Livestock Genetic Improvements through Spermatogonial Stem Cell Transplantation Technology

Suyatno Suyatno

Abstract

Stem cells are unique cells that have the ability to differentiate into cells with specific functions and renew themselves to produce new stem cells. One type of stem cells that are actively studied is Spermatogonial Stem Cells (SSC). SSC is a unipotent cell that develops into spermatozoa in the mammalian testis. SSC can be transplanted into male testis recipients to improve the genetic quality of livestock and propagate valuable livestock. SSC transplantation procedure is started from the isolation of SSC from testis of the donor animal, in vitro culture of SCC for propagation or genetic modification, preparations of recipient males, and transplant SSC into recipient males to produce normal sperm that can fertilize the egg.  SSC transplantation technology has been successfully applied to large animals such as cattle, goats, sheep, buffalo, pigs, other mammals such as monkeys. SSC transplantation is promising biotechnology to improve livestock production in the near future. This review will describe the origins of the SSC, identification, and characterization of SSC, in vitro culture of SSC, and the application of SSC transplantation for genetic quality of livestock improvement.

Keywords

Spermatogonial stem cell; livestock genetic improvement; transplantation

Full Text:

PDF

References

Agung PP, Said S, Sudiro A. 2016. Myostatin gene analysis in the first generation of the Belgian Blue cattle in Indonesia. J Indones Trop Anim Agric. 41:13–20. doi: 10.14710/jitaa.41.1.13-20.

Almunia J, Nakamura K, Murakami M, Takashima S, Takasu M. 2018. Characterization of domestic pig spermatogenesis using spermatogonial stem cell markers in the early months of life. Theriogenology, 107:154–161. doi: 10.1016/j.theriogenology.2017.10. 041.

Aponte PM. 2015. Spermatogonial stem cells: Current biotechnological advances in reproduction and regenerative medicine. World J Stem Cells. 7:669. doi: 10.4252/wjsc.v7.i4.669.

Brinster RL, Zimmermann JW. 1994. Spermatogenesis following male germ-cell transplantation. Proceedings of the National Academy of Sciences of the United States of America. 91:11298–11302.

Chatzeli L, Simons BD. 2020. Tracing the dynamics of stem cell fate. Cold Spring Harbor Perspectives in Biology. 12:a036202. doi: 10.1101/cshperspect.a036202.

Chen Z, Hong F, Wang Z, Hao D, Yang H. 2020. Spermatogonial stem cells are a promising and pluripotent cell source for regenerative medicine. Am J Transl Res. 12:7048–7059.

Chen Z, Li Z, He Z. 2015. Plasticity of male germline stem cells and their applications in reproductive and regenerative medicine. Asian J Androl. 17:367–372. doi: 10.4103/1008-682X.143739.

Cheon YP, Choi D, Lee SH, Kim CG. 2020. YY1 and CP2c in unidirectional spermatogenesis and stemness. Develop Reprod. 24:249–262. doi: 10.12717/DR.2020.24.4.249.

Ciccarelli M., Giassetti MI, Miao D, Oatley MJ, Robbins C, Lopez-Biladeau B, Waqas MS, Tibary A, Whitelaw B, Lillico S, Park CH, Park KE, Telugu B, Fan Z, Liu Y, Regouski M, Polejaeva IA, Oatley JM. 2020. Donor-derived spermatogenesis following stem cell transplantation in sterile NANOS2 knockout males. Proceedings of the National Academy of Sciences of the United States of America. 117:24195–24204. doi: 10.1073/pnas.2010102117.

Costa GMJ, Avelar GF, Rezende-Neto JV, Campos-Junior P HA, Lacerda SMSN, Andrade BSC, Thomé RG, Hofmann MC, Franca LR. 2012. Spermatogonial stem cell markers and niche in equids. PLOS ONE. 7:e44091. doi: 10.1371/journal.pone.0044091

Feng W, Chen S, Do D, Liu Q, Deng Y, Lei X, Luo C, Huang B, Shi D. 2016. Isolation and identification of prepubertal buffalo (Bubalus bubalis) spermatogonial stem cells. Asian-Australas J Anim Sci. 29:1407–1415. doi: 10.5713/ ajas.15.0592.

Fujihara M, Kim SM, Minami N, Yamada M, Imai H. 2011. Characterization and in vitro culture of male germ cells from developing bovine testis. J Reprod Develop. 57:355–364.

Giassetti MI, Ciccarelli M, Oatley JM. 2019. Spermatogonial stem cell transplantation: Insights and outlook for domestic animals. Ann Rev Anim Biosci. 7:385–401. doi: 10.1146/annurev-animal-020518-115239.

Giassetti MI, Goissis MD, Moreira PV, de Barros FRO, Assumpção MEOD, Visintin JA. 2016. Effect of age on expression of spermatogonial markers in bovine testis and isolated cells. Anim Reprod Sci. 170:68–74. doi: 10.1016/j.anireprosci.2016.04.004.

Goissis MD, Giassetti MI, Worst RA, Mendes CM, Moreira PV, Assumpção MEOA, Visintin JA. 2018. Spermatogonial stem cell potential of CXCR4-positive cells from prepubertal bull testes. Anim Reprod Sci. 196:219–229. doi: 10.1016/j.anireprosci. 2018.08.014.

Hamra FK, Richie CT, Harvey BK. 2017. Long Evans rat spermatogonial lines are effective germline vectors for transgenic rat production. Transgenic Res. 26:477–489. doi: 10.1007/s11248-017-0025-2.

Harkey MA, Asano A, Zoulas ME, Torok-Storb B, Nagashima J, Travis A. 2013. Isolation, genetic manipulation, and transplantation of canine spermatogonial stem cells: Progress toward transgenesis through the male germ line. Reproduction. 146:10.1530/REP-13–0086. doi: 10.1530/REP-13-0086.

Heidari B, Rahmati-Ahmadabadi M, Akhondi MM, Zarnani, AH, Jeddi-Tehrani M, Shirazi A, Naderi MM, Behzadi B. 2012. Isolation, identification, and culture of goat spermatogonial stem cells using c-kit and PGP9.5 markers. J Assist Reprod Genet. 29:1029–1038. doi: 10.1007/s10815-012-9828-5.

Hermann BP, Sukhwani M, Winkler F, Pascarella JN, Peters KA, Sheng Y, Valli H, Rodriguez M, Ezzelarab M, Dargo G, Peterson K, Masterson K, Ramsey C, Ward T, Lienesch M, Volk A, Cooper DK, Thomson AW, Kiss JE, Orwig KE. 2012. Spermatogonial stem cell transplantation into Rhesus testes regenerates spermatogenesis producing functional sperm. Cell Stem Cell. 11:715–726. doi: 10.1016/j.stem.2012. 07.017.

Herrid M, Olejnik J, Jackson M, Suchowerska N, Stockwell S, Davey R, Hutton K, Hope S, Hill JR. 2009. Irradiation enhances the efficiency of testicular germ cell transplantation in sheep. Biol Reprod. 81:898–905. doi: 10.1095/biolreprod.109.078279.

Hill JR, Dobrinski I. 2005. Male germ cell transplantation in livestock. Reprod Fertil Develop. 18:13–18. doi: 10.1071/RD05123.

Honaramooz A, Behboodi E, Blash S, Megee SO, Dobrinski I. 2003. Germ cell transplantation in goats. Mol Reprod Develop. 64:422–428. doi: 10.1002/mrd. 10205.

Im JE, Song SH, Kim JY, Kim KL, Baek SH, Lee DR, Suh W. 2012. Vascular differentiation of multipotent spermatogonial stem cells derived from neonatal mouse testis. Experiment Mol Medic. 44:303–309. doi: 10.3858/emm.2012.44.4.034.

Ishikura Y, Yabuta Y, Ohta H, Hayashi K, Nakamura T, Okamoto I, Yamamoto T, Kurimoto K, Shirane K, Sasaki H, Saitou M. 2016. In vitro derivation and propagation of spermatogonial stem cell activity from mouse pluripotent stem cells. Cell Reports. 17:2789–2804. doi: 10.1016/j.celrep.2016.11.026.

Jin J. 2017. Stem cell treatments. JAMA. 317:330. doi: 10.1001/jama.2016.17822.

Kanatsu-Shinohara M, Naoki H, Shinohara T. 2016. Nonrandom germline transmission of mouse spermatogonial stem cells. Develop Cell. 38:248–261. doi: 10.1016/j.devcel.2016.07.011.

Kanatsu-Shinohara M, Shinohara T. 2013. Spermatogonial stem cell self-renewal and development. Ann Rev Cell Develop Biol. 29:163–187. doi: 10.1146/annurev-cellbio-101512-122353.

Kubota H, Brinster RL. 2018. Spermatogonial stem cells. Biol Reprod. 99:52–74. doi: 10.1093/biolre/ioy077.

La HM, Mäkelä JA, Chan AL, Rossello FJ, Nefzger CM, Legrand JMD, De Seram M, Polo JM, Hobbs RM. 2018. Identification of dynamic undifferentiated cell states within the male germline. Nat Communic. 9:2819. doi: 10.1038/s41467-018-04827-z.

Lee KH, Lee WY, Kim JH, Yoon MJ, Kim NH, Kim JH, Uhm SJ, Kim DH, Chung HJ, Song H. 2013. Characterization of GFRα-1-positive and GFRα-1-negative spermatogonia in neonatal pig testis. Reprod Domest Anim Zuchthygiene. 48:954–960. doi: 10.1111/rda.12193.

Lei Q, Pan Q, Ma J, Zhou Z, Li G, Chen S, Hua J. 2017. Establishment and characterization of immortalized bovine male germline stem cell line. J Integrative Agric. 16:2547–2557. doi: 10.1016/S2095-3119(16)61625-8.

Li CH, Yan LZ, Ban WZ, Tu Q, Wu Y, Wang L, Bi R, Ji S, Ma YH, Nie WH, Lv LB, Yao YG, Zhao XD, Zheng P. 2016. Long-term propagation of tree shrew spermatogonial stem cells in culture and successful generation of transgenic offspring. Cell Res. 27:241-252. doi: 10.1038/cr.2016.156.

Liu Y, Giannopoulou EG, Wen D, Falciatori I, Elemento O, Allis CD, Rafii S, Seandel M. 2016. Epigenetic profiles signify cell fate plasticity in unipotent spermatogonial stem and progenitor cells. Nat Communic. 7:11275. doi: 10.1038/ncomms11275.

Melton D. 2014. Chapter 2 ‘Stemness’: Definitions, criteria, and standards. In: Essentials of stem cell biology. 3rd ed. Academic Press. p. 7–17. doi: 10.1016/B978-0-12-409503-8.00002-0.

Oatley J. 2017. Cryopreserving and thawing spermatogonial stem cells. Cold Spring Harbor Protoc 2017. doi: 10.1101/pdb.prot094219.

Residiwati G, Tuska HSA, Budiono, Kawai GKV, Seifi-Jamadi A, Santoro D, Leemans B, Boccart C, Pascottini OB, Opsomer G, Van Soom A. 2020. Practical methods to assess the effects of heat stress on the quality of frozen-thawed Belgian Blue semen in field conditions. Anim Reprod Sci. 221:06572. doi: 10.1016/j.anireprosci.2020.106572.

Sahare M, Otomo A, Komatsu K, Minami N, Yamada M, Imai H. 2015. The role of signaling pathways on proliferation and self-renewal of cultured bovine primitive germ cells. Reprod Med Biol. 14:17–25. doi: 10.1007/s12522-014-0189-x.

Sahare MG, Suyatno, Imai H. 2018. Recent advances of in vitro culture systems for spermatogonial stem cells in mammals. Reprod Med Biol. 17:134-142. doi: 10.1002/rmb2.12087.

Sharma A, Kumaresan A, Mehta P, Nala N, Singh MK, Palta, P, Singla SK, Manik RS, Chauhan MS. 2020. Successful transplantation of transfected enriched buffalo (Bubalus bubalis) spermatogonial stem cells to homologous recipients. Theriogenology. 142:441–449. doi: 10.1016/j.theriogenology.2019.10.019.

Sharma A, Shah SM, Saini N, Mehta P, Kumar BSB, Dua D, Singh MK, Singla SK, Palta P, Manik RS, Chauhan MS. 2019. Optimization of serum-free culture conditions for propagation of putative buffalo (Bubalus bubalis) spermatogonial stem cells. Cell Reprogram. 21:1–10. doi: 10.1089/cell.2018.0018.

Sutermaster BA, Darling EM. 2019. Considerations for high-yield, high-throughput cell enrichment: Fluorescence versus magnetic sorting. Scientific Reports. 9:227. doi: 10.1038/s41598-018-36698-1.

Suyatno, Kitamura Y, Ikeda S, Minami N, Yamada M, Imai H. 2018. Long-term culture of undifferentiated spermatogonia isolated from immature and adult bovine testes. Molec Reprod Develop. 85:236–249. doi: 10.1002/mrd.22958.

Takase HM, Nusse R. 2016. Paracrine Wnt/β-catenin signaling mediates proliferation of undifferentiated spermatogonia in the adult mouse testis. Proceedings of the National Academy of Sciences of the United States of America. 113:E1489-1497. doi: 10.1073/pnas.1601461113.

Valli H, Sukhwani M, Dovey SL, Peters KA, Donohue J, Castro CA, Chu T, Marshall GR, Orwig KE. 2014. Fluorescence- and magnetic-activated cell sorting strategies to isolate and enrich human spermatogonial stem cells. Fertil Steril. 102:566-580. doi: 10.1016/j.fertnstert.2014.04.036.

Wu J, Song W, Zhu H, Niu Z, Mu H, Lei A, Yang C, Peng S, Li X, Li G, Hua J. 2013. Enrichment and characterization of Thy1-positive male germline stem cells (mGSCs) from dairy goat (Capra hircus) testis using magnetic microbeads. Theriogenology. 80:1052–1060. doi: 10.1016/j.theriogenology.2013. 08.003.

Yu X, Riaz H, Dong P, Chong Z, Luo X, Liang A, Yang L. 2014. Identification and IVC of spermatogonial stem cells in prepubertal buffaloes. Theriogenology. 81:1312–1322.doi: 10.1016/j.theriogenology.2014.03. 002.

Zeng W, Tang L, Bondareva A, Honaramooz A, Tanco V, Dores C, Megee S, Modelski M, Rodriguez-Sosa JR, Paczkowski M, Silva E, Wheeler M, Krisher RL, Dobrinski I. 2013. Viral Transduction of male germline stem cells results in transgene transmission after germ cell transplantation in pigs. Biol Reprod. 88:27. doi: 10.1095/biolreprod.112.104422.

Zhang F, Wen Y, Guo X. 2014. CRISPR/Cas9 for genome editing: Progress, implications and challenges. Human Molec Gen. 23:R40–R46. doi: 10.1093/hmg/ ddu125.

Zhang P, Chen X, Zheng Y, Zhu J, Qin Y, Lv Y, Zeng W. 2017. Long-term propagation of porcine undifferentiated spermatogonia. Stem Cells Develop. 26:1121–1131. doi: 10.1089/scd.2017.0018.

Zheng Y, Zhang Y, Qu R, He Y, Tian X, Zeng W. 2014. Spermatogonial stem cells from domestic animals: Progress and prospects. Reprod. 147:R65–R74. doi: 10.1530/REP-13-0466.

Refbacks

  • There are currently no refbacks.

Copyright (c)  2021 WARTAZOA. Indonesian Bulletin of Animal and Veterinary Sciences

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

View My Stats