Protein-protein interactions enable rapid adaptive response to osmotic stress in fish gills

Abstract

Cells respond to changes in osmolality with compensatory adaptations that re-establish ion homeostasis and repair disturbed aspects of cell structure and function. These physiologically complex processes can be separated into two functionally distinct cellular phases. The first phase operates to temporarily minimize cellular damage and stabilize critical cell functions necessary for survival. This phase is contingent upon the ability to generate a rapid adaptive response. For this reason, it occurs largely in the absence of de novo protein synthesis and instead relies upon modifying the activity of existing cellular proteins through protein-protein interactions and post-translational modifications. The second phase of the osmotic stress response is centered upon adjusting the expression of specific effector proteins required to re-establish cellular homeostasis. This phase is dependent on the completion of signal transduction events, as well the transcription and translation of target genes, and is therefore characterized by a significant temporal delay and not detected until several hours post exposure. Osmotic effector proteins central to the second phase, such as ion transporting proteins and organic osmolyte generating enzymes, have been studied in considerable detail. However, knowledge surrounding the first phase of the osmotic stress response is limited. This article focuses on recent insights into the players and interactions governing the first phase of the osmotic stress response with specific emphasis on protein-protein interactions.

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Figures and Tables

Figure 1 Expression profiles of osmotically-regulated genes illustrating the two-phase osmotic stress response (shaded areas). Genes mediating protein-protein interactions (open bars; FKBP-51, TCTP, IGFBP from left to right) and putatively involved in the first phase of the osmotic stress response (darkly shaded area) are significantly differentially expressed earlier than effector proteins (filled bars; Na⁺, K⁺ ATPase alpha subunit, Na⁺ channel IX alpha subunit, organic osmolyte catalyzing enzymes: cysteine sulfinic acid decarboxylase (taurine), glutamate decarboxylase (GABA) and inositol monophosphatase (inositol) (from left to right)) involved in the second phase (lightly shaded area). Because the completion of the second phase is dependent upon osmosensing and signal transduction events, as well as de novo protein synthesis, changes in the abundance of effector proteins are not detected until 12 hours of osmotic stress exposure. Protein-protein interactions, which enable rapid adaptive responses in the absence of changes in gene expression, may therefore underlie the first phase of the osmotic stress response. Expression and significance values were extracted from Evans and Somero,5 and are illustrated as the absolute value of the log fold change. Open asterisks denote earliest time point of significant expression for phase 1 genes. Closed asterisks denote earliest time point of significant expression during of phase 2 effector proteins.

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