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J. Biol. Chem., Vol. 278, Issue 24, 22023-22030, June 13, 2003

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From Lysosomes to the Plasma Membrane

LOCALIZATION OF VACUOLAR TYPE H⁺-ATPase WITH THE a3 ISOFORM DURING OSTEOCLAST DIFFERENTIATION^*

Takao Toyomura , Yoshiko Murata , Akitsugu Yamamoto , Toshihiko Oka , Ge-Hong Sun-Wada , Yoh Wada  and Masamitsu Futai  ¶

From the Division of Biological Sciences, Institute of Scientific and Industrial Research, Osaka University, and Core Research for Evolutional Science and Technology of the Japan Science and Technology Corporation, Osaka 567-0047, Department of Physiology, Kansai Medical University, Moriguchi, Osaka 570-8506, Japan

Osteoclasts generate a massive acid flux to mobilize bone calcium. Local extracellular acidification is carried out by vacuolar type H⁺-ATPase (V-ATPase) localized in the plasma membrane. We have shown that a3, one of the four subunit a isoforms (a1, a2, a3, and a4), is a component of the plasma membrane V-ATPase (Toyomura, T., Oka, T., Yamaguchi, C., Wada, Y., and Futai, M. (2000) J. Biol. Chem. 275, 8760–8765). To establish the unique localization of V-ATPase, we have used a murine macrophage cell line, RAW 264.7, that can differentiate into multinuclear osteoclast-like cells on stimulation with RANKL (receptor activator of nuclear factor B ligand). The V-ATPase with the a3 isoform was localized to late endosomes and lysosomes, whereas those with the a1 and a2 isoforms were localized to organelles other than lysosomes. After stimulation, the V-ATPase with the a3 isoform was immunochemically colocalized with lysosome marker lamp2 and was detected in acidic organelles. These organelles were also colocalized with microtubules, and the signals of lamp2 and a3 were dispersed by nocodazole, a microtubule depolymerizer. In RAW-derived osteoclasts cultured on mouse skull pieces, the a3 isoform was transported to the plasma membrane facing the bone and accumulated inside podosome rings. These findings indicate that V-ATPases with the a3 isoform localized in late endosomes/lysosomes are transported to the cell periphery during differentiation and finally assembled into the plasma membrane of mature osteoclasts.

Received for publication, March 10, 2003 , and in revised form, April 2, 2003.

^* This work was supported by a grant-in-aid from the Ministry of Education, Science and Culture, Japan, the Japan Foundation for Applied Enzymology, and the Japan Society for the Promotion of Science. 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. Tel.: 81-6-6879-8480; Fax: 81-6-6875-5724; E-mail: m-futai{at}sanken.osaka-u.ac.jp.

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