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 Wang, Z.
Right arrow Articles by Kiledjian, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Wang, Z.
Right arrow Articles by Kiledjian, M.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, July 1999, p. 4552-4560, Vol. 19, No. 7
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

An mRNA Stability Complex Functions with Poly(A)-Binding Protein To Stabilize mRNA In Vitro

Zuoren Wang, Nancy Day, Panayiota Trifillis, and Megerditch Kiledjian*

Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, New Jersey 08854-8082

Received 8 February 1999/Returned for modification 8 March 1999/Accepted 7 April 1999

The stable globin mRNAs provide an ideal system for studying the mechanism governing mammalian mRNA turnover. alpha -Globin mRNA stability is dictated by sequences in the 3' untranslated region (3'UTR) which form a specific ribonucleoprotein complex (alpha -complex) whose presence correlates with mRNA stability. One of the major protein components within this complex is a family of two polycytidylate-binding proteins, alpha CP1 and alpha CP2. Using an in vitro-transcribed and polyadenylated alpha -globin 3'UTR, we have devised an in vitro mRNA decay assay which reproduces the alpha -complex-dependent mRNA stability observed in cells. Incubation of the RNA with erythroleukemia K562 cytosolic extract results in deadenylation with distinct intermediates containing a periodicity of approximately 30 nucleotides, which is consistent with the binding of poly(A)-binding protein (PABP) monomers. Disruption of the alpha -complex by sequestration of alpha CP1 and alpha CP2 enhances deadenylation and decay of the mRNA, while reconstitution of the alpha -complex stabilizes the mRNA. Similarly, PABP is also essential for the stability of mRNA in vitro, since rapid deadenylation resulted upon its depletion. An RNA-dependent interaction between alpha CP1 and alpha CP2 with PABP suggests that the alpha -complex can directly interact with PABP. Therefore, the alpha -complex is an mRNA stability complex in vitro which could function at least in part by interacting with PABP.


* Corresponding author. Mailing address: Rutgers University, Department of Cell Biology and Neuroscience, 604 Allison Rd., Piscataway, NJ 08854-8082. Phone: (732) 445-0796. Fax: (732) 445-5870. E-mail: kiledjia{at}biology.rutgers.edu.


Molecular and Cellular Biology, July 1999, p. 4552-4560, Vol. 19, No. 7
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Jiao, X., Chen, H., Chen, J., Herrup, K., Firestein, B. L., Kiledjian, M. (2009). Modulation of Neuritogenesis by a Protein Implicated in X-Linked Mental Retardation. J. Neurosci. 29: 12419-12427 [Abstract] [Full Text]  
  • Lykke-Andersen, S., Brodersen, D. E., Jensen, T. H. (2009). Origins and activities of the eukaryotic exosome. J. Cell Sci. 122: 1487-1494 [Abstract] [Full Text]  
  • Li, Y., Ho, E. S., Gunderson, S. I., Kiledjian, M. (2009). Mutational analysis of a Dcp2-binding element reveals general enhancement of decapping by 5'-end stem-loop structures. Nucleic Acids Res 37: 2227-2237 [Abstract] [Full Text]  
  • Jones, R., Baker, M. B., Weber, M., Harrison, D. G., Bao, G., Searles, C. D. (2009). Molecular beacons can assess changes in expression and 3'-polyadenylation of human eNOS mRNA. Am. J. Physiol. Cell Physiol. 296: C498-C504 [Abstract] [Full Text]  
  • Tian, M., Campagna, D. R., Langer, N., Choe, S.-K., Paw, B. H., Justice, M. J., Fleming, M. D. (2008). Rsp1 Is Indispensable for mRNA Stability during Erythroid Terminal Differentiation. ASH ANNUAL MEETING ABSTRACTS 112: 532-532 [Abstract]  
  • Du, Z., Fenn, S., Tjhen, R., James, T. L. (2008). Structure of a Construct of a Human Poly(C)-binding Protein Containing the First and Second KH Domains Reveals Insights into Its Regulatory Mechanisms. J. Biol. Chem. 283: 28757-28766 [Abstract] [Full Text]  
  • Lin, J.-Y., Li, M.-L., Huang, P.-N., Chien, K.-Y., Horng, J.-T., Shih, S.-R. (2008). Heterogeneous nuclear ribonuclear protein K interacts with the enterovirus 71 5' untranslated region and participates in virus replication. J. Gen. Virol. 89: 2540-2549 [Abstract] [Full Text]  
  • Rowlett, R. M., Chrestensen, C. A., Schroeder, M. J., Harp, M. G., Pelo, J. W., Shabanowitz, J., DeRose, R., Hunt, D. F., Sturgill, T. W., Worthington, M. T. (2008). Inhibition of tristetraprolin deadenylation by poly(A) binding protein. Am. J. Physiol. Gastrointest. Liver Physiol. 295: G421-G430 [Abstract] [Full Text]  
  • Liu, S.-W., Rajagopal, V., Patel, S. S., Kiledjian, M. (2008). Mechanistic and Kinetic Analysis of the DcpS Scavenger Decapping Enzyme. J. Biol. Chem. 283: 16427-16436 [Abstract] [Full Text]  
  • Fujimura, K., Kano, F., Murata, M. (2008). Identification of PCBP2, a facilitator of IRES-mediated translation, as a novel constituent of stress granules and processing bodies. RNA 14: 425-431 [Abstract] [Full Text]  
  • Zhang, J., Tsaprailis, G., Bowden, G. T. (2008). Nucleolin Stabilizes Bcl-XL Messenger RNA in Response to UVA Irradiation. Cancer Res. 68: 1046-1054 [Abstract] [Full Text]  
  • Li, Y., Song, M.-G., Kiledjian, M. (2008). Transcript-Specific Decapping and Regulated Stability by the Human Dcp2 Decapping Protein. Mol. Cell. Biol. 28: 939-948 [Abstract] [Full Text]  
  • Zhang, B., Morace, G., Gauss-Muller, V., Kusov, Y. (2007). Poly(A) binding protein, C-terminally truncated by the hepatitis A virus proteinase 3C, inhibits viral translation. Nucleic Acids Res 35: 5975-5984 [Abstract] [Full Text]  
  • Perera, R., Daijogo, S., Walter, B. L., Nguyen, J. H. C., Semler, B. L. (2007). Cellular Protein Modification by Poliovirus: the Two Faces of Poly(rC)-Binding Protein. J. Virol. 81: 8919-8932 [Abstract] [Full Text]  
  • Emerald, B. S., Chen, Y., Zhu, T., Zhu, Z., Lee, K.-O., Gluckman, P. D., Lobie, P. E. (2007). {alpha}CP1 Mediates Stabilization of hTERT mRNA by Autocrine Human Growth Hormone. J. Biol. Chem. 282: 680-690 [Abstract] [Full Text]  
  • Holtkamp, S., Kreiter, S., Selmi, A., Simon, P., Koslowski, M., Huber, C., Tureci, O., Sahin, U. (2006). Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells. Blood 108: 4009-4017 [Abstract] [Full Text]  
  • Searles, C. D. (2006). Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression. Am. J. Physiol. Cell Physiol. 291: C803-C816 [Abstract] [Full Text]  
  • Wang, S., Zhang, J., Theel, S., Barb, J. J., Munson, P. J., Danner, R. L. (2006). Nitric oxide activation of Erk1/2 regulates the stability and translation of mRNA transcripts containing CU-rich elements. Nucleic Acids Res 34: 3044-3056 [Abstract] [Full Text]  
  • Hosoda, N., Lejeune, F., Maquat, L. E. (2006). Evidence that Poly(A) Binding Protein C1 Binds Nuclear Pre-mRNA Poly(A) Tails. Mol. Cell. Biol. 26: 3085-3097 [Abstract] [Full Text]  
  • Jiang, Y., Xu, X.-S., Russell, J. E. (2006). A Nucleolin-Binding 3' Untranslated Region Element Stabilizes {beta}-Globin mRNA In Vivo.. Mol. Cell. Biol. 26: 2419-2429 [Abstract] [Full Text]  
  • Grudzien, E., Kalek, M., Jemielity, J., Darzynkiewicz, E., Rhoads, R. E. (2006). Differential Inhibition of mRNA Degradation Pathways by Novel Cap Analogs. J. Biol. Chem. 281: 1857-1867 [Abstract] [Full Text]  
  • Patel, G. P., Ma, S., Bag, J. (2005). The autoregulatory translational control element of poly(A)-binding protein mRNA forms a heteromeric ribonucleoprotein complex. Nucleic Acids Res 33: 7074-7089 [Abstract] [Full Text]  
  • Liu, H., Kiledjian, M. (2005). Scavenger Decapping Activity Facilitates 5' to 3' mRNA Decay. Mol. Cell. Biol. 25: 9764-9772 [Abstract] [Full Text]  
  • Weber, M., Hagedorn, C. H., Harrison, D. G., Searles, C. D. (2005). Laminar Shear Stress and 3' Polyadenylation of eNOS mRNA. Circ. Res. 96: 1161-1168 [Abstract] [Full Text]  
  • Sidiqi, M., Wilce, J. A., Vivian, J. P., Porter, C. J., Barker, A., Leedman, P. J., Wilce, M. C. J. (2005). Structure and RNA binding of the third KH domain of poly(C)-binding protein 1. Nucleic Acids Res 33: 1213-1221 [Abstract] [Full Text]  
  • Okochi, K., Suzuki, T., Inoue, J.-i., Matsuda, S., Yamamoto, T. (2005). Interaction of anti-proliferative protein Tob with poly(A)-binding protein and inducible poly(A)-binding protein: implication of Tob in translational control. GENES CELLS 10: 151-163 [Abstract] [Full Text]  
  • LIU, S.-W., JIAO, X., LIU, H., GU, M., LIMA, C. D., KILEDJIAN, M. (2004). Functional analysis of mRNA scavenger decapping enzymes. RNA 10: 1412-1422 [Abstract] [Full Text]  
  • Lindquist, J. N., Parsons, C. J., Stefanovic, B., Brenner, D. A. (2004). Regulation of {alpha}1(I) Collagen Messenger RNA Decay by Interactions with {alpha}CP at the 3'-Untranslated Region. J. Biol. Chem. 279: 23822-23829 [Abstract] [Full Text]  
  • Grosset, C., Boniface, R., Duchez, P., Solanilla, A., Cosson, B., Ripoche, J. (2004). In Vivo Studies of Translational Repression Mediated by the Granulocyte-Macrophage Colony-stimulating Factor AU-rich Element. J. Biol. Chem. 279: 13354-13362 [Abstract] [Full Text]  
  • MILONE, J., WILUSZ, J., BELLOFATTO, V. (2004). Characterization of deadenylation in trypanosome extracts and its inhibition by poly(A)-binding protein Pab1p. RNA 10: 448-457 [Abstract] [Full Text]  
  • CHEKANOVA, J. A., BELOSTOTSKY, D. A. (2003). Evidence that poly(A) binding protein has an evolutionarily conserved function in facilitating mRNA biogenesis and export. RNA 9: 1476-1490 [Abstract] [Full Text]  
  • Chkheidze, A. N., Liebhaber, S. A. (2003). A Novel Set of Nuclear Localization Signals Determine Distributions of the {alpha}CP RNA-Binding Proteins. Mol. Cell. Biol. 23: 8405-8415 [Abstract] [Full Text]  
  • Tran, H., Maurer, F., Nagamine, Y. (2003). Stabilization of Urokinase and Urokinase Receptor mRNAs by HuR Is Linked to Its Cytoplasmic Accumulation Induced by Activated Mitogen-Activated Protein Kinase-Activated Protein Kinase 2. Mol. Cell. Biol. 23: 7177-7188 [Abstract] [Full Text]  
  • PICCIRILLO, C., KHANNA, R., KILEDJIAN, M. (2003). Functional characterization of the mammalian mRNA decapping enzyme hDcp2. RNA 9: 1138-1147 [Abstract] [Full Text]  
  • Chen, C.-Y. A., Shyu, A.-B. (2003). Rapid Deadenylation Triggered by a Nonsense Codon Precedes Decay of the RNA Body in a Mammalian Cytoplasmic Nonsense-Mediated Decay Pathway. Mol. Cell. Biol. 23: 4805-4813 [Abstract] [Full Text]  
  • Waggoner, S. A., Liebhaber, S. A. (2003). Regulation of {alpha}-Globin mRNA Stability. Exp. Biol. Med. 228: 387-395 [Abstract] [Full Text]  
  • Skalweit, A., Doller, A., Huth, A., Kahne, T., Persson, P. B., Thiele, B.-J. (2003). Posttranscriptional Control of Renin Synthesis: Identification of Proteins Interacting With Renin mRNA 3'-Untranslated Region. Circ. Res. 92: 419-427 [Abstract] [Full Text]  
  • Zarudnaya, M. I., Kolomiets, I. M., Potyahaylo, A. L., Hovorun, D. M. (2003). Downstream elements of mammalian pre-mRNA polyadenylation signals: primary, secondary and higher-order structures. Nucleic Acids Res 31: 1375-1386 [Abstract] [Full Text]  
  • Kong, J., Ji, X., Liebhaber, S. A. (2003). The KH-Domain Protein {alpha}CP Has a Direct Role in mRNA Stabilization Independent of Its Cognate Binding Site. Mol. Cell. Biol. 23: 1125-1134 [Abstract] [Full Text]  
  • Ji, X., Kong, J., Liebhaber, S. A. (2003). In Vivo Association of the Stability Control Protein {alpha}CP with Actively Translating mRNAs. Mol. Cell. Biol. 23: 899-907 [Abstract] [Full Text]  
  • Walter, B. L., Parsley, T. B., Ehrenfeld, E., Semler, B. L. (2002). Distinct Poly(rC) Binding Protein KH Domain Determinants for Poliovirus Translation Initiation and Viral RNA Replication. J. Virol. 76: 12008-12022 [Abstract] [Full Text]  
  • Wang, Z., Jiao, X., Carr-Schmid, A., Kiledjian, M. (2002). From the Cover: The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc. Natl. Acad. Sci. USA 99: 12663-12668 [Abstract] [Full Text]  
  • Cosson, B., Couturier, A., Chabelskaya, S., Kiktev, D., Inge-Vechtomov, S., Philippe, M., Zhouravleva, G. (2002). Poly(A)-Binding Protein Acts in Translation Termination via Eukaryotic Release Factor 3 Interaction and Does Not Influence [PSI+] Propagation. Mol. Cell. Biol. 22: 3301-3315 [Abstract] [Full Text]  
  • Jiao, X., Trifillis, P., Kiledjian, M. (2002). Identification of Target Messenger RNA Substrates for the Murine Deleted in Azoospermia-Like RNA-Binding Protein. Biol. Reprod. 66: 475-485 [Abstract] [Full Text]  
  • Bag, J. (2001). Feedback Inhibition of Poly(A)-binding Protein mRNA Translation. A POSSIBLE MECHANISM OF TRANSLATION ARREST BY STALLED 40 S RIBOSOMAL SUBUNITS. J. Biol. Chem. 276: 47352-47360 [Abstract] [Full Text]  
  • Yu, J., Russell, J. E. (2001). Structural and Functional Analysis of an mRNP Complex That Mediates the High Stability of Human {beta}-Globin mRNA. Mol. Cell. Biol. 21: 5879-5888 [Abstract] [Full Text]  
  • Martínez-Salas, E., Ramos, R., Lafuente, E., López de Quinto, S. (2001). Functional interactions in internal translation initiation directed by viral and cellular IRES elements. J. Gen. Virol. 82: 973-984 [Full Text]  
  • Lindquist, J. N., Kauschke, S. G., Stefanovic, B., Burchardt, E. R., Brenner, D. A. (2000). Characterization of the interaction between {alpha}CP2 and the 3'-untranslated region of collagen {alpha}1(I) mRNA. Nucleic Acids Res 28: 4306-4316 [Abstract] [Full Text]  
  • Barnhart, B., Kosinski, P. A., Wang, Z., Ford, G. S., Kiledjian, M., Covey, L. R. (2000). Identification of a Complex that Binds to the CD154 3' Untranslated Region: Implications for a Role in Message Stability During T Cell Activation. J. Immunol. 165: 4478-4486 [Abstract] [Full Text]  
  • Wang, Z., Kiledjian, M. (2000). The Poly(A)-Binding Protein and an mRNA Stability Protein Jointly Regulate an Endoribonuclease Activity. Mol. Cell. Biol. 20: 6334-6341 [Abstract] [Full Text]  
  • Lindquist, J. N., Marzluff, W. F., Stefanovic, B. (2000). Fibrogenesis: III. Posttranscriptional regulation of type I collagen. Am. J. Physiol. Gastrointest. Liver Physiol. 279: G471-G476 [Abstract] [Full Text]  
  • Chkheidze, A. N., Lyakhov, D. L., Makeyev, A. V., Morales, J., Kong, J., Liebhaber, S. A. (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 alpha CP. Mol. Cell. Biol. 19: 4572-4581 [Abstract] [Full Text]  
  • Chekanova, J. A., Shaw, R. J., Wills, M. A., Belostotsky, D. A. (2000). Poly(A) Tail-dependent Exonuclease AtRrp41p from Arabidopsis thaliana Rescues 5.8 S rRNA Processing and mRNA Decay Defects of the Yeast ski6 Mutant and Is Found in an Exosome-sized Complex in Plant and Yeast Cells. J. Biol. Chem. 275: 33158-33166 [Abstract] [Full Text]  
  • Ruiz-Echevarria, M. J., Munshi, R., Tomback, J., Kinzy, T. G., Peltz, S. W. (2001). Characterization of a General Stabilizer Element That Blocks Deadenylation-dependent mRNA Decay. J. Biol. Chem. 276: 30995-31003 [Abstract] [Full Text]  
  • D'Orso, I., Frasch, A. C. C. (2001). Functionally Different AU- and G-rich cis-Elements Confer Developmentally Regulated mRNA Stability in Trypanosoma cruzi by Interaction with Specific RNA-binding Proteins. J. Biol. Chem. 276: 15783-15793 [Abstract] [Full Text]  
  • Feng, Y., Huang, H., Liao, J., Cohen, S. N. (2001). Escherichia coli Poly(A)-binding Proteins That Interact with Components of Degradosomes or Impede RNA Decay Mediated by Polynucleotide Phosphorylase and RNase E. J. Biol. Chem. 276: 31651-31656 [Abstract] [Full Text]  
  • Rodgers, N. D., Wang, Z., Kiledjian, M. (2002). Characterization and Purification of a Mammalian Endoribonuclease Specific for the alpha -Globin mRNA. J. Biol. Chem. 277: 2597-2604 [Abstract] [Full Text]  
  • Deo, R. C., Sonenberg, N., Burley, S. K. (2001). From the Cover: X-ray structure of the human hyperplastic discs protein: An ortholog of the C-terminal domain of poly(A)-binding protein. Proc. Natl. Acad. Sci. USA 98: 4414-4419 [Abstract] [Full Text]