MicroRNA-24 suppression of N-deacetylase/N-sulfotransferase-1 (NDST1) reduces endothelial cell responsiveness to vascular endothelial growth factor a (VEGFA)

Journal of Biological Chemistry

Volumn 288, Issue 36, 2013, Pages 25956-25963

  Kasza, Zsolt ^a   Fuchs, Peder Fredlund ^a   Tamm, Christoffer ^a   Eriksson, Anna S ^a   O'Callaghan, Paul ^a   Heindryckx, Femke ^a   Spillmann, Dorothe ^a   Larsson, Erik ^b   Le Jan, Sébastien ^a   Eriksson, Inger ^a   Gerwins, Pär ^a,c   Kjellén, Lena ^a   Kreuger, Johan ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; CORECEPTORS; HEPARAN SULFATES; MICRORNAS; PATHOPHYSIOLOGICAL; PROTEOGLYCANS; VASCULAR ENDOTHELIAL GROWTH FACTOR-A;

BIOCHEMISTRY; BIOSYNTHESIS; ENDOTHELIAL CELLS;

RNA;

HEPARAN SULFATE; HYDROLASE; MICRORNA 24; N DEACETYLASE N SULFOTRANSFERASE 1; SMALL INTERFERING RNA; SULFOTRANSFERASE; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ARTICLE; BINDING AFFINITY; CELL STIMULATION; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC REGULATION; GLYCOSAMINOGLYCAN METABOLISM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SULFATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANGIOGENESIS; BIOSYNTHESIS; HEPARAN SULFATE; MICRORNA; MIR-24; NDST1; VASCULAR ENDOTHELIAL GROWTH FACTOR (VEGF);

CHEMOTAXIS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEPARITIN SULFATE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICRORNAS; SULFOTRANSFERASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84883708784     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.484360     Document Type: Article

References (49)

1. Jakobsson, L., Kreuger, J., Holmborn, K., Lundin, L., Eriksson, I., Kjellén, L., and Claesson-Welsh, L. (2006) Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell 10, 625-634
2. Abramsson, A., Kurup, S., Busse, M., Yamada, S., Lindblom, P., Schallmeiner, E., Stenzel, D., Sauvaget, D., Ledin, J., Ringvall, M., Landegren, U., Kjellén, L., Bondjers, G., Li, J. P., Lindahl, U., Spillmann, D., Betsholtz, C., and Gerhardt, H. (2007) Defective N-sulfation of heparan sulfate proteoglycans limits PDGF-BB binding and pericyte recruitment in vascular development. Genes Dev. 21, 316-331
3. Adhikari, N., Basi, D. L., Townsend, D., Rusch, M., Mariash, A., Mullegama, S., Watson, A., Larson, J., Tan, S., Lerman, B., Esko, J. D., Selleck, S. B., and Hall, J. L. (2010) Heparan sulfate Ndst1 regulates vascular smooth muscle cell proliferation, vessel size and vascular remodeling. J. Mol. Cell. Cardiol. 49, 287-293
4. Iozzo, R. V., and San Antonio, J. D. (2001) Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J. Clin. Invest. 108, 349-355
5. Xu, D., Fuster, M. M., Lawrence, R., and Esko, J. D. (2011) Heparan sulfate regulates VEGF165- and VEGF121-mediated vascular hyperpermeability. J. Biol. Chem. 286, 737-745
6. Robinson, C. J., Mulloy, B., Gallagher, J. T., and Stringer, S. E. (2006) VEGF165-binding sites within heparan sulfate encompass two highly sulfated domains and can be liberated by K5 lyase. J. Biol. Chem. 281, 1731-1740
7. Kreuger, J., and Kjellén, L. (2012) Heparan sulfate biosynthesis: regulation and variability. J. Histochem. Cytochem. 60, 898-907
8. Grobe, K., and Esko, J. D. (2002) Regulated translation of heparan sulfate N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes by structured 5-untranslated regions and internal ribosome entry sites. J. Biol. Chem. 277, 30699-30706
9. Gallagher, J. T. (2006) Multiprotein signalling complexes: regional assembly on heparan sulphate. Biochem. Soc. Trans. 34, 438-441
10. Bushati, N., and Cohen, S. M. (2008) MicroRNAs in neurodegeneration. Curr. Opin. Neurobiol. 18, 292-296
11. Eulalio, A., Huntzinger, E., and Izaurralde, E. (2008) Getting to the root of miRNA-mediated gene silencing. Cell 132, 9-14
12. Filipowicz, W., Bhattacharyya, S. N., and Sonenberg, N. (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9, 102-114
13. Suárez, Y., Fernández-Hernando, C., Yu, J., Gerber, S. A., Harrison, K. D., Pober, J. S., Iruela-Arispe, M. L., Merkenschlager, M., and Sessa, W. C. (2008) Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 14082-14087
14. Kuehbacher, A., Urbich, C., Zeiher, A. M., and Dimmeler, S. (2007) Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ. Res. 101, 59-68
15. Harris, T. A., Yamakuchi, M., Ferlito, M., Mendell, J. T., and Lowenstein, C. J. (2008) MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule Proc. Natl. Acad. Sci. U.S.A. 105, 1516-1521
16. Wang, S., Aurora, A. B., Johnson, B. A., Qi, X., McAnally, J., Hill, J. A., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2008) The endothelial- specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev. Cell 15, 261-271
17. Wang, X., Hu, G., and Zhou, J. (2010) Repression of versican expression by microRNA-143. J. Biol. Chem. 285, 23241-23250
18. Small, E. M., Sutherland, L. B., Rajagopalan, K. N., Wang, S., and Olson, E. N. (2010) MicroRNA-218 regulates vascular patterning by modulation of Slit-Robo signaling. Circ. Res. 107, 1336-1344
19. Shi, X., Su, S., Long, J., Mei, B., and Chen, Y. (2011) MicroRNA-191 targets N-deacetylase/N-sulfotransferase 1 and promotes cell growth in human gastric carcinoma cell line MGC803. Acta Biochim. Biophys. Sin. 43, 849-856
20. Larsson, E., Fredlund Fuchs, P., Heldin, J., Barkefors, I., Bondjers, C., Genové, G., Arrondel, C., Gerwins, P., Kurschat, C., Schermer, B., Benzing, T., Harvey, S. J., Kreuger, J., and Lindahl, P. (2009) Discovery of microvascular miRNAs using public gene expression data: miR-145 is expressed in pericytes and is a regulator of Fli1. Genome Med. 1, 108
21. Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P., and Burge, C. B. (2003) Prediction of mammalian microRNA targets. Cell 115, 787-798
22. Pettersson, I., Kusche, M., Unger, E., Wlad, H., Nylund, L., Lindahl, U., and Kjellén, L. (1991) Biosynthesis of heparin: purification of a 110-kDa mouse mastocytoma protein required for both glucosaminylN-deacetylation and N-sulfation. J. Biol. Chem. 266, 8044-8049
23. Dagälv, A., Holmborn, K., Kjellén, L., and Abrink, M. (2011) Lowered expression of heparan sulfate/heparin biosynthesis enzyme N-deacetylase/ N-sulfotransferase 1 results in increased sulfation of mast cell heparin. J. Biol. Chem. 286, 44433-44440
24. Ledin, J., Staatz, W., Li, J. P., Götte, M., Selleck, S., Kjellén, L., and Spillmann, D. (2004) Heparan sulfate structure in mice with genetically modified heparan sulfate production. J. Biol. Chem. 279, 42732-42741
25. Holmborn, K., Habicher, J., Kasza, Z., Eriksson, A. S., Filipek-Gorniok, B., Gopal, S., Couchman, J. R., Ahlberg, P. E., Wiweger, M., Spillmann, D., Kreuger, J., and Ledin, J. (2012) On the roles and regulation of chondroitin sulfate and heparan sulfate in zebrafish pharyngeal cartilage morphogenesis. J. Biol. Chem. 287, 33905-33916
26. Kreuger, J., Lindahl, U., and Jemth, P. (2003) Nitrocellulose filter binding to assess binding of glycosaminoglycans to proteins. Methods Enzymol. 363, 327-339
27. Barkefors, I., Le Jan, S., Jakobsson, L., Hejll, E., Carlson, G., Johansson, H., Jarvius, J., Park, J. W., Li Jeon, N., and Kreuger, J. (2008) Endothelial cell migration in stable gradients of vascular endothelial growth factor A and fibroblast growth factor 2: effects on chemotaxis and chemokinesis. J. Biol. Chem. 283, 13905-13912
28. Barkefors, I., Fuchs, P. F., Heldin, J., Bergström, T., Forsberg-Nilsson, K., and Kreuger, J. (2011) Exocyst complex component 3-like 2 (EXOC3L2) associates with the exocyst complex and mediates directional migration of endothelial cells. J. Biol. Chem. 286, 24189-24199
29. 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-23-27-24 clusters. Proc. Natl. Acad. Sci. U.S.A. 108, 8287-8292
30. Chan, M. C., Hilyard, A. C., Wu, C., Davis, B. N., Hill, N. S., Lal, A., Lieberman, J., Lagna, G., and Hata, A. (2010) Molecular basis for antagonism between PDGF and the TGF family of signalling pathways by control of miR-24 expression. EMBO J. 29, 559-573
31. Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H., and Kim, V. N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051-4060
32. Presto, J., Thuveson, M., Carlsson, P., Busse, M., Wilén, M., Eriksson, I., Kusche-Gullberg, M., and Kjellén, L. (2008) Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation. Proc. Natl. Acad. Sci. U.S.A. 105, 4751-4756
33. Ledin, J., Ringvall, M., Thuveson, M., Eriksson, I., Wilén, M., Kusche- Gullberg, M., Forsberg, E., and Kjellén, L. (2006) Enzymatically active N-deacetylase/N-sulfotransferase-2 is present in liver but does not contribute to heparan sulfate N-sulfation. J. Biol. Chem. 281, 35727-35734
34. Le Jan, S., Hayashi, M., Kasza, Z., Eriksson, I., Bishop, J. R., Weibrecht, I., Heldin, J., Holmborn, K., Jakobsson, L., Söderberg, O., Spillmann, D., Esko, J. D., Claesson-Welsh, L., Kjellén, L., and Kreuger, J. (2012) Functional overlap between chondroitin and heparan sulfate proteoglycans during VEGF-induced sprouting angiogenesis. Arterioscler. Thromb. Vasc. Biol. 32, 1255-1263
35. Lindahl, U., and Li, J. P. (2009) Interactions between heparan sulfate and proteins-design and functional implications. Int. Rev. Cell Mol. Biol. 276, 105-159
36. Fiedler, J., Jazbutyte, V., Kirchmaier, B. C., Gupta, S. K., Lorenzen, J., Hartmann, D., Galuppo, P., Kneitz, S., Pena, J. T., Sohn-Lee, C., Loyer, X., Soutschek, J., Brand, T., Tuschl, T., Heineke, J., Martin, U., Schulte- Merker, S., Ertl, G., Engelhardt, S., Bauersachs, J., and Thum, T. (2011) MicroRNA-24 regulates vascularity after myocardial infarction. Circulation 124, 720-730
37. Pellegrini, L., Burke, D. F., von Delft, F., Mulloy, B., and Blundell, T. L. (2000) Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature 407, 1029-1034
38. Fransson, L. A., Belting, M., Cheng, F., Jönsson, M., Mani, K., and Sandgren, S. (2004) Novel aspects of glypican glycobiology. Cell. Mol. Life Sci. 61, 1016-1024
39. Zoeller, J. J., Whitelock, J. M., and Iozzo, R. V. (2009) Perlecan regulates developmental angiogenesis by modulating the VEGF-VEGFR2 axis. Matrix Biol. 28, 284-291
40. Lidholt, K., Weinke, J. L., Kiser, C. S., Lugemwa, F. N., Bame, K. J., Cheifetz, S., Massagué, J., Lindahl, U., and Esko, J. D. (1992) A single mutation affects both N-acetylglucosaminyltransferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 89, 2267-2271
41. Stickens, D., Zak, B. M., Rougier, N., Esko, J. D., and Werb, Z. (2005) Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 132, 5055-5068
42. Bengtsson, J., Eriksson, I., and Kjellén, L. (2003) Distinct effects on heparan sulfate structure by different active site mutations in NDST-1. Biochemistry 42, 2110-2115
43. van Rooij, E., Sutherland, L. B., Liu, N., Williams, A. H., McAnally, J., Gerard, R. D., Richardson, J. A., and Olson, E. N. (2006) A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc. Natl. Acad. Sci. U.S.A. 103, 18255-18260
44. Chhabra, R., Dubey, R., and Saini, N. (2010) Cooperative and individualistic functions of the microRNAs in the miR-23a-27a-24-2 cluster and its implication in human diseases. Mol. Cancer 9, 232
45. Calin, G. A., Ferracin, M., Cimmino, A., Di Leva, G., Shimizu, M., Wojcik, S. E., Iorio, M. V., Visone, R., Sever, N. I., Fabbri, M., Iuliano, R., Palumbo, T., Pichiorri, F., Roldo, C., Garzon, R., Sevignani, C., Rassenti, L., Alder, H., Volinia, S., Liu, C. G., Kipps, T. J., Negrini, M., and Croce, C. M. (2005) A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353, 1793-1801
46. Szczyrba, J., Löprich, E., Wach, S., Jung, V., Unteregger, G., Barth, S., Grobholz, R., Wieland, W., Stöhr, R., Hartmann, A., Wullich, B., and Grässer, F. (2010) The microRNA profile of prostate carcinoma obtained by deep sequencing. Mol. Cancer Res. 8, 529-538
47. Cancer Genome Atlas Network (2012) Comprehensive molecular portraits of human breast tumours. Nature 490, 61-70
48. Cancer Genome Atlas Research Network (2011) Integrated genomic analyses of ovarian carcinoma. Nature 474, 609-615
49. Fuster, M. M., Wang, L., Castagnola, J., Sikora, L., Reddi, K., Lee, P. H., Radek, K. A., Schuksz, M., Bishop, J. R., Gallo, R. L., Sriramarao, P., and Esko, J. D. (2007) Genetic alteration of endothelial heparan sulfate selectively inhibits tumor angiogenesis. J. Cell Biol. 177, 539-549