Single-molecule fluorescence resonance energy transfer assays reveal heterogeneous folding ensembles in a simple RNA stem-loop

J Mol Biol. 2008 Dec 5;384(1):264-78. doi: 10.1016/j.jmb.2008.08.088. Epub 2008 Sep 13.

Abstract

We have examined the folding ensembles present in solution for a series of RNA oligonucleotides that encompass the replicase translational operator stem-loop of the RNA bacteriophage MS2. Single-molecule (SM) fluorescence assays suggest that these RNAs exist in solution as ensembles of differentially base-paired/base-stacked states at equilibrium. There are two distinct ensembles for the wild-type sequence, implying the existence of a significant free energy barrier between "folded" and "unfolded" ensembles. Experiments with sequence variants are consistent with an unfolding mechanism in which interruptions to base-paired duplexes, in this example by the single-stranded loop and a single-base bulge in the base-paired stem, as well as the free ends, act as nucleation points for unfolding. The switch between folded and unfolded ensembles is consistent with a transition that occurs when all base-pairing and/or base-stacking interactions that would orientate the legs of the RNA stem are broken. Strikingly, a U-to-C replacement of a residue in the loop, which creates a high-affinity form of the operator for coat protein binding, results in dramatically different (un)folding behaviour, revealing distinct subpopulations that are either stabilised or destabilised with respect to the wild-type sequence. This result suggests additional reasons for selection against the C-variant stem-loop in vivo and provides an explanation for the increased affinity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Base Sequence
  • Capsid Proteins / chemistry
  • Capsid Proteins / metabolism
  • Fluorescence Resonance Energy Transfer*
  • Kinetics
  • Levivirus / chemistry*
  • Molecular Sequence Data
  • Mutation / genetics
  • Nucleic Acid Conformation*
  • Protein Structure, Secondary
  • RNA, Viral / chemistry*
  • RNA, Viral / genetics
  • RNA, Viral / metabolism*
  • Spectrum Analysis
  • Thermodynamics

Substances

  • Capsid Proteins
  • RNA, Viral