Cited by 185Angiogenesis and VEGF in CancerDevelopmental Biology and Gene RegulationZebrafish Biomedical Research Applications

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Ets1 and Ets2 are required for endothelial cell survival during embryonic angiogenesis

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Wei, Guo, Srinivasan, Ruchika, Cantemir-Stone, Carmen Z., Sharma, Sudarshana M., Santhanam, Ramasamy, Weinstein, Michael, Muthusamy, Natarajan, Man, Albert K., Oshima, Robert G., Leone, Gustavo, Ostrowski, Michael C.·2009·Blood

DOI 10.1182/blood-2009-03-211391PMC PMC2721789

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Abstract

The ras/Raf/Mek/Erk pathway plays a central role in coordinating endothelial cell activities during angiogenesis. Transcription factors Ets1 and Ets2 are targets of ras/Erk signaling pathways that have been implicated in endothelial cell function in vitro, but their precise role in vascular formation and function in vivo remains ill-defined. In this work, mutation of both Ets1 and Ets2 resulted in embryonic lethality at midgestation, with striking defects in vascular branching having been observed. The action of these factors was endothelial cell autonomous as demonstrated using Cre/loxP technology. Analysis of Ets1/Ets2 target genes in isolated embryonic endothelial cells demonstrated down-regulation of Mmp9, Bcl-XL, and cIAP2 in double mutants versus controls, and chromatin immunoprecipitation revealed that both Ets1 and Ets2 were loaded at target promoters. Consistent with these observations, endothelial cell apoptosis was significantly increased both in vivo and in vitro when both Ets1 and Ets2 were mutated. These results establish essential and overlapping functions for Ets1 and Ets2 in coordinating endothelial cell functions with survival during embryonic angiogenesis.

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Background
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Background
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Background
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Influential
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Background
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BackgroundMethodInfluentialSelf-citation
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Background
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“[47] Wei G, Srinivasan R, Cantemir-Stone CZ, Sharma SM, Santhanam R, Weinstein M, et al.”
Background
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“However, expression of a number of transcription factors known to regulate Shh during limb development, including Hand1, Twist1, and Gli3, were not affected in the Etv4/5 null mesenchyme, suggesting the ETS-factor effect might be direct [10].”
BackgroundSelf-citation
Signaling Pathway of Taurine-Induced Upregulation of TXNIP
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Background
SOX9 acts as a dynamic pioneer factor inducing stable changes in the chromatin landscape to reprogram endothelial cellsPreprint
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Background
ETS1 Promotes Aerobic Glycolysis and Growth in Head and Neck Squamous Cell Carcinoma by Targeting RRAS2
Liu, J., Wang, Z., Tian, X., Xie, B., & Liu, K. (2024) · Biochemical Genetics · doi:10.1007/s10528-024-10996-y · Cited by 1
“Previous studies have found that genes in this family play important and complex roles in cell growth, differentiation, apoptosis, angiogenesis (Wei et al. 2009), inflammation (Battaglia et al. 2023), and tumorigenesis (Dittmer 2003).”
The phoenixin-14/GPR173 Axis enhances post-stroke angiogenesis through ETS1-mediated VEGF signaling
Luo, F., Xiaoyun, L. I., Wen, G., Zhu, Z., Junxi, L., & Weng, Y. (2026) · Neuropeptides · doi:10.1016/j.npep.2026.102594 · Cited by 1
A Co-opted Developmental Gene Regulatory Program in Endothelial Progenitors Promotes Tumor Angiogenic Phenotypes
Lee, A., Min, S., Park, S. C., Qiu, M., Bae, J. M., Jin, S. Y., Choi, B., Park, J., Kwon, S. H., Kang, G. H., et al. (2026) · Cancer Research · doi:10.1158/0008-5472.can-25-5094 · Cited by 1
Functional characterisation and pathological significance of variants of MEF2C promoter in tetralogy of Fallot
Wang, S. Q., Zheng, Z.-F., Chen, H., Yang, Q., & He, G. (2026) · Journal of Medical Genetics · doi:10.1136/jmg-2026-111657 · Cited by 1
“…enhancement with ETS1 during cardiac lineage specification and differentiation, jointly driving the expression programme of cardiac-specific genes 12 38–40 ; it forms functional complementarity with Gata3 in the development of cardiac outflow tracts and arterial valves, jointly ensuring the”
Insights into Roles of Immediate-Early Genes in Angiogenesis
Prado-Lourenço, L., Alhendi, A. M. N., & Khachigian, L. M. (2013) · Springer eBooks · doi:10.1007/978-3-7091-1428-5_7 · Cited by 1
The Role of the Transcription Factor Ets1 in Melanocyte Development
Tavares, A. S. (2014) · doi:10.25148/etd.fi14071121 · Cited by 1
Dysregulation of gene expression during gastrulation results in impaired primitive erythropoiesis and vascular development in Trim71-KO embryosPreprint
Beckröge, T., Jux, B., Seifert, H., Theobald, H., Domenico, E. D., Paulusch, S., Beyer, M., Schlitzer, A., Mass, E., & Kolanus, W. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.12.603214 · Cited by 1
Endothelial Transcriptional Networks in the Control of Angiogenesis: the ETS Factor
RANDI, A. M. (2013) · Springer eBooks · doi:10.1007/978-3-7091-1428-5_6
Expressions of transcription factors Ets1 and Ets2 in mouse testis tissue
Yang, L., Bo, J., Bin, G., Lihong, Z., Yushuai, H., Zhanpeng, Y., & Xueming, Z. (2011) · International Conference on Remote Sensing, Environment and Transportation Engineering · doi:10.1109/rsete.2011.5965935
The Role and Regulation of Etv2 in Zebrafish Vascular Development: A Dissertation
Moore, J. C. (2013) · The Journal of the American Medical Association (JAMA) Network (American Medical Association) · doi:10.13028/m21k56
“In addition to its expression in presumptive angioblasts, Ets2 is also expressed in the vasculature of the developing mouse [84] and in the differentiated endothelium of humans [8486].”
BackgroundInfluential
Increased Survival following Tumorigenesis in Ts65Dn Mice
Yang, A., & Reeves, R. H. (2011)
ETS1 AND ETS2 ROLE IN RAS ONCOGENIC TRANSFORMATION IN MOUSE EMBRYONIC FIBROBLASTS
Kabbout, M. (2010) · OhioLink ETD Center (Ohio Library and Information Network)
Latent Kaposi's Sarcoma Herpesvirus regulates host factors to induce Lymphangiogenesis and Angiogenesis
Gutierrez, K. D. (2013) · ResearchWorks at the University of Washington (University of Washington)
CPEB2 m 6 A Methylation Regulates BTB Permeability via Affecting Splicing Factor SRSF5 StabilityPreprint
Zhang, M., Yang, C., Liu, X., Ruan, X., Wang, D., Liu, Y., Cai, H., Zheng, J., Shao, L., Wang, P., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.17.387928
“ETS1 and ETS2 may affect tumor angiogenesis and metastasis in the tumor microenvironment, especially in endothelial cells [42].”
Background
Vascular Molecular Embryology
Vokes, S. A., & Krieg, P. A. (2014) · Springer eBooks · doi:10.1007/978-3-642-37393-0_2-1
Faculty Opinions recommendation of Pten in stromal fibroblasts suppresses mammary epithelial tumours.
Streuli, C. H. (2009) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1165735.628778
Ets-1
Salajegheh, A. (2016) · Springer eBooks · doi:10.1007/978-3-319-28140-7_16
Faculty Opinions recommendation of VEGF amplifies transcription through ETS1 acetylation to enable angiogenesis.
Sharrocks, A. D. (2017) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.730126894.793538840
Faculty Opinions recommendation of Pten in stromal fibroblasts suppresses mammary epithelial tumours.
Yamada, K. M. (2009) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1165735.628805
In vivo and in vitro models for research on Down syndrome
Ganguly, B. B. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-90456-8.00013-2 · Cited by 1
Regulation and Effect of Taurine on Metabolism
Miyazaki, T., Ito, T., Baseggio Conrado, A., & Murakami, S. (2023) · MDPI eBooks · doi:10.3390/books978-3-0365-6874-4
NNMT orchestrates the proangiogenic phenotype of cancer-associated fibroblasts via epigenetically regulating ETS2 in oral squamous cell carcinomaPreprint
Wang, X., Zhao, H., Luo, X., Chen, Y., Shi, C., Wang, Y., Bai, J., Shao, Z., & Shang, Z. (2023) · Research Square · doi:10.21203/rs.3.rs-3642085/v1
Multi-omic profiling identifies malignant subpopulations and a hypoxia-driven angiogenic axis as therapeutic vulnerabilities in sinonasal squamous cell carcinomaPreprint
You, C., Park, J., Jang, J. Y., Yu, M. S., Chung, Y., Kang, K., Park, J., Kim, J. H., & Kang, K. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.01.626270
Transcriptomics of the Anthopleura Sea Anemone Reveals Unique Adaptive Strategies to Shallow‐Water Hydrothermal Vent
Lin, M., Liu, L., & Chen, C. A. (2025) · Ecology and Evolution · doi:10.1002/ece3.71252
“ETS2 and ETS1, evolutionarily conserved across the metazoans (Degnan et al. 1993), are required for endothelial cell survival in mammals (Wei et al. 2009) and play roles in anti-infection processes in invertebrates (Ma et al. 2009).”
Placental Transcriptomic Analysis in Retinopathy of Prematurity Reactivation After Anti-VEGF Treatment
Kang, J., Kim, S., Bae, J. G., & Jang, J. H. (2025) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2025.07.023
Endothelial to mesenchymal transition, Ets2 and the aging heart
Hall, I. F., Kishta, F., & Kovacic, J. C. (2025) · Cardiovascular Research · doi:10.1093/cvr/cvaf273
Temporal Dynamics of Endothelium After Radiation Injury Reveal a Transient Pro-Angiogenic Capillary Subpopulation Associated with Skin Repair
Ren, X., Cai, Y., Gao, C., Qiu, Y., Wang, X., Song, H., Zhu, Y., Zhou, X., Li, J., Zhou, G., et al. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27062879
Découverte de la protéine kinase CDK10 / Cycline M et exploration de ses fonctions biologiques en lien avec le syndrome STAR
Guen, V. J. (2013) · doi:10.70675/3a53ffb3z69e5z4dcez8128z777ec6c8283c
Patient-specific iPSC-derived ECs identify QKI-7 as a key regulator of endothelial dysfunction and potential therapeutic target in diabetes
Cornelius, V. A., Fulton, J., Donaghy, C. L., McKeown, S., Naderi‐Meshkin, H., Zhang, S., Setyaningsih, W. A. W., Yacoub, A., Zampetaki, A., Stitt, A. W., et al. (2026) · Stem Cells Translational Medicine · doi:10.1093/stcltm/szag057
“20,45,46 Here, JUN knock-down reduced ETS1 and QKI-5 expression, key regulators of endothelial health, 21,45 suggesting JUN plays a critical role in diabetic EC dysfunction.”

Authors: Wei, G., Srinivasan, R., Cantemir-Stone, C. Z., Sharma, S. M., Santhanam, R., Weinstein, M., Muthusamy, N., Man, A. K., Oshima, R. G., Leone, G., & Ostrowski, M. C.
Affiliations: Department of Molecular and Cellular Biochemistry,
The Comprehensive Cancer Center,
The Ohio State University (US)
Sanford Burnham Prebys Medical Discovery Institute (US)
ORCID: Sharma, Sudarshana M.
Santhanam, Ramasamy
Muthusamy, Natarajan
Leone, Gustavo
Ostrowski, Michael C.
Venue: Blood
Publisher: American Society of Hematology
Published: 2009-07-30
Volume: 114
Issue: 5
Pages: 1123-1130
ISSN: 0006-4971 (ISSN-L)
1528-0020
DOI: 10.1182/blood-2009-03-211391
PMC: PMC2721789
OpenAlex: W2067611733
Cited by: 185
References: 46
Citations by year: 2026: 6 · 2025: 13 · 2024: 14 · 2023: 13 · 2022: 14 · 2021: 7 · 2020: 12 · 2019: 4 · 2018: 2 · 2017: 12 · 2016: 12 · 2015: 11 · 2014: 5 · 2013: 17 · 2012: 8
FWCI: 5.78
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Blood (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Ohio State University
National Cancer Institute (R01CA053271, P01CA097189, R01-CA53271)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
Keywords: ETS1, ETS2, endothelial cell survival, embryonic angiogenesis, endothelial cell apoptosis, vascular branching, MMP-9, Bcl-xL, cIAP2, Ras/ERK signaling
MeSH terms: Animals, Blood Vessels, Cell Survival, Chimera, Edema, Embryo Transfer, Fetal Death, Fetal Diseases, Genetic Vectors, Hemorrhage, Homozygote, Phenotype, Apoptosis, Mice, Knockout, Gene Expression Regulation, Developmental, Neovascularization, Physiologic, Endothelial Cells, Embryonic Development, Proto-Oncogene Protein c-ets-1, Proto-Oncogene Protein c-ets-2, Mice

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Ets1 and Ets2 are required for endothelial cell survival during embryonic angiogenesis

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