Abstract
At present, the knowledge base on characteristics and biology of spermatogonia in livestock is limited in comparison to rodents, yet the importance of studying these cells for comparative species analysis and enhancing reproductive capacity in food animals is high. Previous studies have established that although many core attributes of organ physiology and mechanisms governing essential cellular functions are conserved across eutherians, significant differences exist between mice and higher order mammals. In this chapter, we briefly discuss distinguishing aspects of testicular anatomy and the spermatogenic lineage in livestock and critical considerations for studying spermatogonial stem cell biology in these species.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Russell LD, Ettlin RA, Hikim APS, Cless ED (1990) Histological and histopathological evaluation of the testis, 1st edn. Cache River Press, St. Louis
Bustos-Obregon E (1976) Ultrastructure and function of the lamina propria of mammalian seminiferous tubules. Andrologia 8(3):179–185
Figueiredo AFA et al (2021) Insights into differentiation and function of the transition region between the seminiferous tubule and rete testis. Differentiation 120:36–47
Dym M (1974) The fine structure of monkey Sertoli cells in the transitional zone at the junction of the seminiferous tubules with the tubuli recti. Am J Anat 140(1):1–25
Hermo L, Dworkin J (1988) Transitional cells at the junction of seminiferous tubules with the rete testis of the rat: their fine structure, endocytic activity, and basement membrane. Am J Anat 181(2):111–131
Aiyama Y et al (2015) A niche for GFRalpha1-positive spermatogonia in the terminal segments of the seminiferous tubules in hamster testes. Stem Cells 33(9):2811–2824
de Rooij DG, Russell LD (2000) All you wanted to know about spermatogonia but were afraid to ask. J Androl 21(6):776–798
Griswold MD (2016) Spermatogenesis: the commitment to meiosis. Physiol Rev 96(1):1–17
Griswold MD (2018) 50 years of spermatogenesis: Sertoli cells and their interactions with germ cells. Biol Reprod 99:87
Clermont Y (1972) Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 52(1):198–236
Staub C, Johnson L (2018) Review: spermatogenesis in the bull. Animal 12(s1):s27–s35
Franca LR, Becker-Silva SC, Chiarini-Garcia H (1999) The length of the cycle of seminiferous epithelium in goats (Capra hircus). Tissue Cell 31(3):274–280
Frankenhuis MT, Kramer MF, de Rooij DG (1982) Spermatogenesis in the boar. Vet Q 4(2):57–61
Courot M, Ortavant R (1981) Endocrine control of spermatogenesis in the ram. J Reprod Fertil Suppl 30:47–60
Amann RP (1962) Reproductive capacity of dairy bulls. IV. Spermatogenesis and testicular germ cell degeneration. Am J Anat 110:69–78
Johnson L, Petty CS, Neaves WB (1980) A comparative study of daily sperm production and testicular composition in humans and rats. Biol Reprod 22(5):1233–1243
Oatley JM, Brinster RL (2008) Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 24:263–286
de Rooij DG (1973) Spermatogonial stem cell renewal in the mouse. I Normal situation. Cell Tissue Kinet 6(3):281–287
Endo T et al (2015) Periodic retinoic acid-STRA8 signaling intersects with periodic germ-cell competencies to regulate spermatogenesis. Proc Natl Acad Sci U S A 112(18):E2347–E2356
Hogarth CA et al (2015) Processive pulses of retinoic acid propel asynchronous and continuous murine sperm production. Biol Reprod 92(2):37
Tegelenbosch RA, de Rooij DG (1993) A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res 290(2):193–200
Koubova J et al (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A 103(8):2474–2479
Brinster RL, Zimmermann JW (1994) Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A 91(24):11298–11302
Brinster RL, Avarbock MR (1994) Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A 91(24):11303–11307
Ciccarelli M et al (2020) Donor-derived spermatogenesis following stem cell transplantation in sterile NANOS2 knockout males. Proc Natl Acad Sci U S A 117(39):24195–24204
Buaas FW et al (2004) Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36(6):647–652
Costoya JA et al (2004) Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36(6):653–659
Kwon J et al (2004) Developmental regulation of ubiquitin C-terminal hydrolase isozyme expression during spermatogenesis in mice. Biol Reprod 71(2):515–521
Oatley MJ et al (2016) Conditions for long-term culture of cattle undifferentiated spermatogonia. Biol Reprod 95(1):14
Herrid M, Davey RJ, Hill JR (2007) Characterization of germ cells from pre-pubertal bull calves in preparation for germ cell transplantation. Cell Tissue Res 330(2):321–329
Clotaire DZJ et al (2019) Functions of promyelocytic leukaemia zinc finger (Plzf) in male germline stem cell development and differentiation. Reprod Fertil Dev 31:1315
Borjigin U et al (2010) Expression of promyelocytic leukaemia zinc-finger in ovine testis and its application in evaluating the enrichment efficiency of differential plating. Reprod Fertil Dev 22(5):733–742
Luo J et al (2006) Protein gene product 9.5 is a spermatogonia-specific marker in the pig testis: application to enrichment and culture of porcine spermatogonia. Mol Reprod Dev 73(12):1531–1540
La HM et al (2018) Identification of dynamic undifferentiated cell states within the male germline. Nat Commun 9(1):2819
Kubota H, Avarbock MR, Brinster RL (2003) Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci U S A 100(11):6487–6492
Shinohara T, Avarbock MR, Brinster RL (1999) beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 96(10):5504–5509
Kanatsu-Shinohara M, Toyokuni S, Shinohara T (2004) CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 70(1):70–75
Lee WY et al (2013) Establishment and in vitro culture of porcine spermatogonial germ cells in low temperature culture conditions. Stem Cell Res 11(3):1234–1249
Reding SC et al (2010) THY1 is a conserved marker of undifferentiated spermatogonia in the pre-pubertal bull testis. Reproduction 139(5):893–903
Abbasi H et al (2013) THY1 as a reliable marker for enrichment of undifferentiated spermatogonia in the goat. Theriogenology 80(8):923–932
Cai H et al (2016) Enrichment and culture of spermatogonia from cryopreserved adult bovine testis tissue. Anim Reprod Sci 166:109–115
Kim YH et al (2013) Stage-specific embryonic antigen-1 expression by undifferentiated spermatogonia in the prepubertal boar testis. J Anim Sci 91(7):3143–3154
Suyatno et al (2018) Long-term culture of undifferentiated spermatogonia isolated from immature and adult bovine testes. Mol Reprod Dev 85(3):236–249
Goel S et al (2007) Identification, isolation, and in vitro culture of porcine gonocytes. Biol Reprod 77(1):127–137
Oatley JM et al (2009) Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development 136(7):1191–1199
Chen H et al (2017) Leydig cell stem cells: identification, proliferation and differentiation. Mol Cell Endocrinol 445:65–73
Tepekoy F et al (2015) CD90 and CD105 expression in the mouse ovary and testis at different stages of postnatal development. Reprod Biol 15(4):195–204
Helsel AR et al (2017) ID4 levels dictate the stem cell state in mouse spermatogonia. Development 144(4):624–634
Chan F et al (2014) Functional and molecular features of the Id4+ germline stem cell population in mouse testes. Genes Dev 28(12):1351–1362
Oatley MJ et al (2011) Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice. Biol Reprod 85(2):347–356
Aloisio GM et al (2014) PAX7 expression defines germline stem cells in the adult testis. J Clin Invest 124(9):3929–3944
Hara K et al (2014) Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states. Cell Stem Cell 14(5):658–672
Sachs C et al (2014) Evaluation of candidate spermatogonial markers ID4 and GPR125 in testes of adult human cadaveric organ donors. Andrology 2(4):607–614
Hermann BP et al (2018) The mammalian spermatogenesis single-cell transcriptome, from spermatogonial stem cells to spermatids. Cell Rep 25(6):1650–1667. e8
Shami AN et al (2020) Single-cell RNA sequencing of human, macaque, and mouse testes uncovers conserved and divergent features of mammalian spermatogenesis. Dev Cell 54(4):529–547. e12
Nakamura Y et al (2021) Transient suppression of transplanted spermatogonial stem cell differentiation restores fertility in mice. Cell Stem Cell 28(8):1443–1456. e7
Ebata KT, Zhang X, Nagano MC (2005) Expression patterns of cell-surface molecules on male germ line stem cells during postnatal mouse development. Mol Reprod Dev 72(2):171–181
Garbuzov A et al (2018) Purification of GFRalpha1+ and GFRalpha1- spermatogonial stem cells reveals a niche-dependent mechanism for fate determination. Stem Cell Rep 10(2):553–567
Zheng K et al (2009) The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse. BMC Dev Biol 9:38
Manova K et al (1990) Gonadal expression of c-kit encoded at the W locus of the mouse. Development 110(4):1057–1069
Yoshinaga K et al (1991) Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 113(2):689–699
Sharma M et al (2019) Identification of EOMES-expressing spermatogonial stem cells and their regulation by PLZF. elife 8:e43352
Kanatsu-Shinohara M et al (2003) Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 69(2):612–616
Kubota H, Avarbock MR, Brinster RL (2004) Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 101(47):16489–16494
Kanatsu-Shinohara M et al (2014) Improved serum- and feeder-free culture of mouse germline stem cells. Biol Reprod 91(4):88
Kanatsu-Shinohara M, Shinohara T (2007) Culture and genetic modification of mouse germline stem cells. Ann N Y Acad Sci 1120:59–71
Shiromoto Y et al (2019) GPAT2 is required for piRNA biogenesis, transposon silencing, and maintenance of spermatogonia in micedagger. Biol Reprod 101(1):248–256
Mulder CL et al (2018) Long-term health in recipients of transplanted in vitro propagated spermatogonial stem cells. Hum Reprod 33(1):81–90
Sato T et al (2013) In vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat Protoc 8(11):2098–2104
Kanatsu-Shinohara M et al (2005) Genetic and epigenetic properties of mouse male germline stem cells during long-term culture. Development 132(18):4155–4163
Helsel AR, Oatley MJ, Oatley JM (2017) Glycolysis-optimized conditions enhance maintenance of regenerative integrity in mouse spermatogonial stem cells during long-term culture. Stem Cell Rep 8:1430
Aponte PM et al (2006) Basic features of bovine spermatogonial culture and effects of glial cell line-derived neurotrophic factor. Theriogenology 65(9):1828–1847
Izadyar F et al (2003) Proliferation and differentiation of bovine type A spermatogonia during long-term culture. Biol Reprod 68(1):272–281
Zhao X et al (2021) Isolation and in vitro expansion of porcine spermatogonial stem cells. Reprod Domest Anim 57(2):210–220
Zhang P et al (2017) Long-term propagation of porcine undifferentiated spermatogonia. Stem Cells Dev 26(15):1121–1131
Zhao HM et al (2016) Isolation, proliferation, and induction of Bama mini-pig spermatogonial stem cells in vitro. Genet Mol Res 15(3). https://doi.org/10.4238/gmr.15038602
Heidari B et al (2012) Isolation, identification, and culture of goat spermatogonial stem cells using c-kit and PGP9.5 markers. J Assist Reprod Genet 29(10):1029–1038
Pramod RK, Mitra A (2014) In vitro culture and characterization of spermatogonial stem cells on Sertoli cell feeder layer in goat (Capra hircus). J Assist Reprod Genet 31(8):993–1001
Zhu H et al (2014) Characterization of immortalized dairy goat male germline stem cells (mGSCs). J Cell Biochem 115(9):1549–1560
Qasemi-Panahi B et al (2018) Isolation and proliferation of spermatogonial cells from Ghezel sheep. Avicenna J Med Biotechnol 10(2):93–97
Binsila KB et al (2018) Isolation and enrichment of putative spermatogonial stem cells from ram (Ovis aries) testis. Anim Reprod Sci 196:9–18
Giassetti MI, Ciccarelli M, Oatley JM (2019) Spermatogonial stem cell transplantation: insights and outlook for domestic animals. Annu Rev Anim Biosci 7:385–401
Herrid M et al (2006) Successful transplantation of bovine testicular cells to heterologous recipients. Reproduction 132(4):617–624
Honaramooz A et al (2003) Fertility and germline transmission of donor haplotype following germ cell transplantation in immunocompetent goats. Biol Reprod 69(4):1260–1264
Honaramooz A et al (2003) Germ cell transplantation in goats. Mol Reprod Dev 64(4):422–428
Honaramooz A, Megee SO, Dobrinski I (2002) Germ cell transplantation in pigs. Biol Reprod 66(1):21–28
Stockwell S et al (2013) Transplanted germ cells persist long-term in irradiated ram testes. Anim Reprod Sci 142(3–4):137–140
Stockwell S et al (2009) Microsatellite detection of donor-derived sperm DNA following germ cell transplantation in cattle. Reprod Fertil Dev 21(3):462–468
Herrid M et al (2009) Irradiation enhances the efficiency of testicular germ cell transplantation in sheep. Biol Reprod 81(5):898–905
Izadyar F et al (2003) Autologous and homologous transplantation of bovine spermatogonial stem cells. Reproduction 126(6):765–774
Rodriguez-Sosa JR, Dobson H, Hahnel A (2006) Isolation and transplantation of spermatogonia in sheep. Theriogenology 66(9):2091–2103
Rodriguez-Sosa JR et al (2009) Transduction and transplantation of spermatogonia into the testis of ram lambs through the extra-testicular rete. Reprod Domest Anim 44(4):612–620
Ogawa T et al (1997) Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 41(1):111–122
Heller CH, Clermont Y (1964) Kinetics of the germinal epithelium in man. Recent Prog Horm Res 20:545–575
Swierstra EE (1968) Cytology and duration of the cycle of the seminiferous epithelium of the boar; duration of spermatozoan transit through the epididymis. Anat Rec 161(2):171–185
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature
About this protocol
Cite this protocol
Ciccarelli, M., Oatley, J.M. (2023). Perspectives: Approaches for Studying Livestock Spermatogonia. In: M. Oatley, J., Hermann, B.P. (eds) Spermatogonial Stem Cells. Methods in Molecular Biology, vol 2656. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3139-3_17
Download citation
DOI: https://doi.org/10.1007/978-1-0716-3139-3_17
Published:
Publisher Name: Humana, New York, NY
Print ISBN: 978-1-0716-3138-6
Online ISBN: 978-1-0716-3139-3
eBook Packages: Springer Protocols