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J. Biol. Chem., Vol. 280, Issue 31, 28424-28429, August 5, 2005

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Prostaglandin Signaling in the Renal Collecting Duct

RELEASE, REUPTAKE, AND OXIDATION IN THE SAME CELL^*

Teruhisa Nomura, Hee Yoon Chang, Run Lu, Joseph Hankin, Robert C. Murphy, and Victor L. Schuster¶||

From the Departments of Medicine and ^¶Physiology & Biophysics, Albert Einstein College of Medicine, Bronx, New York 10461 and the National Jewish Medical and Research Center, Division of Cell Biology, Denver, Colorado 80206

Prostaglandins mediate autacrine and paracrine signaling over short distances. We used the renal collecting duct as a model system to test the hypothesis that local control of prostaglandin signaling is achieved by expressing inactivation in the same cell as synthesis. Immunocytochemical studies demonstrated that renal collecting ducts in situ express the prostaglandin (PG) synthesis enzyme, cyclooxygenase-1 (COX-1), as well as both components of prostaglandin metabolic inactivation, i.e. the prostaglandin uptake carrier prostaglandin transporter (PGT) and the enzyme 15-hydroxyprostaglandin dehydrogenase. We characterized this system further using the collecting duct cell line Madin-Darby canine kidney (MDCK), which retains COX-2 and prostaglandin dehydrogenase expression but which has lost PGT expression. When we reintroduced PGT, it was correctly sorted to the apical membrane where it altered the sidedness of prostaglandin E2 (PGE2) release, a process we call "vectorial release via sided reuptake." Importantly, although COX-2 and prostaglandin dehydrogenase are expressed in the same MDCK cell, they must be compartmentalized because even in the presence of excess dehydrogenase newly synthesized PGE2 is released largely un-oxidized. However, when PGE2 undergoes first release and then PGT-mediated reuptake, significant oxidation takes place, suggesting that PGT imports PGE2 into the prostaglandin dehydrogenase compartment. Our data are consistent with a new model that offers significant new mechanisms for the fine control of eicosanoid signaling.

Received for publication, July 22, 2004 , and in revised form, April 25, 2005.

^* This work was supported by National Institutes of Health Grants R01DK049688 and P50DK064236 (to V. L. S.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental "Methods," Tables 1 and 2, and supplemental Figs. 1–3.

^|| To whom correspondence should be addressed: Albert Einstein College of Medicine, Belfer Bldg., Rm. 1008, 1300 Morris Park Ave., Bronx, NY 10461. Tel.: 718-430-8560; Fax: 718-430-8649; E-mail: schuster{at}aecom.yu.edu.

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