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J. Biol. Chem., Vol. 279, Issue 50, 52270-52281, December 10, 2004

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Acidocalcisomes and the Contractile Vacuole Complex Are Involved in Osmoregulation in Trypanosoma cruzi^*

Peter Rohloff, Andrea Montalvetti, and Roberto Docampo¶

From the Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana-Champaign, Urbana, Illinois 61802

Trypanosoma cruzi, the etiologic agent of Chagas disease, resists extreme fluctuations in osmolarity during its life cycle. T. cruzi possesses a robust regulatory volume decrease mechanism that completely reverses cell swelling when submitted to hypo-osmotic stress. The efflux of amino acids and K⁺ release could account for only part for this volume reversal. In this work we demonstrate that swelling of acidocalcisomes mediated by an aquaporin and microtubule- and cyclic AMP-mediated fusion of acidocalcisomes to the contractile vacuole complex with translocation of this aquaporin and the resulting water movement are responsible for the volume reversal not accounted for by efflux of osmolytes. Contractile vacuole bladders were isolated by subcellular fractionation in iodixanol gradients, showed a high concentration of basic amino acids and inorganic phosphate, and were able to transport protons in the presence of ATP or pyrophosphate. Taken together, these results strongly support a role for acidocalcisomes and the contractile vacuole complex in osmoregulation and identify a functional role for aquaporin in protozoal osmoregulation.

Received for publication, September 9, 2004 , and in revised form, October 1, 2004.

^* This work was supported in part by National Institutes of Health Grant AI-23259 (to R. D.). 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 Movies 1 and 2.

Both authors contributed equally to this work.

Supported in part by a predoctoral fellowship from the American Heart Association, Midwest Affiliate.

^¶ To whom correspondence should be addressed: Laboratory of Molecular Parasitology, Dept. of Pathobiology and Center for Zoonoses Research, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, 2001 S. Lincoln Ave., Urbana, IL 61802. Tel.: 217-333-3845; Fax: 217-244-7421; E-mail: rodoc{at}uiuc.edu.

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