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J. Biol. Chem., Vol. 279, Issue 12, 10855-10863, March 19, 2004

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Identification of Nucleolin as an AU-rich Element Binding Protein Involved in bcl-2 mRNA Stabilization^*

Tapas K. Sengupta, Sumita Bandyopadhyay, Daniel J. Fernandes, and Eleanor K. Spicer¶||

From the Department of Biochemistry and Molecular Biology and ^¶Department of Pharmaceutical Sciences, Medical University of South Carolina, Charleston, South Carolina 29425

bcl-2 mRNA contains an AU-rich element (ARE) that functions in regulating bcl-2 stability. Our earlier studies indicated that taxol- or okadaic acid-induced bcl-2 mRNA destabilization in HL-60 cells is associated with decreased binding of trans-acting factors to the ARE. To identify factors that play a role in the regulation of bcl-2 mRNA stability, bcl-2 ARE-binding proteins were purified from HL-60 cells. Three polypeptides of 100, 70, and 32 kDa were isolated from a bcl-2 ARE affinity matrix. Matrix-assisted laser desorption ionization mass spectroscopy analysis identified these proteins as full-length nucleolin and proteolytic fragments of nucleolin. RNA gel shifts assays indicated that recombinant nucleolin (residues 284–707) binds specifically to bcl-2 ARE RNA. In addition, recombinant nucleolin decreases the rate of decay of mRNA in HL-60 cell extracts in an ARE-dependent manner. Taxol or okadaic acid treatment of HL-60 cells results in proteolysis of nucleolin in a similar time frame as drug-induced bcl-2 mRNA down-regulation. These findings suggest that nucleolin functions as a bcl-2-stabilizing factor and that taxol and okadaic acid treatment induces apoptosis in HL-60 cells through a process that involves down-regulation of nucleolin and destabilization of bcl-2 mRNA.

Received for publication, August 18, 2003 , and in revised form, December 4, 2003.

^* This work was supported in part by development funds awarded to the Hollings Cancer Center by the United States Department of Defense and by Public Health Service Grant CA 87553 (NCI, National Institutes of Health) (to E. K. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

These authors contributed equally to this study.

^|| To whom correspondence should be addressed: Dept. of Biochemistry and Molecular Biology, Medical University of South Carolina, P. O. Box 250509, Charleston, SC 29425. Tel.: 843-792-7475; Fax: 843-792-8565; E-mail: spicer{at}musc.edu.

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