Pronounced toxicity differences between homobifunctional protein cross-linkers and analogous monofunctional electrophiles

Chem Res Toxicol. 2013 Nov 18;26(11):1720-9. doi: 10.1021/tx400290j. Epub 2013 Nov 5.

Abstract

Bifunctional electrophiles have been used in various chemopreventive, chemotherapeutic, and bioconjugate applications. Many of their effects in biological systems are traceable to their reactive properties, whereby they can modify nucleophilic sites in DNA, proteins, and other cellular molecules. Previously, we found that two different bifunctional electrophiles--diethyl acetylenedicarboxylate and divinyl sulfone--exhibited a strong enhancement of toxicity when compared with analogous monofunctional electrophiles in both human colorectal carcinoma cells and baker's yeast. Here, we have compared the toxicities for a broader panel of homobifunctional electrophiles bearing diverse electrophilic centers (e.g., isothiocyanate, isocyanate, epoxide, nitrogen mustard, and aldehyde groups) to their monofunctional analogues. Each bifunctional electrophile showed at least a 3-fold enhancement of toxicity over its monofunctional counterpart, although in most cases, the differences were even more pronounced. To explain their enhanced toxicity, we tested the ability of each bifunctional electrophile to cross-link recombinant yeast thioredoxin 2 (Trx2), a known intracellular target of electrophiles. The bifunctional electrophiles were capable of cross-linking Trx2 to itself in vitro and to other proteins in cells exposed to toxic concentrations. Moreover, most cross-linkers were preferentially reactive with thiols in these experiments. Collectively, our results indicate that thiol-reactive protein cross-linkers in general are much more potent cytotoxins than analogous monofunctional electrophiles, irrespective of the electrophilic group studied.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aldehydes / chemistry
  • Aldehydes / toxicity
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cross-Linking Reagents / chemistry*
  • Cross-Linking Reagents / toxicity
  • Epoxy Compounds / chemistry
  • Epoxy Compounds / toxicity
  • Humans
  • Isocyanates / chemistry
  • Isocyanates / toxicity
  • Mechlorethamine / chemistry
  • Mechlorethamine / toxicity
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Saccharomyces cerevisiae / drug effects
  • Saccharomyces cerevisiae / metabolism
  • Thioredoxins / chemistry*
  • Thioredoxins / genetics
  • Thioredoxins / metabolism

Substances

  • Aldehydes
  • Cross-Linking Reagents
  • Epoxy Compounds
  • Isocyanates
  • Recombinant Proteins
  • Mechlorethamine
  • Thioredoxins