Effects of an outward water flow on potassium currents in a squid giant axon

Kukita, Fumio; Yamagishi, Shunichi

doi:10.1007/bf01870797

Cited by 12 publications

(5 citation statements)

References 23 publications

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“…In this study, an attempt has been made to prevent K+ accumulation by outward water flow maintained by an osmotic gradient across the axolemma. In a previous paper, it was reported that the outward osmotic water flow increased the undershoot of the action potential and the outward K+ current under voltage clamp and decreased the inward tail K+ current (Kukita & Yamagishi, 1983). In this paper, it is demonstrated that these effects were mainly due to the removal of K+ accumulation in the periaxonal space.…”

Section: Introductionmentioning

confidence: 60%

“…Hypertonic conditions without water flow neither change the shape nor amplitude of the action potential, nor the ionic currents, except for the time courses and conductances (Kukita & Yamagishi, 1979;Kukita, 1982). However, when an outward water flow was induced, K+ currents changed (Kukita & Yamagishi, 1983) and here changes are ascribed to the elimination of K+ accumulation in the periaxonal space. K+ accumulation may not be removed by a mere shrinkage of the Schwann cells because the application of hypertonic solutions did not eliminate K+ accumulation unless the outward water flow was induced by creating an osmotic gradient (Fig.…”

Section: Discussionmentioning

confidence: 86%

“…Hindmost stellar giant axons (400-600 ,um in diameter) of squid (Doryteuthis bleekeri) were used. The axon was intracellularly perfused using the modified squeezing method (Kukita, 1982) and voltage clamped as described previously (Kukita & Yamagishi, 1983), except that series resistance compensation was performed as in Cole & Moore (1960). All membrane current data were obtained with a microcomputer (Nicolet 1280, U.S.A.) using a sampling time of 5 4us after passing through a low-pass Bessel filter of 50 kHz.…”

Section: Methodsmentioning

confidence: 99%

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Removal of periaxonal potassium accumulation in a squid giant axon by outward osmotic water flow.

Kukita

1988

The Journal of Physiology

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1. Periaxonal potassium accumulation does not occur in a squid giant axon when outward water flow is maintained by an osmotic gradient across the axolemma. Potassium concentrations in the periaxonal space were calculated from the potassium potentials (EK) for the tail K+ current. With outward water flow, the periaxonal K+ concentration was maintained at values less than or close to the K+ concentration in the bathing solution. 2. Outward osmotic water flow was produced by adding 1 M-urea to the isotonic external solution. This was sufficient to prevent K+ accumulation, but it had no effect if applied to both sides of the axolemma. 3. The thickness of the periaxonal space (theta s) and the permeability of the extracellular barrier (Ps) were estimated using a three-compartment model. Under isotonic conditions they were 25 nm and 3.7 micron/s, respectively. With outward water flow, either Ps or theta s or both must increase by a large factor, since K+ accumulation is prevented. 4. Instantaneous I-V relations with outward water flow showed outward rectification and no time-dependent changes in their shape. When external K+ concentration was increased, the curves became more linear.

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Section: Introductionmentioning

confidence: 60%

Section: Discussionmentioning

confidence: 86%

Section: Methodsmentioning

confidence: 99%

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Removal of periaxonal potassium accumulation in a squid giant axon by outward osmotic water flow.

Kukita

1988

The Journal of Physiology

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“…Ion channels are pores and may be able to pass water as well as ions (Kukita & Yamagishi, 1983). In characean ceils, it is known that pores exist that pass water, but not ions (Kiyosawa & Ogata, 1987).…”

Section: Discussionmentioning

confidence: 99%

Nature of the water channels in the internodal cells ofNitellopsis

Wayne

Tazawa

1990

J. Membrain Biol.

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The hydraulic resistance was measured on internodal cells of Nitellopsis obtusa using the method of transcellular osmosis. The hydraulic resistance was approximately 2.65 pm-1 sec Pa, which corresponds to an osmotic permeability of 101.75 microns sec-1 (at 20 degrees C). p-Chloromercuriphenyl sulfonic acid (pCMPS) (0.1-1 mM, 60 min) reversibly increases the hydraulic resistance in a concentration-dependent manner. pCMPS does not have any effect on the cellular osmotic pressure. pCMPS increases the activation energy of water movement from 16.84 to 32.64 kJ mol-1, indicating that it inhibits water movement by modifying a low resistance pathway. pCMPS specifically increases the hydraulic resistance to exosmosis, but does not influence endosmosis. By contrast, nonyltriethylammonium (C9), a blocking agent of K+ channels, increases the hydraulic resistance to endosmosis, but does not affect that to exosmosis. These data support the hypothesis that water moves through membrane proteins in characean internodal cells and further that the polarity of water movement may be a consequence of the differential gating of membrane proteins on the endo- and exoosmotic ends.

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“…The time to peak of the undershoot from the beginning of the action potential train did not alter. the external solution is doubled by the addition of a nonelectrolyte, producing efflux of water across the axonal membrane and presumably contraction of cells surrounding the giant fibre (Kukita & Yamagishi, 1983;Kukita, 1988;. Figure 2 shows an example of K+ currents evoked by stepwise depolarizations of different duration.…”

Section: Properties Of Action Potential Trainsmentioning

confidence: 99%

K+ accumulation and K+ conductance inactivation during action potential trains in giant axons of the squid Sepioteuthis.

Inoue

Tsutsui

Brown

1997

The Journal of Physiology

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1. During action potential trains in giant axons from the squid Sepioteuthis, decline of the peak level of the undershoot potential was observed. The time course of the decline of the undershoot could be fitted with a three‐exponential function with time constants of approximately 25, approximately 400 and approximately 7,000 ms, respectively. 2. When the osmolarity of the external solution was doubled by adding glucose (1.2 M), the fast component of undershoot decline, but not the medium and slow components, was significantly reduced. 3. Under voltage clamp in high osmolarity solutions where K+ accumulation was completely removed, repeated depolarizing pulses at 40 Hz (designed to mimic a train of action potentials) elicited K+ currents whose peak value declined. The decline is consistent with inactivation of the K+ conductance (gK). The decline of gK was fitted by a two‐exponential function with time constants of approximately 400 and approximately 7,000 ms, respectively. 4. Interventions designed to modify Schwann cell physiology, such as high frequency stimulation (100 Hz, 2 min), externally applied ouabain (100‐500 microM), L‐glutamate (100 microM), ACh (100 microM), Co2+ (5mM), Ba2+ (2mM), or removal of external Ca2+ by EGTA, had no significant effects on the fast, medium or slow components of undershoot decline. 5. The results suggest that the fast component of undershoot decline represents K+ accumulation in the space between Schwann cell and axolemma. The medium and slow components are the result of axonal gK inactivation. Schwann cells appear to be involved in K+ clearance only to the extent that they provide an efficient physical pathway for the clearance of K+ by extracellular diffusion.

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Effects of an outward water flow on potassium currents in a squid giant axon

Cited by 12 publications

References 23 publications

Removal of periaxonal potassium accumulation in a squid giant axon by outward osmotic water flow.

Removal of periaxonal potassium accumulation in a squid giant axon by outward osmotic water flow.

Nature of the water channels in the internodal cells ofNitellopsis

K+ accumulation and K+ conductance inactivation during action potential trains in giant axons of the squid Sepioteuthis.

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