Toll-like receptor-2 plays a fundamental role in periodontal bacteria-accelerated abdominal aortic aneurysms

Circulation Journal

Volumn 77, Issue 6, 2013, Pages 1565-1573

  Aoyama, Norio ^a   Suzuki, Jun ichi ^a,b   Ogawa, Masahito ^a,b   Watanabe, Ryo ^a   Kobayashi, Naho ^a   Hanatani, Tomoya ^a   Ashigaki, Norihiko ^a   Sekinishi, Asuka ^a   Izumi, Yuichi ^a   Isobe, Mitsuaki ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Aneurysm; Inflammation; Matrix metalloproteinase; Porphyromonas gingivalis; Toll like receptor

Indexed keywords

C REACTIVE PROTEIN; GELATINASE A; GELATINASE B; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; VIRULENCE FACTOR;

ABDOMINAL AORTA; ANEURYSM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; AORTA; AORTA ANEURYSM; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; CONTROLLED STUDY; DISEASE COURSE; ELASTIC FIBER; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOPATHOLOGY; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PERIODONTAL DISEASE; POLYMERASE CHAIN REACTION; PORPHYROMONAS GINGIVALIS; PROTEIN EXPRESSION; WESTERN BLOTTING;

ANIMALS; AORTA, ABDOMINAL; AORTIC ANEURYSM, ABDOMINAL; BACTEROIDACEAE INFECTIONS; HUMANS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; PERIODONTIUM; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84878245532     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-12-1191     Document Type: Article

References (45)

1. Ernst CB. Abdominal aortic aneurysm. N Engl J Med 1993; 328: 1167-1172.
2. Alcorn HG, Wolfson SK, Sutton-Tyrrell K, Kuller LH, O'Leary D. Risk factors for abdominal aortic aneurysms in older adults enrolled in the cardiovascular health study. Arterioscler Thromb Vasc Biol 1996; 16: 963-970.
3. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, Baxter BT. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest 2002; 110: 625-632.
4. Freestone T, Turner RJ, Coady A, Higman DJ, Greenhalgh RM, Powell JT. Inflammation and matrix metalloproteinases in the enlarging abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol 1995; 15: 1145-1151.
5. Davis V, Persidskaia R, Baca-Regen L, Itoh Y, Nagase H, Persidsky Y, et al. Matrix metalloproteinase-2 production and its binding to the matrix are increased in abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 1998; 18: 1625-1633.
6. Choi BK, Jung JH, Suh HY, Yoo YJ, Cho KS, Chai JK, et al. Activation of matrix metalloproteinase-2 by a novel oral spirochetal species Treponema lecithinolyticum. J Periodontol 2001; 72: 1594-1600.
7. Oliver RC, Brown LJ, Loe H. Periodontal diseases in the united states population. J Periodontol 1998; 69: 269-278.
8. Salvi GE, Lang NP. Host response modulation in the management of periodontal diseases. J Clin Periodontol 2005; 32(SUPPL. 6): 108-129.
9. Moreillon P, Que YA. Infective endocarditis. Lancet 2004; 363: 139-149.
10. Li X, Kolltveit KM, Tronstad L, Olsen I. Systemic diseases caused by oral infection. Clin Microbiol Rev 2000; 13: 547-558.
11. Hansson GK, Libby P, Schonbeck U, Yan ZQ. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ Res 2002; 91: 281-291.
12. Kurihara N, Inoue Y, Iwai T, Umeda M, Huang Y, Ishikawa I. Detection and localization of periodontopathic bacteria in abdominal aortic aneurysms. Eur J Vasc Endovasc Surg 2004; 28: 553-558.
13. Kumar H, Kawai T, Akira S. Toll-like receptors and innate immunity. Biochem Biophys Res Commun 2009; 388: 621-625.
14. Lien E, Ingalls RR. Toll-like receptors. Crit Care Med 2002; 30: S1-S11.
15. Gibson FC, Hong C, Chou HH, Yumoto H, Chen J, Lien E, et al. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 2004; 109: 2801-2806.
16. Shuto T, Imasato A, Jono H, Sakai A, Xu H, Watanabe T, et al. Glu-cocorticoids synergistically enhance nontypeable haemophilus infu-enzae-induced toll-like receptor 2 expression via a negative crosstalk with p38 map kinase. J Biol Chem 2002; 277: 17263-17270.
17. 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.
18. Kikkert R, Laine ML, Aarden LA, van Winkelhoff AJ. Activation of toll-like receptors 2 and 4 by gram-negative periodontal bacteria. Oral Microbiol Immunol 2007; 22: 145-151.
19. Martin M, Schifferle RE, Cuesta N, Vogel SN, Katz J, Michalek SM. Role of the phosphatidylinositol 3 kinase-Akt pathway in the regulation of IL-10 and IL-12 by Porphyromonas gingivalis lipopolysac-charide. J Immunol 2003; 171: 717-725.
20. Genco CA, Arko RJ. Animal chamber models for study of host-parasite interactions. Methods Enzymol 1994; 235: 120-140.
21. Houri-Haddad Y, Itzchaki O, Ben-Nathan D, Shapira L. The effect of chronic emotional stress on the humoral immune response to Por-phyromonas gingivalis in mice. J Periodontal Res 2003; 38: 204-209.
22. Aoyama N, Suzuki J, Wang D, Ogawa M, Kobayashi N, Hanatani T, et al. Porphyromonas gingivalis promotes murine abdominal aortic aneurysms via matrix metalloproteinase-2 induction. J Periodontal Res 2011; 46: 176-183.
23. Ogawa M, Suzuki J, Hishikari K, Takayama K, Tanaka H, Isobe M. Clarithromycin attenuates acute and chronic rejection via matrix me-talloproteinase suppression in murine cardiac transplantation. J Am Coll Cardiol 2008; 51: 1977-1985.
24. Kuula H, Salo T, Pirila E, Tuomainen AM, Jauhiainen M, Uitto VJ, et al. Local and systemic responses in matrix metalloproteinase 8-deficient mice during Porphyromonas gingivalis-induced periodontitis. Infect Immun 2009; 77: 850-859.
25. Ashimoto A, Chen C, Bakker I, Slots J. Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 1996; 11: 266-273.
26. Suzuki J, Ogawa M, Futamatsu H, Kosuge H, Tanaka H, Isobe M. A cyclooxygenase-2 inhibitor alters Th1/Th2 cytokine balance and suppresses autoimmune myocarditis in rats. J Mol Cell Cardiol 2006; 40: 688-695.
27. Mattila KJ, Nieminen MS, Valtonen VV, Rasi VP, Kesaniemi YA, Syrjala SL, et al. Association between dental health and acute myocardial infarction. BMJ 1989; 298: 779-781.
28. Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S. Periodontal disease and cardiovascular disease. J Periodontol 1996; 67: 1123-1137.
29. Sakurai K, Wang D, Suzuki J, Umeda M, Nagasawa T, Izumi Y, et al. High incidence of Actinobacillus actinomycetemcomitans infection in acute coronary syndrome. Int Heart J 2007; 48: 663-675.
30. Mendez MV, Scott T, LaMorte W, Vokonas P, Menzoian JO, Garcia R. An association between periodontal disease and peripheral vascular disease. Am J Surg 1998; 176: 153-157.
31. Dietrich T, Jimenez M, Krall Kaye EA, Vokonas PS, Garcia RI. Age-dependent associations between chronic periodontitis/edentulism and risk of coronary heart disease. Circulation 2008; 117: 1668-1674.
32. Chiu B. Multiple infections in carotid atherosclerotic plaques. Am Heart J 1999; 138: S534-S536.
33. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
34. Hajishengallis G, Wang M, Liang S. Induction of distinct TLR2-me-diated proinfammatory and proadhesive signaling pathways in response to Porphyromonas gingivalis fmbriae. J Immunol 2009; 182: 6690-6696.
35. Spiller S, Elson G, Ferstl R, Dreher S, Mueller T, Freudenberg M, et al. TLR4-induced IFN-gamma production increases TLR2 sensitivity and drives gram-negative sepsis in mice. J Exp Med 2008; 205: 1747-1754.
36. Madan M, Amar S. Toll-like receptor-2 mediates diet and/or pathogen associated atherosclerosis: Proteomic findings. PLoS One 2008; 3: e3204 (accessed September 19, 2012).
37. Monaco C, Gregan SM, Navin TJ, Foxwell BM, Davies AH, Feldmann M. Toll-like receptor-2 mediates inflammation and matrix degradation in human atherosclerosis. Circulation 2009; 120: 2462-2469.
38. Hajishengallis G, Wang M, Bagby GJ, Nelson S. Importance of TLR2 in early innate immune response to acute pulmonary infection with Porphyromonas gingivalis in mice. J Immunol 2008; 181: 4141-4149.
39. Burns E, Bachrach G, Shapira L, Nussbaum G. Cutting edge: TLR2 is required for the innate response to Porphyromonas gingivalis: Activation leads to bacterial persistence and TLR2 deficiency attenuates induced alveolar bone resorption. J Immunol 2006; 177: 8296-8300.
40. Lockhart PB, Bolger AF, Papapanou PN, Osinbowale O, Trevisan M, Levison ME, et al. Periodontal disease and atherosclerotic vascular disease: Does the evidence support an independent association? A scientific statement from the american heart association. Circulation 2012; 125: 2520-2544.
41. Burns E, Eliyahu T, Uematsu S, Akira S, Nussbaum G. TLR2-depen-dent inflammatory response to Porphyromonas gingivalis is MyD88 independent, whereas MyD88 is required to clear infection. J Immunol 2010; 184: 1455-1462.
42. Bobryshev YV, Lord RS, Parsson H. Immunophenotypic analysis of the aortic aneurysm wall suggests that vascular dendritic cells are involved in immune responses. Cardiovasc Surg 1998; 6: 240-249.
43. Kojima T, Yano K, Ishikawa I. Relationship between serum antibody levels and subgingival colonization of Porphyromonas gingivalis in patients with various types of periodontitis. J Periodontol 1997; 68: 618-625.
44. Yamamoto K, Fukui T, Matsuyama S, Tabata M, Aramoto H, Takanashi S. Prior cardiac and thoracic aortic surgery as a complication risk factor for abdominal aortic aneurysm repair. Circ J 2012; 76: 1380-1384.
45. Kodama A, Narita H, Kobayashi M, Yamamoto K, Komori K. Usefulness of POSSUM physiological score for the estimation of morbidity and mortality risk after elective abdominal aortic aneurysm repair in Japan. Circ J 2011; 75: 550-556.