Elsevier

Theriogenology

Volume 63, Issue 2, 15 January 2005, Pages 319-341
Theriogenology

Epididymal cell secretory activities and the role of proteins in boar sperm maturation

https://doi.org/10.1016/j.theriogenology.2004.09.015Get rights and content

Abstract

The final stages of sperm differentiation occur outside the gonad, in the epididymal tubule. These last maturation steps, essential to the quality of spermatozoa, are not under the genomic control of the germ cells. A series of sequential interactions with the epididymal fluid, mostly specific proteins present in the lumen of different regions, are believed to induce the final steps of sperm maturation. In order to provide the luminal changes required for this maturation to occur, the epithelium may resort to two basic mechanisms: absorption and secretion. Far from being a uniform channel, the epididymal duct is a canal with highly specialized regional differentiation of its epithelial ultrastructure and its secretory and absorptive functions. This review focuses on the ultractructural characteristic of the epithelial cells, their specific secretory activity according to the epididymal regions and their eventual role in sperm maturation of the boar. The chronology of the changes that occur in and on the sperm and in the surrounding environment are described. Relationships between the highly regionalized epididymal activities, sperm characteristics linked to their survival and fertility potential are also presented in this review.

Introduction

The formation of the male gamete is the result of extensive cellular differentiation that occurs during the transformation of a round spermatid into a highly polarized and fully motile cell. Most of these complex biochemical, physiological and morphological events of cellular differentiation take place in the testis during the process of spermiogenesis. During this testicular processing, cellular events are mostly under genomic regulation of the gamete. However, when DNA begins to condense in the elongated spermatids, the transcription process in the germinal DNA decreases and then stops. At the final testicular phase of male gamete differentiation, the spermatozoa that are neither motile nor fertile require additional discrete and essential post-gonadal modification to be able to fertilize eggs. Thus, the presence of a specific sperm environment during the subsequent differentiation stages in the epididymis is believed to play an essential role in controlling or inducing the final sperm changes.

The maturation stage of spermatozoa in the epididymis is out of the control of the germinal genome and is therefore largely the consequence of their interactions with the epididymal fluid, mostly with specific proteins present in the lumen of the epididymal tubule (Fig. 1). This specific microenvironment, which is isolated from the blood by the epididymal-blood barrier, also ensures protection of the gametes until ejaculation as well as regulation of the functionality and integrity of the epididymis.

Understanding of these post-testicular effects on the sperm and on the epididymal environment is essential to obtain good markers for fertility prediction for the animal and for sperm fertility and conservation.

Section snippets

Post-testicular environment of the spermatozoa

From the testis, the spermatozoa are transported into an epididymal tube that forms an organ composed of several regions, such as the caput, corpus and cauda (Fig. 2). The epididymis is formed by a polarized epithelium composed mostly of principal and basal cells and creating an environment around the spermatozoa that is certainly the most complex found in any exocrine gland. This complexity results from two peculiarities: (1) continuous and progressive changes in its composition throughout the

Morphological characteristics of the secretory activity of the epididymal cells

In order to provide the luminal changes required for sperm maturation to occur, the epithelium may resort to two basic mechanisms: absorption and secretion. Far from being a uniform channel, the epididymal duct is a canal with highly specialized regional differentiation of its epithelial ultrastructure.

Sperm membrane remodelling during epididymal transit

As the sperm enter the epididymis, the sperm plasma membrane undergoes substantial remodelling during epididymal transit, both in protein and phospholipid composition and in localization of the components on the gamete. In all the species studied to date, including the boar, it appears that specific testicular sperm surface proteins are removed or further processed as the gametes pass through the epididymis. The disappearance of some of them is clearly related to a specific mechanism of

Effect of the epididymal environment on sperm

The sequential changes associated with the sequential modifications observed in the sperm membrane are believed to be directly or indirectly involved in the maturation stages of sperm during epididymal transit.

Conclusions and perspectives

During their transit through the epididymis, spermatozoa are subjected to a continually changing luminal environment modified by the secretory and endocytic activities of the cells lining the epithelium. Ultimately, it is the coordinated activities of secretion and endocytosis of various substances by the epithelial cells along the duct that influence the final maturation of sperm as well as their concentration, protection and storage. These sequential changes are accompanied by modifications

Acknowledgements

This study was supported by grants from the Institut National de la Recherche Agronomique (INRA, France) and from the Région Centre (France).

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