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Chapter 11 : RNA Tertiary Structure and Protein Recognition in an L11-RNA Complex

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RNA Tertiary Structure and Protein Recognition in an L11-RNA Complex, Page 1 of 2

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Abstract:

This chapter relates the intricate architecture of the L11-RNA complex to previous studies that delineated crucial features of the RNA tertiary structure and protein-RNA interface. In describing the structure, it is interesting to note how conservation and variation of different nucleotides and amino acids serve as a guide to critical features of the complex, and the authors use the extreme conservation of some bases to speculate about functional surfaces of the rRNA domain. Lastly, the chapter discusses the possibility that the functional role of L11-C76 is to promote a correct RNA tertiary fold. Relatively few RNA structures that have noncanonical interactions have been determined at atomic resolution, and of these only tRNA and the P4-P6 domain of group I intron have extensive tertiary structure. From nuclear magnetic resonance (NMR) studies of the free L11 RNA binding domain (L11-C76), it was known that the protein folds into three α-helices that are superimposable on the α-helices of the homeodomain class of DNA binding proteins. Covariation analysis has been an extremely powerful method for predicting rRNA secondary structure and providing clues to tertiary interactions. In melting studies of the 58-nt RNA, it was proposed that the lowest-temperature melting transition is due to unfolding of a set of tertiary interactions that link the three helical elements. In the last decade rRNA has taken center stage as the functional component of ribosomes, and it has been suggested that the primary role of ribosomal proteins is to promote RNA folding.

Citation: Draper D, Conn G, Guhathakurta D, Gittis A, Lattman E, Reynaldo L. 2000. RNA Tertiary Structure and Protein Recognition in an L11-RNA Complex, p 105-114. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch11
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Figures

Image of Figure 1
Figure 1

Folding of the 1051-to-1108 domain of large-subunit rRNA. (A) Phylogenetically conserved secondary structure, as drawn by . The sequence and numbering are shown. (B) Representation of rRNA showing tertiary base-base hydrogen bonds (horizontal red bars) and base stacking (vertical blue bar) and approximate stacking of the bases as seen in the crystal structure. Thin red diagonal lines indicate U imino-phosphate hydrogen bonds characteristic of the U-turn motif. Thin black lines join consecutive nucleotides, with arrows indicating the 5′ → 3′ direction of the backbone. The crystallized sequence contains a U1061 → A mutation that stabilizes the tertiary fold. (C) Representation of the L11- RNA complex structure as determined by crystallography ( ); the two views are rotated about the vertical axis by 180°. The bases are color coded to correspond to panels A and B. Two Mg ions (green spheres) and two Os(NH3)6 ions (magenta spheres) are located within the structure. The L11-C76 backbone is shown as a yellow ribbon.

Citation: Draper D, Conn G, Guhathakurta D, Gittis A, Lattman E, Reynaldo L. 2000. RNA Tertiary Structure and Protein Recognition in an L11-RNA Complex, p 105-114. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch11
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Image of Figure 2
Figure 2

Tertiary interactions within the 1051-to-1108 RNA. (A) A1085 forms a minor-groove triple with G1055-C1104; all three of these bases are invariant. (B) A1088-A1089 sidestep connects a Hoogsteen pair (U1060) and a base triple (A1090- U1101). (C) The C1072(C1092-G1099) base triple and its linkage to a noncanonical A1065-C1073 pair. (D) Hydrogen bonding between the U1066 and U1094 U-turns. Dashed lines indicate potential hydrogen bonds.

Citation: Draper D, Conn G, Guhathakurta D, Gittis A, Lattman E, Reynaldo L. 2000. RNA Tertiary Structure and Protein Recognition in an L11-RNA Complex, p 105-114. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch11
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Image of Figure 3
Figure 3

Schematic of protein contacts with RNA. The bases shown in boldface are conserved in ?97% of rRNA sequences from the three main phylogenetic domains. The base, 2′-OH, and phosphate that form hydrogen bonds to protein are shown in gray. The dashed-line sugars make nonpolar contacts with protein. The A1088 sugar is in gray as a reminder that it is not contiguous with the RNA sequence shown but is intercalated from elsewhere in the RNA. Protein contacts are from the indicated amino acid side chain unless specified as backbone carbonyl (.O) or backbone amide (.NH).

Citation: Draper D, Conn G, Guhathakurta D, Gittis A, Lattman E, Reynaldo L. 2000. RNA Tertiary Structure and Protein Recognition in an L11-RNA Complex, p 105-114. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch11
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Image of Figure 4
Figure 4

Highly conserved residues in the 1051-to-1108 rRNA domain. Residues conserved in greater than 97% of sequences from the three main phylogenetic domains are shown in boldface ( ). Solid boxes, bases involved in base-base tertiary bonding; dashed boxes, bases involved in noncanonical interactions; circles, highly conserved residues; several other highly conserved bases unlikely to be required for proper folding are boldfaced and uncircled.

Citation: Draper D, Conn G, Guhathakurta D, Gittis A, Lattman E, Reynaldo L. 2000. RNA Tertiary Structure and Protein Recognition in an L11-RNA Complex, p 105-114. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch11
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Image of Figure 5
Figure 5

Stability of the 1051-to-1108 rRNA domain tertiary structure. The data are first-derivative melting curves taken in 5 mM MgCl, 100 mM KCl (A) or NHCl (B), and 10 mM MOPS (morpholinepropanesulfonic acid) (pH 7.2). (A) Stabilization of rRNA structure by L11-C76 protein. GACG RNA, a variant in which the tertiary structure unfolds in a distinct first transition from the rest of the structure ( ), was used in these experiments. The molar ratio of protein to RNA is indicated; the RNA concentration was 0.82 M. Note that at the higher protein concentration, the RNA shows no hyperchromicity until ?45°C. (B) Melting of either wild-type (gray) or a U1061A variant (black) RNA fragment. Data are from . Tertiary structure unfolds first in a broad transition in the rRNA fragment, but this tertiary structure is stabilized to much higher temperatures and melts simultaneously with some of the secondary structure in the variant.

Citation: Draper D, Conn G, Guhathakurta D, Gittis A, Lattman E, Reynaldo L. 2000. RNA Tertiary Structure and Protein Recognition in an L11-RNA Complex, p 105-114. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch11
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