Metformin inhibits nuclear factor κb activation and decreases serum high-sensitivity C-reactive protein level in experimental atherogenesis of rabbits

Heart and Vessels

Volumn 24, Issue 6, 2009, Pages 446-453

  Li, Song Nan ^a   Wang, Xiang ^a   Zeng, Qiu Tang ^a   Feng, Yi Bai ^a   Cheng, Xiang ^a   Mao, Xiao Bo ^a   Wang, Tian Hong ^a   Deng, He Ping ^b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Atherosclerosis; High sensitivity C reactive protein; Inflammation; Metformin; Nuclear factor B

Indexed keywords

C REACTIVE PROTEIN; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID; METFORMIN; TRANSCRIPTION FACTOR RELA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIATHEROGENIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; AORTA ATHEROSCLEROSIS; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFICACY; EXPERIMENTAL RABBIT; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; LIPID BLOOD LEVEL; MALE; MORPHOMETRICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ANIMALS; ANTI-INFLAMMATORY AGENTS; AORTA; ATHEROSCLEROSIS; BIOLOGICAL MARKERS; BLOOD GLUCOSE; BLOTTING, WESTERN; C-REACTIVE PROTEIN; DISEASE MODELS, ANIMAL; DOWN-REGULATION; I-KAPPA B PROTEINS; IMMUNOHISTOCHEMISTRY; LIPIDS; MALE; METFORMIN; PHOSPHORYLATION; RABBITS; TIME FACTORS; TRANSCRIPTION FACTOR RELA;

EID: 71049169591     PISSN: 09108327     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00380-008-1137-7     Document Type: Article

References (50)

1. R. Ross 1999 Atherosclerosis: an inflammatory disease N Engl J Med 340 115 126 10.1056/NEJM199901143400207 1:STN:280:DyaK1M%2FptFSqtQ%3D%3D 9887164 (Pubitemid 29054847)
2. P. Libby 2002 Inflammation in atherosclerosis Nature 420 868 874 10.1038/nature01323 1:CAS:528:DC%2BD38XpsFygtb8%3D 12490960 (Pubitemid 36019640)
3. G.K. Hansson 2005 Inflammation, atherosclerosis, and coronary artery disease N Engl J Med 352 1685 1695 10.1056/NEJMra043430 1:CAS:528: DC%2BD2MXjsFCltrc%3D 15843671 (Pubitemid 40530235)
4. G.K. Hansson P. Libby U. Schonbeck Z.-Q. Yan 2002 Innate and adaptive immunity in the pathogenesis of atherosclerosis Circ Res 91 281 291 10.1161/01.RES.0000029784.15893.10 1:CAS:528:DC%2BD38XntVKktro%3D 12193460 (Pubitemid 34976993)
5. M.P. de Winther E. Kanters G. Kraal M.H. Hofker 2005 Nuclear factor kappaB signaling in atherogenesis Arterioscler Thromb Vasc Biol 25 904 914 10.1161/01.ATV.0000160340.72641.87 15731497 (Pubitemid 40627833)
6. K. Brand S. Page G. Rogler A. Bartsch R. Brandl R. Knuechel M. Page C. Kaltschmidt P.A. Baeuerle D. Neumeier 1996 Activated transcription factor nuclear factor-kappa B is present in the atherosclerotic lesion J Clin Invest 97 7 1715 1722 10.1172/JCI118598 1:CAS:528:DyaK28XitVCktrk%3D 8601637
7. S.H. Wilson N.M. Caplice R.D. Simari D.R. Holmes Jr P.J. Carlson A. Lerman 2000 Activated nuclear factor-κB is present in the coronary vasculature in experimental hypercholesterolemia Atherosclerosis 148 23 30 10.1016/S0021-9150(99)00211-7 1:CAS:528:DyaK1MXns1ansLg%3D 10580167
8. J. Jawień M. Gajda Mateuszuk R. Olszanecki A. Jakubowski A. Szlachcic M. Korabiowska R. Korbut 2005 Inhibition of nuclear factor-kappaB attenuates arthrosclerosis in apoE/lDLR-double knockout mice J Physiol Pharmacol 56 3 483 489 16204769
9. C. Monaco E. Paleolog 2004 Nuclear factor kappaB: a potential therapeutic target in atherosclerosis and thrombosis Cardiovasc Res 61 4 671 682 10.1016/j.cardiores.2003.11.038 1:CAS:528:DC%2BD2cXhsVOlsbc%3D 14985064 (Pubitemid 38249466)
10. J. Danesh J.G. Wheeler G.M. Hirschfield S. Eda G. Eiriksdottir A. Rumley G.D. Lowe M.B. Pepys V. Gudnason 2004 C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease N Engl J Med 350 1387 1397 10.1056/NEJMoa032804 1:CAS:528:DC%2BD2cXivVagsbc%3D 15070788 (Pubitemid 38419992)
11. I. Jialal S. Devaraj S.K. Venugopal 2004 C-reactive protein: risk marker or mediator in atherothrombosis Hypertension 44 6 11 10.1161/01.HYP.0000130484. 20501.df 1:CAS:528:DC%2BD2cXltVSqt7w%3D 15148294 (Pubitemid 38823477)
12. J.C. Mamputu N.F. Wiernsperger G. Renier 2003 Antiatherogenic properties of metformin: the experimental evidence Diabetes Metab 29 6S71 6S76 1:CAS:528:DC%2BD2cXitVCksro%3D 14502103
13. Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group (1998) Lancet 352:854-865
14. X.Y. Yang L. Wang H.S. Zeng N. Zhou J. Pu Y.H. Yuan 2006 Effects of simvastatin on nuclear factor κB-DNA binding activity and matrix metalloproteinase-1 and 3 protein expression in atherosclerosis model of rabbit J Huazhong Univ Sci Technol Med Sci 26 2 194 198 1:CAS:528:DC%2BD28Xps1KhtL0%3D 16850745
15. H. Nandeesha B.C. Koner L.N. Dorairajan S.K. Sen 2006 Hyperinsulinemia and dyslipidemia in non-diabetic benign prostatic hyperplasia Clin Chim Acta 370 1-2 89 93 10.1016/j.cca.2006.01.019 1:CAS:528:DC%2BD28XntlWnt74%3D 16516184 (Pubitemid 44080171)
16. R. Ross 1995 Cell biology of atherosclerosis Ann Rev Physiol 57 791 804 10.1146/annurev.ph.57.030195.004043 1:CAS:528:DyaK2MXksVeqsbY%3D
17. U. Siebenlist G. Franzoso K. Brown 1994 Structure, regulation and function of NF-kappa B Annu Rev Cell Biol 10 405 455 10.1146/annurev.cb.10. 110194.002201 1:CAS:528:DyaK2MXitlSnsb8%3D 7888182
18. R. Sen D. Baltimore 1986 Multiple nuclear factors interact with the immunoglobulin enhancer sequences Cell 46 705 716 10.1016/0092-8674(86)90346-6 1:CAS:528:DyaL28XmtVCjs74%3D 3091258
19. R. Sen D. Baltimore 1986 Inducibility of kappa immunoglobulin enhancer-binding protein NF-kappa B by a posttranslational mechanism Cell 47 921 928 10.1016/0092-8674(86)90807-X 1:CAS:528:DyaL2sXot1Oltw%3D%3D 3096580
20. M.S. Hayden S. Ghosh 2004 Signaling to NF-kappaB Genes Dev 18 2195 2224 10.1101/gad.1228704 1:CAS:528:DC%2BD2cXnslCntbY%3D 15371334 (Pubitemid 39209568)
21. Y. Yamamoto R.B. Gaynor 2004 IkappaB kinases: key regulators of the NF-kappaB pathway Trends Biochem Sci 29 72 79 10.1016/j.tibs.2003.12.003 1:CAS:528:DC%2BD2cXhtVOrtr8%3D 15102433 (Pubitemid 38186577)
22. A.S. Baldwin 2001 The transcription factor NF-kappa B and human disease J Clin Invest 107 3 6 10.1172/JCI11891 1:CAS:528:DC%2BD3MXitVOhsQ%3D%3D 11134170
23. S. Ghosh M. Karin 2001 Missing pieces in the NF-kappaB puzzle Cell 109 suppl S81 S96
24. M.E. Ritchie 1998 Nuclear factor-κB is selectively and markedly activated in humans with unstable angina pectoris Circulation 98 1707 1713 1:CAS:528:DyaK1cXnt1KlsrY%3D 9788823
25. P.M. Ridker 2003 High-sensitivity C-reactive protein and cardiovascular risk: rational for screening and primary prevention Am J Cardiol 92 suppl 17k 22k 10.1016/S0002-9149(03)00774-4 1:CAS:528:DC%2BD3sXnvVSht70%3D 12948872
26. V. Pasceri J. Willerson E. Yeh 2000 Direct proinflammatory effect of C-reactive protein on human endothelial cells Circulation 102 2165 2168 1:CAS:528:DC%2BD3cXptVSjtbk%3D 11056086
27. Y. Hattori M. Matsumura K. Kasai 2003 Vascular smooth muscle cell activation by C-reactive protein Cardiovasc Res 58 1 186 195 10.1016/S0008-6363(02)00855-6 1:CAS:528:DC%2BD3sXit12gtrY%3D 12667961 (Pubitemid 36351637)
28. T. Zwaka V. Hombach J. Torzewski 2001 C-reactive proteinmediated low density lipoprotein uptake by macrophages: implications for atherosclerosis Circulation 103 1194 1197 1:CAS:528:DC%2BD3MXisFeksLo%3D 11238260
29. S. Verma M.A. Kuliszewski S.H. Li P.E. Szmitko L. Zucco C.H. Wang M.V. Badiwala D.A. Mickle R.D. Weisel P.W. Fedak D.J. Stewart M.J. Kutryk 2004 C-reactive protein attenuates endothelial progenitor cell survival, differentiation, and function: further evidence of a mechanistic link between C-reactive protein and cardiovascular disease Circulation 109 2058 2067 10.1161/01.CIR.0000127577.63323.24 1:CAS:528:DC%2BD2cXjsVWqsr0%3D 15078802 (Pubitemid 38620212)
30. J. Torzewski M. Torzewski D.E. Bowyer M. Frohlich W. Koenig J. Waltenberger C. Fitzsimmons V. Hombach 1998 C-reactive protein frequently colocalizes with the terminal complement complex in the intima of early atherosclerotic lesions of human coronary arteries Arterioscler Thromb Vasc Biol 18 1386 1392 1:CAS:528:DyaK1cXmtlyitbo%3D 9743226
31. A. Paul K.W. Ko L. Li V. Yechoor M.A. McCrory A.J. Szalai L. Chan 2004 C-reactive protein accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice Circulation 109 5 647 655 10.1161/01.CIR. 0000114526.50618.24 1:CAS:528:DC%2BD2cXos1emtQ%3D%3D 14744975 (Pubitemid 38198873)
32. IDF Clinical Guidelines Task Force 2006 Global guidelines for type 2 diabetes: recommendations for standard, comprehensive, and minimal care Diabet Med 23 579 593 10.1111/j.1464-5491.2006.01918.x (Pubitemid 43830058)
33. N.F. Wiernsperger C.J. Bailey 1999 The antihyperglycaemic effect of metformin: therapeutic and cellular mechanisms Drugs 58Suppl1 31 9 10.2165/00003495-199958001-00009
34. Gin H, Roudaut MF, Vergnot V, Baillet L, Rigalleau V Effect of metformin on fibrinolytic parameters in insulin-treated, type 2 diabetic patients. Diabetes Metab 29(5):505-508
35. D.K. Nagi J.S. Yudkin 2003 Effects of metformin on insulin resistance, risk factors for cardiovascular disease, and plasminogen activator inhibitor in NIDDM subjects: a study of two ethnic groups Diabetes Care 16 4 621 629 10.2337/diacare.16.4.621
36. C. Vitale G. Mercuro A. Cornoldi M. Fini M. Volterrani G.M. Rosano 2005 Metformin improves endothelial function in patients with metabolic syndrome J Intern Med 258 3 250 256 10.1111/j.1365-2796.2005.01531.x 1:CAS:528: DC%2BD2MXhtVOrtL7I 16115299 (Pubitemid 41243057)
37. Y. Tanaka H. Iwamoto T. Onuma R. Kawamari 1997 Inhibitory effect of metformin on formation of advanced glycation end products Curr Ther Res 58 10 693 697 10.1016/S0011-393X(97)80103-8 1:CAS:528:DyaK2sXnsV2jtrc%3D (Pubitemid 27497617)
38. S. Schoonbroodt J. Piette 1997 Oxidative stress interference with the nuclear factor-kappa B activation pathways Biochem Pharmacol 60 8 1075 1083 10.1016/S0006-2952(00)00371-3
39. C.R. Sirtori A. Catapano G.C. Ghiselli A.L. Innocenti J. Rodriguez 1977 Metformin: an antiatherosclerotic agent modifying very low density lipoproteins in rabbits Atherosclerosis 26 79 89 10.1016/0021-9150(77)90142-3 1:CAS:528:DyaE2sXotlOrug%3D%3D 189780 (Pubitemid 8005110)
40. E. Tremoli G. Ghiselli P. Maderna S. Colli C.R. Sirtori 1982 Metformin reduces platelet hypersensitivity in hypercholesterolemic rabbits Atherosclerosis 41 53 60 10.1016/0021-9150(82)90069-7 1:CAS:528: DyaL38XktlehtL8%3D 7073794
41. S.A. Ewis M.S. Abdel-Rahman 1995 Effect of metformin on glutathione and magnesium in normal and streptozotocin-induced diabetic rats J Appl Toxicol 15 387 390 10.1002/jat.2550150508 1:CAS:528:DyaK2MXotlKrtL8%3D 8666722
42. M. Bartnik L. Rydén R. Ferrari K. Malmberg K. Pyorala M. Simoons E. Standl J. Soler-Soler J. Öhrvik 2004 The prevalence of abnormal glucose regulation in patients with coronary artery disease across Europe: The Euro Heart Survey on diabetes and the heart Eur Heart J 25 1880 1890 10.1016/j.ehj.2004.07.027 1:CAS:528:DC%2BD2cXptFOgt7k%3D 15522466 (Pubitemid 39452604)
43. D.Y. Hu C.Y. Pan J.M. Yu 2006 The relationship between coronary artery disease and abnormal glucose regulation in China: the China Heart Survey Eur Heart J 27 2573 2579 10.1093/eurheartj/ehl207 1:CAS:528:DC%2BD28XhtlanurnE 16984927 (Pubitemid 44627302)
44. N. Fujii K. Tsuchihashi H. Sasao M. Eguchi H. Miurakami M. Hase K. Higashiura S. Yuda A. Hashimoto T. Miura N. Ura K. Shimamoto 2008 Insulin resistance functionally limits endothelium-dependent coronary vasodilation in nondiabetic patients Heart Vessels 23 1 9 15 10.1007/s00380-007-1002-0 18273540 (Pubitemid 351276810)
45. K.E. Wellen G.S. Hotamisligil 2005 Inflammation, stress, and diabetes J Clin Invest 115 5 1111 1119 1:CAS:528:DC%2BD2MXktFSksbY%3D 15864338
46. N. Ozer B. Tangurek F. Firat S. Ozer Z. Tartan R. Ozturk B. Ozay F. Ciloglu H. Yilmaz N. Cam 2008 Effects of drug-eluting stents on systemic inflammatory response in patients with unstable angina pectoris undergoing percutaneous coronary intervention Heart Vessels 23 2 75 82 10.1007/s00380-007- 1020-y 18389330
47. J. De Jager A. Kooy P. Lehert D. Bets M.G. Wulffele T. Teerlink P.G. Scheffer C.G. Schalkwijk A.J. Donker C.D. Stehouwer 2005 Effects of short-term treatment with metformin on markers of endothelial function and inflammatory activity in type 2 diabetes mellitus: a randomized, placebo-controlled trial J Intern Med 257 100 109 10.1111/j.1365-2796.2004.01420.x 15606381 (Pubitemid 40129131)
48. K. Isoda J.L. Young A. Zirlik L.A. MacFarlane N. Tsuboi N. Gerdes U. Schonbeck P. Libby 2006 Metformin inhibits proinflammatory responses and nuclear factor-κB in human vascular wall cells Arterioscler Thromb Vasc Biol 26 611 617 10.1161/01.ATV.0000201938.78044.75 1:CAS:528:DC%2BD28XisFarurw%3D 16385087
49. Y. Hattori K. Suzuki S. Hattori K. Kasai 2006 Metformin inhibits cytokine-induced nuclear factor kappaB activation via AMP-activated protein kinase activation in vascular endothelial cells Hypertension 47 1183 1188 10.1161/01.HYP.0000221429.94591.72 1:CAS:528:DC%2BD28XksVOmu7s%3D 16636195 (Pubitemid 44289177)
50. G. Pilon P. Dallaire A. Marette 2004 Inhibition of inducible nitric-oxide synthase by activators of AMP-activated protein kinase: a new mechanism of action of insulin-sensitizing drugs J Biol Chem 279 20 20767 20774 10.1074/jbc.M401390200 1:CAS:528:DC%2BD2cXjvV2ns7o%3D 14985344 (Pubitemid 38656473)