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Volume 272, Number 43, Issue of October 24, 1997 pp. 26926-26933
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.

Novel Testis-specific Protein-DNA Interactions Activate Transcription of the Mouse Protamine 2 Gene during Spermatogenesis

(Received for publication, July 7, 1997, and in revised form, August 12, 1997)

From the Department of Biology, Tufts University, Medford, Massachusetts 02155

The mouse protamines are expressed exclusively in postmeiotic male germ cells and are crucial for the compaction of chromatin during the late stages of spermatogenesis. The temporal expression of the two mouse protamines is transcriptionally regulated in the testis. Recent studies have demonstrated that ubiquitous and testis-specific proteins bind to the promoter of the mouse protamine 2 (mP2) gene. We have performed in vitro transcription and mobility shift assays to characterize the functional significance of the protein-DNA interactions within 180 base pairs upstream of the mP2 transcription start site. Deletion and mutational analyses reveal two positive regulatory sequences for mP2 transcription at positions 59/47 and 83/72 of the mP2 promoter. The proximal element at 59/47 binds to a novel testis-specific protein we name protamine-activating factor 1 (PAF-1). PAF-1 reaches high levels in round spermatids at the time of mP2 transcription. Deletion of the 59/47 sequence results in about a 3-fold reduction of mP2 transcription in vitro. Although the PAF-1 binding site (PAF-responsive element, PAF-RE), contains the sequence GTCA present in the cAMP-responsive element and is very similar to the estrogen-responsive element, mobility shift assays revealed that neither the cAMP-responsive element modulator nor the estrogen receptor is the protein(s) binding to PAF-RE. Competition mobility shift assays reveal that the second positive regulatory element at 83/72 binds a Y-box-binding protein. Using in vitro transcription assays, a 5-fold decrease in mP2 transcription is seen when both the PAF-RE and this Y-box are deleted. These data suggest that the testis-specific PAF-1 and a Y-box-binding protein are needed to activate mP2 transcription in postmeiotic male germ cells.

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