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Originally published In Press as doi:10.1074/jbc.M003323200 on July 27, 2000

J. Biol. Chem., Vol. 275, Issue 44, 34353-34358, November 3, 2000
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Vacuolar H+-ATPase Localized in Plasma Membranes of Malaria Parasite Cells, Plasmodium falciparum, Is Involved in Regional Acidification of Parasitized Erythrocytes*

Mitsuko HayashiDagger §, Hiroshi YamadaDagger ||, Toshihide Mitamura**, Toshihiro Horii**, Akitsugu YamamotoDagger Dagger , and Yoshinori MoriyamaDagger §§

From the Dagger  Department of Biochemistry, Faculty of Pharmaceutical Sciences, Okayama University, Okayama 700-8530, the ** Institute of Microbial Disease, Osaka University, Suita, Osaka 565-0871, and the Dagger Dagger  Department of Physiology, Kansai Medical University, Moriguchi, Osaka 570-8506, Japan

Recent biochemical studies involving 2',7'-bis-(2-carboxyethyl)-5,6-carboxylfluorescein (BCECF)-labeled saponin-permeabilized and parasitized erythrocytes indicated that malaria parasite cells maintain the resting cytoplasmic pH at about 7.3, and treatment with vacuolar proton-pump inhibitors reduces the resting pH to 6.7, suggesting proton extrusion from the parasite cells via vacuolar H+-ATPase (Saliba, K. J., and Kirk, K. (1999) J. Biol. Chem. 274, 33213-33219). In the present study, we investigated the localization of vacuolar H+-ATPase in Plasmodium falciparum cells infecting erythrocytes. Antibodies against vacuolar H+-ATPase subunit A and B specifically immunostained the infecting parasite cells and recognized a single 67- and 55-kDa polypeptide, respectively. Immunoelectron microscopy indicated that the immunological counterpart of V-ATPase subunits A and B is localized at the plasma membrane, small clear vesicles, and food vacuoles, a lower extent being detected at the parasitophorus vacuolar membrane of the parasite cells. We measured the cytoplasmic pH of both infected erythrocytes and invading malaria parasite cells by microfluorimetry using BCECF fluorescence. It was found that a restricted area of the erythrocyte cytoplasm near a parasite cell is slightly acidic, being about pH 6.9. The pH increased to pH 7.3 upon the addition of either concanamycin B or bafilomycin A1, specific inhibitors of vacuolar H+-ATPase. Simultaneously, the cytoplasmic pH of the infecting parasite cell decreased from pH 7.3 to 7.1. Neither vanadate at 0.5 mM, an inhibitor of P-type H+-ATPase, nor ethylisopropylamiloride at 0.2 mM, an inhibitor of Na+/H+-exchanger, affected the cytoplasmic pH of erythrocytes or infecting parasite cells. These results constitute direct evidence that plasma membrane vacuolar H+-ATPase is responsible for active extrusion of protons from the parasite cells.

* This study was supported in part by Grant-in-Aid 08281105 for Scientific Research on Priority Areas from the Ministry of Education, Science, Culture and Sports of Japan.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Supported by the Hayashi Memorial Foundation for Female Natural Scientists and a research fellowship from the Japan Society for the Promotion of Science for Young Scientists.

Contributed equally to the present work.

|| Supported by the Venture Business Laboratory of Okayama University. Present address: Dept. of Biochemistry, Faculty of Medicine, Okayama University, Okayama 700-8558, Japan.

§§ To whom correspondence should be addressed. Tel./Fax: 81-86-251-7933; E-mail: moriyama@pheasant.pharm.okayama-u.ac.jp.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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