The fibrous sheath is a unique cytoskeletal structure located in the principal piece of the sperm flagellum and is constructed of two longitudinal columns connected by closely spaced circumferential ribs. Cyclic AMP-dependent protein kinases are secured within specific cytoplasmic domains by A-kinase anchoring proteins (AKAPs), and the most abundant protein in the fibrous sheath is AKAP4. Several other fibrous sheath proteins have been identified, but how the fibrous sheath assembles is not understood. Yeast two-hybrid assays and deletion mutagenesis were used to identify AKAP4-binding proteins and to map the binding regions on AKAP4 and on the proteins identified. We found that AKAP4 binds AKAP3 and two novel spermatogenic cell-specific proteins, Fibrous Sheath Interacting Proteins 1 and 2 (FSIP1, FSIP2). Transcription of Akap4, Akap3, and Fsip1 begins in early spermatid development, whereas transcription of Fsip2 begins in late spermatocyte development. AKAP3 is synthesized in round spermatids and incorporated into the fibrous sheath concurrently with formation of the rib precursors. However, AKAP4 is synthesized and incorporated into the nascent fibrous sheath late in spermatid development. The AKAP4 precursor is processed in the flagellum and only the mature form of AKAP4 appears to bind AKAP3. These results suggest that AKAP3 is involved in organizing the basic structure of the fibrous sheath, whereas AKAP4 has a major role in completing fibrous sheath assembly.

https://bioone.org/journals/Biology-of-Reproduction/volume-68/issue-6/biolreprod.102.013466/A-Kinase-Anchoring-Protein-4-Binding-Proteins-in-the-Fibrous/10.1095/biolreprod.102.013466.pdf

A-Kinase Anchoring Protein 4 Binding Proteins in the Fibrous Sheath of the Sperm Flagellum

Reproduction is a process that can be organized into distinct developmental and functional phases. In the case of the male, these include fertilization, formation of a patent reproductive tract, production of sperm, manifestation of male-specific behavioral patterns, and expulsion of sperm from the body. This perspective can provide insight that may be missed if reproduction is viewed primarily as an isolated act. For example, although the reproductive tract is fully functional only in the adult, it is formed, for the most part, prior to hatching. Furthermore, although spermatogenesis is associated with puberty, spermatogenesis is not constrained by chronological age but rather by the extent to which testicular cells proliferate and differentiate, which in turn is coupled to the developmental limitations of gonadotropin secretion. Finally, androgens essential to the function of the reproductive tract, the appearance of secondary sexual attributes, and male behavior may have detrimental effects upon the development of immune and connective tissue if the hormonal signal appears during the period of rapid prepubertal growth and differentiation. Thus, this chapter will discuss the process of reproductive system development and function in the male bird.

Reproduction in Male Birds

SUMMARY In many birds, testes undergo dramatic annual changes in size and, as such, are among the most anatomically and physiologically plastic organs found in adult vertebrates. Adult testicular function is modulated by a myriad of external factors and orchestrated by numerous hormones that together enable birds to adapt to and breed in diverse habitats worldwide. These factors have generated a wide range of avian reproductive strategies, which has further shaped testicular structure and function. This chapter describes the mechanisms that control avian exocrine and endocrine testicular functions. It analyzes how these functions are regulated by ecological and behavioral factors and presents an overview of how environmental information is integrated and transduced into appropriate gonadal responses. It also discusses testicular dysfunction and the potential effects of anthropogenic disturbances on testis function. The chapter emphasizes areas where knowledge is lacking or incomplete, with the hope of fostering additional research on this exciting and fruitful area of avian biology.

/pdf/avian-testicular-structure-function-and-regulation-2dadfauq8y.pdf

Avian testicular structure, function, and regulation

Spermiogenesis in the soft-shelled turtle, Pelodiscus sinensis, was examined by transmission electron microscopy. The process includes nuclear elongation, chromatin condensation, acrosomal and flagellar development, and elimination of excess cytoplasm. In stage I, the proacrosomal vesicle occurs next to a shallow fossa of the nucleus, and a dense acrosomal granule forms beneath it. A smaller subacrosomal granule in the middle of the fibrous layer is related to the development of intranuclear tubules. The nucleus begins to move eccentrically. In stage II, the round proacrosomal vesicle is flattened by protrusion of the nuclear fossa, and the dense acrosomal granule diffuses into the vesicle, as the fibrous layer forms the subacrosomal cone. Circular manchettes develop around the nucleus, and the chromatin coagulates into small granules. The movement of the nucleus causes rearrangement of the cytoplasm. In stage III, the front of the elongating nucleus protrudes out of the spermatid and is covered by the flat acrosome; coarse granules replace the small ones within the nucleus. At the posterior pole of the head, mitochondria move backward. Numerous microtubules begin to assemble the axoneme of flagellum. In stage IV, the chromatin concentrates to dense homogeneous phase. The circular manchette is reorganized longitudinally. The Sertoli process covers the acrosome and the residues of the cytoplasmic lobes are eliminated. In stage V, the sperm head matures. After dissolution of the longitudinal manchette, the mitochondria arrange themselves around the proximal and distal centrioles. Caudal to the mitochondrial mass, a fibrous sheath surrounds the proximal portion of the flagellum.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/ar.20587

Spermiogenesis in Soft‐Shelled Turtle, Pelodiscus sinensis

Nuclear condensation during spermiogenesis in the ostrich follows the basic pattern established in other vertebrates. The fine granular nuclear substance of early spermatids is gradually replaced by numbers of coarse dense granules which appear to arise by aggregation of smaller dispersed elements of the chromatin. The granules increase in size and eventually coalesce to form the compact homogenous mass of chromatin typical of the mature sperm. In ostrich spermatids, however, the aggregation of the nuclear material produces large numbers of longitudinally oriented rod-shaped structures in addition to some granular material. Although fibrillar chromatin has been observed during spermiogenesis in a number of vertebrate species, the hollow nature of the rod-shaped chromatin granules in ostrich spermatids is a unique phenomenon. The spiralisation of the chromatin material observed in ostrich spermatids and in some other nonpasserine birds is possibly related to the reduction in nuclear length demonstrated during spermiogenesis in these species. In common with other nonpasserine birds, spermiogenesis in the ostrich is characterised by the appearance both of a circular and a longitudinal manchette. The circular manchette consists of a single row of microtubules reinforced by additional peripherally arranged microtubules. Links between adjacent microtubules, and between the nucleolemma and some of the microtubules, are evident. The longitudinal manchette consists of arrays of interconnected microtubules arranged in approximately 4–6 staggered, ill defined rows. This structure seems to originate as a result of the rearrangement of the microtubules of the circular manchette and is only formed once the process of chromatin condensation is well advanced. Based on the sequence of morphological events observed during spermiogenesis in the ostrich, it is concluded that the circular manchette is responsible for the initial transformation in shape of the spermatid nucleus. Thereafter, the chromatin condenses independently within the confines of the nucleolemma with the circular manchette merely acting to maintain the shape of the nucleus while this process is underway, to compress the nuclear membrane, and possibly to orientate the subunits of the condensing chromatin. The longitudinal manchette appears to assist in the translocation of material during spermatid elongation. There are indications that the developing acrosome is instrumental in effecting nuclear shaping of the apical (subacrosomal) head region of the ostrich spermatid.

Nuclear morphogenesis and the role of the manchette during spermiogenesis in the ostrich (Struthio camelus)

The ultrastructure of 12 steps of spermatid development and the process of spermiation are described for the Japanese quail in order to clarify the classification proposed for determining the stages of the cycle of the seminiferous epithelium (Lin et al. 1990) and to assess disagreements in the literature about sperm development in birds. It was concluded that acrosomal development involves the formation of proacrosomal granules which do not contain dense granules like the mammalian acrosome. Material which forms the perforatorium initially accumulates as a nuclear granule before appearing in the subacrosomal space. A circular and longitudinal manchette develop sequentially during nuclear elongation. Microtubules of the circular manchette initially form around several parts of the spherical nucleus of step 4 spermatids and subsequently occur most frequently around the narrowest regions of the elongating nucleus. Fibrous sheath development starts in step 2 spermatids indicating that it forms much earlier in the quail than in mammals. Spermiation differs from the process described in mammals in that the residual body is released from near the rostral end of the sperm nucleus leaving no cytoplasmic droplet in quail spermatozoa.

R C Jones

Papers

Spermiogenesis and spermiation in the Japanese quail (Coturnix coturnix japonica).