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J. Biol. Chem., Vol. 280, Issue 8, 7262-7272, February 25, 2005

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Cellugyrin Induces Biogenesis of Synaptic-like Microvesicles in PC12 Cells^*

Gabriel M. Belfort, Kyriaki Bakirtzi, and Konstantin V. Kandror

From the Boston University School of Medicine, Boston, Massachusetts 02118

The four-transmembrane domain proteins synaptophysin and synaptogyrin represent the major constituents of synaptic vesicles. Our previous studies in PC12 cells demonstrated that synaptogyrin or its nonneuronal paralog cellugyrin targets efficiently to synaptic-like microvesicles (SLMVs) and dramatically increases the synaptophysin content of SLMVs (Belfort, G. M., and Kandror, K. V. (2003) J. Biol. Chem. 278, 47971–47978). Here, we explored the mechanism of these phenomena and found that ectopic expression of cellugyrin increases the number of SLMVs in PC12 cells. Mutagenesis studies revealed that cellugyrin's hydrophilic cytoplasmic domains are not involved in vesicle biogenesis, whereas small conserved hydrophobic hairpins in the first luminal loop and the carboxyl terminus of cellugyrin were found to be critical for the formation of SLMVs. In addition, the length but not the primary sequence of the second luminal loop was essential for SLMV biogenesis. We suggest that changing the length of this loop similar to disruption of the short hydrophobic hairpins alters the position of the vicinal transmembrane domains that may be crucial for protein function.

Received for publication, April 30, 2004 , and in revised form, November 2, 2004.

^* This work was supported by National Institutes of Health Grants R01 DK52057 and R01 DK56736 (to K. V. K.) and by training grant T32 DK07201 (to G. M. B.). 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: Dept. of Biochemistry, Boston University School of Medicine, K124D, 715 Albany St., Boston, MA 02118. Tel.: 617-638-5049; Fax: 617-638-5339; E-mail: kandror{at}biochem.bumc.bu.edu.

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