MiR-29a Modulates the Angiogenic Properties of Human Endothelial Cells

Overview

Journal Biochem Biophys Res Commun

Publisher Elsevier

Specialty Biochemistry

Date 2013 Apr 2

PMID 23541945

Citations 31

Authors

Zeran Yang

Lingjiao Wu

Xiuming Zhu

Jie Xu

Rong Jin

Guohong Li

Fusheng Wu

Affiliations

Soon will be listed here.

Abstract

Although extensive investigation has been made on miR-29a in relation to malignancies, only a little information has been provided about the angiogenic property of this miRNA so far. Herein, we sought to investigate the role of miR-29a in regulating cell cycle and angiogenic phenotype of endothelial cells. The results showed that miR-29a is highly expressed and upregulated by hypoxia-mimicking reagents in human umbilical vein endothelial cells (HUVEC). Consistent with this preliminary finding, introduction of exogenous agomiR-29a, or Antagomir-29a altered cell cycle progression and promoted, or repressed the proliferation and tube formation of HUVEC, respectively. Furthermore, by using luciferase reporter assay, the expression of HBP1, a suppressor transcription factor was directly regulated by miR-29a through 3'-UTR. Increased or decreased HBP1 protein level was associated with the inhibition or overexpression of miR-29a, respectively. We conclude that miR-29a has a significant role in regulating cell cycle, proliferation and angiogenic properties of HUVEC, and this function is likely mediated through HBP1 protein at the post-transcriptional level. As a novel molecular target, miR-29a may have a potential value for the treatment of angiogenesis-associated diseases such as cardiovascular diseases and cancers.

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References

Kapinas K, Kessler C, Ricks T, Gronowicz G, Delany A . miR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J Biol Chem. 2010; 285(33):25221-31. PMC: 2919085. DOI: 10.1074/jbc.M110.116137. View

Ivan M, Harris A, Martelli F, Kulshreshtha R . Hypoxia response and microRNAs: no longer two separate worlds. J Cell Mol Med. 2008; 12(5A):1426-31. PMC: 3918058. DOI: 10.1111/j.1582-4934.2008.00398.x. View

Pekarsky Y, Croce C . Is miR-29 an oncogene or tumor suppressor in CLL?. Oncotarget. 2010; 1(3):224-7. PMC: 2951328. DOI: 10.18632/oncotarget.129. View

Kuehbacher A, Urbich C, Zeiher A, Dimmeler S . Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res. 2007; 101(1):59-68. DOI: 10.1161/CIRCRESAHA.107.153916. View

Kong G, Zhang J, Zhang S, Shan C, Ye L, Zhang X . Upregulated microRNA-29a by hepatitis B virus X protein enhances hepatoma cell migration by targeting PTEN in cell culture model. PLoS One. 2011; 6(5):e19518. PMC: 3088678. DOI: 10.1371/journal.pone.0019518. View

Santanam U, Zanesi N, Efanov A, Costinean S, Palamarchuk A, Hagan J . Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc Natl Acad Sci U S A. 2010; 107(27):12210-5. PMC: 2901490. DOI: 10.1073/pnas.1007186107. View

Shilo S, Roy S, Khanna S, Sen C . Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arterioscler Thromb Vasc Biol. 2008; 28(3):471-7. DOI: 10.1161/ATVBAHA.107.160655. View

Teichler S, Illmer T, Roemhild J, Ovcharenko D, Stiewe T, Neubauer A . MicroRNA29a regulates the expression of the nuclear oncogene Ski. Blood. 2011; 118(7):1899-902. DOI: 10.1182/blood-2010-09-306258. View

Gebeshuber C, Zatloukal K, Martinez J . miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep. 2009; 10(4):400-5. PMC: 2672883. DOI: 10.1038/embor.2009.9. View

10.

Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K . MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 2006; 108(9):3068-71. DOI: 10.1182/blood-2006-01-012369. View

11.

Wang L, Gu J . Serum microRNA-29a is a promising novel marker for early detection of colorectal liver metastasis. Cancer Epidemiol. 2011; 36(1):e61-7. DOI: 10.1016/j.canep.2011.05.002. View

12.

Nagasawa H . Pathophysiological response to hypoxia - from the molecular mechanisms of malady to drug discovery: drug discovery for targeting the tumor microenvironment. J Pharmacol Sci. 2011; 115(4):446-52. DOI: 10.1254/jphs.10r25fm. View

13.

Zile M, Mehurg S, Arroyo J, Stroud R, DeSantis S, Spinale F . Relationship between the temporal profile of plasma microRNA and left ventricular remodeling in patients after myocardial infarction. Circ Cardiovasc Genet. 2011; 4(6):614-9. PMC: 3535326. DOI: 10.1161/CIRCGENETICS.111.959841. View

14.

Fasanaro P, DAlessandra Y, Stefano V, Melchionna R, Romani S, Pompilio G . MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem. 2008; 283(23):15878-83. PMC: 3259646. DOI: 10.1074/jbc.M800731200. View

15.

Wu F, Yang Z, Li G . Role of specific microRNAs for endothelial function and angiogenesis. Biochem Biophys Res Commun. 2009; 386(4):549-53. PMC: 2821898. DOI: 10.1016/j.bbrc.2009.06.075. View

16.

Shi H, Chen L, Wang H, Zhu S, Dong C, Webster K . Synergistic induction of miR-126 by hypoxia and HDAC inhibitors in cardiac myocytes. Biochem Biophys Res Commun. 2012; 430(2):827-32. PMC: 3638006. DOI: 10.1016/j.bbrc.2012.11.061. View

17.

Paulson K, Rieger-Christ K, McDevitt M, Kuperwasser C, Kim J, Unanue V . Alterations of the HBP1 transcriptional repressor are associated with invasive breast cancer. Cancer Res. 2007; 67(13):6136-45. DOI: 10.1158/0008-5472.CAN-07-0567. View

18.

Escamilla-Powers J, Daniel C, Farrell A, Taylor K, Zhang X, Byers S . The tumor suppressor protein HBP1 is a novel c-myc-binding protein that negatively regulates c-myc transcriptional activity. J Biol Chem. 2009; 285(7):4847-58. PMC: 2836090. DOI: 10.1074/jbc.M109.074856. View

19.

Cui Y, Su W, Xing J, Wang Y, Wang P, Chen X . MiR-29a inhibits cell proliferation and induces cell cycle arrest through the downregulation of p42.3 in human gastric cancer. PLoS One. 2011; 6(10):e25872. PMC: 3187799. DOI: 10.1371/journal.pone.0025872. View

20.

Yang Z, Li J . Stimulation of endothelin-1 gene expression by insulin via phosphoinositide-3 kinase-glycogen synthase kinase-3beta signaling in endothelial cells. Life Sci. 2008; 82(9-10):512-8. DOI: 10.1016/j.lfs.2007.12.005. View