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Originally published In Press as doi:10.1074/jbc.M102233200 on April 27, 2001

J. Biol. Chem., Vol. 276, Issue 28, 26249-26259, July 13, 2001
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Purification, Characterization, Molecular Cloning, and Subcellular Distribution of Neutral Ceramidase of Rat Kidney*

Susumu Mitsutake, Motohiro Tani, Nozomu Okino, Kaoru Mori, Sachiyo IchinoseDagger , Akira OmoriDagger , Hiroshi Iida§, Takashi Nakamura, and Makoto Ito

From the Department of Bioscience and Biotechnology and the § Department of Applied Genetics and Pest Management, Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan and the Dagger  Mitsubishi Kasei Institute of Life Sciences, 11 Minamiooya, Machida 194-8511, Tokyo, Japan

Previously, we reported two types of neutral ceramidase in mice, one solubilized by freeze-thawing and one not. The former was purified as a 94-kDa protein from mouse liver, and cloned (Tani, M., Okino, N., Mori, K., Tanigawa, T., Izu, H., and Ito, M. (2000) J. Biol. Chem. 275, 11229-11234). In this paper, we describe the purification, molecular cloning, and subcellular distribution of a 112-kDa membrane-bound neutral ceramidase of rat kidney, which was completely insoluble by freeze-thawing. The open reading frame of the enzyme encoded a polypeptide of 761 amino acids having nine putative N-glycosylation sites and one possible transmembrane domain. In the ceramidase overexpressing HEK293 cells, 133-kDa (Golgi-form) and 113-kDa (endoplasmic reticulum-form) Myc-tagged ceramidases were detected, whereas these two proteins were converted to a 87-kDa protein concomitantly with loss of activity when expressed in the presence of tunicamycin, indicating that the N-glycosylation process is indispensable for the expression of the enzyme activity. Immunohistochemical analysis clearly showed that the ceramidase was mainly localized at the apical membrane of proximal tubules, distal tubules, and collecting ducts in rat kidney, while in liver the enzyme was distributed with endosome-like organelles in hepatocytes. Interestingly, the kidney ceramidase was found to be enriched in the raft microdomains with cholesterol and GM1 ganglioside.

* This work was supported in part by a grant-in aid for Scientific Research on Priority Area (B) (12140204) from the Ministry of Education, Culture, Sports, Science and Technology, 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.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) AB057433.

To whom all correspondence should be addressed: Dept. of Bioscience and Biotechnology, Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan. Fax: 81-92-642-2900 or 81-92-642-2907; E-mail: makotoi@agr.kyushu-u.ac.jp.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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