The establishment of spermatogenesis in the seminiferous epithelium of the pubertal golden hamster (Mesocricetus auratus).

Abstract

The present study deals with initial spermatogenesis in the pubertal golden hamster (Mesocricetus auratus), in the course of which both the complex process of germ cell proliferation and differentiation and the cyclic pattern of organization of spermatogenesis are established. Germ cells pass through the complete sequence of spermatogenic differentiation from the A-spermatogonium up to the mature spermatid between days 12 and 38. During this period, germ cell development is already based on the pattern of organization and synchronization characteristic of adult spermatogenesis: 1. Judged by the germ cell types present, each of the successively appearing germ cell associations conforms to one of the adult stages of the seminiferous epithelium (stage conformity of the developmental steps of the pubertal seminiferous epithelium). 2. The overall intratesticular variance of the developmental levels reached in different tubular segments each covers almost exactly one cycle length of spermatogenesis. 3. There is a regular, continuous succession of developmental steps along the longitudinal course of the tubules which, in every single tubule, comprises the interval of one spermatogenic cycle ("wave" of the pubertal seminiferous epithelium). 4. Taken together, the latter two results indicate that the tubules of one given testis are equal to one another with respect to their developmental level, i.e., they develop synchronously. Germ cell propagation follows the clonal mode of proliferation. In quantitative terms, stage-related S-phase indices largely parallel the values of adult spermatogenesis. Both the frequently found germ cell apoptosis and degenerating intrameiotic spermatocytes correspond to degenerative phenomena in the adult seminiferous epithelium with respect to degenerative mode and stage-related occurrence. Germ cell development is closely related to the maturation of both Sertoli cells and Leydig cells. At two developmental phases, localized disturbances of germ cell differentiation occur which are specific to the pubertal period and which correlate with a maturational delay of Sertoli cells and Leydig cells, respectively: 1. Completion of Sertoli cell barrier formation may temporarily follow the initial onset of meiosis in the neighboring germ cells. As a result, mitotically dividing germ cells fall under the influence of a (hitherto hypothetic) "meiotic milieu" and characteristically degenerate (arrested germ cell mitoses). This relationship emphasizes the functional significance of the separation of the two seminiferous compartments and, in addition, heightens the understanding of the necessity of normal termination of Sertoli cell proliferation before germ cells initially enter meiosis. 2. The Leydig cell enzyme 11 beta-HSD, which is known to promote testosterone output, is established several days after the leading spermatids initially reach step 6 of spermiogenesis (which is immediately prior to the particularly testosterone-dependent start of elongation). The resulting selective developmental arrest of round spermatids of steps 6-6/7 between days 26 and 30 leads to a localized, partial desynchronization of the seminiferous epithelium, which can be traced for several days after the above-mentioned maturational delay of Leydig cells has been overcome and which is accompanied by an extensive degenerative disposition of the spermatids involved. The present investigation documents an organizational and synchronizational level of initial spermatogenesis that is similar to the situation in the adult animal. The analysis of temporarily occurring perturbations in the process of establishing the pubertal seminiferous epithelium emphasizes and specifies the close structural and functional relationships between the maturational state of somatic cells and germ cell differentiation.