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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Histone Deacetylase Inhibitors Impair Vasculogenic Mimicry from Glioblastoma Cells
Pastorino, O., Gentile, M. T., Mancini, A., Gaudio, N. D., Costanzo, A. D., Bajetto, A., Franco, P., Altucci, L., Florio, T., Stoppelli, M. P., et al. (2019) · Cancers · doi:10.3390/cancers11060747 · Cited by 45
“Even if in vivo models could give more information on the angiogenesis processes, this assay has been widely used to study both normal and alternative angiogenesis, including vasculogenic mimicry [32,49,50] since it investigates at the same time cell proliferation, adhesion, migration and protease activity, all crucia…”
Method
Molecular hydrogen promotes wound healing by inducing early epidermal stem cell proliferation and extracellular matrix deposition
Zhao, P., Dang, Z., Liu, M., Guo, D., Luo, R., Adzavon, Y. M., Zhang, M., Xie, F., Zhang, X., 王友彬, et al. (2023) · Inflammation and Regeneration · doi:10.1186/s41232-023-00271-9 · Cited by 47
“In vitro tube formation assay Tube formation assay was performed as described [50].”
Method
The Retinoid Agonist Tazarotene Promotes Angiogenesis and Wound Healing
Zen, A. A. H., Nawrot, D. A., Howarth, A., Caporali, A., Ebner, D. V., Vernet, A., Schneider, J. E., & Bhattacharya, S. (2016) · Molecular Therapy · doi:10.1038/mt.2016.153 · Cited by 45
Direct writing alginate bioink inside pre-polymers of hydrogels to create patterned vascular networks
Wang, Y., Huang, X., Shen, Y., Hang, R., Zhang, X., Wang, Y., Yao, X., & Tang, B. H. (2019) · Journal of Materials Science · doi:10.1007/s10853-019-03447-2 · Cited by 47
CUDC‑907 reverses pathological phenotype of keloid fibroblasts in vitro and in vivo via dual inhibition of PI3K/Akt/mTOR signaling and HDAC2
Tu, T., Huang, J., Lin, M., Gao, Z., Wu, X., Zhang, W., Zhou, G., Wang, W., & Liu, W. (2019) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2019.4348 · Cited by 45
“After incubation at 37 ̊C for 16 h, images of newly formed capillary-like structures were observed via a phase‐contrast light microscope at x40 magnification and semi-quantitatively analyzed as previously described (23).”
Method
Novel pyrazolo[3,4-d]pyrimidines as potential anticancer agents: Synthesis, VEGFR-2 inhibition, and mechanisms of action
Ruzi, Z., Bozorov, K. A., Nie, L., Zhao, J., & Aisa, H. A. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113948 · Cited by 44
MMGZ01, an anti-DLL4 monoclonal antibody, promotes nonfunctional vessels and inhibits breast tumor growth
Xu, Z., Wang, Z., Jia, X., Wang, L., Chen, Z., Wang, S., Wang, M., Zhang, J., & Wu, M. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.12.025 · Cited by 44
The noni anthraquinone damnacanthal is a multi-kinase inhibitor with potent anti-angiogenic effects
Garcia‐Vilas, J. A., Pino‐Ángeles, A., Martı́nez-Poveda, B., Quesada, A. R., & Medina, M. Á. (2016) · Cancer Letters · doi:10.1016/j.canlet.2016.10.037 · Cited by 44
Lymphatic Endothelial Cells Produce M-CSF, Causing Massive Bone Loss in Mice
Wang, W., Wang, H., Zhou, X., Li, X., Sun, W. S., Dellinger, M. T., Boyce, B. F., & Xing, L. (2016) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3077 · Cited by 44
“The number of tubes/well were analyzed with ImageJ and Angioquant software according to a published protocol.((17))”
Method
A Novel “Inside‐Out” Intraocular Nanomedicine Delivery Mode for Nanomaterials’ Biological Effect Enhanced Choroidal Neovascularization Occlusion and Microenvironment Regulation
Jin, Y., Guo, Y., Yang, J., Chu, X., Huang, X., Wang, Q., Zeng, Y., Su, L., Lu, S. T., Wang, C., et al. (2022) · Advanced Materials · doi:10.1002/adma.202209690 · Cited by 43
Development of a Novel DNA Aptamer Ligand Targeting to Primary Cultured Tumor Endothelial Cells by a Cell-Based SELEX Method
Ara, M. N., Hyodo, M., Ohga, N., Hida, K., & Harashima, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050174 · Cited by 43
AAV-CRISPR/Cas9–Mediated Depletion of VEGFR2 Blocks Angiogenesis In Vitro
Wu, W., Duan, Y., Ma, G., Zhou, G., Park‐Windhol, C., D'Amore, P. A., & Lei, H. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.17-21902 · Cited by 43
VEGF-Encoding, Gene-Activated Collagen-Based Matrices Promote Blood Vessel Formation and Improved Wound Repair
Hwang, J., Kiick, K. L., & Sullivan, M. O. (2023) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.2c23022 · Cited by 43
The Effect of CXCL12 on Endothelial Progenitor Cells: Potential Target for Angiogenesis in Intracerebral Hemorrhage
Li, B., Bai, W., Sun, P., Zhou, B., Hu, B., & Ying, J. (2014) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2014.0004 · Cited by 42
“A Matrigel tube formation assay was performed to assess the ability of EPCs to integrate into a vascular structure as described (Arnaoutova and Kleinman 2010), A 48-well culture plate was coated with Matrigel plus 100 ng/mL VEGF.”
Antisense Oligonucleotides Targeting Y-Box Binding Protein-1 Inhibit Tumor Angiogenesis by Downregulating Bcl-xL-VEGFR2/-Tie Axes
Setoguchi, K., Cui, L., Hachisuka, N., Obchoei, S., Shinkai, K., Hyodo, F., Kato, K., Wada, F., Yamamoto, T., Harada‐Shiba, M., et al. (2017) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2017.09.004 · Cited by 42
“We next examined the effects of YB-1 ASO on angiogenesis by in vitro tube formation assay mimicking capillary-like structure formation of angiogenic endothelial cells in the critical process of angiogenesis in vivo.(19) Tube formation was significantly inhibited to approximately 20% and 10% of control levels in HUVECs…”
Increased myocardial stiffness activates cardiac microvascular endothelial cell via VEGF paracrine signaling in cardiac hypertrophy
Shen, J., Xie, Y., Liu, Z., Zhang, S., Wang, Y., Jia, L., Wang, Y., Cai, Z., Ma, H., & Xiang, M. (2018) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2018.08.014 · Cited by 47
Micro RNA ‐137 and micro RNA ‐195* inhibit vasculogenesis in brain arteriovenous malformations
HUANG, J. C., Song, J., Qu, M., Wang, Y., An, Q., Song, Y., Yan, W., Wang, B., Wang, X., Zhang, S., et al. (2017) · Annals of Neurology · doi:10.1002/ana.25015 · Cited by 42
“Tube Formation Assay Tube formation assays were carried out as previously described.(22) Briefly, 36 hours after transfection of miRNA mimics or inhibitors, cells were seeded on Matrigel (BD Biosciences) in a half-area 96-well plate.”
Method
Gelatin scaffold with multifunctional curcumin-loaded lipid-PLGA hybrid microparticles for regenerating corneal endothelium
Li, P., Chen, S.-C., Hsueh, Y., Shen, Y.-C., Tsai, M., Hsu, L.-W., Yeh, C., Chen, H., & Huang, C. (2020) · Materials Science and Engineering C · doi:10.1016/j.msec.2020.111753 · Cited by 42
Cdc42 functions as a regulatory node for tumour‐derived microvesicle biogenesis
Wang, J., Zhuang, X., Greene, K. S., Si, H., Antonyak, M. A., Druso, J. E., Wilson, K. F., Cerione, R. A., Feng, Q., & Wang, H. (2021) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12051 · Cited by 41
“…from the same number of MDAMB231 cell expressing empty vector, Cdc42F28L, or Cdc42F28L37A were isolated and examined for their ability to stimulate angiogenesis in vitro by the tubulogenesis assays as described above (Al-Nedawi et al., 2008, 2009; Arnaoutova & Kleinman, 2010; Feng et al., 2017).”
Proteomic Profiling of Exosomes From Hemorrhagic Moyamoya Disease and Dysfunction of Mitochondria in Endothelial Cells
Wang, X., Han, C., Jia, Y., Wang, J., Ge, W., & Duan, L. (2021) · Stroke · doi:10.1161/strokeaha.120.032297 · Cited by 43
BMP9-ID1 Signaling Activates HIF-1α and VEGFA Expression to Promote Tumor Angiogenesis in Hepatocellular Carcinoma
Chen, H., Nio, K., Tang, H., Yamashita, T., Okada, H., Li, Y.-Y., Doan, P. T. B., Li, R., Lv, J., Sakai, Y., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031475 · Cited by 42
“The lumen formation assay was assessed in 96-well plates coated with growth factorreduced Matrigel (BD Biosciences, Franklin Lakes, NJ, USA) as described previously [18].”
Method
Toluquinol, a marine fungus metabolite, is a new angiosuppresor that interferes the Akt pathway
García‐Caballero, M., Marí‐Beffa, M., Cañedo, L. M., Medina, M. Á., & Quesada, A. R. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.04.007 · Cited by 42
Injectable anti-cancer drug loaded silk-based hydrogel for the prevention of cancer recurrence and post-lumpectomy tissue regeneration aiding triple-negative breast cancer therapy
Jaiswal, C., Gupta, T., Jadi, P. K., Moses, J. C., & Mandal, B. B. (2022) · Biomaterials Advances · doi:10.1016/j.bioadv.2022.213224 · Cited by 41
MicroRNA-126-3p Inhibits Angiogenic Function of Human Lung Microvascular Endothelial Cells via LAT1 (L-Type Amino Acid Transporter 1)-Mediated mTOR (Mammalian Target of Rapamycin) Signaling
Cao, D., Mikosz, A. M., Ringsby, A. J., Anderson, K. C., Beatman, E. L., Koike, K., & Petrache, I. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.313800 · Cited by 41
Antitumor and Antiangiogenic Properties of Gold(III) Complexes Containing Cycloaurated Triphenylphosphine Sulfide Ligands
Reddy, T. S., Privér, S. H., Mirzadeh, N., Luwor, R. B., Reddy, V. G., Ramesan, S., & Bhargava, S. K. (2020) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.0c00423 · Cited by 41
Altered feto-placental vascularization, feto-placental malperfusion, and fetal growth restriction in mice with Egfl7 loss-of-function
Lacko, L. A., Hurtado, R., Hinds, S., Poulos, M. G., Butler, J. M., & Stuhlmann, H. (2017) · Development · doi:10.1242/dev.147025 · Cited by 40
“Finally, we assayed the ability of the placental ECs to form a capillary-like network using a cord formation assay (Kubota et al., 1988; Arnaoutova and Kleinman, 2010).”
Method
Self-Assembly of an Antiangiogenic Nanofibrous Peptide Hydrogel
Nguyen, P. K., Sarkar, B., Siddiqui, Z., McGowan, M., Iglesias-Montoro, P., Rachapudi, S. S., Kim, S., Gao, W., Lee, E. J., & Kumar, V. (2018) · ACS Applied Bio Materials · doi:10.1021/acsabm.8b00283 · Cited by 40
PERK-eIF2α-ERK1/2 axis drives mesenchymal-endothelial transition of cancer-associated fibroblasts in pancreatic cancer
Cai, W., Sun, X., Jin, F., Xiao, D., Li, H., Sun, H., Wang, Y., Lu, Y., Liu, J., Huang, C., et al. (2021) · Cancer Letters · doi:10.1016/j.canlet.2021.05.021 · Cited by 40
LHT7, a chemically modified heparin, inhibits multiple stages of angiogenesis by blocking VEGF, FGF2 and PDGF-B signaling pathways
Chung, S. W., Bae, S. M., Lee, M., Al-Hilal, T. A., Lee, C. K., Kim, J. K., Kim, I., Kim, S. Y., & Byun, Y. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.10.004 · Cited by 39
“tube formation assay as described previously [12].”
Biology and flow cytometry of proangiogenic hematopoietic progenitors cells
Rose, J. A., ERZURUM, S. C., & Asosingh, K. (2014) · Cytometry Part A · doi:10.1002/cyto.a.22596 · Cited by 41
“These assays include the in vitro tube formation assay (73), in vivo Matrigel plug assay (74), hindlimb ischemia mouse model (17,75), and tumor xenograft mouse model (15,76).”
Method
Combretastatin A-4 Conjugated Antiangiogenic Micellar Drug Delivery Systems Using Dendron–Polymer Conjugates
Bolu, B. S., Gecici, E. M., & Sanyal, R. (2016) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.5b00931 · Cited by 39
Therapeutic implication of ‘Iturin A’ for targeting MD-2/TLR4 complex to overcome angiogenesis and invasion
Dey, G., Bharti, R., Ojha, P. K., Pal, I., Rajesh, Y., Banerjee, I., Banik, P., Parida, S., Parekh, A., Sen, R., et al. (2017) · Cellular Signalling · doi:10.1016/j.cellsig.2017.03.017 · Cited by 40
Monoclonal Antibodies Directed against Cadherin RGD Exhibit Therapeutic Activity against Melanoma and Colorectal Cancer Metastasis
Bartolomé, R. A., Aizpurúa, C., Jaén, M., Torres, S., Calviño, E., Imbaud, J. I., & Casal, J. I. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-1444 · Cited by 39
“After 24-hour incubation, images of the wells were taken under a microscope with 10 phase contrast and tubules from five different wells were counted by two different observers (21).”
Method
Loss of Dnmt3b in Chondrocytes Leads to Delayed Endochondral Ossification and Fracture Repair
Wang, C., Abu‐Amer, Y., O’Keefe, R. J., & Shen, J. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3305 · Cited by 39
“The tube formation assays were performed as described,((28)) with modifications.”
Method
Inhibition of TGF-β Signaling in SHED Enhances Endothelial Differentiation
Xu, J., Gong, T., Wang, Y., Zou, T., Heng, B. C., Yang, Y., & Zhang, C. F. (2017) · Journal of Dental Research · doi:10.1177/0022034517733741 · Cited by 39
Vasculogenic and angiogenic potential of adipose stromal vascular fraction cell populations in vitro
Zakhari, J. S., Zabonick, J., Gettler, B. C., & Williams, S. K. (2017) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-017-0213-7 · Cited by 39
“…and angiogenesis have been aided by in vitro models that have utilized the ability to culture expand endothelial cells and establish conditions that support the development of endothelial tube-like structures in 2D culture (Madri and Williams 1983; Staton et al. 2009; Arnaoutova and Kleinman 2010).”
Background
Oxidized LDL, homocysteine, homocysteine thiolactone and advanced glycation end products act as pro-oxidant metabolites inducing cytokine release, macrophage infiltration and pro-angiogenic effect in ARPE-19 cells
Babu, K. A., Sen, P., & Angayarkanni, N. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216899 · Cited by 39
Regulatory effect of microRNA‐34a on osteogenesis and angiogenesis in glucocorticoid‐induced osteonecrosis of the femoral head
Zha, X., Sun, B., Zhang, R., Li, C., Yan, Z., & Chen, J. (2017) · Journal of Orthopaedic Research® · doi:10.1002/jor.23613 · Cited by 38
Enhanced TGF-β Signaling Contributes to the Insulin-Induced Angiogenic Responses of Endothelial Cells
Budi, E. H., Mamaï, O., Hoffman, S. C., Akhurst, R. J., & Derynck, R. (2019) · iScience · doi:10.1016/j.isci.2018.12.038 · Cited by 38
“In this assay, HUVECs, cultured on Matrigel, differentiate gradually with formation of cell adhesion junction complexes and form tube-like structures that connect to each other through node- and mesh-like structures (Arnaoutova and Kleinman, 2010; DeCicco-Skinner et al., 2014).”
Method
Enhanced survival of ischemic skin flap by combined treatment with bone marrow-derived stem cells and low-level light irradiation
Moon, J. H., Rhee, Y., Ahn, J., Kim, B., Lee, S. J., & Chung, P. (2017) · Lasers in Medical Science · doi:10.1007/s10103-017-2312-9 · Cited by 37
Impaired Fetoplacental Angiogenesis in Growth-Restricted Fetuses With Abnormal Umbilical Artery Doppler Velocimetry Is Mediated by Aryl Hydrocarbon Receptor Nuclear Translocator (ARNT)
Su, E. J., Xin, H., Yin, P., Dyson, M. T., Coon, J. S., Farrow, K. N., Mestan, K. K. L., & Ernst, L. M. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2385 · Cited by 37
Ionic silicon improves endothelial cells' survival under toxic oxidative stress by overexpressing angiogenic markers and antioxidant enzymes
do Monte, F. A., Cebe, T., Ripperger, D., Ighani, F., Kojouharov, H. V., Chen‐Charpentier, B. M., Kim, H. K. W., Aswath, P. B., & Varanasi, V. G. (2018) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2744 · Cited by 37
CD38 in cancer-associated fibroblasts promotes pro-tumoral activity
Baruch, B. B., Mantsur, E., Franco‐Barraza, J., Blacher, E., Cukierman, E., & Stein, R. (2020) · Laboratory Investigation · doi:10.1038/s41374-020-0458-8 · Cited by 37
Soluble Klotho, a biomarker and therapeutic strategy to reduce bronchopulmonary dysplasia and pulmonary hypertension in preterm infants
Batlahally, S., Franklin, A. D., Damianos, A., Huang, J., Chen, P., Sharma, M., Duara, J. L., Keerthy, D., Zambrano, R. A. P., Shehadeh, L. A., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-69296-1 · Cited by 37
sFRP2 Supersedes VEGF as an Age-related Driver of Angiogenesis in Melanoma, Affecting Response to Anti-VEGF Therapy in Older Patients
Fane, M. E., Ecker, B. L., Kaur, A., Marino, G. E., Alicea, G. M., Douglass, S. M., Chhabra, Y., Webster, M. R., Marshall, A., Colling, R. T., et al. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-0446 · Cited by 38
“Cells were thawed and allowed to grow for two passages before the assay was performed as described previously (24).”
Method
The transition of M-CSF–derived human macrophages to a growth-promoting phenotype
Hamidzadeh, K., Belew, A. T., El-Sayed, N. M., & Mosser, D. M. (2020) · Blood Advances · doi:10.1182/bloodadvances.2020002683 · Cited by 38

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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