Skip to main content

Advertisement

SpringerLink
Log in

Role of microRNA-93 in regulation of angiogenesis

  • Review
  • Published:
Tumor Biology

Abstract

Angiogenesis is essential for a wide variety of physiological and pathological processes. To date, many angiogenic microRNAs (miRNAs) have been identified and several of them were further investigated to elucidate the mechanisms of specific miRNAs in regulating angiogenesis. In recent studies concerning tumor and ischemia, the miRNA-93 had been demonstrated to be able to modulate angiogenesis in different molecular pathways. The miRNA-93 can promote angiogenesis via enhancing endothelial cell proliferation, migration, and tube formation. Additionally, miRNA-93-over-expressing cells developed a relationship with the blood vessels allowing tumor cells to survive and to grow well. However, high expression of miRNA-93 can depress the vascular endothelial growth factor (VEGF) secretion and its downstream molecular targets in in vivo and vitro experiments. MiRNA-93’s effects on angiogenesis are dependent on the interaction of other multiple genes and signal pathways, such as P21, E2F1, integrin-β8, LATS2, etc. Future investigation should involve mapping the network by which miRNA-93 exerts its functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Siomi H, Siomi MC. Posttranscriptional regulation of microRNA biogenesis in animals. Mol Cell. 2010;38:323–32.

    Article  CAS  PubMed  Google Scholar 

  2. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG, et al. In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell. 2011;147:382–95.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA. 2004;10:1507–17.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al. Combinatorial microRNA target predictions. Nat Genet. 2005;37:495–500.

    Article  CAS  PubMed  Google Scholar 

  5. Yamakuchi M, Lotterman CD, Bao C, Hruban RH, Karim B, Mendell JT, et al. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc Natl Acad Sci U S A. 2010;107:6334–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Dao P, Jarray R, Smith N, Lepelletier Y, Coq JL, Lietha D, et al. Inhibition of both focal adhesion kinase and fibroblast growth factor receptor 2 pathways induces anti-tumor and anti-angiogenic activities. Cancer Lett. 2014.

  7. Hong L, Li S, Han Y, Du J, Zhang H, Li J, et al. Angiogenesis-related molecular targets in esophageal cancer. Expert Opin Investig Drugs. 2011;20:637–44.

    Article  CAS  PubMed  Google Scholar 

  8. Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, et al. MicroRNAs regulate brain morphogenesis in zebrafish. Science. 2005;308:833–8.

    Article  CAS  PubMed  Google Scholar 

  9. Matsuda S, Ichigotani Y, Okuda T, Irimura T, Nakatsugawa S, Hamaguchi M. Molecular cloning and characterization of a novel human gene (HERNA) which encodes a putative RNA-helicase. Biochim Biophys Acta. 2000;1490:163–9.

    Article  CAS  PubMed  Google Scholar 

  10. Suarez Y, Fernandez-Hernando C, Yu J, Gerber SA, Harrison KD, Pober JS, et al. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci U S A. 2008;105:14082–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, et al. MiR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008;15:272–84.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, et al. MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 2006;108:3068–71.

    Article  CAS  PubMed  Google Scholar 

  13. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, et al. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet. 2006;38:1060–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science. 2009;324:1710–3.

    Article  CAS  PubMed  Google Scholar 

  15. Dews M, Fox JL, Hultine S, Sundaram P, Wang W, Liu YY, et al. The Myc-miR-17~92 axis blunts TGF{beta} signaling and production of multiple TGF{beta}-dependent antiangiogenic factors. Cancer Res. 2010;70:8233–46.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Li F, Liu J, Li S. MicroRNA 106b approximately 25 cluster and gastric cancer. Surg Oncol. 2013;22:e7–10.

    Article  PubMed  Google Scholar 

  17. Yeung ML, Yasunaga J, Bennasser Y, Dusetti N, Harris D, Ahmad N, et al. Roles for microRNAs, miR-93 and miR-130b, and tumor protein 53-induced nuclear protein 1 tumor suppressor in cell growth dysregulation by human T-cell lymphotrophic virus 1. Cancer Res. 2008;68:8976–85.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Du L, Schageman JJ, Subauste MC, Saber B, Hammond SM, Prudkin L, et al. MiR-93, miR-98, and miR-197 regulate expression of tumor suppressor gene FUS1. Mol Cancer Res. 2009;7:1234–43.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Hazarika S, Farber CR, Dokun AO, Pitsillides AN, Wang T, Lye RJ, et al. MicroRNA-93 controls perfusion recovery after hindlimb ischemia by modulating expression of multiple genes in the cell cycle pathway. Circulation. 2013;127:1818–28.

    Article  CAS  PubMed  Google Scholar 

  20. Savita U, Karunagaran D. MicroRNA-106b-25 cluster targets beta-TRCP2, increases the expression of snail and enhances cell migration and invasion in H1299 (non small cell lung cancer) cells. Biochem Biophys Res Commun. 2013;434:841–7.

    Article  CAS  PubMed  Google Scholar 

  21. Fang L, Deng Z, Shatseva T, Yang J, Peng C, Du WW, et al. MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-beta8. Oncogene. 2011;30:806–21.

    Article  CAS  PubMed  Google Scholar 

  22. Fang L, Du WW, Yang W, Rutnam ZJ, Peng C, Li H, et al. MiR-93 enhances angiogenesis and metastasis by targeting LATS2. Cell Cycle. 2012;11:4352–65.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Dang LT, Lawson ND, Fish JE. MicroRNA control of vascular endothelial growth factor signaling output during vascular development. Arterioscler Thromb Vasc Biol. 2013;33:193–200.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Ling S, Birnbaum Y, Nanhwan MK, Thomas B, Bajaj M, Ye Y. MicroRNA-dependent cross-talk between VEGF and HIF1 alpha in the diabetic retina. Cell Signal. 2013;25:2840–7.

    Article  CAS  PubMed  Google Scholar 

  25. Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, et al. Mirna-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One. 2006;1:e116.

    Article  PubMed Central  PubMed  Google Scholar 

  26. Long J, Wang Y, Wang W, Chang BH, Danesh FR. Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem. 2010;285:23457–65.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Yang IP, Tsai HL, Hou MF, Chen KC, Tsai PC, Huang SW, et al. MicroRNA-93 inhibits tumor growth and early relapse of human colorectal cancer by affecting genes involved in the cell cycle. Carcinogenesis. 2012;33:1522–30.

    Article  CAS  PubMed  Google Scholar 

  28. Liakouli V, Cipriani P, Marrelli A, Alvaro S, Ruscitti P, Giacomelli R. Angiogenic cytokines and growth factors in systemic sclerosis. Autoimmun Rev. 2011;10:590–4.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported partially by the Tianjin Natural Science Funds (13JCYBJC24200) and the National Natural Science Foundation (81302250) of China.

Conflicts of interest

None

Author information

Authors and Affiliations

  1. Department of Cancer Prevention Center, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin, China

    Fangxuan Li, Xiaofeng Liang, Shixia Li & Juntian Liu

  2. Department of Gynecologic Oncology, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin, China

    Ying Chen

Authors
  1. Fangxuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaofeng Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ying Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shixia Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juntian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juntian Liu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, F., Liang, X., Chen, Y. et al. Role of microRNA-93 in regulation of angiogenesis. Tumor Biol. 35, 10609–10613 (2014). https://doi.org/10.1007/s13277-014-2605-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13277-014-2605-6

Keywords

Search

Navigation