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Ets1 and Ets2 are required for endothelial cell survival during embryonic angiogenesis
Open accessAbstract
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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“Genes possibly repressed by SOX9 include endothelial markers, such as VWF and PECAM1, as well as genes encoding TFs important for endothelial cell functions, including ERG (60) and ETS2 (61).”
From SOX9 reprograms endothelial cells by altering the chromatin landscape (2022) · cites this paper as [61]
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“F or p er so na l u se o nl y. H1 S1 S2 H2 H3 S3 S4 H4 H5HI-2HI-1 H0 H1 H2 H3 H4 H5H2' ETS domain ** ETS1, ETS2 GABPA, ETV6 ELK4 FLI1, SPI1, SPDEF, ELF3, ELF5, ELK1 ERG, FLI1, ETV6, Yan GABPA, SPDEF ETS1, ETS2, Pnt-P2 PNT domain SAM domain H1 S1 S2 H2 H3 S3 S4 H4 H5 HI-2 HI-1 H0 H1 H2 H3 H4 H5 H2' * * a b SRR N PNT C…”
InfluentialPten in stromal fibroblasts suppresses mammary epithelial tumours
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Self-citationThe ETS family of oncogenic transcription factors in solid tumours
Sizemore, G. M., Pitarresi, J. R., Balakrishnan, S., & Ostrowski, M. C. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2017.20 · Cited by 371
Self-citationReview of Ets1 structure, function, and roles in immunity
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The role of the transcription factor Ets1 in carcinoma
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The mitochondrial heme exporter FLVCR1b mediates erythroid differentiation
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“A similar phenotype of hemorrhages associated with reduced vasculature complexity was reported in another mouse model (29).”
Kabbout, M., Garcia, M. M., Fujimoto, J., Liu, D. D., Woods, D. M., Chow, C.-W. B., Mendoza, G., Momin, A. A., James, B. P., Solis, L. M., et al. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-0341 · Cited by 192
“During embryonic development, ETS2 was shown to insure proper development of the trophoblast (6) and to regulate endothelial cell survival during embryonic angiogenesis (7).”
BackgroundFGF-dependent regulation of VEGF receptor 2 expression in mice
Murakami, M., Nguyen, L. T., Hatanaka, K., Schachterle, W., Chen, P., Zhuang, Z. W., Black, B. L., & Simons, M. (2011) · Journal of Clinical Investigation · doi:10.1172/jci44762 · Cited by 187
Srinivasan, R., Zabuawala, T., Huang, H., Zhang, J., Gulati, P., Fernández, S., Karlo, J. C., Landreth, G. E., Leone, G. W., & Ostrowski, M. C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008283 · Cited by 183
Self-citationSingle-nucleus multiregion transcriptomic analysis of brain vasculature in Alzheimer’s disease
Sun, N., Akay, L. A., Murdock, M. H., Park, Y., Galiana-Melendez, F., Bubnys, A., Galani, K., Mathys, H., Jiang, X., Ng, A. P., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01334-3 · Cited by 186
Etv2/ER71 induces vascular mesoderm from Flk1+PDGFRα+ primitive mesoderm
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The molecular regulation of arteriovenous specification and maintenance
Fish, J. E., & Wythe, J. D. (2015) · Developmental Dynamics · doi:10.1002/dvdy.24252 · Cited by 161
“For example, deletion of both Ets1 and Ets2 results in vascular branching defects during mouse development, while deletion of the individual genes does not result in vascular defects (Wei et al., 2009).”
BackgroundEts-1 and Ets-2 Regulate the Expression of MicroRNA-126 in Endothelial Cells
Harris-Tryon, T. A., Yamakuchi, M., Kondo, M., Oettgen, P., & Lowenstein, C. J. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.211706 · Cited by 148
Shah, A. V., Birdsey, G. M., & RANDI, A. M. (2016) · Vascular Pharmacology · doi:10.1016/j.vph.2016.05.003 · Cited by 157
Transcriptional Regulation of Endothelial Cell and Vascular Development
Park, C., Kim, T., & Malik, A. B. (2013) · Circulation Research · doi:10.1161/circresaha.113.301078 · Cited by 145
Endothelial cell apoptosis in angiogenesis and vessel regression
Watson, E. L., Grant, Z. L., & Coultas, L. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2577-y · Cited by 146
“in vivo [132], and by Angiotensin-II in vitro [133].”
VEGF amplifies transcription through ETS1 acetylation to enable angiogenesis
Chen, J., Fu, Y., Day, D. S., Sun, Y., Wang, S., Liang, X., Gu, F., Zhang, F., Stevens, S. M., Zhou, P., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00405-x · Cited by 129
Richardson, P. G. G., Wolf, J., Jakubowiak, A. J., Zonder, J., Lonial, S., Irwin, D. H., Densmore, J. J., Krishnan, A. Y., Raje, N. S., Bar, M. H., et al. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2010.33.9788 · Cited by 121
ETS1 is a genome-wide effector of RAS/ERK signaling in epithelial cells
Plotnik, J. P., Budka, J. A., Ferris, M. W., & Hollenhorst, P. C. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku929 · Cited by 120
“ETS2 had a similar effect as ETS1 T38A/S41A, again pointing to a role for ETS2 in attenuating migration.”
BackgroundInfluentialAn Ets2 -Driven Transcriptional Program in Tumor-Associated Macrophages Promotes Tumor Metastasis
Zabuawala, T., Taffany, D. A., Sharma, S. M., Merchant, A. S., Adair, B., Srinivasan, R., Rosol, T. J., Fernández, S., Huang, K., Leone, G. W., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-1474 · Cited by 117
“The conditional Ets2 allele used for this study contained LoxP sites flanking exon3-exon5 so that Cre-mediated recombination of the region resulted in the generation of a null allele (19).”
Self-citationShah, F. H., Nam, Y. S., Bang, J. Y., Hwang, I. S., Kim, D. H., Ki, M., & Lee, H. (2025) · Archives of Pharmacal Research · doi:10.1007/s12272-025-01545-1 · Cited by 114
“2) The Raf-MEK-ERK cascade, along with PLCγ/PKC, activates the activity of different transcription factors (ETS (Wei et al. 2009), Elf-1, and NFAT), aiding in differentiation (Holmes et al. 2007; Koch et al. 2011; Koch and Claesson-Welsh 2012).”
Small G Proteins in the Cardiovascular System: Physiological and Pathological Aspects
Loirand, G., Sauzeau, V., & Pacaud, P. (2013) · Physiological Reviews · doi:10.1152/physrev.00021.2012 · Cited by 112
Transcription factor Ets-1 in cytokine and chemokine gene regulation
Russell, L., & Garrett‐Sinha, L. A. (2010) · Cytokine · doi:10.1016/j.cyto.2010.03.006 · Cited by 105
“Although Ets-1 knockout mice do not appear to have any significant defects in endothelial development or migration, mice that are deficient in Ets-1 and express a hypomorphic allele of the closely-related Ets family member Ets-2 demonstrate aberrant endothelial cell function during angiogenesis in embryonic developmen…”
BackgroundUnderstanding the Role of ETS-Mediated Gene Regulation in Complex Biological Processes
Findlay, V. J., LaRue, A. C., Turner, D. P., Watson, P. M., & Watson, D. K. (2013) · Advances in cancer research · doi:10.1016/b978-0-12-407190-2.00001-0 · Cited by 103
Regulation of endothelial cell development by ETS transcription factors
Meadows, S. M., Myers, C. T., & Krieg, P. A. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.09.009 · Cited by 93
Luo, Y., Jiang, N., May, H. I., Luo, X., Ferdous, A., Schiattarella, G. G., Chen, G., Li, Q., Li, C., Rothermel, B. A., et al. (2021) · Circulation · doi:10.1161/circulationaha.120.052384 · Cited by 85
“Floxed ETS2 mice were a generous gift from Dr. Michael C. Ostrowski (Department of Biochemistry and Molecular Biology, Medical University of South Carolina) 18 .”
The manipulation of miRNA-gene regulatory networks by KSHV induces endothelial cell motility
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“Luciferase assays were used to confirm the predicted interaction of miR-221 with the 3 UTR of ETS2. miR-221 repressed a construct containing the ETS2 3 UTR downstream of the luciferase gene (Figure 5H left panel).”
BackgroundInfluentialMEF2 transcription factors are key regulators of sprouting angiogenesisPreprint
Sacilotto, N., Chouliaras, K. M., Nikitenko, L. L., Lu, Y. W., Fritzsche, M., Wallace, M. D., Nornes, S., García‐Moreno, F., Payne, S., Bridges, E., et al. (2016) · Genes & Development · doi:10.1101/gad.290619.116 · Cited by 82
“While depletion of Dll4 levels can have a proangiogenic effect, loss or depletion of direct MEF2 targets ETS1, ELK3, and HLX can have anti-angiogenic effects in vivo (Pham et al. 2007; Wei et al. 2009; Herbert et al. 2012; Weinl et al. 2014).”
BackgroundRegulation of angiogenesis by ETS transcription factors
RANDI, A. M., Sperone, A., Dryden, N. H., & Birdsey, G. M. (2009) · Biochemical Society Transactions · doi:10.1042/bst0371248 · Cited by 79
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Patrick, R., Naval-Sánchez, M., Deshpande, N., Huang, Y., Zhang, J., Chen, X., Yang, Y., Tiwari, K., Esmaeili, M., Tran, M., et al. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.06.006 · Cited by 76
Gourlaouen, M., Welti, J. C., Vasudev, N. S., & Reynolds, A. R. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.446401 · Cited by 74
Injury-Mediated Vascular Regeneration Requires Endothelial ER71/ETV2
Park, C., Lee, T., Bhang, S. H., Liu, F., Nakamura, R. E. I., Oladipupo, S. S., Pitha, I., Capoccia, B. J., Choi, H. S., Kim, T., et al. (2015) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.115.306430 · Cited by 67
“Importantly, there is functional redundancy in these ETS factors in angiogenesis.(5,8,9) Distinct from these ETS factors, Etv2 (aka Er71, etsrp) is transiently expressed in the primitive streak, yolk sac blood islands, and large vessels, including the dorsal aorta during embryogenesis.”
BackgroundShi, X., Richard, J. J., Zirbes, K. M., Gong, W., Lin, G., Kyba, M., Thomson, J., Koyano‐Nakagawa, N., & Garry, D. J. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.02.018 · Cited by 65
“0 (Wei et al., 2009).”
ETS transcription factors in embryonic vascular development
Craig, M. P., & Sumanas, S. (2016) · Angiogenesis · doi:10.1007/s10456-016-9511-z · Cited by 66
“In PTEN-deficient stromal fibroblasts, Ets2 is upregulated, phosphorylated and recruited to the promoters of target genes known to be involved in ECM remodeling and angiogenesis [85].”
InfluentialItoh, T., Takeda, S., & Akao, Y. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.105080 · Cited by 65
ETS-dependent regulation of a distal Gata4 cardiac enhancer
Schachterle, W., Rojas, A., Xu, S.-M., & Black, B. L. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.10.023 · Cited by 64
“ETS1 and ERG each play important roles in endothelial gene regulation and function (Gao et al., 2010; Hashiya et al., 2004; Loughran et al., 2008; Nikolova-Krstevski et al., 2009; Pham et al., 2007; Taoudi et al., 2011; Wei et al., 2009; Ye et al., 2010), and ETS1 and ERG are expressed broadly throughout the endotheli…”
InfluentialThe ETS Factor, ETV2: a Master Regulator for Vascular Endothelial Cell Development
Oh, S.-Y., Kim, J. Y., & Park, C. (2015) · Molecules and Cells · doi:10.14348/molcells.2015.0331 · Cited by 66
“This fact suggests the redundant functions of the ETS factors for at least some members in vessel development (Craig et al., 2015; Pham et al., 2007; Wei et al., 2009).”
BackgroundANGPTL2 increases bone metastasis of breast cancer cells through enhancing CXCR4 signaling
Masuda, T., Endo, M., Yamamoto, Y., Odagiri, H., Kadomatsu, T., Nakamura, T., Tanoue, H., Ito, H., Yugami, M., Miyata, K., et al. (2015) · Scientific Reports · doi:10.1038/srep09170 · Cited by 64
Pourebrahim, R., Zhang, Y., Liu, B., Gao, R., Xiong, S., Lin, P. P., McArthur, M. J., Ostrowski, M. C., & Lozano, G. (2017) · Genes & Development · doi:10.1101/gad.304972.117 · Cited by 62
“Ets2 floxed mice (Ets2fl, FVB/N) has been described (Wei et al. 2009).”
BackgroundSelf-citationPossible cooption of a VEGF-driven tubulogenesis program for biomineralization in echinoderms
Morgulis, M., Gildor, T., Roopin, M., Sher, N., Malik, A., Lalzar, M., Dines, M., de-Leon, S. B.-T., Khalaily, L., & de‐Leon, S. B. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1902126116 · Cited by 61
“Multiple gene duplications have occurred in vertebrates leading to several paralogs of every sea urchin gene, for example, Ets1/2 duplication into Ets1 and Ets2, Erg duplication into Erg and Fli, and the multiple vertebrates’ paralogs of FoxO, VEGF and VEGFR (45–51).”
BackgroundInfluentialEts family members induce lymphangiogenesis through physical and functional interaction with Prox1
Yoshimatsu, Y., Yamazaki, T., Mihira, H., Itoh, T., Suehiro, J., Yuki, K., Harada, K., Morikawa, M., Iwata, C., Minami, T., et al. (2011) · Journal of Cell Science · doi:10.1242/jcs.083998 · Cited by 62
“In accordance with these in vitro findings, double-mutant mice for Ets-1 and Ets-2 exhibit defective blood vessel branching (Wei et al., 2009), whereas mice that were single-mutant for either Ets1 or Ets-2 exhibited no phenotypic changes in the vascular development of the embryo proper (Bories et al.”
BackgroundResultInfluentialZhou, P., Gu, F., Zhang, L., Akerberg, B. N., Ma, Q., Li, K., He, A., Lin, Z., Stevens, S. M., Zhou, B., et al. (2017) · eLife · doi:10.7554/elife.22039 · Cited by 57
“…hand, ETS-containing regions were highly enriched for functional terms linked to angiogenesis, also consistent with the key roles of ETS factors in angiogenesis ( Wei et al., 2009 ) and our prior finding that the ETS motif is enriched in dynamic VEGF-dependent EC enhancers ( Zhang et al., 2013 ).”
BackgroundSinh, N. D., Endo, K., Miyazawa, K., & Saitoh, M. (2017) · Cancer Science · doi:10.1111/cas.13214 · Cited by 59
Kato, T., Fujita, Y., Nakane, K., Kojima, T., 義則, 野., Deguchi, T., & Ito, M. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.12.047 · Cited by 53
Hdac3 regulates lymphovenous and lymphatic valve formation
Janardhan, H. P., Milstone, Z. J., Shin, M., Lawson, N. D., Keaney, J. F., & Trivedi, C. M. (2017) · Journal of Clinical Investigation · doi:10.1172/jci92852 · Cited by 52
Xie, L., Wang, X., Ma, Y., Ma, H., Shen, J., Chen, J., Wang, Y., Su, S., Chen, K., Xu, L., et al. (2023) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.122.318625 · Cited by 54
Kanki, Y., Nakaki, R., Shimamura, T., Matsunaga, T., Yamamizu, K., Katayama, S., Suehiro, J., Osawa, T., Aburatani, H., Kodama, T., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx159 · Cited by 49
“In addition to Etv2, it is generally accepted that transcription factors from the Ets family such as Ets1, Ets2, Fli1 and Erg are important for EC differentiation and maintenance (3,43,44).”
Cdk5 controls lymphatic vessel development and function by phosphorylation of Foxc2
Liebl, J., Zhang, S., Moser, M., Agalarov, Y., Demir, C. S., Hager, B., Bibb, J. A., Adams, R. H., Kiefer, F., Miura, N., et al. (2015) · Nature Communications · doi:10.1038/ncomms8274 · Cited by 50
ETS transcription factors and prostate cancer: The role of the family prototype ETS-1 (Review)
Wernert, N. (2012) · International Journal of Oncology · doi:10.3892/ijo.2012.1380 · Cited by 49
Genome‐scale study of transcription factor expression in the branching mouse lung
Herriges, J. C., Yi, L., Hines, E. A., Harvey, J. F., Xu, G., Gray, P. A., Ma, Q., & Sun, X. (2012) · Developmental Dynamics · doi:10.1002/dvdy.23823 · Cited by 46
“5 and display severe hemorrhaging due to a drastic decrease of embryonic vasculature (Wei et al., 2009).”
BackgroundRole of the COP1 protein in cancer development and therapy
Song, Y., Liu, Y., Pan, S., Xie, S., Wang, Z. P., & Zhu, X. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.02.001 · Cited by 47
Bian, C., Xu, T., Zhu, H., Pan, D., Liu, Y., Luo, Y., Wu, P., & Li, D. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144877 · Cited by 47
Feedback Mechanisms Regulate Ets Variant 2 (Etv2) Gene Expression and Hematoendothelial Lineages
Koyano‐Nakagawa, N., Shi, X., Rasmussen, T. L., Das, S., Walter, C. A., & Garry, D. J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.662197 · Cited by 44
“Although we have observed that both overexpressed Ets1 and Ets2 can transactivate the Etv2-luciferase reporter in the transcriptional assays (data not shown), the lack of early hematoendothelial lineage defects in Ets1 mutant mice (58 – 60) as well as the Ets1 and Ets2 double knockout embryos (61) support the notion t…”
BackgroundWalters, R., Vasilaki, E., Aman, J., Chen, C.-N., Wu, Y., Liang, O. D., Ashek, A., Dubois, O., Zhao, L., Sabrin, F., et al. (2023) · Circulation · doi:10.1161/circulationaha.122.061940 · Cited by 43
“YK-4279 specifically inhibits ERG transcription and ERG-mediated cell migration and proliferation in prostate cancer (42).”
BackgroundItoh, T., Andô, M., Tsukamasa, Y., & Akao, Y. (2012) · FEBS Letters · doi:10.1016/j.febslet.2012.04.014 · Cited by 41
“The Ets transcription factor family is closely involved in the regulation of cell differentiation [26], metastasis [17], apoptosis [27], and angiogenesis [28], and plays critical roles in osteogenesis [29].”
BackgroundWang, L., Lin, L., Qi, H., Chen, J., & Grossfeld, P. (2022) · Circulation Research · doi:10.1161/circresaha.121.319955 · Cited by 41
Ets2 in Tumor Fibroblasts Promotes Angiogenesis in Breast Cancer
Wallace, J. A., Li, F., Balakrishnan, S., Cantemir-Stone, C. Z., Pécot, T., Martin, C. K., Kladney, R. D., Sharma, S. M., Trimboli, A. J., Fernández, S., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071533 · Cited by 39
“Ets2 Deletion Specifically Effects Tumor Progression from the Fibroblast Compartment in Multiple Breast Cancer Models The ablation of a conditional Ets2 allele [27] was studied both in mammary stromal fibroblasts and in mammary tumor epithelial cells in the MMTV-PyMT (PyMT) mammary cancer model [28].”
BackgroundSelf-citationETS‐targeted therapy: can it substitute for MEK inhibitors?
Tetsu, O., & McCormick, F. P. (2017) · Clinical and Translational Medicine · doi:10.1186/s40169-017-0147-4 · Cited by 42
ETS Transcription Factor ETV2/ER71/Etsrp in Hematopoietic and Vascular Development
Sumanas, S., & Choi, K. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.01.005 · Cited by 39
Transcription factors regulating vasculogenesis and angiogenesis
Payne, S., Neal, A., & Val, S. D. (2023) · Developmental Dynamics · doi:10.1002/dvdy.575 · Cited by 48
“2,19,113 While it is possible that the uniquely early expression pattern of Etv2 contributes to the severe consequences of deletion, overexpression of Fli1 , Erg and Ets1 in ETV2-null embryoid body culture systems could not fully rescue the formation of the endothelial lineage.”
BackgroundInfluentialPitarresi, J. R., Liu, X., Sharma, S. M., Cuitiño, M. C., Kladney, R. D., Mace, T. A., Donohue, S., Nayak, S. G., Qu, C., Lee, J., et al. (2016) · Neoplasia · doi:10.1016/j.neo.2016.07.006 · Cited by 36
Self-citationHemanthakumar, K. A., Fang, S., Anisimov, A., Mäyränpää, M. I., Mervaala, E. M. A., & Kivelä, R. (2021) · eLife · doi:10.7554/elife.62678 · Cited by 39
SOX9 reprograms endothelial cells by altering the chromatin landscape
Fuglerud, B. M., Drissler, S., Lotto, J., Stephan, T. L., Thakur, A., Cullum, R., & Hoodless, P. A. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac652 · Cited by 35
“Genes possibly repressed by SOX9 include endothelial markers, such as VWF and PECAM1, as well as genes encoding TFs important for endothelial cell functions, including ERG (60) and ETS2 (61).”
BackgroundZanini, F., Che, X., Knutsen, C., Liu, M., Suresh, N. E., Domingo-Gonzalez, R., Dou, S. H., Zhang, D., Pryhuber, G., Jones, R. C., et al. (2022) · iScience · doi:10.1016/j.isci.2023.106097 · Cited by 38
Nagarajan, P., Chin, S. S., Wang, D., Liu, S., Sinha, S., & Garrett‐Sinha, L. A. (2010) · Journal of Cell Science · doi:10.1242/jcs.062240 · Cited by 38
“Other laboratories have demonstrated that Ets1 also directly regulates the Mmp3 and Mmp9 genes (Baillat et al., 2006; Wei et al., 2009).”
BackgroundSingle-Cell View of Tumor Microenvironment Gradients in Pleural Mesothelioma
Giotti, B., Dolasia, K., Zhao, W., Cai, P., Sweeney, R. E., Merritt, E., Kiner, E., Kim, G. S., Bhagwat, A., Nguyen, T., et al. (2024) · Cancer Discovery · doi:10.1158/2159-8290.cd-23-0017 · Cited by 34
A yeast one‐hybrid and microfluidics‐based pipeline to map mammalian gene regulatory networks
Gubelmann, C., Waszak, S. M., Isakova, A., Holcombe, W., Hens, K., Hafner, A., Feuz, J., Raghav, S. K., Simicevic, J., & Deplancke, B. (2013) · Molecular Systems Biology · doi:10.1038/msb.2013.38 · Cited by 33
John, S. A., Russell, L., Chin, S. S., Luo, W., Oshima, R. G., & Garrett‐Sinha, L. A. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00612-13 · Cited by 33
“Indeed, there is evidence of functional redundancy between these two factors in regulating vascular development (41).”
BackgroundSelf-citationMultiple Myeloma Treatment Strategies with Novel Agents in 2011: A European Perspective
Ludwig, H., Beksaç, M., Bladé, J., Cavenagh, J. D., Cavo, M., Delforge, M., Dimopoulos, M. A., Drach, J. W., Einsele, H., Facon, T. T. F., et al. (2011) · The Oncologist · doi:10.1634/theoncologist.2010-0386 · Cited by 33
Liao, Z., Yu, J. H., Chu, Y., Wu, H., Li, X., Deng, Z., Feng, S., Chen, N., Luo, Z., Zheng, X., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03271-6 · Cited by 32
Increased Survival following Tumorigenesis in Ts65Dn Mice That Model Down Syndrome
Yang, A., & Reeves, R. H. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-4489 · Cited by 32
“NPcis and Ets2þ/ mice were genotyped by PCR as described (15, 16).”
The Evolution of Biomineralization through the Co-Option of Organic Scaffold Forming Networks
de‐Leon, S. B. (2022) · Cells · doi:10.3390/cells11040595 · Cited by 34
Post-transcriptional mechanisms contribute to Etv2 repression during vascular development
Moore, J. C., Sheppard-Tindell, S., Shestopalov, I. A., Yamazoe, S., Chen, J., & Lawson, N. D. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.08.028 · Cited by 31
Complex contributions of Ets2 to craniofacial and thymus phenotypes of trisomic “Down syndrome” mice
Hill, C. A., Sussan, T. E., Reeves, R. H., & Richtsmeier, J. T. (2009) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.33012 · Cited by 32
“Ts65Dn mice carrying a null allele of Ets2 (herein Ts65Dn, Ets2þ/ mice, [Wei et al., 2009]) were backcrossed for six or more generations onto C57BL/6J (B6) before being used in these experiments.”
MethodZhang, M., Yang, C., Liu, X., Ruan, X., Wang, D., Liu, L., Cai, H., Zheng, J., Shao, L., Wang, P., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03878-9 · Cited by 31
The Role of Ets Factors in Tumor Angiogenesis
Oettgen, P. (2010) · Journal of Oncology · doi:10.1155/2010/767384 · Cited by 29
“When both Ets-1 and Ets-2 were simultaneously targeted, this led to striking defects in vascular development [18].”
BackgroundLong-range enhancers modulate Foxf1 transcription in blood vessels of pulmonary vascular network
Seo, H.-J., Kim, J., Park, G.-H., Kim, Y., & Cho, S. W. (2016) · Histochemistry and Cell Biology · doi:10.1007/s00418-016-1445-4 · Cited by 28
Bras, A. L., Samson, C., Trentini, M., Caëtano, B., Lelièvre, E., Mattot, V., Beermann, F., & Soncin, F. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012156 · Cited by 27
“On the other hand, a gene co-inactivation approach recently showed that Ets-1 and Ets-2 are together involved in vessel branching and endothelial survival [61].”
BackgroundUchiumi, F., Miyazaki, S., & Tanuma, S.-I. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0674-x · Cited by 27
“Expression of antiapoptotic genes, including Bcl-XL and cIAP, is regulated by Ets1 and Ets2 during embryonic development [101].”
BackgroundChetty, S. C., & Sumanas, S. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.06.007 · Cited by 27
“[PubMed: 20086248] Wei G, Srinivasan R, Cantemir-Stone CZ, Sharma SM, Santhanam R, Weinstein M, Muthusamy N, Man AK, Oshima RG, Leone G, Ostrowski MC, 2009 Ets1 and Ets2 are required for endothelial cell survival during embryonic angiogenesis.”
BackgroundResultInfluentialRole of Hmbox1 in Endothelial Differentiation of Bone-Marrow Stromal Cells by a Small Molecule
Su, L., Zhao, H., Sun, C., Zhao, B., Zhao, J., Zhang, S., Su, H., & Miao, J. (2010) · ACS Chemical Biology · doi:10.1021/cb100153r · Cited by 28
Gill, J. G., Langer, E. M., Lindsley, R. C., Cai, M., Murphy, T. L., & MURPHY, K. M. M. (2011) · Stem Cells and Development · doi:10.1089/scd.2011.0194 · Cited by 26
“These genes are also known to be important in vasculogenesis [26,27].”
Yang, L., Zhu, Y., Kong, D., Gong, J., Yu, W. L., Liang, Y., Nie, Y., & Teng, C. (2019) · International Journal of Biological Sciences · doi:10.7150/ijbs.34985 · Cited by 24
“ETS2 is a member of the ETS (E26 transformation-specific sequence) family of transcription factors that participates in cellular proliferation, differentiation and apoptosis, thus playing important roles in embryo development [50-53], senescence [54], vasculogenesis [55], immunity [56-59], osteogenesis [60], adipogene…”
BackgroundIchise, T., Yoshida, N., & Ichise, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051639 · Cited by 24
“demonstrated that genetically engineered mice lacking both Ets1 and Ets2 die at mid-gestation and exhibit defects in vascular branching of blood vessels and impaired blood endothelial cell (BEC) survival [38].”
BackgroundPlotnik, J. P., & Hollenhorst, P. C. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx039 · Cited by 24
“Genetic and biochemical studies demonstrate many functional redundancies between ETS1 and ETS2 during early development, cell survival, cell proliferation and oncogenesis (12,13).”
BackgroundLiu, Y., Xu, J., Gu, R., Zhu, L., Wang, K., Qi, Y., Sun, X., Xie, J., Wang, L. Y., Xu, B., et al. (2020) · Aging · doi:10.18632/aging.103651 · Cited by 23
“Ets1, as a transcription factor of MMP9 [20], was required for endothelial cell survival during angiogenesis [21].”
BackgroundMicroRNA 17-92 Cluster Mediates ETS1 and ETS2-Dependent RAS-Oncogenic Transformation
Kabbout, M., Dakhlallah, D. A., Sharma, S. M., Bronisz, A., Srinivasan, R., Piper, M. G., Marsh, C. B., & Ostrowski, M. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100693 · Cited by 22
Self-citationBreccia, M., & Alimena, G. (2011) · BioDrugs · doi:10.2165/11591840-000000000-00000 · Cited by 22
Etv2 regulates enhancer chromatin status to initiate Shh expression in the limb bud
Koyano‐Nakagawa, N., Gong, W., Das, S., Theisen, J. W. M., Swanholm, T. B., Ly, D., Dsouza, N., Singh, B. N., Kawakami, H., Young, S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31848-6 · Cited by 21
“Genomic DNA fragments corresponding to regions i (1-656), ii (657-1401), and iii (1402-1682) of ZRS were amplified from pGL4-TATA-ZRS23 by PCR (see Supplementary Table 3 for primer sequences) and subcloned into the KpnI-BamHI fragment including the vector backbone of pGL4-TATA-ZRS23.”
MethodETV2/ER71 Transcription Factor as a Therapeutic Vehicle for Cardiovascular Disease
Lee, D. H., Kim, T. M., Kim, J. K., & Park, C. (2019) · Theranostics · doi:10.7150/thno.35300 · Cited by 20
“For example, Ets1 deficiency in mice is compatible with the normal vascular development, but compound knockout of Ets1 and Ets2 leads to defects in vessel formation [13, 14].”
BackgroundEndothelialErgexpression is required for embryogenesis and vascular integrity
Han, R., Pacifici, M., Iwamoto, M., & Trojanowska, M. E. (2015) · Organogenesis · doi:10.1080/15476278.2015.1031435 · Cited by 20
“5.(28) Whether Erg/Fli1 double null mutants would have an even more severe defect in angiogenesis/vasculogenesis than single null mutants shown here and previously awaits further investigation.”
BackgroundThe Use of Mouse Models for Understanding the Biology of Down Syndrome and Aging
Vacano, G. N., Duval, N., & Patterson, D. W. (2012) · Current Gerontology and Geriatrics Research · doi:10.1155/2012/717315 · Cited by 26
“[152] employed the Ets2A72 allele to produce an Ets1/Ets2 double “null” to investigate the role of both genes in the ras/Raf/Mek/Erk pathway and prevent rescue of the individual null phenotypes.”
MethodWang, X., Zhao, H., Luo, X., Yang, C., Shi, C., Wang, Y., Bai, J., Shao, Z., & Shang, Z. (2024) · Oncogene · doi:10.1038/s41388-024-03112-2 · Cited by 19
“ETS2, a member of the ETS family transcription factors, is recognized for its contribution to endothelial cell branching and tube formation [19, 20].”
The transcription factors Ets1 and Sox10 interact during murine melanocyte development
Saldana-Caboverde, A., Perera, E. M., Watkins‐Chow, D. E., Hansen, N. F., Vemulapalli, M., Mullikin, J. C., Program, N. C. S., Pavan, W. J., & Kos, L. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.04.012 · Cited by 19
“Ets1 is required for the survival of various cell lineages, including thymocytes, T cells (Muthusamy et al., 1995), and endothelial cells (Wei et al., 2009).”
BackgroundYang, J., Joshi, S. S., Wang, Q., Li, P., Wang, H., Xiong, Y., Xiao, Y. Q., Wang, J., Parker‐Thornburg, J., Behringer, R. R., et al. (2017) · Cell & Bioscience · doi:10.1186/s13578-017-0186-y · Cited by 19
“Mice lacking both Ets1 and Ets2 have been reported to be embryonic lethal due to vascular defects and enhanced endothelial cell apoptosis [61], indicating an important role for Ets1 and Ets2, the miR-126 regulators, in maintenance of vascular integrity.”
Critical role of WNK1 in MYC-dependent early mouse thymocyte development
Köchl, R., Vanes, L., Sopeña, M. L., Chakravarty, P., Hartweger, H., Fountain, K., White, A. J., Cowan, J. E., Anderson, G., & Tybulewicz, V. L. J. (2020) · eLife · doi:10.7554/elife.56934 · Cited by 18
“ETS1 regulates the expression of the anti-apoptotic Bcl2A1 gene in endothelial cells (Wei et al., 2009), suggesting that it may perform a similar function in thymocytes.”
Background
Metadata
- 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
- 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
- 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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