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| Establishment and characterization of immortalized bovine male germline stem cell line |
| LEI Qi-jing1, PAN Qin1, MA Ju-hong1, ZHOU Zhe1, LI Guang-peng2, CHEN Shu-lin1, HUA Jin-lian1 |
1 College of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering and Technology, Northwest A&F University, Yangling 712100, P.R.China
2 Key Laboratory for Mammalian Reproductive Biology and Biotechnology, Ministry of Education/Inner Mongolia University, Hohhot 010021, P.R.China |
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Abstract Male germline stem cells (mGSCs) are unique adult germ cells with self-renewal potential and spermatogenesis function in the testis. However, further studies are needed to establish a long-term cultural system of mGSCs in vitro, especially for large animals such as bovine mGSCs. In this study, we first established a stable immortalized bovine male germline stem cell line by transducing Simian virus 40 (SV40) large T antigen. The proliferation of these cells was improved significantly. These cells could express spermatogonial stem cell (SSC)-specific markers, such as PLZF, PGP9.5, VASA, LIN28A, and CD49F, both in the mRNA and protein levels. Additionally, these cells could be differentiated into three germ layer cells to enter meiosis, form colonies, and proliferate in the seminiferous tubules of busulfan-induced infertile mice. The immortalized bovine mGSCs maintain the criteria of mGSCs.
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Received: 22 February 2017
Accepted:
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| Fund: This work was supported by the National Major Project for Production of Transgenic Breeding of China (2014ZX08007-002), the National Basic Research Program of China (2016YFA0100203) and the Program of National Natural Science Foundation of China (31572399, 31272518). |
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Corresponding Authors:
Correspondence Hua Jin-lian, E-mail: jinlianhua@nwsuaf.edu.cn; Chen Shu-lin, E-mail: csl_1359@163.com; Li Guang-peng, Tel/Fax: +86-471-4992495, E-mail: gpengli@immu.edu.cn
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| About author: Lei Qi-jing, E-mail: qijinglei@nwafu.edu.cn |
Cite this article:
LEI Qi-jing, PAN Qin, MA Ju-hong, ZHOU Zhe, LI Guang-peng, CHEN Shu-lin, HUA Jin-lian.
2017.
Establishment and characterization of immortalized bovine male germline stem cell line. Journal of Integrative Agriculture, 16(11): 2547-2557.
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| Amann R P. 1986. Detection of alterations in testicular and epididymal function in laboratory animals. Environmental Health Perspectives, 70, 149–158.Aponte P M, Soda T, Kant H J G V D, Rooij D G D. 2006. Basic features of bovine spermatogonial culture and effects of glial cell line-derived neurotrophic factor. Theriogenology, 65, 1828–1847.Auvergne R, Sim F, Su W, Chandler-Militello D, Burch J, Alfanek Y, Davis D, Benraiss A, Walter K, Achanta P. 2013. Transcriptional differences between normal and glioma-derived glial progenitor cells identify a core set of dysregulated genes. Cell Reports, 3, 2127–2141.Brinster R L, Avarbock M R. 1994. Germline transmission of donor haplotype following spermatogonial transplantation. Proceedings of the National Academy of Sciences of the United States of America, 91, 11303–11307.Brinster R L, Zimmermann J W. 1994. Spermatogenesis following male germ-cell transplantation. Proceedings of the National Academy of Sciences of the United States of America, 91, 11298–11302.Busada J T, Geyer C B. 2015. The role of retinoic acid (RA) in spermatogonial differentiation. Biology of Reproduction, 94, doi: 10.1095/biolreprod.115.135145Cai H, Tang B, Wu J Y, Zhao X X, Wang Z Z, An X L, Lai L X, Li Z Y, Zhang X M. 2016. Enrichment and in vitro features of the putative gonocytes from cryopreserved testicular tissue of neonatal bulls. Andrology, 4, 1150–1158.Chen Z, Sun M, Yuan Q, Niu M, Yao C, Hou J, Wang H, Wen L, Liu Y, Li Z. 2016. Generation of functional hepatocytes from human spermatogonial stem cells. Oncotarget, 13, 8879–8895.Dym M. 1994. Spermatogonial stem cells of the testis. Proceedings of the National Academy of Sciences of the United States of America, 91, 11287–11289.Feng L X, Chen Y, Dettin L, Pera R A, Herr J C, Goldberg E, Dym M. 2002. Generation and in vitro differentiation of a spermatogonial cell line. Science, 297, 392–395.García-Escudero V, García-Gómez A, Gargini R, Martín-Bermejo M J, Langa E, de Yébenes J G, Delicado A, Avila J, Moreno-Flores M T, Lim F. 2010. Prevention of senescence progression in reversibly immortalized human ensheathing glia permits their survival after deimmortalization. Molecular Therapy, 18, 394–403.Hansen K D, Sabunciyan S, Langmead B, Noemi Nagy N, Curley R, Klein G, Klein E, Daniel Salamon D, Andrew P, Feinberg A P. 2013. Large-scale hypomethylated blocks associated with Epstein-Barr virus-induced B-cell immortalization. Genome Research, 24, 177–184.Hao L Y, Armanios M, Strong M A, Karim B, Feldser D M, Huso D, Greider C W. 2006. Short telomeres, even in the presence of telomerase, limit tissue renewal capacity. Cell, 123, 1121–1131.Hofmann M C, Braydich-Stolle L, Dettin L, Johnson E, Dym M. 2005. Immortalization of mouse germ line stem cells. Stem Cells, 23, 200–210.Hou J, Niu M, Liu L, Zhu Z, Wang X, Sun M, Yuan Q, Yang S, Zeng W, Liu Y. 2015. Establishment and characterization of human germline stem cell line with unlimited proliferation potentials and no tumor formation. Scientific Reports, 5, 237–240.Kanatsushinohara M, Morimoto H, Shinohara T. 2015. Enrichment of mouse spermatogonial stem cells by a stem cell dye CDy1. Biology of Reproduction, 94, doi: 10.1095/biolreprod.115.135707Kang N Y, Yun S W, Ha H H, Park S J, Chang Y T. 2011. Embryonic and induced pluripotent stem cell staining and sorting with the live-cell fluorescence imaging probe CDy1. Nature Protocols, 6, 1044–1052.Kohli M, Jorgensen T J. 1999. The influence of SV40 immortalization of human fibroblasts on p53-dependent radiation responses. Biochemical & Biophysical Research Communications, 257, 168–176.Kubota H, Avarbock M R, Brinster R L. 2003. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 6487–6492.Laronda M M, Jameson J L. 2009. Induction of sox3 upon differentiation of primary spermatogonia by retinoic acid in vitro. Biology of Reproduction, 80, 202.Li B, Zhuang M, Wu C, Niu B, Zhang Z, Li X, Wei Z, Li G, Hua J. 2016. Bovine male germline stem-like cells cultured in serum- and feeder-free medium. Cytotechnology, 68, 2145–2157.Li N, Mu H, Zheng L, Li B, Wu C, Niu B, Shen Q, He X, Hua J. 2016. EIF2S3Y suppresses the pluripotency state and promotes the proliferation of mouse embryonic stem cells. Oncotarget, 7, 11321–11331.Ludlow J W. 1993. Interactions between SV40 large-tumor antigen and the growth suppressor proteins pRB and p53. The FASEB Journal Official Publication of the Federation of American Societies for Experimental Biology, 7, 866–871.Mahla R S, Reddy N, Goel S. 2012. Spermatogonial stem cells (SSCs) in buffalo (Bubalus bubalis) testis. PLoS ONE, 7, 292–293.Miao X Y. 2011. Production of transgenic animals using spermatogonial stem cells. Journal of Integrative Agriculture, 10, 762–768.Nakao Y, Yang X, Yokoyama M, Ferenczy A, Tang S C, Pater M M, Pater A. 1997. Induction of p16 during immortalization by HPV 16 and 18 and not during malignant transformation. British Journal of Cancer, 75, 1410–1416.Oatley J M, Brinster R L. 2003. Regulation of spermatogonial stem cell self-renewal in mammals. Annual Review of Cell & Developmental Biology, 24, 263.Oatley J M, Reeves J J, Mclean D J. 2004. Biological activity of cryopreserved bovine spermatogonial stem cells during in vitro culture. Biology of Reproduction, 71, 942–947.Oatley M J, Kaucher A V, Yang Q E, Waqas M S, Oatley J M. 2016. Conditions for long-term culture of cattle undifferentiated spermatogonia. Biology of Reproduction, 95, doi: 10.1095/biolreprod.116.139832Pech M F, Garbuzov A, Hasegawa K, Sukhwani M, Zhang R J, Benayoun B A, Brockman S A, Lin S, Brunet A, Orwig K E. 2015. High telomerase is a hallmark of undifferentiated spermatogonia and is required for maintenance of male germline stem cells. Genes & Development, 29, 2420–2434.Reding S C, Stepnoski A L, Cloninger E W, Oatley J M. 2010. THY1 is a conserved marker of undifferentiated spermatogonia in the pre-pubertal bull testis. Reproduction, 139, 893–903.Rooij D G D, Grootegoed J A. 1998. Spermatogonial stem cells. Annual Review of Biomedical Sciences, 10, 105–114.Sahare M, Kim S M, Otomo A, Komatsu K, Minami N, Yamada M, Imai H. 2015. Factors supporting long-term culture of bovine male germ cells. Reproduction Fertility & Development, 28, 2039–2050.Schrans-Stassen B H G J, Van de Kant H J G, de Rooij D G, van Pelt A M M. 1999. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology, 140, 5894–5900.Snyder E M, Small C, Griswold M D. 2010. Retinoic acid availability drives the asynchronous initiation of spermatogonial differentiation in the mouse. Biology of Reproduction, 83, 783–790.Wang H, Wen L, Yuan Q, Sun M, Niu M, He Z. 2016. Establishment and applications of male germ cell and Sertoli cell lines. Reproduction, 152, R31–R40.Wang S, Wang X, Ma L, Lin X, Zhang D, Li Z, Wu Y, Zheng C, Feng X, Liao S. 2016. Retinoic acid is sufficient for the in vitro induction of mouse spermatocytes. Stem Cell Reports, 7, 80–94.Wu J, Liao M, Zhu H, Kang K, Mu H, Song W, Niu Z, He X, Bai C, Li G. 2014. CD49f-positive testicular cells in Saanen dairy goat were identified as spermatogonia-like cells by miRNA profiling analysis. Journal of Cellular Biochemistry, 115, 1712–1723.Yin Z, Wang Q, Li Y, Wei H, Shi J, Li A. 2016. A novel method for banking stem cells from human exfoliated deciduous teeth: Lentiviral TERT immortalization and phenotypical analysis. Stem Cell Research & Therapy, 7, 1–11.Zhang S, Sun J, Pan S, Zhu H, Wang L, Hu Y, Wang J, Wang F, Cao H, Yan X. 2011. Retinol (vitamin A) maintains self-renewal of pluripotent male germline stem cells (mGSCs) from adult mouse testis. Journal of Cellular Biochemistry, 112, 1009–1021.Zhang Z, Gong Y, Ying G, Hai Y, Hao Y, Shi Y, Yang L, Meng M, Liu L, Zheng L. 2013. Direct transdifferentiation of spermatogonial stem cells to morphological, phenotypic and functional hepatocyte-like cells via the ERK1/2 and Smad2/3 signaling pathways and the inactivation of cyclin A, cyclin B and cyclin E. Cell Communication & Signaling, 11, 4586–4592.Zheng L, Zhu H, Mu H, Wu J, Song W, Zhai Y, Peng S, Li G, Hua J. 2016. CD49f promotes proliferation of male dairy goat germline stem cells. Cell Proliferation, 49, 27–35.Zhu H, Liu C, Sun J, Li M, Hua J. 2012. Effect of GSK-3 inhibitor on the proliferation of multipotent male germ line stem cells (mGSCs) derived from goat testis. Theriogenology, 77, 1939–1950.Zhu H, Ma J, Du R, Zheng L, Wu J, Song W, Niu Z, He X, Du E, Zhao S, Hua J. 2014. Characterization of immortalized dairy goat male germline stem cells (mGSCs). Journal of Cellular Biochemistry, 115, 1549–1560. |
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