Local Organization at Ser-Pro and pSer-Pro Sequences: Stabilization of the cis-amide via C—H/O Interaction

Researcher(s)

  • Harrison Oven, Biochemistry, University of Delaware

Faculty Mentor(s)

  • Neal Zondlo, Chemistry & Biochemistry, University of Delaware

Abstract

Serine-Proline sequences are particularly abundant in the human proteome, with over 75% of all proteins including the two-residue motif. Furthermore, these sites are hotspots for post-translational modification, accounting for over 25% of all phosphorylation sites in proteins. This prevalence indicates a role in the local stabilization and ordering of a variety of secondary structures. To better define the range of structures that can be adopted by Ser-Pro motifs and to characterize the intramolecular interactions stabilizing those conformations, a series of dipeptide derivatives was synthesized with the intention of encouraging a larger relative population of the more difficult to observe cis-amide rotamer and aiding crystallization for X-ray analysis. 2S,4S-Hydroxyproline-(4-iodophenyl)-methyl ester was synthesized via Mitsunobu reaction at the 4th ring position of Boc-2S,4R-hydroxyproline-methyl ester and coupled to serine to make both Boc and Ac N-capped dipeptides (Boc-Ser-hyp-4-(p-IPh)-OMe and Ac-Ser-hyp-4-(p-IPh)-OMe) which were analyzed by NMR and conformationally characterized by X-ray crystallography. These dipeptides were then phosphorylated and analyzed by NMR while awaiting crystallization. 1H-NMR indicated the derivatives had Ktrans/cis values as low as 2.2, in significant contrast to most observed Ser-Pro residues with a Ktrans/cis over 5.0. The phosphorylated dipeptides exhibited a decrease in Ktrans/cis to as low as 1.8. The unit cell of Ac-Ser-hyp-4-(p-IPh)-OMe contains two trans-amide structures with Pro exhibiting an δ geometry, while Ser exhibited both β sheet and polyproline II helix (PPII) geometries. Both of the conformations are stabilized by backbone n → π* interactions and Ser side chain hydrogen bonds with the amide carbonyl and proton respectively. More significantly, the Boc-Ser-hyp-4-(p-IPh)-OMe crystal uniquely contained both cis- and trans-amide strucutres, with Pro adopting δ and PPII geometries, and Ser adopting β sheet and PPII geometries respectively. The cis-structure shows a novel C—H/O interaction of 2.79 Å occurring between Ser-OH and Pro-Hα similar to the mechanism proposed to explain the cis-stabilization observed in phosphorylated residues that has been correlated to multiple chronic illnesses. We aim to confirm this via X-ray crystallography of the phosphorylated dipeptides in the future. Alongside characterizing these novel noncovalent interactions in isolated crystal structures, a bioinformatic analysis of SP sequences in the PDB confirmed their biological relevance. The wide variety of conformations observed at Ser-Pro motifs is indicative of their uniquely promiscuous ability to stabilize many common structures and helps to explain their abundance in the human proteome as a versatile residue in protein folding and in the dynamic stabilization of multiple structures.