Segregation of late outgrowth endothelial cells into functional endothelial CD34− and progenitor-like CD34+ cell populations

Angiogenesis

Volumn 18, Issue 1, 2015, Pages 47-68

  Ferreras, Cristina ^a   Cole, Claire L ^a   Urban, Katharina ^b   Jayson, Gordon C ^a   Avizienyte, Egle ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

ALDH; Angiogenesis; CD34; Late outgrowth endothelial cells; MMP 1; PAR 1; Peripheral blood

Indexed keywords

CD34 ANTIGEN; COLLAGEN; DRUG COMBINATION; INTERSTITIAL COLLAGENASE; LAMININ; MATRIGEL; PRIMER DNA; PROTEOGLYCAN; SMALL INTERFERING RNA; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL; CELL MOTION; CELL SEPARATION; CYTOLOGY; DRUG COMBINATION; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENETICS; HUMAN; IMMUNOBLOTTING; METABOLISM; MICROARRAY ANALYSIS; MOUSE; PHYSIOLOGY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; ANTIGENS, CD34; CELL MOVEMENT; CELL SEPARATION; COLLAGEN; DNA PRIMERS; DRUG COMBINATIONS; ENDOTHELIAL CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOBLOTTING; LAMININ; MATRIX METALLOPROTEINASE 1; MICE; MICROARRAY ANALYSIS; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEOGLYCANS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84920072936     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-014-9446-1     Document Type: Article

References (41)

1. Fadini GP, Losordo D, Dimmeler S (2012) Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 110:624–637
2. Hirschi KK, Ingram DA, Yoder MC (2008) Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 28:1584–1595
3. Ingram DA, Mead LE, Tanaka H et al (2004) Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104:2752–2760
4. Yoder MC, Mead LE, Prater D et al (2007) Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109:1801–1809
5. Roncalli JG, Tongers J, Renault MA, Losordo DW (2008) Endothelial progenitor cells in regenerative medicine and cancer: a decade of research. Trends Biotechnol 26:276–283
6. Rouhl RP, van Oostenbrugge RJ, Damoiseaux J et al (2008) Endothelial progenitor cell research in stroke: a potential shift in pathophysiological and therapeutical concepts. Stroke 39:2158–2165
7. Dudek AZ (2010) Endothelial lineage cell as a vehicle for systemic delivery of cancer gene therapy. Transl Res 156:136–146
8. Bodempudi V, Ohlfest JR, Terai K et al (2010) Blood outgrowth endothelial cell-based systemic delivery of antiangiogenic gene therapy for solid tumours. Cancer Gene Ther 17:855–863
9. 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
10. Bieback K, Vinci M, Elvers-Hornung S et al (2013) Recruitment of human cord blood-derived endothelial colony-forming cells to sites of tumour angiogenesis. Cytotherapy 15:1–14
11. Martin-Ramirez J, Hofman M, van den Biggelaar M et al (2012) Establishment of outgrowth endothelial cells from peripheral blood. Nat Protoc 7:1709–1715
12. Cole CL, Hansen SU, Baráth M et al (2010) Synthetic heparan sulfate oligosaccharides inhibit endothelial cell functions essential for angiogenesis. PLoS ONE 5:e11644
13. Ferreras C, Rushton G, Cole CL et al (2012) Endothelial heparan sulfate 6-O-sulfation levels regulate angiogenic responses of endothelial cells to fibroblast growth factor 2 and vascular endothelial growth factor. J Biol Chem 287:36132–36146
14. Albig AR, Schiemann WP (2005) Identification and characterization of regulator of G protein signaling 4 (RGS4) as a novel inhibitor of tubulogenesis: RGS4 inhibits mitogen-activated protein kinases and vascular endothelial growth factor signaling. Mol Biol Cell 16:609–625
15. Goerge T, Barg A, Schnaeker EM et al (2006) Tumour-derived matrix metalloproteinase-1 targets endothelial proteinase-activated receptor 1 promoting endothelial cell activation. Cancer Res 66:7766–7774
16. Boncela J, Przygodzka P, Wyroba E et al (2013) Secretion of SerpinB2 from endothelial cells activated with inflammatory stimuli. Exp Cell Res 319:1213–1219
17. Sato Y, Okamura K, Morimoto A et al (1993) Indispensable role of tissue-type plasminogen activator in growth factor-dependent tube formation of human microvascular endothelial cells in vitro. Exp Cell Res 204:223–229
18. Kroon ME, Koolwijk P, van der Vecht B, van Hinsbergh VW (2000) Urokinase receptor expression on human microvascular endothelial cells is increased by hypoxia: implications for capillary-like tube formation in a fibrin matrix. Blood 96:2775–2783
19. Krneta J, Kroll J, Alves F et al (2006) Dissociation of angiogenesis and tumourigenesis in follistatin- and activin-expressing tumours. Cancer Res 66:5686–5695
20. Schreiber AB, Winkler ME, Derynck R (1986) Transforming growth factor-alpha: a more potent angiogenic mediator than epidermal growth factor. Science 232:1250–1253
21. Fantin A, Vieira JM, Plein A et al (2013) NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis. Blood 121(12):2352–2362
22. Favier B, Alam A, Barron P et al (2006) Neuropilin-2 interacts with VEGFR-2 and VEGFR-3 and promotes human endothelial cell survival and migration. Blood 108(4):1243–1250
23. Austin KM, Covic L, Kuliopulos A (2013) Matrix metalloproteases and PAR-1 activation. Blood 121:431–439
24. Smadja DM, Bieche I, Uzan G et al (2005) PAR-1 activation on human late endothelial progenitor cells enhances angiogenesis in vitro with upregulation of the SDF-1/CXCR4 system. Arterioscler Thromb Vasc Biol 25:2321–2327
25. Basire A, Sabatier F, Ravet S et al (2006) High urokinase expression contributes to the angiogenic properties of endothelial cells derived from circulating progenitors. Thromb Haemost 95:678–688
26. Varani J, Perone P, Warner RL et al (2008) Vascular tube formation on matrix metalloproteinase-1-damaged collagen. Br J Cancer 98:1646–1652
27. Mazor R, Alsaigh T, Shaked H et al (2013) Matrix metalloproteinase-1-mediated up-regulation of vascular endothelial growth factor-2 in endothelial cells. J Biol Chem 288:598–607
28. Jiang A, Pan W, Milbauer LC et al (2007) A practical question based on cross-platform microarray data normalization: are OECS more like large vessel or microvascular endothelial cells or neither of them? J Bioinform Comput Biol 5:875–893
29. Urbich C, Dimmeler S (2004) Endothelial progenitor cells functional characterization. Trends Cardiovasc Med 14:318–322
30. Khodarev NN, Yu J, Labay E et al (2003) Tumour-endothelium interactions in co-culture: coordinated changes of gene expression profiles and phenotypic properties of endothelial cells. J Cell Sci 116:1013–1022
31. Wang Z, Kong D, Banerjee S et al (2007) Down-regulation of platelet-derived growth factor-D inhibits cell growth and angiogenesis through inactivation of Notch-1 and nuclear factor-kappaB signaling. Cancer Res 67:11377–11385
32. Weber KS, Nelson PJ, Gröne HJ et al (1999) Expression of CCR2 by endothelial cells: implications for MCP-1 mediated wound injury repair and in vivo inflammatory activation of endothelium. Arterioscler Thromb Vasc Biol 19:2085–2093
33. Kozian DH, Ziche M, Augustin HG (1997) The activin-binding protein follistatin regulates autocrine endothelial cell activity and induces angiogenesis. Lab Invest 76:267–276
34. Timmermans F, Plum J, Yoder MC et al (2008) Endothelial progenitor cells: identity defined? J Cell Mol Med 13:87–102
35. Masuda H, Alev C, Akimaru H et al (2011) Methodological development of a clonogenic assay to determine endothelial progenitor cell potential. Circ Res 109:20–37
36. Gunetti M, Noghero A, Molla F et al (2011) Ex vivo-expanded bone marrow cd34(+) for acute myocardial infarction treatment: in vitro and in vivo studies. Cytotherapy 13:1140–1152
37. Tura O, Skinner EM, Barclay GR et al (2013) Late outgrowth endothelial cells resemble mature endothelial cells and are not derived from bone marrow. Stem Cells 31:338–348
38. Ingram DA, Mead LE, Moore DB et al (2005) Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 105:2783–2786
39. de la Puente P, Muz B, Azab F et al (2013) Cell trafficking of endothelial progenitor cells in tumour progression. Clin Cancer Res 19:3360–336839
40. Rancourt C, Robertson MW 3rd, Wang M et al (1998) Endothelial cell vehicles for delivery of cytotoxic genes as a gene therapy approach for carcinoma of the ovary. Clin Cancer Res 4:265–270
41. Dudek AZ, Bodempudi V, Welsh BW et al (2007) Systemic inhibition of tumour angiogenesis by endothelial cell-based gene therapy. Br J Cancer 97:513–522