Cilostazol activates function of bone marrow-derived endothelial progenitor cell for re-endothelialization in a carotid balloon injury model

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Kawabe Yako, Rie ^a,b   Ii, Masaaki ^a,c   Masuo, Osamu ^b   Asahara, Takayuki ^a,d   Itakura, Toru ^b  

^a INSTITUTE OF BIOMEDICAL RESEARCH AND INNOVATION   (Japan)

^b WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^c OSAKA MEDICAL COLLEGE   (Japan)

^d TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RECEPTOR; BETA GALACTOSIDASE; CHEMOKINE RECEPTOR CXCR4; CILOSTAZOL; MESSENGER RNA; STROMAL CELL DERIVED FACTOR 1ALPHA; VASCULOTROPIN; VITRONECTIN RECEPTOR; TETRAZOLE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW TRANSPLANTATION; CAROTID ARTERY DISEASE; CAROTID BALLOON INJURY; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG INHIBITION; ENDOTHELIAL PROGENITOR CELL; ENZYME REGULATION; IN VITRO STUDY; MALE; NEOINTIMA; NONHUMAN; PROTEIN EXPRESSION; RAT; TREATMENT RESPONSE; ANIMAL; BALLOON DILATATION; BONE MARROW CELL; CAROTID ARTERY INJURY; CYTOLOGY; DRUG EFFECT; ENDOTHELIUM CELL; MOUSE; SPRAGUE DAWLEY RAT; STEM CELL;

MUS; RATTUS;

ANIMALS; BALLOON DILATION; BONE MARROW CELLS; CAROTID ARTERY INJURIES; ENDOTHELIAL CELLS; MALE; MICE; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS; TETRAZOLES;

EID: 80052618800     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024646     Document Type: Article

References (61)

1. Liistro F, Colombo A, (2001) Late acute thrombosis after paclitaxel eluting stent implantation. Heart 86: 262-264.
2. Asahara T, Isner JM, (2002) Endothelial progenitor cells for vascular regeneration. J Hematother Stem Cell Res 11: 171-178.
3. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, et al. (1999) Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5: 434-438.
4. Laufs U, Werner N, Link A, Endres M, Wassmann S, et al. (2004) Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 109: 220-226.
5. Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, et al. (2002) Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation 105: 3017-3024.
6. Werner N, Priller J, Laufs U, Endres M, Bohm M, et al. (2002) Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition. Arterioscler Thromb Vasc Biol 22: 1567-1572.
7. Iwakura A, Luedemann C, Shastry S, Hanley A, Kearney M, et al. (2003) Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation 108: 3115-3121.
8. Strehlow K, Werner N, Berweiler J, Link A, Dirnagl U, et al. (2003) Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation 107: 3059-3065.
9. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, et al. (1999) VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. Embo J 18: 3964-3972.
10. Cho HJ, Kim HS, Lee MM, Kim DH, Yang HJ, et al. (2003) Mobilized endothelial progenitor cells by granulocyte-macrophage colony-stimulating factor accelerate reendothelialization and reduce vascular inflammation after intravascular radiation. Circulation 108: 2918-2925.
11. Kong D, Melo LG, Gnecchi M, Zhang L, Mostoslavsky G, et al. (2004) Cytokine-induced mobilization of circulating endothelial progenitor cells enhances repair of injured arteries. Circulation 110: 2039-2046.
12. Kimura Y, Tani T, Kanbe T, Watanabe K, (1985) Effect of cilostazol on platelet aggregation and experimental thrombosis. Arzneimittelforschung 35: 1144-1149.
13. Kambayashi J, Liu Y, Sun B, Shakur Y, Yoshitake M, et al. (2003) Cilostazol as a unique antithrombotic agent. Curr Pharm Des 9: 2289-2302.
14. Matsumoto M, (2005) Cilostazol in secondary prevention of stroke: impact of the Cilostazol Stroke Prevention Study. Atheroscler Suppl 6: 33-40.
15. Ishizaka N, Taguchi J, Kimura Y, Ikari Y, Aizawa T, et al. (1999) Effects of a single local administration of cilostazol on neointimal formation in balloon-injured rat carotid artery. Atherosclerosis 142: 41-46.
16. Takahashi S, Oida K, Fujiwara R, Maeda H, Hayashi S, et al. (1992) Effect of cilostazol, a cyclic AMP phosphodiesterase inhibitor, on the proliferation of rat aortic smooth muscle cells in culture. J Cardiovasc Pharmacol 20: 900-906.
17. Tsuchikane E, Fukuhara A, Kobayashi T, Kirino M, Yamasaki K, et al. (1999) Impact of cilostazol on restenosis after percutaneous coronary balloon angioplasty. Circulation 100: 21-26.
18. Douglas JS Jr, Holmes DR Jr, Kereiakes DJ, Grines CL, Block E, et al. (2005) Coronary stent restenosis in patients treated with cilostazol. Circulation 112: 2826-2832.
19. Zhang Z, Foster JK, Kolm P, Jurkovitz CT, Parker KM, et al. (2006) Reduced 6-month resource use and costs associated with cilostazol in patients after successful coronary stent implantation: results from the Cilostazol for RESTenosis (CREST) trial. Am Heart J 152: 770-776.
20. Takigawa T, Matsumaru Y, Hayakawa M, Nemoto S, Matsumura A, (2010) Cilostazol reduces restenosis after carotid artery stenting. J Vasc Surg 51: 51-56.
21. Kim KY, Shin HK, Choi JM, Hong KW, (2002) Inhibition of lipopolysaccharide-induced apoptosis by cilostazol in human umbilical vein endothelial cells. J Pharmacol Exp Ther 300: 709-715.
22. Morishita R, Higaki J, Hayashi SI, Yo Y, Aoki M, et al. (1997) Role of hepatocyte growth factor in endothelial regulation: prevention of high D-glucose-induced endothelial cell death by prostaglandins and phosphodiesterase type 3 inhibitor. Diabetologia 40: 1053-1061.
23. Aoki M, Morishita R, Hayashi S, Jo N, Matsumoto K, et al. (2001) Inhibition of neointimal formation after balloon injury by cilostazol, accompanied by improvement of endothelial dysfunction and induction of hepatocyte growth factor in rat diabetes model. Diabetologia 44: 1034-1042.
24. Shin HK, Kim YK, Kim KY, Lee JH, Hong KW, (2004) Remnant lipoprotein particles induce apoptosis in endothelial cells by NAD(P)H oxidase-mediated production of superoxide and cytokines via lectin-like oxidized low-density lipoprotein receptor-1 activation: prevention by cilostazol. Circulation 109: 1022-1028.
25. Otsuki M, Saito H, Xu X, Sumitani S, Kouhara H, et al. (2001) Cilostazol represses vascular cell adhesion molecule-1 gene transcription via inhibiting NF-kappaB binding to its recognition sequence. Atherosclerosis 158: 121-128.
26. Nishio Y, Kashiwagi A, Takahara N, Hidaka H, Kikkawa R, (1997) Cilostazol, a cAMP phosphodiesterase inhibitor, attenuates the production of monocyte chemoattractant protein-1 in response to tumor necrosis factor-alpha in vascular endothelial cells. Horm Metab Res 29: 491-495.
27. Omi H, Okayama N, Shimizu M, Fukutomi T, Nakamura A, et al. (2004) Cilostazol inhibits high glucose-mediated endothelial-neutrophil adhesion by decreasing adhesion molecule expression via NO production. Microvasc Res 68: 119-125.
28. Zampetaki A, Kirton JP, Xu Q, (2008) Vascular repair by endothelial progenitor cells. Cardiovasc Res 78: 413-421.
29. Sanada F, Taniyama Y, Azuma J, Iekushi K, Dosaka N, et al. (2009) Hepatocyte growth factor, but not vascular endothelial growth factor, attenuates angiotensin II-induced endothelial progenitor cell senescence. Hypertension 53: 77-82.
30. Leone AM, Valgimigli M, Giannico MB, Zaccone V, Perfetti M, et al. (2009) From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells. Eur Heart J 30: 890-899.
31. Hristov M, Weber C, (2004) Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J Cell Mol Med 8: 498-508.
32. Giannotti G, Doerries C, Mocharla PS, Mueller MF, Bahlmann FH, et al. (2010) Impaired endothelial repair capacity of early endothelial progenitor cells in prehypertension: relation to endothelial dysfunction. Hypertension 55: 1389-1397.
33. Hristov M, Zernecke A, Bidzhekov K, Liehn EA, Shagdarsuren E, et al. (2007) Importance of CXC chemokine receptor 2 in the homing of human peripheral blood endothelial progenitor cells to sites of arterial injury. Circ Res 100: 590-597.
34. Sorrentino SA, Bahlmann FH, Besler C, Muller M, Schulz S, et al. (2007) Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: restoration by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. Circulation 116: 163-173.
35. Dimmeler S, Zeiher AM, (2004) Vascular repair by circulating endothelial progenitor cells: the missing link in atherosclerosis? J Mol Med 82: 671-677.
36. Urbich C, Aicher A, Heeschen C, Dernbach E, Hofmann WK, et al. (2005) Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Mol Cell Cardiol 39: 733-742.
37. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, et al. (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967.
38. Dzau VJ, Gnecchi M, Pachori AS, Morello F, Melo LG, (2005) Therapeutic potential of endothelial progenitor cells in cardiovascular diseases. Hypertension 46: 7-18.
39. Lamping K, (2007) Endothelial progenitor cells: sowing the seeds for vascular repair. Circ Res 100: 1243-1245.
40. Chavakis E, Aicher A, Heeschen C, Sasaki K, Kaiser R, et al. (2005) Role of beta2-integrins for homing and neovascularization capacity of endothelial progenitor cells. J Exp Med 201: 63-72.
41. Chavakis E, Hain A, Vinci M, Carmona G, Bianchi ME, et al. (2007) High-mobility group box 1 activates integrin-dependent homing of endothelial progenitor cells. Circ Res 100: 204-212.
42. Rahman S, Patel Y, Murray J, Patel KV, Sumathipala R, et al. (2005) Novel hepatocyte growth factor (HGF) binding domains on fibronectin and vitronectin coordinate a distinct and amplified Met-integrin induced signalling pathway in endothelial cells. BMC Cell Biol 6: 8.
43. Dufourcq P, Couffinhal T, Alzieu P, Daret D, Moreau C, et al. (2002) Vitronectin is up-regulated after vascular injury and vitronectin blockade prevents neointima formation. Cardiovasc Res 53: 952-962.
44. Schober A, Knarren S, Lietz M, Lin EA, Weber C, (2003) Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein E-deficient mice. Circulation 108: 2491-2497.
45. Sainz J, Sata M, (2007) CXCR4, a key modulator of vascular progenitor cells. Arterioscler Thromb Vasc Biol 27: 263-265.
46. Karshovska E, Zernecke A, Sevilmis G, Millet A, Hristov M, et al. (2007) Expression of HIF-1alpha in injured arteries controls SDF-1alpha mediated neointima formation in apolipoprotein E deficient mice. Arterioscler Thromb Vasc Biol 27: 2540-2547.
47. Zernecke A, Schober A, Bot I, von Hundelshausen P, Liehn EA, et al. (2005) SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res 96: 784-791.
48. Yin Y, Zhao X, Fang Y, Yu S, Zhao J, et al. (2010) SDF-1alpha involved in mobilization and recruitment of endothelial progenitor cells after arterial injury in mice. Cardiovasc Pathol 19: 218-227.
49. Chen L, Wu F, Xia WH, Zhang YY, Xu SY, et al. (2010) CXCR4 gene transfer contributes to in vivo reendothelialization capacity of endothelial progenitor cells. Cardiovasc Res 88: 462-470.
50. Hiatt WR, (2002) Pharmacologic therapy for peripheral arterial disease and claudication. J Vasc Surg 36: 1283-1291.
51. Shin HK, Lee HR, Lee DH, Hong KW, Lee JH, et al. (2010) Cilostazol enhances neovascularization in the mouse hippocampus after transient forebrain ischemia. J Neurosci Res 88: 2228-2238.
52. Hashimoto A, Miyakoda G, Hirose Y, Mori T, (2006) Activation of endothelial nitric oxide synthase by cilostazol via a cAMP/protein kinase A- and phosphatidylinositol 3-kinase/Akt-dependent mechanism. Atherosclerosis 189: 350-357.
53. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, et al. (2003) Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9: 1370-1376.
54. Dimmeler S, Aicher A, Vasa M, Mildner-Rihm C, Adler K, 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.
55. Imanishi T, Kobayashi K, Kuki S, Takahashi C, Akasaka T, (2006) Sirolimus accelerates senescence of endothelial progenitor cells through telomerase inactivation. Atherosclerosis 189: 288-296.
56. Zhang P, Huang L, Zhu GX, Cui B, Song MB, et al. (2006) [Sirolimus inhibits the differentiation, proliferation and migration of endothelial progenitor cells in vitro]. Zhonghua Xin Xue Guan Bing Za Zhi 34: 1021-1025.
57. Hofma SH, van der Giessen WJ, van Dalen BM, Lemos PA, McFadden EP, et al. (2006) Indication of long-term endothelial dysfunction after sirolimus-eluting stent implantation. Eur Heart J 27: 166-170.
58. Fukuda D, Sata M, Tanaka K, Nagai R, (2005) Potent inhibitory effect of sirolimus on circulating vascular progenitor cells. Circulation 111: 926-931.
59. Miyamoto N, Tanaka R, Shimura H, Watanabe T, Mori H, et al. (2010) Phosphodiesterase III inhibition promotes differentiation and survival of oligodendrocyte progenitors and enhances regeneration of ischemic white matter lesions in the adult mammalian brain. J Cereb Blood Flow Metab 30: 299-310.
60. Akiyama H, Kudo S, Odomi M, Shimizu T, (1985) High-performance liquid chromatographic procedure for the determination of a new antithrombotic and vasodilating agent, cilostazol, in human plasma. J Chromatogr 338: 456-459.
61. Tsuruta W, Yamamoto T, Suzuki K, Yoshida F, Matsumura A, (2007) Simple new method for making a rat carotid artery post-angioplasty stenosis model. Neurol Med Chir (Tokyo) 47: 525-529.