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Vol. 14, Issue 7, 2768-2780, July 2003

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Intercellular Organelle Traffic through Cytoplasmic Bridges in Early Spermatids of the Rat: Mechanisms of Haploid Gene Product Sharing

Sami Ventelä ^*  , Jorma Toppari , and Martti Parvinen ^*

^*Department of Anatomy, Turku Graduate School of Biomedical Science, Department of Physiology and Pediatrics, University of Turku, FIN-20520 Turku, Finland

Submitted October 11, 2002; Revised February 27, 2003; Accepted February 27, 2003
Monitoring Editor: Randy Schekman

Stable cytoplasmic bridges (or ring canals) connecting the clone of spermatids are assumed to facilitate the sharing of haploid gene products and synchronous development of the cells. We have visualized these cytoplasmic bridges under phase-contrast optics and recorded the sharing of cytoplasmic material between the spermatids by a digital time-lapse imaging system ex vivo. A multitude of small (ca. 0.5 µm) granules were seen to move continuously over the bridges, but only 28% of those entering the bridge were actually transported into other cell. The average speed of the granules decreased significantly during the passage. Immunocytochemistry revealed that some of the shared granules contained haploid cell-specific gene product TRA54. We also demonstrate the novel function for the Golgi complex in acrosome system formation by showing that TRA54 is processed in Golgi complex and is transported into acrosome system of neighboring spermatid. In addition, we propose an intercellular transport function for the male germ cell-specific organelle chromatoid body. This mRNA containing organelle, ca. 1.8 µm in diameter, was demonstrated to go over the cytoplasmic bridge from one spermatid to another. Microtubule inhibitors prevented all organelle movements through the bridges and caused a disintegration of the chromatoid body. This is the first direct demonstration of an organelle traffic through cytoplasmic bridges in mammalian spermatogenesis. Golgi-derived haploid gene products are shared between spermatids, and an active involvement of the chromatoid body in intercellular material transport between round spermatids is proposed.

Online version of this article contains video material. Online version is available at www.molbiolcell.org.

Corresponding author. E-mail address: satuve{at}utu.fi.

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