nach oben

Erschienen in:

01.07.2020 | Review Paper

Embryonic circulating endothelial progenitor cells

Erschienen in: Angiogenesis | Ausgabe 4/2020

Einloggen, um Zugang zu erhalten

Abstract

The development of vascular system in vertebrates has been traditionally explained by early vasculogenic assembly of angioblasts followed by angiogenic outgrowth of pre-existing vessels. The discovery of adult endothelial progenitor cells (Asahara et al. in Science 275(5302):964–967, 1997) challenged this view, since postnatal vascular growth could be accomplished by recruitment of circulating cells with the ability to differentiate into endothelial cells. However, the existence of embryonic circulating endothelial progenitor cells and their actual contribution to vascular development is far less known. We review in this paper the literature concerning the features, origin and physiological functions of embryonic and foetal circulating endothelial progenitors. Our review includes the early (E7.5) progenitors isolated from yolk sac, the hematovascular progenitors identified in the foetal liver, the yolk sac-derived erythro-myeloid progenitors, circulating hematopoietic cells from the G2-GATA4 lineage and the endothelial colony-forming cells isolated from the placenta and umbilical cord blood. We highlight the need of further characterization of these populations and the relationships between them.

Ribatti D, Nico B, Crivellato E (2015) The development of the vascular system: a historical overview. Methods Mol Biol 1214:1–14. https://doi.org/10.1007/978-1-4939-1462-3_1CrossRefPubMed

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(5302):964–967. https://doi.org/10.1126/science.275.5302.964CrossRefPubMed

Chong MS, Ng WK, Chan JK (2016) Concise review: endothelial progenitor cells in regenerative medicine: applications and challenges. Stem Cells Transl Med 5(4):530–538. https://doi.org/10.5966/sctm.2015-0227CrossRefPubMedPubMedCentral

Medina RJ, Barber CL, Sabatier F, Dignat-George F, Melero-Martin JM, Khosrotehrani K, Ohneda O, Randi AM, Chan JKY, Yamaguchi T, Van Hinsbergh VWM, Yoder MC, Stitt AW (2017) Endothelial progenitors: a consensus statement on nomenclature. Stem Cells Transl Med 6(5):1316–1320. https://doi.org/10.1002/sctm.16-0360CrossRefPubMedPubMedCentral

Chopra H, Hung MK, Kwong DL, Zhang CF, Pow EHN (2018) Insights into endothelial progenitor cells: origin, classification, potentials, and prospects. Stem Cells Int 2018:9847015. https://doi.org/10.1155/2018/9847015CrossRefPubMedPubMedCentral

Gumina DL, Su EJ (2017) Endothelial progenitor cells of the human placenta and fetoplacental circulation: a potential link to fetal, neonatal, and long-term health. Front Pediatr 5:41. https://doi.org/10.3389/fped.2017.00041CrossRefPubMedPubMedCentral

Minami Y, Nakajima T, Ikutomi M, Morita T, Komuro I, Sata M, Sahara M (2015) Angiogenic potential of early and late outgrowth endothelial progenitor cells is dependent on the time of emergence. Int J Cardiol 186:305–314. https://doi.org/10.1016/j.ijcard.2015.03.166CrossRefPubMed

Göthert JR, Gustin SE, van Eekelen JA, Schmidt U, Hall MA, Jane SM, Green AR, Göttgens B, Izon DJ, Begley CG (2004) Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood 104(6):1769–1777CrossRef

Purhonen S, Palm J, Rossi D, Kaskenpää N, Rajantie I, Ylä-Herttuala S, Alitalo K, Weissman IL, Salven P (2008) Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc Natl Acad Sci USA 105(18):6620–6625. https://doi.org/10.1073/pnas.0710516105CrossRefPubMed

10.

Aicher A, Rentsch M, Sasaki K, Ellwart JW, Fändrich F, Siebert R, Cooke JP, Dimmeler S, Heeschen C (2007) Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ Res 100(4):581–589CrossRef

11.

Zengin E, Chalajour F, Gehling UM, Ito WD, Treede H, Lauke H, Weil J, Reichenspurner H, Kilic N, Ergün S (2006) Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development 133(8):1543–1551CrossRef

12.

Ergün S, Tilki D, Hohn HP, Gehling U, Kilic N (2007) Potential implications of vascular wall resident endothelial progenitor cells. Thromb Haemost 98(5):930–939PubMed

13.

Klein D, Hohn HP, Kleff V, Tilki D, Ergün S (2010) Vascular wall-resident stem cells. Histol Histopathol 25(5):681–689PubMed

14.

Yoder MC (2010) Is endothelium the origin of endothelial progenitor cells? Arterioscler Thromb Vasc Biol 30(6):1094–1103. https://doi.org/10.1161/ATVBAHA.109.191635CrossRefPubMed

15.

Lin RZ, Moreno-Luna R, Muñoz-Hernandez R, Li D, Jaminet SC, Greene AK, Melero-Martin JM (2013) Human white adipose tissue vasculature contains endothelial colony-forming cells with robust in vivo vasculogenic potential. Angiogenesis 16(4):735–744. https://doi.org/10.1007/s10456-013-9350-0CrossRefPubMedPubMedCentral

16.

Pardanaud L, Eichmann A (2006) Identification, emergence and mobilization of circulating endothelial cells or progenitors in the embryo. Development 133(13):2527–2537CrossRef

17.

Pardanaud L, Altmann C, Kitos P, Dieterlen-Lièvre F, Buck C (1987) Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100:339–349PubMed

18.

Caprioli A, Jaffredo T, Gautier R, Dubourg C, Dieterlen-Lièvre F (1998) Blood-borne seeding by hematopoietic and endothelial precursors from the allantois. Proc Natl Acad Sci USA 95(4):1641–1646CrossRef

19.

Pardanaud L, Eichmann A (2011) Extraembryonic origin of circulating endothelial cells. PLoS ONE 6(10):e25889. https://doi.org/10.1371/journal.pone.0025889CrossRefPubMedPubMedCentral

20.

Pozzoli O, Vella P, Iaffaldano G, Parente V, Devanna P, Lacovich M, Lamia CL, Fascio U, Longoni D, Cotelli F, Capogrossi MC, Pesce M (2011) Endothelial fate and angiogenic properties of human CD34+ progenitor cells in zebrafish. Arterioscler Thromb Vasc Biol 31(7):1589–1597. https://doi.org/10.1161/ATVBAHA.111.226969CrossRefPubMed

21.

Hatzopoulos AK, Folkman J, Vasile E, Eiselen GK, Rosenberg RD (1998) Isolation and characterization of endothelial progenitor cells from mouse embryos. Development 125(8):1457–1468PubMed

22.

Kupatt C, Horstkotte J, Vlastos GA, Pfosser A, Lebherz C, Semisch M, Thalgott M, Büttner K, Browarzyk C, Mages J, Hoffmann R, Deten A, Lamparter M, Müller F, Beck H, Büning H, Boekstegers P, Hatzopoulos AK (2005) Embryonic endothelial progenitor cells expressing a broad range of proangiogenic and remodeling factors enhance vascularization and tissue recovery in acute and chronic ischemia. FASEB J 19(11):1576–1578CrossRef

23.

Kupatt C, Hinkel R, Lamparter M, von Brühl ML, Pohl T, Horstkotte J, Beck H, Müller S, Delker S, Gildehaus FJ, Büning H, Hatzopoulos AK, Boekstegers P (2005) Retroinfusion of embryonic endothelial progenitor cells attenuates ischemia-reperfusion injury in pigs: role of phosphatidylinositol 3-kinase/AKT kinase. Circulation 112(9 Suppl):117–122

24.

Hecht N, Schneider UC, Czabanka M, Vinci M, Hatzopoulos AK, Vajkoczy P, Woitzik J (2014) Endothelial progenitor cells augment collateralization and hemodynamic rescue in a model of chronic cerebral ischemia. J Cereb Blood Flow Metab 34(8):1297–1305. https://doi.org/10.1038/jcbfm.2014.78CrossRefPubMedPubMedCentral

25.

Wei J, Blum S, Unger M, Jarmy G, Lamparter M, Geishauser A, Vlastos GA, Chan G, Fischer KD, Rattat D, Debatin KM, Hatzopoulos AK, Beltinger C (2004) Embryonic endothelial progenitor cells armed with a suicide gene target hypoxic lung metastases after intravenous delivery. Cancer Cell 5(5):477–488CrossRef

26.

Vajkoczy P, Blum S, Lamparter M, Mailhammer R, Erber R, Engelhardt B, Vestweber D, Hatzopoulos AK (2003) Multistep nature of microvascular recruitment of ex vivo-expanded embryonic endothelial progenitor cells during tumor angiogenesis. J Exp Med 197(12):1755–1765CrossRef

27.

Defresne F, Bouzin C, Grandjean M, Dieu M, Raes M, Hatzopoulos AK, Kupatt C, Feron O (2011) Preconditioned endothelial progenitor cells reduce formation of melanoma metastases through SPARC-driven cell-cell interactions and endocytosis. Cancer Res 71(14):4748–4757. https://doi.org/10.1158/0008-5472.CAN-10-2449CrossRefPubMed

28.

Ratliff BB, Ghaly T, Brudnicki P, Yasuda K, Rajdev M, Bank M, Mares J, Hatzopoulos AK, Goligorsky MS (2010) Endothelial progenitors encapsulated in bioartificial niches are insulated from systemic cytotoxicity and are angiogenesis competent. Am J Physiol Renal Physiol 299(1):F178–186. https://doi.org/10.1152/ajprenal.00102.2010CrossRefPubMedPubMedCentral

29.

Pfosser A, El-Aouni C, Pfisterer I, Dietz M, Globisch F, Stachel G, Trenkwalder T, Pinkenburg O, Horstkotte J, Hinkel R, Sperandio M, Hatzopoulos AK, Boekstegers P, Bals R, Kupatt C (2010) NF kappaB activation in embryonic endothelial progenitor cells enhances neovascularization via PSGL-1 mediated recruitment: novel role for LL37. Stem Cells 28(2):376–385. https://doi.org/10.1002/stem.280CrossRefPubMed

30.

Hinkel R, El-Aouni C, Olson T, Horstkotte J, Mayer S, Müller S, Willhauck M, Spitzweg C, Gildehaus FJ, Münzing W, Hannappel E, Bock-Marquette I, DiMaio JM, Hatzopoulos AK, Boekstegers P, Kupatt C (2008) Thymosin beta4 is an essential paracrine factor of embryonic endothelial progenitor cell-mediated cardioprotection. Circulation 117(17):2232–2240. https://doi.org/10.1161/CIRCULATIONAHA.107.758904CrossRefPubMedPubMedCentral

31.

Safa RN, Peng XY, Pentassuglia L, Lim CC, Lamparter M, Silverstein C, Walker J, Chen B, Geisberg C, Hatzopoulos AK, Sawyer DB (2011) Neuregulin-1β regulation of embryonic endothelial progenitor cell survival. Am J Physiol Heart Circ Physiol 300(4):H1311–1319. https://doi.org/10.1152/ajpheart.01104.2009CrossRefPubMedPubMedCentral

32.

Ryzhov S, Solenkova NV, Goldstein AE, Lamparter M, Fleenor T, Young PP, Greelish JP, Byrne JG, Vaughan DE, Biaggioni I, Hatzopoulos AK, Feoktistov I (2008) Adenosine receptor-mediated adhesion of endothelial progenitors to cardiac microvascular endothelial cells. Circ Res 102(3):356–363CrossRef

33.

Langer H, May AE, Daub K, Heinzmann U, Lang P, Schumm M, Vestweber D, Massberg S, Schönberger T, Pfisterer I, Hatzopoulos AK, Gawaz M (2006) Adherent platelets recruit and induce differentiation of murine embryonic endothelial progenitor cells to mature endothelial cells in vitro. Circ Res 98(2):e2–10CrossRef

34.

Cherqui S, Kurian SM, Schussler O, Hewel JA, Yates JR 3rd, Salomon DR (2006) Isolation and angiogenesis by endothelial progenitors in the fetal liver. Stem Cells 24(1):44–54CrossRef

35.

Göthert JR, Gustin SE, Hall MA, Green AR, Göttgens B, Izon DJ, Begley CG (2005) In vivo fate-tracing studies using the Scl stem cell enhancer: embryonic hematopoietic stem cells significantly contribute to adult hematopoiesis. Blood 105(7):2724–2732CrossRef

36.

García-Ortega AM, Cañete A, Quinter C, Silberstein L, Piquer-Gil M, Álvarez-Dolado M, Dekel B, Gottgens B, Sánchez MJ (2010) Enhanced hematovascular contribution of SCL 3' enhancer expressing fetal liver cells uncovers their potential to integrate in extramedullary adult niches. Stem Cells 28(1):100–112. https://doi.org/10.1002/stem.228CrossRefPubMed

37.

Cañete A, Comaills V, Prados I, Castro AM, Hammad S, Ybot-Gonzalez P, Bockamp E, Hengstler JG, Gottgens B, Sánchez MJ (2017) Characterization of a fetal liver cell population endowed with long-term multiorgan endothelial reconstitution potential. Stem Cells 35(2):507–521. https://doi.org/10.1002/stem.2494CrossRefPubMed

38.

Bockamp E, Antunes C, Liebner S, Schmitt S, Cabezas-Wallscheid N, Heck R, Ohnngemach S, Oesch-Bartlomowicz B, Rickert C, Sanchez MJ, Hengstler J, Kaina B, Wilson A, Trumpp A, Eshkind L (2009) In vivo fate mapping with SCL regulatory elements identifies progenitors for primitive and definitive hematopoiesis in mice. Mech Dev 126(10):863–872. https://doi.org/10.1016/j.mod.2009.07.005CrossRefPubMed

39.

Rojas A, De Val S, Heidt AB, Xu SM, Bristow J, Black BL (2005) Gata4 expression in lateral mesoderm is downstream of BMP4 and is activated directly by Forkhead and GATA transcription factors through a distal enhancer element. Development 132:3405–3417CrossRef

40.

Cañete A, Carmona R, Ariza L, Sánchez MJ, Rojas A, Muñoz-Chápuli R (2017) A population of hematopoietic stem cells derives from GATA4-expressing progenitors located in the placenta and lateral mesoderm of mice. Haematologica 102(4):647–655. https://doi.org/10.3324/haematol.2016.155812CrossRefPubMedPubMedCentral

41.

Carmona R, Barrena S, López Gambero AJ, Rojas A, Muñoz-Chápuli R (2020) Epicardial cell lineages and the origin of the coronary endothelium. FASEB J. https://doi.org/10.1096/fj.201902249RRCrossRefPubMed

42.

Wu B, Zhang Z, Lui W, Chen X, Wang Y, Chamberlain AA, Moreno-Rodriguez RA, Markwald RR, O'Rourke BP, Sharp DJ, Zheng D, Lenz J, Baldwin HS, Chang CP, Zhou B (2012) Endocardial cells form the coronary arteries by angiogenesis through myocardial-endocardial VEGF signaling. Cell 151(5):1083–1096. https://doi.org/10.1016/j.cell.2012.10.023CrossRefPubMedPubMedCentral

43.

Hoeffel G, Chen J, Lavin Y, Low D, Almeida FF, See P, Beaudin AE, Lum J, Low I, Forsberg EC, Poidinger M, Zolezzi F, Larbi A, Ng LG, Chan JK, Greter M, Becher B, Samokhvalov IM, Merad M, Ginhoux F (2015) C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42(4):665–678. https://doi.org/10.1016/j.immuni.2015.03.01CrossRefPubMedPubMedCentral

44.

McGrath KE, Frame JM, Fegan KH, Bowen JR, Conway SJ, Catherman SC, Kingsley PD, Koniski AD, Palis J (2015) Distinct sources of hematopoietic progenitors emerge before HSCs and provide functional blood cells in the mammalian embryo. Cell Rep 11(12):1892–1904. https://doi.org/10.1016/j.celrep.2015.05.036CrossRefPubMedPubMedCentral

45.

Plein A, Fantin A, Denti L, Pollard JW, Ruhrberg C (2018) Erythro-myeloid progenitors contribute endothelial cells to blood vessels. Nature 562(7726):223–228. https://doi.org/10.1038/s41586-018-0552-xCrossRefPubMedPubMedCentral

46.

Rapp BM, Saadatzedeh MR, Ofstein RH, Bhavsar JR, Tempel ZS, Moreno O, Morone P, Booth DA, Traktuev DO, Dalsing MC, Ingram DA, Yoder MC, March KL, Murphy MP (2011) Resident endothelial progenitor cells from human placenta have greater vasculogenic potential than circulating endothelial progenitor cells from umbilical cord blood. Cell Med 2(3):85–96. https://doi.org/10.3727/215517911X617888CrossRefPubMedPubMedCentral

47.

Patel J, Seppanen E, Chong MS, Yeo JS, Teo EY, Chan JK, Fisk NM, Khosrotehrani K (2013) Prospective surface marker-based isolation and expansion of fetal endothelial colony-forming cells from human term placenta. Stem Cells Transl Med 2(11):839–847. https://doi.org/10.5966/sctm.2013-0092CrossRefPubMedPubMedCentral

48.

Gumina DL, Black CP, Balasubramaniam V, Winn VD, Baker CD (2017) Umbilical cord blood circulating progenitor cells and endothelial colony-forming cells are decreased in preeclampsia. Reprod Sci 24(7):1088–1096. https://doi.org/10.1177/1933719116678692CrossRefPubMed

49.

Solomon I, O'Reilly M, Ionescu L, Alphonse RS, Rajabali S, Zhong S, Vadivel A, Shelley WC, Yoder MC, Thébaud B (2016) Functional differences between placental micro- and macrovascular endothelial colony-forming cells. Stem Cells Transl Med 5(3):291–300. https://doi.org/10.5966/sctm.2014-0162CrossRefPubMedPubMedCentral

50.

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(9):2752–2760CrossRef

51.

Prasain N, Meador JL, Yoder MC (2012) Phenotypic and functional characterization of endothelial colony forming cells derived from human umbilical cord blood. J Vis Exp 62:3872. https://doi.org/10.3791/3872CrossRef

52.

Zhang H, Tao Y, Ren S, Liu H, Zhou H, Hu J, Tang Y, Zhang B, Chen H (2017) Isolation and characterization of human umbilical cord-derived endothelial colony-forming cells. Exp Ther Med 14(5):4160–4166. https://doi.org/10.3892/etm.2017.5035CrossRefPubMedPubMedCentral

53.

Bompais H, Chagraoui J, Canron X, Crisan M, Liu XH, Anjo A, Tolla-Le Port C, Leboeuf M, Charbord P, Bikfalvi A, Uzan G (2004) Human endothelial cells derived from circulating progenitors display specific functional properties compared with mature vessel wall endothelial cells. Blood 103(7):2577–2584CrossRef

54.

Javed MJ, Mead LE, Prater D, Bessler WK, Foster D, Case J, Goebel WS, Yoder MC, Haneline LS, Ingram DA (2008) Endothelial colony forming cells and mesenchymal stem cells are enriched at different gestational ages in human umbilical cord blood. Pediatr Res 64(1):68–73. https://doi.org/10.1203/PDR.0b013e31817445e9CrossRefPubMed

55.

Baker CD, Ryan SL, Ingram DA, Seedorf GJ, Abman SH, Balasubramaniam V (2009) Endothelial colony-forming cells from preterm infants are increased and more susceptible to hyperoxia. Am J Respir Crit Care Med 180(5):454–461. https://doi.org/10.1164/rccm.200901-0115OCCrossRefPubMedPubMedCentral

56.

Safranow K, Kotowski M, Lewandowska J, Machalińska A, Dziedziejko V, Czajka R, Celewicz Z, Rudnicki J, Machaliński B (2012) Circulating endothelial progenitor cells in premature infants: is there an association with premature birth complications? J Perinat Med 40(4):455–462. https://doi.org/10.1515/jpm-2011-0199CrossRefPubMed

57.

Borghesi A, Massa M, Campanelli R, Bollani L, Tzialla C, Figar TA, Ferrari G, Bonetti E, Chiesa G, de Silvestri A, Spinillo A, Rosti V, Stronati M (2009) Circulating endothelial progenitor cells in preterm infants with bronchopulmonary dysplasia. Am J Respir Crit Care Med 180(6):540–546. https://doi.org/10.1164/rccm.200812-1949OCCrossRefPubMed

58.

Muñoz-Hernandez R, Miranda ML, Stiefel P, Lin RZ, Praena-Fernández JM, Dominguez-Simeon MJ, Villar J, Moreno-Luna R, Melero-Martin JM (2014) Decreased level of cord blood circulating endothelial colony-forming cells in preeclampsia. Hypertension 64(1):165–171. https://doi.org/10.1161/HYPERTENSIONAHA.113.03058CrossRefPubMedPubMedCentral

59.

Grundmann M, Haidar M, Placzko S, Niendorf R, Darashchonak N, Hubel CA, von Versen-Höynck F (2012) Vitamin D improves the angiogenic properties of endothelial progenitor cells. Am J Physiol Cell Physiol 303(9):C954–962. https://doi.org/10.1152/ajpcell.00030.2012CrossRefPubMedPubMedCentral

60.

von Versen-Höynck F, Brodowski L, Dechend R, Myerski AC, Hubel CA (2014) Vitamin D antagonizes negative effects of preeclampsia on fetal endothelial colony forming cell number and function. PLoS ONE 9(6):e98990. https://doi.org/10.1371/journal.pone.0098990CrossRef

61.

Attar A, Monabati A, Parsanezhad ME (2017) Endothelial progenitor cell subsets and preeclampsia: findings and controversies. J Chin Med Assoc 80(10):615–622. https://doi.org/10.1016/j.jcma.2017.06.013CrossRefPubMed

62.

Ligi I, Simoncini S, Tellier E, Vassallo PF, Sabatier F, Guillet B, Lamy E, Sarlon G, Quemener C, Bikfalvi A, Marcelli M, Pascal A, Dizier B, Simeoni U, Dignat-George F, Anfosso F (2011) A switch toward angiostatic gene expression impairs the angiogenic properties of endothelial progenitor cells in low birth weight preterm infants. Blood 118(6):1699–1709. https://doi.org/10.1182/blood-2010-12-325142CrossRefPubMed

63.

Sipos PI, Rens W, Schlecht H, Fan X, Wareing M, Hayward C, Hubel CA, Bourque S, Baker PN, Davidge ST, Sibley CP, Crocker IP (2013) Uterine vasculature remodeling in human pregnancy involves functional macrochimerism by endothelial colony forming cells of fetal origin. Stem Cells 31(7):1363–1370. https://doi.org/10.1002/stem.1385CrossRefPubMedPubMedCentral

64.

Sipos PI, Bourque SL, Hubel CA, Baker PN, Sibley CP, Davidge ST, Crocker IP (2013) Endothelial colony-forming cells derived from pregnancies complicated by intrauterine growth restriction are fewer and have reduced vasculogenic capacity. J Clin Endocrinol Metab 98(12):4953–4960. https://doi.org/10.1210/jc.2013-2580CrossRefPubMedPubMedCentral

65.

Gui J, Rohrbach A, Borns K, Hillemanns P, Feng L, Hubel CA, von Versen-Höynck F (2015) Vitamin D rescues dysfunction of fetal endothelial colony forming cells from individuals with gestational diabetes. Placenta 36(4):410–418. https://doi.org/10.1016/j.placenta.2015.01.195CrossRefPubMed

66.

Kim H, Prasain N, Vemula S, Ferkowicz MJ, Yoshimoto M, Voytik-Harbin SL, Yoder MC (2015) Human platelet lysate improves human cord blood derived ECFC survival and vasculogenesis in three dimensional (3D) collagen matrices. Microvasc Res 101:72–81. https://doi.org/10.1016/j.mvr.2015.06.006CrossRefPubMedPubMedCentral

67.

Reid E, Guduric-Fuchs J, O'Neill CL, Allen LD, Chambers SEJ, Stitt AW, Medina RJ (2018) Preclinical evaluation and optimization of a cell therapy using human cord blood-derived endothelial colony-forming cells for ischemic retinopathies. Stem Cells Transl Med 7(1):59–67. https://doi.org/10.1002/sctm.17-0187CrossRefPubMed

68.

Ingram DA, Mead LE, Moore DB, Woodard W, Fenoglio A, Yoder MC (2005) Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 105(7):2783–2786CrossRef

69.

Huang L, Critser PJ, Grimes BR, Yoder MC (2011) Human umbilical cord blood plasma can replace fetal bovine serum for in vitro expansion of functional human endothelial colony-forming cells. Cytotherapy 13(6):712–721CrossRef

70.

Lacaud G, Kouskoff V (2017) Hemangioblast, hemogenic endothelium, and primitive versus definitive hematopoiesis. Exp Hematol 49:19–24. https://doi.org/10.1016/j.exphem.2016.12.009CrossRefPubMed

71.

Muñoz-Chápuli R, Carmona R, Guadix JA, Macías D, Pérez-Pomares JM (2005) The origin of the endothelial cells: an evo-devo approach for the invertebrate/vertebrate transition of the circulatory system. Evol Dev 7(4):351–358CrossRef

Titel: Embryonic circulating endothelial progenitor cells
Publikationsdatum: 01.07.2020
Erschienen in: Angiogenesis / Ausgabe 4/2020
Print ISSN: 0969-6970
Elektronische ISSN: 1573-7209
DOI: https://doi.org/10.1007/s10456-020-09732-y

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

Die „Zehn Gebote“ des Endokarditis-Managements

30.04.2024 Endokarditis Leitlinie kompakt

Worauf kommt es beim Management von Personen mit infektiöser Endokarditis an? Eine Kardiologin und ein Kardiologe fassen die zehn wichtigsten Punkte der neuen ESC-Leitlinie zusammen.

Strenge Blutdruckeinstellung lohnt auch im Alter noch

30.04.2024 Arterielle Hypertonie Nachrichten

Ältere Frauen, die von chronischen Erkrankungen weitgehend verschont sind, haben offenbar die besten Chancen, ihren 90. Geburtstag zu erleben, wenn ihr systolischer Blutdruck < 130 mmHg liegt. Das scheint selbst für 80-Jährige noch zu gelten.

Frauen bekommen seltener eine intensive Statintherapie

30.04.2024 Statine Nachrichten

Frauen in den Niederlanden erhalten bei vergleichbarem kardiovaskulärem Risiko seltener eine intensive Statintherapie als Männer. Ihre LDL-Zielwerte erreichen sie aber fast ähnlich oft.

Reizdarmsyndrom: Diäten wirksamer als Medikamente

29.04.2024 Reizdarmsyndrom Nachrichten

Bei Reizdarmsyndrom scheinen Diäten, wie etwa die FODMAP-arme oder die kohlenhydratreduzierte Ernährung, effektiver als eine medikamentöse Therapie zu sein. Das hat eine Studie aus Schweden ergeben, die die drei Therapieoptionen im direkten Vergleich analysierte.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 4/2020

Roxadustat (FG-4592) accelerates pulmonary growth, development, and function in a compensatory lung growth model

Angiopoietin-2 as a marker of endothelial activation is a good predictor factor for intensive care unit admission of COVID-19 patients

Leopold Auerbach’s achievements in the field of vascular system

Pleiotrophin selectively binds to vascular endothelial growth factor receptor 2 and inhibits or stimulates cell migration depending on ανβ3 integrin expression

Are antiangiogenics a good ‘partner’ for immunotherapy in ovarian cancer?