific cysteine proteinase gingipain K in expression of interleukin-8 and monocyte chemoattractant protein in Porphyromonas gingivalis-infected endothelial cells. Infect Immun. 2002;70:268-276.
35. Malek R, Fisher JG, Caleca A, et al. Inactivation of the Porphyromonas gingivalis fimA gene blocks periodontal damage in gnotobiotic rats. J Bacteriol. 1994;176:1052-1059.
36. Gibson FC III, Genco CA. Prevention of Porphyromonas gingivalis-induced oral bone loss following immunization with gingipain R1. Infect Immun. 2001;69:7959-7963.
37. Garcia L, Tercero JC, Legido B, et al. Rapid detection of Actinobacillus actinomycetemcomitans, Prevotella intermedia and Porphyromonas gingivalis by multiplex PCR. J Periodontal Res. 1998;33:59-64.
38. Nakashima Y, Plump AS, Raines EW, et al. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 1994;14:133-140.
39. Moazed TC, Campbell LA, Rosenfeld ME, et al. Chlamydia pneumoniae infection accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice. J Infect Dis. 1999;180:238-241.
40. Shah PK, Nilsson J, Kaul S, et al. Effects of recombinant apolipoprotein A-I(Milano) on aortic atherosclerosis in apolipoprotein E-deficient mice. Circulation. 1998;97:780-785.
41. Lee JY, Sojar HT, Amano A, et al. Purification of major fimbrial proteins of Porphyromonas gingivalis. Protein Exp Purif. 1995;6:496-500.
42. Qiao JH, Xie PZ, Fishbein MC, et al. Pathology of atheromatous lesions in inbred and genetically engineered mice: genetic determination of arterial calcification. Arterioscler Thromb. 1994;14:1480-1497.
43. Tangirala RK, Rubin EM, Palinski W. Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptor-deficient and apolipoprotein E-deficient mice. J Lipid Res. 1995; 36:2320-2328.
44. 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.
45. Bainbridge BW, Darveau RP. Porphyromonas gingivalis lipopolysaccharide: an unusual pattern recognition receptor ligand for the innate host defense system. Acta Odontol Scand. 2001;59:131-138.
46. Hajishengallis G, Martin M, Sojar HT, et al. Dependence of bacterial protein adhesins on toll-like receptors for proinflammatory cytokine induction. Clin Diagn Lab Immunol. 2002;9:403-411.
47. Asai Y, Ohyama Y, Gen K, et al. Bacterial fimbriae and their peptides activate human gingival epithelial cells through Toll-like receptor 2. Infect Immun. 2001;69:7387-7395.
48. Cario E, Podolsky DK. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun. 2000;68:7010-7017.
49. Abel B, Thieblemont N, Quesniaux VJ, et al. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice. J Immunol. 2002;169:3155-3162.