Physical Origins of Codon Positions That Strongly Influence Cotranslational Folding: A Framework for Controlling Nascent-Protein Folding.

An emerging paradigm in the field of in vivo protein biophysics is that nascent-protein behavior is a type of nonequilibrium phenomenon, where translation-elongation kinetics can be more important in determining nascent-protein behavior than the thermodynamic properties of the protein. Synonymous co...

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Published in:Journal of the American Chemical Society Vol. 138; no. 4; pp. 1180 - 1196
Main Authors: Sharma, Ajeet K., O'Brien, Edward P., Bukau, Bernd
Format: Article
Published: American Chemical Society 2/3/2016
Subjects:
Online Access:View this record in EBSCOhost
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        10.1021/jacs.5b08145
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        atl: Physical Origins of Codon Positions That Strongly Influence Cotranslational Folding: A Framework for Controlling Nascent-Protein Folding.
      aug:
        au:
          Sharma, Ajeet K.
          O'Brien, Edward P.
          Bukau, Bernd
        affil:
          Department of Chemistry, Pennsylvania State University, University Park, Pennsylvania 16802, United States
          Center for Molecular Biology of the University of Heidelberg (ZMBH), DKFZ-ZMBH Alliance, Im Neuenheimer Feld 282, Heidelberg D-69120, Germany
      su:
        Genetic code
        Protein folding
        Messenger RNA
        Signal recognition particle
        Nonequilibrium thermodynamics
      sug:
        subj:
          Genetic code
          Protein folding
          Messenger RNA
          Signal recognition particle
          Nonequilibrium thermodynamics
      ab: An emerging paradigm in the field of in vivo protein biophysics is that nascent-protein behavior is a type of nonequilibrium phenomenon, where translation-elongation kinetics can be more important in determining nascent-protein behavior than the thermodynamic properties of the protein. Synonymous codon substitutions, which change the translation rate at select codon positions along a transcript, have been shown to alter cotranslational protein folding, suggesting that evolution may have shaped synonymous codon usage in the genomes of organisms in part to increase the amount of folded and functional nascent protein. Here, we develop a Monte Carlo-master-equation method that allows for the control of nascent-chain folding during translation through the rational design of mRNA sequences to guide the cotranslational folding process. We test this framework using coarse-grained molecular dynamics simulations and find it provides optimal mRNA sequences to control the simulated, cotranslational folding of a protein in a user-prescribed manner. With this approach we discover that some codon positions in a transcript can have a much greater impact on nascent-protein folding than others because they tend to be positions where the nascent chain populates states that are far from equilibrium, as well as being dependent on a complex ratio of time scales. As a consequence, different cotranslational profiles of the same protein can have different critical codon positions and different numbers of synonymous mRNA sequences that encode for them. These findings explain that there is a fundamental connection between the nonequilibrium nature of cotranslational processes, nascent-protein behavior, and synonymous codon usage.
      pubtype: Academic Journal
      doctype: Article
      src: R
    language: English
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