Presence of endothelial colony-forming cells is associated with reduced microvascular obstruction limiting infarct size and left ventricular remodelling in patients with acute myocardial infarction

Basic Research in Cardiology

Volumn 106, Issue 6, 2011, Pages 1397-1410

  Meneveau, Nicolas ^a,b   Deschaseaux, Frédéric ^c   Séronde, Marie France ^a   Chopard, Romain ^a   Schiele, François ^a   Jehl, Jérome ^c   Tiberghien, Pierre ^c   Bassand, Jean Pierre ^a   Kantelip, Jean Pierre ^a   Davani, Siamak ^a  

^a Bâtiment Socrate   (France)

^b UNIVERSITY HOSPITAL JEAN MINJOZ   (France)

^c UNIVERSITÉ DE FRANCHE COMTÉ   (France)

Author keywords

Endothelial progenitor cells; Interleukin 8; Microvascular obstruction; Myocardial infarction

Indexed keywords

CD34 ANTIGEN; VASCULOTROPIN;

ACUTE HEART INFARCTION; ADULT; AGED; ARTICLE; CARDIOVASCULAR RISK; COLONY FORMING CELL; DISEASE ASSOCIATION; DISEASE MARKER; ENDOTHELIUM CELL; FEMALE; FOLLOW UP; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE VOLUME; HEART VENTRICLE REMODELING; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; MICROANGIOPATHY; NUCLEAR MAGNETIC RESONANCE IMAGING; RISK REDUCTION; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION;

CORONARY VESSELS; ENDOTHELIAL CELLS; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MICROVESSELS; MIDDLE AGED; MYOCARDIAL INFARCTION; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; STEM CELLS; VENTRICULAR REMODELING;

EID: 84856705422     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-011-0220-x     Document Type: Article

References (65)

1. Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ (2004) Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110:3300-3305 (Pubitemid 39557491)
2. Ahrens I, Domeij H, Eisenhardt S, Topcic D, Albrecht M, Leitner E, Viitaniemi K, Jowett J, Lappas M, Bode C, Haviv I, Peter K (2011) Opposing effects of monomeric and pentameric C-reactive protein on endothelial progenitor cells. Basic Res Cardiol 106:879-895. doi:10.1007/s00395-011-0191-y
3. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964-967 (Pubitemid 27087709)
4. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, Rovner A, Ellis SG, Thomas JD, Di Corleto PE, Topol EJ, Penn MS (2003) Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362:697-703. doi:10.1016/S0140-6736(03) 14232-8 (Pubitemid 37101067)
5. Bassand JP, Hamm C (2007) New European guidelines for the management of patients with unstable angina/non-ST-elevation myocardial infarction-what are the new and key messages. Pol Arch Med Wewn 117:391-393
6. Bolognese L, Carrabba N, Parodi G, Santoro GM, Buonamici P, Cerisano G, Antoniucci D (2004) Impact of microvascular dysfunction on left ventricular remodeling and long-term clinical outcome after primary coronary angioplasty for acute myocardial infarction. Circulation 109:1121-1126. doi:10.1161/01. CIR.0000 118496.44135. A7 (Pubitemid 38332616)
7. Bondarenko O, Beek AM, Hofman MB, Kuhl HP, Twisk JW, van Dockum WG, Visser CA, van Rossum AC (2005) Standardizing the definition of hyperenhancement in the quantitative assessment of infarct size and myocardial viability using delayed contrastenhanced CMR. J Cardiovasc Magn Reson 7:481-485 (Pubitemid 40563339)
8. Breuckmann F, Nassenstein K, Bucher C, Konietzka I, Kaiser G, Konorza T, Naber C, Skyschally A, Gres P, Heusch G, Erbel R, Barkhausen J (2009) Systematic analysis of functional and structural changes after coronary microembolization: a cardiac magnetic resonance imaging study. JACC Cardiovasc Imaging 2:121-130. doi:10.1016/j.jcmg.2008.10.011
9. Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, Pennell DJ, Rumberger JA, Ryan T, Verani MS (2002) Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart: a statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association. Circulation 105:539-542 (Pubitemid 34262671)
10. Cesari F, Caporale R, Marcucci R, Caciolli S, Stefano PL, Capalbo A, Macchi C, Vannucci M, Gensini GF, Abbate R, Gori AM (2008) NT-proBNP and the anti-inflammatory cytokines are correlated with endothelial progenitor cells' response to cardiac surgery. Atherosclerosis 199:138-146 (Pubitemid 351842693)
11. Cochet AA, Lorgis L, Lalande A, Zeller M, Beer JC, Walker PM, Touzery C, Wolf JE, Brunotte F, Cottin Y (2009) Major prognostic impact of persistent microvascular obstruction as assessed by contrast-enhanced cardiac magnetic resonance in reperfused acute myocardial infarction. Eur Radiol 19:2117-2126. doi: 10.1007/s00330-009-1395-5
12. Comte A, Lalande A, Walker PM, Cochet A, Legrand L, Cottin Y, Wolf JE, Brunotte F (2004) Visual estimation of the global myocardial extent of hyperenhancement on delayed contrastenhanced MRI. Eur Radiol 14:2182-2187 (Pubitemid 40057928)
13. Davani S, Gozalo C, Gambert S, Chalmers D, Gambert P, Schiele F, Kantelip JP, Meneveau N (2010) The polymorphism Trp719Arg in the kinesin-like protein 6 is associated with the presence of late outgrowth endothelial progenitor cells in acute myocardial infarction. Atherosclerosis 210:48-50. doi:10.1016/j. atherosclerosis.2009.11.041
14. De Luca G, van't Hof AW, de Boer MJ, Ottervanger JP, Hoorntje JC, Gosselink AT, Dambrink JH, Zijlstra F, Suryapranata H (2004) Time-to-treatment significantly affects the extent of ST-segment resolution and myocardial blush in patients with acute myocardial infarction treated by primary angioplasty. Eur Heart J 25:1009-1013 (Pubitemid 38869418)
15. Deschaseaux F, Selmani Z, Falcoz PE, Mersin N, Meneveau N, Penfornis A, Kleinclauss C, Chocron S, Etievent JP, Tiberghien P, Kantelip JP, Davani S (2007) Two types of circulating endothelial progenitor cells in patients receiving long term therapy by HMG-CoA reductase inhibitors. Eur J Pharmacol 562:111-118 (Pubitemid 46466754)
16. Friedrich EB, Werner C, Walenta K, Bohm M, Scheller B (2009) Role of extracellular signal-regulated kinase for endothelial progenitor cell dysfunction in coronary artery disease. Basic Res Cardiol 104:613-620. doi:10.1007/s00395-009-0022-6
17. Gaspardone A, Menghini F, Mazzuca V, Skossyreva O, Barbato G, de Fabritiis P (2006) Progenitor cell mobilisation in patients with acute and chronic coronary artery disease. Heart 92:253-254 (Pubitemid 43131973)
18. Gerber BL, Rochitte CE, Melin JA, McVeigh ER, Bluemke DA, Wu KC, Becker LC, Lima JA (2000) Microvascular obstruction and left ventricular remodeling early after acute myocardial infarction. Circulation 101:2734-2741 (Pubitemid 30390578)
19. Grothues F, Smith GC, Moon JC, Bellenger NG, Collins P, Klein HU, Pennell DJ (2002) Comparison of interstudy reproducibility of cardiovascular magnetic resonance with two-dimensional echocardiography in normal subjects and in patients with heart failure or left ventricular hypertrophy. Am J Cardiol 90:29-34 (Pubitemid 34671198)
20. Grundmann F, Scheid C, Braun D, Zobel C, Reuter H, Schwinger RH, Muller-Ehmsen J (2007) Differential increase of CD34, KDR/CD34, CD133/CD34 and CD117/CD34 positive cells in peripheral blood of patients with acute myocardial infarction. Clin Res Cardiol 96:621-627. doi:10.1007/s00392-007-0543-7 (Pubitemid 47400818)
21. Gulati R, Jevremovic D, Peterson TE, Chatterjee S, Shah V, Vile RG, Simari RD (2003) Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ Res 93:1023-1025 (Pubitemid 37485031)
22. Heusch G, Kleinbongard P, Bose D, Levkau B, Haude M, Schulz R, Erbel R (2009) Coronary microembolization: from bedside to bench and back to bedside. Circulation 120:1822-1836. doi: 10.1161/CIRCULATIONAHA.109.888784
23. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T (2003) Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348:593-600 (Pubitemid 36204953)
24. Hirschi KK, Ingram DA, Yoder MC (2008) Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 28:1584-1595
25. Hur J, Yoon CH, Kim HS, Choi JH, Kang HJ, Hwang KK, Oh BH, Lee MM, Park YB (2004) Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler Thromb Vasc Biol 24:288-293 (Pubitemid 38197580)
26. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, Pollok K, Ferkowicz MJ, Gilley D, Yoder MC (2004) Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104:2752-2760 (Pubitemid 39434958)
27. Isner JM, Asahara T (1999) Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest 103:1231-1236 (Pubitemid 29218292)
28. Kaur S, Kumar T, Uruno A, Sugawara A, Jayakumar K, Kartha C (2009) Genetic engineering with endothelial nitric oxide synthase improves functional properties of endothelial progenitor cells from patients with coronary artery disease: an in vitro study. Basic Res Cardiol 104:739-749. doi:10.1007/s00395- 009-0039-x
29. Laterveer L, Lindley IJ, Heemskerk DP, Camps JA, Pauwels EK, Willemze R, Fibbe WE (1996) Rapid mobilization of hematopoietic progenitor cells in rhesus monkeys by a single intravenous injection of interleukin-8. Blood 87:781-788 (Pubitemid 26030335)
30. Leone AM, Rutella S, Bonanno G, Abbate A, Rebuzzi AG, Giovannini S, Lombardi M, Galiuto L, Liuzzo G, Andreotti F, Lanza GA, Contemi AM, Leone G, Crea F (2005) Mobilization of bone marrow-derived stem cells after myocardial infarction and left ventricular function. Eur Heart J 26:1196-1204. doi: 10.1093/eurheartj/ehi164 (Pubitemid 40863126)
31. Leone AM, Valgimigli M, Giannico MB, Zaccone V, Perfetti M, D' Amario D, Rebuzzi AG, Crea F (2009) From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells. Eur Heart J 30:890-899
32. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105:71-77 (Pubitemid 30036389)
33. Ma J, Ge J, Zhang S, Sun A, Shen J, Chen L, Wang K, Zou Y (2005) Time course of myocardial stromal cell-derived factor 1 expression and beneficial effects of intravenously administered bone marrow stem cells in rats with experimental myocardial infarction. Basic Res Cardiol 100:217-223. doi:10.1007/s00395-005-0521-z (Pubitemid 41348812)
34. Massa M, Campanelli R, Bonetti E, Ferrario M, Marinoni B, Rosti V (2009) Rapid and large increase of the frequency of circulating endothelial colony-forming cells (ECFCs) generating late outgrowth endothelial cells in patients with acute myocardial infarction. Exp Hematol 37:8-9. doi:10.1016/j.exphem.2008. 09.007
35. Massa M, Rosti V, Ferrario M, Campanelli R, Ramajoli I, Rosso R, De Ferrari GM, Ferlini M, Goffredo L, Bertoletti A, Klersy C, Pecci A, Moratti R, Tavazzi L (2005) Increased circulating hematopoietic and endothelial progenitor cells in the early phase of acute myocardial infarction. Blood 105:199-206 (Pubitemid 40053083)
36. Nijveldt R, Beek AM, Hirsch A, Stoel MG, Hofman MBM, Umans VAWM, Algra PR, Twisk JWR, van Rossum AC (2008) Functional recovery after acute myocardial infarction: comparison between angiography, electrocardiography, and cardiovascular magnetic resonance measures of microvascular injury. J Am Coll Cardiol 52:181-189 (Pubitemid 351915778)
37. Nijveldt R, Hofman MBM, Hirsch A, Beek AM, Umans VAWM, Algra PR, Piek JJ, van Rossum AC (2009) Assessment of microvascular obstruction and prediction of short-term remodeling after acute myocardial infarction: cardiac MR imaging study 1. Radiology 250:363-370. doi:10.1148/radiol.2502080739
38. Numaguchi Y, Sone T, Okumura K, Ishii M, Morita Y, Kubota R, Yokouchi K, Imai H, Harada M, Osanai H, Kondo T, Murohara T (2006) The impact of the capability of circulating progenitor cell to differentiate on myocardial salvage in patients with primary acute myocardial infarction. Circulation 114: I114-I119. doi: 10.1161/CIRCULATIONAHA.105.000588 (Pubitemid 44297138)
39. Ørn S, Manhenke C, Greve OJ, Larsen AI, Bonarjee VVS, Edvardsen T, Dickstein K (2009) Microvascular obstruction is a major determinant of infarct healing and subsequent left ventricular remodelling following primary percutaneous coronary intervention. Eur Heart J 30:1978-1985. doi:10.1093/eurheartj/ehp219
40. Roberts N, Xiao Q, Weir G, Xu Q, Jahangiri M (2007) Endothelial progenitor cells are mobilized after cardiac surgery. Ann Thorac Surg 83:598-605 (Pubitemid 46135472)
41. Rochitte CE, Lima JAC, Bluemke DA, Reeder SB, McVeigh ER, Furuta T, Becker LC, Melin JA (1998) Magnitude and time course of microvascular obstruction and tissue injury after acute myocardial infarction. Circulation 98:1006-1014 (Pubitemid 28446654)
42. Sandstedt J, Jonsson M, Lindahl A, Jeppsson A, Asp J (2010) C-kit+ CD45-cells found in the adult human heart represent a population of endothelial progenitor cells. Basic Res Cardiol 105:545-556. doi:10.1007/s00395-010-0088-1
43. Schomig K, Busch G, Steppich B, Sepp D, Kaufmann J, Stein A, Schomig A, Ott I (2006) Interleukin-8 is associated with circulating CD133+ progenitor cells in acute myocardial infarction. Eur Heart J 27:1032-1037
44. Seeger F, Sedding D, Langheinrich A, Haendeler J, Zeiher A, Dimmeler S (2010) Inhibition of the p38 MAP kinase in vivo improves number and functional activity of vasculogenic cells and reduces atherosclerotic disease progression. Basic Res Cardiol 105:389-397. doi:10.1007/s00395-009-0072-9
45. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T (2001) Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 103:2776-2779 (Pubitemid 32550062)
46. Sieveking DP, Buckle A, Celermajer DS, Ng MK (2008) Strikingly different angiogenic properties of endothelial progenitor cell subpopulations: insights from a novel human angiogenesis assay. J Am Coll Cardiol 51:660-668. doi:10.1016/j.jacc.2007. 09.059 (Pubitemid 351186872)
47. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T (1999) Ischemia-and cytokineinduced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5:434-438 (Pubitemid 29180584)
48. Thiele H, Nagel E, Paetsch I, Schnackenburg B, Bornstedt A, Kouwenhoven M, Wahl A, Schuler G, Fleck E (2001) Functional cardiac MR imaging with steady-state free precession (SSFP) significantly improves endocardial border delineation without contrast agents. J Magn Reson Imaging 14:362-367. doi:10.1002/jmri (Pubitemid 32906553)
49. Thygesen K, Alpert JS, White HD, Jaffe AS, Apple FS, Galvani M, Katus HA, Newby LK, Ravkilde J, Chaitman B, Clemmensen PM, Dellborg M, Hod H, Porela P, Underwood R, Bax JJ, Beller GA, Bonow R, Van der Wall EE, Bassand JP, Wijns W, Ferguson TB, Steg PG, Uretsky BF, Williams DO, Armstrong PW, Antman EM, Fox KA, Hamm CW, Ohman EM, Simoons ML, Poole-Wilson PA, Gurfinkel EP, Lopez-Sendon JL, Pais P, Mendis S, Zhu JR, Wallentin LC, Fernandez-Aviles F, Fox KM, Parkhomenko AN, Priori SG, Tendera M, Voipio-Pulkki LM, Vahanian A, Camm AJ, De Caterina R, Dean V, Dickstein K, Filippatos G, Funck-Brentano C, Hellemans I, Kristensen SD, McGregor K, Sechtem U, Silber S, Tendera M, Widimsky P, Zamorano JL, Morais J, Brener S, Harrington R, Morrow D, Lim M, Martinez-Rios MA, Steinhubl S, Levine GN, Gibler WB, Goff D, Tubaro M, Dudek D, Al-Attar N (2007) Universal definition of myocardial infarction. Circulation 116:2634-2653 (Pubitemid 350182388)
50. Urbich C, Aicher A, Heeschen C, Dernbach E, Hofmann WK, Zeiher AM, Dimmeler S (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 (Pubitemid 41464410)
51. Urbich C, Dimmeler S (2004) Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95:343-353. doi:10.1161/01. RES.0000137877.89448.78 (Pubitemid 39100452)
52. Van Craenenbroeck E, Hoymans V, Beckers P, Possemiers N, Wuyts K, Paelinck B, Vrints C, Conraads V (2010) Exercise training improves function of circulating angiogenic cells in patients with chronic heart failure. Basic Res Cardiol 105:665-676. doi:10.1007/s00395-010-0105-4
53. Van De Werf F, Bax J, Betriu A, Blomstrom-Lundqvist C, Crea F, Falk V, Filippatos G, Fox K, Huber K, Kastrati A, Rosengren A, Steg PG, Tubaro M, Verheugt F, Weidinger F, Weis M, Vahanian A, Camm J, De Caterina R, Dean V, Dickstein K, Filippatos G, Funck-Brentano C, Hellemans I, Kristensen SD, McGregor K, Sechtem U, Silber S, Tendera M, Widimsky P, Zamorano JL, Silber S, Aguirre FV, Al-Attar N, Alegria E, Andreotti F, Benzer W, Breithardt O, Danchin N, Di Mario C, Dudek D, Gulba D, Halvorsen S, Kaufmann P, Kornowski R, Lip GY, Rutten F (2008) Management of acute myocardial infarction in patients presenting with persistent ST-segment elevation: the Task Force on the Management of ST-Segment Elevation Acute Myocardial Infarction of the European Society of Cardiology. Eur Heart J 29:2909-2945
54. Voo S, Eggermann J, Dunaeva M, Ramakers-van Oosterhoud C, Waltenberger J (2008) Enhanced functional response of CD133+ circulating progenitor cells in patients early after acute myocardial infarction. Eur Heart J 29:241-250
55. Walenta KL, Bettink S, Bohm M, Friedrich EB (2011) Differential chemokine receptor expression regulates functional specialization of endothelial progenitor cell subpopulations. Basic Res Cardiol 106:299-305. doi:10.1007/s00395-010-0142-z
56. Wang Y, Haider H, Ahmad N, Zhang D, Ashraf M (2006) Evidence for ischemia induced host-derived bone marrow cell mobilization into cardiac allografts. J Mol Cell Cardiol 41:478-487. doi:10.1016/j.yjmcc.2006.06.074 (Pubitemid 44349132)
57. Werner N, Wassmann S, Ahlers P, Schiegl T, Kosiol S, Link A, Walenta K, Nickenig G (2007) Endothelial progenitor cells correlate with endothelial function in patients with coronary artery disease. Basic Res Cardiol 102:565-571. doi:10.1007/s00395-007-0680-1 (Pubitemid 47578401)
58. Wojakowski W, Kucia M, Kazmierski M, Ratajczak MZ, Tendera M (2008) Circulating progenitor cells in stable coronary heart disease and acute coronary syndromes: relevant reparatory mechanism? Heart 94:27-33
59. Xiao Q, Ye S, Oberhollenzer F, Mayr A, Jahangiri M, Willeit J, Kiechl S, Xu Q (2008) SDF1 gene variation is associated with circulating SDF1alpha level and endothelial progenitor cell number: the Bruneck Study. PLoS ONE 3: e4061. doi:10.1371/journal.pone.0004061
60. Yamaguchi J, Kusano KF, Masuo O, Kawamoto A, Silver M, Murasawa S, Bosch-Marce M, Masuda H, Losordo DW, Isner JM, Asahara T (2003) Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107:1322-1328 (Pubitemid 36314418)
61. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, Krasich R, Temm CJ, Prchal JT, Ingram DA (2007) Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109:1801-1809. doi:10.1182/blood-2006-08-043471 (Pubitemid 46348173)
62. Yoon CH, Hur J, Park KW, Kim JH, Lee CS, Oh IY, Kim TY, Cho HJ, Kang HJ, Chae IH, Yang HK, Oh BH, Park YB, Kim HS (2005) Synergistic neovascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases. Circulation 112:1618-1627. doi:10.1161/CIRCULATIONAHA.104. 503433 (Pubitemid 41324524)
63. Yu Y, Gao Y, Qin J, Kuang C-Y, Song M-B, Yu S-Y, Cui B, Chen J-F, Huang L (2010) CCN1 promotes the differentiation of endothelial progenitor cells and reendothelialization in the early phase after vascular injury. Basic Res Cardiol 105:713-724. doi: 10.1007/s00395-010-0117-0
64. Zernecke A, Weber C (2005) Inflammatory mediators in atherosclerotic vascular disease. Basic Res Cardiol 100:93-101. doi: 10.1007/s00395-005-0511-6 (Pubitemid 40361602)
65. Zhang Y, Ingram DA, Murphy MP, Saadatzadeh MR, Mead LE, Prater DN, Rehman J (2009) Release of proinflammatory mediators and expression of proinflammatory adhesion molecules by endothelial progenitor cells. Am J Physiol Heart Circ Physiol 296: H1675-H1682. doi:10.1152/ajpheart.00665.2008