Abstract
Myosin VI (MVI) is a versatile actin-based motor protein that has been implicated in a variety of different cellular processes, including endo- and exocytic vesicle trafficking, Golgi morphology, and actin structure stabilization. A role for MVI in crucial actin-based processes involved in sperm maturation was demonstrated in Drosophila. Because of the prominence and importance of actin structures in mammalian spermiogenesis, we investigated whether MVI was associated with actin-mediated maturation events in mammals. Both immunofluorescence and ultrastructural analyses using immunogold labeling showed that MVI was strongly linked with key structures involved in sperm development and maturation. During the early stage of spermiogenesis, MVI is associated with the Golgi and with coated and uncoated vesicles, which fuse to form the acrosome. Later, as the acrosome spreads to form a cap covering the sperm nucleus, MVI is localized to the acroplaxome, an actin-rich structure that anchors the acrosome to the nucleus. Finally, during the elongation/maturation phase, MVI is associated with the actin-rich structures involved in nuclear shaping: the acroplaxome, manchette, and Sertoli cell actin hoops. Since this is the first report of MVI expression and localization during mouse spermiogenesis and MVI partners in developing sperm have not yet been identified, we discuss some probable roles for MVI in this process. During early stages, MVI is hypothesized to play a role in Golgi morphology and function as well as in actin dynamics regulation important for attachment of developing acrosome to the nuclear envelope. Next, the protein might also play anchoring roles to help generate forces needed for spermatid head elongation. Moreover, association of MVI with actin that accumulates in the Sertoli cell ectoplasmic specialization and other actin structures in surrounding cells suggests additional MVI functions in spermatid movement across the seminiferous epithelium and in sperm release.
Highlights
Spermiogenesis is a complex developmental process that entails extensive morphological and biochemical alternations resulting in formation of fully differentiated male gametes—spermatozoa
MVa-decorated vesicles surround a portion of the chromatoid body, suggesting a possible role of actin filaments in the disposal of nuclear material generated during spermiogenesis (Kierszebaum et al 2003a and see review by Kierszenbaum and Tres 2004)
Four Myosin VI (MVI) posttranscriptional splice variants (Fig. 2a) can be expressed in mammals due to the presence of two inserts [long (LI) and short (SI)] in the C-terminal globular tail: MVI with LI only, with SI only, with both long and short (LI + SI) or with no insert (NoI). Given that these isoforms are differentially expressed in various tissues/cell types where they have diverse localization and function, we first examined which of the MVI splice variants were expressed in mouse testes
Summary
Spermiogenesis is a complex developmental process that entails extensive morphological and biochemical alternations resulting in formation of fully differentiated male gametes—spermatozoa. Two key events of spermiogenesis are acrosome biogenesis and nuclear shaping, accompanied by sperm tail formation This process in mammals is typically divided into three main phases, during which round spermatids transform into elongated mature sperm (Fig. 1): the Golgi, acrosome cap/elongation, and maturation phases (see review by Toshimori 2009). The apical ectoplasmic specialization associated with the tubulobulbar complexes at the concave side of the elongating spermatid head contains actin filaments These actin structures form a stack of hoops stabilized by espin and adhesion protein complexes (Kierszenbaum et al 2003b and see reviews by Kierszenbaum and Tres 2004; Kierszenbaum et al 2007; Xiao and Yang 2007). F-actin structures seem to play important roles during the key events of spermiogenesis in mammals, the molecular basis of their regulation and roles in the processes is still poorly understood
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