Thermodynamic coupling between backbone hydrogen bonding and the hydrophobic effect in protein folding energetics

ORGN 943

Jianmin Gao, jmgao@scripps.edu, Daryl A. Bosco, Evan T Powers, epowers@scripps.edu, and Jeffery W. Kelly, jkelly@scripps.edu. Department of Chemistry, The Scripps Research Institute, 10550 N. Torrey Pines Rd., BCC265, La Jolla, CA 92037
Recent literature (Nature, 2004, 430, 101) shows that backbone hydrogen bonds make context-dependent contribution to protein stability. We hypothesized that hydrophobic packing and H-bonding may stabilize the protein structure synergistically; that is, upon protein folding, hydrophobic packing buries H-bonds and strengths them, which further enhances the hydrophobic effect which is established to be an important contributor to protein stability. The hypothesis was tested in both alpha-helical (B domain of protein A) and beta-sheet (PIN WW domain) folds using a double mutant cycle analysis approach. A side chain proximal to the H-bond of interest was changed to alter the solvent accessibility of the H-bond, such that there is a variant whose large side chain protects the H-bond from solvent interaction and another whose small side chain allows solvent access. Amide-to-ester mutations were used to assess H-bond strength in the case of the large and the small side chain variants. Double mutant cycle analysis revealed that H-bonds are significantly stronger when excluded from solvent contact by bulky hydrophobic side chains. The increased H-bond strength accounts for at least 30% of the overall protein stability gain when a small hydrophobic side chain is replaced by a larger one. Our results indicate that the hydrophobic effect and H-bonding are thermodynamically linked in protein structures and that only a few residues make substantial contributions to protein stability.