Receptor-mediated signaling leads to transient changes in redox state, resulting in reversible oxidation of protein cysteine thiols. Numerous signaling proteins have been identified as being redox sensitive; however, to date, most investigations have focused on the ramifications of isolated protein modifications on cellular phenotypes. We propose that reversible thiol oxidation of proteins in a signaling network and their systemic interactions introduce features in the dynamics and control of cellular responses that are unique compared with isolated oxidative protein modifications. Simulations of dynamic redox regulation in different cellular contexts reveal feasible regulatory features for future experimental investigation. We suggest that location within a network, compartmentalization, and the degree of connectivity between redox proteins can dramatically modulate cellular information processing.