Chloride Transport Across Isolated Opercular Epithelium of Killifish: A Membrane Rich in Chloride Cells

Karnaky, Karl John; Degnan, Kevin J.; Zadunaisky, J. A.

doi:10.1126/science.831273

Cited by 149 publications

(45 citation statements)

References 24 publications

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“…This is also the case for the leakiness of tight junctions, which promote paracellular Na + extrusion across gill epithelium (Karnaky et al, 1977;Degnan and Zadunaisky, 1980). The decreased osmotic permeability of gill and opercular epithelia in fish exposed to strongly hyperhaline environments represents a qualitative shift in the adaptive strategy relative to the increase in osmotic permeability that occurs when euryhaline fish are acclimated from freshwater to regular seawater (35 g kg…”

Section: Osmoregulatory Strategies At Extreme Salinitiesmentioning

confidence: 99%

Physiological mechanisms used by fish to cope with salinity stress

Kültz

2015

Journal of Experimental Biology

325

161

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Salinity represents a critical environmental factor for all aquatic organisms, including fishes. Environments of stable salinity are inhabited by stenohaline fishes having narrow salinity tolerance ranges. Environments of variable salinity are inhabited by euryhaline fishes having wide salinity tolerance ranges. Euryhaline fishes harbor mechanisms that control dynamic changes in osmoregulatory strategy from active salt absorption to salt secretion and from water excretion to water retention. These mechanisms of dynamic control of osmoregulatory strategy include the ability to perceive changes in environmental salinity that perturb body water and salt homeostasis (osmosensing), signaling networks that encode information about the direction and magnitude of salinity change, and epithelial transport and permeability effectors. These mechanisms of euryhalinity likely arose by mosaic evolution involving ancestral and derived protein functions. Most proteins necessary for euryhalinity are also critical for other biological functions and are preserved even in stenohaline fish. Only a few proteins have evolved functions specific to euryhaline fish and they may vary in different fish taxa because of multiple independent phylogenetic origins of euryhalinity in fish. Moreover, proteins involved in combinatorial osmosensing are likely interchangeable. Most euryhaline fishes have an upper salinity tolerance limit of approximately 2× seawater (60 g kg −1). However, some species tolerate up to 130 g kg −1 salinity and they may be able to do so by switching their adaptive strategy when the salinity exceeds 60 g kg −1. The superior salinity stress tolerance of euryhaline fishes represents an evolutionary advantage favoring their expansion and adaptive radiation in a climate of rapidly changing and pulsatory fluctuating salinity. Because such a climate scenario has been predicted, it is intriguing to mechanistically understand euryhalinity and how this complex physiological phenotype evolves under high selection pressure.

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Section: Osmoregulatory Strategies At Extreme Salinitiesmentioning

confidence: 99%

Physiological mechanisms used by fish to cope with salinity stress

Kültz

2015

Journal of Experimental Biology

325

161

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“…The opercular epithelium lining the inside of the gill chamber of the teleost F. 1heteroclitu8 contains an abundance of chloride cells (Burns &( Copeland, 1950;Karnaky & Kinter, 1977) identical in fine structure to the chloride cells of the gill epithelium (Karnaky & Kinter, 1977). In a preliminary report, Karnaky, Degnan & Zadunaisky (1977) mounted the opercular epithelium of 100 % seawateradapted F. heteroclitw9 as a flat sheet between two halves of a Lucite chamber and demonstrated that the measured short-circuit current was equivalent to the net active secretion of CO-ions from the blood side to the seawater side of this epithelium. This third alternative approach to the study of teleost osmoregulation, the isolated, short-circuited opercular epithelium of F. heteroclitu8, avoids many of the technical problems involved in intact fish and isolated, perfused gill preparations and can provide some of the needed biophysical data required for a better understanding of teleost osmoregulation.…”

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confidence: 97%

Active chloride transport in the in vitro opercular skin of a teleost (Fundulus heteroclitus), a gill‐like epithelium rich in chloride cells

Degnan¹,

Karnaky²,

Zadunaisky³

1977

The Journal of Physiology

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194

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K. J. DEGNAN AND OTHERS net Cl-blood side to seawater side flux of 162-8 isA/cm2 which was not statistically different (P > 0.70) from the mean short-circuit current of 158-6 + 163 ,uA/cm2 for these flux studies. The mean Na+ blood side to seawater side flux was 32-2 + 3-3 ,uA/cm2 and the mean Na+ seawater side to blood side flux was 34-8 + 4-1 isA/cm2, resulting in no significant (P > 0*20) net flux of this cation. Similar results were obtained with short-circuited epithelia of seawater-adapted fish when bathed on both sides with Ringer and gassed with 95 % 02/5 % CO2.5. Ouabain (105 M), furosemide (10-3 M), thiocyanate (10-2 M), adrenaline (1I0 M), and anoxia (100 % N2) decreased the short-circuit current 92*7, 85-0, 45-3, 62-6, and 83'3 % respectively. Theophylline (104 M) stimulated the short-circuit current 54-9 %. Increasing the HC03-concentration in the bathing solutions had a stimulatory effect on the short-circuit current and the potential difference across epithelia from seawater-adapted fish.6. The opercular epithelia of freshwater-adapted F. heteroclitU8, when bathed on both sides with Ringer, displayed a mean short-circuit current of 94-1 + 10 4 #sA/cm2, a mean transepithelial potential difference of 14-8 + 1*9 mV (blood side positive), and a mean d.c. resistance of 169-0 + 14-0 Q. cm2 (mean + S.E. of mean; n = 20). Isotope flux studies across these short-circuited epithelia revealed a net Cl-blood side to freshwater side flux of 95-2 + 16-1 ,uA/cm2 and no significant net flux of Na+.7. The opercular epithelia of 200 % seawater-adapted F. heteroclitus, when bathed on both sides with Ringer, displayed a mean short-circuit current of 33-5 + 8-5 IzA/cm2, a mean transepithelial potential difference of 10*5 + 2*5 mV (blood side positive), and a mean transepithelial d.c. resistance of 440 7 + 62*6 Q.cm2 (mean + S.E. of mean n = 18). Isotope flux studies across these short-circuited epithelia revealed a net Cl-blood side to seawater side flux of 96-2 + 51*5 ,uA/cm2 and a net Na+ blood side to seawater side flux of 65'3 + 28-6 ,uA/cm2.

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“…Thus active Cl − extrusion would be reduced. To our knowledge, there is no published information on the effect of severe hypoxia on active ion transport rates in killifish in vivo, but in the isolated opercular epithelium of SW-acclimated killifish studied in vitro, complete anoxia reduces the active Cl − current by 75-83% (Karnaky et al, 1977;Barnes et al, 2014). This effect, together with the fact that the reduced TEP in the current study results in about a 70% increase in the electrochemical gradient driving Na + entry, suggests that the electrical response to hypoxia would be deleterious to ionoregulatory homeostasis in SW-acclimated killifish.…”

Section: Resultsmentioning

confidence: 99%

Electrical aspects of the osmorespiratory compromise: TEP responses to hypoxia in the euryhaline killifish (Fundulus heteroclitus) in fresh water and sea water

Wood

Grosell

2015

Journal of Experimental Biology

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The osmorespiratory compromise, the trade-off between the requirements for respiratory and ionoregulatory homeostasis at the gills, becomes more intense during environmental hypoxia. One aspect that has been previously overlooked is possible change in transepithelial potential (TEP) caused by hypoxia, which will influence branchial ionic fluxes. Using the euryhaline killifish, we show that acute hypoxia reduces the TEP across the gills by approximately 10 mV in animals acclimated to both freshwater (FW) and seawater (SW), with a higher P O2 threshold in the former. TEP becomes negative in FW, and less positive in SW. The effects are immediate, stable for at least 3 h, and reverse immediately upon return to normoxia. Hypoxia also blocks the normal increase in TEP that occurs upon transfer from FW to SW, but does not reduce the fall in TEP that occurs with transfer in the opposite direction. These effects may be beneficial in FW but not in SW.

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Chloride Transport Across Isolated Opercular Epithelium of Killifish: A Membrane Rich in Chloride Cells

Cited by 149 publications

References 24 publications

Physiological mechanisms used by fish to cope with salinity stress

Physiological mechanisms used by fish to cope with salinity stress

Active chloride transport in the in vitro opercular skin of a teleost (Fundulus heteroclitus), a gill‐like epithelium rich in chloride cells

Electrical aspects of the osmorespiratory compromise: TEP responses to hypoxia in the euryhaline killifish (Fundulus heteroclitus) in fresh water and sea water

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