Cited by 763Angiogenesis and VEGF in CancerCell Adhesion Molecules ResearchCellular Mechanics and Interactions

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In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract

Arnaoutova, Irina, Kleinman, Hynda K·2010·Nature Protocols

DOI 10.1038/nprot.2010.6

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Abstract

A protocol is presented here for a rapid, quantitative and reliable in vitro angiogenesis assay that can be adapted for high throughput use. Endothelial cells are plated on a gelled basement matrix, their natural substrate, and form capillary-like structures with a lumen. The assay can be used to identify inhibitors or stimulators of angiogenesis, as well as genes and signaling pathways involved in angiogenesis. It has also been used to identify endothelial progenitor cells. This assay involves endothelial cell adhesion, migration, protease activity and tubule formation. This tube formation assay is preferred, as other in vitro assays for angiogenesis, such as cell adhesion, migration and invasion, measure limited steps in the angiogenesis process. The tube formation assay on basement membrane can be completed in a day because transformed endothelial cells form tubes within 3 h, whereas non-transformed endothelial cells form tubes within 6 h.

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Botulinum Toxin A: Dose-dependent Effect on Reepithelialization and Angiogenesis
Gugerell, A., Kober, J., Schmid, M., Buchberger, E., Kamolz, L., & Keck, M. K. (2016) · Plastic & Reconstructive Surgery Global Open · doi:10.1097/gox.0000000000000852 · Cited by 29
Stimulation of vascularization of a subcutaneous scaffold applicable for pancreatic islet‐transplantation enhances immediate post‐transplant islet graft function but not long‐term normoglycemia
Smink, A. M., Li, S., Swart, D. H., Hertsig, D. T., de Haan, B. J., Kamps, J. A. A. M., Schwab, L. W., van Apeldoorn, A. A., de Koning, E. J. P., Faas, M. M., et al. (2017) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.36101 · Cited by 29
“In general, the tube formation assay is considered to be a quick and quantifiable way of measuring angiogenesis in vitro.(48,49) It is a useful method to determine growth factors that potentially play a role in vivo vascularization.”
Method
Targeting eIF4E inhibits growth, survival and angiogenesis in retinoblastoma and enhances efficacy of chemotherapy
Wang, G., Li, Z., Li, Z., Huang, Y., Mao, X., Xu, C., & Cui, S. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.10.034 · Cited by 29
Paneth cells promote angiogenesis and regulate portal hypertension in response to microbial signals
Hassan, M., Moghadamrad, S., Sorribas, M., Guixé‐Muntet, S., Kellmann, P., Trentesaux, C., Fraudeau, M., Nanni, P., Wolski, W., Keller, I., et al. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.03.019 · Cited by 30
Intravitreal injectable hydrogel rods with long-acting bevacizumab delivery to the retina
Lee, S., Hong, H. K., Song, J. S., Jeong, S. I., Chung, J., Woo, S. J., & Park, K. D. (2023) · Acta Biomaterialia · doi:10.1016/j.actbio.2023.09.025 · Cited by 28
Aminoacyl-tRNA synthetase dependent angiogenesis revealed by a bioengineered macrolide inhibitor
Mirando, A. C., Fang, P., Williams, T. F., Baldor, L. C., Howe, A. K., Ebert, A. M., Wilkinson, B. M., Lounsbury, K. M., Guo, M., & Francklyn, C. S. (2015) · Scientific Reports · doi:10.1038/srep13160 · Cited by 28
In vivo self-assembly and delivery of VEGFR2 siRNA-encapsulated small extracellular vesicles for lung metastatic osteosarcoma therapy
Yu, L., Fan, G., Wang, Q., Zhu, Y., Zhu, H., Chang, J., Wang, Z., Zhan, S., Hua, X., She, D., et al. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-06159-3 · Cited by 28
“Tube formation assay An in vitro tube formation assay was performed as previously described [41].”
Method
Valve Interstitial Cells Act in a Pericyte Manner Promoting Angiogensis and Invasion by Valve Endothelial Cells
Arevalos, C. A., Berg, J. M., Nguyen, J. M. V., Godfrey, E. L., Iriondo, C., & Grande-Allen, K. J. (2016) · Annals of Biomedical Engineering · doi:10.1007/s10439-016-1567-9 · Cited by 28
Mast Cells Interact with Endothelial Cells to Accelerate In Vitro Angiogenesis
de Souza, D. A., Mazucato, V. M., Santana, A., Oliver, C., & Jamur, M. C. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18122674 · Cited by 28
“During in vitro angiogenesis [41,42], when mast cells were co-cultured with endothelial cells, an association between mast cells and endothelial cells was observed.”
Background
The Neurotrophic Receptor Ntrk2 Directs Lymphoid Tissue Neovascularization during Leishmania donovani Infection
Dalton, J. E., Glover, A. C., Hoodless, L. J., Lim, E., Beattie, L., Kirby, A. C., & Kaye, P. M. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004681 · Cited by 27
“Angiogenesis assays were carried out as described previously [54].”
Method
Modulation of Lumen Formation by Microgeometrical Bioactive Cues and Migration Mode of Actin Machinery
Lei, Y., Zouani, O. F., Rami, L., Chanseau, C., & Durrieu, M. (2012) · Small · doi:10.1002/smll.201202410 · Cited by 27
A Quininib Analogue and Cysteinyl Leukotriene Receptor Antagonist Inhibits Vascular Endothelial Growth Factor (VEGF)-independent Angiogenesis and Exerts an Additive Antiangiogenic Response with Bevacizumab
Butler, C. T., Reynolds, A., Tosetto, M., Dillon, E., Guiry, P. J., Cagney, G., O'Sullivan, J. N., & Kennedy, B. N. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.747766 · Cited by 27
“stage processes of in vivo angiogenesis such as endothelial cell adhesion, migration, protease activity, and tubule formation (45) and can be significantly enhanced using the native ligand VEGF-A165 (42, 43, 46).”
Background
Activation of CD137 Signaling Promotes Angiogenesis in Atherosclerosis via Modulating Endothelial Smad1/5‐NFATc1 Pathway
Weng, J., Wang, C., Zhong, W. H., Li, B., Wang, Z., Shao, C., Chen, Y., & Yan, J. (2017) · Journal of the American Heart Association · doi:10.1161/jaha.116.004756 · Cited by 27
“Matrigel HUVEC Tube Formation Assay Tube formation assay was performed as described.(16) HUVECs were grown on growth factor-reduced Matrigel (Trevigen).”
Method
Retracted
The Antiangiogenic Activity of Naturally Occurring and Synthetic Homoisoflavonoids from the Hyacinthaceae (sensu APGII)
Schwikkard, S., Whitmore, H. A. B., Sishtla, K. L., Sulaiman, R. S., Shetty, T., Basavarajappa, H. D., Waller, C., Alqahtani, A. M., Frankemoelle, L., Chapman, A. M., et al. (2019) · Journal of Natural Products · doi:10.1021/acs.jnatprod.8b00989 · Cited by 27
RA Fibroblast-Like Synoviocytes Derived Extracellular Vesicles Promote Angiogenesis by miRNA-1972 Targeting p53/mTOR Signaling in Vascular Endotheliocyte
Chen, Y., Dang, J., Lin, X., Wang, M., Liu, Y., Chen, J., Chen, Y., Luo, X., Hu, Z., Weng, W., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.793855 · Cited by 27
“Tubule Formation Assay To explore the angiogenesis capacity of EVs, tubule formation assay was employed as previously reported (53).”
Method
Angiogenic Activity and Mechanism for Bisphenols on Endothelial Cell and Mouse: Evidence of a Structural-Selective Effect
Lu, L., Shen, L., Cui, S., Huang, Y., Gao, Y., Zhu, X., Lu, S., Zhang, C., & Zhuang, S. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c03883 · Cited by 27
Dermatopontin augments angiogenesis and modulates the expression of transforming growth factor beta 1 and integrin alpha 3 beta 1 in endothelial cells
Krishnaswamy, V. R., Balaguru, U. M., Chatterjee, S., & Korrapati, P. S. (2017) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2017.02.007 · Cited by 27
SNX9 determines the surface levels of integrin β1 in vascular endothelial cells: Implication in poor prognosis of human colorectal cancers overexpressing SNX9
Tanigawa, K., Maekawa, M., Kiyoi, T., Nakayama, J., Kitazawa, R., Kitazawa, S., Semba, K., Taguchi, T., Akita, S., Yoshida, M., et al. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28346 · Cited by 27
Vasohibin-1 suppresses colon cancer
Liu, S., Han, B., Zhang, Q., Dou, J., Wang, F., Lin, W., Sun, Y., & Peng, G. (2015) · Oncotarget · doi:10.18632/oncotarget.3493 · Cited by 27
“Angiogenesis activity mediated by VASH1 expression was analyzed based on the human umbilical vein endothelial cell (HUVEC) tube formation assay, as previously described [28].”
MethodInfluential
A versatileex vivotechnique for assaying tumor angiogenesis and microglia in the brain
Ghoochani, A., Yakubov, E., Sehm, T., Fan, Z., Hock, S. W., Buchfelder, M., Eyüpoglu, I. Y., & Savaskan, N. E. (2015) · Oncotarget · doi:10.18632/oncotarget.6550 · Cited by 27
“com/oncotarget angiogenesis independent of the particular conditions present in the brain microenvironment [20, 21].”
CCL8 mediates crosstalk between endothelial colony forming cells and triple-negative breast cancer cells through IL-8, aggravating invasion and tumorigenicity
Kim, E., Nam, S.-M., Song, H. K., Lee, S., Kim, K., Lim, H. K., Lee, H., Kang, K.-T., Kwon, Y., Chun, Y.-J., et al. (2021) · Oncogene · doi:10.1038/s41388-021-01758-w · Cited by 26
Alginate–Chitosan Hydrogel Formulations Sustain Baculovirus Delivery and VEGFA Expression Which Promotes Angiogenesis for Wound Dressing Applications
Schaly, S., Islam, P., Abosalha, A. K., Boyajian, J. L., Shum‐Tim, D., & Prakash, S. (2022) · Pharmaceuticals · doi:10.3390/ph15111382 · Cited by 26
“The wound-healing ability was evaluated using an open-access ImageJ plugin [24].”
Method
Improving cardiovascular outcomes in rheumatic diseases: Therapeutic potential of circulating endothelial progenitor cells
Reynolds, J. A., Robertson, A., Bruce, I. N., & Alexander, M. Y. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.12.008 · Cited by 25
Thrombospondin-1 Modulates the Angiogenic Phenotype of Human Cerebral Arteriovenous Malformation Endothelial Cells
Stapleton, C. J., Armstrong, D. L., Zidovetzki, R., Liu, C. Y., Giannotta, S. L., & Hofman, F. M. (2011) · Neurosurgery · doi:10.1227/neu.0b013e31820c0a68 · Cited by 26
“formation efficiency, the total number of completed tubelike structures was compared with the total number of tubule branches or sprouts.(31)”
Result
Endothelial Rictor is crucial for midgestational development and sustained and extensive FGF2-induced neovascularization in the adult
Aimi, F., Georgiopoulou, S., Kalus, I., Lehner, F., Hegglin, A., Limani, P., de Lima, V. G., Rüegg, M. A., Hall, M. N., Lindenblatt, N., et al. (2015) · Scientific Reports · doi:10.1038/srep17705 · Cited by 26
Glioblastoma microvesicles promote endothelial cell proliferation through Akt/beta-catenin pathway.
Liu, S., Sun, J., & Lan, Q. (2014) · Europe PMC (PubMed Central) · Cited by 26
Two-Cell Spheroid Angiogenesis Assay System Using Both Endothelial Colony Forming Cells and Mesenchymal Stem Cells
Shah, S., & Kang, K. (2018) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2018.134 · Cited by 26
“The one-cell angiogenesis assays commonly use human umbilical vein endothelial cells or human dermal microvascular endothelial cells because of their ready availability (Arnaoutova and Kleinman, 2010).”
Background
HOXB4 Promotes Hemogenic Endothelium Formation without Perturbing Endothelial Cell Development
Teichweyde, N., Kasperidus, L., Carotta, S., Kouskoff, V., Lacaud, G., Horn, P. A., Heinrichs, S., & Klump, H. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.01.009 · Cited by 25
“For this purpose, we evaluated the developmental fate of pooled colonies by subjecting those cells into an angiogenic tube formation assay inMatrigel (Arnaoutova and Kleinman, 2010).”
Method
Serotonin uptake is required for Rac1 activation in Kras‐induced acinar‐to‐ductal metaplasia in the pancreas
Saponara, E., Visentin, M., Baschieri, F., Seleznik, G. M., Martinelli, P., Esposito, I., Buschmann, J., Chen, R., Parrotta, R., Borgeaud, N., et al. (2018) · The Journal of Pathology · doi:10.1002/path.5147 · Cited by 25
“Tube formation assays with HUVECs were performed according to [18], and as detailed in supplementary material, Supplementary materials and methods.”
Method
A New Approach to Inhibiting Triple-Negative Breast Cancer: In Vitro, Ex Vivo and In Vivo Antiangiogenic Effect of BthTx-II, a PLA2-Asp-49 from Bothrops jararacussu Venom
Azevedo, F. V. P. D. V., Lopes, D. S., Zóia, M. A. P., Correia, L. I. V., Saito, N., Fonseca, B. B., Polloni, L., Teixeira, S. C., Goulart, L. R., & Rodrigues, V. D. M. (2022) · Biomolecules · doi:10.3390/biom12020258 · Cited by 25
“After 18 h, cells were photographed in an inverted optical microscope (Nikon Eclipse TS100) and the vessels enumerated [30].”
Method
GNAQ/GNA11 Mosaicism Causes Aberrant Calcium Signaling Susceptible to Targeted Therapeutics
Zecchin, D., Knöpfel, N., Gluck, A., Stevenson, M., Sauvadet, A., Polubothu, S., Barberan-Martin, S., Michailidis, F., Bryant, D., Inoue, A., et al. (2023) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2023.08.028 · Cited by 25
Identification of Early-Onset Preeclampsia-Related Genes and MicroRNAs by Bioinformatics Approaches
Song, J., Li, Y., & An, R. F. (2015) · Reproductive Sciences · doi:10.1177/1933719115570898 · Cited by 25
“Besides, multiple research have illustrated that adhesion and migration of endothelial cell which is connected to extracellular matrix at focal adhesions are necessary for angiogenesis.(35,36) Considering that impaired response to vasodilatory stimuli and defective placental angiogenesis(37) are the characteristics of…”
Background
Identification of vascular disruptor compounds by analysis in zebrafish embryos and mouse embryonic endothelial cells
McCollum, C. W., Conde‐Vancells, J., Hans, C., Vázquez–Chantada, M., Kleinstreuer, N., Tal, T. L., Knudsen, T. B., Shah, S. S., Merchant, F. A., Finnell, R. H., et al. (2016) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.11.005 · Cited by 27
“that form capillary-like structures (tubes) on a basement membrane matrix [28].”
Background
Granulin Secreted by the Food-Borne Liver Fluke Opisthorchis viverrini Promotes Angiogenesis in Human Endothelial Cells
Haugen, B., Karinshak, S. E., Mann, V. H., Popratiloff, A. S., Loukas, A. C., Brindley, P. J., & Smout, M. J. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00030 · Cited by 26
“Tubule Formation assay (TFa) Growth factor-reduced Matrigel (Corning, Corning, NY, USA) was plated into a 96-well μ-angiogenesis plate (ibidi, Planegg, Germany) at 10 μl/well, and incubated at 37°C in 5% CO2 in air for 60 min as described (14).”
BackgroundMethodInfluential
The role of pirfenidone in alkali burn rat cornea
Jiang, N., Ma, M., Li, Y., Su, T., Zhou, X., Ye, L., Yuan, Q., Zhu, P., Min, Y., Shi, W., et al. (2018) · International Immunopharmacology · doi:10.1016/j.intimp.2018.08.032 · Cited by 25
Notch signaling pathway is a potential therapeutic target for extracranial vascular malformations
Davis, R. B., Pahl, K. S., Datto, N. C., Smith, S. V., Shawber, C. J., Caron, K. M., & Blatt, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-36628-1 · Cited by 27
Intracellular availability of poorly soluble drugs from lipid nanocapsules
Bohley, M., Haunberger, A., & Göpferich, A. M. (2019) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2019.03.007 · Cited by 26
Inhibitory Effects of Pectic Polysaccharide Isolated from Diospyros kaki Leaves on Tumor Cell Angiogenesis via VEGF and MMP-9 Regulation
Park, J. Y., & Shin, M. (2020) · Polymers · doi:10.3390/polym13010064 · Cited by 25
“This process is thought to mimic the process by which endothelial cells form capillaries in vivo [24,25].”
Background
Histamine promotes angiogenesis through a histamine H1 receptor-PKC-VEGF-mediated pathway in human endothelial cells
Hatipoğlu, Ö. F., Nishinaka, T., Nishibori, M., Watanabe, M., Toyomura, T., Mori, S., Yaykaşlı, K. O., Wake, H., & Takahashi, H. K. (2023) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2023.02.006 · Cited by 24
Sodium Butyrate Inhibits Neovascularization Partially via TNXIP/VEGFR2 Pathway
Xiao, X., Chen, M., Xu, Y., Huang, S., Liang, J., Cao, Y., & Chen, H. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/6415671 · Cited by 24
“The capillary-like tube formation was performed on 3DMatrigel Matrix (BD Biosciences, 356230) according previous protocol [31].”
Method

Authors: Arnaoutova, I., & Kleinman, H. K.
Affiliations: Trevigen (US)
National Institutes of Health (US)
Corresponding author: Arnaoutova, Irina
Kleinman, Hynda K
ORCID: Kleinman, Hynda K
Venue: Nature Protocols
Publisher: Springer Science and Business Media LLC
Published: 2010-03-11
Volume: 5
Issue: 4
Pages: 628-635
ISSN: 1750-2799 (ISSN-L)
1754-2189
DOI: 10.1038/nprot.2010.6
OpenAlex: W2015186671
Cited by: 760
References: 35
Citations by year: 2026: 29 · 2025: 60 · 2024: 55 · 2023: 54 · 2022: 60 · 2021: 62 · 2020: 57 · 2019: 56 · 2018: 59 · 2017: 66 · 2016: 54 · 2015: 31 · 2014: 41 · 2013: 33 · 2012: 26
FWCI: 9.89
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Protocols (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Keywords: in vitro angiogenesis assay, endothelial tube formation, basement membrane extract, capillary-like structures, endothelial cell adhesion, endothelial cell migration, proteolytic activity, endothelial progenitor cells, angiogenesis inhibitors, high-throughput screening
MeSH terms: Basement Membrane, Capillaries, Cells, Cultured, Cytological Techniques, Gels, Humans, Neovascularization, Physiologic, Endothelial Cells, In Vitro Techniques

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In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract

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