©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
A Temperature-dependent Conformational Rearrangement in the Ribosomal Protein S416 S rRNA Complex (*)

(Received for publication, October 3, 1994)

Ted Powers (§) Harry F. Noller

From the Sinsheimer Laboratories, University of California, Santa Cruz, California 95064

ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
FOOTNOTES
ACKNOWLEDGEMENTS
REFERENCES

ABSTRACT

Ribosomal protein S4 protects a characteristic set of bases in 16 S rRNA from attack by chemical probes. Use of hydroxyl radical as a probe of the RNA backbone shows that ribose residues in these same regions are also protected by S4, confirming the localization of its interactions with 16 S rRNA to the junction of five helical elements in the proximal region of the 5` domain. At 0 °C, the nucleotides protected by S4 from base-specific probes are confined almost exclusively to the two compound helices formed by residues 404-499. After subsequent heating of the complex briefly at 30 or 42 °C, nucleotides in the three adjacent helices are additionally protected, resulting in a pattern of protection that is identical to that which is observed when S4 is incubated with 16 S rRNA under in vitro reconstitution conditions. Preincubation of the protein or the RNA (or both) separately at elevated temperature does not substitute for heating the S4bulletRNA complex. The regions in the RNA affected by the heat step are known to interact with proteins S12 and S16, both of which depend upon S4 for their binding to the RNA. Thus, the finding that S4 recruits additional sites of interaction in the RNA following its initial binding suggests a possible mechanism to insure the sequential addition of proteins during ribosomal assembly.


INTRODUCTION

Ribosomal protein S4 is one of the most extensively studied of the small subunit proteins that bind directly and independently to 16 S rRNA. In addition to its central role in ribosome assembly, it also functions as a translational repressor by binding to its own mRNA (Nomura et al., 1984) and has long served as a model for the study of protein-RNA interaction (for review, see Zimmermann(1980) and Garrett et al.(1984)). The first experiments attempting to localize the RNA binding site for S4 involved partial ribonuclease digestion of S4bullet16 S rRNA complexes and sequence analysis of the resulting protein-protected RNA fragments (Schaup et al., 1971; Zimmermann et al., 1972; Ungewickell et al., 1975). The protected RNA encompassed several hundred nucleotides of the 5` region of 16 S rRNA, unexpectedly large to be the binding site of a protein of mass 23,000. However, almost exactly the same subfragments of 16 S rRNA were protected in the absence of protein, under somewhat milder digestion conditions, using carrier-bound nuclease (Ehresmann et al., 1977). This result suggested that much of what had been attributed to protection of 16 S rRNA by protein S4 was in fact due to self-structuring of the RNA; its 5` region was inherently nuclease-resistant (Garrett et al., 1977). There remained the question of which specific structural features of the 5` region actually interact with S4.

Two approaches were devised to address this question. Development of rapid chemical and enzymatic probing methods (Moazed et al., 1986; Stern et al., 1988b) made it possible to examine protein-RNA interactions at single-nucleotide resolution using microgram amounts of material. Examination of the S4bullet16 S rRNA complex using this approach showed that only a modest number of bases in the 5` domain were protected by bound S4 (Stern et al., 1986, 1988a). The protected bases were confined to a limited region of the domain comprising the junction of five helical elements, which was termed the ``S4 junction.'' This region of the RNA lies within the RNase-resistant fragments characterized in the earlier nuclease protection studies, but it defines a compact RNA substructure that could more plausibly constitute the actual binding site for a protein of the size of S4. Direct cross-linking of S4 to one of the helices that forms the S4 junction supports this assignment (Greuer et al., 1987).

Using another approach, Vartikar and Draper(1988) studied the RNA binding site requirements for protein S4 by constructing synthetic subfragments of 16 S rRNA using in vitro transcription and testing the ability of the synthetic rRNA analogues to bind S4. They found that deletion of regions of the RNA containing two of the five implicated helical elements had little or no effect on the specific binding of S4 to the RNA, in apparent contradiction to our findings.

In the present study, interaction of S4 with 16 S rRNA is reexamined. The results of hydroxyl radical protection, which probes interactions involving the RNA backbone, strongly support the conclusions from our earlier studies; all of the S4-dependent protections of the RNA backbone are localized to the S4 junction region. In addition, we find that S4bulletRNA interaction involves two separable steps; using base-specific probes, one set of protections is observed at 0 °C, while an additional set is seen only after incubation of the complex at elevated temperature. The 0 °C effects involve only nucleotides that are located in the subfragments identified by Draper and co-workers (Sapag etal., 1990), while the heat-dependent protections include all of the protected nucleotide positions that lie outside of their RNA binding fragments. Since the latter authors carried out their binding reactions at 0 °C, our data appear to resolve the apparent contradiction. The ability of protein S4 to participate in two distinct and separable interactions with different structural features of 16 S rRNA raises new questions concerning mechanisms of RNA-protein interactions in the ribosome.


EXPERIMENTAL PROCEDURES

Ribosomes, 30 S ribosomal subunits, 30 S ribosomal proteins, and 16 S rRNA were isolated as described previously (Stern et al., 1988b). Complexes between 16 S rRNA and S4 were formed at 0 °C by combining 5 µg of 16 S rRNA with 4 mol eq of purified S4 protein in 25 µl of reconstitution buffer containing 80 mM potassium Hepes (pH 7.6), 20 mM MgCl(2), 300 mM KCl, 6 mM 2-mercaptoethanol, 0.01% (w/v) Nikkol detergent (octaethylene glycol mono-n-dodecyl ether; Nikko Chemical Co. Ltd.), followed by incubation at either 0 °C for 60 min, 30 °C for 10 min, or 42 °C for 30 min. The resulting complexes were incubated for an additional 30 min at 0 °C prior to the addition of chemical modification reagents. For comparison, 5 µg of naked 16 S rRNA was also probed in parallel, following incubation first at 42 °C for 30 min and then at 0 °C for 30 min.

Dimethyl sulfate and kethoxal modifications were performed at 0 °C as described previously (Stern et al., 1988b). Fe(II)-EDTA-generated hydroxyl radical cleavage reactions were performed essentially as described by Cech and co-workers (Latham and Cech, 1989; Celander and Cech, 1990) and by Tullius and co-workers (Tullius and Dombroski, 1986; Burkhoff and Tullius, 1987). 1 µl of each of the following four solutions (prepared freshly prior to each experiment) was added to the top of a 1.5-ml Eppendorf tube, containing 25 µl of sample, and mixed by centrifugation for 2-5 s in an Eppendorf microcentrifuge (all procedures were carried out at 4 °C): 1) 50 mM Fe(NH(4))(2)(SO(4))(2)bullet6H(2)O (final concentration, 2 mM); 2) 100 mM EDTA (final concentration, 4 mM); 3) 250 mM ascorbic acid (final concentration, 10 mM); 4) 2.5% H(2)O(2) (final concentration, 0.1%). Samples were then incubated on ice for 10 min, and the cleavage reaction was stopped by addition of 10 µl of 0.1 M thiourea. Samples were precipitated by the addition of 25 µl of 0.3 M sodium acetate (pH 6.5) and 200 µl of 95% ethanol. After modification, 16 S rRNA was repurified by phenol extraction, and the sites of modification and cleavage were determined by primer extension and gel electrophoresis as described previously (Stern et al., 1988b).


RESULTS

Effect of Temperature on the Interaction Between 16 S rRNA and S4

We examined the reactivity of 16 S rRNA toward the base-specific probes dimethyl sulfate (DMS) (^1)and kethoxal, both in its naked form and in complexes with protein S4 formed at each of three different temperatures, 0, 30, and 42 °C. When the S4bullet16 S rRNA complex is formed at 42 °C, an extensive set of protections and enhancements is observed, compared with naked RNA. These effects are found primarily in the 5` domain (Fig. 1, a-e; compare lanes1 and 4; Table 1) and are essentially identical to those reported previously (Stern et al., 1986, 1988a). No differences are observed when the complex is formed at 30 rather than 42 °C (Fig. 1, a-e; compare lanes3 and 4). In contrast, several differences are evident when the 16 S rRNAbulletS4 complex is formed at 0 °C; most striking is the absence of characteristic S4-dependent effects in the 530 stem-loop region (Fig. 1a). Other differences include the lack of significant protection of residues G and A in the complex formed at 0 °C (Fig. 1c).


Figure 1: a-e, results of DMS and kethoxal (KE) probing of 16 S rRNA following incubation with protein S4 at different temperatures. Lane1, naked 16 S rRNA; lane2, 16 S rRNA + S4, incubated at 0 °C; lane3, 16 S rRNA + S4, incubated at 30 °C; lane4, 16 S rRNA + S4, incubated at 42 °C. f, control experiment demonstrating that the effects observed with 16 S rRNA + S4 at 30 °C and 42 °C require heating both the RNA and protein together. Lane1, unmodified 16 S rRNA; lane2, naked 16 S rRNA; lane3, 16 S rRNA + S4, incubated together at 0 °C; lane4, 16 S rRNA incubated alone at 42 °C and then incubated with S4 at 0 °C; lane5, S4 incubated alone at 42 °C and then incubated with 16 S rRNA at 0 °C; lane6, 16 S rRNA and S4 each heated separately at 42 °C and then incubated together at 0 °C; lane7, 16 S rRNA + S4, incubated together at 42 °C. Samples in lanes2-7 were modified with DMS at 0 °C. Dots on the left are positioned every 10th nucleotide. Primers used are as follows: a and f, 683; b, 480; c, 162; d, 1046; e, 1257.





Maximum binding of S4 to 16 S rRNA has been shown to require heating of the complex to temperatures above 30 °C (Schulte et al., 1974). The temperature-dependent differences that we observe do not simply reflect an overall increase in the number of stable complexes formed, however, as complete protection of many residues in 16 S rRNA is observed in the complex formed at 0 °C, including A, G, and A (Fig. 1a; Table 1). Interestingly, the reactivities of A and G are enhanced in the presence of S4 at 0 °C but are then protected when the complex is heated (Fig. 1, a and c, respectively), suggesting that transient protein-induced conformational alterations in RNA structure accompany assembly of S4.

A trivial explanation for these effects is that the heating step renatures either S4 or 16 S rRNA or both. To test this possibility, complexes were formed after heating one or both components individually at 42 °C, followed by incubating them together at 0 °C. Only when the RNA and protein are heated together are these additional protections and enhancements observed (Fig. 1f; compare lanes3-6 with lane7; for simplicity, only DMS probing data for the 500 region are shown). These results demonstrate that the heat step is not required simply for renaturation of one of the components but rather for a structural rearrangement in the assembling ribonucleoprotein.

Probing the 16 S rRNAbulletS4 Complex with Hydroxyl Radicals

Recently, it has been shown that the susceptibility of the sugar-phosphate backbone of RNA to cleavage by Fe(II)-EDTA-generated hydroxyl radicals is insensitive to RNA secondary structure (Latham and Cech, 1989; Celander and Cech, 1990). This property, as well as its small molecular dimensions and apparent lack of base-sequence specificity, makes hydroxyl radical a potentially valuable reagent for obtaining high resolution information concerning protein-RNA interactions. Thus, we used hydroxyl radicals to define further the site of interaction of S4 on 16 S rRNA (Fig. 2).


Figure 2: Results of Fe(II)-EDTA generated hydroxyl radical probing of the S4bullet16 S rRNA complex. Lanes1 and 4, unmodified 16 S rRNA; lanes2 and 5, naked 16 S rRNA; lanes3 and 6, 16 S rRNA + S4. Samples where incubated either at 0 °C (lanes1-3) or 42 °C (lanes4-6) followed by modification with hydroxyl radicals at 0 °C, as described under ``Experimental Procedures.'' Primers used are as follows: a, 480; b, and c, 565; d, 161. Other symbols are as described in the legend to Fig. 1.



When naked 16 S rRNA is treated with hydroxyl radicals, strand scission occurs at essentially every position, generating a nearly uniform cleavage pattern (Fig. 2; lanes2 and 5). Following incubation with S4 at 42 °C, strong protection against cleavage is observed around position A (Fig. 2a). Several other regions in the 5` domain also show significant protection by S4 (Fig. 2). Significantly, all residues protected by S4 from hydroxyl radical attack are located exclusively within the S4 junction (see Fig. 4). Unlike the behavior observed for the base-specific probes, protection of the RNA by S4 from hydroxyl radical attack was independent of temperature; identical results were obtained whether the probing was done at 0 or 42 °C (Fig. 2).


Figure 4: Schematic secondary structure of the S4 junction in the 5` domain of 16 S rRNA (Stern et al., 1986), summarizing results of probing the S4bullet16 S rRNA complex with hydroxyl radicals. Circles indicate reduced reactivities in the S4-16 S rRNA complex versus naked 16 S rRNA. Smallsymbols indicate weak effects. Similar results were obtained when the complex was formed at 0 or 42 °C. Data are from Fig. 2.



Weak protection of bases in the 500 region by S4 against hydroxyl radical attack was surprising in light of the strong protections this protein affords against base-specific probes (compare Fig. 1a and Fig. 2c). To test the possibility that hydroxyl radicals disrupt the 16 S rRNAbulletS4 complex, we first modified the complex with Fe(II)-EDTA, followed by treatment of this same sample with DMS. No decrease in the level of protection of residues in 16 S rRNA from DMS attack by S4 is observed after prior modification of the 16 S rRNAbulletS4 complex with Fe(II)-EDTA, indicating that hydroxyl radicals do not, in fact, perturb the interaction between 16 S rRNA and S4 (data not shown).


DISCUSSION

These findings confirm our earlier conclusions that the principle interactions between protein S4 and 16 S rRNA are localized to a relatively compact region of the 5` domain, which we call the S4 junction (Stern et al., 1986, 1988a) ( Fig. 3and 4). In our earlier work, a significant number of S4-dependent changes in the chemical probing pattern involved bases outside of the S4 junction. We reasoned that most of the latter were unlikely to interact with S4, based on the findings that they 1) were not contained within the large nuclease-resistant S4 binding-site fragments or 2) showed increased reactivity in the presence of bound S4, indicating an S4-dependent conformational change. Conversely, we argued that clusters of strongly protected bases would be likely indicators of S4bulletRNA interactions. Use of hydroxyl radical as a probe of the RNA backbone is a method that is complementary to base-specific probing and carries with it the advantage that it is not susceptible to certain ambiguities of interpretation of the latter approach such as, for example, protein-dependent base pair formation. However, the fact that tertiary folding of tRNA results in some protection of its backbone from hydroxyl radical attack (Latham and Cech, 1989) shows that some degree of caution must be maintained. In this work, we observed no S4-dependent protection of 16 S rRNA from hydroxyl radical outside of the S4 junction region (Fig. 4). This is consistent with our earlier interpretation that this region of the RNA contains most of the important contacts with S4. It is still possible, however, that the protein could interact with certain RNA bases without affecting the reactivities of their associated or neighboring ribose moieties.


Figure 3: Schematic secondary structure of the S4 junction in the 5` domain of 16 S rRNA (Stern et al., 1986), summarizing results of probing the S4-16 S rRNA complex with base-specific probes DMS and kethoxal. 0 °C, reactivity differences in the S4bullet16 S rRNA complex formed at 0 °C versus naked 16 S rRNA; 42 °C, reactivity differences in the S4bullet16 S rRNA complex formed at 42 °C (or 30 °C) versus the complex formed at 0 °C. Circles and triangles indicate reduced and enhanced reactivities, respectively. Smallsymbols indicate weak effects. Data are from Fig. 1and Table 1.



Another approach to analysis of the S4 binding site was taken by Vartikar and Draper(1989). These authors constructed a series of 12 fragments of 16 S rRNA by in vitro transcription of deleted versions of the 16 S rRNA gene and tested the ability of the fragments to bind S4. Their findings were generally consistent with our interpretation, with three main exceptions. 1) Full binding activity was observed with a fragment spanning positions 1-559 in which residues 501-544 had been deleted; this deletion removes several S4-protected nucleotides in the 501-510 region, involving one of the five junction helices (Fig. 3). 2) Full binding activity was also observed for a fragment comprising residues 39-559; this fragment excludes another of the junction helices, which contains protections involving positions 30-33 (Fig. 3). 3) A fragment spanning residues 27-559, but missing residues 53-352, showed sharply decreased binding, although the deleted regions lie outside the junction proper (Fig. 3).

One significant difference between the experiments of Vartikar and Draper(1989) and our own studies concerns the temperature of the binding reaction. Binding was carried out in one case at 0 °C (Vartikar and Draper, 1989) and in the other at 30 or 42 °C, similar to temperatures used for in vitro reconstitution of 30 S subunits (Stern et al., 1986, 1988a). When we reexamined the protection of 16 S rRNA from base-specific probes by S4 as a function of the temperature of the binding reaction, the results were striking (Fig. 3). At 0 °C, almost no effects are observed in the two helices (30/550 and 510/540 regions, respectively) that were disrupted in two of the experiments of Vartikar and Draper(1989); after incubation at 30 or 42 °C, an extensive set of additional nucleotides is protected, many of which are found in the two helices in question (Fig. 3). Thus, the results of Vartikar and Draper(1989) are entirely consistent with the results of chemical probing for the 0 °C complex. However, it is clear that there is also a second, heat-dependent event, which must involve conformational rearrangement of the protein-RNA complex, since preincubation of the isolated components at 42 °C prior to binding is insufficient to effect the second step of S4bulletRNA interaction. Whether this second step affects the association constant for the interaction is not addressed by our chemical probing studies. However, early experiments by Schulte et al.(1974) show that heating of the S4bulletRNA complex to temperatures of 30 °C or higher was required for maximal binding, suggesting that the second step may contribute to the stability of the interaction.

In contrast to results using base-specific probes, temperature has no detectable effect on the protection by S4 from hydroxyl radicals (Fig. 2). Since hydroxyl radicals are believed to attack the ribose moiety of RNA, we conclude that the heat-dependent conformational change in the S4 ribonucleoprotein results in no changes in the accessibilities of riboses. This suggests that the temperature-dependent differences seen for the base-specific probing are caused by changes in base-base or base-protein interactions.

Ofengand and co-workers (Weitzmann etal., 1993) have recently investigated the ability of a synthetic RNA fragment, corresponding to residues 1-526 of 16 S rRNA, to self-assemble into a ribosomal subdomain, following reconstitution with total 30 S proteins at 42 °C. Four proteins were found to bind specifically to this RNA fragment, S4, S16, S17, and S20; however, the stoichiometry of S4 was found to be significantly lower compared with the other three proteins. Since the 30/550 and 510/540 helices are disrupted in this RNA, these findings are consistent with their possible importance for the stable binding of S4 to 16 S rRNA.

It is less obvious why deletion of residues 53-352 from the 27-559 fragment should cause such a strong decrease in S4 binding if in fact its binding site lies completely within the boundaries of the junction region. One possible explanation is that some features of the lower half of the 5` domain make RNA-RNA interactions with the S4 junction region that help to form or stabilize its S4-compatible conformation. Indeed, partial nuclease digestion experiments suggested that the upper and lower halves of the 5` domain could be held together by noncovalent interactions (Ehresmann et al., 1977). Another possibility is that the deleted fragment folds anomalously, thereby perturbing the S4 binding site indirectly. Such an explanation might also account for the deleterious effects of other deletions in 16 S rRNA outside of the S4 junction (Sapag et al., 1990).

The temperature-dependent conformational change reported here provides support for an earlier suggestion for the mechanism of sequential assembly of ribosomal proteins (Stern et al., 1989). Proteins S12 and S16 depend on prior binding of S4 to 16 S rRNA for their own assembly (Held et al., 1974). Among the characteristic effects of these two proteins is protection of groups of bases in the 520 and 360 regions, respectively (Stern et al., 1989). However, these bases are unreactive in naked 16 S rRNA, and only become reactive during the heat-dependent step of S4 assembly (Table 1). Thus, it may be that the conformational rearrangement of the S4bullet16 S rRNA complex observed here is an obligatory step leading to the assembly of the latter two proteins. Finally, it seems likely that similar effects will be found upon detailed examination of other ribosomal protein-rRNA interactions, and may even turn out to be a common device in orchestrating an orderly, sequential pathway for ribosome assembly.


FOOTNOTES

*
This work was supported by Grant GM17129 from the National Institutes of Health and by a grant to the Center for Molecular Biology of RNA from the Lucille P. Markey Charitable Trust. 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.

§
Present address: Dept. of Biochemistry and Biophysics, University of California, San Francisco, CA 94143.

(^1)
The abbreviation used is: DMS, dimethyl sulfate.


ACKNOWLEDGEMENTS

We thank Gary Daubresse for contribution to the initial stages of this work and for helpful discussions. We also thank Li-Ming Changchien for providing the purified S4 protein used in this study.


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