ROS are evolutionary conserved cell-to-cell signals

Abstract

Cell-to-cell communication is fundamental to multicellular organisms, as well as to unicellular organisms living in a microbiome. It is thought to have evolved as a stress- or quorum-sensing mechanism in unicellular organisms. A unique cell-to-cell communication mechanism that uses reactive oxygen species (ROS) as a signal (termed the ROS wave) was recently identified in flowering plants. This process is essential for systemic signaling and plant acclimation to stress and can spread from a small group of cells to the entire plant within minutes. Whether this signaling process is found in other organisms is however unknown. Here we report that a ROS-mediated cell-to-cell signaling process, like the ROS wave, can be found in ferns, mosses, multicellular and unicellular algae, amoeba, and mammalian cells. We further show that this process can be triggered by extracellular H2O2 application and blocked by inhibition of NADPH oxidases, and that at least in unicellular algae growing as a lawn on an agar plate, it communicates important stress-response signals between cells. Taken together, our findings suggest that an active process of cell-to-cell ROS signaling, like the ROS wave, evolved before unicellular and multicellular organisms diverged. This mechanism could have communicated an environmental stress signal between cells and coordinated the acclimation response of cells living in a community. The finding of a signaling process, like the ROS wave, in mammalian cells further contributes to our understanding of different diseases and could impact the development of new drugs that target, for example cancer or heart disease.

Systemic stomatal responses in plants: Coordinating development, stress, and pathogen defense under a changing climate

“…Cell‐to‐cell communication can be found in films or microbiomes composed of unicellular organisms (Combarnous & Nguyen, 2020; Fichman et al, 2023). It is also at the foundation and origin of multicellular organisms.…”

“…It is also at the foundation and origin of multicellular organisms. A recent study has shown that the ROS wave is a highly conserved cell‐to‐cell signal that can be found in communities of unicellular eukaryotes, plants from different lineages, monolayers of mammalian cells, and even organs of animals (Fichman et al, 2023). Basic cell‐to‐cell signals such as the ROS wave, electric wave and perhaps even the calcium wave could have therefore evolved to link different specialized cell types (e.g., different hair cells) with each other, as well as with other cell types, in a multicellular organism, very early on.…”

Role of NLRP3 in Parkinson's disease: Specific activation especially in dopaminergic neurons

“…ROS are chemically active compounds characterized by unpaired electrons and high oxygen content. They result in both cellular stress and the cellular immune response [ [89] , [90] , [91] , [92] ]. ROS in biological systems can arise from cellular oxidative metabolism or be generated by intracellular oxidases like cyclooxygenase and nicotinamide adenine dinucleotide phosphate oxidase [ [93] , [94] , [95] ].…”

Homeostasis and evolution in relation to regeneration and repair

“…Many details of the processes involved in regeneration, repair and tumourigenesis are still unknown, particularly in mammals. The metabolic and cellular processes that are activated by damage are equivalent to those found in invertebrates and lower vertebrates and are mediated in a lesser or greater degree by processes that involve oxidation-reduction reactions triggering oxidative stress (Fichman et al, 2023;Rennolds & Bely, 2023;Seifert et al, 2023).…”

“…There is a prevalence of glycolysis and pentose phosphate pathway during regeneration in amphibians (Varela-Rodriguez et al, 2020). ROS are early signals that play an essential role during tissue regeneration across the animal kingdom by regulating transcription factors via redox modifications (Fichman et al, 2023). ROS levels are controlled, and low levels stimulate proliferation or promote differentiation of different types of cells, whereas higher levels favour growth arrest; even, pathological high levels of ROS are cytotoxic.…”