Cooperative folding of a polytopic α-helical membrane protein involves a compact N-terminal nucleus and nonnative loops

Wojciech Paslawski, Ove K Lillelund, Julie Veje Kristensen, Nicholas P Schafer, Rosanna P Baker, Sinisa Urban, Daniel E Otzen

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Abstract

Despite the ubiquity of helical membrane proteins in nature and their pharmacological importance, the mechanisms guiding their folding remain unclear. We performed kinetic folding and unfolding experiments on 69 mutants (engineered every 2-3 residues throughout the 178-residue transmembrane domain) of GlpG, a membrane-embedded rhomboid protease from Escherichia coli. The only clustering of significantly positive ϕ-values occurs at the cytosolic termini of transmembrane helices 1 and 2, which we identify as a compact nucleus. The three loops flanking these helices show a preponderance of negative ϕ-values, which are sometimes taken to be indicative of nonnative interactions in the transition state. Mutations in transmembrane helices 3-6 yielded predominantly ϕ-values near zero, indicating that this part of the protein has denatured-state-level structure in the transition state. We propose that loops 1-3 undergo conformational rearrangements to position the folding nucleus correctly, which then drives folding of the rest of the domain. A compact N-terminal nucleus is consistent with the vectorial nature of cotranslational membrane insertion found in vivo. The origin of the interactions in the transition state that lead to a large number of negative ϕ-values remains to be elucidated.

Original languageEnglish
JournalProceedings of the National Academy of Sciences
Volume112
Issue6
Pages (from-to)7978-7983
Number of pages6
ISSN0027-8424
DOIs
Publication statusPublished - 10 Feb 2015

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