Antagonistic function of the RNA-binding protein HuR and miR-200b in post-transcriptional regulation of vascular endothelial growth factor-a expression and angiogenesis

Journal of Biological Chemistry

Volumn 288, Issue 7, 2013, Pages 4908-4921

  Chang, Sung Hee ^a   Lu, Yi Chien ^a   Li, Xi ^a   Hsieh, Wan Ying ^a   Xiong, Yuquan ^a   Ghosh, Mallika ^c   Evans, Todd ^a   Elemento, Olivier ^b   Hla, Timothy ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; EMBRYONIC VASCULAR DEVELOPMENT; POST-TRANSCRIPTIONAL; POST-TRANSCRIPTIONAL REGULATIONS; REGULATORY MECHANISM; RNA-BINDING PROTEIN; TUMOR ANGIOGENESIS; VASCULAR ENDOTHELIAL GROWTH FACTOR-A; ZEBRAFISH;

MACROPHAGES; PROTEINS;

RNA;

ARGONAUTE 2 PROTEIN; CD11B ANTIGEN; CD31 ANTIGEN; HUR PROTEIN; JAGGED1; MESSENGER RNA; MICRORNA; MICRORNA 1249; MICRORNA 126; MICRORNA 143; MICRORNA 196A; MICRORNA 199A; MICRORNA 200B; MICRORNA 3108; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN A;

3' UNTRANSLATED REGION; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BLOOD VESSEL PERMEABILITY; BONE MARROW CELL; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE CONTROL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; IN VIVO STUDY; JAGGED 1 GENE; KNOCKOUT MOUSE; MACROPHAGE; MOLECULAR DYNAMICS; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NITRIC OXIDE SYNTHASE 2 GENE; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN ENDOPEROXIDE SYNTHASE 2 GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN RNA BINDING; TUMOR GROWTH; UPREGULATION; VASCULAR CELL ADHESION MOLECULE 1 GENE; VEGF A GENE; ZEBRA FISH;

3' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD11B; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; MACROPHAGES; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PATHOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A; ZEBRAFISH;

EID: 84874027192     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.423871     Document Type: Article

References (54)

1. Keene, J. D. (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev. Genet. 8, 533-543
2. Moore, M. J. (2005) From birth to death: the complex lives of eukaryotic mRNAs. Science 309, 1514-1518
3. Shaw, G., and Kamen, R. (1986) A conserved AU sequence from the 3'-untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46, 659-667
4. Brennan, C. M., and Steitz, J. A. (2001) HuR and mRNA stability. Cell. Mol. Life Sci. 58, 266-277
5. Mukherjee, N, and Corcoran., D. L., Nusbaum, J. D., Reid, D. W., Georgiev, S., Hafner, M., Ascano, M., Jr., Tuschl, T., Ohler, U., and Keene, J. D. (2011) Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol. Cell 43, 327-339
6. Lebedeva, S., Jens, M., Theil, K., Schwanhäusser, B., Selbach, M., Landthaler, M., and Rajewsky, N. (2011) Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol. Cell 43, 340-352
7. Kishore, S., Jaskiewicz, L., Burger, L., Hausser, J., Khorshid, M., and Zavolan, M. (2011) A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nat Methods8, 559-564
8. Uren, P. J., Burns, S. C, Ruan, J., Singh, K. K., Smith, A. D., and Penalva, L. O. (2011) Genomic analyses of the RNA-binding protein Hu antigen R (HuR) identify a complex network of target genes and novel characteristics of its binding sites. J. Biol. Chem. 286, 37063-37066
9. López de Silanes, I., Zhan, M., Lal, A., Yang, X., and Gorospe, M. (2004) Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. U.S.A. 101, 2987-2992
10. Katsanou, V., Milatos, S., Yiakouvaki, A., Sgantzis, N., Kotsoni, A., Alexiou, M., Harokopos, V., Aidinis, V., Hemberger, M., and Kontoyiannis, D. L. (2009) The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development. Mol. Cell. Biol. 29, 2762-2776
11. Ghosh, M., and Aguila., H. L., Michaud, J., Ai, Y., Wu, M. T., Hemmes, A., Ristimaki, A., Guo, C, Furneaux, H., and Hla, T. (2009) Essential role of the RNA-binding protein HuR in progenitor cell survival in mice. J. Clin. Invest. 119, 3530-3543
12. Papadaki, O., Milatos, S., Grammenoudi, S., Mukherjee, N., and Keene., J. D., and Kontoyiannis, D. L. (2009) Control of thymic T cell maturation, deletion and egress by the RNA-binding protein HuR. J. Immunol. 182, 6779-6788
13. Katsanou, V., Papadaki, O., Milatos, S., Blackshear, P. J., Anderson, P., Kollias, G., and Kontoyiannis, D. L. (2005) HuR as a negative posttran-scriptional modulator in inflammation. Mol. Cell 19, 777-789
14. Yiakouvaki, A., Dimitriou, M., Karakasiliotis, I., Eftychi, C, Theocharis, S., and Kontoyiannis, D. L. (2012) Myeloid cell expression of the RNA-binding protein HuR protects mice from pathologic inflammation and colorectal carcinogenesis. J. Clin. Invest. 122, 48-61
15. 2 integrin-mediated, HuR-dependent stabilization of angiogenic factor-encoding mRNAs in inflammatory angiogenesis. Am. J. Pathol. 180, 1751-1760
16. Du, R., and Lu., K. V., Petritsch, C, Liu, P., Ganss, R., Passegué, E., Song, H., Vandenberg, S., Johnson, R. S., Werb, Z., and Bergers, G. (2008) HIF1α induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13, 206-220
17. Dvorak, H. F. (2002) Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 20, 4368-4380
18. Jain, R. K. (2003) Molecular regulation of vessel maturation. Nat. Med. 9, 685-693
19. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K. S., Powell-Braxton, L., Hillan, K. J., and Moore, M. W. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442
20. Oosthuyse, B., Moons, L., Storkebaum, E., Beck, H., Nuyens, D., Brusselmans, K., Van Dorpe, J., Hellings, P., Gorselink, M., Heymans, S., Thei-lmeier, G., Dewerchin, M., Laudenbach, V., Vermylen, P., Raat, H., Acker, T., Vleminckx, V., Van Den Bosch, L., Cashman, N., Fujisawa, H, Drost, M. R., Sciot, R., Bruyninckx, F., Hicklin, D. J., Ince, C, Gressens, P., Lupu, F., Plate, K. H, Robberecht, W., Herbert, J. M., Collen, D., and Carmeliet, P. (2001) Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat. Genet. 28, 131-138
21. Ray, P. S., Jia, J., Yao, P., Majumder, M., Hatzoglou, M., and Fox, P. L. (2009) A stress-responsive RNA switch regulates VEGF-A expression. Nature 457, 915-919
22. Levy, N. S., Chung, S., Furneaux, H, and Levy, A. P. (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273, 6417-6423
23. Claffey, K. P., Shih, S. C, Mullen, A., Dziennis, S., Cusick, J. L., Abrams, K. R., Lee, S. W., and Detmar, M. (1998) Identification of a human VPF/ VEGF 3'-untranslated region mediating hypoxia-induced mRNA stability. Mol. Biol. Cell 9, 469-481
24. Fellows, A., and Griffin., M. E., Petrella, B. L., Zhong, L., Parvin-Nejad, F. P., Fava, R., Morganelli, P., Robey, R. B., and Nichols, R. C (2012) AUF1/ hnRNP D represses expression of VEGF in macrophages. Mol. Biol. Cell 23, 1414-1422
25. Essafi-Benkhadir, K., Onesto, C, Stebe, E., Moroni, C, and Pagès, G. (2007) Tristetraprolin inhibits Ras-dependent tumor vascularization by inducing vascular endothelial growth factor mRNA degradation. Mol. Biol. Cell 18, 4648-4658
26. Jafarifar, F., Yao, P., Eswarappa, S. M., and Fox, P. L. (2011) Repression of VEGFA by CA-rich element-binding microRNAs is modulated by hnRNP L. EMBOJ. 30, 1324-1334
27. Chang, S. H., and Hla, T. (2011) Gene regulation by RNA-binding proteins and microRNAs in angiogenesis. Trends Mol. Med. 17, 650-658
28. Filipowicz, W., and 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
29. Chan, C. S., Elemento, O., and Tavazoie, S. (2005) Revealing posttran-scriptional regulatory elements through network-level conservation. PLoS Comput. Biol. 1, e69
30. Jacobsen, A., Wen, J., Marks, D. S., and Krogh, A. (2010) Signatures of RNA-binding proteins globally coupled to effective microRNA target sites. Genome Res. 20, 1010-1019
31. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I., and Filipowicz, W. (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111-1124
32. Kim, H. H, Kuwano, Y., Srikantan, S., Lee, E. K., Martindale, J. L., and Gorospe, M. (2009) HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 23, 1743-1748
33. Clausen, B. E., Burkhardt, C, Reith, W., Renkawitz, R., and Förster, I. (1999) Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8, 265-277
34. Weischenfeldt, J., and Porse, B. (2008) Bone marrow-derived macrophages (BMM): isolation and application. Cold Spring Harb. Protoc. 2008, pdb.prot5080
35. Salomonis, N., and Schlieve., C. R., Pereira, L., Wahlquist, C, Colas, A., Zambon, A. C, Vranizan, K., Spindler, M. J., Pico, A. R., Cline, M. S., Clark, T. A., Williams, A., Blume, J. E., Samal, E., Mercola, M., Merrill, B. J., and Conklin, B. R. (2010) Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc. Natl. Acad. Sci. U.S.A. 107, 10514-10519
36. Bakheet, T., and Williams., B. R., and Khabar, K. S. (2006) ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res. 34, D111-114
37. Elemento, O., Slonim, N., and Tavazoie, S. (2007) A universal framework for regulatory element discovery across all genomes and data types. Mol. Cell 28, 337-350
38. Zygmunt, T., Gay, CM., Blondelle, J., Singh, M.K., Flaherty, K.M., Means, P. C, Herwig, L., Krudewig, A., Belting, H. G., Affolter, M., Epstein, J. A., and Torres-Vázquez, J. (2011) Semaphorin-Plexin D1 signaling limits angiogenic potential via the VEGF decoy receptor sFlt1. Dev. Cell 21, 301-314
39. Avraham-Davidi, I., Ely, Y., and Pham., V. N., Castranova, D., Grunspan, M., Malkinson, G., Gibbs-Bar, L., Mayseless, O., Allmog, G., Lo, B., Warren, C. M., Chen, T. T., Ungos, J., Kidd, K., Shaw, K., Rogachev, I., Wan, W., Murphy, P. M., Farber, S. A., Carmel, L., Shelness, G. S., Iruela-Arispe, M. L., Weinstein, B. M., and Yaniv, K. (2012) ApoB-containing lipoproteins regulate angiogenesis by modulating expression of VEGF receptor 1. Nat. Med. 18, 967-973
40. Qian, B. Z., and Pollard, J. W. (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141, 39-51
41. Good, P. J. (1995) A conserved family of elav-like genes in vertebrates. Proc. Natl. Acad. Sci. U.S.A. 92, 4557-4561
42. Trabucchi, M., Briata, P., Garcia-Mayoral, M., Haase, A. D., Filipowicz, W., Ramos, A., Gherzi, R., and Rosenfeld, M. G. (2009) The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 459, 1010-1014
43. Hua, Z., Lv, Q., Ye, W., Wong, C K., Cai, G., Gu, D., Ji, Y., Zhao, C, Wang, J., Yang, B. B., and Zhang, Y. (2006) miRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One 1, e116
44. Kedde, M., and Strasser., M. J., Boldajipour, B., Oude Vrielink, J. A., Slanchev, K., le Sage, C, Nagel, R., Voorhoeve, P. M., van Duijse, J., Ørom, U. A., Lund, A. H., Perrakis, A., Raz, E., and Agami, R. (2007) RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131, 1273-1286
45. Kundu, P., and Fabian., M. R., Sonenberg, N., Bhattacharyya, S. N., and Filipowicz, W. (2012) HuR protein attenuates miRNA-mediated repression by promoting miRISC dissociation from the target RNA. Nucleic Acids Res. 40, 5088-5100
46. Lin, E. Y., and Li., J. F., Gnatovskiy, L., Deng, Y., Zhu, L., and Grzesik., D. A., Qian, H., Xue, X. N., and Pollard, J. W. (2006) Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 66, 11238-11246
47. Galbán, S., Kuwano, Y., Pullmann, R., Jr., Martindale, J. L., Kim, H. H., Lal, A., Abdelmohsen, K., Yang, X., Dang, Y., Liu, J. O., Lewis, S. M., Holcik, M., and Gorospe, M. (2008) RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1a. Mol. Cell. Biol. 28, 93-107
48. McArthur, K., Feng, B., Wu, Y., Chen, S., and Chakrabarti, S. (2011) MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes 60, 1314-1323
49. Chan, Y. C, Roy, S., Khanna, S., and Sen, C. K. (2012) Down-regulation of endothelial microRNA-200b supports cutaneous wound angiogenesis by desilencing GATA binding protein 2 and vascular endothelial growth factor receptor 2. Arterioscler. Thromb. Vasc. Biol. 32, 1372-1382
50. Chan, Y. C, Khanna, S., Roy, S., and Sen, C. K. (2011) miR-200b targets Ets-1 and is down-regulated by hypoxia to induce angiogenic response of endothelial cells. J. Biol. Chem. 286, 2047-2056
51. Takeda, Y., Mishima, Y., Fujiwara, T., Sakamoto, H., and Inoue, K. (2009) DAZL relieves miRNA-mediated repression of germ-line mRNAs by controlling poly(A) tail length in zebrafish. PLoS One 4, e7513
52. Maragkakis, M., Vergoulis, T., Alexiou, P., Reczko, M., Plomaritou, K., Gousis, M., Kourtis, K., Koziris, N., Dalamagas, T., and Hatzigeorgiou, A.G.(2011) DIANA-micro T Webserver upgradesupports Flyand Worm miRNA target prediction and bibliographic miRNA to disease association. Nucleic Acids Res. 39, W145-148
53. Westerfield, M. (1994) in The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Brachydanio rerio), 2.1 Ed., Institute of Neuroscience, University of Oregon, Eugene, OR
54. Keniry, A., Oxley, D., Monnier, P., Kyba, M., Dandolo, L., Smits, G., and Reik, W. (2012) The H19 lincRNAis a developmental reservoir of miR-675 that suppresses growth and lgf1r. Nat. Cell Biol. 14, 659-665