ELAV multimerizes on conserved AU4-6 motifs important for ewg splicing regulation

Molecular and Cellular Biology

Volumn 25, Issue 17, 2005, Pages 7580-7591

  Soller, Matthias ^a   White, Kalpana ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUR PROTEIN; MESSENGER RNA PRECURSOR; NUCLEOTIDE; RNA;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; ELECTROPHORETIC MOBILITY; INTRON; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; TRANSGENE; UNTRANSLATED REGION; WESTERN BLOTTING;

ANIMALS; AT RICH SEQUENCE; BASE SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEUROPEPTIDES; PHYLOGENY; PROTEIN BINDING; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS;

MELANOGASTER;

EID: 23844507523     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.17.7580-7591.2005     Document Type: Article

References (65)

1. Abe, R., E. Sakashita, K. Yamamoto, and H. Sakamoto. 1996. Two different RNA binding activities for the AU-rich element and the poly(A) sequence of the mouse neuronal protein mHuC. Nucleic Acids Res. 24:4895-4901.
2. Amir-Ahmady, B., P. L. Boutz, V. Markovtsov, M. L. Phillips, and D. L. Black. 2005. Exon repression by polypyrimidine tract binding protein. RNA 11:699-716.
3. Anantharaman, V., E. V. Koonin, and L. Aravind. 2002. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res. 30:1427-1464.
4. Antic, D., and J. D. Keene. 1997. Embryonic lethal abnormal visual RNA-binding proteins involved in growth, differentiation, and posttranscriptional gene expression. Am. J. Hum. Genet. 61:273-278.
5. Antic, D., and J. D. Keene. 1998. Messenger ribonucleoprotein complexes containing human ELAV proteins: interactions with cytoskeleton and translational apparatus. J. Cell Sci. 111:183-197.
6. Antic, D., N. Lu, and J. D. Keene. 1999. ELAV tumor antigen, hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes Dev. 13:449-461.
7. Aronov, S., G. Aranda, L. Behar, and I. Ginzburg. 2002. Visualization of translated tau protein in the axons of neuronal P19 cells and characterization of tau RNP granules. J. Cell Sci. 115:3817-3827.
8. Blanchette, M., and B. Chabot. 1999. Modulation of exon skipping by high-affinity hnRNP A1-binding sites and by intron elements that repress splice site utilization. EMBO J. 18:1939-1952.
9. Brennan, C. M., and J. A. Steitz. 2001. HuR and mRNA stability. Cell Mol. Life Sci. 58:266-277.
10. Burd, C. G., and G. Dreyfuss. 1994. Conserved structures and diversity of functions of RNA binding proteins. Science 265:615-621.
11. Chou, M. Y., J. G. Underwood, J. Nikolic, M. H. Luu, and D. L. Black. 2000. Multisite RNA binding and release of polypyrimidine tract binding protein during the regulation of c-src neural-specific splicing. Mol. Cell 5:949-957.
12. Conway, G., J. Wooley, T. Bibring, and W. M. LeStourgeon. 1988. Ribonucleoproteins package 700 nucleotides of pre-mRNA into a repeating array of regular particles. Mol. Cell. Biol. 8:2884-2895.
13. Damgaard, C. K., T. O. Tange, and J. Kjems. 2002. hnRNP A1 controls HIV-1 mRNA splicing through cooperative binding to intron and exon splicing silencers in the context of a conserved secondary structure. RNA 8:1401-1415.
14. Daneholt, B. 2001. Assembly and transport of a premessenger RNP particle. Proc. Natl. Acad. Sci. USA 98:7012-7017.
15. Darnell, J. C., K. B. Jensen, P. Jin, V. Brown, S. T. Warren, and R. B. Darnell. 2001. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107:489-499.
16. Dredge, B. K., and R. B. Darnell. 2003. Nova regulates GABA(A) receptor gamma2 alternative splicing via a distal downstream UCAU-rich intronic splicing enhancer. Mol. Cell. Biol. 23:4687-4700.
17. Dreyfuss, G., V. N. Kim, and N. Kataoka. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell. Biol. 3:195-205.
18. Dreyfuss, G., M. J. Matunis, S. Pinol-Roma, and C. G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
19. Ford, L. P., J. Watson, J. D. Keene, and J. Wilusz. 1999. ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system. Genes Dev. 13:188-201.
20. Gao, F. B., C. C. Carson, T. Levine, and J. D. Keene. 1994. Selection of a subset of mRNAs from combinatorial 3′ untranslated region libraries using neuronal RNA-binding protein Hel-N1. Proc. Natl. Acad. Sci. USA 91: 11207-11211.
21. Giot, L., J. S. Bader, C. Brouwer, et al. 2003. A protein interaction map of Drosophila melanogaster. Science 302:1727-1736.
22. Handa, N., O. Nureki, K. Kurimoto, I. Kim, H. Sakamoto, Y. Shimura, Y. Muto, and S. Yokoyama. 1999. Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature 398:579-585.
23. Huang, M., J. E. Rech, S. J. Northington, P. F. Flicker, A. Mayeda, A. R. Krainer, and W. M. LeStourgeon. 1994. The C-protein tetramer binds 230 to 240 nucleotides of pre-mRNA and nucleates the assembly of 40S heterogeneous nuclear ribonucleoprotein particles. Mol. Cell. Biol. 14:518-533.
24. Kambach, C., S. Walke, R. Young, J. M. Avis, E. Delafortelle, V. A. Raker, R. Luhrmann, J. Li, and K. Nagai. 1999. Crystal structure of two Sm protein complexes and their implications for the assembly of the splicosomal snRNPs. Cell 96:375-387.
25. Kasashima, K., E. Sakashita, K. Saito, and H. Sakamoto. 2002. Complex formation of the neuron-specific ELAV-like Hu RNA-binding proteins. Nucleic Acids Res. 30:4519-4526.
26. Keene, J. D., and S. A. Tenenbaum. 2002. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9:1161-1167.
27. Koushika, S. P., M. J. Lisbin, and K. White. 1996. ELAV, a Drosophila neuron-specific protein, mediates the generation of an alternatively spliced neural protein isoform. Curr. Biol. 6:1634-1641.
28. Koushika, S. P., M. Soller, S. M. DeSimone, D. M. Daub, and K. White. 1999. Differential and inefficient splicing of a broadly expressed Drosophila erect wing transcript results in tissue-specific enrichment of the vital EWG protein isoform. Mol. Cell. Biol. 19:3998-4007.
29. Koushika, S. P., M. Soller, and K. White. 2000. The neuron-enriched splicing pattern of Drosophila erect wing is dependent on the presence of ELAV protein. Mol. Cell. Biol. 20:1836-1845.
30. Krecic, A. M., and M. S. Swanson. 1999. hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11:363-371.
31. 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.
32. Levine, T. D., F. Gao, P. H. King, L. G. Andrews, and J. D. Keene. 1993. Hel-N1: an autoimmune RNA-binding protein with specificity for 3′ uridylate-rich untranslated regions of growth factor mRNAs. Mol. Cell. Biol. 13:3494-3504.
33. Levy, N. S., S. Chung, H. Furneaux, and A. P. Levy. 1998. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273:6417-6423.
34. Lisbin, M. J., J. Qiu, and K. White. 2001. The neuron-specific RNA-binding protein ELAV regulates neuroglian alternative splicing in neurons and binds directly to its pre-mRNA. Genes Dev. 15:2546-2561.
35. Lopez de Silanes, I., M. Zhan, A. Lal, X. Yang, and M. Gorospe. 2004. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. USA 101:2987-2992.
36. Loria, P. M., A. Duke, J. B. Rand, and O. Hobert. 2003. Two neuronal, nuclear-localized RNA binding proteins involved in synaptic transmission. Curr. Biol. 13:1317-1323.
37. Lothstein, L., H. P. Arenstorf, S. Y. Chung, B. W. Walker, J. C. Wooley, and W. M. LeStourgeon. 1985. General organization of protein in HeLa 40S nuclear ribonucleoprotein particles. J. Cell Biol. 100:1570-1581.
38. Markovtsov, V., J. M. Nikolic, J. A. Goldman, C. W. Turck, M. Y. Chou, and D. L. Black. 2000. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol. Cell. Biol. 20:7463-7479.
39. McAfee, J., M. Huang, S. Soltaninassab, J. Rech, S. Iyengar, and W. LeStourgeon. 1997. The packaging of pre-mRNA, p. 68-102. In A. Krainer (ed.), Eukaryatioc mRNA Processing. IRL Press at Oxford University Press, Oxford, United Kingdom.
40. Melin, L., D. Soldati, R. Mital, A. Streit, and D. Schumperli. 1992. Biochemical demonstration of complex formation of histone pre-mRNA with U7 small nuclear ribonucleoprotein and hairpin binding factors. EMBO J. 11: 691-697.
41. Oh, Y. L., B. Hahm, Y. K. Kim, H. K. Lee, J. W. Lee, O. Song, K. Tsukiyama-Kohara, M. Kohara, A. Nomoto, and S. K. Jang. 1998. Determination of functional domains in polypyrimidine-tract-binding protein. Biochem. J. 331: 169-175.
42. Okano, H. J., and R. B. Darnell. 1997. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J. Neurosci. 17:3024-3037.
43. Pascale, A., P. A. Gusev, M. Amadio, T. Dottorini, S. Govoni, D. L. Alkon, and A. Quattrone. 2004. Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc. Natl. Acad. Sci. USA 101:1217-1222.
44. Perez, I., J. G. McAfee, and J. G. Patton. 1997. Multiple RRMs contribute to RNA binding specificity and affinity for polypyrimidine tract binding protein. Biochemistry 36:11881-11890.
45. Perrone-Bizzozero, N., and F. Bolognani. 2002. Role of HuD and other RNA-binding proteins in neural development and plasticity. J. Neurosci. Res. 68:121-126.
46. Polydorides, A. D., H. J. Okano, Y. Y. Yang, G. Stefani, and R. B. Darnell. 2000. A brain-enriched polypyrimidine tract-binding protein antagonizes the ability of Nova to regulate neuron-specific alternative splicing. Proc. Natl. Acad. Sci. USA 97:6350-6355.
47. Reimann, I., A. Huth, H. Thiele, and B. J. Thiele. 2002. Suppression of 15-lipoxygenase synthesis by hnRNP E1 is dependent on repetitive nature of LOX mRNA 3′-UTR control element DICE. J. Mol. Biol. 315:965-974.
48. Robinow, S., A. R. Campos, K. M. Yao, and K. White. 1988. The elav gene product of Drosophila, required in neurons, has three RNP consensus motifs. Science 242:1570-1572. (Erratum, 243:12, 1989.)
49. Ryder, S. P., L. A. Prater, D. L. Abramovitz, E. B. Goodwin, and J. R. Williamson. 2004. RNA target specificity of the STAR/GSG domain posttranscriptional regulatory protein GLD-1. Nat. Struct. Mol. Biol. 11:20-28.
50. Samson, M. L., and F. Chalvet. 2003. Found in neurons, a third member of the Drosophila elav gene family, encodes a neuronal protein and interacts with elav. Mech. Dev. 120:373-383.
51. Shahied, L., E. H. Braswell, W. M. LeStourgeon, and A. M. Krezel. 2001. An antiparallel four-helix bundle orients the high-affinity RNA binding sites in hnRNP C: a mechanism for RNA chaperonin activity. J. Mol. Biol. 305:817-828.
52. Shamoo, Y., N. Abdul-Manan, and K. R. Williams. 1995. Multiple RNA binding domains (RBDs) just don't add up. Nucleic Acids Res. 23:725-728.
53. Simpson, P. J., T. P. Monie, A. Szendroi, N. Davydova, J. K. Tyzack, M. R. Conte, C. M. Read, P. D. Cary, D. I. Svergun, P. V. Konarev, S. Curry, and S. Matthews. 2004. Structure and RNA interactions of the N-terminal RRM domains of PTB. Structure (Cambridge) 12:1631-1643.
54. Smith, C. L., R. Afroz, G. J. Bassell, H. M. Furneaux, N. I. Perrone-Bizzozero, and R. W. Burry. 2004. GAP-43 mRNA in growth cones is associated with HuD and ribosomes. J. Neurobiol. 61:222-235.
55. Soller, M., and K. White. 2003. ELAV inhibits 3′-end processing to promote neural splicing of ewg pre-mRNA. Genes Dev. 17:2526-2538.
56. Tange, T. O., C. K. Damgaard, S. Guth, J. Valcarcel, and J. Kjems. 2001. The hnRNP A1 protein regulates HIV-1 tat splicing via a novel intron silencer element. EMBO J. 20:5748-5758.
57. Tenenbaum, S. A., C. C. Carson, P. J. Lager, and J. D. Keene. 2000. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc. Natl. Acad. Sci. USA 97:14085-14090.
58. UIe, J., K. B. Jensen, M. Ruggiu, A. Mele, A. Ule, and R. B. Darnell. 2003. CLIP identifies Nova-regulated RNA networks in the brain. Science 302: 1212-1215.
59. Varani, G., and K. Nagai. 1998. RNA recognition by RNP proteins during RNA processing. Annu. Rev. Biophys. Biomol. Struct. 27:407-445.
60. Wang, X., and T. M. Tanaka Hall. 2001. Structural basis for recognition of AU-rich element RNA by the HuD protein. Nat. Struct. Biol. 8:141-145.
61. Weighardt, F., G. Biamonti, and S. Riva. 1996. The roles of heterogeneous nuclear ribonucleoproteins (hnRNP) in RNA metabolism. Bioessays 18:747-756.
62. Yannoni, Y. M., and K. White. 1997. Association of the neuron-specific RNA binding domain-containing protein ELAV with the coiled body in Drosophila neurons. Chromosoma 105:332-341.
63. 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.
64. Yao, K. M., and K. White. 1991. Organizational analysis of elav gene and functional analysis of ELAV protein of Drosophila melanogaster and Drosophila virilis. Mol. Cell. Biol. 11:2994-3000.
65. Zhu, J., A. Mayeda, and A. R. Krainer. 2001. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol. Cell 8:1351-1361.