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Molecular and Cellular Biology, March 2000, p. 2167-2175, Vol. 20, No. 6
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
The H3-H4 N-Terminal Tail Domains Are the Primary
Mediators of Transcription Factor IIIA Access to 5S DNA within
a Nucleosome
Joseph M.
Vitolo,
Christophe
Thiriet, and
Jeffrey J.
Hayes*
Department of Biochemistry and Biophysics,
University of Rochester Medical Center, Rochester, New York
Received 15 October 1999/Accepted 4 December 1999
Reconstitution of a DNA fragment containing a Xenopus
borealis somatic type 5S rRNA gene into a nucleosome greatly
restricts the binding of transcription factor IIIA (TFIIIA) to its
cognate DNA sequence within the internal promoter of the gene. Removal of all core histone tail domains by limited trypsin proteolysis or
acetylation of the core histone tails significantly relieves this
inhibition and allows TFIIIA to exhibit high-affinity binding to
nucleosomal DNA. Since only a single tail or a subset of tails may be
primarily responsible for this effect, we determined whether removal of
the individual tail domains of the H2A-H2B dimer or the H3-H4 tetramer
affects TFIIIA binding to its cognate DNA site within the 5S nucleosome
in vitro. The results show that the tail domains of H3 and H4, but not
those of H2A and/or H2B, directly modulate the ability of TFIIIA to
bind nucleosomal DNA. In vitro transcription assays carried out with
nucleosomal templates lacking individual tail domains show that
transcription efficiency parallels the binding of TFIIIA. In addition,
we show that the stoichiometry of core histones within the 5S DNA-core
histone-TFIIIA triple complex is not changed upon TFIIIA association.
Thus, TFIIIA binding occurs by displacement of H2A-H2B-DNA contacts
but without complete loss of the dimer from the nucleoprotein complex.
These data, coupled with previous reports (M. Vettese-Dadey, P. A. Grant, T. R. Hebbes, C. Crane-Robinson, C. D. Allis, and
J. L. Workman, EMBO J. 15:2508-2518, 1996; L. Howe, T. A. Ranalli, C. D. Allis, and J. Ausio, J. Biol. Chem.
273:20693-20696, 1998), suggest that the H3/H4 tails are the primary
arbiters of transcription factor access to intranucleosomal DNA.
*
Corresponding author. Mailing address: Department of
Biochemistry and Biophysics, University of Rochester Medical Center, 601 Elmwood Ave., Box 712, Rochester, NY 14642. Phone: (716) 273-4887. Fax: (716) 271-2683. E-mail:
jjhs{at}uhura.cc.rochester.edu.
Molecular and Cellular Biology, March 2000, p. 2167-2175, Vol. 20, No. 6
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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