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J. Biol. Chem., Vol. 282, Issue 30, 21866-21872, July 27, 2007

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Evidence against Functional Interaction between Aquaporin-4 Water Channels and Kir4.1 Potassium Channels in Retinal Müller Cells^*

From the Departments of Medicine and Physiology, Cardiovascular Research Institute, University of California, San Francisco, California, 94143-0521

Indirect evidence suggests that the Müller/glial cell water channel aquaporin-4 (AQP4) modulates K⁺ channel function of the closely associated Kir4.1 protein. We used patch clamp to compare Kir4.1 K⁺ channel function in freshly isolated Müller cells from retinas of wild-type (+/+) and AQP4 knock-out (-/-) mice. Immunocytochemistry showed a comparable Kir4.1 protein expression pattern in Müller cells from +/+ and -/- retinas, with greatest expression at their end feet. Osmotic water permeability was >4-fold reduced in -/- than in +/+ Müller cells. Resting membrane potential did not differ significantly in +/+ versus -/- Müller cells (-64 ± 1 versus -64 ± 1 mV, S.E., n = 24). Whole-cell K⁺ currents recorded with a micropipette inserted into the cell soma were Ba²⁺-sensitive and showed no significant differences in magnitude in +/+ versus -/- Müller cells (1.3 ± 0.1 versus 1.2 ± 0.1 nA at -160 mV) or in inwardly rectifying current-voltage relationships. Spatially resolved K⁺ currents generated by pulsed K⁺ injections along Müller cell bodies were also comparable in +/+ versus -/- Müller cells. Single-channel cell-attached patch clamp showed comparable unitary conductance, current-voltage data, and open probability in +/+ versus -/- Müller cells. Thus, contrary to the generally accepted view, our results provide direct evidence against functionally significant AQP4 modulation of Müller cell Kir4.1 K⁺ channel function.

Received for publication, April 17, 2007 , and in revised form, May 21, 2007.

^* The work was supported by National Institutes of Health Grants EY13574, DK35124, EB00415, HL73856, HL59198, and DK72517 and Research Development Program and Drug Discovery grants from the Cystic Fibrosis Foundation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ These authors contributed equally.

² To whom correspondence should be addressed: 1246 Health Sciences East Tower, Cardiovascular Research Institute, University of California, San Francisco, CA 94143-0521. Tel.: 415-476-8530; Fax: 415-665-3847; E-mail: verkman{at}itsa.ucsf.edu.

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