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Molecular and Cellular Biology, June 2004, p. 5496-5509, Vol. 24, No. 12
0270-7306/04/$08.00+0     DOI: 10.1128/MCB.24.12.5496-5509.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Coordination of Cell Signaling, Chromatin Remodeling, Histone Modifications, and Regulator Recruitment in Human Matrix Metalloproteinase 9 Gene Transcription

Zhendong Ma, Reesha C. Shah, Mi Jung Chang, and Etty N. Benveniste*

Department of Cell Biology, University of Alabama at Birmingham, Birmingham, Alabama 35294-0005

Received 1 January 2004/ Returned for modification 12 February 2004/ Accepted 19 March 2004

Transcriptional activation of eukaryotic genes depends on the precise and ordered recruitment of activators, chromatin modifiers/remodelers, coactivators, and general transcription factors to the promoters of target genes. Using the human matrix metalloproteinase 9 (MMP-9) gene as a model system, we investigated the sequential assembly and dynamic formation of transcription complexes on a human promoter under the influence of mitogen signaling. We find that, coincident with activation of the MMP-9 gene, activators, chromatin remodeling complexes, and coactivators are recruited to the preassembled MMP-9 promoter in a stepwise and coordinated order, which is dependent on activation of MEK-1/extracellular signal-regulated kinase and NF-{kappa}B signaling pathways. Conversely, corepressor complexes are released from the MMP-9 promoter after transcriptional activation. Histone modifications shift from repressive to permissive modifications concurrent with activation of the MMP-9 gene. Chromatin remodeling induced by Brg-1 is required for MMP-9 gene transcription, which is concomitant with initiation of transcription. Therefore, coordination of cell signaling, chromatin remodeling, histone modifications, and stepwise recruitment of transcription regulators is critical to precisely regulate MMP-9 gene transcription in a temporally and spatially dependent manner. Given the important role of MMP-9 in both normal development and pathological conditions, understanding MMP-9 gene regulation is of great relevance.

* Corresponding author. Mailing address: Department of Cell Biology, MCLM 395, University of Alabama at Birmingham, Birmingham, AL 35294-0005. Phone: (205) 934-7667. Fax: (205) 975-6748. E-mail: tika{at}uab.edu.

Molecular and Cellular Biology, June 2004, p. 5496-5509, Vol. 24, No. 12
0022-538X/04/$08.00+0     DOI: 10.1128/MCB.24.12.5496-5509.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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