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Autoregulation of glypican-1 by intronic microRNA-149 fine-tunes the angiogenic response to fibroblast growth factor in human endothelial cells

Chamorro-Jorganes, Aránzazu, Araldi, Elisa, Rotllan, Noemi, Cirera-Salinas, Daniel, Suárez, Yajaira·2014·Journal of Cell Science

Abstract

MiR-149 is located within the first intron of glypican-1 (GPC1) gene. GPC1 is low affinity receptor for fibroblast growth factor (FGF2) that favors FGF2- binding to its receptor (FGFR1), subsequently promoting FGF2-FGFR1 activation and signaling. Using bioinformatic approaches, both GPC1 and FGFR1 were identified and subsequently validated as targets for miR-149 (both mature and passenger strands) in endothelial cells (ECs). ?As a consequence of their targeting activity towards GPC1 and FGFR1, both miR-149 and miR-149* regulated FGF2 signaling and FGF2-induced responses in ECs, namely proliferation, migration and cord formation. Moreover, lentiviral overexpression of miR-149 reduced in vivo tumor-induced neovascularization. Importantly, FGF2 transcriptionally stimulated the expression of miR-149 independently of its host gene, therefore assuring the steady state of FGF2-induced responses through the regulation of the GPC1-FGFR1 binary complex in ECs.

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Research works printed but not linked: 59

  1. Aikawa T., Whipple C. A., Lopez M. E., Gunn J., Young A., Lander A. D., Korc M. (2008). Glypican-1 modulates the angiogenic and metastatic potential of human and mouse cancer cells. J. Clin. Invest. 118, 89–99 10.1172/JCI32412 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  2. Bartel D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233 10.1016/j.cell.2009.01.002 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  3. Betel D., Koppal A., Agius P., Sander C., Leslie C. (2010). Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol. 11, R90 10.1186/gb-2010-11-8-r90 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  4. Betel D., Wilson M., Gabow A., Marks D. S., Sander C. (2008). The microRNA.org resource: targets and expression. Nucleic Acids Res. 36, D149–D53 10.1093/nar/gkm995 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  5. Bushati N., Cohen S. M. (2007). microRNA functions. Annu. Rev. Cell Dev. Biol. 23, 175–205 10.1146/annurev.cellbio.23.090506.123406 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  6. Caporali A., Emanueli C. (2011). MicroRNA regulation in angiogenesis. Vascul. Pharmacol. 55, 79–86 10.1016/j.vph.2011.06.006 [DOI] [PubMed] [Google Scholar] · DOI
  7. Carmeliet P. (2005). Angiogenesis in life, disease and medicine. Nature 438, 932–936 10.1038/nature04478 [DOI] [PubMed] [Google Scholar] · DOI
  8. Chamorro-Jorganes A., Araldi E., Penalva L. O., Sandhu D., Fernández-Hernando C., Suárez Y. (2011). MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler. Thromb. Vasc. Biol. 31, 2595–2606 10.1161/ATVBAHA.111.236521 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  9. Cross M. J., Claesson-Welsh L. (2001). FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol. Sci. 22, 201–207 10.1016/S0165-6147(00)01676-X [DOI] [PubMed] [Google Scholar] · DOI
  10. Elfenbein A., Lanahan A., Zhou T. X., Yamasaki A., Tkachenko E., Matsuda M., Simons M. (2012). Syndecan 4 regulates FGFR1 signaling in endothelial cells by directing macropinocytosis. Sci. Signal. 5, ra36 10.1126/scisignal.2002495 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  11. Ernst J., Kellis M. (2010). Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat. Biotechnol. 28, 817–825 10.1038/nbt.1662 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  12. Fico A., Maina F., Dono R. (2011). Fine-tuning of cell signaling by glypicans. Cell. Mol. Life Sci. 68, 923–929 10.1007/s00018-007-7471-6 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  13. Filmus J., Capurro M., Rast J. (2008). Glypicans. Genome Biol. 9, 224 10.1186/gb-2008-9-5-224 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  14. Folkman J. (1984). What is the role of endothelial cells in angiogenesis? Lab. Invest. 51, 601–604 [PubMed] [Google Scholar]
  15. Gengrinovitch S., Berman B., David G., Witte L., Neufeld G., Ron D. (1999). Glypican-1 is a VEGF165 binding proteoglycan that acts as an extracellular chaperone for VEGF165. J. Biol. Chem. 274, 10816–10822 10.1074/jbc.274.16.10816 [DOI] [PubMed] [Google Scholar] · DOI
  16. Gerwins P., Sköldenberg E., Claesson-Welsh L. (2000). Function of fibroblast growth factors and vascular endothelial growth factors and their receptors in angiogenesis. Crit. Rev. Oncol. Hematol. 34, 185–194 10.1016/S1040-8428(00)00062-7 [DOI] [PubMed] [Google Scholar] · DOI
  17. Hon L. S., Zhang Z. (2007). The roles of binding site arrangement and combinatorial targeting in microRNA repression of gene expression. Genome Biol. 8, R166 10.1186/gb-2007-8-8-r166 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  18. Inui M., Martello G., Piccolo S. (2010). MicroRNA control of signal transduction. Nat. Rev. Mol. Cell Biol. 11, 252–263 10.1038/nrm2868 [DOI] [PubMed] [Google Scholar] · DOI
  19. Iozzo R. V., Sanderson R. D. (2011). Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J. Cell. Mol. Med. 15, 1013–1031 10.1111/j.1582-4934.2010.01236.x [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  20. Jain R. K. (2005). Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307, 58–62 10.1126/science.1104819 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  21. Jih Y. J., Lien W. H., Tsai W. C., Yang G. W., Li C., Wu L. W. (2001). Distinct regulation of genes by bFGF and VEGF-A in endothelial cells. Angiogenesis 4, 313–321 10.1023/A:1016080321956 [DOI] [PubMed] [Google Scholar] · DOI
  22. Jin L., Hu W. L., Jiang C. C., Wang J. X., Han C. C., Chu P., Zhang L. J., Thorne R. F., Wilmott J., Scolyer R. A. et al. (2011). MicroRNA-149*, a p53-responsive microRNA, functions as an oncogenic regulator in human melanoma. Proc. Natl. Acad. Sci. USA 108, 15840–15845 10.1073/pnas.1019312108 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  23. Kleeff J., Ishiwata T., Kumbasar A., Friess H., Büchler M. W., Lander A. D., Korc M. (1998). The cell-surface heparan sulfate proteoglycan glypican-1 regulates growth factor action in pancreatic carcinoma cells and is overexpressed in human pancreatic cancer. J. Clin. Invest. 102, 1662–1673 10.1172/JCI4105 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  24. Kleeff J., Wildi S., Kumbasar A., Friess H., Lander A. D., Korc M. (1999). Stable transfection of a glypican-1 antisense construct decreases tumorigenicity in PANC-1 pancreatic carcinoma cells. Pancreas 19, 281–288 10.1097/00006676-199910000-00009 [DOI] [PubMed] [Google Scholar] · DOI
  25. Li D., Chen P., Li X. Y., Zhang L. Y., Xiong W., Zhou M., Xiao L., Zeng F., Li X. L., Wu M. H. et al. (2011). Grade-specific expression profiles of miRNAs/mRNAs and docking study in human grade I-III astrocytomas. OMICS 15, 673–682 10.1089/omi.2011.0064 [DOI] [PubMed] [Google Scholar] · DOI
  26. Lin R. J., Lin Y. C., Yu A. L. (2010). miR-149* induces apoptosis by inhibiting Akt1 and E2F1 in human cancer cells. Mol. Carcinog. 49, 719–727 [DOI] [PubMed] [Google Scholar]
  27. Löffler D., Brocke-Heidrich K., Pfeifer G., Stocsits C., Hackermüller J., Kretzschmar A. K., Burger R., Gramatzki M., Blumert C., Bauer K. et al. (2007). Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 110, 1330–1333 10.1182/blood-2007-03-081133 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  28. Lutter D., Marr C., Krumsiek J., Lang E. W., Theis F. J. (2010). Intronic microRNAs support their host genes by mediating synergistic and antagonistic regulatory effects. BMC Genomics 11, 224 10.1186/1471-2164-11-224 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  29. Matsuda K., Maruyama H., Guo F., Kleeff J., Itakura J., Matsumoto Y., Lander A. D., Korc M. (2001). Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Res. 61, 5562–5569 [PubMed] [Google Scholar]
  30. Megraw M., Sethupathy P., Gumireddy K., Jensen S. T., Huang Q. H., Hatzigeorgiou A. G. (2010). Isoform specific gene auto-regulation via miRNAs: a case study on miR-128b and ARPP-21. Theor. Chem. Acc. 125, 593–598 10.1007/s00214-009-0647-4 [DOI] [Google Scholar] · DOI
  31. Mi H., Dong Q., Muruganujan A., Gaudet P., Lewis S., Thomas P. D. (2010). PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res. 38, D204–D210 10.1093/nar/gkp1019 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  32. Monteys A. M., Spengler R. M., Wan J., Tecedor L., Lennox K. A., Xing Y., Davidson B. L. (2010). Structure and activity of putative intronic miRNA promoters. RNA 16, 495–505 10.1261/rna.1731910 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  33. Nikolic I., Plate K. H., Schmidt M. H. (2010). EGFL7 meets miRNA-126: an angiogenesis alliance. J. Angiogenes Res. 2, 9 10.1186/2040-2384-2-9 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  34. Okamura K., Phillips M. D., Tyler D. M., Duan H., Chou Y. T., Lai E. C. (2008). The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution. Nat. Struct. Mol. Biol. 15, 354–363 10.1038/nsmb.1409 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  35. Olsson A. K., Dimberg A., Kreuger J., Claesson-Welsh L. (2006). VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7, 359–371 10.1038/nrm1911 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  36. Øster B., Linnet L., Christensen L. L., Thorsen K., Ongen H., Dermitzakis E. T., Sandoval J., Moran S., Esteller M., Hansen T. F. et al. (2013). Non-CpG island promoter hypomethylation and miR-149 regulate the expression of SRPX2 in colorectal cancer. Int. J. Cancer 132, 2303–2315 [DOI] [PubMed] [Google Scholar]
  37. Presta M., Dell'Era P., Mitola S., Moroni E., Ronca R., Rusnati M. (2005). Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 16, 159–178 10.1016/j.cytogfr.2005.01.004 [DOI] [PubMed] [Google Scholar] · DOI
  38. Qiao D., Meyer K., Mundhenke C., Drew S. A., Friedl A. (2003). Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 signaling in brain endothelial cells. Specific role for glypican-1 in glioma angiogenesis. J. Biol. Chem. 278, 16045–16053 10.1074/jbc.M211259200 [DOI] [PubMed] [Google Scholar] · DOI
  39. Qiao D., Yang X., Meyer K., Friedl A. (2008). Glypican-1 regulates anaphase promoting complex/cyclosome substrates and cell cycle progression in endothelial cells. Mol. Biol. Cell 19, 2789–2801 10.1091/mbc.E07-10-1025 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  40. Qiao D., Meyer K., Friedl A. (2012). Glypican-1 stimulates Skp2 autoinduction loop and G1/S transition in endothelial cells. J. Biol. Chem. 287, 5898–5909 10.1074/jbc.M111.325282 [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted] · DOI
  41. Rayner K. J., Suárez Y., Dávalos A., Parathath S., Fitzgerald M. L., Tamehiro N., Fisher E. A., Moore K. J., Fernández-Hernando C. (2010). MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328, 1570–1573 10.1126/science.1189862 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  42. Reynolds L. P., Redmer D. A. (2001). Angiogenesis in the placenta. Biol. Reprod. 64, 1033–1040 10.1095/biolreprod64.4.1033 [DOI] [PubMed] [Google Scholar] · DOI
  43. Ro S., Park C., Young D., Sanders K. M., Yan W. (2007). Tissue-dependent paired expression of miRNAs. Nucleic Acids Res. 35, 5944–5953 10.1093/nar/gkm641 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  44. Sasisekharan R., Shriver Z., Venkataraman G., Narayanasami U. (2002). Roles of heparan-sulphate glycosaminoglycans in cancer. Nat. Rev. Cancer 2, 521–528 10.1038/nrc842 [DOI] [PubMed] [Google Scholar] · DOI
  45. Su G., Meyer K., Nandini C. D., Qiao D., Salamat S., Friedl A. (2006). Glypican-1 is frequently overexpressed in human gliomas and enhances FGF-2 signaling in glioma cells. Am. J. Pathol. 168, 2014–2026 10.2353/ajpath.2006.050800 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  46. Suárez Y., Sessa W. C. (2009). MicroRNAs as novel regulators of angiogenesis. Circ. Res. 104, 442–454 10.1161/CIRCRESAHA.108.191270 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  47. Suárez Y., Fernández-Hernando C., Pober J. S., Sessa W. C. (2007). Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ. Res. 100, 1164–1173 10.1161/01.RES.0000265065.26744.17 [DOI] [PubMed] [Google Scholar] · DOI
  48. Suárez Y., Fernández-Hernando C., Yu J., Gerber S. A., Harrison K. D., Pober J. S., Iruela-Arispe M. L., Merkenschlager M., Sessa W. C. (2008). Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc. Natl. Acad. Sci. USA 105, 14082–14087 10.1073/pnas.0804597105 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  49. Suárez Y., Wang C., Manes T. D., Pober J. S. (2010). Cutting edge: TNF-induced microRNAs regulate TNF-induced expression of E-selectin and intercellular adhesion molecule-1 on human endothelial cells: feedback control of inflammation. J. Immunol. 184, 21–25 10.4049/jimmunol.0902369 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  50. Suzuki H. I., Yamagata K., Sugimoto K., Iwamoto T., Kato S., Miyazono K. (2009). Modulation of microRNA processing by p53. Nature 460, 529–533 10.1038/nature08199 [DOI] [PubMed] [Google Scholar] · DOI
  51. Thum T. (2012). MicroRNA therapeutics in cardiovascular medicine. EMBO Mol. Med. 4, 3–14 10.1002/emmm.201100191 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  52. Urbich C., Kuehbacher A., Dimmeler S. (2008). Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc. Res. 79, 581–588 10.1093/cvr/cvn156 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  53. van Rooij E., Sutherland L. B., Qi X., Richardson J. A., Hill J., Olson E. N. (2007). Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316, 575–579 10.1126/science.1139089 [DOI] [PubMed] [Google Scholar] · DOI
  54. Wang S., Olson E. N. (2009). AngiomiRs – key regulators of angiogenesis. Curr. Opin. Genet. Dev. 19, 205–211 10.1016/j.gde.2009.04.002 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  55. Wang Y., Zheng X., Zhang Z., Zhou J., Zhao G., Yang J., Xia L., Wang R., Cai X., Hu H. et al. (2012). MicroRNA-149 inhibits proliferation and cell cycle progression through the targeting of ZBTB2 in human gastric cancer. PLoS ONE 7, e41693 10.1371/journal.pone.0041693 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  56. Wang F., Ma Y. L., Zhang P., Shen T. Y., Shi C. Z., Yang Y. Z., Moyer M. P., Zhang H. Z., Chen H. Q., Liang Y. et al. (2013). SP1 mediates the link between methylation of the tumour suppressor miR-149 and outcome in colorectal cancer. J. Pathol. 229, 12–24 10.1002/path.4078 [DOI] [PubMed] [Google Scholar] · DOI
  57. Yancopoulos G. D., Davis S., Gale N. W., Rudge J. S., Wiegand S. J., Holash J. (2000). Vascular-specific growth factors and blood vessel formation. Nature 407, 242–248 10.1038/35025215 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  58. Yang J. S., Phillips M. D., Betel D., Mu P., Ventura A., Siepel A. C., Chen K. C., Lai E. C. (2011). Widespread regulatory activity of vertebrate microRNA* species. RNA 17, 312–326 10.1261/rna.2537911 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  59. Zhang Z., Coomans C., David G. (2001). Membrane heparan sulfate proteoglycan-supported FGF2-FGFR1 signaling: evidence in support of the “cooperative end structures” model. J. Biol. Chem. 276, 41921–41929 10.1074/jbc.M106608200 [DOI] [PubMed] [Google Scholar] · DOI

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Authors
Chamorro-Jorganes, A., Araldi, E., Rotllan, N., Cirera-Salinas, D., & Suárez, Y.
Venue
Journal of Cell Science
Published
2014-01-01
ISSN
  • 1477-9137
  • 0021-9533
Cited by
36
References
0
Language
en

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