Synthetic lethality between gene defects affecting a single non-essential molecular pathway with reversible steps

PLoS Comput Biol. 2013 Apr;9(4):e1003016. doi: 10.1371/journal.pcbi.1003016. Epub 2013 Apr 4.

Abstract

Systematic analysis of synthetic lethality (SL) constitutes a critical tool for systems biology to decipher molecular pathways. The most accepted mechanistic explanation of SL is that the two genes function in parallel, mutually compensatory pathways, known as between-pathway SL. However, recent genome-wide analyses in yeast identified a significant number of within-pathway negative genetic interactions. The molecular mechanisms leading to within-pathway SL are not fully understood. Here, we propose a novel mechanism leading to within-pathway SL involving two genes functioning in a single non-essential pathway. This type of SL termed within-reversible-pathway SL involves reversible pathway steps, catalyzed by different enzymes in the forward and backward directions, and kinetic trapping of a potentially toxic intermediate. Experimental data with recombinational DNA repair genes validate the concept. Mathematical modeling recapitulates the possibility of kinetic trapping and revealed the potential contributions of synthetic, dosage-lethal interactions in such a genetic system as well as the possibility of within-pathway positive masking interactions. Analysis of yeast gene interaction and pathway data suggests broad applicability of this novel concept. These observations extend the canonical interpretation of synthetic-lethal or synthetic-sick interactions with direct implications to reconstruct molecular pathways and improve therapeutic approaches to diseases such as cancer.

Publication types

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

MeSH terms

  • Algorithms
  • Animals
  • Catalysis
  • Computational Biology / methods
  • Computer Simulation
  • DNA / metabolism
  • DNA Repair
  • Drosophila melanogaster
  • Enzymes / chemistry
  • Gene Expression Profiling
  • Gene Expression Regulation*
  • Gene Regulatory Networks
  • Humans
  • Models, Genetic
  • Mutation*
  • Neoplasms / metabolism*
  • Neoplasms / pathology
  • Neoplasms / therapy
  • Recombination, Genetic

Substances

  • Enzymes
  • DNA