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J. Biol. Chem., Vol. 279, Issue 10, 8732-8739, March 5, 2004

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The Glycolytic Enzyme Aldolase Mediates Assembly, Expression, and Activity of Vacuolar H⁺-ATPase^*

Ming Lu, Yuri Y. Sautin¶, L. Shannon Holliday||**, and Stephen L. Gluck

From the Department of Medicine, University of California, San Francisco, California 94143 and the Departments of ^¶Medicine and ^**Anatomy and Cell Biology, University of Florida College of Medicine and the ^||Department of Orthodontics, University of Florida College of Dentistry, Gainesville, Florida 32610

Vacuolar H⁺-ATPases (V-ATPases) are a family of highly conserved proton pumps that couple hydrolysis of cytosolic ATP to proton transport out of the cytosol. How ATP is supplied for V-ATPase-mediated hydrolysis and for coupling of proton transport is poorly understood. We have reported that the glycolytic enzyme aldolase physically associates with V-ATPase (Lu, M., Holliday, L. S., Zhang, L., Dunn, W. A., and Gluck, S. L. (2001) J. Biol. Chem. 276, 30407–30413). Here we show that aldolase interacts with three different subunits of V-ATPase (subunits a, B, and E). The binding sites for the V-ATPase subunits on aldolase appear to be on distinct interfaces of the glycolytic enzyme. Aldolase deletion mutant cells were able to grow in medium buffered at pH 5.5 but not at pH 7.5, displaying a growth phenotype similar to that observed in V-ATPase subunit deletion mutants. Abnormalities in V-ATPase assembly and protein expression observed in aldolase deletion mutant cells could be fully rescued by aldolase complementation. The interaction between aldolase and V-ATPase increased dramatically in the presence of glucose, suggesting that aldolase may act as a glucose sensor for V-ATPase regulation. Taken together, these findings provide functional evidence that the ATP-generating glycolytic pathway is directly coupled to the ATP-hydrolyzing proton pump through physical interaction between aldolase and V-ATPase.

Received for publication, April 14, 2003 , and in revised form, December 4, 2003.

^* This work was supported in part by National Institutes of Health Grants DK64977 (to M. L.) and DK64095 (to S. L. G.). 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.

To whom correspondence should be addressed: Dept. of Medicine, University of California, San Francisco, HSE 672, Box 0532, 513 Parnassus Ave., San Francisco, CA 94143-0532. Tel.: 415-502-7996; Fax: 415-476-3381; E-mail: minglu{at}medicine.ucsf.edu.

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