Letters to the Editor


    ABSTRACT

The following is the abstract of the article discussed in the subsequent letter:

Walker, V. E., J. W. Stelling, H. E. Miley, and T. J. C. Jacob. Effect of coupling on volume-regulatory response of ciliary epithelial cells suggests mechanism for secretion. Am. J. Physiol. 276 (Cell Physiol. 45): C1432-C1438, 1999.---The ciliary epithelium of the eye secretes the aqueous humor. It is a double epithelium arranged so that the apical surfaces of the nonpigmented ciliary epithelial (NPCE) and pigmented ciliary epithelial (PCE) cells face each other and the basolateral membranes face the inside of the eye and the blood, respectively. We have investigated the volume responses of both single cells and coupled pairs from this tissue to osmotic challenge. Both NPCE and PCE cells undergo regulatory volume increase (RVI) and decrease (RVD) when exposed to hyper- and hyposmotic solution, respectively. In hyposmotic solution single cells swell and return to their original volumes within ~3 min. In nonpigmented cells RVD could be inhibited by blockers of volume-activated Cl- channels [tamoxifen (100%) > quinidine (87%) > DIDS (84%) > 5-nitro-2-(3-phenylpropylamino)benzoic acid (80%) > SITS (58%)] and K+ channels [Ba2+ (31%)]. However, in PCE cells these inhibitors and additionally tetraethylammonium and Gd3+ were without effect. Only bumetanide, an inhibitor of Na+-K+-2Cl- cotransport, was found to have any effect on RVD in PCE cells. NPCE-PCE cell coupled pairs also underwent RVD, but with altered kinetics. The onset of RVD of the PCE cell in a pair occurred approx 80 s before that of the NPCE cell, and the peak swell was reduced. This is consistent with fluid movement from the PCE to the NPCE cell. The effect of the volume-activated Cl- channel inhibitor tamoxifen was to eliminate this difference in the times of onset of RVD in coupled cell pairs and to inhibit RVD in both the NPCE and PCE cells partially. On the basis of these observations we suggest that fluid is transferred from the PCE to the NPCE cell in coupled pairs during cell swelling and the subsequent RVD. Furthermore, we speculate that reciprocal RVI-RVD could underlie aqueous humor secretion.


    LETTER

On volume regulation leading to epithelial fluid transport

To the Editor: This letter is about a paper recently published by Walker et al. (4). While the experiments and the conclusions presented are certainly meritorious, I will point out what I regard as an omission in the introductory statements. I refer to the paragraph that reads:

If these mechanisms were sited on opposite membranes in epithelia, then this arrangement would provide a mechanism for the vectorial transport of solute, and hence water.

This statement is provided without a reference. One implication is that the references cited in the sentences above to the work of Civan et al. (1) or to the review by Hoffmann and Simonsen (3) are sufficient to support that statement. Yet a reading of those materials does not provide such reference. In fact, the only prior publication that has advanced such an idea is apparently a review by Fischbarg (2) and which partially reads:

We hypothesise that transendothelial fluid transport is pulsatile, and is based on cyclic, sequential transient activation of two different sets of osmolyte (ion and solute) transporters and/or channels triggered by changes in cell volume. One set of transporters/channels would serve for cell gain of osmolyte and fluid, and would be the same set the cell utilises during a regulatory volume increase response (RVI set); conversely, the second set of transporters/channels would serve for cell loss of osmolyte and fluid, and would be the same set the cell utilises during a regulatory volume decrease response (RVD set). . . . . Sets of transporters and channels that get separately activated during RVI and RVD (RV sets) are common to most cells; what would distinguish transporting epithelia is that in them these sets would be separately located, one on the basolateral and the other one in the apical cell membranes. Epithelial cells are known to be polarised; for pulsatile fluid transport to work, they would be polarised with the RVI set on one side of the cell, and the RVD set on the other side. As an obvious corollary, in secretory epithelia the RVI set would be basolateral and the RVD set apical, while absorptive epithelia would have the RVI set apical and the RVD set basolateral.

A segment of the text was italicized precisely to highlight the introduction of the new concept.

By the same token, the idea of cyclic volume changes illustrated in Fig. 7 of Walker et al. (4) has a direct precedent in the title, the text, and Fig. 3 of Fischbarg (2), which ought to have been cited in that connection as well.

As an additional benefit, since the 1997 review (2) contains a detailed description of pulsatile fluid secretion, readers of the American Journal of Physiology may find in it several testable hypotheses.


    REFERENCES

1.   Civan, M. M., K. Peterson-Yantorno, M. Coca-Prados, and R. E. Yantorno. Regulatory volume decrease by cultured non-pigmented ciliary epithelial cells. Exp. Eye Res. 54: 181-191, 1992[Medline].

2.   Fischbarg, J. Mechanism of fluid transport across corneal endothelium and other epithelial layers: a possible explanation based on cyclic cell volume regulatory changes. Br. J. Ophthalmol. 81: 85-89, 1997[Free Full Text].

3.   Hoffmann, E. K., and L. O. Simonsen. Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol. Rev. 69: 315-382, 1989[Free Full Text].

4.   Walker, V. E., J. W. Stelling, H. E. Miley, and T. J. C. Jacob. Effect of coupling on volume-regulatory response of ciliary epithelial cells suggests mechanism for secretion. Am. J. Physiol. 276 (Cell Physiol. 45): C1432-C1438, 1999[Abstract/Free Full Text].

Jorge Fischbarg,
Department of Physiology
and Cellular Biophysics
Columbia University
College of Physicians & Surgeons
New York, NY 10032


Am J Physiol Cell Physiol 277(5):C1019-C1019
0002-9513/99 $5.00 Copyright © 1999 the American Physiological Society




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