The 3′ untranslated region complex involved in stabilization of human α-globin mRNA assembles in the nucleus and serves an independent role as a splice enhancer

Molecular and Cellular Biology

Volumn 27, Issue 9, 2007, Pages 3290-3302

  Ji, Xinjun ^a   Kong, Jian ^a   Carstens, Russ P ^a   Liebhaber, Stephen A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GLOBIN; MESSENGER RNA; GLOBIN; PCBP2 PROTEIN, HUMAN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTRON; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SPLICING; RNA STABILITY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; REGULATORY RNA SEQUENCE; TUMOR CELL LINE;

EUKARYOTA;

3' UNTRANSLATED REGIONS; CELL LINE, TUMOR; CELL NUCLEUS; GLOBINS; HUMANS; INTRONS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA SPLICING; RNA STABILITY; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC;

EID: 34247617164     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02289-05     Document Type: Article

References (53)

1. Andersson, L. C., K. Nilsson, and C. G. Gahmberg. 1979. K562 - a human erythroleukemic cell line. Int. J. Cancer 23:143-147.
2. Black, D. L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72:291-336.
3. Blyn, L. B., J. S. Towner, B. L. Semler, and E. Ehrenfeld. 1997. Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA. J. Virol. 71:6243-6246.
4. Bourdon, V., A. Harvey, and D. M. Lonsdale. 2001. Introns and their positions affect the translational activity of mRNA in plant cells. EMBO Rep. 2:394-398.
5. Broderick, J., J. Wang, and A. Andreadis. 2004. Heterogeneous nuclear ribonucleoprotein E2 binds to tau exon 10 and moderately activates its splicing. Gene 331:107-114.
6. Carstens, R. P., W. L. McKeehan, and M. A. Garcia-Blanco. 1998. An intronic sequence element mediates both activation and repression of rat fibroblast growth factor receptor 2 pre-mRNA splicing. Mol. Cell. Biol. 18:2205-2217.
7. Chen, C. Y., N. Xu, W. Zhu, and A. B. Shyu. 2004. Functional dissection of hnRNP D suggests that nuclear import is required before hnRNP D can modulate mRNA turnover in the cytoplasm. RNA 10:669-680.
8. Chkheidze, A. N., D. L. Lyakhov, A. V. Makeyev, J. Morales, J. Kong, and S. A. Liebhaber. 1999. Assembly of the alpha-globin mRNA stability complex reflects binary interaction between the pyrimidine-rich 3′ untranslated region determinant and poly(C) binding protein αCP. Mol. Cell. Biol. 19:4572-4581.
9. Chkheidze, A. N., and S. A. Liebhaber. 2003. A novel set of nuclear localization signals determine distributions of the αCP RNA-binding proteins. Mol. Cell. Biol. 23:8405-8415.
10. Clegg, J. B., D. J. Weatherall, and P. F. Milner. 1971. Haemoglobin Constant Spring - a chain termination mutant? Nature 234:337-340.
11. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
12. Funke, B., B. Zuleger, R. Benavente, T. Schuster, M. Goller, J. Stevenin, and I. Horak. 1996. The mouse poly(C)-binding protein exists in multiple isoforms and interacts with several RNA-binding proteins. Nucleic Acids Res. 24:3821-3828.
13. Gamarnik, A., and R. Andino. 1997. Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3:882-892.
14. Gibson, T. J., J. T. Thompson, and J. Heringa. 1993. The KH domain occurs in a diverse set of RNA-binding proteins that include the antiterminator NusA and is probably involved in binding to nucleic acid. FEBS Lett. 324: 361-366.
15. Hazelrigg, T. 1998. The destinies and destinations of RNAs. Cell 95:451-460.
16. Hentze, M. W., and A. E. Kulozik. 1999. A perfect message: RNA surveillance and nonsense-mediated decay. Cell 96:307-310.
17. Holcik, M., and S. A. Liebhaber. 1997. Four highly stable eukaryotic mRNAs assemble 3′ untranslated region RNA-protein complexes sharing cis and trans components. Proc. Natl. Acad. Sci. USA 94:2410-2414.
18. Hovhannisyan, R. H., and R. P. Carstens. 2005. A novel intronic cis element, ISE/ISS-3, regulates rat fibroblast growth factor receptor 2 splicing through activation of an upstream exon and repression of a downstream exon containing a noncanonical branch point sequence. Mol. Cell. Biol. 25:250-263.
19. Jensen, K. B., B. K. Dredge, G. Stefani, R. Zhong, R. J. Buckanovich, H. J. Okano, Y. Y. Yang, and R. B. Darnell. 2000. Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25:359-371.
20. Ji, X., J. Kong, and S. A. Liebhaber. 2003. In vivo association of the stability control protein αCP with actively translating mRNAs. Mol. Cell. Biol. 23: 899-907.
21. Kim, J. H., B. Hahm, Y. K. Kim, M. Choi, and S. K. Jang. 2000. Protein-protein interaction among hnRNPs shuttling between nucleus and cytoplasm. J. Mol. Biol. 298:395-405.
22. Kong, J., X. Ji, and S. A. Liebhaber. 2003. The KH-domain protein αCP has a direct role in mRNA stabilization independent of its cognate binding site. Mol. Cell. Biol. 23:1125-1134.
23. Kong, J., M. Sumaroka, D. Eastmond, and S. A. Liebhaber. 2006. Shared stabilization functions of pyrimidine-rich determinants in the erythroid 15-lipoxygenase and α-globin mRNAs. Mol. Cell. Biol. 26:5603-5614.
24. Laig, M., M. Pape, J. Hundrieser, G. Flatz, T. Sanguansermsri, B. M. Das, R. Deka, P. Yongvanit, and N. Mularlee. 1990. The distribution of the Hb constant spring gene in Southeast Asian populations. Hum. Genet. 84:188-190.
25. Leffers, H., K. Dejgaard, and J. E. Celis. 1995. Characterisation of two major cellular poly(rC)-binding human proteins, each containing three K-homologous (KH) domains. Eur. J. Biochem. 230:447-453.
26. Le Hir, H., E. Izaurralde, L. E. Maquat, and M. J. Moore. 2000. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19:6860-6869.
27. Le Hir, H., A. Nott, and M. J. Moore. 2003. How introns influence and enhance eukaryotic gene expression. Trends Biochem. Sci. 28:215-220.
28. Lejeune, F., and L. E. Maquat. 2005. Mechanistic links between nonsense-mediated mRNA decay and pre-mRNA splicing in mammalian cells. Curr. Opin. Cell Biol. 17:309-315.
29. Liebhaber, S. A., Z. Wang, F. E. Cash, B. Monks, and J. E. Russell. 1996. Developmental silencing of the embryonic zeta-globin gene: concerted action of the promoter and the 3′-flanking region combined with stage-specific silencing by the transcribed segment. Mol. Cell. Biol. 16:2637-2646.
30. Makeyev, A. V., and S. A. Liebhaber. 2000. Identification of two novel mammalian genes establishes a subfamily of KH-domain RNA-binding proteins. Genomics 67:301-316.
31. Makeyev, A. V., and S. A. Liebhaber. 2002. The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. RNA 8:265-278.
32. Matsumoto, K., and A. P. Wolffe. 1998. Gene regulation by Y-box proteins: coupling control of transcription and translation. Trends Cell Biol. 8:318-323.
33. Mili, S., H. J. Shu, Y. Zhao, and S. Pinol-Roma. 2001. Distinct RNP complexes of shuttling hnRNP proteins with pre-mRNA and mRNA: candidate intermediates in formation and export of mRNA. Mol. Cell. Biol. 21:7307-7319.
34. Mintz, P. J., S. D. Patterson, A. F. Neuwald, C. S. Spahr, and D. L. Spector. 1999. Purification and biochemical characterization of interchromatin granule clusters. EMBO J. 18:4308-4320.
35. Moore, M. J. 2005. From birth to death: the complex lives of eukaryotic mRNAs. Science 309:1514-1518.
36. Noe, V., S. MacKenzie, and C. J. Ciudad. 2003. An intron is required for dihydrofolate reductase protein stability. J. Biol. Chem. 278:38292-38300.
37. Nott, A., H. Le Hir, and M. J. Moore. 2004. Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes Dev. 18:210-222.
38. Ostareck, D. H., A. Ostareck-Lederer, M. Wilm, B. J. Thiele, M. Mann, and M. W. Hentze. 1997. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89:597-606.
39. Ostareck-Lederer, A., D. H. Ostareck, and M. W. Hentze. 1998. Cytoplasmic regulatory functions of the KH-domain proteins hnRNPs K and E1/E2. Trends Biochem. Sci. 23:409-411.
40. Paulding, W. R., and M. F. Czyzyk-Krzeska. 1999. Regulation of tyrosine hydroxylase mRNA stability by protein-binding, pyrimidine-rich sequence in the 3′-untranslated region. J. Biol. Chem. 274:2532-2538.
41. Perrotti, D., V. Cesi, R. Trotta, C. Guerzoni, G. Santilli, K. Campbel, A. Iervolino, F. Condorelli, C. Gambacorti-Passerini, M. A. Caligiuri, and B. Calabretta. 2002. BCR-ABL suppresses C/EBPalpha expression through inhibitory action of hnRNP E2. Nat. Genet. 30:48-58.
42. Persons, D. A., and J. F. Tisdale. 2004. Gene therapy for the hemoglobin disorders. Semin. Hematol. 41:279-286.
43. Shyu, A. B., and M. F. Wilkinson. 2000. The double lives of shuttling mRNA binding proteins. Cell 102:135-138.
44. Siomi, H., M. J. Matunis, W. M. Michael, and G. Dreyfuss. 1993. The pre-mRNA binding K protein contains a novel evolutionary conserved motif. Nucleic Acids Res. 21:1193-1198.
45. Stefanovic, B., C. Hellerbrand, M. Holcik, M. Briendl, S. A. Liebhaber, and D. A. Brenner. 1997. Posttranscriptional regulation of collagen alpha1(I) mRNA in hepatic stellate cells. Mol. Cell. Biol. 17:5201-5209.
46. 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.
47. Waggoner, S. A., and S. A. Liebhaber. 2003. Regulation of alpha-globin mRNA stability. Exp. Biol. Med. 228:387-395.
48. Waggoner, S. A., and S. A. Liebhaber. 2003. Identification of mRNAs associated with αCP2-containing RNP complexes. Mol. Cell. Biol. 23:7055-7067.
49. Wagner, E. J., and M. A. Garcia-Blanco. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol. 21:3281-3288.
50. Wang, X., M. Kiledjian, I. M. Weiss, and S. A. Liebhaber. 1995. Detection and characterization of a 3′ untranslated region ribonucleoprotein complex associated with human alpha-globin mRNA stability. Mol. Cell. Biol. 15: 1769-1777.
51. Weiss, I. M., and S. A. Liebhaber. 1995. Erythroid cell-specific mRNA stability elements in the alpha 2-globin 3′ nontranslated region. Mol. Cell. Biol. 15:2457-2465.
52. Wiegand, H. L., S. Lu, and B. R. Cullen. 2003. Exon junction complexes mediate the enhancing effect of splicing on mRNA expression. Proc. Natl. Acad. Sci. USA 100:11327-11332.
53. Zhang, J., X. Sun, Y. Qian, J. P. LaDuca, and L. E. Maquat. 1998. At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol. Cell. Biol. 18:5272-5283.