Large-Scale, Quantitative Protein Assays on a High-Throughput DNA Sequencing Chip

Mol Cell. 2019 Mar 7;73(5):1075-1082.e4. doi: 10.1016/j.molcel.2019.02.019.

Abstract

High-throughput DNA sequencing techniques have enabled diverse approaches for linking DNA sequence to biochemical function. In contrast, assays of protein function have substantial limitations in terms of throughput, automation, and widespread availability. We have adapted an Illumina high-throughput sequencing chip to display an immense diversity of ribosomally translated proteins and peptides and then carried out fluorescence-based functional assays directly on this flow cell, demonstrating that a single, widely available high-throughput platform can perform both sequencing-by-synthesis and protein assays. We quantified the binding of the M2 anti-FLAG antibody to a library of 1.3 × 104 variant FLAG peptides, exploring non-additive effects of combinations of mutations and discovering a "superFLAG" epitope variant. We also measured the enzymatic activity of 1.56 × 105 molecular variants of full-length human O6-alkylguanine-DNA alkyltransferase (SNAP-tag). This comprehensive corpus of catalytic rates revealed amino acid interaction networks and cooperativity, linked positive cooperativity to structural proximity, and revealed ubiquitous positively cooperative interactions with histidine residues.

Keywords: SNAP tag; antibody characterization; high-throughput; in vitro translation; protein array; protein engineering; protein evolution; ribosome display; sequencer hacking; superFLAG.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies / metabolism*
  • Antibody Affinity
  • Antibody Specificity
  • Automation, Laboratory
  • Binding Sites, Antibody
  • Catalysis
  • DNA Mutational Analysis / instrumentation
  • DNA Mutational Analysis / methods*
  • High-Throughput Nucleotide Sequencing / instrumentation
  • High-Throughput Nucleotide Sequencing / methods*
  • Kinetics
  • Mutation
  • O(6)-Methylguanine-DNA Methyltransferase / genetics
  • O(6)-Methylguanine-DNA Methyltransferase / metabolism*
  • Oligonucleotide Array Sequence Analysis / instrumentation
  • Oligonucleotide Array Sequence Analysis / methods*
  • Oligopeptides / genetics
  • Oligopeptides / metabolism*
  • Protein Array Analysis / instrumentation
  • Protein Array Analysis / methods*
  • Protein Binding
  • Protein Engineering
  • Workflow

Substances

  • Antibodies
  • Oligopeptides
  • FLAG peptide
  • O(6)-Methylguanine-DNA Methyltransferase