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THE CELL BIOLOGY OF GAMETOGENESIS IN THE MALE DON W. FAWCETT* In a long and varied career in microscopic anatomy, no organ has proved more interesting than the male gonad and no developmental process more fascinating than spermatogenesis. In recent years, I have devoted an increasing share ofmy research effort to the male reproductive tract, because of the many challenges it presents to the cell biologist and because if we understood it better, we could contribute significandy to the solution of one of the most urgent problems confronting humankind—the control of its own numbers. The traditional approach to an understanding ofspermatogenesis has been largely endocrinological. The classical studies of Moore [1] and his colleagues here at Chicago nearly 50 years ago demonstrated dependence of the process upon testosterone secreted by the interstitial cells, and it was subsequently shown that these cells are in turn under the control of the pituitary gonadotropin, luteinizing hormone (LH). But this approach was unable to explain the cyclic nature of the process, the synchrony of germ cell differentiation, or the mechanism of sperm release . This has required painstaking autoradiographic studies of stemcell renewal [2-4]; detailed ultrastructural analysis of the topographic relations ofdie cells; their membrane specializations for attachment; and their mechanisms for cell-to-cell communication [5-7]. It is some ofthese latter studies that I will review briefly. Régnier de Graaf [8], in his classical account of the structure of the testis in 1668, described it as consisting entirely of minute convoluted tubules. Save for the hormone-secreting interstitial cells ofLeydig, which were not described until 1850 [9], his description still holds (fig. 1). There are approximately 1 80 m of seminiferous tubules in each testis, and the continual proliferation of cells in their lining epithelium makes possible the production of some 30,000,000 spermatozoa a day diroughout the long reproductive lifetime of the male. The multiplicity of cell types in the seminiferous epithelium, their superimposition, and interdigitation made it exceedingly difficult to interpret its organization with "Hersey Professor of Anatomy, Harvard Medical School, 25 Shattuck Street, Boston, Massachusetts 021 15.© 1979 by The University of Chicago. 0031-5982/79/2222-0004J01.00 S56 I Don W. Fawcett ¦ Gametogenesis in the Male Fig. 1.—Cutaway drawing of the internal structure of the testis showing the convoluted seminiferous tubules. One has been unraveled to illustrate its form and continuity with the rete testis. The continuous proliferation of germ cells in the lining epithelium of die tubules results in production ofvery large numbers ofspermatozoa (modified after Hamilton [10]). the light microscope (fig. 2), but the electron microscope overcame some of diese difficulties and has enabled us to describe a number of unique organizational features that we believe are essential to sperm development and possibly hold the key to control of the process. In a simple epithelium such as that lining die intestine, the columnar cells are in close apposition, but the intercellularclefts may be invaded by occasional migratory cells such as lymphocytes (fig. 3, left). In the fetal testis, actively amoeboid primordial germ cells invade the epithelium of the testis cords, becoming a quiescent resident population until puberty when they begin proliferating in expanded intercellular spaces between the columnar Sertoli cells. They soon greatly outnumber the supporting cells (fig. 3, right). Thus, in die adult, the seminiferous epitheliumconsists of two distinct categories of cells—a fixed population of nondividing Sertoli cells extending from base to lumen, and a mobile population of germ cells that proliferate near the periphery of die tubules and slowly move inward as they differentiate into spermatozoa (fig. 4). Perspectives in Biology andMedicine · Winter 1979 · Part 2 | S57 The analogy to lymphocytes in otiier epithelia applies only to their intercellular location. The lymphocytes are capable ofindependent existence in almost any extracellular space. The germ cells, on the other hand, appear to be totally dependent for their survival and development upon a special microenvironment created for them by their supporting epithelial cells. This dependent relationship is probably more obligatory than that ofthe neurons in die brain upon their supporting glial cells. In order to maintain an optimal environment for neural activity, the cells of the brain are isolated from die...


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