Porphyromonas Gingivalis Invasion of Human Aortic Smooth Muscle Cells
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Abstract
Periodontal disease, a form of chronic inflammatory bacterial infectious disease, is known to be a risk factor for cardiovascular disease (CVD). Porphyromonas gingivalis has been implicated in periodontal disease and widely studied for its role in the pathogenesis of CVD. A previous study demonstrating that periodontopathic P. gingivalis is involved in CVD showed that invasion of endothelial cells by the bacterium is accompanied by an increase in cytokine production, which may result in vascular atherosclerotic changes. The present study was performed in order to further elucidate the role of P. gingivalis in the process of atherosclerosis and CVD. For this purpose, invasion of human aortic smooth muscle cells (HASMC) by P. gingivalis 381 and its isogenic mutants of KDP150 (fimA-), CW120 (ppk-) and KS7 (relA-) was assessed using a metronidazole protection assay. Wild type P. gingivalis invaded HASMCs with an efficiency of 0.12 %. In contrast, KDP150 failed to demonstrate any invasive ability. CW120 and KS7 showed relatively higher invasion efficiencies, but results for these variants were still negligible when compared to the wild type invasiveness. These results suggest that fimbriae are required for invasion and that energy metabolism in association with regulatory genes involved in stress and stringent response may also be important for this process. ELISA assays revealed that the invasive P. gingivalis 381 increased production of the proinflammatory cytokine interleukin (IL)-1β‚ and the chemotactic cytokines (chemokine) IL (interleukin)-8 and monocyte chemotactic (MCP) protein-1 during the 30-90 min incubation periods (P<0.05). Expression of RANTES (regulation upon activation, normal T cell expressed and secreted) and Tolllike receptor (TLR)-4, a pattern recognition receptor (PRR), was increased in HASMCs infected with P. gingivalis 381 by RT-PCR analysis. P. gingivalis infection did not alter interferon-γ-inducible protein-10 expression in HASMCs. HASMC nonspecific necrosis and apoptotic cell death were measured by lactate dehydrogenase (LDH) and caspase activity assays, respectively. LDH release from HASMCs and HAMC caspase activity were significantly higher after a 90 min incubation with P. gingivalis 381. Taken together, P. gingivalis invasion of HASMCs induces inflammatory cytokine production, apoptotic cell death, and expression of TLR-4, a PRR which may react with the bacterial molecules and induce the expression of the chemokines IL-8, MCP-1 and RANTES. Overall, these results suggest that invasive P. gingivalis may participate in the pathogenesis of atherosclerosis, leading to CVD.
참고문헌 (95)
- Al-Katma MK, "Control of periodontal infection reduces the severity of active rheumatoid arthritis", Journal of Clinical Rheumatology, 13, pp.134~137 (2007)
- Barkocy-Gallagher GA, "Analysis of the prtP gene encoding porphypain, a cysteine proteinase of Porphyromonas gingivalis", Journal of Bacteriology, 178, pp.2734~2741 (1996)
- Belton CM, "Fluorescence image analysis of the association between Porphyromonas gingivalis and gingival epithelial cells", Cellular Microbiology, 1, pp.215~223 (1999)
- Blum E, "Polyphosphate kinase is a component of the Escherichia coli RNA degradsome", Molecular Microbiology, 26, pp.387~398 (1997)
- Boutaga K, "The additional value of real-time PCR in the quantitative detection of periodontal pathogens", Journal of Clinical Periodontology, 33, pp.427~433 (2006)
- Brown MR, "Pathophysiology of acute myocardial infarction", Medical Clinics of North America, 91, pp.553~572 (2007)
- Chen W, "Role of polyphosphate kinase in biofilm formation by Porphyromonas gingivalis", Infection and Immunity, 70, pp.4708~4715 (2002)
- Chou HH, "Porphyromonas gingivalis fimbria-dependent activation of inflammatory genes in human aortic endothelial cells", Infection and Immunity, 73, pp.5367~5378 (2005)
- Ciornei CD, "Human antimicrobial peptide LL-37 is present in atherosclerotic plaques and induces death of vascular smooth muscle cells: a laboratory study", BMC Cardiovascular Disorders, 6, pp.49~60 (2006)
- Clarke M, "Defining the role of vascular smooth muscle cell apoptosis in atherosclerosis", Cell Cycle, (5), pp.2329~2331 (2006)
- Clarke M, "The emerging role of vascular smooth muscle cell apoptosis in atherosclerosis and plaque stability", American Journal of Nephrology, 26, pp.531~535 (2006)
- Clarke MCH, "Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis", Nature Medicine, 12, pp.1075~1080 (2006)
- Cohen DW, "The periodontal-medical risk relationship", Compendium of continuing education in dentistry, 22, pp.7~11 (2001)
- Darveau RP, "Ability of bacteria associated with chronic inflammatory disease to stimulate E-selection expression and promote neutrophil adhesion", Infection and Immunity, 63, pp.1311~1317 (1995)
- Dengler TJ, "Cytomegalovirus infection of vascular cells induces expression of pro-inflammatory adhesion molecules by paracrine action of secreted interleukin-1β", Transplantation, 69, pp.1160~1168 (2000)
- Deshpande RG, "Invasion of aortic and heart endothelial cells by Porphyromonas gingivalis", Infection and Immunity, 66, pp.5337~5343 (1998)
- DeStefano F, "Dental disease and risk of coronary heart disease and mortality", British Medical Journal, 306, pp.688~691 (1993)
- Dorn BR, "Invasion of endothelial and epithelial cells by strains of Porphyromonas gingivalis", FEMS Microbiology Letters, 187, pp.139~144 (2000)
- Dorn BR, "Invasion of coronary artery cells by periodontal pathogens", Infection and Immunity, 67, pp.5792~5798 (1999)
- Dorn BR, "Invasion of vascular cells in vitro by Porphyromonas endodontalis", International Endodontic Journal, 35, pp.366~371 (2002)
- Döfer CE, "The association of gingivitis and periodontitis with ischemic stroke", Journal of Clinical Periodontology, 31, pp.396~401 (2004)
- Falkow S, "Bacterial entry into eucaryotic cells", Cell, 65, pp.1099~1102 (1991)
- Faure E, "Bacterial lipopolysaccharide activates NF-kB through toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells. Differential expression of TLR-4 and TLR-2 in endothelial cells", Journal of Biological Chemistry, 275, pp.11058~11063 (2000)
- Ford PJ, "Inflammation, heat shock proteins and periodontal pathogens in atherosclerosis:an immunohistologic study", Oral Microbiology and Immunology, 21, pp.206~211 (2006)
- Gaffar A, "Inflammation, periodontal diseases, and systemic health", Compendium of continuing education in dentistry, 25(7), pp.4~6 (2004)
- Genco R, "Periodontal disease and cardiovascular disease: epidemiology and possible mechanisms", Journal of the American Dental Association, 133, pp.14S~22S (2002)
- Genco RJ, "Overview of risk factors for periodontal disease and implications for diabetes and cardiovascular disease", Compendium of continuing education in dentistry, 19, pp.40~45 (1998)
- Gibbons RJ, "Bacterial adhesion to oral tissues: a model for infectious diseases", Journal of Dental Research, 68, pp.750~760 (1989)
- Gibson FC III, "Innate immune recognition of invasive bacteria accelerated atherosclerosis in apolipoprotein Edeficient mice", Circulation, 109, pp.2801~2806 (2004)
- Gravel SP, "Roles of an IkappaB kinase-related pathway in human cytomegalovirus-infected vascular smooth muscle cells: a molecular link in pathogen-induced proatherosclerotic conditions", Journal of Biological Chemistry, 280, pp.7477~7486 (2005)
- Hajishengallis G, "Interactions of oral pathogens with toll-like receptors: possible role in atherosclerosis", Annals of periodontology, 2002, pp.7, 72~78
- Hajishengalis G, "Intracellular signaling and cytokine induction upon interactions of Porphyromonas gingivalis fimbriae with pattern-recognition receptor", Immunological Investigations, 33, pp.157~172 (2004)
- Hao H, "Arterial smooth muscle cell heterogeneity. Implications for atherosclerosis and restenosis development", Arteriosclerosis Thrombosis and Vascular Biology, 23, pp.1510~1520 (2003)
- Haraszthy VI, "Identification of periodontal pathogens in atheromatous plaques", Journal of Periodontology, 71, pp.1554~1560 (2000)
- Herzberg MC, "The platelet as an inflammatory cell in periodontal diseases:interaction with Porphyromonas gingivalis. In: Molecular Pathogenesis of periodontal Disease, Genco R, Hamada S, Lehner T, McGhee J, Mergenhagen", pp.247~255
- American Society for Microbiology, Washington DC, 1994. Hirose K, Isogai E, Ueda I, "Porphyromonas gingivalis fimbriae induce adhesion of monocytic cell line U937 to endothelial cells", Microbiology and Immunology, 44, pp.17~22 (2000)
- Hoge M, "Role of interleukin-1 in bacterial atherogenesis", Drugs of Today, 42, pp.683~688 (2006)
- Ito T, "Inflammatory cytokines and cardiovascular disease", Curr Drug Targets Inflamm Allergy, 2, pp.257~265 (2003)
- Kang I-C, "Induction of monocyte chemoattractant protein-1 by Porphyromonas gingivalis in human endothelial cells", FEMS Immunology and Medical Microbiology, 34, pp.311~317 (2002)
- Khlgatian M, "Fimbria-dependent activation of cell adhesion molecule expression in Porphyromonas gingivalis-infected endothelial cells", Infection and Immunity, 70, pp.257~267 (2002)
- Khuseyinova N, "Biomarkers of outcome from cardiovascular disease", Current Opinion in Critical Care, 12, pp.412~419 (2006)
- Kornberg A, "Inorganic polyphosphate:a molecule of many functions", Annual Review of Biochemistry, 68, pp.89~125 (1999)
- Kuramitsu HK, "Interactions of Porphyromonas gingivalis with host cells: implication for cardiovascular diseases", Journal of Periodontology, 74, pp.85~89 (2003)
- Kuramitsu HK, "Role for periodontal bacteria in cardiovascular diseases", Annals of periodontology, 2001, pp.6, 41~47
- Lamont RJ, "Porphyromonas gingivalis invasion of gingival epithelial cells", Infection and Immunity, 63, pp.3878~3885 (1995)
- Lamont RJ, "Interaction of Porphyromonas gingivalis with gingival epithelial cells maintained in culture", Oral Microbiology and Immunology, 7, pp.364~367 (1992)
- Lee J-Y, "Possibility of Involvement of Porphyromonas gingivalis in Coronary Heart Disease", Journal of the Korean Society for Microbiology, 35(3), pp.203~214 (2000), 대한미생물학회
- Lee J-Y, "Purification of major fimbrial proteins of Porphyromonas gingivalis", Protein Expression and Purification, 6, pp.496~500 (1995)
- Li L, "Porphyomonas gingivalis accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model", Circulation, 105, pp.861~867 (2002)
- McCarthy NJ, "The regulation of vascular smooth muscle cell apoptosis", Cardiovascular Research, 45, pp.747~755 (2000)
- Madianos PN, "Porphyromonas gingivalis FDC381 multiplies and persists within human oral epithelial cells in vitro", Infect and Immunity, 64, pp.660~664 (1996)
- Mao S, "CD14-mediated induction of interleukin-8 and monocyte chemoattractant protein-1 by a heat-resistant constituent of Porphyromonas gingivalis in endothelial cells", Scandinavian Journal of Immunology, 56, pp.484~491 (2002)
- ttila KJ, "Dental infections as a risk factor for acute myocardial infarction", EUROPEAN HEART JOURNAL, 14(K), pp.51~53 (1993)
- Mattila KJ, "Association between dental health and acute myocardial infarction", British Medical Journal, 298, pp.779~781 (1989)
- Mealey BL, "Diabetes mellitus and periodontal diseases", Journal of Periodontology, 77, pp.1289~1303 (2006)
- Morgando A, "Helicobacter pylori seropositivity in myocardial infection", Lancet, 345, pp.1380~ (1995)
- Nakagawa I, "Functional differences among FimA variants of Porphyromonas gingivalis and their effects on adhesion to and invasion of human epithelial cells", Infection and Immunity, 70, pp.277~285 (2002)
- Nakagawa I, "Invasion of epithelial cells and proteolysis of cellular focal adhesion components by distinct types of Porphyromonas gingivalis fimbriae", Infect and Immunity, 74, pp.3773~3782 (2006)
- Nassar H, "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 and Immunity, 70, pp.268~276 (2002)
- Njoroge T, "A role for fimbriae in Porphyromonas gingivalis invasion of oral epithelial cells", Infect and Immunity, 65, pp.1980~1984 (1997)
- Nonnenmacher C, "Real-time polymerase chain reaction for detection and quantification of bacteria in periodontal patients", Journal of Periodontology, 76, pp.1542~1549 (2005)
- Nonnenmacher C, "Flores-de-Jacoby L. Periodontal microbiota in patients with coronary artery disease measured by real-time polymerase chain reaction: a casecontrol study", Journal of Periodontology, 78, pp.1724~1730 (2007)
- Offenbacher S, "Periodontitis: a potential risk factor for spontaneous preterm", Compendium of continuing education in dentistry, 19, pp.32~39 (1998)
- Offenbacher S, "A perspective on the potential cardioprotective benefits of periodontal therapy", AMERICAN HEART JOURNAL, 149, pp.950~954 (2005)
- Papapanou PN, "Porphyromonas gingivalis may multiply and advance within stratified human junctional epithelium in vitro", Journal of Periodontal Research, 29, pp.374~375 (1994)
- Pooling Project Research Group, "Relationship of blood pressure, serum cholesterol, smoking habit, relative weight and ECG abnormalities to incidence of major coronary events: final report of the pooling project", Journal of Chronic Diseases, 31, pp.201~306 (1978)
- Pucar A, "Correlation between atherosclerosis and periodontal putative pathogenic bacterial infections in coronary and internal mammary arteries", Journal of Periodontology, 78, pp.677~682 (2007)
- Qi M, "Porphyromonas gingivalis induces murine macrophage foam cell formation", MICROBIAL PATHOGENESIS, 35, pp.259~267 (2003)
- Ross R, "The pathogenesis of atherosclerosis: a perspective for the 1990s", Nature, 362, pp.801~809 (1993)
- Roth GA, "Porphyromonas ginigivalis infection and cell death in human aortic endothelial cells", FEMS Microbiology Letters, 272, pp.106~113 (2007)
- Roth GA, "Infection with a periodontal pathogen induces procoagulant effects in human aortic endothelial cells", Journal of Thrombosis and Haemostasis, 4, pp.2256~2261 (2006)
- Saglie FR, "Intragingival occurrence of Actinobacillus actinomycetemcomitans and Bacteroides gingivalis in active destructive periodontal lesions", Journal of Periodontology, 59, pp.259~265 (1988)
- Sandros J, "Porphyromonas gingivalis invades oral epithelial cells in vitro", Journal of Periodontal Research, 28, pp.219~226 (1993)
- Sandros J, "Porphyromonas gingivalis invades human pocket epithelium in vitro", Journal of Periodontal Research, 29, pp.62~69 (1994)
- Sawada N, "Tolllike receptor 4-dependent recognition of structurally different forms of chemically synthesized lipid As of Porphyromonas gingivalis", CLINICAL AND EXPERIMENTAL IMMUNOLOGY, 148, pp.529~536 (2007)
- Sen K, "Characterization of the relA gene of Porphyromonas gingivalis", Journal of Bacteriology, 182, pp.3302~3304 (2000)
- Setsuda J, "Interleukin-18, interferon-g, IP-10, and Mig expression in Epstein-Barr virus-induced infectious mononucleosis and posttransplant lymphoproliferative disease", American Journal of Pathology, 155, pp.257~265 (1999)
- Sharma A, "Porphyromonas gingivalis platelet aggregation activity: Outer membrane vesicles are potent activators of murine platelets", Oral Microbiology and Immunology, 15, pp.393~396 (2000)
- Socransky SS, "Microbial mechanisms in the pathogenesis of destructive Periodontal diseases: a critical assessment", Journal of Periodontal Research, 26, pp.195~212 (1991)
- Socransky SS, "Bacterial etiology of destructive periodontal disease: current concepts", Journal of Periodontology, 63, pp.322~331 (1992)
- Steinhubl SR, "The role of the platelet in the pathogenesis of atherothrombosis", American Journal of Cardiovascular Drugs, 5, pp.399~408 (2005)
- Stoll LL, "Regulation of endotoxin-induced proinflammatory activation in human coronary artery cells: expression of functional membrane-bound CD14 by human coronary artery smooth muscle cells", Journal of Immunology, 173, pp.1336~1343 (2004)
- Stoll LL, "Potential role of endotoxin as a proinflammatory mediator of atherosclerosis", Arteriosclerosis Thrombosis and Vascular Biology, 24, pp.2227~2236 (2004)
- Streblow DN, "Do pathogens accelerate atherosclerosis?", Journal of Nutrition, 131, pp.2798S~2804S (2001)
- Sugano N, "Differential cytokine induction by two types of Porphyromonas gingivalis", Oral Microbiology and Immunology, 19, pp.121~123 (2004)
- Takahashi Y, "Fimbria-dependent activation of pro-inflammatory molecules in Porphyromonas gingivalis infected human aortic endothelial cells", Cellular Microbiology, 8, pp.738~757 (2006)
- Thom DH, "Association of prior infection with Chlamydia pneumoniae and angiographically demonstrated coronary artery disease", Journal of the American Medical Association, 268, pp.68~72 (1992)
- Ueshima J, "Purification, gene cloning, gene expression, and mutants of Dps from the obligate anaerobe Porphyromonas gingivalis", Infection and Immunity, 71, pp.1170~1178 (2003)
- Umino M, "Systemic disease in elderly dental patients", International dental journal, 43, pp.213~218 (1993)
- Vercellotti GM, "Potential role of viruses in thrombosis and atherosclerosis", Trends in Cardiovascular Medicine, 5, pp.128~133 (1995)
- Weber C, "Platelets and chemokines in atherosclerosis: partners in crime", Circulation Research, 96, pp.612~616 (2005)
- Weinberg A, "Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells", Infection and Immunity, 65, pp.313~316 (1997)
- Wu YM, "Effect of Porphyromonas gingivalis PrtC on cytokine expression in ECV304 endothelial cells and its level in subgingival plaques from patients with chronic periodontitis", ACTA PHARMACOLOGICA SINICA, 28, pp.1015~1023 (2007)
- Yumoto H, "Gibson FC III, Genco CA. Sensitization of human aortic endothelial cells to lipopolysaccharide via regulation of Toll-like receptor 4 by bacterial fimbria-dependent invasion", Infection and Immunity, 73, pp.8050~8059 (2005)
- Zhou YF, "The immediate early gene products of human cytomegalovirus increase vascular smooth muscle cell migration, proliferation, and expression of PDGF beta-receptor", Biochemical and Biophysical Research Communications, 256, pp.608~613 (1999)
