Circulating endothelial progenitor cells do not contribute to regeneration of endothelium after murine arterial injury

Cardiovascular Research

Volumn 93, Issue 2, 2012, Pages 223-231

  Hagensen, Mette K ^a   Raarup, Merete K ^b   Mortensen, Martin B ^a   Thim, Troels ^a   Nyengaard, Jens R ^b   Falk, Erling ^a   Bentzon, Jacob F ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Endothelial cells; Endothelial progenitor cells; Regeneration; TIE2 GFP mice; Wire injury

Indexed keywords

BETA GALACTOSIDASE; GREEN FLUORESCENT PROTEIN; VASCULAR ENDOTHELIAL CADHERIN; VON WILLEBRAND FACTOR;

ANASTOMOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY INJURY; ARTERY TRANSPLANTATION; ARTICLE; BRIGHT FIELD MICROSCOPY; CELL HOMING; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; TISSUE REGENERATION; VASCULARIZATION;

ANIMALS; CAROTID ARTERY INJURIES; ENDOTHELIAL CELLS; FEMALE; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; REGENERATION; STEM CELLS;

EID: 84856166753     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr278     Document Type: Article

References (44)

1. Schomig A, Kastrati A, Dirschinger J, Mehilli J, Schricke U, Pache J et al. Coronary stenting plus platelet glycoprotein IIb/IIIa blockade compared with tissue plasminogen activator in acute myocardial infarction. Stent versus Thrombolysis for Occluded Coronary Arteries in Patients with Acute Myocardial Infarction Study Investigators. N Engl J Med 2000;343:385-391. (Pubitemid 30626120)
2. Asahara T, Bauters C, Pastore C, Kearney M, Rossow S, Bunting S et al. Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery. Circulation 1995;91: 2793-2801.
3. Bauters C, Isner JM. The biology of restenosis. Prog Cardiovasc Dis 1997;40:107-116. (Pubitemid 27431108)
4. Kinlay S, Libby P, Ganz P. Endothelial function and coronary artery disease. Curr Opin Lipidol 2001;12:383-389. (Pubitemid 32675498)
5. Libby P, Schwartz D, Brogi E, Tanaka H, Clinton SK. A cascade model for restenosis. A special case of atherosclerosis progression. Circulation 1992;86:III47-III52.
6. Schwartz SM, Haudenschild CC, Eddy EM. Endothelial regeneration. I. Quantitative analysis of initial stages of endothelial regeneration in rat aortic intima. Lab Invest 1978;38:568-580. (Pubitemid 8381136)
7. Fishman JA, Ryan GB, Karnovsky MJ. Endothelial regeneration in the rat carotid artery and the significance of endothelial denudation in the pathogenesis of myointimal thickening. Lab Invest 1975;32:339-351.
8. Clopath P, Muller K, Staubli W, Burk RR. In vivo and in vitro studies on endothelial regeneration. Haemostasis 1979;8:149-157. (Pubitemid 10235805)
9. Itoh Y, Toriumi H, Yamada S, Hoshino H, Suzuki N. Resident endothelial cells surrounding damaged arterial endothelium reendothelialize the lesion. Arterioscler Thromb Vasc Biol 2010;30:1725-1732.
10. Werner N, Junk S, Laufs U, Link A, Walenta K, Bohm M et al. Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res 2003;93:e17-e24.
11. Werner N, Priller J, Laufs U, Endres M, Bohm M, Dirnagl U et al. Bone marrowderived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition. Arterioscler Thromb Vasc Biol 2002;22:1567-1572.
12. Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T et al. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation 2002; 105:3017-3024. (Pubitemid 34693836)
13. Iwakura A, Luedemann C, Shastry S, Hanley A, Kearney M, Aikawa R et al. Estrogenmediated, endothelial nitric oxide synthase-dependent mobilization of bone marrowderived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation 2003;108:3115-3121. (Pubitemid 38031801)
14. Lin HH, Chen YH, Yet SF, Chau LY. After vascular injury, heme oxygenase-1/carbon monoxide enhances re-endothelialization via promoting mobilization of circulating endothelial progenitor cells. J Thromb Haemost 2009;7:1401-1408.
15. Ii M, Takenaka H, Asai J, Ibusuki K, Mizukami Y, Maruyama K et al. Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circ Res 2006;98:697-704.
16. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B et al. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 2004;113:1258-1265. (Pubitemid 39069924)
17. Yoder MC. Is endothelium the origin of endothelial progenitor cells? Arterioscler Thromb Vasc Biol 2010;30:1094-1103.
18. Kong D, Melo LG, Gnecchi M, Zhang L, Mostoslavsky G, Liew CC et al. Cytokine-induced mobilization of circulating endothelial progenitor cells enhances repair of injured arteries. Circulation 2004;110:2039-2046. (Pubitemid 39331919)
19. Laufs U, Werner N, Link A, Endres M, Wassmann S, Jurgens K et al. Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 2004;109:220-226. (Pubitemid 38114143)
20. Zhao X, Huang L, Yin Y, Fang Y, Zhou Y. Autologous endothelial progenitor cells transplantation promoting endothelial recovery in mice. Transpl Int 2007;20:712-721. (Pubitemid 47024918)
21. Wassmann S, Werner N, Czech T, Nickenig G. Improvement of endothelial function by systemic transfusion of vascular progenitor cells. Circ Res 2006;99:e74-e83. (Pubitemid 44556373)
22. Sorrentino SA, Bahlmann FH, Besler C, Muller M, Schulz S, Kirchhoff N et al. Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: restoration by the peroxisome proliferatoractivated receptor-gamma agonist rosiglitazone. Circulation 2007;116:163-173. (Pubitemid 47057522)
23. Granada JF, Inami S, Aboodi MS, Tellez A, Milewski K, Wallace-Bradley D et al. Development of a novel prohealing stent designed to deliver sirolimus from a biodegradable abluminal matrix. Circ Cardiovasc Interv 2010;3:257-266.
24. Co M, Tay E, Lee CH, Poh KK, Low A, Lim J et al. Use of endothelial progenitor cell capture stent (Genous Bio-Engineered R Stent) during primary percutaneous coronary intervention in acute myocardial infarction: intermediate-to long-term clinical follow-up. Am Heart J 2008;155:128-132. (Pubitemid 350234778)
25. Aoki J, Serruys PW, van BH, Ong AT, McFadden EP, Sianos G et al. Endothelial progenitor cell capture by stents coated with antibody against CD34: the HEALING-FIM (Healthy Endothelial Accelerated Lining Inhibits Neointimal Growth-First In Man) Registry. J Am Coll Cardiol 2005;45:1574-1579. (Pubitemid 40704488)
26. Rohde E, Malischnik C, Thaler D, Maierhofer T, Linkesch W, Lanzer G et al. Blood monocytes mimic endothelial progenitor cells. Stem Cells 2006;24:357-367. (Pubitemid 44464805)
27. Tsuzuki M. Bone marrow-derived cells are not involved in reendothelialized endothelium as endothelial cells after simple endothelial denudation in mice. Basic Res Cardiol 2009;104:601-611.
28. Hagensen MK, Shim J, Falk E, Bentzon JF. Flanking recipient vasculature, not circulating progenitor cells, contributes to endothelium and smooth muscle in murine allograft vasculopathy. Arterioscler Thromb Vasc Biol 2011;31:808-813.
29. Hagensen MK, Shim J, Thim T, Falk E, Bentzon JF. Circulating endothelial progenitor cells do not contribute to plaque endothelium in murine atherosclerosis. Circulation 2010;121:898-905.
30. Motoike T, Loughna S, Perens E, Roman BL, Liao W, Chau TC et al. Universal GFP reporter for the study of vascular development. Genesis 2000;28:75-81.
31. Bentzon JF, Weile C, Sondergaard CS, Hindkjaer J, Kassem M, Falk E. Smooth muscle cells in atherosclerosis originate from the local vessel wall and not circulating progenitor cells in ApoE knockout mice. Arterioscler Thromb Vasc Biol 2006;26:2696-2702.
32. Hammerle H, Betz E, Herr D. Human endothelial cells are stimulated and vascular smooth muscle cells are inhibited in their proliferation and migration by heparins. Vasa 1991;20:207-215.
33. Xu Q, Zhang Z, Davison F, Hu Y. Circulating progenitor cells regenerate endothelium of vein graft atherosclerosis, which is diminished in ApoE-deficient mice. Circ Res 2003; 93:e76-e86.
34. Bentzon JF, Falk E. Circulating smooth muscle progenitor cells in atherosclerosis and plaque rupture: current perspective and methods of analysis. Vascul Pharmacol 2010; 52:11-20.
35. Reidy MA, Schwartz SM. Endothelial regeneration. III. Time course of intimal changes after small defined injury to rat aortic endothelium. Lab Invest 1981;44:301-308. (Pubitemid 11156721)
36. Hillebrands JL, Klatter FA, van Dijk WD, Rozing J. Bone marrow does not contribute substantially to endothelial-cell replacement in transplant arteriosclerosis. Nat Med 2002;8:194-195. (Pubitemid 34250078)
37. Hu Y, Davison F, Zhang Z, Xu Q. Endothelial replacement and angiogenesis in arteriosclerotic lesions of allografts are contributed by circulating progenitor cells. Circulation 2003;108:3122-3127. (Pubitemid 38031802)
38. Sirker AA, Astroulakis ZM, Hill JM. Vascular progenitor cells and translational research: the role of endothelial and smooth muscle progenitor cells in endogenous arterial remodelling in the adult. Clin Sci (Lond) 2009;116:283-299.
39. Timmermans F, Plum J, Yoder MC, Ingram DA, Vandekerckhove B, Case J. Endothelial progenitor cells: identity defined? J Cell Mol Med 2009;13:87-102.
40. Urbich C, Aicher A, Heeschen C, Dernbach E, Hofmann WK, Zeiher AM et al. Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Mol Cell Cardiol 2005;39:733-742. (Pubitemid 41464410)
41. Brazelton TR, Blau HM. Optimizing techniques for tracking transplanted stem cells in vivo. Stem Cells 2005;23:1251-1265. (Pubitemid 41504913)
42. Filipe C, Lam Shang Leen L, Brouchet L, Billon A, Benouaich V, Fontaine V et al. Estradiol accelerates endothelial healing through the retrograde commitment of uninjured endothelium. Am J Physiol Heart Circ Physiol 2008;294:H2822-H2830.
43. Tian C, Bagley J, Kaye J, Iacomini J. Induction of T cell tolerance to a protein expressed in the cytoplasm through retroviral-mediated gene transfer. J Gene Med 2003;5: 359-365. (Pubitemid 40309694)
44. Gambotto A, Dworacki G, Cicinnati V, Kenniston T, Steitz J, Tuting T et al. Immunogenicity of enhanced green fluorescent protein (EGFP) in BALB/c mice: identification of an H2-Kd-restricted CTL epitope. Gene Ther 2000;7:2036-2040. (Pubitemid 32036770)