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
Right arrow Citation Map
Services
Right arrow E-mail this article to a friend
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, September 2000, p. 6334-6341, Vol. 20, No. 17
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

The Poly(A)-Binding Protein and an mRNA Stability Protein Jointly Regulate an Endoribonuclease Activity

Zuoren Wang and Megerditch Kiledjian*

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

Received 13 April 2000/Returned for modification 10 May 2000/Accepted 13 June 2000

We previously identified a sequence-specific erythroid cell-enriched endoribonuclease (ErEN) activity involved in the turnover of the stable alpha -globin mRNA. We now demonstrate that ErEN activity is regulated by the poly(A) tail. The unadenylated alpha -globin 3' untranslated region (3'UTR) was an efficient substrate for ErEN cleavage, while the polyadenylated 3'UTR was inefficiently cleaved in an in vitro decay assay. The influence of the poly(A) tail was mediated through the poly(A)-binding protein (PABP) bound to the poly(A) tail, which can inhibit ErEN activity. ErEN cleavage of an adenylated alpha -globin 3'UTR was accentuated upon depletion of PABP from the cytosolic extract, while addition of recombinant PABP reestablished the inhibition of endoribonuclease cleavage. PABP inhibited ErEN activity indirectly through an interaction with the alpha CP mRNA stability protein. Sequestration of alpha CP resulted in an increase of ErEN cleavage activity, regardless of the polyadenylation state of the RNA. Using electrophoretic mobility shift assays, PABP was shown to enhance the binding efficiency of alpha CP to the alpha -globin 3'UTR, which in turn protected the ErEN target sequence. Conversely, the binding of PABP to the poly(A) tail was also augmented by alpha CP, implying that a stable higher-order structural network is involved in stabilization of the alpha -globin mRNA. Upon deadenylation, the interaction of PABP with alpha CP would be disrupted, rendering the alpha -globin 3'UTR more susceptible to endoribonuclease cleavage. The data demonstrated a specific role for PABP in protecting the body of an mRNA in addition to demonstrating PABP's well-characterized effect of stabilizing the poly(A) tail.

* Corresponding author. Mailing address: Rutgers University, Dept. of Cell Biology and Neuroscience, 604 Allison Rd., Piscataway, NJ 08854-8082. Phone: (732) 445-0796. Fax: (732) 445-0104. E-mail: kiledjia{at}biology.rutgers.edu.

Molecular and Cellular Biology, September 2000, p. 6334-6341, Vol. 20, No. 17
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Schwede, A., Manful, T., Jha, B. A., Helbig, C., Bercovich, N., Stewart, M., Clayton, C. (2009). The role of deadenylation in the degradation of unstable mRNAs in trypanosomes. Nucleic Acids Res 37: 5511-5528 [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]  
  • von Roretz, C., Gallouzi, I.-E. (2008). Decoding ARE-mediated decay: is microRNA part of the equation?. JCB 181: 189-194 [Abstract] [Full Text]  
  • Yang, F., Peng, Y., Murray, E. L., Otsuka, Y., Kedersha, N., Schoenberg, D. R. (2006). Polysome-Bound Endonuclease PMR1 Is Targeted to Stress Granules via Stress-Specific Binding to TIA-1. Mol. Cell. Biol. 26: 8803-8813 [Abstract] [Full Text]  
  • Sen, G. L., Blau, H. M. (2006). A brief history of RNAi: the silence of the genes. FASEB J. 20: 1293-1299 [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]  
  • Ma, S., Musa, T., Bag, J. (2006). Reduced Stability of Mitogen-activated Protein Kinase Kinase-2 mRNA and Phosphorylation of Poly(A)-binding Protein (PABP) in Cells Overexpressing PABP. J. Biol. Chem. 281: 3145-3156 [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]  
  • Zekri, L., Chebli, K., Tourriere, H., Nielsen, F. C., Hansen, T. V. O., Rami, A., Tazi, J. (2005). Control of Fetal Growth and Neonatal Survival by the RasGAP-Associated Endoribonuclease G3BP. Mol. Cell. Biol. 25: 8703-8716 [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]  
  • Ehlers, I., Horke, S., Reumann, K., Rang, A., Grosse, F., Will, H., Heise, T. (2004). Functional Characterization of the Interaction between Human La and Hepatitis B Virus RNA. J. Biol. Chem. 279: 43437-43447 [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]  
  • Melo, E. O., Dhalia, R., de Sa, C. M., Standart, N., de Melo Neto, O. P. (2003). Identification of a C-terminal Poly(A)-binding Protein (PABP)-PABP Interaction Domain: ROLE IN COOPERATIVE BINDING TO POLY(A) AND EFFICIENT CAP DISTAL TRANSLATIONAL REPRESSION. J. Biol. Chem. 278: 46357-46368 [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]  
  • Liang, T., Spence, J., Liu, L., Strother, W. N., Chang, H. W., Ellison, J. A., Lumeng, L., Li, T.-K., Foroud, T., Carr, L. G. (2003). alpha -Synuclein maps to a quantitative trait locus for alcohol preference and is differentially expressed in alcohol-preferring and -nonpreferring rats. Proc. Natl. Acad. Sci. USA 100: 4690-4695 [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]  
  • 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]  
  • Kosinski, P. A., Laughlin, J., Singh, K., Covey, L. R. (2003). A Complex Containing Polypyrimidine Tract-Binding Protein Is Involved in Regulating the Stability of CD40 Ligand (CD154) mRNA. J. Immunol. 170: 979-988 [Abstract] [Full Text]  
  • Uchida, N., Hoshino, S.-i., Imataka, H., Sonenberg, N., Katada, T. (2002). A Novel Role of the Mammalian GSPT/eRF3 Associating with Poly(A)-binding Protein in Cap/Poly(A)-dependent Translation. J. Biol. Chem. 277: 50286-50292 [Abstract] [Full Text]  
  • Zhao, M., Tang, D., Lechpammer, S., Hoffman, A., Asea, A., Stevenson, M. A., Calderwood, S. K. (2002). Double-stranded RNA-dependent Protein Kinase (pkr) Is Essential for Thermotolerance, Accumulation of HSP70, and Stabilization of ARE-containing HSP70 mRNA during Stress. J. Biol. Chem. 277: 44539-44547 [Abstract] [Full Text]  
  • Luo, Y., Goss, D. J. (2001). Homeostasis in mRNA Initiation. WHEAT GERM POLY(A)-BINDING PROTEIN LOWERS THE ACTIVATION ENERGY BARRIER TO INITIATION COMPLEX FORMATION. J. Biol. Chem. 276: 43083-43086 [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]  
  • Heise, T., Guidotti, L. G., Chisari, F. V. (2001). Characterization of Nuclear RNases That Cleave Hepatitis B Virus RNA near the La Protein Binding Site. J. Virol. 75: 6874-6883 [Abstract] [Full Text]  
  • Kozlov, G., Trempe, J.-F., Khaleghpour, K., Kahvejian, A., Ekiel, I., Gehring, K. (2001). Structure and function of the C-terminal PABC domain of human poly(A)-binding protein. Proc. Natl. Acad. Sci. USA 10.1073/pnas.071024998v1 [Abstract] [Full Text]  
  • Tang, A., Curthoys, N. P. (2001). Identification of zeta -Crystallin/NADPH:Quinone Reductase as a Renal Glutaminase mRNA pH Response Element-binding Protein. J. Biol. Chem. 276: 21375-21380 [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]  
  • Kozlov, G., Trempe, J.-F., Khaleghpour, K., Kahvejian, A., Ekiel, I., Gehring, K. (2001). From the Cover: Structure and function of the C-terminal PABC domain of human poly(A)-binding protein. Proc. Natl. Acad. Sci. USA 98: 4409-4413 [Abstract] [Full Text]  


Copyright © 2010 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»