Asymmetry of Spermiation and Sperm Surface Charge Patterns over the Giant Acrosome in the Musk Shrew

Spermatozoa of the shrew Suncus murinus, a mammal with abdominal testes, exhibit four unusual features: a giant acrosome; a dorsoventral asymmetry of their spermiation; a dorsoventral asymmetry of their head surface character; and also apparent surface maturity as they enter the epididymis. A Sertoli cell-periacrosomal cisternal complex envelops the giant acrosome during spermatid maturation. Spermiation is heralded by asymmetrical disorganization of the subplasmalemmal components of this complex and is completed by retraction of the Sertoli cell from the ventral and then the dorsal face of the spermatid head. This sequence of release is correlated with an asynchronous acquisition of negative surface charges on the spermatid headmdemonstrable on glutaraldehyde-stabilized cells by the binding at pH 1.8 of positively charged colloidal particles of ferric oxide. Mature epididymal spermatozoa exhibit an asymmetry in the patterns of distribution of bound colloid over the dorsal vs. ventral surfaces of the sperm head, as well as regional differences between the tail midpiece and principal piece. Surface distributions of anionic residues and lectin (Con A)-binding sites characteristic of mature Suncus spermatozoa are demonstrable within the testis, unlike the situation in most mammals where distinct modifications of the sperm surface occur during epididymal passage. In all mammals studied to date, spermatozoa entering the epididymis from the testis are incompetent to fertilize ova and acquire this ability as they pass through the epididymis. Such functional maturation must involve change in several structural and biochemical characteristics, only some of which are elucidated (3). Chemical modifications of the surface overlying the mammalian sperm head and tail have been demonstrated during epididymal transit. These were first detected at physiological pH as a difference in the electrophoretic mobility and orientation of populations of cooled rabbit spermatozoa recovered from the caput and cauda epididymidis, respectively (2). Subsequently, regional differentiation of the sperm surface during epididymal passage has been confirmed in the rabbit and other scrotal mammals, using positively charged ferric oxide hydrosols at pHs of less than 2.0. Such electron-dense colloids allow one to visualize the surface distribution of fixed negative charges which appear to be acquired in species-specific patterns on different regions of the sperm surface during transit through the epididymis (10, 6, 7, 31, 32). This, and additional TIlE .JOURNAL OF CELL BIOLOGY 9 VOLUME 69, 1976 9 pages 415-428 415 on A ril 5, 2017 D ow nladed fom Published May 1, 1976