Prolactin and Extracellular Osmolality Regulate Branchial clc2c Expression in Tilapia
Paige L.K. KeithBethany L HuntMayu InokuchiYoko YamaguchiAndré P. SealeDarren T. LernerE. Gordon GrauJason P. Breves
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Abstract:
Varying and contending models have been proposed to explain how teleost ionocytes facilitate ion uptake from freshwater environments. A recently characterized member of the clc Cl − channel family ( clc2c ) has been proposed as a conduit for basolateral Cl − transport by Na + /Cl − cotransporter ( ncc )‐expressing ionocytes of stenohaline zebrafish. It is unknown to what extent clc2c is expressed in gill of euryhaline species, such as Mozambique tilapia, and whether expression is modulated in response to extrinsic (salinity) and intrinsic (hormones) factors. Here, we investigated prolactin (Prl) and local osmotic control of clc2c mRNA levels. First, branchial clc2c expression was markedly enhanced in freshwater‐acclimated tilapia compared with seawater‐acclimated tilapia. To investigate endocrine control of this salinity‐dependent expression, we injected hypophysectomized tilapia with ovine Prl. Ovine Prl induced a >8000‐fold increase in clc2c expression from saline‐injected controls. To then test whether Prl regulates clc2c expression in a gill‐autonomous fashion, we incubated gill filaments for 24 hours in the presence of homologous Prls, Prl 177 and Prl 188 . By 24 hours, Prl 188 stimulated clc2c expression ~5‐fold from controls. We then incubated filaments in media ranging from 280 to 450 mOsm/kg for 3 hours to investigate the possibility that extracellular osmolality exerts a local effect on clc2c expression. clc2c showed higher expression with decreasing media osmolalities. Collectively, our results suggest that both hormonal and extracellular osmotic conditions direct clc2c expression in branchial ionocytes. We propose that multifactorial modulation of clc2c expression contributes to the excellent adaptability of Mozambique tilapia to variations in environmental salinity. Support or Funding Information Supported by Start‐Up Funds (Skidmore College) to J.P.B.Keywords:
Euryhaline
Osmoregulation
Osmotic concentration
Oreochromis mossambicus
Euryhaline
Oreochromis mossambicus
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Euryhaline
Oreochromis mossambicus
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Euryhaline
Oreochromis mossambicus
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Euryhaline
Oreochromis mossambicus
Osmoregulation
Osmotic shock
Osmotic concentration
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Oreochromis mossambicus
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1. The euryhaline marine ciliate, Miamiensis avidus, was investigated for its ability to regulate solutes and water when exposed to different external salinities. 2. In 100% sea water-culture medium, M. avidus had the following inorganic ion concentrations (mM/kg cells): Na+—87.9; K+—73.7; Ca++3.7;—Mg++—28.5; Cl-—60.8. 3. In 100% sea water-culture medium, [Na+]i, [Cl-]i, [Mg++]i and [Ca++]i were lower than the environmental values and [K+]i was greater than [K+]o. [Na+]i and [Cl-]i changed with changes in external salinity, but were kept lower than [Na+]o and [Cl-]o. [K+]i, [Mg++]i and [Ca++]i were maintained at fairly constant internal concentrations. 4. The contractile vacuole output was related to external osmolarity. Osmolarities greater than that of 100% sea water resulted in decreased vacuole output. In dilute sea water, output increased. 5. Cell volume determinations indicated a return toward the original volume after swelling or shrinking caused by transfer to media of different osmolarities. 6. The results suggest that M. avidus maintains itself hyperosmotic to the environment at all salinities. The contractile vacuole regulates cell volume by expelling water that enters passively.
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Osmoregulation
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WATER BALANCE IN TELEOST FISH IS MAINTAINED WITH CONTRIBUTIONS FROM THE MAJOR OSMOREGULATORY ORGANS: intestine, gills, and kidney. Overall water fluxes have been studied in all of these organs but not until recently has it become possible to approach the mechanisms of water transport at the molecular level. This mini-review addresses the role of the kidney in osmoregulation with special emphasis on euryhaline teleosts. After a short review of current knowledge of renal functional morphology and regulation, we turn the focus to recent molecular investigations of the role of aquaporins in water and solute transport in the teleost kidney. We conclude that there is much to be achieved in understanding water transport and its regulation in the teleost kidney and that effort should be put into systematic mapping of aquaporins to their tubular as well as cellular localization.
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Osmoregulation
Water Transport
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Oreochromis mossambicus
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Osmotic concentration
Plasma osmolality
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Euryhaline teleost fish are characterized by their ability to tolerate a wide range of environmental salinities by modifying the function of osmoregulatory cells and tissues. In this study, we experimentally addressed the age-related decline in the sensitivity of osmoregulatory transcripts associated with a transfer from fresh water (FW) to seawater (SW) in the euryhaline teleost, Mozambique tilapia, Oreochromis mossambicus. The survival rates of tilapia transferred from FW to SW were inversely related with age, indicating that older fish require a longer acclimation period during a salinity challenge. The relative expression of Na+/K+/2Cl- cotransporter 1a (nkcc1a), which plays an important role in hyposmoregulation, was significantly upregulated in younger fish after SW transfer, indicating a clear effect of age in the sensitivity of branchial ionocytes. Prolactin (Prl), a hyperosmoregulatory hormone in O. mossambicus, is released in direct response to a fall in extracellular osmolality. Prl cells of 4-month-old tilapia were sensitive to hyposmotic stimuli, while those of >24-month-old fish did not respond. Moreover, the responsiveness of branchial ionocytes to Prl was more robust in younger fish. Taken together, multiple aspects of osmotic homeostasis, from osmoreception to hormonal and environmental control of osmoregulation, declined in older fish. This decline appears to undermine the ability of older fish to survive transfer to hyperosmotic environments.
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Fish that inhabit an environment of fluctuating salinity (e.g. estuaries, intertidal zones) are frequently exposed to osmotic challenges. These euryhaline fish must cope with unpredictable salinity changes, and thus must respond quickly to alterations in environmental osmolality. Some euryhaline fish, e.g. tilapia, also face irregular and longer periods of high salinity, for instance during seasonal droughts in arid areas. Even though teleosts are osmoregulators, hyperosmotic stress leads to a significant increase in plasma osmolality. To prevent the detrimental effects that result from hyperosmotic stress if unaccounted for, cells must compensate for increased plasma osmolality. A previously immortalized Mozambique tilapia ( Oreochromis mossambicus ) cell line derived from the brain (OmB) was utilized to expose the mechanisms individual cells employ to survive this stress. Cultured cells were exposed to either control isosmotic media (300mOsm/kg), 450mOsm/kg, which is physiologically relevant for fish plasma, or maximum cellular tolerance levels of 700mOsm/kg for 8 days. Hyperosmotic medium was prepared by increasing NaCl concentration. Cell proliferation and time to confluency, as well as passage numbers, were monitored in treatment and control cells. The morphology and general appearance of experimental and control cells were also periodically monitored via phase contrast microscopy. In addition, proteins that are altered in their abundance by hyperosmolality were identified by label‐free quantitative proteomics to explain cellular phenotypes associated with hyperosmotic stress acclimation. Based on our results we conclude that the tilapia proteome is extensively and specifically modulated during hyperosmotic stress to adjust cellular physiology, stress tolerance, and morphology. Support or Funding Information This work was supported by National Science Foundation, IOB 1355098.
Oreochromis mossambicus
Euryhaline
Osmotic concentration
Osmotic shock
Osmoregulation
Proteome
Plasma osmolality
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