Myxomavirus anti-inflammatory chemokine binding protein reduces the increased plaque growth induced by chronic porphyromonas gingivalis oral infection after balloon angioplasty aortic injury in mice

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Lucas, Alexandra R ^a   Verma, Raj K ^b   Dai, Erbin ^a   Liu, Liying ^a   Chen, Hao ^a   Kesavalu, Sheela ^b   Rivera, Mercedes ^b   Velsko, Irina ^b   Ambadapadi, Sriram ^a   Chukkapalli, Sasanka ^b   Kesavalu, Lakshmyya ^b  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; BINDING PROTEIN; CHEMOKINE; IMMUNOGLOBULIN G ANTIBODY; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN M T7; PROTEIN SERP 1; PROTEINASE; SERINE PROTEINASE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; VIRUS PROTEIN; ALPHA 1 ANTITRYPSIN; INTERFERON RECEPTOR; M-T7 PROTEIN, MYXOMA VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AORTA INJURY; ARTICLE; CELL INVASION; CHRONIC DISEASE; CONTROLLED STUDY; MONOCYTE; MOUSE; MOUTH INFECTION; MOUTH PLAQUE; MYXOMAVIRUS; NONHUMAN; PERCUTANEOUS TRANSLUMINAL ANGIOPLASTY; PORPHYROMONAS GINGIVALIS; POXVIRUS; PROTEIN EXPRESSION; RESTENOSIS; SIGNAL TRANSDUCTION; TOOTH PLAQUE; ADVERSE EFFECTS; ANIMAL; AORTA; BACTEROIDACEAE INFECTIONS; COMPLICATION; DENTAL PLAQUE; DRUG EFFECTS; MICROBIOLOGY; PATHOGENICITY; PLAQUE, ATHEROSCLEROTIC; SURGERY;

MUS; PORPHYROMONAS GINGIVALIS;

ALPHA 1-ANTITRYPSIN; ANGIOPLASTY, BALLOON; ANIMALS; AORTA; BACTEROIDACEAE INFECTIONS; DENTAL PLAQUE; MICE; PLAQUE, ATHEROSCLEROTIC; PORPHYROMONAS GINGIVALIS; RECEPTORS, INTERFERON; VIRAL PROTEINS;

EID: 84908577776     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111353     Document Type: Article

References (43)

1. Chaabane C, Otsuka F, Virmani R, Bochaton-Piallat ML (2013) Biological responses in stented arteries. Cardiovasc Res 99: 353-363.
2. Jukema JW, Verschuren JJ, Ahmed TA, Quax PH (2012) Restenosis after PCI. Part 1: pathophysiology and risk factors. Nat Rev Cardiol 9: 53-62.
3. Arora RR, Rai F (2009) Antiplatelet intervention in acute coronary syndrome. Am J Ther 16: e29-40.
4. Burt B, Research S, Therapy Committee of the American Academy of P (2005) Position paper: epidemiology of periodontal diseases. J Periodontol 76: 1406-1419.
5. Lockhart PB, Bolger AF, Papapanou PN, Osinbowale O, Trevisan M, et al. (2012) Periodontal disease and atherosclerotic vascular disease: does the evidence support an independent association?: a scientific statement from the American Heart Association. Circulation 125: 2520-2544.
6. Paquette DW, Brodala N, Nichols TC (2007) Cardiovascular disease, inflammation, and periodontal infection. Periodontol 2000 44: 113-126.
7. Mustapha IZ, Debrey S, Oladubu M, Ugarte R (2007) Markers of systemic bacterial exposure in periodontal disease and cardiovascular disease risk: a systematic review and meta-analysis. J Periodontol 78: 2289-2302.
8. Kobayashi N, Suzuki J, Ogawa M, Aoyama N, Hanatani T, et al. (2012) Porphyromonas gingivalis accelerates neointimal formation after arterial injury. J Vasc Res 49: 417-424.
9. Kesavalu L, Lucas AR, Verma RK, Liu L, Dai E, et al. (2012) Increased atherogenesis during Streptococcus mutans infection in ApoE-null mice. J Dent Res 91: 255-260.
10. 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.
11. Velsko IM, Chukkapalli SS, Rivera MF, Lee JY, Chen H, et al. (2014) Active Invasion of Oral and Aortic Tissues by Porphyromonas gingivalis in Mice Causally Links Periodontitis and Atherosclerosis. Plos One 9.
12. Haraszthy VI, Zambon JJ, Trevisan M, Zeid M, Genco RJ (2000) Identification of periodontal pathogens in atheromatous plaques. J Periodontol 71: 1554-1560.
13. Zhang SH, Reddick RL, Piedrahita JA, Maeda N (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258: 468-471.
14. Bartee MY, Chen H, Dai E, Liu LY, Davids JA, et al. (2014) Defining the antiinflammatory activity of a potent myxomaviral chemokine modulating protein, M-T7, through site directed mutagenesis. Cytokine 65: 79-87.
15. Kobayashi N, Suzuki J, Ogawa M, Aoyama N, Hanatani T, et al. (2012) Porphyromonas gingivalis accelerates neointimal formation after arterial injury. J Vasc Res 49: 417-424.
16. Yuan H, Zelka S, Burkatovskaya M, Gupte R, Leeman SE, et al. (2013) Pivotal role of NOD2 in inflammatory processes affecting atherosclerosis and periodontal bone loss. Proc Natl Acad Sci U S A 110: E5059-5068.
17. Madan M, Bishayi B, Hoge M, Messas E, Amar S (2007) Doxycycline affects diet- and bacteria-associated atherosclerosis in an ApoE heterozygote murine model: cytokine profiling implications. Atherosclerosis 190: 62-72.
18. Madan M, Bishayi B, Hoge M, Amar S (2008) Atheroprotective role of interleukin-6 in diet- and/or pathogen-associated atherosclerosis using an ApoE heterozygote murine model. Atherosclerosis 197: 504-514.
19. Liu L, Lalani A, Dai E, Seet B, Macauley C, et al. (2000) The viral antiinflammatory chemokine-binding protein M-T7 reduces intimal hyperplasia after vascular injury. J Clin Invest 105: 1613-1621.
20. Dai E, Liu LY, Wang H, McIvor D, Sun YM, et al. (2010) Inhibition of chemokine-glycosaminoglycan interactions in donor tissue reduces mouse allograft vasculopathy and transplant rejection. PLoS One 5: e10510.
21. Viswanathan K, Richardson J, Togonu-Bickersteth B, Dai E, Liu L, et al. (2009) Myxoma viral serpin, Serp-1, inhibits human monocyte adhesion through regulation of actin-binding protein filamin B. J Leukoc Biol 85: 418-426.
22. Chen H, Zheng D, Davids J, Bartee MY, Dai E, et al. (2011) Viral serpin therapeutics from concept to clinic. Methods Enzymol 499: 301-329.
23. Tardif JC, L'Allier PL, Gregoire J, Ibrahim R, McFadden G, et al. (2010) A randomized controlled, phase 2 trial of the viral serpin Serp-1 in patients with acute coronary syndromes undergoing percutaneous coronary intervention. Circ Cardiovasc Interv 3: 543-548.
24. Lucas A, Liu L, Dai E, Bot I, Viswanathan K, et al. (2009) The serpin saga; development of a new class of virus derived anti-inflammatory protein immunotherapeutics. Adv Exp Med Biol 666: 132-156.
25. Chen H, Zheng D, Abbott J, Liu L, Bartee MY, et al. (2013) Myxomavirusderived serpin prolongs survival and reduces inflammation and hemorrhage in an unrelated lethal mouse viral infection. Antimicrob Agents Chemother 57: 4114-4127.
26. Kesavalu L, Sathishkumar S, Bakthavatchalu V, Matthews C, Dawson D, et al. (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75: 1704-1712.
27. Rivera MF, Lee JY, Aneja M, Goswami V, Liu L, et al. (2013) Polymicrobial infection with major periodontal pathogens induced periodontal disease and aortic atherosclerosis in hyperlipidemic ApoE(null) mice. PLoS One 8: e57178.
28. Dai E, Viswanathan K, Sun YM, Li X, Liu LY, et al. (2006) Identification of myxomaviral serpin reactive site loop sequences that regulate innate immune responses. J Biol Chem 281: 8041-8050.
29. Lucas A, Liu L, Macen J, Nash P, Dai E, et al. (1996) Virus-encoded serine proteinase inhibitor SERP-1 inhibits atherosclerotic plaque development after balloon angioplasty. Circulation 94: 2890-2900.
30. Bot I, von der Thusen JH, Donners MM, Lucas A, Fekkes ML, et al. (2003) Serine protease inhibitor Serp-1 strongly impairs atherosclerotic lesion formation and induces a stable plaque phenotype in ApoE2/2mice. Circ Res 93: 464-471.
31. Bartee MY, Dai E, Liu L, Munuswamy-Ramanujam G, Macaulay C, et al. (2009) 10 M-T7: measuring chemokine-modulating activity. Methods Enzymol 460: 209-228.
32. Liu L, Dai E, Miller L, Seet B, Lalani A, et al. (2004) Viral chemokine-binding proteins inhibit inflammatory responses and aortic allograft transplant vasculopathy in rat models. Transplantation 77: 1652-1660.
33. Bainbridge B, Verma RK, Eastman C, Yehia B, Rivera M, et al. (2010) Role of Porphyromonas gingivalis phosphoserine phosphatase enzyme SerB in inflammation, immune response, and induction of alveolar bone resorption in rats. Infect Immun 78: 4560-4569.
34. Jiang J, Arp J, Kubelik D, Zassoko R, Liu W, et al. (2007) Induction of indefinite cardiac allograft survival correlates with toll-like receptor 2 and 4 downregulation after serine protease inhibitor-1 (Serp-1) treatment. Transplantation 84: 1158-1167.
35. Dai E, Guan H, Liu L, Little S, McFadden G, et al. (2003) Serp-1, a viral antiinflammatory serpin, regulates cellular serine proteinase and serpin responses to vascular injury. J Biol Chem 278: 18563-18572.
36. Petrov L, Laurila H, Hayry P, Vamvakopoulos JE (2005) A mouse model of aortic angioplasty for genomic studies of neointimal hyperplasia. J Vasc Res 42: 292-300.
37. Humphrey LL, Fu R, Buckley DI, Freeman M, Helfand M (2008) Periodontal disease and coronary heart disease incidence: a systematic review and metaanalysis. J Gen Intern Med 23: 2079-2086.
38. Holt SC, Kesavalu L, Walker S, Genco CA (1999) Virulence factors of Porphyromonas gingivalis. Periodontol 2000 20: 168-238.
39. Upton C, Macen JL, Wishart DS, McFadden G (1990) Myxoma virus and malignant rabbit fibroma virus encode a serpin-like protein important for virus virulence. Virology 179: 618-631.
40. Macen JL, Upton C, Nation N, McFadden G (1993) SERP1, a serine proteinase inhibitor encoded by myxoma virus, is a secreted glycoprotein that interferes with inflammation. Virology 195: 348-363.
41. Turner PC, Moyer RW (1995) Orthopoxvirus fusion inhibitor glycoprotein SPI- 3 (open reading frame K2L) contains motifs characteristic of serine proteinase inhibitors that are not required for control of cell fusion. J Virol 69: 5978-5987.
42. Hamalainen M, Nieminen R, Uurto I, Salenius JP, Kellomaki M, et al. (2013) Dexamethasone-eluting vascular stents. Basic Clin Pharmacol Toxicol 112: 296-301.
43. Scott NA (2006) Restenosis following implantation of bare metal coronary stents: pathophysiology and pathways involved in the vascular response to injury. Adv Drug Deliv Rev 58: 358-376.