Atherosclerosis
Volume 197, Issue 2 , Pages 504-514 , April 2008

Atheroprotective role of interleukin-6 in diet- and/or pathogen-associated atherosclerosis using an ApoE heterozygote murine model

Received 3 November 2006 ,Revised 1 February 2007 ,Accepted 21 February 2007.

References 

  1. Ross R. Atherosclerosis—an inflammatory disease. N Engl J Med. 1999;340:115–126
  2. Epstein SE, Zhou YF, Zhu J. Infection and atherosclerosis: emerging mechanistic paradigms. Circulation. 1999;100:e20–e28
  3. Aronson D, Rayfield EJ. How hyperglycemia promotes atherosclerosis: molecular mechanism. Cardiovasc Diabetol. 2002;1:1475–2840
  4. Alvaro-Gonzalez LC, Freijo-Guerrero MM, Sadaba-Garay F. Inflammatory mechanisms, arteriosclerosis and ischemic stroke: clinical data and perspectives. Rev Neurol. 2002;35:452–462
  5. Gerrity RG. The role of the monocyte in atherogenesis. II. Migration of foam cells from atherosclerotic lesions. Am J Pathol. 1981;103:191–200
  6. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801–809
  7. Gosling J, Slaymaker S, Gu L, et al. MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein B. J Clin Invest. 1999;103:773–778
  8. Ikeda U, Ito T, Shimada K. Interleukin-6 and acute coronary syndrome. Clin Cardiol. 2001;24:701–704
  9. Yudkin JS, Kumari M, Humphries SE, Mohamed-Ali V. Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link?. Atherosclerosis. 2000;148:209–214
  10. Fattori E, Cappelletti M, Costa P, et al. Defective inflammatory response in interleukin 6-deficient mice. J Exp Med. 1994;180:1243–1250
  11. Ruzek MC, Miller AH, Opal SM, Pearce BD, Biron CA. Characterization of early cytokine responses and an interleukin (IL)-6-dependent pathway of endogenous glucocorticoid induction during murine cytomegalovirus infection. J Exp Med. 1997;185:1185–1192
  12. Xing Z, Gauldie J, Cox G, et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest. 1998;101:311–320
  13. Schieffer B, Selle T, Hilfiker A, et al. Impact of interleukin-6 on plaque development and morphology in experimental atherosclerosis. Circulation. 2004;110:3493–3500
  14. Huber SA, Sakkinen P, Conze D, Hardin N, Tracy R. Interleukin-6 exacerbates early atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 1999;19:2364–2367
  15. Li L, Messas E, Batista EL, Levine RA, Amar S. Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation. 2002;105:861–867
  16. Pussinen PJ, Mattila K. Periodontal infections and atherosclerosis: mere associations?. Curr Opin Lipidol. 2004;15:583–588
  17. Genco R, Offenbacher S, Beck J. Periodontal disease and cardiovascular disease: epidemiology and possible mechanisms. J Am Dent Assoc. 2002;133(Suppl):14S–22S
  18. Chi H, Messas E, Levine RA, Graves DT, Amar S. Interleukin-1 receptor signaling mediates atherosclerosis associated with bacterial exposure and/or a high-fat diet in a murine apolipoprotein E heterozygote model: pharmacotherapeutic implications. Circulation. 2004;110:1678–1685
  19. Bhanji SWB, Sheller B, Elwood T, Mancl L. Transient bacteremia induced by toothbrushing a comparison of the Sonicare toothbrush with a conventional toothbrush. Pediatr Dent. 2002;24:295–299
  20. Elhage R, Clamens S, Besnard S, et al. Involvement of interleukin-6 in atherosclerosis but not in the prevention of fatty streak formation by 17[beta]-estradiol in apolipoprotein E-deficient mice. Atherosclerosis. 2001;156:315–320
  21. Wank HALM, Rose LF, Cohen DW. A quantitative measurement of bacteremia and its relationship to plaque control. J Periodontol. 1976;47:683–686
  22. Sukovich DA, Kauser K, Shirley FD, et al. Expression of interleukin-6 in atherosclerotic lesions of male ApoE-knockout mice: inhibition by 17β-estradiol. Arterioscler Thromb Vasc Biol. 1998;18:1498–1505
  23. Palinski W, Ord VA, Plump AS, et al. ApoE-deficient mice are a model of lipoprotein oxidation in atherogenesis. Demonstration of oxidation-specific epitopes in lesions and high titers of autoantibodies to malondialdehyde-lysine in serum. Arterioscler Thromb. 1994;14:605–616
  24. Madan M, Bishayi B, Hoge M, Messas E, Amar S. Doxycycline affects diet- and bacteria-associated atherosclerosis in an ApoE heterozygote murine model: cytokine profiling implications. Atherosclerosis. 2007;190:62–72
  25. Plump AS, Smith JD, Hayek T, et al. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343–353
  26. Mallat Z, Corbaz A, Scoazec A, et al. Interleukin-18/interleukin-18 binding protein signaling modulates atherosclerotic lesion development and stability. Circ Res. 2001;89:41e–45e
  27. Lu H, Raptis M, Black E, et al. Influence of diabetes on the exacerbation of an inflammatory response in cardiovascular tissue. Endocrinology. 2004;145:4934–4939
  28. Kadokami T, McTiernan CF, Kubota T, Frye CS, Feldman AM. Sex-related survival differences in murine cardiomyopathy are associated with differences in TNF-receptor expression. J Clin Invest. 2000;106:589–597
  29. Kantarci A, Van Dyke TE. Neutrophil-mediated host response to Porphyromonas gingivalis. J Int Acad Periodontol. 2002;4:119–125
  30. Hulthe J, Fagerberg B. Circulating oxidized LDL is associated with subclinical atherosclerosis development and inflammatory cytokines (AIR Study). Arterioscler Thromb Vasc Biol. 2002;22:1162–1167
  31. Zhou Q, Desta T, Fenton M, Graves DT, Amar S. Cytokine profiling of macrophages exposed to Porphyromonas gingivalis, its lipopolysaccharide, or its FimA protein. Infect Immun. 2005;73:935–943
  32. Ross R, Glomset JA. The pathogenesis of atherosclerosis (second of two parts). N Engl J Med. 1976;295:420–425
  33. Ross R, Glomset JA. The pathogenesis of atherosclerosis (first of two parts). N Engl J Med. 1976;295:369–377
  34. Schmidt AM, Yan SD, Wautier J-L, Stern D. Activation of receptor for advanced glycation end products: a mechanism for chronic vascular dysfunction in diabetic vasculopathy and atherosclerosis. Circ Res. 1999;84:489–497
  35. Dimmeler S, Hermann C, Zeiher AM. Apoptosis of endothelial cells. Contribution to the pathophysiology of atherosclerosis?. Eur Cytokine Netw. 1998;9:697–698
  36. Hegyi L, Hardwick SJ, Siow RC, Skepper JN. Macrophage death and the role of apoptosis in human atherosclerosis. J Hematother Stem Cell Res. 2001;10:27–42
  37. Scheidegger KJ, James RW, Delafontaine P. Differential effects of low density lipoproteins on insulin-like growth factor-1 (IGF-1) and IGF-1 receptor expression in vascular smooth muscle cells. J Biol Chem. 2000;275:26864–26869
  38. Davies MJ. The composition of coronary-artery plaques. N Engl J Med. 1997;336:1312–1314
  39. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2000;20:1262–1275
  40. Mallat Z, Hugel B, Ohan J, et al. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity. Circulation. 1999;99:348–353
  41. Darlington GJ, Wilson DR, Revel M, Kelly JH. Response of liver genes to acute phase mediators. Ann NY Acad Sci. 1989;557:310–5; discussion 315–6
  42. Johnson-Tidey RR, McGregor JL, Taylor PR, Poston RN. Increase in the adhesion molecule P-selectin in endothelium overlying atherosclerotic plaques. Coexpression with intercellular adhesion molecule-1. Am J Pathol. 1994;144:952–961
  43. Kai H, Hideo Yasukawa HI, Kai M, et al., Imaizumi T Peripheral blood levels of matrix metalloproteases-2 and -9 are elevated in patients with acute coronary syndromes. J Am Coll Cardiol. 1998;32:368–372
  44. Pawlak K, Pawlak D, Mysliwiec M. Extrinsic coagulation pathway activation and metalloproteinase-2/TIMPs system are related to oxidative stress and atherosclerosis in hemodialysis patients. Thromb Haemost. 2004;92:646–653
  45. Xu X-P, Meisel SR, Ong JM, et al. Oxidized low-density lipoprotein regulates matrix metalloproteinase-9 and its tissue inhibitor in human monocyte-derived macrophages. Circulation. 1999;99:993–998

PII: S0021-9150(07)00128-1

doi: 10.1016/j.atherosclerosis.2007.02.023

Atherosclerosis
Volume 197, Issue 2 , Pages 504-514 , April 2008

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