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II.1.3 Physiology of Spermatogenesis M 272 II.1 Understanding Normal Anatomy and Function translation initiation site circumvents an amino-terminal Simard J, Rheaume E, Mebarki F, Sanchez R, New MI, Morel Y, DAX1nonsensemutationleadingtoamildformofX-linked Labrie F (1995) Molecular basis of human 3 beta-hydroxy- adrenal hypoplasia congenita. J Clin Endocrinol Metab steroid dehydrogenase deficiency. J Steroid Biochem Mol Bi- 88:417–423 ol 53:127–138 PelletierJ,BrueningW,KashtanCE,MauerSM,ManivelJC, Sinclair AH, Berta P, Palmer MS, Hawkins JR, Grittiths BL, StriegelJE,HoughtonDC,JunienC,HabibR,FouserL,Fine Smith MJ, Foster JW, Frischauf A-M, Lovell-Badge R, Good- RN, Silverman BL, Housman D (1991a) Germline mutations fellow PN (1990) A gene from the human sex-determining in the Wilms’ tumor suppressor gene disrupt urogenital de- region encodes a protein with homology to a conserved velopment in humans. Cell 67:437–447 DNA-binding motif. Nature 346:240–244 Pelletier J, Bruening W, Li FP, Haber DA, Glaser T, Housman Wigley WC, Prihoda JS, Mowszowicz I, Mendonca BB, New MI, DE (1991b) WT1 mutations contribute to abnormal genital Wilson JD, Russel DW (1994) Natural mutagenesis study of system development and hereditary Wilms’ tumour. Nature the human steroid 5 alpha-reductase 2 isozyme. Biochemis- 353:431–434 try 33:1265–1270 Quigley CA, De Bellis A, Marschke KB, El-Awady MK, Wilson Wilson JD, Griffin JE, Russell DW (1993) Steroid 5-alpha-re- EM, French FS (1995) Androgen receptor defects: historical, ductase 2 deficiency. Endocr Rev 14:577–593 clinical, and molecular perspectives. Endocr Rev 16:271–321 II.1.3 Physiology of Spermatogenesis M. Bergmann Summary Spermatogenesis includes multiplication of sper- rect DNA integrity and condensation due to failure matogonia, meiosis of spermatocytes and differen- in histone to protamine exchange may be an im- tiation of spermatids into the male gamete, which is portant factor predicting the outcome of assisted capable of motility and fertilizing an egg. Spermato- reproduction by in vitro fertilization or testicular genesis occurs within the testicular seminiferous sperm extraction/intracytoplasmic sperm injec- tubules, which consist of peritubular tissue and the tion. seminiferous epithelium. The latter is composed of germ cells and somatic Sertoli cells. Somatic Sertoli cells divide the seminiferous epithelium into basal II.1.3.1 and adluminal compartments by inter-Sertoli cell Spermatogenesis junctional complexes protecting spermatocytes and spermatids from the immune system. They support Spermatogenesis represents the entire process of germ and trigger germ cell development by mediating cell development within the seminiferous epithelium of hormonal stimuli because they are the only cells the adult testis. It can be divided into four phases and within the epithelium possessing follicle-stimulat- includes: (1) the proliferation and differentiation of ing hormone and androgen receptors. Germ cell spermatogonia, (2) meiotic divisions of spermatocytes, apoptosis is most important during pubertal estab- (3) the transformation of haploid round spermatids lishment of the species-specific ratio of germ cells to arising from the second meiotic division into sperma- Sertoli cells, and is increased together with sper- tozoa (spermiogenesis), which (4) are released into the matogenic impairment. There are six different, spe- lumen of the seminiferous tubules (spermiation) cific germ cell associations within the seminiferous (Fig. II. 1.8a, b). epithelium: “stages of spermatogenesis”. These II.1 stages are sequentially arranged along the length of II.1.3.2 a tubule: “wave of spermatogenesis”. The duration Seminiferous Tubules of this wave is the “cycle of spermatogenesis”. It takes 16 days; the whole process of spermatogenesis Seminiferous tubules have a diameter of about 180 µm from the spermatogonium to the release of the sper- and consist of peritubular tissue (lamina propria) and matozoon takes about 70–75 days. the seminiferous epithelium. The lamina propria Spermatogenic efficiency is within the range of (8 µm) is composed of four to five layers of contractile other primates and shows that sperm number is not myofibroblasts and connective tissue. The seminifer- limited by germ cell loss during meiosis but depends ous epithelium (80 µm) rests on a basal lamina and on the number of spermatogonia entering meiosis. consists of germ cells in different developmental stages Spermatogenic impairment is regularly associat- and the supporting somatic Sertoli cells, which provide ed with Sertoli cell maturation deficiency, and incor- an extreme cytoplasmic ramification and surround ad- jacent germ cells (Fig. II. 1.9a, b). II.1.3 Physiology of Spermatogenesis 273 spermiogenesis elongated spermatid, 1n1C spermatogenesis round spz II, 1n2C meiosis spz I, 2n4C type B mitosis spermatogonium, 2n2C a type A b Fig. II.1.8a, b. Seminiferous epithelium and process of spermatogenesis. a Normal seminiferous epithelium. [Ap Spermatogonium type A (pale), Ad spermatogonium type A (dark), sgB spermatogonium type B, P primary pachytene spermatocyte, rsd round spermatid, elsd elongated spermatid.] Paraffin section, haematoxylin and eosin, primary magnification, ×40. b Process of sper- matogenesis 9 8 Lc 7 Lc bv 7 2 6 3 4 3 II.1 1 5 a b Fig. II.1.9a, b. Normal seminiferous epithelium. a Seminiferous tubules with intact seminiferous epithelium (arrows)andintersti- tial tissue containing blood vessels (bv), and Leydig cells (Lc); paraffin section, haematoxylin and eosin, primary magnification, ×20. b Schematic drawing of the seminiferous epithelium. [1 Basal compartment, 2 adluminal compartment, 3 Sertoli cell nucle- us, 4 inter-Sertoli cell junctional complex, 5 type a (pale) spermatogonium, 6 primary pachytene spermatocyte, 7 round sperma- tid, 8 elongated spermatid, 9 residual body.] From Holstein (1994) 274 II.1 Understanding Normal Anatomy and Function “synaptonemal complexes” which are only visible us- II.1.3.3 ing an electron microscope. In the pachytene stage, Spermatogonia there is an exchange of genetic material derived from Spermatogonia are the diploid (2n2 C) stem cells of maternal and paternal sources between sister chroma- spermatogenesis, and can be divided into type A and tids of homologous chromosomes involving DNA type B. They undergo mitotic divisions and thus repre- breakage and repair in autosomes but not in the hetero- sent the renewing stem cell population. The classifica- somes “x” and “y”. The pairing of chromosomes leads tion is mainly based on differences of nuclear chroma- to a “crossover” of adjacent sister chromatids. When tin pattern. Type A spermatogonia have an oval eu- the chromosomes start to separate in the pachytene chromatic nucleus in contrast to type B spermatogonia, stage, these sites become visible and are termed “chias- which have a round heterochromatic nucleus. In pri- mata”. In the diplotene stage, chromosomes separate mates including humans, type A spermatogonia are with the exception of the chiasmata sites. The end of the further divided into A pale (Ap) and A dark (Ad) ac- meiotic prophase is recognized as “diakinesis”, when cording to their differing nuclear appearance. In con- chromosomes shorten and the four separate chroma- trast to Ap, Ad spermatogonia are characterized by a tids become visible. Finally, the nuclear membrane dis- dark nucleus showing a light halo. A possible function- appears and chromosomes are subsequently arranged al significance in respect of mitotic activity remains in the metaphase plate. After formation of the spindle controversial. In non-human primates Ad spermatogo- apparatus,chromosomesmovetooppositepoles,but, niahavenooronlyweakproliferativeactivity(Schlatt in contrast to mitotic division, chromatids remain in- and Weinbauer 1994), whereas S-phase-specific Ki-67 terconnected. Thus the number of chromosomes in re- immunoreactivity indicating mitotic activity was sulting secondary spermatocytes is haploid, but the found in both Ap and Ad spermatogonia by Steger et al. DNA content is still diploid (1n2 C). (1998) in the human. It is generally agreed that type B spermatogonia are II.1.3.4.2 able to differentiate and enter the process of meiosis. Secondary Spermatocytes Due to incomplete cytokinesis, type B spermatogonia remain interconnected after the last mitotic division by Secondary spermatocytes undergo the second meiotic intercellular bridges forming cellular clones, which al- division after a short interphase of about 6 h in the hu- low synchrony of germ cell maturation. These intercel- man without DNA synthesis. By this division, chroma- lular bridges persist until late spermiogenesis. In sper- tids are finally separated leading to round spermatids matogonia, genomic imprinting for parent-of-origin- with a haploid number of chromosomes and DNA con- dependent regulation of gene expression via DNA tent (1n1 C). methylation takes place and is finished before the first meiotic division (Kierszenbaum 2002). II.1.3.5 Spermatids/Spermiogenesis II.1.3.4 Early round spermatids are postmitotic cells, exhibit a Spermatocytes/Meiosis nucleus with a homogenous chromatin pattern and can be identified by the perinuclear acrosome vesicle, II.1.3.4.1 which can easily be seen after periodic acid Schiff (PAS) Primary Spermatocytes reaction on formalin, or Bouin-fixed paraffin-embed- Meiosis starts with DNA synthesis of type B spermato- ded sections or at the ultrastructural level. gonia which lose contact with the basal lamina (prelep- The transformation of conventional round cell sper-
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