Circulating Porphyromonas gingivalis lipopolysaccharide resets cardiac homeostasis in mice through a matrix metalloproteinase-9-dependent mechanism

Physiological Reports

Volumn 1, Issue 5, 2013, Pages

  Deleon Pennell, Kristine Y ^a   Brás, Lisandra E de Castro ^a   Lindsey, Merry L ^a,b  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b G V SONNY MONTGOMERY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cardiac function; Inflammation; Matrix metalloproteinase 9; Periodontal disease; Porphyromonas gingivalis; Proteomics

Indexed keywords

C REACTIVE PROTEIN; GELATINASE B; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCYTE CHEMOTACTIC PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 3; MONOCYTE CHEMOTACTIC PROTEIN 5; PORPHYROMONAS GINGIVALIS LIPOPOLYSACCHARIDE; STEM CELL FACTOR; TROPONIN I; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR PARAMETERS; CAROTID ARTERY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FRACTIONAL SHORTENING; HEART FUNCTION; HEART LEFT VENTRICLE; HEART MUSCLE INJURY; HISTOLOGY; HOMEOSTASIS; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; MACROPHAGE; MALE; MOUSE; NONHUMAN; PERIODONTAL DISEASE; PORPHYROMONAS GINGIVALIS; PROTEIN DETERMINATION; REAL TIME POLYMERASE CHAIN REACTION; TRANSTHORACIC ECHOCARDIOGRAPHY; WESTERN BLOTTING; WILD TYPE;

EID: 85009108022     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.1002/phy2.79     Document Type: Article

References (33)

1. Adams, J. E. 3rd, G. S. Bodor, V.G. Davila-Roman, J. A. Delmez, F. S. Apple, J. H. Ladenson, et al. 1993. Cardiac troponin I. A marker with high specificity for cardiac injury. Circulation 88: 101–106.
2. Ashigaki, N., J. Suzuki, M. Ogawa, R. Watanabe, N. Aoyama, N. Kobayashi, et al. Periodontal bacteria aggravate experimental autoimmune myocarditis in mice. Am. J. Physiol. Heart Circ. Physiol. 304: H740–H748.
3. Bradley, L. M., M. F. Douglass, D. Chatterjee, S. Akira, and B. J. Baaten. 2012. Matrix metalloprotease 9 mediates neutrophil migration into the airways in response to influenza virus-induced toll-like receptor signaling. PLoS Pathog. 8: e1002641.
4. Cassetta, L., E. Cassol, and G. Poli. 2011. Macrophage polarization in health and disease. ScientificWorldJournal 11: 2391–2402.
5. Chiao, Y. A., Q. Dai, J. Zhang, J. Lin, E. F. Lopez, S. S. Ahuja, et al. 2011. Multi-analyte profiling reveals matrix metalloproteinase-9 and monocyte chemotactic protein-1 as plasma biomarkers of cardiac aging. Circ. Cardiovasc. Genet. 4: 455–462.
6. De Nichilo, M. O., and G. F. Burns. 1993. Granulocytemacrophage and macrophage colony-stimulating factors differentially regulate alpha v integrin expression on cultured human macrophages. Proc. Natl Acad. Sci. USA 90: 2517–2521.
7. Ducharme, A., S. Frantz, M. Aikawa, E. Rabkin, M. Lindsey, L. E. Rohde, et al. 2000. Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J. Clin. Invest. 106: 55–62.
8. Gemmell, E., K. Yamazaki, and G. J. Seymour. 2007. The role of T cells in periodontal disease: homeostasis and autoimmunity. Periodontol 2000 43: 14–40.
9. Gitlin, J. M., and C. D. Loftin. 2009. Cyclooxygenase-2 inhibition increases lipopolysaccharide-induced atherosclerosis in mice. Cardiovasc. Res. 81: 400–407.
10. Griffen, A. L., M. R. Becker, S. R. Lyons, M. L. Moeschberger, and E. J. Leys. 1998. Prevalence of Porphyromonas gingivalis and periodontal health status. J. Clin. Microbiol. 36: 3239–3242.
11. Gu, Y., H. M. Lee, T. Sorsa, A. Salminen, M. E. Ryan, M. J. Slepian, et al. 2011. Non-antibacterial tetracyclines modulate mediators of periodontitis and atherosclerotic cardiovascular disease: a mechanistic link between local and systemic inflammation. Pharmacol. Res. 64: 573–579.
12. Hessel, M. H., D. E. Atsma, E. J. van der Valk, W. H. Bax, M. J. Schalij, and A. van der Laarse. 2008. Release of cardiac troponin I from viable cardiomyocytes is mediated by integrin stimulation. Pflugers Arch. 455: 979–986.
13. Humphrey, L. L., R. Fu, D. I. Buckley, M. Freeman, and M. Helfand. 2008. Periodontal disease and coronary heart disease incidence: a systematic review and meta-analysis. J. Gen. Intern. Med. 23: 2079–2086.
14. Kaisare, S., J. Rao, and N. Dubashi. 2007. Periodontal disease as a risk factor for acute myocardial infarction. A case-control study in Goans highlighting a review of the literature. Br. Dent. J. 203: E5; discussion 144–145.
15. Koch, A. E., S. L. Kunkel, L. A. Harlow, D. D. Mazarakis, G. K. Haines, M. D. Burdick, et al. 1994. Macrophage inflammatory protein-1 alpha. A novel chemotactic cytokine for macrophages in rheumatoid arthritis. J. Clin. Invest. 93: 921–928.
16. Lindsey, M. L., G. P. Escobar, L. W. Dobrucki, D. K. Goshorn, S. Bouges, J. T. Mingoia, et al. 2006. Matrix metalloproteinase-9 gene deletion facilitates angiogenesis after myocardial infarction. Am. J. Physiol. Heart Circ. Physiol. 290: H232–H239.
17. Luttun, A., E. Lutgens, A. Manderveld, K. Maris, D. Collen, P. Carmeliet, et al. 2004. Loss of matrix metalloproteinase-9 or matrix metalloproteinase-12 protects apolipoprotein E-deficient mice against atherosclerotic media destruction but differentially affects plaque growth. Circulation 109: 1408–1414.
18. Manginas, A., E. Bei, A. Chaidaroglou, D. Degiannis, K. Koniavitou, V. Voudris, et al. 2005. Peripheral levels of matrix metalloproteinase-9, interleukin-6, and C-reactive protein are elevated in patients with acute coronary syndromes: correlations with serum troponin I. Clin. Cardiol. 28: 182–186.
19. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677–686.
20. McGrory, K., C. M. Flaitz, and J. R. Klein. 2004. Chemokine changes during oral wound healing. Biochem. Biophys. Res. Commun. 324: 317–320.
21. Nelson, M. P., B. S. Christmann, J. L. Werner, A. E. Metz, J. L. Trevor, C. A. Lowell, et al. 2011. IL-33 and M2a alveolar macrophages promote lung defense against the atypical fungal pathogen Pneumocystis murina. J. Immunol. 186: 2372–2381.
22. Okada, M., M. Saio, Y. Kito, N. Ohe, H. Yano, S. Yoshimura, et al. 2009. Tumor-associated macrophage/microglia infiltration in human gliomas is correlated with MCP-3, but not MCP-1. Int. J. Oncol. 34: 1621–1627.
23. Pussinen, P. J., K. Tuomisto, P. Jousilahti, A. S. Havulinna, J. Sundvall, and V. Salomaa. 2007. Endotoxemia, immune response to periodontal pathogens, and systemic inflammation associate with incident cardiovascular disease events. Arterioscler. Thromb. Vasc. Biol. 27: 1433–1439.
24. Roth, J., J. L. McClellan, M. J. Kluger, and E. Zeisberger. 1994. Attenuation of fever and release of cytokines after repeated injections of lipopolysaccharide in guinea-pigs. J. Physiol. 477: 177–185.
25. Scannapieco, F. A., R. B. Bush, and S. Paju. 2003. Associations between periodontal disease and risk for nosocomial bacterial pneumonia and chronic obstructive pulmonary disease. A systematic review. Ann. Periodontol. 8: 54–69.
26. Sharma, C. G., and A. R. Pradeep. 2006. Gingival crevicular fluid osteopontin levels in periodontal health and disease. J. Periodontol. 77: 1674–1680.
27. Silva, T. A., G. P. Garlet, S. Y. Fukada, J. S. Silva, and F. Q. Cunha. 2007. Chemokines in oral inflammatory diseases: apical periodontitis and periodontal disease. J. Dent. Res. 86: 306–319.
28. Tomioka, H., W. W. Maw, K. Sato, and H. Saito. 1996. The role of tumour necrosis factor-alpha in combination with interferon-gamma or interleukin-1 in the induction of immunosuppressive macrophages because of Mycobacterium avium complex infection. Immunology 88: 61–67.
29. Tonetti, M. S., F. D’Aiuto, L. Nibali, A. Donald, C. Storry, M. Parkar, et al. 2007. Treatment of periodontitis and endothelial function. N. Engl. J. Med. 356: 911–920.
30. Uzuelli, J. A., C. A. Dias-Junior, and J. E. Tanus-Santos. 2008. Severity dependent increases in circulating cardiac troponin I and MMP-9 concentrations after experimental acute pulmonary thromboembolism. Clin. Chim. Acta 388: 184–188.
31. West, M. A., and A. Koons. 2008. Endotoxin tolerance in sepsis: concentration-dependent augmentation or inhibition of LPS-stimulated macrophage TNF secretion by LPS pretreatment. J. Trauma 65: 893–898; discussion 898–900.
32. Wolk, K., W. D. Docke, V. von Baehr, H. D. Volk, and R. Sabat. 2000. Impaired antigen presentation by human monocytes during endotoxin tolerance. Blood 96: 218–223.
33. Wolk, K., S. Kunz, N. E. Crompton, H. D. Volk, and R. Sabat. 2003. Multiple mechanisms of reduced major histocompatibility complex class II expression in endotoxin tolerance. J. Biol. Chem. 278: 18030–18036.