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Am J Physiol Renal Physiol (May 18, 2004). doi:10.1152/ajprenal.00439.2003
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Submitted on December 11, 2003
Accepted on May 17, 2004

Membrane organization and function of M1- and M23- isoforms of aquaporin-4 in epithelial cells

Claudia Silberstein1, Richard Bouley1, Yan Huang1, Pingke Fang1, Nuria Pastor-Soler1, Dennis Brown1, and Alfred N. Van Hoek1*

1 Massachusetts General Hospital and Harvard Medical School, Renal Unit and Program in Membrane Biology, Boston, MA 02114, USA

* To whom correspondence should be addressed. E-mail: vanhoek{at}receptor.mgh.harvard.edu.

Aquaporin-4 water channels (AQP4) exist as heterotetramers of M1 and M23 splice variants and appear to be present in orthogonal arrays of intramembraneous particles (OAPs) visualized by freeze-fracture microscopy. We report that AQP4 forms OAPs in rat gastric parietal cells, but not in parietal cells from the mouse or kangaroo rat. Furthermore, the organization of principal cell OAPs in Brattleboro rat kidney is perturbed by vasopressin (AVP). Membranes of LLC-PK1 cells expressing M23-AQP4 showed large, abundant OAPs, but none were detectable in cells expressing M1-AQP4. Measurements of osmotic swelling of transfected LLC-PK1 cells using video microscopy, gave Pf values (cm/s), of 0.018 (M1-AQP4), 0.019 (M23-AQP4) and 0.003 (control). Quantitative immunoblot and immunofluorescence showed an 8-fold greater expression of M1- over M23-AQP4 in the cell lines, suggesting that single-channel pf (cm3/s) is much greater for the M23 variant. Somatic fusion of M1- and M23-AQP4 cells (Pf = 0.028 cm/s) yielded OAPs that were fewer and smaller than in M23-cells alone and M1:M23 expression ratios (~1:4), normalized to AQP4 in M1 or M23 cells indicated a reduced single-channel pf for the M23 variant. Expression of an S111E-M23-AQP4 mutant produced ~1.5-fold greater single-channel pf and OAPs that were up to 2.5-fold larger than wild type M23-AQP4 OAPs, suggesting that a putative PKA phosphorylation site S111 is involved in OAP formation. We conclude that the higher order organization of AQP4 in OAPs increases single channel osmotic water permeability by one order of magnitude and that differential cellular expression levels of the two isoforms could regulate this organization.




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