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Papers In Press, published online ahead of print June 30, 2000
J. Biol. Chem, 10.1074/jbc.M909467199
Submitted on November 30, 1999
Accepted on June 30, 2000

Role of Smad proteins and transcription factor Sp1 in p21WAF-1/Cip-1 regulation by transforming growth factor-beta

Katerina Pardali, Akira Kurisaki, Anita Moren, Peter ten Dijke, Dimitris Kardassis, and Aristidis Moustakas

Ludwig Institute for Cancer Research, Uppsala SE-751 24

Corresponding Author: aris.moustakas{at}licr.uu.se

Transforming growth factor-beta (TGF-beta ) inhibits cell cycle progression, in part through upregulation of gene expression of the p21WAF1/Cip1 (p21) cell cycle inhibitor. Previously we have reported that the intracellular effectors of TGF-beta , Smad3 and Smad4, functionally cooperate with Sp1 to activate the human p21 promoter in hepatoma HepG2 cells. In this study we show that Smad3 and Smad4 when overexpressed in HaCaT keratinocytes, lead to activation of the p21 promoter. Activation requires the binding sites for the ubiquitous transcription factor Sp1 on the proximal promoter. Induction of the endogenous HaCaT p21 gene by TGF-beta 1 is further enhanced after overexpression of Smad3 and Smad4, whereas dominant negative mutants of Smad3 and Smad4 and the inhibitory Smad7 all inhibit p21 induction by TGF-beta 1 in a dose dependent manner. We show that Sp1 expressed in the Sp1-deficient Drosophila SL 2 cells binds to the proximal p21 promoter sequences whereas Smad proteins do not. In support of this finding, we show that DNA-binding domain mutants of Smad3 and Smad4 are capable of transactivating the p21 promoter as efficiently as wild type Smads. Co-expression of Smad3 with Smad4 and Sp1 in SL-2 cells or co-incubation of phosphorylated Smad3, Smad4 and Sp1 in vitro results in enhanced binding of Sp1 to the p21 proximal promoter sequences. We demonstrate that Sp1 physically and directly interacts with Smad2, Smad3 and weakly with Smad4 via their amino-terminal (Mad-Homology 1) domain. Finally, using GAL4 fusion proteins we show that the glutamine-rich sequences in the transactivation domain of Sp1 contribute to the cooperativity with Smad proteins. In conclusion, Smad proteins play important roles in regulation of the p21 gene by TGF-beta and the functional cooperation of Smad proteins with Sp1 involves the physical interaction of these two types of transcription factors.


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