Porphyromonas gingivalis Strain Specific Interactions with Human Coronary Artery Endothelial Cells: A Comparative Study

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Rodrigues, Paulo H ^a,c   Reyes, Leticia ^a   Chadda, Amandeep S ^a   Bélanger, Myriam ^a,d   Wallet, Shannon M ^a   Akin, Debra ^b   Dunn, William ^b   Progulske Fox, Ann ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 12P40; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; SELECTIN; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; AUTOPHAGY; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL ACTIVATION; CELL CULTURE; COMPARATIVE STUDY; CONTROLLED STUDY; CORONARY ARTERY; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATION; NONHUMAN; PORPHYROMONAS GINGIVALIS; STRAIN DIFFERENCE;

EID: 84871587268     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052606     Document Type: Article

References (74)

1. Nakano K, Wada K, Nomura R, Nemoto H, Inaba H, et al. (2011) Characterization of aortic aneurysms in cardiovascular disease patients harboring Porphyromonas gingivalis. Oral Diseases 17: 370-378.
2. Wada K, Kamisaki Y, (2010) Roles of oral bacteria in cardiovascular diseases-from molecular mechanisms to clinical cases: Involvement of Porphyromonas gingivalis in the development of human aortic aneurysm. J Pharmacol Sci 113: 115-119.
3. Kebschull M, Demmer RT, Papapanou PN, (2010) "Gum bug, leave my heart alone!"-epidemiologic and mechanistic evidence linking periodontal infections and atherosclerosis. J Dent Res 89: 879-902.
4. Hayashi C, Gudino CV, Gibson FC III, Genco CA, (2010) Review: Pathogen-induced inflammation at sites distant from oral infection: bacterial persistence and induction of cell-specific innate immune inflammatory pathways. Mol Oral Microbiol 25: 305-316.
5. Carrion J, Scisci E, Miles B, Sabino GJ, Zeituni AE, et al. (2012) Microbial Carriage State of Peripheral Blood Dendritic Cells (DCs) in Chronic Periodontitis Influences DC Differentiation, Atherogenic Potential. J Immunol 189: 3178-3187.
6. Castillo DM, Sanchez-Beltran MC, Castellanos JE, Sanz I, Mayorga-Fayad I, et al. (2011) Detection of specific periodontal microorganisms from bacteraemia samples after periodontal therapy using molecular-based diagnostics. J Clin Periodontol 38: 418-427.
7. Kozarov EV, Dorn BR, Shelburne CE, Dunn WA Jr, Progulske-Fox A, (2005) Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler Thromb Vasc Biol 25: e17-18.
8. Padilla C, Lobos O, Hubert E, Gonzalez C, Matus S, et al. (2006) Periodontal pathogens in atheromatous plaques isolated from patients with chronic periodontitis. J Periodontal Res 41: 350-353.
9. Zaremba M, Gorska R, Suwalski P, Kowalski J, (2007) Evaluation of the incidence of periodontitis-associated bacteria in the atherosclerotic plaque of coronary blood vessels. J Periodontol 78: 322-327.
10. Kozarov E, Sweier D, Shelburne C, Progulske-Fox A, Lopatin D, (2006) Detection of bacterial DNA in atheromatous plaques by quantitative PCR. Microbes Infect 8: 687-693.
11. Mahendra J, Mahendra L, Kurian VM, Jaishankar K, Mythilli R, (2010) 16S rRNA-based detection of oral pathogens in coronary atherosclerotic plaque. Indian J Dent Res 21: 248-252.
12. Marcelino SL, Gaetti-Jardim E Jr, Nakano V, Canonico LA, Nunes FD, et al. (2010) Presence of periodontopathic bacteria in coronary arteries from patients with chronic periodontitis. Anaerobe 16: 629-632.
13. Figuero E, Sanchez-Beltran M, Cuesta-Frechoso S, Tejerina JM, del Castro JA, et al. (2011) Detection of periodontal bacteria in atheromatous plaque by nested polymerase chain reaction. J Periodontol 82: 1469-1477.
14. Rafferty B, Jonsson D, Kalachikov S, Demmer RT, Nowygrod R, et al. (2011) Impact of monocytic cells on recovery of uncultivable bacteria from atherosclerotic lesions. J Intern Med 270: 273-280.
15. Ohki T, Itabashi Y, Kohno T, Yoshizawa A, Nishikubo S, et al. (2012) Detection of periodontal bacteria in thrombi of patients with acute myocardial infarction by polymerase chain reaction. Am Heart J 163: 164-167.
16. Pereira RB, Vasquez EC, Stefanon I, Meyrelles SS, (2011) Oral P. gingivalis infection alters the vascular reactivity in healthy and spontaneously atherosclerotic mice. Lipids Health Dis 10: 80.
17. Hokamura K, Inaba H, Nakano K, Nomura R, Yoshioka H, et al. (2010) Molecular analysis of aortic intimal hyperplasia caused by Porphyromonas gingivalis infection in mice with endothelial damage. J Periodontal Res 45: 337-344.
18. Inaba H, Hokamura K, Nakano K, Nomura R, Katayama K, et al. (2009) Upregulation of S100 calcium-binding protein A9 is required for induction of smooth muscle cell proliferation by a periodontal pathogen. FEBS Lett 583: 128-134.
19. Delbosc S, Alsac JM, Journe C, Louedec L, Castier Y, et al. (2011) Porphyromonas gingivalis participates in pathogenesis of human abdominal aortic aneurysm by neutrophil activation. Proof of concept in rats. PLoS One 6: e18679.
20. Aoyama N, Suzuki JI, Ogawa M, Watanabe R, Kobayashi N, et al. (2012) Clarithromycin suppresses the periodontal bacteria-accelerated abdominal aortic aneurysms in mice. J Periodontal Res 47: 463-469.
21. Aoyama N, Suzuki J, Wang D, Ogawa M, Kobayashi N, et al. (2011) Porphyromonas gingivalis promotes murine abdominal aortic aneurysms via matrix metalloproteinase-2 induction. J Periodontal Res 46: 176-183.
22. Fukasawa A, Kurita-Ochiai T, Hashizume T, Kobayashi R, Akimoto Y, et al. (2011) Porphyromonas gingivalis accelerates atherosclerosis in C57BL/6 mice fed a high-fat diet. Immunopharmacol Immunotoxicol.
23. Hayashi C, Viereck J, Hua N, Phinikaridou A, Madrigal AG, et al. (2011) Porphyromonas gingivalis accelerates inflammatory atherosclerosis in the innominate artery of ApoE deficient mice. Atherosclerosis 215: 52-59.
24. 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.
25. Madan M, Amar S, (2008) Toll-like receptor-2 mediates diet and/or pathogen associated atherosclerosis: proteomic findings. PLoS One 3: e3204.
26. Maekawa T, Takahashi N, Tabeta K, Aoki Y, Miyashita H, et al. (2011) Chronic oral infection with Porphyromonas gingivalis accelerates atheroma formation by shifting the lipid profile. PLoS One 6: e20240.
27. Brodala N, Merricks EP, Bellinger DA, Damrongsri D, Offenbacher S, et al. (2005) Porphyromonas gingivalis bacteremia induces coronary and aortic atherosclerosis in normocholesterolemic and hypercholesterolemic pigs. Arterioscler Thromb Vasc Biol 25: 1446-1451.
28. Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, et al. (2007) Treatment of periodontitis and endothelial function. N Engl J Med 356: 911-920.
29. Deshpande RG, Khan MB, Genco CA, (1998) Invasion of aortic and heart endothelial cells by Porphyromonas gingivalis. Infect Immun 66: 5337-5343.
30. Dorn BR, Burks JN, Seifert KN, Progulske-Fox A, (2000) Invasion of endothelial and epithelial cells by strains of Porphyromonas gingivalis. FEMS Microbiol Lett 187: 139-144.
31. Li L, Michel R, Cohen J, Decarlo A, Kozarov E, (2008) Intracellular survival and vascular cell-to-cell transmission of Porphyromonas gingivalis. BMC Microbiol 8: 26.
32. Khlgatian M, Nassar H, Chou HH, Gibson FC III, Genco CA, (2002) Fimbria-dependent activation of cell adhesion molecule expression in Porphyromonas gingivalis-infected endothelial cells. Infect Immun 70: 257-267.
33. Takahashi Y, Davey M, Yumoto H, Gibson FC III, Genco CA, (2006) Fimbria-dependent activation of pro-inflammatory molecules in Porphyromonas gingivalis infected human aortic endothelial cells. Cell Microbiol 8: 738-757.
34. Chou HH, Yumoto H, Davey M, Takahashi Y, Miyamoto T, et al. (2005) Porphyromonas gingivalis fimbria-dependent activation of inflammatory genes in human aortic endothelial cells. Infect Immun 73: 5367-5378.
35. Yumoto H, Chou HH, Takahashi Y, Davey M, Gibson FC III, et al. (2005) Sensitization of human aortic endothelial cells to lipopolysaccharide via regulation of Toll-like receptor 4 by bacterial fimbria-dependent invasion. Infect Immun 73: 8050-8059.
36. Dorn BR, Dunn WA Jr, Progulske-Fox A, (2001) Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect Immun 69: 5698-5708.
37. Roth GA, Ankersmit HJ, Brown VB, Papapanou PN, Schmidt AM, et al. (2007) Porphyromonas gingivalis infection and cell death in human aortic endothelial cells. FEMS Microbiol Lett 272: 106-113.
38. Pollreisz A, Huang Y, Roth GA, Cheng B, Kebschull M, et al. (2010) Enhanced monocyte migration and pro-inflammatory cytokine production by Porphyromonas gingivalis infection. J Periodontal Res 45: 239-245.
39. Gibson FC III, 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.
40. Nakano K, Inaba H, Nomura R, Nemoto H, Takeuchi H, et al. (2008) Distribution of Porphyromonas gingivalis fimA genotypes in cardiovascular specimens from Japanese patients. Oral Microbiol Immunol 23: 170-172.
41. Nishikawa K, Duncan MJ, (2010) Histidine kinase-mediated production and autoassembly of Porphyromonas gingivalis fimbriae. J Bacteriol 192: 1975-1987.
42. Igboin CO, Griffen AL, Leys EJ, (2009) Porphyromonas gingivalis strain diversity. J Clin Microbiol 47: 3073-3081.
43. Vita JA, Loscalzo J, (2002) Shouldering the risk factor burden: infection, atherosclerosis, and the vascular endothelium. Circulation 106: 164-166.
44. Hansson GK, Robertson AK, Soderberg-Naucler C, (2006) Inflammation and atherosclerosis. Annu Rev Pathol 1: 297-329.
45. Zhang YL, Cao YJ, You SJ, Li RX, Liu HH, et al. (2010) [Protective effects of autophagy against oxidized LDL-induced injury in endothelial cells]. Zhonghua Yi Xue Za Zhi 90: 2792-2796.
46. Nassar H, Chou HH, Khlgatian M, Gibson FC III, Van Dyke TE, et al. (2002) 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 70: 268-276.
47. Rodrigues PH, Progulske-Fox A, (2005) Gene expression profile analysis of Porphyromonas gingivalis during invasion of human coronary artery endothelial cells. Infect Immun 73: 6169-6173.
48. Song H, Belanger M, Whitlock J, Kozarov E, Progulske-Fox A, (2005) Hemagglutinin B is involved in the adherence of Porphyromonas gingivalis to human coronary artery endothelial cells. Infect Immun 73: 7267-7273.
49. Yuan L, Rodrigues PH, Belanger M, Dunn WA Jr, Progulske-Fox A, (2008) Porphyromonas gingivalis htrA is involved in cellular invasion and in vivo survival. Microbiology 154: 1161-1169.
50. Miyamoto T, Yumoto H, Takahashi Y, Davey M, Gibson FC III, et al. (2006) Pathogen-accelerated atherosclerosis occurs early after exposure and can be prevented via immunization. Infect Immun 74: 1376-1380.
51. Amano A, Kuboniwa M, Nakagawa I, Akiyama S, Morisaki I, et al. (2000) Prevalence of specific genotypes of Porphyromonas gingivalis fimA and periodontal health status. J Dent Res 79: 1664-1668.
52. Amano A, (2010) Bacterial adhesins to host components in periodontitis. Periodontol 2000 52: 12-37.
53. Nakagawa I, Amano A, Kuboniwa M, Nakamura T, Kawabata S, et al. (2002) Functional differences among FimA variants of Porphyromonas gingivalis and their effects on adhesion to and invasion of human epithelial cells. Infect Immun 70: 277-285.
54. Aduse-Opoku J, Slaney JM, Hashim A, Gallagher A, Gallagher RP, et al. (2006) Identification and characterization of the capsular polysaccharide (K-antigen) locus of Porphyromonas gingivalis. Infect Immun 74: 449-460.
55. Amar S, Wu SC, Madan M, (2009) Is Porphyromonas gingivalis cell invasion required for atherogenesis? Pharmacotherapeutic implications. J Immunol 182: 1584-1592.
56. Yamatake K, Maeda M, Kadowaki T, Takii R, Tsukuba T, et al. (2007) Role for gingipains in Porphyromonas gingivalis traffic to phagolysosomes and survival in human aortic endothelial cells. Infect Immun 75: 2090-2100.
57. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
58. Eskelinen EL, (2006) Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol Aspects Med 27: 495-502.
59. Hansson GK, Libby P, (2006) The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 6: 508-519.
60. Braunersreuther V, Mach F, Steffens S, (2007) The specific role of chemokines in atherosclerosis. Thromb Haemost 97: 714-721.
61. Walter C, Zahlten J, Schmeck B, Schaudinn C, Hippenstiel S, et al. (2004) Porphyromonas gingivalis strain-dependent activation of human endothelial cells. Infect Immun 72: 5910-5918.
62. Roldan V, Marin F, Lip GY, Blann AD, (2003) Soluble E-selectin in cardiovascular disease and its risk factors. A review of the literature. Thromb Haemost 90: 1007-1020.
63. Papadopoulos NG, Dedoussis GV, Spanakos G, Gritzapis AD, Baxevanis CN, et al. (1994) An improved fluorescence assay for the determination of lymphocyte-mediated cytotoxicity using flow cytometry. J Immunol Methods 177: 101-111.
64. Progulske-Fox A, Kozarov E, Dorn B, Dunn W Jr, Burks J, et al. (1999) Porphyromonas gingivalis virulence factors and invasion of cells of the cardiovascular system. J Periodontal Res 34: 393-399.
65. Takeuchi H, Furuta N, Amano A, (2011) Cell entry and exit by periodontal pathogen via recycling pathway. Commun Integr Biol 4: 587-589.
66. Kim KJ, Elliott SJ, Di Cello F, Stins MF, Kim KS, (2003) The K1 capsule modulates trafficking of E. coli-containing vacuoles and enhances intracellular bacterial survival in human brain microvascular endothelial cells. Cell Microbiol 5: 245-252.
67. Prasad A, Zhu J, Halcox JP, Waclawiw MA, Epstein SE, et al. (2002) Predisposition to atherosclerosis by infections: role of endothelial dysfunction. Circulation 106: 184-190.
68. Singh A, Wyant T, Anaya-Bergman C, Aduse-Opoku J, Brunner J, et al. (2011) The capsule of Porphyromonas gingivalis leads to a reduction in the host inflammatory response, evasion of phagocytosis, and increase in virulence. Infect Immun 79: 4533-4542.
69. Brunner J, Scheres N, El Idrissi NB, Deng DM, Laine ML, et al. (2010) The capsule of Porphyromonas gingivalis reduces the immune response of human gingival fibroblasts. BMC Microbiol 10: 5.
70. Perez-Chaparro PJ, Lafaurie GI, Gracieux P, Meuric V, Tamanai-Shacoori Z, et al. (2009) Distribution of Porphyromonas gingivalis fimA genotypes in isolates from subgingival plaque and blood sample during bacteremia. Biomedica 29: 298-306.
71. Belanger M, Rodrigues P, Progulske-Fox A, (2007) Genetic manipulation of Porphyromonas gingivalis. Curr Protoc Microbiol Chapter 13: Unit13C 12.
72. Chen T, Duncan MJ, (2004) Gingipain adhesin domains mediate Porphyromonas gingivalis adherence to epithelial cells. Microb Pathog 36: 205-209.
73. Park Y, Simionato MR, Sekiya K, Murakami Y, James D, et al. (2005) Short fimbriae of Porphyromonas gingivalis and their role in coadhesion with Streptococcus gordonii. Infect Immun 73: 3983-3989.
74. Lamont RJ, Chan A, Belton CM, Izutsu KT, Vasel D, et al. (1995) Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 63: 3878-3885.