Cited by 157Angiogenesis and VEGF in CancerMesenchymal stem cell researchCell Adhesion Molecules Research

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A comparison of the tube forming potentials of early and late endothelial progenitor cells

Mukai, Nana, Akahori, Taichi, Komaki, Motohiro, Li, Qin, Kanayasu-Toyoda, Toshie, Ishii-Watabe, Akiko, Kobayashi, Akiko, Yamaguchi, Teruhide, Abe, Mayumi, Amagasa, Teruo, Morita, Ikuo·2008·Experimental Cell Research

DOI 10.1016/j.yexcr.2007.11.016

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Abstract

The identification of circulating endothelial progenitor cells (EPCs) has revolutionized approaches to cell-based therapy for injured and ischemic tissues. However, the mechanisms by which EPCs promote the formation of new vessels remain unclear. In this study, we obtained early EPCs from human peripheral blood and late EPCs from umbilical cord blood. Human umbilical vascular endothelial cells (HUVECs) were also used. Cells were evaluated for their tube-forming potential using our novel in vitro assay system. Cells were seeded linearly along a 60 mum wide path generated by photolithographic methods. After cells had established a linear pattern on the substrate, they were transferred onto Matrigel. Late EPCs formed tubular structures similar to those of HUVECs, whereas early EPCs randomly migrated and failed to form tubular structures. Moreover, late EPCs participate in tubule formation with HUVECs. Interestingly, late EPCs in Matrigel migrated toward pre-existing tubular structures constructed by HUVECs, after which they were incorporated into the tubules. In contrast, early EPCs promote sprouting of HUVECs from tubular structures. The phenomena were also observed in the in vivo model. These observations suggest that early EPCs cause the disorganization of pre-existing vessels, whereas late EPCs constitute and orchestrate vascular tube formation.

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Background
High-reproducible flow cytometric endothelial progenitor cell determination in human peripheral blood as CD34+/CD144+/CD3− lymphocyte sub-population
Redondo, S., Hristov, M., Gordillo‐Moscoso, A., Ruiz, E., Weber, C., & Tejerina, T. (2008) · Journal of Immunological Methods · doi:10.1016/j.jim.2008.02.011 · Cited by 31
Dysregulation of Vascular Endothelial Growth Factor Receptor-2 by Multiple miRNAs in Endothelial Colony-Forming Cells of Coronary Artery Disease
Su, S., Wu, C., Chiu, Y.-L., Chang, S., Lo, H.-H., Liao, K., Tsai, C.-F., Tsai, T.-N., Lin, C.-H., Cheng, S., et al. (2017) · Journal of Vascular Research · doi:10.1159/000449202 · Cited by 30
Cord blood-endothelial colony forming cells are immunotolerated and participate at post-ischemic angiogenesis in an original dorsal chamber immunocompetent mouse model
Proust, R., Ponsen, A., Rouffiac, V., Schenowitz, C., Montespan, F., Roux, K. S., Leeuw, F. D., Laplace‐Builhé, C., Mauduit, P., Carosella, E. D., et al. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01687-7 · Cited by 29
“In vitro, mainly two distinct cell types have been identified [15]: (i) early EPCs or colony forming unit-endothelial cells (CFU-ECs) with myeloid phenotype displaying, in vivo, a paracrine angiogenic effect [16] and (ii) late EPCs or endothelial colony forming cells (ECFCs), also known as outgrowth endothelial cells…”
Background
Derivation of endothelial cells from human embryonic stem cells in fully defined medium enables identification of lysophosphatidic acid and platelet activating factor as regulators of eNOS localization
Costa, M., Sourris, K., Lim, S. M., Yu, Q. C., Hirst, C. E., Parkington, H. C., Jokubaitis, V. J., Dear, A. E., Liu, H. B., Micallef, S. J., et al. (2012) · Stem Cell Research · doi:10.1016/j.scr.2012.10.003 · Cited by 29
Cathepsin L in Bone Marrow-Derived Cells Is Required for Retinal and Choroidal Neovascularization
Shimada, N., Ohno‐Matsui, K., Iseki, S., Koike, M., Uchiyama, Y., Wang, J., Yoshida, T., Sato, T., Peters, C., Mochizuki, M., et al. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.091027 · Cited by 29
Self-citation
Effects and mechanisms of natural plant active compounds for the treatment of osteoclast-mediated bone destructive diseases
Xu, Q., Cao, Z., JiaQiang, X., Dai, M., Zhang, B., Lai, Q., & Liu, X. (2021) · Journal of drug targeting · doi:10.1080/1061186x.2021.2013488 · Cited by 28
A critical role of CXCR2 PDZ-mediated interactions in endothelial progenitor cell homing and angiogenesis
Hou, Y., Wu, Y., Farooq, S. M., Guan, X., Wang, S., Liu, Y., Oblak, J. J., Holcomb, J., Jiang, Y., Strieter, R. M., et al. (2014) · Stem Cell Research · doi:10.1016/j.scr.2014.12.001 · Cited by 29
“incorporating into endothelial network and provide building blocks for neovascularization [4, 35, 36].”
Background
Regression and persistence: remodelling in a tissue engineered axial vascular assembly
Polykandriotis, E., Euler, S. A., Arkudas, A., Pryymachuk, G., Beier, J. P., Greil, P., Adrian Dragu, A., Lametschwandtner, A., Kneser, U., & Horch, R. E. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00828.x · Cited by 27
“Experiments with endothelial cells or their progenitor cells in vitro have zeroed on profiles of VEGF expression or total length of generated tubule-like-structures [25].”
Background
Endothelial Nitric Oxide Synthase as A Marker for Human Endothelial Progenitor Cells
Qiao, W., Niu, L., Liu, Z., Qiao, T., & Liu, C. (2010) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.221.19 · Cited by 26
“Mukai et al. (2008) have compared the tube formation potentials of the two types of cells and found that EC-like cells caused the disorganization of pre-existing vessels, whereas EOCs constituted and orchestrated vascular tube formation.”
Combinatorial approach for improving the outcome of angiogenic therapy in ischemic tissues
(Grigorescu), G. O., Preda, M. B., Radu, E., Rosca, A., Ţuţuianu, R., Mitroi, D. N., Simionescu, M., & Burlacu, A. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.05.002 · Cited by 26
miR-150 regulates endothelial progenitor cell differentiation via Akt and promotes thrombus resolution
Du, X., Hu, N., Yu, H., Hong, L., Ran, F., Huang, D., Zhou, M., Li, C., & Li, X. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01871-9 · Cited by 24
In vitro vessel-forming capacity of endothelial progenitor cells in high glucose conditions
Jiraritthamrong, C., Kheolamai, P., U‐pratya, Y., Chayosumrit, M., Supokawej, A., Manochantr, S., Tantrawatpan, C., Sritanaudomchai, H., & Issaragrisil, S. (2011) · Annals of Hematology · doi:10.1007/s00277-011-1300-6 · Cited by 24
“Matrigel and incorporate into preexisting mature endothelial cells resulting in new blood vessel formation [12, 13].”
Background
Stem cell therapy targeting the right ventricle in pulmonary arterial hypertension: is it a potential avenue of therapy?
Loisel, F., Provost, B., Haddad, F., Guihaire, J., Amsallem, M., Vrtovec, B., Fadel, É., Uzan, G., & Mercier, O. M. (2018) · Pulmonary Circulation · doi:10.1177/2045893218755979 · Cited by 24
Angiogenic activity of endothelial progenitor cells through angiopoietin-1 and angiopoietin-2
Siavashi, V., Sariri, R., Nassiri, S. M., Esmaeilivand, M., Asadian, S., Cheraghi, H., Barekati‐Mowahed, M., & Rahbarghazi‬, R. (2016) · Animal Cells and Systems · doi:10.1080/19768354.2016.1189961 · Cited by 23
“Matrigel tube formation assay was performed as previously described with some modifications (Mukai et al. 2008).”
Method
Transcriptome Analysis in Endothelial Progenitor Cell Biology
Gremmels, H., Fledderus, J. O., van Balkom, B. W. M., & Verhaar, M. C. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3594 · Cited by 22
“It was discovered that CACs have little or no proliferative capacity (55, 146) and are unable to form tubular networks on basement membrane matrix (Matrigel) (85).”
Angiogenic Role of MMP‐2/9 Expressed on the Cell Surface of Early Endothelial Progenitor Cells/Myeloid Angiogenic Cells
Kanayasu‐Toyoda, T., Tanaka, T., Ishii‐Watabe, A., Kitagawa, H., Matsuyama, A., Uchida, E., & Yamaguchi, T. (2015) · Journal of Cellular Physiology · doi:10.1002/jcp.25002 · Cited by 21
“Nucera et al. (2011) proposed that the generation of proangiogenic Mf from embryonic stem cells may provide a source of therapeutic cells for the treatment of ischemia, injured tissues, and chronic wounds.”
BackgroundSelf-citation
Enhanced Adhesion of Early Endothelial Progenitor Cells to Radiation-induced Senescence-like Vascular Endothelial Cells in vitro
Sermsathanasawadi, N., Ishii, H., IGARASHI, K., Miura, M., Yoshida, M., Inoue, Y., & Iwai, T. (2009) · Journal of Radiation Research · doi:10.1269/jrr.09036 · Cited by 20
Capability of human umbilical cord blood progenitor-derived endothelial cells to form an efficient lining on a polyester vascular graft in vitro
Bérard, X., Rémy, M., Bourget, C., Turner, N. J., Bareille, R., Daculsi, R., & Bordenave, L. (2008) · Acta Biomaterialia · doi:10.1016/j.actbio.2008.10.002 · Cited by 20
Short-term fibronectin treatment induces endothelial-like and angiogenic properties in monocyte-derived immature dendritic cells: Involvement of intracellular VEGF and MAPK regulation
Berger, S., Dyugovskaya, L., Polyakov, A., & Lavie, L. (2012) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2012.02.003 · Cited by 19
Effect and Mechanism of Thrombospondin-1 on the Angiogenesis Potential in Human Endothelial Progenitor Cells: An In Vitro Study
Qin, Q., Qian, J., Ge, L., Shen, L., Jia, J., Jin, J., & Ge, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088213 · Cited by 19
“After 7 days in culture, adherent cells found to endocytose DiI-AcLDL and immunostained positive for VEGFR2 and CD31 are early EPCs (Figure 1C) as reported [21,22].”
BackgroundResult
Cell-printing and transfer technology applications for bone defects in mice
Tsugawa, J., Komaki, M., Yoshida, T., Nakahama, K., Amagasa, T., & Morita, I. (2011) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.366 · Cited by 18
“The patterned glass substrate was prepared by coating glass with PEG and by performing photo-lithography with a photo-mask to form a cellattached area and a non-attached area (Akahori et al., 2010; Mukai et al., 2008; Kobayashi et al., 2007).”
MethodSelf-citation
Pericytes in the Periodontal Ligament
Komaki, M. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-11093-2_10 · Cited by 18
Self-citation
Exploring Endothelial Colony-Forming Cells to Better Understand the Pathophysiology of Disease: An Updated Review
Zhang, Q., Cannavicci, A., & Kutryk, M. J. B. (2022) · Stem Cells International · doi:10.1155/2022/4460041 · Cited by 18
Differential Expression of Distinct Surface Markers in Early Endothelial Progenitor Cells and Monocyte-Derived Macrophages
Cheng, S., Chang, S., Tsai, T.-N., Wu, C., Lin, W.-S., Lin, W., & Cheng, C. (2013) · Gene Expression · doi:10.3727/105221613x13776146743307 · Cited by 16
“In contrast, eEPCs indirectly augment tubulogenesis even when physically separated from their target by a Transwell membrane, which implies that their effectiveness occurs via a cytokine-based paracrine mechanism (6,7).”
Background
Effects of various monomers and micro-structure of polyhydroxyalkanoates on the behavior of endothelial progenitor cells and endothelial cells for vascular tissue engineering
Yao, C., Chen, J.-H., & Lee, C.-H. (2017) · Journal of Polymer Research · doi:10.1007/s10965-017-1341-1 · Cited by 15
Reprogramming of Adult Peripheral Blood Cells into Human Induced Pluripotent Stem Cells as a Safe and Accessible Source of Endothelial Cells
Šimara, P., Tesařová, L., Řeháková, D., Farkaš, Š., Šalingová, B., Kutálková, K., Vavrečková, E., Matula, P., Matula, P., Veverková, L., et al. (2017) · Stem Cells and Development · doi:10.1089/scd.2017.0132 · Cited by 16
“Late-outgrowth EPCs, unlike early-outgrowth EPCs, contribute to blood vessels formation and reparation by direct incorporation into their endothelial lining [56,57].”
The Use of Live Cell Imaging and Automated Image Analysis to Assist With Determining Optimal Parameters for Angiogenic Assay in vitro
Huuskes, B. M., Debuque, R. J., Kerr, P. G., Samuel, C. S., & Ricardo, S. D. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00045 · Cited by 15
“Conversely, time-lapse microscopy offers the advantage of visualizing tube formation over multiple time points and therefore fixation of tubes at specific time points (Mukai et al., 2008) is not necessary.”
Background
Endothelial Progenitor Cells in Moyamoya Disease: Current Situation and Controversial Issues
Yu, J., Du, Q., Hu, M., Zhang, J., & Chen, J. (2020) · Cell Transplantation · doi:10.1177/0963689720913259 · Cited by 15
Differential gene expression in Lin-/VEGF-R2+ bone marrow-derived endothelial progenitor cells isolated from diabetic mice
Barthelmes, D., Zhu, L., Shen, W., Gillies, M. C., & Irhimeh, M. R. (2014) · Cardiovascular Diabetology · doi:10.1186/1475-2840-13-42 · Cited by 14
“These EPCs play an important role in regenerating the endothelium through migration, proliferation, differentiation and by secreting pro-angiogenic cytokines [13].”
Background
Bioreactor Systems for Tissue Engineering II
Kasper, C., van Griensven, M., & Pörtner, R. (2010) · Springer eBooks · doi:10.1007/978-3-642-16051-6 · Cited by 15
Occludin as a functional marker of vascular endothelial cells on tube‐forming activity
Kanayasu‐Toyoda, T., Ishii‐Watabe, A., Kikuchi, Y., Kitagawa, H., Suzuki, H., Tamura, H., Tada, M., Suzuki, T., Mizuguchi, H., & Yamaguchi, T. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.26082 · Cited by 14
“Two types of cells, early EPCs and late EPCs, have been reported as ex vivo expanded EPCs frombloodMNCs (Cheng et al., 2013;Hur et al., 2004; Mukai et al., 2008).”
BackgroundSelf-citation
Subtypes of endothelial progenitor cells affect healing of segmental bone defects differently
Giles, E., Godbout, C., Chi, W., Glick, M. A., Lin, T. W., Li, R., Schemitsch, E. H., & Nauth, A. (2017) · International Orthopaedics · doi:10.1007/s00264-017-3613-0 · Cited by 13
“For instance, other authors have noted that E-EPC cultures could not form tubule-like structures in vitro [22], while others [23] did observe tubulogenic activity, as we did.”
Result
Kinetic analyses of vasculogenesis inform mechanistic studies
Varberg, K. M., Winfree, S., Chu, C., Tu, W., Blue, E. K., Gohn, C. R., Dunn, K. W., & Haneline, L. S. (2017) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00367.2016 · Cited by 13
“Modeling vasculogenesis by seeding cells in extracellular matrix is a standard quantitative measurement to assess function in vitro (4, 27, 31), allowing for rapid analysis of cells to perform basic tasks of network or vessel formation (15, 17, 38).”
Background
Amyloid β Enhances Migration of Endothelial Progenitor Cells by Upregulating CX3CR1 in Response to Fractalkine, Which May Be Associated With Development of Choroidal Neovascularization
Wang, J., Ohno‐Matsui, K., Nakahama, K., Okamoto, A., Yoshida, T., Shimada, N., Mochizuki, M., & Morita, I. (2011) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.215517 · Cited by 12
Self-citation
Contribution of Rat Endothelial Progenitor Cells on Three-Dimensional Network Formation In Vitro
Koga, M., Sudo, R., Abe, Y., Yamamoto, K., Ando, J., Ikeda, M., & Tanishita, K. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0417 · Cited by 11
Beneficial Role of Vitamin D on Endothelial Progenitor Cells (EPCs) in Cardiovascular Diseases
Sen, A., Vincent, V., Thakkar, H., Abraham, R. A., & Ramakrishnan, L. (2022) · Journal of Lipid and Atherosclerosis · doi:10.12997/jla.2022.11.3.229 · Cited by 11
Identification of novel diabetes impaired miRNA-transcription factor co-regulatory networks in bone marrow-derived Lin-/VEGF-R2+ endothelial progenitor cells
Irhimeh, M. R., Hamed, M., Barthelmes, D., Gladbach, Y. S., Helms, V., Shen, W., & Gillies, M. C. (2018) · PLoS ONE · doi:10.1371/journal.pone.0200194 · Cited by 11
“These Lin/VEGF-R2 EPCs play an important role in regenerating the endothelium through migration, proliferation, differentiation and by secreting pro-angiogenic cytokines [9].”
Background
The secretome of liver X receptor agonist-treated early outgrowth cells decreases atherosclerosis in Ldlr −/− mice
Rasheed, A., Shawky, S. A., Tsai, R., Jung, R. G., Simard, T., Saikali, M. F., Hibbert, B. M., Rayner, K. J., & Cummins, C. L. (2020) · Stem Cells Translational Medicine · doi:10.1002/sctm.19-0390 · Cited by 9
“EOCs participate in endothelial repair through the secretion of factors, whereas late outgrowth cells differentiate to endothelial-like cells and promote vascular homeostasis through direct incorporation.(24-27)”
Background
Formação in vitro de túbulos capilares a partir de células de sangue de cordão umbilical humano com perspectivas para aplicação terapêutica
Senegaglia, A. C., Brofman, P. R. S., Aita, C. A. M., Dallagiovanna, B., Rebelatto, C. L. K., Suss, P. H., Barchiki, F., & Krieger, M. A. (2008) · Brazilian Journal of Cardiovascular Surgery · doi:10.1590/s0102-76382008000400003 · Cited by 11
“[23] confirmed the findings of this study, showing that cultivated EPCs could form blood vessels, unlike from EPCs without cultivation, which would promote angiogenesis through the migration and proliferation of mature ECs, suggesting that these two cell populations would have a different role in in vivo neovasculariz…”
Expanded CD133+ Cells from Human Umbilical Cord Blood Improved Heart Function in Rats after Severe Myocardial Infarction
Correa, A., Ottoboni, G. S., Senegaglia, A. C., Capriglione, L. G. A., Miyague, N. I., Leite, L. M. B., Jamur, V. R., Rebelatto, C. L. K., Olandoski, M., & Brofman, P. R. S. (2018) · Stem Cells International · doi:10.1155/2018/5412478 · Cited by 10
Transient Extremity Ischemia Augments CD34+ Progenitor Cell Availability
Czeiger, D., Dukhno, O., Douvdevani, A., Porat, Y. B.-A., Shimoni, D., Fulga, V., Ament, J. D., & Shaked, G. (2011) · Stem Cell Reviews and Reports · doi:10.1007/s12015-011-9234-x · Cited by 10
“Early EPCs have been shown to have poor tube forming capacity compared to late EPCs [18].”
ResultInfluential
Endothelial Stem and Progenitor Cells for Regenerative Medicine
Banno, K., & Yöder, M. C. (2019) · Current Stem Cell Reports · doi:10.1007/s40778-019-00160-3 · Cited by 10
Isolation and characterization of peripheral blood-derived endothelial progenitor cells from broiler chickens
Bi, S., Tan, X., Ali, S. Q., & Wei, L.-J. (2014) · The Veterinary Journal · doi:10.1016/j.tvjl.2014.08.017 · Cited by 10
Clinical implication of endothelial progenitor cells
Foresta, C., Toni, L. D., Ferlin, A., & Mambro, A. D. (2009) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.09.80 · Cited by 10
Identification of Functional Progenitor Cells in the Pulmonary Vasculature
Firth, A. L., & Yuan, J. X. ‐. (2012) · Pulmonary Circulation · doi:10.4103/2045-8932.94841 · Cited by 9

Authors: Mukai, N., Akahori, T., Komaki, M., Li, Q., Kanayasu-Toyoda, T., Ishii-Watabe, A., Kobayashi, A., Yamaguchi, T., Abe, M., Amagasa, T., & Morita, I.
Affiliations: Tokyo Medical and Dental University (JP)
National Institute of Health Sciences (JP)
Corresponding author: Morita, Ikuo
ORCID: Komaki, Motohiro
Li, Qin
Kobayashi, Akiko
Yamaguchi, Teruhide
Venue: Experimental Cell Research
Publisher: Elsevier BV
Published: 2008-02
Volume: 314
Issue: 3
Pages: 430-440
ISSN: 0014-4827 (ISSN-L)
DOI: 10.1016/j.yexcr.2007.11.016
OpenAlex: W2084413357
Cited by: 157
References: 37
Citations by year: 2026: 1 · 2025: 4 · 2024: 1 · 2023: 4 · 2022: 6 · 2021: 10 · 2020: 8 · 2019: 3 · 2018: 8 · 2017: 11 · 2016: 8 · 2015: 8 · 2014: 15 · 2013: 9 · 2012: 16
FWCI: 4.37
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Experimental Cell Research (publishedVersion)
PubMed (publishedVersion)
Funders: Japan Society for the Promotion of Science (KH31031)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
Keywords: endothelial progenitor cells, tube formation, angiogenesis, endothelial cell migration, sprouting angiogenesis, umbilical cord blood, peripheral blood, human umbilical vein endothelial cells, cell therapy
MeSH terms: Age Factors, Biological Assay, Cell Differentiation, Cells, Cultured, Collagen, Drug Combinations, Fluorescent Dyes, Humans, Infant, Newborn, Laminin, Microscopy, Electron, Organoids, Photochemistry, Proteoglycans, Stem Cells, Time Factors, Titanium, Neovascularization, Physiologic, Cell Culture Techniques, Tissue Engineering, Organogenesis, Endothelial Cells

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A comparison of the tube forming potentials of early and late endothelial progenitor cells

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