©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
The Interaction of TFIIIA with Specific RNA-DNA Heteroduplexes (*)

(Received for publication, July 10, 1995; and in revised form, August 1, 1995)

Karl P. Nightingale Alan P. Wolffe (§)

From the Laboratory of Molecular Embryology, NICHD, National Institutes of Health, Bethesda, Maryland 20892-2710

ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
FOOTNOTES
REFERENCES

ABSTRACT

We examine the association of transcription factor TFIIIA with RNA-DNA heteroduplexes containing sequences from the Xenopus borealis 5 S rRNA gene. Under conditions where TFIIIA selectively binds to 5 S rRNA or the internal control region of the 5 S rRNA gene, no specific association of TFIIIA with DNA-RNA heteroduplexes containing either strand of 5 S DNA could be detected. We discuss our results with respect to specific models of TFIIIA recognition of the internal control region and of DNA-RNA hybrids by zinc finger proteins.


INTRODUCTION

TFIIIA is a positive transcription factor for the 5 S ribosomal RNA gene (Engelke et al., 1980; Pelham and Brown, 1980). The protein has a modular structure comprised of nine zinc finger domains (Hanas et al., 1983; Smith et al., 1984; Ginsberg et al., 1984; Miller et al., 1985) that are linked to a carboxyl-terminal domain that interacts with other transcription factors (Hayes et al., 1989; Mao and Darby, 1993). The nine zinc fingers bind as a linear array along the internal control region (ICR) (^1)of the 5 S rRNA gene (Smith et al., 1984; Vrana et al., 1988). The exact mode of interaction of the zinc fingers with the ICR has been controversial (Fairall et al., 1992; Fairall and Rhodes, 1992). A feature of early models was the suggestion that A-type DNA could be involved in TFIIIA binding (Rhodes and Klug, 1986; Fairall et al., 1989). Other experiments suggested that TFIIIA recognizes B-type DNA (Gottesfeld et al., 1987; Hayes et al., 1990). In addition, the path of DNA is known to be distorted through interaction with TFIIIA (Schroth et al., 1989; Bazett-Jones and Brown, 1989). The solution of the crystal structure of the zinc finger protein Zif 268 indicated that zinc finger proteins of the TFIIIA class can interact with a B-type helix (Pavletich and Pabo, 1991; Nekludova and Pabo, 1994). However, the contacts made with the double helix by Zif 268 are predominantly to a single strand of the helix. It has recently been suggested that a combination of an A-type DNA structure and predominant recognition of a single strand of the double helix might allow TFIIIA to bind in a sequence-selective manner to a DNA-RNA heteroduplex (Shi and Berg, 1995).

Gottesfeld and colleagues have clearly established that distinct clusters of zinc fingers within TFIIIA have different affinities for DNA sequences compared with RNA sequences (Liao et al., 1992; Clemens et al., 1993, 1994; McBryant et al., 1995). These studies indicate that TFIIIA utilizes distinct domains to confer specificity to the interaction with 5 S DNA and 5 S RNA; however, all zinc finger domains contribute to the stability of association with nucleic acid. Other experiments that examine the interaction of TFIIIA with 5 S rRNA are consistent with the protein recognizing RNA through different mechanisms than the recognition of DNA (Darby and Joho, 1992; Theunissen et al., 1992; Romaniuk et al., 1987; You et al., 1991; Sands and Bogenhagen, 1987, 1991). Since TFIIIA can recognize both DNA and RNA with sequence selectivity it is possible that TFIIIA might recognize RNA-DNA heteroduplexes with comparable sequence selectivity.

In this work we directly examine the interaction of TFIIIA with DNA-RNA heteroduplexes containing either strand of the 5 S rRNA gene as DNA. In contrast with earlier speculations (Rhodes and Klug, 1986; Fairall et al., 1989; Shi and Berg, 1995), we find that TFIIIA does not have sequence-selective interactions with these specific RNA-DNA heteroduplexes under the same conditions that it selectively binds to 5 S rRNA or the 5 S rRNA gene.


MATERIALS AND METHODS

Preparation of RNA-DNA Heteroduplex

RNA-DNA heteroduplexes containing either the ``sense'' or ``antisense'' RNA strand were prepared by initial generation of the appropriate RNA from EcoRI-digested pXP14 and pXP10 plasmids, respectively (Wolffe et al., 1986). These plasmids contain a single copy of the Xenopus 5 S rRNA gene oriented next to a SP6 polymerase promoter such that in vitro transcription generates antisense 5 S rRNA from pXP10 and sense 5 S rRNA from pXP14. Briefly, RNA was produced by incubation of 5 µg of EcoRI-digested plasmid with 10 mM dithiothreitol, 0.5 mM NTPs (Pharmacia Biotech Inc.), 50 units of human placental ribonuclease inhibitor (Life Technologies, Inc.), and 20 units of SP6 RNA polymerase (Promega) in a total volume of 100 µl. A 1-h incubation at 42 °C typically generated 3 µg of RNA. The DNA template was then removed by addition of 2 units of RNase-free DNase I (Promega) and incubated for 10 min at 37 °C, and the sample was subsequently phenol/chloroform-extracted and precipitated. The RNA was annealed to 1 µg of an appropriate 5`-labeled 20-mer primer (pXP10, 5`-CGGGATCCGGCTGGGCCCCC-3`; pXP14, 5`-CGGGATCCATCTGTTCGGGG-3`) by resuspension in 50 mM KCl, 25 mM Hepes, pH 7.5, and heating to 90 °C followed by slow cooling to 50 °C over an hour. Following precipitation the primer was extended using reverse transcriptase (Life Technologies, Inc.) at 42 °C for 60 min. After phenol/chloroform extraction and precipitation, the DNA-RNA heteroduplex was separated and eluted from 6% native polyacrylamide gels.

Purification of TFIIIA

7 S storage particles and TFIIIA were purified as described by Smith et al.(1984). In brief, immature ovary homogenate was fractionated on glycerol gradients, bound to diethylaminoethyl cellulose, and eluted on a salt gradient. The 7 S particle fractions were adjusted to 0.1 M KCl in 50 mM HEPES (pH 7.5), 5 mM MgCl(2), 1 mM dithiothreitol, 10 µM ZnCl(2), 20% glycerol (buffer A). RNase A was added to the mixture (50 µg of enzyme/mg of protein), which was incubated for 5 min, and then the volume was brought up 2-fold with buffer A containing 10 M urea (to a final urea concentration of 5 M). The mixture was then loaded onto a 2-ml (bed volume) Bio-Rex 70 column, and TFIIIA was eluted with an increasing concentration of KCl (the protein eluting at a final concentration of 1 M). No other proteins were detectable by SDS-polyacrylamide gel electrophoresis and silver staining.

TFIIIA Gel Shifts

TFIIIA gel shifts were performed as described previously (Lee et al., 1993). Briefly, 5 ng of end-labeled heteroduplex, DNA, or RNA was incubated with 5-120 ng of TFIIIA in a total volume of 10 µl of binding buffer (20 mM Hepes, pH 7.5, 70 mM NH(4)Cl, 7 mM MgCl(2), 10 µM ZnCl(2), 10 mM dithiothreitol, 3% (v/v) glycerol, 20 µg/ml bovine serum albumin). Reactions were incubated at room temperature for 15 min and loaded directly onto 0.8% agarose gels in 0.5 TB buffer (45 mM Tris borate, pH 8.0) with applied voltage of 4 V/cm for 3 h at room temperature. EDTA was omitted in all binding and electrophoresis buffers to avoid denaturing TFIIIA. In the competition studies, 5 ng of end-labeled heteroduplex and 15 ng of TFIIIA was co-incubated with either 5-2500 ng of EcoRI-HindIII fragment from pXP10 (``specific DNA'') or pBR322 (``nonspecific DNA'') and allowed to equilibrate for 15 min prior to loading onto agarose gels. The experiments examining TFIIIA binding to DNA or RNA utilized an identical protocol for either a 298-bp EcoRI-HindIII DNA fragment from pXP10 or in vitro transcribed 5 S rRNA.

DNase I Footprinting

TFIIIA complexes with either DNA or heteroduplex were digested with DNase I prior to separation on 0.8% agarose gels. The approximate concentration of DNase I (Boehringer Mannheim) was determined empirically and performed at room temperature for 4 min prior to direct loading onto the gel. After electrophoresis the wet gel is placed on x-ray film, and the nucleoprotein complexes of interest excised and eluted. Following phenol/chloroform extraction and precipitation the samples are resuspended in formamide buffer and resolved on 8% denaturing acrylamide gels.


RESULTS

Experimental Strategy

We prepared heteroduplexes by initially transcribing linearized DNA templates using bacteriophage SP6 RNA polymerase to generate RNA molecules of 298 nucleotides (Wolffe et al., 1986). These single-stranded RNA molecules were annealed to DNA oligonucleotides near their 3` termini, which were then extended by reverse transcriptase to generate RNA-DNA heteroduplexes of 285 bp in length, which were purified on non-denaturing polyacrylamide gels (Fig. 1). Where necessary RNA or DNA were radiolabeled either by the inclusion of radioactive RNA precursors during transcription by SP6 RNA polymerase or by end labeling of the oligonucleotide, respectively.


Figure 1: Preparation of ``sense'' or ``antisense'' RNA-DNA heteroduplexes containing the Xenopus 5 S rRNA gene sequence. The scheme illustrates the organization of the plasmid pXP10, where the arrowedregion represents the 5 S rRNA gene and the hatchedarea the ICR to which TFIIIA binds. The alternative construct used shows pXP14 contains the same 5 S rRNA sequence, but it is inverted (Wolffe et al., 1986). The arrow at 1 indicates the start of the SP6 polymerase transcript.



TFIIIA Binds to 5 S rRNA, 5 S DNA, and to Both 5 S RNA-DNA Heteroduplexes

We initially established conditions under which the interaction of TFIIIA with 5 S rRNA, 5 S DNA, and 5 S RNA-DNA heteroduplexes could be detected by a gel retardation assay (Lee et al., 1993). An increasing excess of TFIIIA relative to 5 S DNA led to the accumulation of a single complex and then multiple complexes until an aggregate appears (Fig. 2A, lanes 1-6). This reflects the initial association of a single molecule of TFIIIA with the internal control region (Smith et al., 1984; see Fig. 5later), followed by the nonspecific sequestration of additional TFIIIA molecules (Daly and Wu, 1989). Similar results are obtained on analysis of TFIIIA binding to 5 S rRNA (Fig. 2A, lanes 7-12) (see also Romaniuk et al.(1987), Sands and Bogenhagen(1987), Darby and Joho(1992), and Clemens et al. (1993)). It should be noted that the higher order complexes observed with both 5 S DNA and 5 S RNA at high TFIIIA concentrations could have been eliminated by the inclusion of additional nonspecific competitor DNA in the binding reactions (not shown). Under these binding conditions, the stable association of TFIIIA with RNA-DNA heteroduplexes containing either strand of the 5 S rRNA gene as DNA could be detected (Fig. 2B, lanes 1-10). A single complex appears followed by other complexes that are increasingly retarded in their mobility through the gel. We conclude that TFIIIA will bind to RNA-DNA heteroduplexes containing 5 S DNA and RNA sequences. We next examined the specificity of this interaction.


Figure 2: Gel retardation assays showing TFIIIA binding to both DNA-RNA heteroduplexes and to DNA and 5 S rRNA. A, DNA and 5 S rRNA. TFIIIA binding to a 298-bp fragment of the Xenopus 5 S rRNA gene (DNA, lanes 1-6) or to 5 S rRNA (RNA, lanes 7-12) is shown. 5 ng of end-labeled nucleic acid (lanes1 and 7) was incubated with 0.15 ng (lanes2 and 8), 0.3 ng (lanes3 and 9), 0.6 ng (lanes4 and 10), 1.2 ng (lanes5 and 11), and 2.4 ng (lanes6 and 12) of TFIIIA. Complexes were resolved on a 0.7% agarose gel. The resolution of free nucleic acid (Free) and the binding of single (1) or multiple TFIIIA molecules (2, 3) to the fragments is indicated, as are the generation of nucleoprotein aggregates. B, DNA-RNA heteroduplex. 5 ng of ``sense'' (XP14) (lanes1-5) or ``antisense'' (XP10) (lanes 6-10) RNA-DNA heteroduplex (lanes1 and 6) was incubated with 15 ng (lanes2 and 7), 30 ng (lanes3 and 8), 60 ng (lanes4 and 9), and 120 ng (lanes5 and 10) of TFIIIA.




Figure 5: Footprinting analysis of TFIIIA binding to both DNA-RNA heteroduplexes and to DNA. A, TFIIIA binding to 5` end-labeled ``sense'' (XP14) and ``antisense'' (XP10) heteroduplexes was analyzed by DNase I digestion as described under ``Materials and Methods.'' The lanes are labeled as follows: lanes2 and 6, DNase I digestion of free heteroduplex; lanes3 and 4 or 7 and 8, digestion of heteroduplex with one and two TFIIIA molecules bound to the fragment, respectively. Lanes1 and 2 show labeled G cleared fragments in a Maxam-Gilbert G ladder. B, TFIIIA binding to double-stranded DNA of the same sequence present in the heteroduplexes. The lanes are labeled as follows: -, DNase I digestion of free DNA (lanes10 and 13); +, DNase I digestion of the same fragment bound by a single TFIIIA molecule (lanes11 and 14). Lanes9 and 12 are of labeled G cleared fragments in a Maxam-Gilbert G ladder. The position of the ICR is indicated.



TFIIIA Binds to 5 S RNA-DNA Heteroduplexes Nonspecifically

We examine the nature of TFIIIA association with 5 S RNA-DNA heteroduplexes in three ways. We initially determined the binding affinity of TFIIIA to both 5 S heteroduplexes in comparison to the interaction with 5 S DNA. TFIIIA interacts with both heteroduplexes equivalently (Fig. 3). Quantitation of binding indicates that TFIIIA binds to both heteroduplexes with dissociation constants of 2 times 10M in comparison to the interaction with DNA that has a dissociation constant of 2 times 10M (see also Clemens et al.(1993)). We next determined the specificity of disruption of the complex of TFIIIA with the heteroduplex using specific and nonspecific DNA sequences as competitors (Fig. 4). TFIIIA was specifically competed off either RNA (Fig. 4A, lanes 1-8) or DNA (Fig. 4A, lanes 9-16) using specific 5 S DNA sequences as a competitor, while no specific competition is detectable when TFIIIA is bound to a heteroduplex containing the non-coding DNA strand of the 5 S rRNA gene (Fig. 4B, lanes 1-10). Similar results were obtained with heteroduplexes containing the coding strand of the 5 S rRNA gene (not shown). We suggest that TFIIIA does not form a specific complex with the 5 S heteroduplex that can be more efficiently competed with specific compared with nonspecific DNA. This reflects the relatively low affinity of TFIIIA for the RNA-DNA heteroduplex.


Figure 3: Binding titration for TFIIIA binding to either ``antisense'' () or ``sense'' DNA-RNA heteroduplexes (⊡). Autoradiographs of gel mobility shifts were scanned with a laser densitometer, and the fraction of bound nucleic acid was plotted against the TFIIIA concentration used. A titration curve of TFIIIA binding to DNA is included for comparison (bullet).




Figure 4: Specificity and strength of TFIIIA binding to DNA-RNA heteroduplexes. A, TFIIIA binding to either a fragment of the 5 S rRNA gene (DNA, lanes 9-16) or 5 S rRNA (5S rRNA, lanes 1-8). The complexes formed by mixing 5 ng of nucleic acid and 3 ng of TFIIIA (lanes 2-10) were incubated with 10-fold (lanes 3, 6, 11, and 14), 100-fold (lanes 4, 7, 12, and 15), and 500-fold excesses (lanes 5, 8, 13, and 16) of either specific (Sp. containing the 5 S rRNA sequence) or nonspecific DNA (NSp. pBR322) and separated on a 0.7% agarose gel. The resolution of free nucleic acid (Free) and the binding of single (1) or multiple TFIIIA molecules to the fragments is indicated. B, 5 ng of DNA-RNA heteroduplex (``antisense'') (lane1) was incubated with TFIIIA (120 ng) to generate a mixed population of TFIIIA-heteroduplex complexes (lane2). Binding was then assessed upon titration of specific (Sp.) or nonspecific competitor DNA (NSp.) such that the samples contained a 1-fold (lanes3 and 7), 10-fold (lanes4 and 8), 100-fold (lanes5 and 9), or 500-fold excess (lanes6 and 10). The resultant nucleoprotein complexes were separated on a 0.7% agarose gel. C shows the mobility of naked nucleic acid, and T shows the mobility of the complex of TFIIIA with nucleic acid without competitor.



Our final assessment of TFIIIA interaction with the RNA-DNA heteroduplexes was to examine whether sequence-selective binding occurred by DNase I footprinting. Our strategy was to carry out the DNase I cleavage reaction after mixing TFIIIA either with the RNA-DNA heteroduplex or with DNA as a control before resolving the nucleoprotein complexes on a non-denaturing gel (Hayes and Wolffe, 1992). The nucleoprotein complex of interest was then eluted from the gel, and the radiolabeled nucleic acid was isolated and resolved on a denaturing polyacrylamide gel to reveal any footprint. Resolution of the first complex formed when a single molecule of TFIIIA is bound to 5 S DNA reveals a clear footprint over the ICR (Fig. 5B, lanes 9-14). Identical analysis of both DNA-RNA heteroduplexes does not reveal a footprint (Fig. 5A, lanes 1-8). Thus although TFIIIA will bind to either heteroduplex, this interaction is not sequence selective.


DISCUSSION

The early analysis of TFIIIA interactions with the 5 S RNA gene suggested that TFIIIA might bind preferentially in a sequence-specific manner to the non-coding DNA strand (Sakonju and Brown, 1982). Subsequent studies have clearly established that such selective interactions can occur for both TFIIIA and other zinc finger proteins within the context of double helical DNA (Fairall et al., 1986; Pavletich and Pabo, 1991). The suggestion that comparable strand- and sequence-specific interactions detected in the binding of zinc finger proteins to DNA-RNA heteroduplexes (Shi and Berg, 1995) might also occur with TFIIIA is not supported by our results (Fig. 3Fig. 4Fig. 5). We find that TFIIIA will associate with a DNA-RNA heteroduplex (Fig. 2) but that this interaction is relatively weak and nonspecific compared with binding to 5 S DNA or RNA (Fig. 3Fig. 4Fig. 5) (Clemens et al., 1993).

The lack of sequence-specific recognition of heteroduplexes containing either strand of 5 S DNA is consistent with previous data indicating that TFIIIA recognizes the internal control region as B-type DNA (Gottesfeld et al., 1987; Hayes et al., 1990). Since DNA-RNA heteroduplexes approximate to an A-type conformation (Hall, 1993), our results provide yet further evidence against the proposal that equivalent recognition of DNA and RNA might be mediated by the same zinc fingers within TFIIIA (Rhodes and Klug, 1986; Fairall et al., 1986, 1989). Our results are entirely consistent with the definition of distinct domains of TFIIIA that interact with DNA or RNA in a sequence-selective manner (see Clemens et al.(1993), Darby and Joho(1992), and Theunissen et al.(1992)).

Proteins such as the histones will not interact stably with RNA-DNA heteroduplexes (Dunn and Griffith, 1980; Hovatter and Martinson, 1987). Our results suggest that the interaction of TFIIIA with the 5 S RNA gene will be destabilized by the generation of any RNA-DNA heteroduplex during transcription. Thus the generation of RNA-DNA heteroduplexes might provide a means of destabilizing nucleoprotein complexes within the chromosome. It should, however, be noted that in our experiments we generate very long heteroduplexes (298 bp) whereas in vivo any heteroduplex formed during transcription would be much shorter. TFIIIA in isolation is displaced from DNA by transit of bacteriophage RNA polymerase (Campbell and Setzer, 1991) yet remains bound to DNA within the intact transcription complex (Bogenhagen et al., 1982; Wolffe et al., 1986). Presumably multiple contacts between TFIIIA and other transcription factors that bind outside of the transcribed region facilitate the retention of TFIIIA on the 5 S rRNA gene during the transcription process (Wolffe and Morse, 1990; Kassavetis et al., 1990).


FOOTNOTES

*
The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore by hereby marked ``advertisement'' in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§
To whom correspondence should be addressed. Tel.: 301-402-2722; Fax: 301-402-1323; awlme{at}helix.nih.gov.

(^1)
The abbreviations used are: ICR, internal control region; bp, base pair(s).


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