Mono-anionic phosphopeptides produced by unexpected histidine alkylation exhibit high Plk1 polo-box domain-binding affinities and enhanced antiproliferative effects in HeLa cells

Biopolymers. 2014 Nov;102(6):444-55. doi: 10.1002/bip.22569.

Abstract

Binding of polo-like kinase 1 (Plk1) polo-box domains (PBDs) to phosphothreonine (pThr)/phosphoserine (pSer)-containing sequences is critical for the proper function of Plk1. Although high-affinity synthetic pThr-containing peptides provide starting points for developing PBD-directed inhibitors, to date the efficacy of such peptides in whole cell assays has been poor. This potentially reflects limited cell membrane permeability arising, in part, from the di-anionic nature of the phosphoryl group or its mimetics. In our current article we report the unanticipated on-resin N(τ)-alkylation of histidine residues already bearing a N(π)- alkyl group. This resulted in cationic imidazolium-containing pThr peptides, several of which exhibit single-digit nanomolar PBD-binding affinities in extracellular assays and improved antimitotic efficacies in intact cells. We enhanced the cellular efficacies of these peptides further by applying bio-reversible pivaloyloxymethyl (POM) phosphoryl protection. New structural insights presented in our current study, including the potential utility of intramolecular charge masking, may be useful for the further development of PBD-binding peptides and peptide mimetics.

Keywords: Plk1; cationic dialkyl histidine; crystal structure; intramolecular charge masking; phosphopeptides; polo kinase; polo-box domain.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Alkylation
  • Anions
  • Cell Cycle Proteins / chemistry*
  • Cell Cycle Proteins / metabolism*
  • Cell Proliferation / drug effects
  • Chromatography, Liquid
  • Crystallization
  • Enzyme Stability / drug effects
  • Enzyme-Linked Immunosorbent Assay
  • Esterases / metabolism
  • Fluorescence Polarization
  • HeLa Cells
  • Histidine / chemistry
  • Histidine / metabolism*
  • Humans
  • Phosphopeptides / chemical synthesis*
  • Phosphopeptides / chemistry
  • Phosphopeptides / pharmacology*
  • Polo-Like Kinase 1
  • Prodrugs / pharmacology
  • Protein Binding / drug effects
  • Protein Serine-Threonine Kinases / chemistry*
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Structure, Tertiary
  • Proto-Oncogene Proteins / chemistry*
  • Proto-Oncogene Proteins / metabolism*
  • Tandem Mass Spectrometry

Substances

  • Anions
  • Cell Cycle Proteins
  • Phosphopeptides
  • Prodrugs
  • Proto-Oncogene Proteins
  • Histidine
  • Protein Serine-Threonine Kinases
  • Esterases