The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development

Molecular and Cellular Biology

Volumn 29, Issue 10, 2009, Pages 2762-2776

  Katsanou, Vicky ^a   Milatos, Stavros ^a   Yiakouvaki, Anthie ^a   Sgantzis, Nikos ^a   Kotsoni, Anastasia ^a   Alexiou, Maria ^a   Harokopos, Vaggelis ^a   Aidinis, Vassilis ^a   Hemberger, Myriam ^b   Kontoyiannis, Dimitris L ^a  

^a Institute of Immunology   (Greece)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; HUR PROTEIN; MESSENGER RNA; ELAV-LIKE PROTEIN 1; MEMBRANE ANTIGEN; RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPLENIA; CELL DIFFERENTIATION; CONTROLLED STUDY; DATA ANALYSIS; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; LIMB; MORPHOGENESIS; MOUSE; NONHUMAN; OSSIFICATION; PHENOTYPE; PLACENTA; PREGNANCY; PRIORITY JOURNAL; SYNCYTIOTROPHOBLAST; TRANSGENIC MOUSE; TROPHOBLAST; VASCULARIZATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CONGENITAL MALFORMATION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; METABOLISM; MUSCULOSKELETAL SYSTEM MALFORMATION; PATHOLOGY; PRENATAL DEVELOPMENT; SPLEEN;

ANIMALS; ANTIGENS, SURFACE; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MORPHOGENESIS; MUSCULOSKELETAL ABNORMALITIES; PHENOTYPE; PLACENTA; PREGNANCY; RNA, MESSENGER; RNA-BINDING PROTEINS; SPLEEN;

EID: 66349125085     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01393-08     Document Type: Article

References (62)

1. Abdelmohsen, K., A. Lal, H. H. Kim, and M. Gorospe. 2007. Posttranscriptional orchestration of an anti-apoptotic program by HuR. Cell Cycle 6:1288-1292.
2. Abdelmohsen, K., R. Pullmann, Jr., A. Lal, H. H. Kim, S. Galban, X. Yang, J. D. Blethrow, M. Walker, J. Shubert, D. A. Gillespie, H. Furneaux, and M. Gorospe. 2007. Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol. Cell 25:543-557.
3. Anson-Cartwright, L., K. Dawson, D. Holmyard, S. J. Fisher, R. A. Lazzarini, and J. C. Cross. 2000. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 25:311-314.
4. Barreau, C., L. Paillard, and H. B. Osborne. 2006. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33:7138-7150.
5. Bell, S. E., M. J. Sanchez, O. Spasic-Boskovic, T. Santalucia, L. Gambardella, G. J. Burton, J. J. Murphy, J. D. Norton, A. R. Clark, and M. Turner. 2006. The RNA binding protein Zfp36l1 is required for normal vascularisation and post-transcriptionally regulates VEGF expression. Dev. Dyn. 235:3144-3155.
6. Bhattacharyya, S. N., and W. Filipowicz. 2007. Argonautes and company: sailing against the wind. Cell 128:1027-1028.
7. Brendolan, A., M. M. Rosado, R. Carsetti, L. Selleri, and T. N. Dear. 2007. Development and function of the mammalian spleen. Bioessays 29:166-177.
8. Brennan, C. M., I. E. Gallouzi, and J. A. Steitz. 2000. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151:1-14.
9. Brennan, C. M., and J. A. Steitz. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58:266-277.
10. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
11. Chen, F., and M. R. Capecchi. 1997. Targeted mutations in hoxa-9 and hoxb-9 reveal synergistic interactions. Dev. Biol. 181:186-196.
12. Cherry, J., V. Karschner, H. Jones, and P. H. Pekala. 2006. HuR, an RNA-binding protein, involved in the control of cellular differentiation. In Vivo 20:17-23.
13. Colnot, C. 2005. Cellular and molecular interactions regulating skeletogenesis. J. Cell Biochem. 95:688-697.
14. Cross, J. C., Z. Werb, and S. J. Fisher. 1994. Implantation and the placenta: key pieces of the development puzzle. Science 266:1508- 1518.
15. DeLaurier, A., R. Schweitzer, and M. Logan. 2006. Pitx1 determines the morphology of muscle, tendon, and bones of the hindlimb. Dev. Biol. 299:22-34.
16. Fan, X. C., and J. A. Steitz. 1998. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. USA 95:15293-15298.
17. Figueroa, A., A. Cuadrado, J. Fan, U. Atasoy, G. E. Muscat, P. Munoz-Canoves, M. Gorospe, and A. Munoz. 2003. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol. Cell. Biol. 23:4991-5004.
18. Gallouzi, I. E., and J. A. Steitz. 2001. Delineation of mRNA export pathways by the use of cell-permeable peptides. Science 294:1895-1901.
19. Goodman, F. R. 2002. Limb malformations and the human HOX genes. Am. J. Med. Genet. A 112:256-265.
20. Gouble, A., and D. Morello. 2000. Synchronous and regulated expression of two AU-binding proteins, AUF1 and HuR, throughout murine development. Oncogene 19:5377-5384.
21. Graus, F., J. Dalmou, R. Rene, M. Tora, N. Malats, J. J. Verschuuren, F. Cardenal, N. Vinolas, J. Garcia del Muro, C. Vadell, W. P. Mason, R. Rosell, J. B. Posner, and F. X. Real. 1997. Anti-Hu antibodies in patients with small-cell lung cancer: association with complete response to therapy and improved survival. J. Clin. Oncol. 15:2866-2872.
22. Gringhuis, S. I., J. J. Garcia-Vallejo, B. van het Hof, and W. van Dijk. 2005. Convergent actions of IκB kinase β and protein kinase Cδ modulate mRNA stability through phosphorylation of 14-3-3β complexed with tristetraprolin. Mol. Cell. Biol. 25:6454-6463.
23. Gustafsson, E., C. Brakebusch, K. Hietanen, and R. Fassler. 2001. Tie-1-directed expression of Cre recombinase in endothelial cells of embryoid bodies and transgenic mice. J. Cell Sci. 114:671-676.
24. Guttinger, S., P. Muhlhausser, R. Koller-Eichhorn, J. Brennecke, and U. Kutay. 2004. Transportin2 functions as importin and mediates nuclear import of HuR. Proc. Natl. Acad. Sci. USA 101:2918-2923.
25. Hayashi, S., T. Tenzen, and A. P. McMahon. 2003. Maternal inheritance of Cre activity in a Sox2Cre deleter strain. Genesis 37:51-53.
26. Hemberger, M., and J. C. Cross. 2001. Genes governing placental development. Trends Endocrinol. Metab. 12:162-168.
27. Ishikawa, T., Y. Tamai, A. M. Zorn, H. Yoshida, M. F. Seldin, S. Nishikawa, and M. M. Taketo. 2001. Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development 128:25-33.
28. Katsanou, V., O. Papadaki, S. Milatos, P. J. Blackshear, P. Anderson, G. Kollias, and D. L. Kontoyiannis. 2005. HuR as a negative posttranscriptional modulator in inflammation. Mol. Cell 19:777-789.
29. Keene, J. D. 1999. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc. Natl. Acad. Sci. USA 96:5-7.
30. Keene, J. D., and S. A. Tenenbaum. 2002. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9:1161-1167.
31. Khabar, K. S. 2005. The AU-rich transcriptome: more than interferons and cytokines, and its role in disease. J. Interferon Cytokine Res. 25:1-10.
32. Kim, H. H., K. Abdelmohsen, A. Lal, R. Pullmann, Jr., X. Yang, S. Galban, S. Srikantan, J. L. Martindale, J. Blethrow, K. M. Shokat, and M. Gorospe. 2008. Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev. 22:1804-1815.
33. King, M., J. S. Arnold, A. Shanske, and B. E. Morrow. 2006. T-genes and limb bud development. Am. J. Med. Genet. A 140:1407-1413.
34. Kullmann, M., U. Gopfert, B. Siewe, and L. Hengst. 2002. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′ UTR. Genes Dev. 16:3087-3099.
35. Lehmann, O. J., J. C. Sowden, P. Carlsson, T. Jordan, and S. S. Bhattacharya. 2003. Fox's in development and disease. Trends Genet. 19:339-344.
36. Levadoux-Martin, M., A. Gouble, B. Jegou, V. Vallet-Erdtmann, J. Auriol, P. Mercier, and D. Morello. 2003. Impaired gametogenesis in mice that overexpress the RNA-binding protein HuR. EMBO Rep. 4:394-399.
37. Li, H., S. Park, B. Kilburn, M. A. Jelinek, A. Henschen-Edman, D. W. Aswad, M. R. Stallcup, and I. A. Laird-Offringa. 2002. Lipopolysaccharide- induced methylation of HuR, an mRNA-stabilizing protein, by CARM1. Coactivator-associated arginine methyltransferase. J. Biol. Chem. 277:44623-44630.
38. Manley, G. T., P. S. Smitt, J. Dalmau, and J. B. Posner. 1995. Hu antigens: reactivity with Hu antibodies, tumor expression, and major immunogenic sites. Ann. Neurol. 38:102-110.
39. Mazan-Mamczarz, K., S. Galban, I. Lopez de Silanes, J. L. Martindale, U. Atasoy, J. D. Keene, and M. Gorospe. 2003. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. USA 100:8354-8359.
40. Mazroui, R., S. Di Marco, E. Clair, C. von Roretz, S. A. Tenenbaum, J. D. Keene, M. Saleh, and I. E. Gallouzi. 2008. Caspase-mediated cleavage of HuR in the cytoplasm contributes to pp32/PHAP-I regulation of apoptosis. J. Cell Biol. 180:113-127.
41. Monkley, S. J., S. J. Delaney, D. J. Pennisi, J. H. Christiansen, and B. J. Wainwright. 1996. Targeted disruption of the Wnt2 gene results in placentation defects. Development 122:3343-3353.
42. Mukherjee, D., M. Gao, J. P. O'Connor, R. Raijmakers, G. Pruijn, C. S. Lutz, and J. Wilusz. 2002. The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J. 21:165-174.
43. Naiche, L. A., and V. E. Papaioannou. 2003. Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 130:2681-2693.
44. Naiche, L. A., and V. E. Papaioannou. 2007. Tbx4 is not required for hindlimb identity or post-bud hindlimb outgrowth. Development 134:93-103.
45. Niswander, L. 2003. Pattern formation: old models out on a limb. Nat. Rev. Genet. 4:133-143.
46. Pullmann, R., Jr., H. H. Kim, K. Abdelmohsen, A. Lal, J. L. Martindale, X. Yang, and M. Gorospe. 2007. Analysis of turnover and translation regulatory RNA-binding protein expression through binding to cognate mRNAs. Mol. Cell. Biol. 27:6265-6278.
47. Raineri, I., D. Wegmueller, B. Gross, U. Certa, and C. Moroni. 2004. Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res. 32:1279-1288.
48. Rebane, A., A. Aab, and J. A. Steitz. 2004. Transportins 1 and 2 are redundant nuclear import factors for hnRNP A1 and HuR. RNA 10:590-599.
49. Robert, B. 2007. Bone morphogenetic protein signaling in limb outgrowth and patterning. Dev. Growth Differ. 49:455-468.
50. Rossant, J., and J. C. Cross. 2001. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2:538-548.
51. Schwenk, F., U. Baron, and K. Rajewsky. 1995. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23:5080-5081.
52. Sekine, K., H. Ohuchi, M. Fujiwara, M. Yamasaki, T. Yoshizawa, T. Sato, N. Yagishita, D. Matsui, Y. Koga, N. Itoh, and S. Kato. 1999. Fgf10 is essential for limb and lung formation. Nat. Genet. 21:138-141.
53. Stumpo, D. J., N. A. Byrd, R. S. Phillips, S. Ghosh, R. R. Maronpot, T. Castranio, E. N. Meyers, Y. Mishina, and P. J. Blackshear. 2004. Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc finger protein of the tristetraprolin family. Mol. Cell. Biol. 24:6445-6455.
54. Tanaka, M., M. Gertsenstein, J. Rossant, and A. Nagy. 1997. Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev. Biol. 190:55-65.
55. Tranchevent, L. C., R. Barriot, S. Yu, S. Van Vooren, P. Van Loo, B. Coessens, B. De Moor, S. Aerts, and Y. Moreau. 2008. ENDEAVOUR update: a web resource for gene prioritization in multiple species. Nucleic Acids Res. 36:W377-W384.
56. van der Giessen, K., S. Di-Marco, E. Clair, and I. E. Gallouzi. 2003. RNAi-mediated HuR depletion leads to the inhibition of muscle cell differentiation. J. Biol. Chem. 278:47119-47128.
57. van der Giessen, K., and I. E. Gallouzi. 2007. Involvement of transportin 2-mediated HuR import in muscle cell differentiation. Mol. Biol. Cell 18:2619-2629.
58. Verschuuren, J. J., J. Dalmau, R. Hoard, and J. B. Posner. 1997. Paraneoplastic anti-Hu serum: studies on human tumor cell lines. J. Neuroimmunol. 79:202-210.
59. Wen, F., J. A. Tynan, G. Cecena, R. Williams, J. Munera, G. Mavrothalassitis, and R. G. Oshima. 2007. Ets2 is required for trophoblast stem cell self-renewal. Dev. Biol. 312:284-299.
60. Wu, L., A. de Bruin, H. I. Saavedra, M. Starovic, A. Trimboli, Y. Yang, J. Opavska, P. Wilson, J. C. Thompson, M. C. Ostrowski, T. J. Rosol, L. A. Woollett, M. Weinstein, J. C. Cross, M. L. Robinson, and G. Leone. 2003. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421:942-947.
61. Yao, K. M., M. L. Samson, R. Reeves, and K. White. 1993. Gene elav of Drosophila melanogaster: a prototype for neuronal-specific RNA binding protein gene family that is conserved in flies and humans. J. Neurobiol. 24:723-739.
62. Zhao, Q., R. R. Behringer, and B. de Crombrugghe. 1996. Prenatal folic acid treatment suppresses acrania and meroanencephaly in mice mutant for the Cart1 homeobox gene. Nat. Genet. 13:275-283.