Transplantation of spermatogonial stem cells in stallions.
Abstract: Spermatogonial stem cells originate from gonocytes and undergo self-renewal and differentiation to generate mature spermatozoa via spermatogenesis in the seminiferous tubules of the testis in male mammals. Owing to the unique capacity of these cells, the spermatogonial stem cell transplantation technique, which enables the restoration of male fertility by transfer of germlines between donor and recipient males, has been developed. Thus, spermatogonial stem cell transplantation can be used as an important next-generation reproductive and breeding tool in livestock production. However, in large animals, this approach is associated with many technical limitations and inefficiency. Furthermore, research regrading spermatogonial stem cell transplantation in stallions is limited. Therefore, this review article describes the history and current knowledge regarding spermatogonial stem cell transplantation in animals and challenges in establishing an experimental protocol for successful spermatogonial stem cell transplantation in stallions, which have been presented under the following heads: spermatogonial stem cell isolation, recipient preparation, and spermatogonial stem cell transplantation. Additionally, we suggest that further investigation based on previous unequivocal evidence regarding donor-derived spermatogenesis in large animals must be conducted. A detailed and better understanding of the physical and physiological aspects is required to discuss the current status of this technique field and develop future directions for the establishment of spermatogonial stem cell transplantation in stallions.
© Copyright 2024 Korean Society of Animal Science and Technology.
Publication Date: 2024-07-31 PubMed ID: 39165739PubMed Central: PMC11331362DOI: 10.5187/jast.2024.e30Google Scholar: Lookup
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Summary
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This research article discusses the development and challenges of transplanting spermatogonial stem cells (cells involved in sperm production) in stallions (male horses), a potentially important tool for enhancing livestock production.
Introduction to Spermatogonial Stem Cell Transplantation
- Spermatogonial stem cells (SSCs), which are responsible for the generation of mature sperm cells in male mammals, are derived from a type of stem cell called gonocytes.
- SSCs possess certain unique attributes, such as self-renewal (ability to produce copies of themselves) and differentiation (evolution into other types of cells).
- Through a process known as SSC transplantation, transferring these cells between different males can restore fertility in those who may be infertile.
- This transplant technique has potential uses in livestock production systems as a next-generation reproductive tool.
Challenges in SSC Transplantation in Large Animals
- Despite the potential advantages of SSC transplantation, implementing it in larger animals, particularly stallions, has proven challenging due to various technical limitations and issues of inefficiency.
- The article mentions a lack of detailed research on SSC transplantation in stallions, signaling a need for further study in this area.
Key Aspects of SSC Transplantation
- The research article highlights three main areas to focus on when performing SSC transplantation: SSC isolation, recipient preparation, and the transplantation itself.
- The authors stress on the need for an in-depth understanding of the physical and physiological aspects involved in the process for progress in this field.
Conclusion and Future Directions
- The researchers suggest that more conclusive evidence is needed regarding donor-derived spermatogenesis in large animals.
- This would entail further investigation and the establishment of clear experimental protocols for SSC transplantation in stallions.
- Success in these areas could help overcome the current technical challenges and inefficiencies observed in this field, and open up new possibilities for reproductive interventions in livestock production.
Cite This Article
APA
Jung H, Yoon M.
(2024).
Transplantation of spermatogonial stem cells in stallions.
J Anim Sci Technol, 66(4), 635-644.
https://doi.org/10.5187/jast.2024.e30 Publication
Researcher Affiliations
- Research Center for Horse Industry, Kyungpook National University, Sangju 37224, Korea.
- Research Center for Horse Industry, Kyungpook National University, Sangju 37224, Korea.
- Department of Horse, Companion and Wild Animal Science, Kyungpook National University, Sangju 37224, Korea.
Conflict of Interest Statement
No potential conflict of interest relevant to this article was reported.
References
This article includes 75 references
- Griswold MD. Spermatogenesis: the commitment to meiosis.. Physiol Rev 2016;96:1–17.
- Smith LB, Walker WH. The regulation of spermatogenesis by androgens.. Semin Cell Dev Biol 2014;30:2–13.
- Kubota H, Brinster RL. Spermatogonial stem cells.. Biol Reprod 2018;99:52–74.
- Ogawa T, Aréchaga JM, Avarbock MR, Brinster RL. Transplantation of testis germinal cells into mouse seminiferous tubules.. Int J Dev Biol 1997;41:111–22.
- Nagano M, Avarbock MR, Brinster RL. Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes.. Biol Reprod 1999;60:1429–36.
- Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation.. Proc Natl Acad Sci USA 1994;91:11298–302.
- Honaramooz A, Megee SO, Dobrinski I. Germ cell transplantation in pigs.. Biol Reprod 2002;66:21–8.
- Zeng W, Tang L, Bondareva A, Honaramooz A, Tanco V, Dores C. Viral transduction of male germline stem cells results in transgene transmission after germ cell transplantation in pigs.. Biol Reprod 2013;88:27.
- Kim BG, Kim YH, Lee YA, Kim BJ, Kim KJ, Jung SE. Production of transgenic spermatozoa by lentiviral transduction and transplantation of porcine spermatogonial stem cells.. Tissue Eng Regen Med 2014;11:458–66.
- Izadyar F, Den Ouden K, Stout TA, Stout J, Coret J, Lankveld DP. Autologous and homologous transplantation of bovine spermatogonial stem cells.. Reproduction 2003;126:765–74.
- Herrid M, Vignarajan S, Davey R, Dobrinski I, Hill JR. Successful transplantation of bovine testicular cells to heterologous recipients.. Reproduction 2006;132:617–24.
- Stockwell S, Herrid M, Davey R, Brownlee A, Hutton K, Hill JR. Microsatellite detection of donor-derived sperm DNA following germ cell transplantation in cattle.. Reprod Fertil Dev 2009;21:462–8.
- Honaramooz A, Behboodi E, Megee SO, Overton SA, Galantino-Homer H, Echelard Y. Fertility and germline transmission of donor haplotype following germ cell transplantation in immunocompetent goats.. Biol Reprod 2003;69:1260–4.
- Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation.. Proc Natl Acad Sci USA 1994;91:11303–7.
- Honaramooz A, Megee S, Zeng W, Destrempes MM, Overton SA, Luo J. Adeno-associated virus (AAV)-mediated transduction of male germ line stem cells results in transgene transmission after germ cell transplantation.. FASEB J 2008;22:374–82.
- Li CH, Yan LZ, Ban WZ, Tu Q, Wu Y, Wang L. Long-term propagation of tree shrew spermatogonial stem cells in culture and successful generation of transgenic offspring.. Cell Res 2017;27:241–52.
- Schlatt S, Foppiani L, Rolf C, Weinbauer GF, Nieschlag E. Germ cell transplantation into X-irradiated monkey testes.. Hum Reprod 2002;17:55–62.
- Schlatt S, Rosiepen G, Weinbauer GF, Rolf C, Brook PF, Nieschlag E. Germ cell transfer into rat, bovine, monkey and human testes.. Hum Reprod 1999;14:144–50.
- Jahnukainen K, Ehmcke J, Quader MA, Saiful Huq M, Epperly MW, Hergenrother S. Testicular recovery after irradiation differs in prepubertal and pubertal non-human primates, and can be enhanced by autologous germ cell transplantation.. Hum Reprod 2011;26:1945–54.
- Kim Y, Turner D, Nelson J, Dobrinski I, McEntee M, Travis AJ. Production of donor-derived sperm after spermatogonial stem cell transplantation in the dog.. Reproduction 2008;136:823–31.
- Harkey MA, Asano A, Zoulas ME, Torok-Storb B, Nagashima J, Travis A. Isolation, genetic manipulation, and transplantation of canine spermatogonial stem cells: progress toward transgenesis through the male germ-line.. Reproduction 2013;146:75–90.
- Herrid M, Nagy P, Juhasz J, Morrell JM, Billah M, Khazanehdari K. Donor sperm production in heterologous recipients by testis germ cell transplantation in the dromedary camel.. Reprod Fertil Dev 2019;31:538–46.
- Smith E. Spermatogonial stem cell transfer to a mule [Master’s thesis]. Murfreesboro, TN: Middle Tennessee State University; 2015.
- Jung H, Yoon M. Germ cell transplantation in stallion testes.. J Equine Vet Sci 2021;106:103748.
- Oatley JM, Brinster RL. The germline stem cell niche unit in mammalian testes.. Physiol Rev 2012;92:577–95.
- de Rooij DG. The nature and dynamics of spermatogonial stem cells.. Development 2017;144:3022–30.
- Swierstra EE, Gebauer MR, Pickett BW. Reproductive physiology of the stallion: I. spermatogenesis and testis composition.. J Reprod Fertil 1974;40:113–23.
- França LR, Avelar GF, Almeida FFL. Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs.. Theriogenology 2005;63:300–18.
- Costa GMJ, Avelar GF, Rezende-Neto JV, Campos-Junior PHA, Lacerda SMSN, Andrade BSC. Spermatogonial stem cell markers and niche in equids.. PLOS ONE 2012;7:e44091.
- Johnson L, Blanchard TL, Varner DD, Scrutchfield WL. Factors affecting spermatogenesis in the stallion.. Theriogenology 1997;48:1199–216.
- Johnson L. Seasonal differences in equine spermatocytogenesis.. Biol Reprod 1991;44:284–91.
- Morel MCGD. Equine reproductive physiology, breeding and stud management.. 4th ed. Wallingford, Oxfordshire: CABI; 2015.
- Holstein AF, Schulze W, Davidoff M. Understanding spermatogenesis is a prerequisite for treatment.. Reprod Biol Endocrinol 2003;1:107.
- Chang YF, Lee-Chang JS, Panneerdoss S, MacLean JA 2nd, Rao MK. Isolation of Sertoli, Leydig, and spermatogenic cells from the mouse testis.. BioTechniques 2011;51:341–4.
- Heidari B, Rahmati-Ahmadabadi M, Akhondi MM, Zarnani AH, Jeddi-Tehrani M, Shirazi A. Isolation, identification, and culture of goat spermatogonial stem cells using c-kit and PGP9.5 markers.. J Assist Reprod Genet 2012;29:1029–38.
- Izadyar F, den Ouden K, Creemers LB, Posthuma G, Parvinen M, de Rooij DG. Proliferation and differentiation of bovine type A spermatogonia during long-term culture.. Biol Reprod 2003;68:272–81.
- Rafeeqi T, Kaul G. Isolation and enrichment of type A spermatogonia from pre-pubertal buffalo (Bubalus bubalis) testis.. Andrologia 2013;45:195–203.
- Hermann BP, Sukhwani M, Lin CC, Sheng Y, Tomko J, Rodriguez M. Characterization, cryopreservation, and ablation of spermatogonial stem cells in adult rhesus macaques.. Stem Cells 2007;25:2330–8.
- Lee KH, Lee WY, Kim JH, Yoon MJ, Kim NH, Kim JH. Characterization of GFRα-1-positive and GFRα-1-negative spermatogonia in neonatal pig testis.. Reprod Domest Anim 2013;48:954–60.
- Dores C, Alpaugh W, Dobrinski I. From in vitro culture to in vivo models to study testis development and spermatogenesis.. Cell Tissue Res 2012;349:691–702.
- Mikkola M, Sironen A, Kopp C, Taponen J, Sukura A, Vilkki J. Transplantation of normal boar testicular cells resulted in complete focal spermatogenesis in a boar affected by the immotile short-tail sperm defect.. Reprod Domest Anim 2006;41:124–8.
- Herrid M, Olejnik J, Jackson M, Suchowerska N, Stockwell S, Davey R. Irradiation enhances the efficiency of testicular germ cell transplantation in sheep.. Biol Reprod 2009;81:898–905.
- Kanatsu-Shinohara M, Morimoto H, Shinohara T. Enrichment of mouse spermatogonial stem cells by melanoma cell adhesion molecule expression.. Biol Reprod 2012;87:139.
- Tagelenbosch RAJ, de Rooij DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse.. Mutat Res 1993;290:193–200.
- Honaramooz A, Behboodi E, Hausler CL, Blash S, Ayres S, Azuma C. Depletion of endogenous germ cells in male pigs and goats in preparation for germ cell transplantation.. J Androl 2005;26:698–705.
- Zhao X, Wan W, Zhang X, Wu Z, Yang H. Spermatogonial stem cell transplantation in large animals.. Animals 2021;11:918.
- Jung H, Yoon M. Isolation of germ cells from testes of stallions using collagenase and trypsin-ethylenediaminetetraacetic acid.. J Equine Vet Sci 2016;43:82–7.
- Jung H, Roser JF, Yoon M. UTF1, a putative marker for spermatogonial stem cells in stallions.. PLOS ONE 2014;9:e108825.
- Jung HJ, Song H, Yoon MJ. Stage-dependent DAZL localization in stallion germ cells.. Anim Reprod Sci 2014;147:32–8.
- Choi Y, Jung Y, Kim S, Kim J, Jung H, Yoon M. Stage-dependent expression of protein gene product 9.5 in donkey testes.. Animals 2020;10:2169.
- Jung H, Song H, Yoon M. The KIT is a putative marker for differentiating spermatogonia in stallions.. Anim Reprod Sci 2015;152:39–46.
- Kim JT, Jung HJ, Song H, Yoon MJ. Acrosin-binding protein (ACRBP) in the testes of stallions.. Anim Reprod Sci 2015;163:179–86.
- Kim JY, Jung HJ, Yoon MJ. VASA (DDX4) is a putative marker for spermatogonia, spermatocytes and round spermatids in stallions.. Reprod Domest Anim 2015;50:1032–8.
- Lee G, Jung H, Yoon M. The Lin28 expression in stallion testes.. PLOS ONE 2016;11:e0165011.
- Kanatsu-Shinohara M, Miki H, Inoue K, Ogonuki N, Toyokuni S, Ogura A. Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions.. Biol Reprod 2005;72:985–91.
- Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S. Long-term proliferation in culture and germline transmission of mouse male germline stem cells.. Biol Reprod 2003;69:612–6.
- Zhang P, Chen X, Zheng Y, Zhu J, Qin Y, Lv Y. Long-term propagation of porcine undifferentiated spermatogonia.. Stem Cells Dev 2017;26:1121–31.
- Zheng Y, Tian X, Zhang Y, Qin J, An J, Zeng W. In vitro propagation of male germline stem cells from piglets.. J Assist Reprod Genet 2013;30:945–52.
- Brinster CJ, Ryu BY, Avarbock MR, Karagenc L, Brinster RL, Orwig KE. Restoration of fertility by germ cell transplantation requires effective recipient preparation.. Biol Reprod 2003;69:412–20.
- Igdoura SA, Wiebe JP. Suppression of spermatogenesis by low-level glycerol treatment.. J Androl 1994;15:234–43.
- Wiebe JP, Barr KJ. The control of male fertility by 1,2,3-trihydroxypropane (THP; glycerol): rapid arrest of spermatogenesis without altering libido, accessory organs, gonadal steroidogenesis, and serum testosterone, LH and FSH.. Contraception 1984;29:291–302.
- Creemers LB, Meng X, den Ouden K, van Pelt AMM, Izadyar F, Santoro M. Transplantation of germ cells from glial cell line-derived neurotrophic factor-overexpressing mice to host testes depleted of endogenous spermatogenesis by fractionated irradiation.. Biol Reprod 2002;66:1579–84.
- Shuttlesworth GA, De Rooij DG, Huhtaniemi I, Reissmann T, Russell LD, Shetty G. Enhancement of A spermatogonial proliferation and differentiation in irradiated rats by gonadotropin-releasing hormone antagonist administration.. Endocrinology 2000;141:37–49.
- Ma W, Wang J, Gao W, Jia H. The safe recipient of SSC transplantation prepared by heat shock with busulfan treatment in mice.. Cell Transplant 2018;27:1451–8.
- Ma W, An L, Wu Z, Wang X, Guo M, Miao K. Efficient and safe recipient preparation for transplantation of mouse spermatogonial stem cells: pretreating testes with heat shock.. Biol Reprod 2011;85:670–7.
- Jung H, Yoon M. Effects of intravenous multiple busulfan injection on suppression of endogenous spermatogenesis in recipient stallion testes.. J Anim Sci Technol 2021;63:1194–203.
- Jung H, Yoon M. Effects of intratesticular injection of 70% glycerin of stallions.. J Equine Vet Sci 2017;49:1–10.
- Gul M, Hildorf S, Dong L, Thorup J, Hoffmann ER, Jensen CFS. Review of injection techniques for spermatogonial stem cell transplantation.. Hum Reprod Update 2020;26:368–91.
- Dym M. The mammalian rete testis — a morphological examination.. Anat Rec 1976;186:493–523.
- Kim YH, Kang HG, Kim BJ, Jung SE, Karmakar PC, Kim SM. Enrichment and in vitro culture of spermatogonial stem cells from pre-pubertal monkey testes.. Tissue Eng Regen Med 2017;14:557–66.
- Baert Y, Braye A, Struijk RB, van Pelt AMM, Goossens E. Cryopreservation of testicular tissue before long-term testicular cell culture does not alter in vitro cell dynamics.. Fertil Steril 2015;104:1244–52.E4.
- Reda A, Hou M, Winton TR, Chapin RE, Söder O, Stukenborg JB. In vitro differentiation of rat spermatogonia into round spermatids in tissue culture.. Mol Hum Reprod 2016;22:601–12.
- Honaramooz A, Snedaker A, Boiani M, Schöler H, Dobrinski I, Schlatt S. Sperm from neonatal mammalian testes grafted in mice.. Nature 2002;418:778–81.
- Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes.. Biol Reprod 1999;60:515–21.
- Clouthier DE, Avarbock MR, Maika SD, Hammer RE, Brinster RL. Rat spermatogenesis in mouse testis.. Nature 1996;381:418–21.
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