Transforming Growth Factor β-regulated MicroRNA-29a Promotes Angiogenesis through Targeting the Phosphatase and Tensin Homolog in Endothelium
Open accessAbstract
The TGF-β pathway plays an important role in physiological and pathological angiogenesis. MicroRNAs (miRNAs) are a class of 18- to 25-nucleotide, small, noncoding RNAs that function by regulating gene expression. A number of miRNAs have been found to be regulated by the TGF-β pathway. However, the role of endothelial miRNAs in the TGF-β-mediated control of angiogenesis is still largely unknown. Here we investigated the regulation of endothelial microRNA-29a (miR-29a) by TGF-β signaling and the potential role of miR-29a in angiogenesis. MiR-29a was directly up-regulated by TGF-β/Smad4 signaling in human and mice endothelial cells. In a chick chorioallantoic membrane assay, miR-29a overexpression promoted the formation of new blood vessels, and miR-29a suppression completely blocked TGF-β1-stimulated angiogenesis. Consistently, miR-29a overexpression increased tube formation and migration in endothelial cultures. Mechanistically, miR-29a directly targeted the phosphatase and tensin homolog (PTEN) in endothelial cells, leading to activation of the AKT pathway. PTEN knockdown recapitulated the role of miR-29a in endothelial migration, whereas AKT inhibition completely attenuated the stimulating role of miR-29a in angiogenesis. Taken together, these results reveal a crucial role of a TGF-β-regulated miRNA in promoting angiogenesis by targeting PTEN to stimulate AKT activity.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
TGFβ family members stimulate astrocyte responses and modify angiogenesis and neuroinflammation.
“TGFβ family members stimulate astrocyte responses and modify angiogenesis and neuroinflammation30,31.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [31]
The Discussion reports that TGF-β signaling promotes angiogenesis by up-regulating miR-29a in endothelial cells. The paper does not address astrocyte responses or neuroinflammation (searched: astrocyte responses, neuroinflammation, brain inflammation), so it supports only the angiogenesis part of the sentence. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
MicroRNAs: Target Recognition and Regulatory Functions
Bartel, D. P. (2009) · Cell · doi:10.1016/j.cell.2009.01.002 · Cited by 20,068 · see citing works
Mechanisms of TGF-β Signaling from Cell Membrane to the Nucleus
Shi, Y., & Massagué, J. (2003) · Cell · doi:10.1016/s0092-8674(03)00432-x · Cited by 5,860 · see citing works
Molecular mechanisms and clinical applications of angiogenesis
Carmeliet, P., & Jain, R. K. (2011) · Nature · doi:10.1038/nature10144 · Cited by 5,467 · see citing works
The Endothelial-Specific MicroRNA miR-126 Governs Vascular Integrity and Angiogenesis
Wang, S., Aurora, A. B., Johnson, B. A., Qi, X., McAnally, J., Hill, J. A., Richardson, J. A., Bassel‐Duby, R., & Olson, E. N. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.07.002 · Cited by 1,825 · see citing works
Tumor angiogenesis: molecular pathways and therapeutic targets
Weis, S. M., & Cheresh, D. A. (2011) · Nature Medicine · doi:10.1038/nm.2537 · Cited by 1,726 · see citing works
SMAD proteins control DROSHA-mediated microRNA maturation
Davis‐Dusenbery, B. N., Hilyard, A. C., Lagna, G., & Hata, A. (2008) · Nature · doi:10.1038/nature07086 · Cited by 1,243 · see citing works
MicroRNA-92a Controls Angiogenesis and Functional Recovery of Ischemic Tissues in Mice
Bonauer, A., Carmona, G., Iwasaki, M., Mione, M., Koyanagi, M., Fischer, A., Burchfield, J. S., Fox, H., Doebele, C., Ohtani, K., et al. (2009) · Science · doi:10.1126/science.1174381 · Cited by 1,214 · see citing works
Balancing the activation state of the endothelium via two distinct TGF‐β type I receptors
Goumans, M., Valdimarsdóttir, G., Itoh, S., Rosendahl, A., Sideras, P., & ten Dijke, P. (2002) · The EMBO Journal · doi:10.1093/emboj/21.7.1743 · Cited by 1,127 · see citing works
Defective haematopoiesis and vasculogenesis in transforming growth factor-β1 knock out mice
Dickson, M. C., Martin, J. S., Cousins, F. M., Kulkarni, A. B., Karlsson, S., & Akhurst, R. J. (1995) · Development · doi:10.1242/dev.121.6.1845 · Cited by 1,029 · see citing works
Fasanaro, P., D'Alessandra, Y., Di Stefano, V., Melchionna, R., Romani, S., Pompilio, G., Capogrossi, M. C., & Martelli, F. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800731200 · Cited by 912 · see citing works
Defective Angiogenesis in Mice Lacking Endoglin
Li, D. Y., Sorensen, L. K., Brooke, B. S., Urness, L. D., Davis, E. C., Taylor, D. G., Boak, B. B., & Wendel, D. P. (1999) · Science · doi:10.1126/science.284.5419.1534 · Cited by 853 · see citing works
Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis
Roderburg, C., Urban, G.-W., Bettermann, K., Vucur, M., Zimmermann, H. W., Schmidt, S., Janssen, J., Koppe, C., Knolle, P. A., Castoldi, M., et al. (2010) · Hepatology · doi:10.1002/hep.23922 · Cited by 802 · see citing works
MicroRNAs modulate the angiogenic properties of HUVECs
Poliseno, L., Tuccoli, A., Mariani, L., Evangelista, M., Citti, L., Woods, K., Mercatanti, A., Hammond, S. M., & Rainaldi, G. (2006) · Blood · doi:10.1182/blood-2006-01-012369 · Cited by 754 · see citing works
Kong, W. W., Yang, H., He, L., Zhao, J., Coppola, D., Dalton, W. S., & Cheng, J. Q. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00941-08 · Cited by 689 · see citing works
TGF-β Receptor Type II Deficiency Results in Defects of Yolk Sac Hematopoiesis and Vasculogenesis
Oshima, M., Oshima, H., & Taketo, M. M. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0259 · Cited by 651 · see citing works
TGF-β/Smad3 Signaling Promotes Renal Fibrosis by Inhibiting miR-29
Qin, W., Chung, A. C. K., Huang, X. R., Meng, X., Hui, D. S. C., Yu, C., Sung, J. J. �., & Lan, H. Y. (2011) · Journal of the American Society of Nephrology · doi:10.1681/asn.2010121308 · Cited by 568 · see citing works
MicroRNA‐29, a key regulator of collagen expression in systemic sclerosis
Maurer, B., Stańczyk, J., Jüngel, A., Akhmetshina, A., Trenkmann, M., Brock, M., Kowal‐Bielecka, O., Gay, R. E., Michel, B. A., Distler, J. H. W., et al. (2010) · Arthritis & Rheumatism · doi:10.1002/art.27443 · Cited by 536 · see citing works
Angiogenesis selectively requires the p110α isoform of PI3K to control endothelial cell migration
Graupera, M., Guillermet‐Guibert, J., Foukas, L. C., Phng, L., Cain, R. J., Salpekar, A., Pearce, W. P., Meek, S. E., Millán, J., Cutillas, P. R., et al. (2008) · Nature · doi:10.1038/nature06892 · Cited by 521 · see citing works
miR-29 Is a Major Regulator of Genes Associated with Pulmonary Fibrosis
Cushing, L., Kuang, P. P., Qian, J., Shao, F., Wu, J., Little, F. F., Thannickal, V. J., Cardoso, W. V., & Lü, J. (2010) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2010-0323oc · Cited by 503 · see citing works
MiR-21 Induced Angiogenesis through AKT and ERK Activation and HIF-1α Expression
Liu, L.-Z., Li, C.-Y., Chen, Q., Yi, J., Carpenter, R. L., Jiang, Y., Kung, H., Lai, L., & Jiang, B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019139 · Cited by 492 · see citing works
Chapter 2 PI3K/PTEN Signaling in Angiogenesis and Tumorigenesis
(2009) · Advances in Cancer Research · doi:10.1016/s0065-230x(09)02002-8 · Cited by 486 · see citing works
A murine model of hereditary hemorrhagic telangiectasia
Bourdeau, A., Dumont, D., & Letarte, M. (1999) · Journal of Clinical Investigation · doi:10.1172/jci8088 · Cited by 471 · see citing works
miR-296 Regulates Growth Factor Receptor Overexpression in Angiogenic Endothelial Cells
Würdinger, T., Tannous, B. A., Saydam, O., Skog, J., Grau, S., Soutschek, J., Weissleder, R., Breakefield, X. O., & Krichevsky, A. M. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.10.005 · Cited by 460 · see citing works
Chen, Y., & Gorski, D. H. (2007) · Blood · doi:10.1182/blood-2007-07-104133 · Cited by 454 · see citing works
Arteriovenous malformations in mice lacking activin receptor-like kinase-1
Urness, L. D., Sorensen, L. K., & Li, D. Y. (2000) · Nature Genetics · doi:10.1038/81634 · Cited by 443 · see citing works
MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis
Nicoli, S., Standley, C., Walker, P., Hurlstone, A. F. L., Fogarty, K. E., & Lawson, N. D. (2010) · Nature · doi:10.1038/nature08889 · Cited by 441 · see citing works
Ghosh, G., Subramanian, I. V., Adhikari, N., Zhang, X., Joshi, H. P., Basi, D. L., Chandrashekhar, Y., Hall, J. L., Roy, S., Zeng, Y., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci42980 · Cited by 417 · see citing works
Signaling by members of the TGF-β family in vascular morphogenesis and disease
Pardali, E., Goumans, M., & ten Dijke, P. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.06.006 · Cited by 402 · see citing works
Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5
Yang, X. Y., Castilla, L. H., Xu, X., Li, C., Gotay, J., Weinstein, M. B., Liu, P. P., & Deng, C. (1999) · Development · doi:10.1242/dev.126.8.1571 · Cited by 388 · see citing works
Self-citationDoebele, C., Bonauer, A., Fischer, A., Scholz, A., Reiss, Y., Urbich, C., Hofmann, W., Zeiher, A. M., & Dimmeler, S. (2010) · Blood · doi:10.1182/blood-2010-01-264812 · Cited by 362 · see citing works
Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126
Kuhnert, F., Mancuso, M. R., Hampton, J. P., Stankunas, K., Asano, T., Chen, C., & Kuo, C. J. (2008) · Development · doi:10.1242/dev.029736 · Cited by 344 · see citing works
Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23∼27∼24 clusters
Zhou, Q., Gallagher, R., Ufret-Vincenty, R., Li, X., Olson, E. N., & Wang, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105254108 · Cited by 341 · see citing works
Kumarswamy, R., Volkmann, I. R., Jazbutyte, V., Dangwal, S., Park, D., & Thum, T. (2011) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.111.234286 · Cited by 294 · see citing works
TGF-β Regulates miR-206 and miR-29 to Control Myogenic Differentiation through Regulation of HDAC4
Winbanks, C. E., Wang, B., Beyer, C., Koh, P., White, L. J., Kantharidis, P., & Gregorevic, P. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.192625 · Cited by 265 · see citing works
Transforming growth factor- -regulated miR-24 promotes skeletal muscle differentiation
Sun, Q., Zhang, Y., Yang, G., Chen, X., Zhang, Y., Cao, G., Wang, J., Sun, Y., Zhang, Y., Fan, M., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn032 · Cited by 261 · see citing works
Self-citationLi, F., Lan, Y., Wang, Y., Wang, J., Yang, G., Meng, F., Han, H., Meng, A., Wang, Y., & Yang, X. Y. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.01.011 · Cited by 259 · see citing works
Self-citationTranscriptional suppression of mir-29b-1/mir-29a promoter by c-Myc, hedgehog, and NF-kappaB
Mott, J. L., Kurita, S., Cazanave, S. C., Bronk, S. F., Werneburg, N. W., & Fernandez‐Zapico, M. E. (2010) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22630 · Cited by 233 · see citing works
MicroRNA-27a/b controls endothelial cell repulsion and angiogenesis by targeting semaphorin 6A
Urbich, C., Kaluza, D., Frömel, T., Knau, A., Bennewitz, K., Boon, R. A., Bonauer, A., Doebele, C., Boeckel, J., Hergenreider, E., et al. (2011) · Blood · doi:10.1182/blood-2011-08-373886 · Cited by 231 · see citing works
MCP-1 mediates TGF-β–induced angiogenesis by stimulating vascular smooth muscle cell migration
Ma, J., Wang, Q., Fei, T., Han, J. J., & Chen, Y. (2006) · Blood · doi:10.1182/blood-2006-07-036400 · Cited by 213 · see citing works
Cardiomyocyte overexpression of miR-27b induces cardiac hypertrophy and dysfunction in mice
Wang, J., Song, Y., Zhang, Y., Xiao, H., Sun, Q., Hou, N., Guo, S., Wang, Y., Fan, K., Zhan, D., et al. (2011) · Cell Research · doi:10.1038/cr.2011.132 · Cited by 203 · see citing works
Self-citationPTEN Modulates Vascular Endothelial Growth Factor-Mediated Signaling and Angiogenic Effects
Huang, J., & Kontos, C. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110219200 · Cited by 191 · see citing works
The microRNA-30 family targets DLL4 to modulate endothelial cell behavior during angiogenesis
Bridge, G. E. M., Monteiro, R. M., Henderson, S. R., Emuss, V., Lagos, D., Georgopoulou, D., Patient, R. K., & Boshoff, C. (2012) · Blood · doi:10.1182/blood-2012-04-423004 · Cited by 185 · see citing works
Targeted Mutagenesis of Smad1 Reveals an Essential Role in Chorioallantoic Fusion
Lechleider, R. J., Ryan, J. L., Garrett, L. J., Eng, C., Deng, C., Wynshaw-Boris, A. J., & Roberts, A. B. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0469 · Cited by 185 · see citing works
miR-21 Promotes Keratinocyte Migration and Re-epithelialization During Wound Healing
Yang, X., Wang, J., Guo, S.-L., Fan, K.-J., Li, J., Wang, Y.-L., Teng, Y., & Yang, X. (2011) · International Journal of Biological Sciences · doi:10.7150/ijbs.7.685 · Cited by 180 · see citing works
Self-citationKong, G., Zhang, J., Zhang, S., Shan, C., Ye, L., & Zhang, X. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019518 · Cited by 172 · see citing works
High glucose down‐regulates miR‐29a to increase collagen IV production in HK‐2 cells
Du, B., Ma, L., Huang, M., Zhou, H., Huang, H., Shao, P., Chen, Y., & Qu, L. (2010) · FEBS Letters · doi:10.1016/j.febslet.2009.12.053 · Cited by 168 · see citing works
MicroRNAs: Opening a New Vein in Angiogenesis Research
Fish, J. E., & Srivastava, D. (2009) · Science Signaling · doi:10.1126/scisignal.252pe1 · Cited by 160 · see citing works
van Mil, A., Grundmann, S., Goumans, M., Lei, Z., Oerlemans, M. I. F. J., Jaksani, S., Doevendans, P. A., & Sluijter, J. P. G. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs003 · Cited by 152 · see citing works
Essential Role of Endothelial Smad4 in Vascular Remodeling and Integrity
Lan, Y., Liu, B., Yao, H., Li, F., Weng, T., Yang, G., Li, W., Cheng, X., Mao, N., & Yang, X. Y. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00577-07 · Cited by 120 · see citing works
Self-citationmiR-1 and miR-206 regulate angiogenesis by modulating VegfA expression in zebrafish
Stahlhut, C. E., Suárez, Y., Lü, J., Mishima, Y., & Giráldez, A. J. (2012) · Development · doi:10.1242/dev.083774 · Cited by 108 · see citing works
Muramatsu, F., Kidoya, H., Naito, H., Sakimoto, S., & Takakura, N. (2012) · Oncogene · doi:10.1038/onc.2012.68 · Cited by 107 · see citing works
MicroRNA profiling of diverse endothelial cell types
McCall, M. N., Kent, O. A., Yu, J., Fox-Talbot, K., Zaiman, A., & Halushka, M. K. (2011) · BMC Medical Genomics · doi:10.1186/1755-8794-4-78 · Cited by 100 · see citing works
miR-29a and miR-142-3p downregulation and diagnostic implication in human acute myeloid leukemia
Wang, F., Wang, X., Yang, G., Zhai, P.-F., Xiao, Z., Xia, L., Chen, L., Wang, Y., Wang, X., Bi, L., et al. (2011) · Molecular Biology Reports · doi:10.1007/s11033-011-1026-5 · Cited by 91 · see citing works
Self-citationChen, Y., Banda, M., Speyer, C. L., Smith, J. S., Rabson, A. B., & Gorski, D. H. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.01237-09 · Cited by 86 · see citing works
The manipulation of miRNA-gene regulatory networks by KSHV induces endothelial cell motility
Wu, Y., Hu, T.-F., Chen, Y.-C., Tsai, Y.-N., Tsai, Y.-H., Cheng, C., & Wang, H. (2011) · Blood · doi:10.1182/blood-2011-01-330589 · Cited by 84 · see citing works
Alaiti, M. A., Ishikawa, M., Masuda, H., Simon, D. I., Jain, M. K., Asahara, T., & Costa, M. A. (2012) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2012.01557.x · Cited by 77 · see citing works
Guduric‐Fuchs, J., O’Connor, A., Cullen, A., Harwood, L., Medina, R. J., O’Neill, C. L., Stitt, A. W., Curtis, T. M., & Simpson, D. A. C. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24084 · Cited by 73 · see citing works
Chow, J. Y. C., Dong, H., Quach, K. T., Nguyen, P. N. V., Chen, K., & Carethers, J. M. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00411.2007 · Cited by 70 · see citing works
Perry, B. N., Banyard, J., McLaughlin, E. R., Watnick, R., Sohn, A. M., Brindley, D. N., Obata, T., Cantley, L. C., Cohen, C., & Arbiser, J. L. (2007) · Archives of Dermatology · doi:10.1001/archderm.143.4.504 · Cited by 63 · see citing works
TGF-β downregulates PTEN via activation of NF-κB in pancreatic cancer cells
Chow, J. Y. C., Ban, M., Wu, H. L., Nguyen, F., Huang, M. J., Chung, H., Dong, H., & Carethers, J. M. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00344.2009 · Cited by 55 · see citing works
Hereditary Haemorrhagic Telangiectasia (HHT): Genetic and Molecular Aspects
Lenato, G. M., & Guanti, G. (2006) · Current Pharmaceutical Design · doi:10.2174/138161206776361291 · Cited by 53 · see citing works
Chow, J. Y. C., Cabral, J., Chang, J. K., & Carethers, J. M. (2008) · Cancer Biology & Therapy · doi:10.4161/cbt.7.10.6665 · Cited by 32 · see citing works
Flagged first, then by citations
1 of the 63 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Zhou, Q., Gallagher, R., Ufret-Vincenty, R., Li, X., Olson, E. N., and Wang, S. (2011) Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23ϳ27ϳ24 clusters. Proc. Natl. Acad. Sci. U.S.A. 108, 8287-8292
Cited by
Sorted by citations
The roles of TGFβ in the tumour microenvironment
Pickup, M. W., Novitskiy, S. V., & Moses, H. L. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3603 · Cited by 915 · see citing works
The H19 long noncoding RNA is a novel negative regulator of cardiomyocyte hypertrophy
Liu, L., An, X., Li, Z., Song, Y., Li, L., Zuo, S., Liu, N., Yang, G., Wang, H., Cheng, X., et al. (2016) · Cardiovascular Research · doi:10.1093/cvr/cvw078 · Cited by 235 · see citing works
Self-citationTumor angiogenesis revisited: Regulators and clinical implications
Ronca, R., Benkheil, M., Mitola, S. M. F., Struyf, S., & Liekens, S. (2017) · Medicinal Research Reviews · doi:10.1002/med.21452 · Cited by 193 · see citing works
GDF10 is a signal for axonal sprouting and functional recovery after stroke
Li, S., Nie, E. H., Yin, Y., Benowitz, L. I., Tung, S., Vinters, H. V., Bahjat, F. R., Stenzel-Poore, M. P., Kawaguchi, R., Coppola, G., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4146 · Cited by 181 · see citing works
“TGF β family members stimulate astrocyte responses and modify angiogenesis and neuroinflammation 30,31 .”
Lyu, G., Guan, Y., Zhang, C., Zong, L., Sun, L., Huang, X., Huang, L., Zhang, L., Tian, X., Zhou, Z., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04994-z · Cited by 176 · see citing works
Transforming growth factor‐β signalling in renal fibrosis: from Smads to non‐coding RNAs
Tang, P. M., Zhang, Y., Mak, T. S., Tang, P. C., Huang, X., & Lan, H. Y. (2018) · The Journal of Physiology · doi:10.1113/jp274492 · Cited by 118 · see citing works
Dichotomous roles of TGF-β in human cancer
Huang, J. J., & Blobe, G. C. (2016) · Biochemical Society Transactions · doi:10.1042/bst20160065 · Cited by 108 · see citing works
Extracellular vesicles shed by glioma cells: pathogenic role and clinical value
Chistiakov, D. A., & Chekhonin, V. P. (2014) · Tumor Biology · doi:10.1007/s13277-014-2262-9 · Cited by 87 · see citing works
MiR-29a : a potential therapeutic target and promising biomarker in tumors
Wang, J., Zhang, Q., Wang, D., Yan, W., Sha, H., Zhao, J., Yang, S., Zhang, H.-D., Hou, J., Xu, H., et al. (2017) · Bioscience Reports · doi:10.1042/bsr20171265 · Cited by 80 · see citing works
Self-citationShen, H., Li, L., Yang, S., Wang, D., Zhong, S., Zhao, J., & Tang, J. (2016) · Gene · doi:10.1016/j.gene.2016.08.016 · Cited by 77 · see citing works
Dual targeting of ANGPT1 and TGFBR2 genes by miR-204 controls angiogenesis in breast cancer
Flores‐Pérez, A., Marchat, L. A., Rodriguez-Cuevas, S. A., Bautista‐Piña, V., Hidalgo‐Miranda, A., Aréchaga-Ocampo, E., Martínez, M. S., Flores, C. P., Fonseca-Sánchez, M. A., la Vega, H. A., et al. (2016) · Scientific Reports · doi:10.1038/srep34504 · Cited by 75 · see citing works
Kim, J. O., Song, D. W., Kwon, E. J., Hong, S., Song, H. K., Min, C. K., & Kim, D. H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122509 · Cited by 74 · see citing works
Antiangiogenic Effect of Alkaloids
Alasvand, M., Assadollahi, V., Ambra, R., Hedayati, E., Kooti, W., & Peluso, I. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/9475908 · Cited by 71 · see citing works
Global microRNA depletion suppresses tumor angiogenesisPreprint
Chen, S., Xue, Y., Wu, X., Cong, L., Bhutkar, A. J., Bell, E. L., Zhang, F., Langer, R., & Sharp, P. A. (2014) · Genes & Development · doi:10.1101/gad.239681.114 · Cited by 67 · see citing works
The Role of TGF-β Signaling Pathways in Cancer and Its Potential as a Therapeutic Target
Yang, Y., Ye, W.-L., Zhang, R., He, X., Wang, J., Liu, Y., Wang, Y., Yang, X., Zhang, Y., & Gan, W.-J. (2021) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2021/6675208 · Cited by 66 · see citing works
Self-citationRen, L., Wei, C., Li, K., & Lu, Z. (2018) · Bioscience Reports · doi:10.1042/bsr20180226 · Cited by 63 · see citing works
RetractedLuteolin-7-diglucuronide attenuates isoproterenol-induced myocardial injury and fibrosis in mice
Ning, B.-B., Zhang, Y., Wu, D., Cui, J., Liu, L., Wang, P., Wang, W., Zhu, W., Chen, Y., & Zhang, T. (2017) · Acta Pharmacologica Sinica · doi:10.1038/aps.2016.142 · Cited by 62 · see citing works
MicroRNAs Are Stored in Human MII Oocyte and Their Expression Profile Changes in Reproductive Aging
Battaglia, R., Vento, M. E., Ragusa, M., Barbagallo, D., Ferlita, A. L., Emidio, G. D., Borzi, P., Artini, P. G., Scollo, P., Tatone, C., et al. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.116.142711 · Cited by 60 · see citing works
Wronska, A. (2022) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.121.001152 · Cited by 59 · see citing works
Shi, X., Valizadeh, A., Mir, S. M., Asemi, Z., Karimian, A., Majidina, M., Safa, A., & Yosefi, B. (2020) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2020.173138 · Cited by 58 · see citing works
TGF β : A player on multiple fronts in the tumor microenvironment
Čaja, F., & Vannucci, L. E. (2014) · Journal of Immunotoxicology · doi:10.3109/1547691x.2014.945667 · Cited by 56 · see citing works
MicroRNAs in the cornea: Role and implications for treatment of corneal neovascularization
Mukwaya, A., Jensen, L. D., Peebo, B. B., & Lagali, N. (2019) · The Ocular Surface · doi:10.1016/j.jtos.2019.04.002 · Cited by 56 · see citing works
Zhou, C., Zou, Q., Li, H., Wang, R.-F., Liu, A., Magness, R. R., & Zheng, J. J. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-00849 · Cited by 52 · see citing works
Kennedy, D. C., Coen, B. A., Wheatley, A. M., & McCullagh, K. J. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010452 · Cited by 46 · see citing works
Transforming growth factor-β in tumour development
Trelford, C. B., Dagnino, L., & Guglielmo, G. M. D. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.991612 · Cited by 43 · see citing works
MicroRNA signature and function in retinal neovascularization
Agrawal, S. (2014) · World Journal of Biological Chemistry · doi:10.4331/wjbc.v5.i1.1 · Cited by 43 · see citing works
Brain protection against ischemic stroke using choline as a new molecular bypass treatment
Jin, X., Wang, R.-H., Wang, H., Long, C.-L., & Wang, H. (2015) · Acta Pharmacologica Sinica · doi:10.1038/aps.2015.104 · Cited by 41 · see citing works
Noncoding RNAs in Tumor Angiogenesis
Khorshidi, A., Dhaliwal, P., & Yang, B. B. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-1498-7_8 · Cited by 39 · see citing works
Yu, C.-C., Chen, H.-L., Chen, M.-H., Lu, C.-H., Tsai, N.-W., Huang, C.-C., Chang, Y.-Y., Li, S.-H., Chen, Y.-S., Chiang, P.-L., et al. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/2591248 · Cited by 37 · see citing works
Freitas, L. S., Silveira, A. C., Martins, F. C., Costa-Hong, V., Lebkuchen, A., Cardozo, K. H. M., Bernardes, F. M., Bortolotto, L. A., Lorenzi-Filho, G., Oliveira, E. M., et al. (2020) · Sleep and Breathing · doi:10.1007/s11325-019-02003-1 · Cited by 37 · see citing works
Kim, Y., Park, D., Kim, H., Choi, M., Lee, H., Lee, Y. S., Choe, J., Kim, Y. M., & Jeoung, D. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.502047 · Cited by 37 · see citing works
The short and long of noncoding sequences in the control of vascular cell phenotypes
Miano, J. M., & Long, X. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1936-9 · Cited by 37 · see citing works
CircRNA-Mediated Regulation of Angiogenesis: A New Chapter in Cancer Biology
Jiang, S., Fu, R., Shi, J., Wu, H., Mai, J., Hua, X., Huan, C., Liu, J., Lu, M.-Q., & Li, N. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.553706 · Cited by 34 · see citing works
Contribution of microRNA to pathological fibrosis in cardio-renal syndrome: impact of uremic toxins
Rana, I., Kompa, A. R., Skommer, J., Wang, B. H., Lekawanvijit, S., Kelly, D. J., Krum, H., & Charchar, F. J. (2015) · Physiological Reports · doi:10.14814/phy2.12371 · Cited by 31 · see citing works
Spatiotemporal dynamics of microRNA during epithelial collective cell migration
Dean, Z., Riahi, R., & Wong, P. K. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.10.022 · Cited by 30 · see citing works
Targeting angiogenesis in gliomas: Potential role of phytochemicals
Sanati, M., Afshari, A. R., Amini, J., Mollazadeh, H., Jamialahmadi, T., & Sahebkar, A. (2022) · Journal of Functional Foods · doi:10.1016/j.jff.2022.105192 · Cited by 29 · see citing works
Hines, M. J., Coffre, M., Mudianto, T., Panduro, M., Wigton, E. J., Tegla, C., Osorio-Vasquez, V., Kageyama, R., Benhamou, D., Perez, O. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108436 · Cited by 27 · see citing works
Liu, Y., Xia, T., Zhang, W., Zhong, Y., Zhang, L., Wang, X., & Yu, H. (2013) · Radiation Oncology · doi:10.1186/1748-717x-8-189 · Cited by 27 · see citing works
Hong, Q., Yu, S., Geng, X., Duan, L., Zheng, W., Fan, M., Chen, X., & Wu, D. (2015) · Microcirculation · doi:10.1111/micc.12200 · Cited by 26 · see citing works
Chuang, P.-C., Lu, C.-W., Tsai, C.-C., Tseng, S.-H., & Su, W.-H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010215 · Cited by 23 · see citing works
Transforming Growth Factor-β Regulates Endothelial Function During High Salt Intake in Rats
Ying, W., Aaron, K. J., & Sanders, P. W. (2013) · Hypertension · doi:10.1161/hypertensionaha.113.01835 · Cited by 22 · see citing works
Knockout of Angiotensin AT2 receptors accelerates healing but impairs quality
Faghih, M., Hosseini, S. M., Smith, B., Ansari, A. M., Lay, F., Ahmed, A. K., Inagami, T., Marti, G. P., Harmon, J. W., Walston, J. D., et al. (2015) · Aging · doi:10.18632/aging.100868 · Cited by 22 · see citing works
Poole, E. L., da Silva, M. C. C., Huang, C., Perera, M. R., Jackson, S. E., Groves, I. J., Wills, M. R., Rana, A. A., & Sinclair, J. H. (2021) · mBio · doi:10.1128/mbio.00227-21 · Cited by 22 · see citing works
Liu, C., Zhong, Q., & Huang, Y. (2017) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.241.183 · Cited by 18 · see citing works
Upregulation of microRNA-574-3p in a human gastric cancer cell line AGS by TGF-β1
Zhang, R., Wang, M., Sui, P., Ding, L., & Yang, Q. (2016) · Gene · doi:10.1016/j.gene.2016.12.032 · Cited by 18 · see citing works
Transforming growth factor β1 alters the 3′-UTR of mRNA to promote lung fibrosis
Ko, J., Mills, T., Huang, J., Chen, N., Mertens, T. C. J., Collum, S. D., Lee, G., Xiang, Y., Han, L., Zhou, Y., et al. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.009148 · Cited by 17 · see citing works
Wang, S., Zan, J., Wu, M., Zhao, W., Li, Z., Pan, Y., Sun, Z., & Zhu, J. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.05.019 · Cited by 16 · see citing works
Regulatory RNAs controlling vascular (dys)function by affecting TGF-ß family signalling
Kurakula, K., Goumans, M., & ten Dijke, P. (2015) · EXCLI journal · doi:10.17179/excli2015-423 · Cited by 14 · see citing works
Zhou, C., Freel, C., Mills, O., Yang, X., Yan, Q., & Zheng, J. J. (2023) · The Journal of Physiology · doi:10.1113/jp284746 · Cited by 13 · see citing works
Self-citationSu, W., Wang, C.-J., Hung, Y.-Y., Lu, C.-W., Ou, C.-Y., Tseng, S.-H., Tsai, C.-C., Kao, Y.-T., & Chuang, P.-C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20235859 · Cited by 14 · see citing works
Transforming Growth Factor‐β Pathway: Biological Functions and Therapeutic Targets
Mekky, R. H., Fetoh, M. E. A., Faheem, S. A., Radwan, A., Fawzy, M. H., Mustafa, A. M., Said, M. A., Călina, D. C., Sharifi‐Rad, J., & Cho, W. C. S. (2025) · MedComm · doi:10.1002/mco2.70278 · Cited by 15 · see citing works
Chuang, P.-C., Chen, P., Wang, C., Su, W.-H., Chen, Y., & Huang, E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105524 · Cited by 12 · see citing works
ox‐LDL increases microRNA‐29a transcription through upregulating YY1 and STAT1 in macrophages
Jian, D., Dai, B., Hu, X., Yao, Q., Zheng, C., & Zhu, J. (2017) · Cell Biology International · doi:10.1002/cbin.10803 · Cited by 10 · see citing works
Roles of TGF-β in cancer hallmarks and emerging onco-therapeutic design
Dai, X., Hua, D., & Lu, X. (2022) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2022.37 · Cited by 10 · see citing works
Colorectal cancer cells differentially impact migration and microRNA expression in endothelial cells
Kim, D., Lee, S., & Bae, Y. (2019) · Oncology Letters · doi:10.3892/ol.2019.11055 · Cited by 10 · see citing works
MicroRNAs Associated with Preeclampsia
Vashukova, E. S., Glotov, A. S., & Баранов, В. С. (2020) · Russian Journal of Genetics · doi:10.1134/s1022795419080167 · Cited by 9 · see citing works
TGF-β-Regulated MicroRNAs and Their Function in Cancer Biology
Yang, P., Zhang, Y., Markowitz, G. J., Guo, X., & Wang, X. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2966-5_21 · Cited by 8 · see citing works
Pang, Y., Guo, T., Zhou, Y., Jiang, S., Li, Y., Ni, J., Chu, X., Chu, L., Chen, F., Yang, X., et al. (2025) · Clinical and Translational Medicine · doi:10.1002/ctm2.70483 · Cited by 7 · see citing works
Self-citationJackson, A. O., Tang, H., & Yin, K. (2019) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-019-09891-4 · Cited by 7 · see citing works
Xu, X., Tang, L.-C., Hao, F., & Jin, L. (2021) · Journal of Hypertension · doi:10.1097/hjh.0000000000002837 · Cited by 6 · see citing works
Hsa‐miRNA‐29a protects against high glucose‐induced damage in human umbilical vein endothelial cells
Huang, Z., Li, N., Shan, Y., & Liang, C. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.27871 · Cited by 6 · see citing works
Transforming Growth Factor-β1 and Tumor Development
Dahl, L. (2023) · Science Insights · doi:10.15354/si.23.re298 · Cited by 1 · see citing works
Dean, Z. (2015) · UA Campus Repository (The University of Arizona)
Bridge, G. E. M. (2013) · UCL Discovery (University College London)
- Authors
- Wang, J., Wang, Y., Wang, Y., Ma, Y., Lan, Y., & Yang, X.
- Affiliations
- State Key Laboratory of Proteomics (CN)
- Shanghai Jiao Tong University (CN)
- Corresponding author
- Lan, Yu
- Yang, Xiao
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2013-04
- Volume
- 288
- Issue
- 15
- Pages
- 10418-10426
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3624424
- OpenAlex
- W1999532467
- Cited by
- 64
- References
- 63
- Citations by year
- 2025: 2 · 2023: 2 · 2022: 5 · 2021: 5 · 2020: 6 · 2019: 6 · 2018: 4 · 2017: 6 · 2016: 7 · 2015: 11 · 2014: 5 · 2013: 5
- FWCI
- 3.28
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (31030040, 31171410)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- miR-29a, TGF-beta signaling, angiogenesis, endothelial cells, PTEN, AKT pathway, SMAD4, endothelial cell migration, tube formation, chick chorioallantoic membrane assay, microRNA regulation
- MeSH terms
- Animals, Cell Line, Cell Movement, Chick Embryo, Humans, Signal Transduction, Neovascularization, Physiologic, MicroRNAs, Proto-Oncogene Proteins c-akt, PTEN Phosphohydrolase, Mice, Smad4 Protein, Transforming Growth Factor beta1, Gene Knockdown Techniques, Human Umbilical Vein Endothelial Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review