Nitric oxide-donating statin improves multiple functions of circulating angiogenic cells

British Journal of Pharmacology

Volumn 164, Issue 2 B, 2011, Pages 570-583

  Mangialardi, G ^a   Monopoli, A ^b   Ongini, E ^b   Spinetti, G ^c   Fortunato, O ^c   Emanueli, C ^a   Madeddu, P ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b Nicox Research Institute   (Italy)

^c IRCCS MULTIMEDICA   (Italy)

Author keywords

angiogenesis; circulating angiogenic cells; diabetes; NO; statin

Indexed keywords

6 (NITROOXY)HEXYL 7 [2 (4 FLUOROPHENYL) 5 ISOPROPYL 3 PHENYL 4 (PHENYLCARBAMOYL) 1H PYRROL 1 YL] 3,5 DIHYDROXYHEPTANOATE; ATORVASTATIN; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; METFORMIN; NCX 547; NITRIC OXIDE DONOR; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ADULT; AGED; APOPTOSIS; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL GROWTH; CELL MIGRATION; CELL VIABILITY; CIRCULATING ANGIOGENIC CELL; CLINICAL ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; DRUG EFFICACY; DRUG STRUCTURE; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SENESCENCE;

AGED; ANTICHOLESTEREMIC AGENTS; APOPTOSIS; BENZOATES; CARDIOVASCULAR AGENTS; CARDIOVASCULAR DISEASES; CELL AGING; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; IMIDAZOLES; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; NEOVASCULARIZATION, PHYSIOLOGIC; NITRATES; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE III; ORNITHINE; PROTO-ONCOGENE PROTEINS C-AKT; PYRROLES; STEM CELLS;

EID: 80052226689     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01423.x     Document Type: Article

References (53)

1. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, et al,. (2003). Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9: 1370-1376. (Pubitemid 37466185)
2. Assmus B, Urbich C, Aicher A, Hofmann WK, Haendeler J, Rossig L, et al,. (2003). HMG-CoA reductase inhibitors reduce senescence and increase proliferation of endothelial progenitor cells via regulation of cell cycle regulatory genes. Circ Res 92: 1049-1055. (Pubitemid 36588505)
3. Assmus B, Fischer-Rasokat U, Honold J, Seeger FH, Fichtlscherer S, Tonn T, et al,. (2007). Transcoronary transplantation of functionally competent BMCs is associated with a decrease in natriuretic peptide serum levels and improved survival of patients with chronic postinfarction heart failure: results of the TOPCARE-CHD Registry. Circ Res 100: 1234-1241. (Pubitemid 46684137)
4. Bao XM, Wu CF, Lu GP, (2010). Atorvastatin inhibits homocysteine-induced dysfunction and apoptosis in endothelial progenitor cells. Acta Pharmacol Sin 31: 476-484.
5. Baraldi PG, Fruttarolo F, Tabrizi MA, Romagnoli R, Preti D, Bovero A, et al,. (2004a). Synthesis and biological evaluation of novel N6-[4-(substituted) sulfonamidophenylcarbamoyl]adenosine-5′-uronamides as A3 adenosine receptor agonists. J Med Chem 47: 5535-5540. (Pubitemid 39382800)
6. Baraldi PG, Romagnoli R, Del Carmen Nunez M, Perretti M, Paul-Clark MJ, Ferrario M, et al,. (2004b). Synthesis of nitro esters of prednisolone, new compounds combining pharmacological properties of both glucocorticoids and nitric oxide. J Med Chem 47: 711-719. (Pubitemid 38129728)
7. Bolla M, Almirante N, Benedini F, (2005). Therapeutic potential of nitrate esters of commonly used drugs. Curr Top Med Chem 5: 707-720. (Pubitemid 41179729)
8. Borghi V, Bastia E, Guzzetta M, Chiroli V, Toris CB, Batugo MR, et al,. (2010). A novel nitric oxide releasing prostaglandin analog, NCX 125, reduces intraocular pressure in rabbit, dog, and primate models of glaucoma. J Ocul Pharmacol Ther 26: 125-132.
9. Boyle AJ, Whitbourn R, Schlicht S, Krum H, Kocher A, Nandurkar H, et al,. (2006). Intra-coronary high-dose CD34+ stem cells in patients with chronic ischemic heart disease: a 12-month follow-up. Int J Cardiol 109: 21-27.
10. Chen YH, Lin SJ, Lin FY, Wu TC, Tsao CR, Huang PH, et al,. (2007). High glucose impairs early and late endothelial progenitor cells by modifying nitric oxide-related but not oxidative stress-mediated mechanisms. Diabetes 56: 1559-1568.
11. Crawford JH, Isbell TS, Huang Z, Shiva S, Chacko BK, Schechter AN, et al,. (2006). Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood 107: 566-574. (Pubitemid 43076380)
12. Dimmeler S, Aicher A, Vasa M, Mildner-Rihm C, Adler K, Tiemann M, et al,. (2001). HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J Clin Invest 108: 391-397. (Pubitemid 32730785)
13. Emanueli C, Monopoli A, Kraenkel N, Meloni M, Gadau S, Campesi I, et al,. (2007). Nitropravastatin stimulates reparative neovascularisation and improves recovery from limb Ischaemia in type-1 diabetic mice. Br J Pharmacol 150: 873-882. (Pubitemid 46536620)
14. Fujii T, Onimaru M, Yonemitsu Y, Kuwano H, Sueishi K, (2008). Statins restore ischemic limb blood flow in diabetic microangiopathy via eNOS/NO upregulation but not via PDGF-BB expression. Am J Physiol Heart Circ Physiol 294: H2785-H2791.
15. Handa O, Stephen J, Cepinskas G, (2008). Role of endothelial nitric oxide synthase-derived nitric oxide in activation and dysfunction of cerebrovascular endothelial cells during early onsets of sepsis. Am J Physiol Heart Circ Physiol 295: H1712-H1719.
16. Iwakura A, Shastry S, Luedemann C, Hamada H, Kawamoto A, Kishore R, et al,. (2006). Estradiol enhances recovery after myocardial infarction by augmenting incorporation of bone marrow-derived endothelial progenitor cells into sites of ischemia-induced neovascularization via endothelial nitric oxide synthase-mediated activation of matrix metalloproteinase-9. Circulation 113: 1605-1614. (Pubitemid 43739420)
17. Kawasaki K, Smith RS Jr, Hsieh CM, Sun J, Chao J, Liao JK, (2003). Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol Cell Biol 23: 5726-5737. (Pubitemid 36951336)
18. Kawashima S, Yokoyama M, (2004). Dysfunction of endothelial nitric oxide synthase and atherosclerosis. Arterioscler Thromb Vasc Biol 24: 998-1005. (Pubitemid 38737823)
19. Krankel N, Adams V, Linke A, Gielen S, Erbs S, Lenk K, et al,. (2005). Hyperglycemia reduces survival and impairs function of circulating blood-derived progenitor cells. Arterioscler Thromb Vasc Biol 25: 698-703. (Pubitemid 40463856)
20. Krankel N, Katare RG, Siragusa M, Barcelos LS, Campagnolo P, Mangialardi G, et al,. (2008). Role of kinin B2 receptor signaling in the recruitment of circulating progenitor cells with neovascularization potential. Circ Res 103: 1335-1343.
21. Krankel N, Armstrong SP, McArdle CA, Dayan C, Madeddu P, (2010). Distinct kinin-induced functions are altered in circulating cells of young type 1 diabetic patients. PLoS ONE 5: e11146.
22. Kuki S, Imanishi T, Kobayashi K, Matsuo Y, Obana M, Akasaka T, (2006). Hyperglycemia accelerated endothelial progenitor cell senescence via the activation of p38 mitogen-activated protein kinase. Circ J 70: 1076-1081. (Pubitemid 44161749)
23. Landmesser U, Engberding N, Bahlmann FH, Schaefer A, Wiencke A, Heineke A, et al,. (2004). Statin-induced improvement of endothelial progenitor cell mobilization, myocardial neovascularization, left ventricular function, and survival after experimental myocardial infarction requires endothelial nitric oxide synthase. Circulation 110: 1933-1939. (Pubitemid 39331904)
24. Liang C, Ren Y, Tan H, He Z, Jiang Q, Wu J, et al,. (2009). Rosiglitazone via upregulation of Akt/eNOS pathways attenuates dysfunction of endothelial progenitor cells, induced by advanced glycation end products. Br J Pharmacol 158: 1865-1873.
25. Llevadot J, Murasawa S, Kureishi Y, Uchida S, Masuda H, Kawamoto A, et al,. (2001). HMG-CoA reductase inhibitor mobilizes bone marrow-derived endothelial progenitor cells. J Clin Invest 108: 399-405. (Pubitemid 32730786)
26. Loomans CJ, de Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, de Boer HC, et al,. (2004). Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53: 195-199. (Pubitemid 38044715)
27. Madeddu P, Kraenkel N, Barcelos LS, Siragusa M, Campagnolo P, Oikawa A, et al,. (2008). Phosphoinositide 3-kinase gamma gene knockout impairs postischemic neovascularization and endothelial progenitor cell functions. Arterioscler Thromb Vasc Biol 28: 68-76.
28. Momi S, Impagnatiello F, Guzzetta M, Caracchini R, Guglielmini G, Olivieri R, et al,. (2007). NCX 6560, a nitric oxide-releasing derivative of atorvastatin, inhibits cholesterol biosynthesis and shows anti-inflammatory and anti-thrombotic properties. Eur J Pharmacol 570: 115-124. (Pubitemid 47247669)
29. Moncada S, Higgs A, Furchgott R, (1997). International Union of Pharmacology Nomenclature in Nitric Oxide Research. Pharmacol Rev 49: 137-142. (Pubitemid 27291031)
30. Ohkawara H, Ishibashi T, Saitoh SI, Inoue N, Sugimoto K, Kamioka M, et al,. (2010). Preventive effects of pravastatin on thrombin-triggered vascular responses via Akt/eNOS and RhoA/Rac1 pathways in vivo. Cardiovasc Res 88: 492-501.
31. Ongini E, Impagnatiello F, Bonazzi A, Guzzetta M, Govoni M, Monopoli A, et al,. (2004). Nitric oxide (NO)-releasing statin derivatives, a class of drugs showing enhanced antiproliferative and antiinflammatory properties. Proc Natl Acad Sci USA 101: 8497-8502. (Pubitemid 38736603)
32. Potente M, Urbich C, Sasaki K, Hofmann WK, Heeschen C, Aicher A, et al,. (2005). Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest 115: 2382-2392. (Pubitemid 41266200)
33. Qiao W, Niu L, Liu Z, Qiao T, Liu C, (2010). Endothelial nitric oxide synthase as a marker for human endothelial progenitor cells. Tohoku J Exp Med 221: 19-27.
34. Rehman J, Li J, Orschell CM, March KL, (2003). Peripheral blood 'endothelial progenitor cells' are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107: 1164-1169. (Pubitemid 36297209)
35. Sasaki K, Heeschen C, Aicher A, Ziebart T, Honold J, Urbich C, et al,. (2006). Ex vivo pretreatment of bone marrow mononuclear cells with endothelial NO synthase enhancer AVE9488 enhances their functional activity for cell therapy. Proc Natl Acad Sci USA 103: 14537-14541. (Pubitemid 44484785)
36. Schachinger V, Assmus B, Britten MB, Honold J, Lehmann R, Teupe C, et al,. (2004). Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year results of the TOPCARE-AMI Trial. J Am Coll Cardiol 44: 1690-1699. (Pubitemid 39369805)
37. Seeger FH, Tonn T, Krzossok N, Zeiher AM, Dimmeler S, (2007). Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction. Eur Heart J 28: 766-772. (Pubitemid 46439231)
38. Segal MS, Shah R, Afzal A, Perrault CM, Chang K, Schuler A, et al,. (2006). Nitric oxide cytoskeletal-induced alterations reverse the endothelial progenitor cell migratory defect associated with diabetes. Diabetes 55: 102-109. (Pubitemid 43343304)
39. Song P, Wu Y, Xu J, Xie Z, Dong Y, Zhang M, et al,. (2007). Reactive nitrogen species induced by hyperglycemia suppresses Akt signaling and triggers apoptosis by upregulating phosphatase PTEN (phosphatase and tensin homologue deleted on chromosome 10) in an LKB1-dependent manner. Circulation 116: 1585-1595. (Pubitemid 47511422)
40. Spyridopoulos I, Haendeler J, Urbich C, Brummendorf TH, Oh H, Schneider MD, et al,. (2004). Statins enhance migratory capacity by upregulation of the telomere repeat-binding factor TRF2 in endothelial progenitor cells. Circulation 110: 3136-3142. (Pubitemid 39492010)
41. Tatsumi T, Ashihara E, Yasui T, Matsunaga S, Kido A, Sasada Y, et al,. (2007). Intracoronary transplantation of non-expanded peripheral blood-derived mononuclear cells promotes improvement of cardiac function in patients with acute myocardial infarction. Circ J 71: 1199-1207. (Pubitemid 47201778)
42. Tepper OM, Capla JM, Galiano RD, Ceradini DJ, Callaghan MJ, Kleinman ME, et al,. (2005). Adult vasculogenesis occurs through in situ recruitment, proliferation, and tubulization of circulating bone marrow-derived cells. Blood 105: 1068-1077. (Pubitemid 40170877)
43. Thum T, Fraccarollo D, Schultheiss M, Froese S, Galuppo P, Widder JD, et al,. (2007). Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 56: 666-674. (Pubitemid 46348461)
44. Urbich C, Dernbach E, Zeiher AM, Dimmeler S, (2002). Double-edged role of statins in angiogenesis signaling. Circ Res 90: 737-744. (Pubitemid 34640894)
45. Urbich C, Knau A, Fichtlscherer S, Walter DH, Bruhl T, Potente M, et al,. (2005). FOXO-dependent expression of the proapoptotic protein Bim: pivotal role for apoptosis signaling in endothelial progenitor cells. FASEB J 19: 974-976. (Pubitemid 40827722)
46. Vaughan CJ, Murphy MB, Buckley BM, (1996). Statins do more than just lower cholesterol. Lancet 348: 1079-1082. (Pubitemid 26343606)
47. Wallace JL, Viappiani S, Bolla M, (2009). Cyclooxygenase-inhibiting nitric oxide donators for osteoarthritis. Trends Pharmacol Sci 30: 112-117.
48. Weis M, Heeschen C, Glassford AJ, Cooke JP, (2002). Statins have biphasic effects on angiogenesis. Circulation 105: 739-745. (Pubitemid 34157379)
49. White WB, Schnitzer TJ, Fleming R, Duquesroix B, Beekman M, (2009). Effects of the cyclooxygenase inhibiting nitric oxide donator naproxcinod versus naproxen on systemic blood pressure in patients with osteoarthritis. Am J Cardiol 104: 840-845.
50. Yang YM, Huang A, Kaley G, Sun D, (2009). eNOS uncoupling and endothelial dysfunction in aged vessels. Am J Physiol Heart Circ Physiol 297: H1829-H1836.
51. Yoder MC, Du XX, Williams DA, (1993). High proliferative potential colony-forming cell heterogeneity identified using counterflow centrifugal elutriation. Blood 82: 385-391. (Pubitemid 23206100)
52. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, et al,. (2007). Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell prin cipals. Blood 109: 1801-1809. (Pubitemid 46348173)
53. Zhang W, Wang X, Jin H, Qian R, Zhang G, Chen S, et al,. (2008). Effects of high glucose plus high insulin on proliferation and apoptosis of mouse endothelial progenitor cells. Inflamm Res 57: 571-576.