This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sànchez, R.
Right arrow Articles by Marzluff, W. F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sànchez, R.
Right arrow Articles by Marzluff, W. F.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, October 2002, p. 7093-7104, Vol. 22, No. 20
0270-7306/02/$04.00+0     DOI: 10.1128/MCB.22.20.7093-7104.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

The Stem-Loop Binding Protein Is Required for Efficient Translation of Histone mRNA In Vivo and In Vitro

Ricardo Sànchez and William F. Marzluff*

Program in Molecular Biology and Biotechnology, Department of Biochemistry and Biophysics, University of North Carolina, Chapel Hill, North Carolina 27599

Received 6 May 2002/ Returned for modification 9 July 2002/ Accepted 17 July 2002

Metazoan replication-dependent histone mRNAs end in a conserved stem-loop rather than in the poly(A) tail found on all other mRNAs. The 3' end of histone mRNA binds a single class of proteins, the stem-loop binding proteins (SLBP). In Xenopus, there are two SLBPs: xSLBP1, the homologue of the mammalian SLBP, which is required for processing of histone pre-mRNA, and xSLBP2, which is expressed only during oogenesis and is bound to the stored histone mRNA in Xenopus oocytes. The stem-loop is required for efficient translation of histone mRNAs and substitutes for the poly(A) tail, which is required for efficient translation of other eucaryotic mRNAs. When a rabbit reticulocyte lysate is programmed with uncapped luciferase mRNA ending in the histone stem-loop, there is a three- to sixfold increase in translation in the presence of xSLBP1 while xSLBP2 has no effect on translation. Neither SLBP affected the translation of a luciferase mRNA ending in a mutant stem-loop that does not bind SLBP. Capped luciferase mRNAs ending in the stem-loop were injected into Xenopus oocytes after overexpression of either xSLBP1 or xSLBP2. Overexpression of xSLBP1 in the oocytes stimulated translation, while overexpression of xSLBP2 reduced translation of the luciferase mRNA ending in the histone stem-loop. A small region in the N-terminal portion of xSLBP1 is required to stimulate translation both in vivo and in vitro. An MS2-human SLBP1 fusion protein can activate translation of a reporter mRNA ending in an MS2 binding site, indicating that xSLBP1 only needs to be recruited to the 3' end of the mRNA but does not need to be directly bound to the histone stem-loop to activate translation.

* Corresponding author. Mailing address: Program in Molecular Biology and Biotechnology, CB #7100, University of North Carolina, Chapel Hill, NC 27599. Phone: (919) 962-8920. Fax: (919) 966-6821. E-mail: marzluff{at}med.unc.edu.

Molecular and Cellular Biology, October 2002, p. 7093-7104, Vol. 22, No. 20
0022-538X/02/$04.00+0     DOI: 10.1128/MCB.22.20.7093-7104.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Godfrey, A. C., White, A. E., Tatomer, D. C., Marzluff, W. F., Duronio, R. J. (2009). The Drosophila U7 snRNP proteins Lsm10 and Lsm11 are required for histone pre-mRNA processing and play an essential role in development. RNA 15: 1661-1672 [Abstract] [Full Text]  
  • Sullivan, K. D., Mullen, T. E., Marzluff, W. F., Wagner, E. J. (2009). Knockdown of SLBP results in nuclear retention of histone mRNA. RNA 15: 459-472 [Abstract] [Full Text]  
  • Cakmakci, N. G., Lerner, R. S., Wagner, E. J., Zheng, L., Marzluff, W. F. (2008). SLIP1, a Factor Required for Activation of Histone mRNA Translation by the Stem-Loop Binding Protein. Mol. Cell. Biol. 28: 1182-1194 [Abstract] [Full Text]  
  • Mullen, T. E., Marzluff, W. F. (2008). Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5' to 3' and 3' to 5'. Genes Dev. 22: 50-65 [Abstract] [Full Text]  
  • Yang, X.-c., Purdy, M., Marzluff, W. F., Dominski, Z. (2006). Characterization of 3'hExo, a 3' Exonuclease Specifically Interacting with the 3' End of Histone mRNA. J. Biol. Chem. 281: 30447-30454 [Abstract] [Full Text]  
  • Townley-Tilson, W.H. D., Pendergrass, S. A., Marzluff, W. F., Whitfield, M. L. (2006). Genome-wide analysis of mRNAs bound to the histone stem-loop binding protein. RNA 12: 1853-1867 [Abstract] [Full Text]  
  • Wang, H. X., Weerasinghe, R. R., Perdue, T. D., Cakmakci, N. G., Taylor, J. P., Marzluff, W. F., Jones, A. M. (2006). A Golgi-localized Hexose Transporter Is Involved in Heterotrimeric G Protein-mediated Early Development in Arabidopsis. Mol. Biol. Cell 17: 4257-4269 [Abstract] [Full Text]  
  • Wagner, E. J., Marzluff, W. F. (2006). ZFP100, a Component of the Active U7 snRNP Limiting for Histone Pre-mRNA Processing, Is Required for Entry into S Phase.. Mol. Cell. Biol. 26: 6702-6712 [Abstract] [Full Text]  
  • Wagner, E. J., Ospina, J. K., Hu, Y., Dundr, M., Matera, A. G., Marzluff, W. F. (2006). Conserved zinc fingers mediate multiple functions of ZFP100, a U7snRNP associated protein. RNA 12: 1206-1218 [Abstract] [Full Text]  
  • GODFREY, A. C., KUPSCO, J. M., BURCH, B. D., ZIMMERMAN, R. M., DOMINSKI, Z., MARZLUFF, W. F., DURONIO, R. J. (2006). U7 snRNA mutations in Drosophila block histone pre-mRNA processing and disrupt oogenesis.. RNA 12: 396-409 [Abstract] [Full Text]  
  • Borchers, C. H., Thapar, R., Petrotchenko, E. V., Torres, M. P., Speir, J. P., Easterling, M., Dominski, Z., Marzluff, W. F. (2006). Combined top-down and bottom-up proteomics identifies a phosphorylation site in stem-loop-binding proteins that contributes to high-affinity RNA binding. Proc. Natl. Acad. Sci. USA 103: 3094-3099 [Abstract] [Full Text]  
  • Kaygun, H., Marzluff, W. F. (2005). Translation Termination Is Involved in Histone mRNA Degradation when DNA Replication Is Inhibited. Mol. Cell. Biol. 25: 6879-6888 [Abstract] [Full Text]  
  • GORGONI, B., ANDREWS, S., SCHALLER, A., SCHUMPERLI, D., GRAY, N. K., MULLER, B. (2005). The stem-loop binding protein stimulates histone translation at an early step in the initiation pathway. RNA 11: 1030-1042 [Abstract] [Full Text]  
  • Chowdhary, R., Ali, R. A., Albig, W., Doenecke, D., Bajic, V. B (2005). Promoter modeling: the case study of mammalian histone promoters. Bioinformatics 21: 2623-2628 [Abstract] [Full Text]  
  • Erkmann, J. A., Wagner, E. J., Dong, J., Zhang, Y., Kutay, U., Marzluff, W. F. (2005). Nuclear Import of the Stem-Loop Binding Protein and Localization during the Cell Cycle. Mol. Biol. Cell 16: 2960-2971 [Abstract] [Full Text]  
  • ERKMANN, J. A., SANCHEZ, R., TREICHEL, N., MARZLUFF, W. F., KUTAY, U. (2005). Nuclear export of metazoan replication-dependent histone mRNAs is dependent on RNA length and is mediated by TAP. RNA 11: 45-58 [Abstract] [Full Text]  
  • Tanaka, M., Kihara, M., Hennebold, J. D., Eppig, J. J., Viveiros, M. M., Emery, B. R., Carrell, D. T., Kirkman, N. J., Meczekalski, B., Zhou, J., Bondy, C. A., Becker, M., Schultz, R. M., Misteli, T., De La Fuente, R., King, G. J., Adashi, E. Y. (2005). H1FOO Is Coupled to the Initiation of Oocytic Growth. Biol. Reprod. 72: 135-142 [Abstract] [Full Text]  
  • Zhao, X., McKillop-Smith, S., Muller, B. (2004). The human histone gene expression regulator HBP/SLBP is required for histone and DNA synthesis, cell cycle progression and cell proliferation in mitotic cells. J. Cell Sci. 117: 6043-6051 [Abstract] [Full Text]  
  • Whitfield, M. L., Kaygun, H., Erkmann, J. A., Townley-Tilson, W. H. D., Dominski, Z., Marzluff, W. F. (2004). SLBP is associated with histone mRNA on polyribosomes as a component of the histone mRNP. Nucleic Acids Res 32: 4833-4842 [Abstract] [Full Text]  
  • Barends, S., Rudinger-Thirion, J., Florentz, C., Giege, R., Pleij, C. W. A., Kraal, B. (2004). tRNA-Like Structure Regulates Translation of Brome Mosaic Virus RNA. J. Virol. 78: 4003-4010 [Abstract] [Full Text]  
  • Sanchez, R., Marzluff, W. F. (2004). The Oligo(A) Tail on Histone mRNA Plays an Active Role in Translational Silencing of Histone mRNA during Xenopus Oogenesis. Mol. Cell. Biol. 24: 2513-2525 [Abstract] [Full Text]  
  • Lanzotti, D. J., Kupsco, J. M., Yang, X.-C., Dominski, Z., Marzluff, W. F., Duronio, R. J. (2004). Drosophila Stem-Loop Binding Protein Intracellular Localization Is Mediated by Phosphorylation and Is Required for Cell Cycle-regulated Histone mRNA Expression. Mol. Biol. Cell 15: 1112-1123 [Abstract] [Full Text]  
  • Robertson, A. J., Howard, J. T., Dominski, Z., Schnackenberg, B. J., Sumerel, J. L., McCarthy, J. J., Coffman, J. A., Marzluff, W. F. (2004). The sea urchin stem-loop-binding protein: a maternally expressed protein that probably functions in expression of multiple classes of histone mRNA. Nucleic Acids Res 32: 811-818 [Abstract] [Full Text]  
  • Ye, X., Wei, Y., Nalepa, G., Harper, J. W. (2003). The Cyclin E/Cdk2 Substrate p220NPAT Is Required for S-Phase Entry, Histone Gene Expression, and Cajal Body Maintenance in Human Somatic Cells. Mol. Cell. Biol. 23: 8586-8600 [Abstract] [Full Text]  
  • Wei, Y., Jin, J., Harper, J. W. (2003). The Cyclin E/Cdk2 Substrate and Cajal Body Component p220NPAT Activates Histone Transcription through a Novel LisH-Like Domain. Mol. Cell. Biol. 23: 3669-3680 [Abstract] [Full Text]  
  • Zheng, L., Dominski, Z., Yang, X.-C., Elms, P., Raska, C. S., Borchers, C. H., Marzluff, W. F. (2003). Phosphorylation of Stem-Loop Binding Protein (SLBP) on Two Threonines Triggers Degradation of SLBP, the Sole Cell Cycle-Regulated Factor Required for Regulation of Histone mRNA Processing, at the End of S Phase. Mol. Cell. Biol. 23: 1590-1601 [Abstract] [Full Text]  
  • Allard, P., Champigny, M. J., Skoggard, S., Erkmann, J. A., Whitfield, M. L., Marzluff, W. F., Clarke, H. J. (2002). Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo. J. Cell Sci. 115: 4577-4586 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»