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M110515200v1
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Papers In Press, published online ahead of print May 14, 2002
J. Biol. Chem, 10.1074/jbc.M110515200
Submitted on November 1, 2001
Revised on May 2, 2002
Accepted on May 14, 2002

A close association of ganglioside-specific sialidase, Neu 3, with caveolin in membrane microdomains

Yan Wang, Kazunori Yamaguchi, Tadashi Wada, Keiko Hata, Xuejian Zhao, Toyoshi Fujimoto, and Taeko Miyagi

Division of Biochemistry, Research Institute, Miyagi Prefectural Cancer Center, Natori, Miyagi 981-1293

Corresponding Author: tmiyagi{at}mcc.pref.miyagi.jp

The ganglioside-specific sialidase, Neu 3, has been suggested to play essential roles in regulation of cell surface functions, because of its major localization in the plasma membrane and strict substrate preference for gangliosides involved in signal transduction. Here we show that human Neu 3 sialidase is enriched in caveolae microdomains and closely associated with caveolin, like other caveolin-binding signaling molecules. Using HeLa cells and Neu 3-transfected COS-1 cells, endogenous and exogenous Neu 3 was found to concentrate together with caveolin-1 in low density Triton X-100 insoluble membrane fractions on sucrose density gradients of the respective cell extracts, as assessed by enzyme activity assays and immunobloting with a monoclonal antibody to human Neu 3. The presence of a putative caveolin-binding motif within Neu 3 prompted us to determine whether Neu 3 binds to caveolin-1. In transfectants expressing a polyhistidine-tagged form of Neu 3, caveolin-1 co-eluted with Neu 3 on affinity column chromatography. A mutation with a single amino acid change in the caveolin-binding motif led to inhibition of recruitment of the sialidase to the microdomain, accompanied by reduction of the enzyme activity. Neu 3 also failed to associate with caveolin-enriched microdomains by cholesterol depletion with b-cyclodextrin, with concomitant decrease of the sialidase activity, whereas Neu 3 was activated by increased caveolin-1 expression. The tight association of Neu 3 with caveolin-1 was supported further by co-immunoprecipitation of Neu 3 by anti-caveolin-1 antibody. These results strongly suggest that Neu 3 functions as a caveolin-related signaling molecule within caveolin-rich microdomains.


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