Regulation of osmotic stress transcription factor 1 (Ostf1) in tilapia (Oreochromis mossambicus) gill epithelium during salinity stress

J Exp Biol. 2006 Aug;209(Pt 16):3257-65. doi: 10.1242/jeb.02352.

Abstract

Mechanisms of induction of osmotic stress transcription factor 1 (Ostf1) were analyzed in gill epithelium of tilapia exposed to salinity stress. Experiments with primary cultures of gill epithelial cells revealed that hyperosmotic Ostf1 induction was independent of systemic factors. In addition, the synthetic glucocorticoid receptor agonist dexamethasone did not affect Ostf1 levels, arguing against cortisol being the signal for Ostf1 induction during hyperosmotic stress. Exposure of primary gill cell cultures to a hyperosmotic agent that is cell permeable and non-hypertonic (glycerol) did not trigger Ostf1 induction. However, when gill cells were exposed to hypertonicity (either in the form of NaCl or other forms) Ostf1 was rapidly and significantly induced. Analysis of hnRNA and mRNA levels revealed that Ostf1 upregulation in gill cells of intact fish and primary cultures of gill epithelial cells was mediated by transient mRNA stabilization. In addition to the initial transient mRNA stabilization a subsequent transcriptional induction of Ostf1 was observed. In cultured gill cells increase in Ostf1 mRNA synthesis was stable and very potent, whereas in gill cells of intact fish this increase was transient. This observation suggests positive feedback by Ostf1 or one of its targets and negative feedback by systemic factors on Ostf1 transcription. We conclude that Ostf1 induction in gill epithelial cells of tilapia exposed to salinity stress (1) is independent of cortisol or other systemic factors; (2) depends on hypertonicity as the signal; and (3) is based on transient mRNA stabilization. Moreover, our data on primary cell cultures show that systemic signals are necessary to prevent sustained transcriptional induction of Ostf1 during hyperosmotic stress, indicating feedback regulation and a high degree of complexity of osmosensing and signaling networks in euryhaline fishes.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Cells, Cultured
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelium / drug effects
  • Epithelium / metabolism
  • Fish Proteins / genetics*
  • Fish Proteins / metabolism
  • Gills / cytology
  • Gills / drug effects
  • Gills / metabolism*
  • Hydrocortisone / metabolism
  • Osmotic Pressure
  • Polymerase Chain Reaction
  • RNA Stability
  • RNA, Heterogeneous Nuclear / metabolism
  • RNA, Messenger / chemistry
  • RNA, Messenger / metabolism
  • Sequence Analysis, RNA
  • Sodium Chloride / pharmacology*
  • Tilapia / genetics*
  • Tilapia / metabolism
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Up-Regulation* / drug effects

Substances

  • Fish Proteins
  • RNA, Heterogeneous Nuclear
  • RNA, Messenger
  • Transcription Factors
  • Sodium Chloride
  • Hydrocortisone