reticulum translocate ectoplasmic specializations and hence spermatids are also translocated [48].
Spermiation
During spermiation, mature spermatids are released from SC into ST lumen prior to their subsequent passage to the epididymis. For spermiation, mature spermatids are oriented toward the lumen of the ST and subsequently released into the lumen by spermiation machinery over several days. Spermiation involves remodeling of the spermatid head and cytoplasm, removal of specialized adhesion structures between SC and mature spermatids, and the final expulsion of mature spermatid heads from the SC crypts [49].
Phagocytosis
After spermiation, SC phagocytose degenerated residual bodies of released spermatids. Moreover, SC phagocytose the germ cell degenerated during spermatogenesis [50]. Moreover, SC are capable of pinocytosis in the adluminal compartment and receptor‐mediated endocytosis in the basal compartment of the ST [51].
Secretions
SC secrete different types of proteases, protease inhibitors, hormones, energy substrates, growth factors, paracrine factors, and extracellular matrix components. Proteases and protease inhibitors from SC participate in ST maintenance, repair, growth, remodeling, and restructuring. Protease inhibitors are required for germ cell translocation across the blood–testis barrier and for spermiation [52]. Moreover, protease inhibitors are involved in assembly and disassembly of cellular junctions in the ST [53].
SC secrete adluminal fluid and maintain a specific environment for differentiation of germ cells toward lumen of the ST [33]. FSH‐regulated functions of SC include transfer of testosterone and glucose and germ cell nurturing by provision of lactate and pyruvate. Under the influence of FSH and androgens, SC secrete proteins necessary for germ cells and interstitial cells of the testes and secrete androgen binding proteins to ensure bioavailability of androgens [54, 55]. Inhibin and activins from SC act on the hypothalamic–pituitary–gonadal axis and also on Leydig cells [56]. The iron carrier protein, transferrin, is produced by SC and its concentration in seminal plasma is correlated with fertility and spermatogenic capacity in the bull [57]. SC co‐cultured with germ cells stimulate DNA and RNA synthesis in the germ cells [58]. Seminiferous growth factor is involved in spermatogonial proliferation, nerve growth factor is required for DNA synthesis in preleptotene spermatocytes, and insulin‐like growth factor‐1 helps in germ cell differentiation [59].
The germ cells residing in the adluminal compartment cannot receive nutrients directly from blood due to the blood–testis barrier. The spermatocytes and spermatids in the adluminal compartment are nursed by amino acids, carbohydrates, lipids, vitamins, and metal ions from SC [34].
The Junctional Role of Sertoli Cells
SC make and break junctions among themselves and with different types of germ cells. Major junctions formed by SC are tight junctions, anchoring junctions, ectoplasmic specialization, tubulobulbar complexes, and communication junctions. Tight junctions are present between adjacent SC at the level of the blood–testis barrier and function as a semipermeable barrier – the barrier function. Tight junctions divide SC into basal and adluminal, preventing mixing of molecules in the two compartments – the fence function. Anchoring junctions include adherens junctions (also known as zonula adherens), focal contacts or adhesions, desmosomes, and hemidesmosomes. All these anchoring junctions are biochemically and structurally different from one another and mainly function to connect adjacent cells to one another or to extracellular matrix through cytoskeleton, thus maintaining tissue integrity. Anchoring junctions also function in signal transduction to regulate cell proliferation, differentiation, and translocation. Ectoplasmic specialization is a modified form of adherent junctions and mainly functions in spermiation and maintenance of other junctions present between adjacent SC and, SC and germ cells. Tubulobulbar complexes, also a modified form of zonula adherens, are present between adjacent SC at the level of tight junctions and between SC and mature spermatids ready for spermiation. Focal contacts are actin‐based junctions between testicular cells and extracellular matrix and play an adhesive function at ectoplasmic specialization. Desmosomes are intermediate filament‐based junctions found between SC and SC, and SC and germ cells. Hemidesmosomes are intermediate filament‐based junctions found only between SC and basal lamina; these have adhesive function. Communication junctions are either chemical synapses or gap junctions. Gap junctions, intercellular channels formed by connexons, transduce signals between SC and germ cells and thus participate in germ cell translocation. Gap junctions are present between SC and SC, SC and germ cells, and between two Leydig cells [34].
Sertoli Cells and Spermatogenic Capacity
In the bull, DSP is correlated with total SC number (R = +0.83) and SC per gram (R = +0.47) but is not correlated with the number of germ cells supported per SC. Testicular parenchyma weight is also correlated with total SC number (R = +0.61). Total SC number is the foremost determinant of the variation in DSP among bulls (R2 = 68.2%) [60, 61]. However, total SC number and the number of germ cells per SC are not correlated with the quality of either fresh or frozen bull semen [62]. Moreover, SC number in the horse (R2 = 68) and human (R2 = 39) is also correlated with DSP. The association between SC and DSP goes back to the association between SC and the number of A1 spermatogonia (R2 = 55 for the horse) [33].
In the bull, the majority of SC proliferation happens during fetal life in utero. SC number increases by five times from birth until puberty and no increase in SC number occurs after puberty. Once mitosis in SC stops, the cells differentiate to mature SC and continue their adult function for the reproductive life of the bull [63]. However, the stallion being a seasonal breeder has no permanent SC number after puberty and SC number and volume of SC nuclei per testes increase during the breeding season for a 4‐ to 20‐year‐old stallion. The size of horse SC does not differentiate with respect to breeding season [33]. A concurrent increase in the number of A spermatogonia accompanies increased SC number during the breeding season [64].
References
1 1 Oatley, J. and Brinster, R. (2006). Spermatogonial stem cells. Methods Enzymol. 419: 259–282.
2 2 Waqas M. Enhancing sperm production in the bull. PhD Dissertation 2018 (accessed 9 November 2020). Available from https://research.libraries.wsu.edu/xmlui/bitstream/handle/2376/16407/waqas_wsu_0251e_12450.pdf?sequence=1&isallowed=y.
3 3 Oatley, J. (2010). Spermatogonial stem cell biology in the bull: development of isolation, culture, and transplantation methodologies and their potential impacts on cattle production. Soc. Reprod. Fertil. Suppl. 67: 133–143.
4 4 Griswold, M. and Oatley, J. (2013). Concise review: defining characteristics of mammalian spermatogenic stem cells. Stem Cells 31: 8–11.
5 5 McLaren, A. (2000). Establishment of the germ cell lineage in mammals. J. Cell. Physiol. 182: 141–143.
6 6 McLaren, A. (1998). Gonad development: assembling the mammalian testis. Curr. Biol. 8: R175–R177.
7 7 Yoshioka, H., McCarrey, J., and Yamazaki, Y. (2009). Dynamic nuclear organization of constitutive heterochromatin during fetal male germ cell development in mice. Biol. Reprod. 80: 804–812.
8 8 Tagelenbosch, R. and de Rooij, D. (1993). A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F 1 hybrid mouse. Mutat. Res./Fundam. Mol. Mech. Mutagen. 290: 193–200.
9 9 Huckins, C. (1971). The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat. Rec. 169: 533–557.
10 10 Oakberg, E. (1971). Spermatogonial stem‐cell renewal in the mouse. Anat. Rec. 169: 515–531.
11 11 Nakagawa, T., Sharma, M., Nabeshima, Y. et al. (2010). Functional hierarchy and reversibility within the