Nitric oxide-donating atorvastatin attenuates neutrophil recruitment during vascular inflammation independent of changes in plasma cholesterol

Cardiovascular Drugs and Therapy

Volumn 27, Issue 3, 2013, Pages 211-219

  Baetta, Roberta ^a,c   Granata, Agnese ^a   Miglietta, Daniela ^b   Oliva, Francesca ^b   Arnaboldi, Lorenzo ^a   Bonomo, Alessandra ^a   Ferri, Nicola ^a   Ongini, Ennio ^b   Bellosta, Stefano ^a   Corsini, Alberto ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b NicOx Research Institute   (Italy)

^c CENTRO CARDIOLOGICO MONZINO   (Italy)

Author keywords

Atherosclerosis; Inflammation; Leukocytes; NCX 6560; Neutrophil (polymorphonuclear leukocyte PMN ); Nitric oxide; NO statins; Statins

Indexed keywords

4 (NITROOXY)BUTYL 7 [2 (4 FLUOROPHENYL) 5 ISOPROPYL 3 PHENYL 4 (PHENYLCARBAMOYL) 1H PYRROL 1 YL] 3,5 DIHYDROXYHEPTANOATE; ATORVASTATIN; CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INTERLEUKIN 8; NCX 6560; UNCLASSIFIED DRUG; HEPTANOIC ACID DERIVATIVE; NITRIC OXIDE DONOR; PYRROLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CAROTID ARTERY; CELL MIGRATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG EFFECT; ENDOTHELIUM CELL; EXPERIMENTAL RABBIT; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL COUNT; NONHUMAN; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; VASCULITIS; ACUTE DISEASE; ANIMAL; ATHEROSCLEROSIS; BLOOD; CELL SURVIVAL; CHEMICAL STRUCTURE; CYTOLOGY; IMMUNOLOGY; MONOCYTE; NEUTROPHIL; PATHOLOGY; RABBIT; UMBILICAL VEIN ENDOTHELIAL CELL;

ACUTE DISEASE; ANIMALS; ATHEROSCLEROSIS; CAROTID ARTERIES; CELL SURVIVAL; CHEMOTAXIS, LEUKOCYTE; CHOLESTEROL; HEPTANOIC ACIDS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERLEUKIN-8; MALE; MOLECULAR STRUCTURE; MONOCYTES; NEUTROPHIL INFILTRATION; NEUTROPHILS; NITRIC OXIDE DONORS; PYRROLES; RABBITS;

EID: 84887360636     PISSN: 09203206     EISSN: 15737241     Source Type: Journal    
DOI: 10.1007/s10557-013-6445-1     Document Type: Article

References (40)

1. World Health Organization (WHO). Cardiovascular diseases (CVDs). Fact sheet N.°317, September 2011. http://www.who.int/ mediacentre/factsheets/ fs317/en/index.html
2. Allender S, Scarborough P, Peto V, et al. European cardiovascular disease statistics 2008 ed. EH Network; 2008
3. Baigent C, Blackwell L, Emberson J, et al. Efficacy and safety of more intensive lowering of LDL cholesterol: a meta-analysis of data from 170,000 participants in 26 randomised trials. Lancet. 2010;376:1670-81.
4. Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med. 2011;17:1410-22.
5. Tedgui A. Focus on inflammation. Arterioscler Thromb Vasc Biol. 2011;31:958-9.
6. Charo IF, Taub R. Anti-inflammatory therapeutics for the treatment of atherosclerosis. Nat Rev Drug Discov. 2011;10:365-76.
7. Zernecke A, Bot I, Djalali-Talab Y, et al. Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res. 2008;102:209-17.
8. Drechsler M, Megens RT, van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation. 2010;122:1837-45.
9. Baetta R, Corsini A. Role of polymorphonuclear neutrophils in atherosclerosis: Current state and future perspectives. Atherosclerosis. 2010;210:1-13.
10. Murphy AJ, Woollard KJ, Suhartoyo A, et al. Neutrophil activation is attenuated by high-density lipoprotein and apolipoprotein A-I in in vitro and in vivo models of inflammation. Arterioscler Thromb Vasc Biol. 2011;31:1333-41.
11. Nicholls SJ, Dusting GJ, Cutri B, et al. Reconstituted high-density lipoproteins inhibit the acute pro-oxidant and proinflammatory vascular changes induced by a periarterial collar in normocholesterolemic rabbits. Circulation. 2005;111:1543-50.
12. Puranik R, Bao S, Nobecourt E, et al. Low dose apolipoprotein A-I rescues carotid arteries from inflammation in vivo. Atherosclerosis. 2008;196:240-7.
13. Wu BJ, Yan L, Charlton F, et al. Evidence that niacin inhibits acute vascular inflammation and improves endothelial dysfunction independent of changes in plasma lipids. Arterioscler Thromb Vasc Biol. 2010;30:968-75.
14. Murad F. Shattuck Lecture. Nitric oxide and cyclic GMP in cell signaling and drug development. N Engl J Med. 2006;355:2003-11.
15. Pepine CJ. The impact of nitric oxide in cardiovascular medicine: untapped potential utility. Am J Med. 2009;122:S10-5.
16. Maskrey BH, Megson IL, Whitfield PD, Rossi AG. Mechanisms of resolution of inflammation: a focus on cardiovascular disease. Arterioscler Thromb Vasc Biol. 2011;31:1001-6.
17. Bolla M, Almirante N, Benedini F. Therapeutic potential of nitrate esters of commonly used drugs. Curr TopMed Chem. 2005;5:707-20.
18. Ongini E, Impagnatiello F, Bonazzi A, et al. Nitric oxide (NO)- releasing statin derivatives, a class of drugs showing enhanced antiproliferative and antiinflammatory properties. Proc Natl Acad Sci U S A. 2004;101:8497-502.
19. Rossiello MR, Momi S, Caracchini R, et al. A novel nitric oxidereleasing statin derivative exerts an antiplatelet/antithrombotic activity and inhibits tissue factor expression. J Thromb Haemost. 2005;3:2554-62.
20. Momi S, Impagnatiello F, Guzzetta M, et al. NCX 6560, a nitric oxide-releasing derivative of atorvastatin, inhibits cholesterol biosynthesis and shows anti-inflammatory and anti-thrombotic properties. Eur J Pharmacol. 2007;570:115-24.
21. Emanueli C, Monopoli A, Kraenkel N, et al. Nitropravastatin stimulates reparative neovascularisation and improves recovery from limb Ischaemia in type-1 diabetic mice. Br J Pharmacol. 2007;150:873-82.
22. Dever G, Spickett CM, Kennedy S, et al. The nitric oxide-donating pravastatin derivative, NCX 6550 [(1S-[1alpha(betaS*, deltaS*), 2alpha, 6alpha, 8beta-(R*), 8a alpha]]-1,2,6,7,8,8a-Hexahydro-beta, delta, 6-trihydroxy-2-methyl-8-(2-methyl-1-oxobutoxy)-1-naphtalene- heptanoic acid 4-(nitrooxy)butyl ester)], reduces splenocyte adhesion and reactive oxygen species generation in normal and atherosclerotic mice. J Pharmacol Exp Ther. 2007;320:419-26.
23. Amoruso A, Bardelli C, Fresu LG, et al. The nitric oxide-donating pravastatin, NCX 6550, inhibits cytokine release and NF-kappaB activation while enhancing PPARgamma expression in human monocyte/macrophages. Pharmacol Res. 2010;62:391-9.
24. Mangialardi G, Monopoli A, Ongini E, et al. Nitric oxide-donating statin improves multiple functions of circulating angiogenic cells. Br J Pharmacol. 2011;164:570-83.
25. Momi S, Monopoli A, Alberti PF, et al. Nitric oxide enhances the antiinflammatory and anti-atherogenic activity of atorvastatin in a mouse model of accelerated atherosclerosis. Cardiovasc Res. 2012;94:428-38.
26. Djian JP, Maucci R, Guilmin L, Ferreira T, Pfister P. NCX 6560, a Novel Nitric Oxyde Donating Atorvastatin With a Promising Safety and Efficacy Profile: A Randomised. Double Blind Placebo and Active Control Study. Circulation. 2010;122:A14267.
27. Donetti E, Baetta R, Comparato C, et al. Polymorphonuclear leukocyte-myocyte interaction: an early event in collar-induced rabbit carotid intimal thickening. Exp Cell Res. 2002;274:197-206.
28. Baetta R, Camera M, Comparato C, et al. Fluvastatin reduces tissue factor expression and macrophage accumulation in carotid lesions of cholesterol-fed rabbits in the absence of lipid lowering. Arterioscler Thromb Vasc Biol. 2002;22:692-8.
29. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest. 1973;52:2745-56.
30. Arnaboldi L, Baetta R, Ferri N, et al. Inhibition of smooth muscle cell migration and proliferation by statins. Immunology, Endocrine and Metabolic Agents - Medicinal Chemistry. 2008;8:122-40.
31. Lea AP, McTavish D. Atorvastatin. A review of its pharmacology and therapeutic potential in the management of hyperlipidaemias. Drugs. 1997;53:828-47.
32. Stern RH, Yang BB, Hounslow NJ, et al. Pharmacodynamics and pharmacokinetic-pharmacodynamic relationships of atorvastatin, an HMG-CoA reductase inhibitor. J Clin Pharmacol. 2000;40:616-23.
33. Bevilacqua MP. Endothelial-leukocyte adhesion molecules. Annu Rev Immunol. 1993;11:767-804.
34. Kasama T, Strieter RM, Standiford TJ, Burdick MD, Kunkel SL. Expression and regulation of human neutrophil-derived macrophage inflammatory protein 1 alpha. J Exp Med. 1993;178:63-72.
35. Soehnlein O, Zernecke A, Eriksson EE, et al. Neutrophil secretion products pave the way for inflammatory monocytes. Blood. 2008;112:1461-71.
36. Pruefer D, Scalia R, Lefer AM. Simvastatin inhibits leukocyteendothelial cell interactions and protects against inflammatory processes in normocholesterolemic rats. Arterioscler Thromb Vasc Biol. 1999;19:2894-900.
37. Pruefer D, Makowski J, Schnell M, et al. Simvastatin inhibits inflammatory properties of Staphylococcus aureus alpha-toxin. Circulation. 2002;106:2104-10.
38. Scalia R, Gooszen ME, Jones SP, et al. Simvastatin exerts both anti-inflammatory and cardioprotective effects in apolipoprotein Edeficient mice. Circulation. 2001;103:2598-603.
39. Nakamura K, Sasaki T, Cheng XW, et al. Statin prevents plaque disruption in apoE-knockout mouse model through pleiotropic effect on acute inflammation. Atherosclerosis. 2009;206:355-61.
40. Stenmark KR, Yeager ME, El Kasmi KC, et al. The adventitia: essential regulator of vascular wall structure and function. Annu Rev Physiol. 2013; vol. 75. epub 12/12/2012