Chronic oral infection with porphyromonas gingivalis accelerates atheroma formation by shifting the lipid profile

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Maekawa, Tomoki ^a,b   Takahashi, Naoki ^a,b   Tabeta, Koichi ^a   Aoki, Yukari ^a,b   Miyashita, Hirotaka ^a,b   Miyauchi, Sayuri ^a,b   Miyazawa, Haruna ^a,b   Nakajima, Takako ^a,c   Yamazaki, Kazuhisa ^a,b  

^a NIIGATA UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^c NIIGATA UNIVERSITY MEDICAL AND DENTAL HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; BACTERIUM LIPOPOLYSACCHARIDE; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIVER X RECEPTOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; VERY LOW DENSITY LIPOPROTEIN; LIPID;

ALVEOLAR BONE; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; ARTICLE; ATHEROGENESIS; ATHEROMA; ATHEROSCLEROSIS; BACTERIUM CULTURE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL TRANSPORT; CHRONIC PERIODONTITIS; CONTROLLED STUDY; GENE EXPRESSION; LIPID BLOOD LEVEL; MALE; MOUSE; MOUTH INFECTION; NONHUMAN; OSTEOLYSIS; PERITONEUM MACROPHAGE; PORPHYROMONAS GINGIVALIS; ANIMAL; ATHEROSCLEROTIC PLAQUE; BLOOD; C57BL MOUSE; GENE EXPRESSION PROFILING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOUTH DISEASE; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); MUS; PORPHYROMONAS GINGIVALIS;

ANIMALS; GENE EXPRESSION PROFILING; LIPIDS; MICE; MICE, INBRED C57BL; MOUTH DISEASES; PLAQUE, ATHEROSCLEROTIC; PORPHYROMONAS GINGIVALIS;

EID: 79956289191     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020240     Document Type: Article

References (40)

1. O'Connor S, Taylor C, Campbell LA, Epstein S, Libby P, (2001) Potential infectious etiologies of atherosclerosis: a multifactorial perspective. Emerg Infect Dis 7: 780-788.
2. Chiu B, Viira E, Tucker W, Fong IW, (1997) Chlamydia pneumoniae, cytomegalovirus, and herpes simplex virus in atherosclerosis of carotid artery. Circulation 96: 2144-2148.
3. Mendall MA, Goggin PM, Molineaux N, Levy J, Toosy T, et al. (1994) Relation of Helicobacter pylori infection and coronary heart disease. Br Heart J 71: 437-439.
4. Bahekar AA, Singh S, Saha S, Molnar J, Arora R, (2007) The prevalence and incidence of coronary heart disease is significantly increased in periodontitis: a meta-analysis. Am Heart J 154: 830-837.
5. Humphrey LL, Fu R, Buckley DI, Freeman M, Helfand M, (2008) Periodontal disease and coronary heart disease incidence: a systematic review and meta-analysis. J Gen Intern Med 23: 2079-2086.
6. Epstein SE, Zhou YF, Zhu J, (1999) Infection and atherosclerosis: emerging mechanistic paradigms. Circulation 100: e20-28.
7. Buhlin K, Hultin M, Norderyd O, Persson L, Pockley AG, et al. (2009) Periodontal treatment influences risk markers for atherosclerosis in patients with severe periodontitis. Atherosclerosis 206: 518-522.
8. Nakajima T, Honda T, Domon H, Okui T, Kajita K, et al. (2010) Periodontitis-associated up-regulation of systemic inflammatory mediator level may increase the risk of coronary heart disease. J Periodont Res 45: 116-122.
9. Gibson FC 3rd, Hong C, Chou HH, Yumoto H, Chen J, et al. (2004) Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 109: 2801-2806.
10. Lalla E, Lamster IB, Hofmann MA, Bucciarelli L, Jerud AP, et al. (2003) Oral infection with a periodontal pathogen accelerates early atherosclerosis in apolipoprotein E-null mice. Arterioscler Thromb Vasc Biol 23: 1405-1411.
11. Li L, Messas E, Batista EL Jr, Levine RA, Amar S, (2002) Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation 105: 861-867.
12. Wilson W, Taubert KA, Gewitz M, Lockhart PB, Baddour LM, et al. (2007) Prevention of infective endocarditis: guidelines from the American Heart Association: a guideline from the American Heart Association Rheumatic Fever, Endocarditis, and Kawasaki Disease Committee, Council on Cardiovascular Disease in the Young, and the Council on Clinical Cardiology, Council on Cardiovascular Surgery and Anesthesia, and the Quality of Care and Outcomes Research Interdisciplinary Working Group. Circulation 116: 1736-1754.
13. D'Aiuto F, Parkar M, Nibali L, Suvan J, Lessem J, et al. (2006) Periodontal infections cause changes in traditional and novel cardiovascular risk factors: results from a randomized controlled clinical trial. Am Heart J 151: 977-984.
14. Ramirez-Tortosa MC, Quiles JL, Battino M, Granados S, Morillo JM, et al. (2010) Periodontitis is associated with altered plasma fatty acids and cardiovascular risk markers. Nutr Metab Cardiovasc Dis 20: 133-139.
15. Rufail ML, Schenkein HA, Koertge TE, Best AM, Barbour SE, et al. (2007) Atherogenic lipoprotein parameters in patients with aggressive periodontitis. J Periodont Res 42: 495-502.
16. Seymour GJ, Gemmell E, Reinhardt RA, Eastcott J, Taubman MA, (1993) Immunopathogenesis of chronic inflammatory periodontal disease: cellular and molecular mechanisms. J Periodont Res 28: 478-486.
17. Blessing E, Campbell LA, Rosenfeld ME, Chough N, Kuo CC, (2001) Chlamydia pneumoniae infection accelerates hyperlipidemia induced atherosclerotic lesion development in C57BL/6J mice. Atherosclerosis 158: 13-17.
18. Maekawa T, Takahashi N, Honda T, Yonezawa D, Miyashita H, et al. (2009) Porphyromonas gingivalis antigens and interleukin-6 stimulate the production of monocyte chemoattractant protein-1 via the upregulation of early growth response-1 transcription in human coronary artery endothelial cells. J Vasc Res 47: 346-354.
19. Liao H, Langmann T, Schmitz G, Zhu Y, (2002) Native LDL upregulation of ATP-binding cassette transporter-1 in human vascular endothelial cells. Arterioscler Thromb Vasc Biol 22: 127-132.
20. Norata GD, Ongari M, Uboldi P, Pellegatta F, Catapano AL, (2005) Liver X receptor and retinoic X receptor agonists modulate the expression of genes involved in lipid metabolism in human endothelial cells. Int J Mol Med 16: 717-722.
21. Tang C, Oram JF, (2009) The cell cholesterol exporter ABCA1 as a protector from cardiovascular disease and diabetes. Biochim Biophys Acta 1791: 563-572.
22. Castrillo A, Joseph SB, Vaidya SA, Haberland M, Fogelman AM, et al. (2003) Crosstalk between LXR and toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol Cell 12: 805-816.
23. Domon H, Honda T, Oda T, Yoshie H, Yamazaki K, (2008) Early and preferential induction of IL-1 receptor-associated kinase-M in THP-1 cells by LPS derived from Porphyromonas gingivalis. J Leukoc Biol 83: 672-679.
24. Zelcer N, Hong C, Boyadjian R, Tontonoz P, (2009) LXR regulates cholesterol uptake through Idol-dependent ubiquitination of the LDL receptor. Science 325: 100-104.
25. Li L, Thompson PA, Kitchens RL, (2008) Infection induces a positive acute phase apolipoprotein E response from a negative acute phase gene: role of hepatic LDL receptors. J Lipid Res 49: 1782-1793.
26. Lambert G, Charlton F, Rye KA, Piper DE, (2009) Molecular basis of PCSK9 function. Atherosclerosis 203: 1-7.
27. Feingold KR, Moser AH, Shigenaga JK, Patzek SM, Grunfeld C, (2008) Inflammation stimulates the expression of PCSK9. Biochemical and biophysical research communications 374: 341-344.
28. Frikke-Schmidt R, Nordestgaard BG, Stene MC, Sethi AA, Remaley AT, et al. (2008) Association of loss-of-function mutations in the ABCA1 gene with high-density lipoprotein cholesterol levels and risk of ischemic heart disease. JAMA 299: 2524-2532.
29. Gonzalez-Baro MR, Lewin TM, Coleman RA, (2007) Regulation of triglyceride metabolism. II. Function of mitochondrial GPAT1 in the regulation of triacylglycerol biosynthesis and insulin action. Am J Physiol Gastrointest Liver Physiol 292: G1195-1199.
30. Schultz JR, Tu H, Luk A, Repa JJ, Medina JC, et al. (2000) Role of LXRs in control of lipogenesis. Genes Dev 14: 2831-2838.
31. Chen G, Liang G, Ou J, Goldstein JL, Brown MS, (2004) Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc Natl Acad Sci U S A 101: 11245-11250.
32. Shimazaki Y, Saito T, Yonemoto K, Kiyohara Y, Iida M, et al. (2007) Relationship of metabolic syndrome to periodontal disease in Japanese women: the Hisayama Study. J Dent Res 86: 271-275.
33. Yamazaki K, Honda T, Domon H, Okui T, Kajita K, et al. (2007) Relationship of periodontal infection to serum antibody levels to periodontopathic bacteria and inflammatory markers in periodontitis patients with coronary heart disease. Clin Exp Immunol 149: 445-452.
34. Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, et al. (2004) Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res 45: 1169-1196.
35. Matsushima Y, Hayashi S, Tachibana M, (1999) Spontaneously hyperlipidemic (SHL) mice: Japanese wild mice with apolipoprotein E deficiency. Mamm Genome 10: 352-357.
36. Matsushima Y, Sakurai T, Ohoka A, Ohnuki T, Tada N, et al. (2001) Four strains of spontaneously hyperlipidemic (SHL) mice: phenotypic distinctions determined by genetic backgrounds. J Atheroscler Thromb 8: 71-79.
37. Baker PJ, Evans RT, Roopenian DC, (1994) Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 39: 1035-1040.
38. Ashimoto A, Chen C, Bakker I, Slots J, (1996) Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 11: 266-273.
39. Paigen B, Morrow A, Holmes PA, Mitchell D, Williams RA, (1987) Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis 68: 231-240.
40. Venkateswaran A, Laffitte BA, Joseph SB, Mak PA, Wilpitz DC, et al. (2000) Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXRα. Proc Natl Acad Sci U S A 97: 12097-12102.