Progress in in vitro culture and gene editing of porcine spermatogonial stem cells

Yi-Zhuo Sun; Si-Tong Liu; Xiao-Meng Li; Kang Zou

doi:10.24272/j.issn.2095-8137.2019.051

Volume 40 Issue 5

Sep. 2019

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Article Navigation > Zoological Research > 2019 > 40(5): 343-348

Yi-Zhuo Sun, Si-Tong Liu, Xiao-Meng Li, Kang Zou. Progress in in vitro culture and gene editing of porcine spermatogonial stem cells. Zoological Research, 2019, 40(5): 343-348. doi: 10.24272/j.issn.2095-8137.2019.051

Citation:

Yi-Zhuo Sun, Si-Tong Liu, Xiao-Meng Li, Kang Zou. Progress in in vitro culture and gene editing of porcine spermatogonial stem cells. Zoological Research, 2019, 40(5): 343-348. doi: 10.24272/j.issn.2095-8137.2019.051

Progress in in vitro culture and gene editing of porcine spermatogonial stem cells

doi: 10.24272/j.issn.2095-8137.2019.051

1.
Germline Stem Cells and Microenvironment Lab, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Jiangsu 210095, China
2.
College of Life Sciences, Jilin University, Changchun Jilin 130012, China
3.
Key Laboratory of Molecular Epigenetics of MOE, Institute of Genetics and Cytology, Northeast Normal University, Changchun Jilin 130024, China

Funds: the Fundamental Research Funds for the Central Universities in China(KYDS201807);China(2016YFE0128500)

More Information

Corresponding author: Xiao-Meng Li,Kang Zou
Received Date: 2019-05-09
Publish Date: 2019-09-18

Abstract

Research on in vitro culture and gene editing of domestic spermatogonial stem cells (SSCs) is of considerable interest but remains a challenging issue in animal science. In recent years, some progress on the isolation, purification, and genetic manipulation of porcine SSCs has been reported. Here, we summarize the characteristics of porcine SSCs as well current advances in their in vitro culture, potential usage, and genetic manipulation. Furthermore, we discuss the current application of gene editing in pig cloning technology. Collectively, this commentary aims to summarize the progress made and obstacles encountered in porcine SSC research to better serve animal husbandry, improve livestock fecundity, and enhance potential clinical use.

References

[1]

null	Abbasi H , Tahmoorespur M , Hosseini SM , Nasiri Z , Bahadorani M , Hajian M , Nasiri MR , Nasr-Esfahani MH . 2013. THY1 as a reliable marker for enrichment of undifferentiated spermatogonia in the goat. Theriogenology, 80(8): 923–932.
null	Belluzzi A . 2004. Polyunsaturated fatty acids (n-3 PUFAs) and inflammatory bowel disease (IBD): pathogenesis and treatment. European Review for Medical and Pharmacological Sciences, 8(5): 225–229.
null	Bellvé AR , Cavicchia JC , Millette CF , O'brien DA , Bhatnagar YM , Dym M . 1977. Spermatogenic cells of the prepuberal mouse: Isolation and morphological characterization. Journal of Cell Biology, 74(1): 68–85.
null	Borjigin U , Davey R , Hutton K , Herrid M . 2010. Expression of promyelocytic leukaemia zinc-finger in ovine testis and its application in evaluating the enrichment efficiency of differential plating. Reproduction, Fertility and Development, 22(5): 733–742.
null	Brinster RL , Avarbock MR . 1994. Germline transmission of donor haplotype following spermatogonial transplantation. Proceedings of the National Academy of Sciences of the United States of America, 91(24): 11303–11307.
null	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(24): 11298–11302.
null	Buageaw A , Sukhwani M , Ben-Yehudah A , Ehmcke J , Rawe VY , Pholpramool C , Orwig KE, Schlatt S . 2005. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biology of Reproduction, 73(5): 1011–1016.
null	Chiarini-Garcia H , Raymer AM , Russell LD . 2003. Non-random distribution of spermatogonia in rats: evidence of niches in the seminiferous tubules. Reproduction, 126(5): 669–680.
null	Costa GMJ , Avelar GF , Rezende-Neto JV , Campos-Junior PHA , SMSN Lacerda , Andrade BSC , Thomé RG , M-C Hofmann , Franca LR . 2012. Spermatogonial stem cell markers and niche in equids. PLoS One, 7(8): e44091.
null	de Rooij DG . 1998. Stem cells in the testis. International Journal of Experimental Pathology, 79(2): 67–80.
null	de Rooij DG , Russell LD . 2000. All you wanted to know about spermatogonia but were afraid to ask. Journal of Andrology, 21(6): 776–798.
null	de Rooij DG , van Beek MEAB . 2013. Computer simulation of the rodent spermatogonial stem cell niche. Biology of Reproduction, 88(5): 131.
null	Dym M . 1994. Spermatogonial stem cells of the testis. Proceedings of the National Academy of Sciences of the United States of America, 91(24): 11287–11289.
null	Encinas G , Zogbi C , Stumpp T . 2012. Detection of four germ cell markers in rats during testis morphogenesis: Differences and similarities with mice. Cells Tissues Organs, 195(5): 443–455.
null	Ferranti F , Muciaccia B , Ricci G , Dovere L , Canipari R , Magliocca F , Stefanini M , Catizone A , Vicini E . 2012. Glial cell line-derived neurotrophic factor promotes invasive behaviour in testicular seminoma cells. International Journal of Andrology, 35(5): 758–768.
null	Gonen S , Jenko J , Gorjanc G , Mileham AJ , Whitelaw CBA , Hickey JM . 2017. Potential of gene drives with genome editing to increase genetic gain in livestock breeding programs. Genetics Selection Evolution, 49(1): 3.
null	Gori JL , Hsu PD , Maeder ML , Shen S , Welstead GG , Bumcrot D . 2015. Delivery and specificity of CRISPR-Cas9 genome editing technologies for human gene therapy. Human Gene Therapy, 26(7): 443.
null	Hampton T . 2017. Gene editing could help pave the way for pig-to-human transplantations. Circulation, 136(21): 2083–2084.
null	Hofmann MC . 2008. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Molecular and Cellular Endocrinology, 288(1–2): 95–103.
null	Huckins C , Clermont Y . 1968. Evolution of gonocytes in the rat testis during late embryonic and early post-natal life. Archives D'anatomie, D'histologie et D'embryologie Normales et Experimentales, 51(1): 341–354.
null	Hwang WY , Fu Y , Reyon D , Maeder ML , Tsai SQ , Sander JD , Peterson RT , Yeh JR , Joung JK . 2013. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nature Biotechnology, 31(3): 227–229.
null	Kim MS , Park MH , Park JE , Yun JI , Choi JH , Lee E , Lee ST . 2019. Establishment of an electroporation-mediated gene delivery system in porcine spermatogonial stem cells. In Vitro Cellular & Developmental Biology - Animal, 55(3): 177–188.
null	Kubota H , Brinster RL . 2006. Technology Insight: in vitro culture of spermatogonial stem cells and their potential therapeutic uses. Nature Clinical Practice Endocrinology & Metabolism, 2(2): 99–108.
null	Kubota H , Avarbock MR , Brinster RL . 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(11): 6487–6492.
null	Kubota H , Wu X , Goodyear SM , Avarbock MR , Brinster RL . 2011. Glial cell line-derived neurotrophic factor and endothelial cells promote self-renewal of rabbit germ cells with spermatogonial stem cell properties. The FASEB Journal, 25(8): 2604–2614.
null	Kuijk EW , Colenbrander B , Roelen BAJ . 2009. The effects of growth factors on in vitro-cultured porcine testicular cells. Reproduction, 138(4): 721–731.
null	Lee YA , Kim YH , Ha SJ , Kim KJ , Kim BJ , Kim BG , Choi SH , Kim IC , Schmidt JA , Ryu BY . 2014. Cryopreservation of porcine spermatogonial stem cells by slow-freezing testis tissue in trehalose. Journal of Animal Science, 92(3): 984–995.
null	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 . 2017. Long-term propagation of tree shrew spermatogonial stem cells in culture and successful generation of transgenic offspring. Cell Research, 27(2): 241.
null	Li H , Wang G , Hao Z , Zhang G , Qing Y , Liu S , Qing L , Pan W , Chen L , Liu G , Zhao P , Jia B , Zeng L , Guo J , Zhao L , Zhao H , Lv C , Xu K , Cheng W , Li H , Zhao H , Wang W , Wei H . 2016. Generation of biallelic knock-out sheep via gene-editing and somatic cell nuclear transfer. Scientific Reports, 6: 33675.
null	Lin Z , Bao J , Kong Q , Bai Y , Luo F , Zhou S , Wu Y , Huang J . 2017. Effective production of recipient male pigs for spermatogonial stem cell transplantation by intratesticular injection with busulfan. Theriogenology, 89: 365–373.e2.
null	Liu TT , Zhang P , Li TJ , Chen XX , Zhu ZS , Lyu YH , Li XL , Tian X , Zeng WX . 2017. SETDB1 plays an essential role in maintenance of gonocyte survival in pigs. Reproduction, 154(1): 23–34.
null	Luo J , Song Z , Yu S , Cui D , Wang B , Ding F , Li S , Dai Y , Li N . 2014. Efficient generation of myostatin (MSTN) biallelic mutations in cattle using zinc finger nucleases. PLoS One, 9(4): e95225.
null	Ma X , Wong SY , Tam HY , Tsui YK , Chung LS , Feng B . 2018. In vivo genome editing thrives with diversified CRISPR technologies. Zoological Research, 39(2): 58–71.
null	Meachem S , Sch?nfeldt VV , Schlatt S . 2001. Spermatogonia: stem cells with a great perspective. Reproduction, 121(6): 825–834.
null	Meng X , Lindahl M , Hyv?nen ME , Parvinen M , de Rooij DG , Hess MW , Raatikainen-Ahokas A , Sainio K , Rauvala H , Lakso M , Pichel JG , Westphal H , Saarma M , Sariola H . 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science, 287(5457): 1489–1493.
null	Nagano M , Avarbock MR , Leonida EB , Brinster CJ , Brinster RL . 1998. Culture of mouse spermatogonial stem cells. Tissue and Cell, 30(4): 389–397.
null	Park HJ , Lee R , Lee WY , Kim JH , Do JT , Park C , Song H . 2017a. Stage-specific expression of Sal-like protein 4 in boar testicular germ cells. Theriogenology, 101: 44–52.
null	Park JE , Park MH , Kim MS , Park YR , Yun JI , Cheong HT , Kim M , Choi JH , Lee E , Lee ST . 2017b. Porcine spermatogonial stem cells self-renew effectively in a three dimensional culture microenvironment. Cell Biology International, 41(12): 1316–1324.
null	Park K , Kim MS , Kang M , Kang T , Kim B , Lee ST . 2019. Successful genetic modification of porcine spermatogonial stem cells via an electrically responsive Au nanowire injector. Biomaterials, 193: 22–29.
null	Park KE, Kaucher AV , Powell A , Waqas MS , Sandmaier SE , Oatley MJ , Park CH , Tibary A , Donovan DM , Blomberg LA , Lillico SG , Bruce C , Whitelaw A , Mileham A , Telugu BP , Oatley JM . 2017c. Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Scientific Reports, 7: 40176.
null	Polejaeva IA , Chen SH , Vaught TD , Page RL , Mullins J , Ball S , Dai Y , Boone J , Walker S , Ayares DL , Colman A , Campbell KHS . 2000. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature, 407(6800): 86–90.
null	Proudfoot C , Carlson DF , Huddart R , Long CR , Pryor JH , King TJ , Lillico SG , Mileham AJ , Mclaren DG , Whitelaw CBA , Fahrenkrug SC . 2015. Genome edited sheep and cattle. Transgenic Research, 24(1): 147–153.
null	Ran L , Lee WY , Park HJ , Ha WT , Woo JS , Chung HJ , Lee JH , Hong K , Song H . 2018. Stage-specific expression of DDX4 and C-kit at different developmental stages of the porcine testis. Animal Reproduction Science, 190: 18–26.
null	Reding SC , Stepnoski AL , Cloninger EW , Oatley JM . 2010. THY1 is a conserved marker of undifferentiated spermatogonia in the pre-pubertal bull testis. Reproduction, 139(5): 893–903.
null	Sapsford CS . 1962. Changes in the cells of the Sex Cords and Seminiferous Tubules during the development of the Testis of the rat and mouse. Australian Journal of Zoology, 10(2): 178–192.
null	Schlatt S . 2002. Spermatogonial stem cell preservation and transplantation. Molecular and Cellular Endocrinology, 187(1–2): 107–111.
null	Shinohara T , Avarbock MR , Brinster RL . 1999. β1- and α6-integrin are surface markers on mouse spermatogonial stem cells. Proceedings of the National Academy of Sciences of the United States of America, 96(10): 5504–5509.
null	Shinohara T , Avarbock MR , Brinster RL . 2000a. Functional analysis of spermatogonial stem cells in steel and cryptorchid infertile mouse models. Developmental Biology, 220(2): 401–411.
null	Shinohara T , Orwig KE, Avarbock MR , Brinster RL . 2000b. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proceedings of the National Academy of Sciences of the United States of America, 97(15): 8346–8351.
null	Sun F , Xu Q , Zhao D , Chen CD . 2015. Id4 marks spermatogonial stem cells in the mouse testis. Scientific Reports, 5: 17594.
null	Takagi S , Itoh N , Kimura M , Sasao T , Tsukamoto T . 2001. Spermatogonial proliferation and apoptosis in hypospermatogenesis associated with nonobstructive azoospermia. Fertility and Sterility, 76(5): 901–907.
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null	Zhang P , Qin Y , Zheng Y , Zeng W . 2017a. Phospholipase D family member 6 (PLD6) is a surface marker for enrichment of undifferentiated spermatogonia in the pre-pubertal boars. Stem Cells and Development, 27(1)： 55–64.
null	Zhang P , Chen X , Zheng Y , Zhu J , Qin Y , Lv Y , Zeng W . 2017b. Long-term propagation of porcine undifferentiated spermatogonia. Stem Cells and Development, 26(15): 1121–1131.
null	Zhao H , Nie J , Zhu X , Lu Y , Liang X , Xu H , Yang X , Zhang Y , Lu K , Lu S . 2018. In vitro differentiation of spermatogonial stem cells using testicular cells from Guangxi Bama mini-pig. Journal of Veterinary Science, 19(5): 592–599.
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沈阳化工大学材料科学与工程学院沈阳 110142

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Progress in in vitro culture and gene editing of porcine spermatogonial stem cells

1. Germline Stem Cells and Microenvironment Lab, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing Jiangsu 210095, China

2. College of Life Sciences, Jilin University, Changchun Jilin 130012, China

3. Key Laboratory of Molecular Epigenetics of MOE, Institute of Genetics and Cytology, Northeast Normal University, Changchun Jilin 130024, China

Funds: the Fundamental Research Funds for the Central Universities in China(KYDS201807);China(2016YFE0128500)

Corresponding author: Xiao-Meng Li,Kang Zou

Received Date: 2019-05-09

Publish Date: 2019-09-18

Abstract: Research on in vitro culture and gene editing of domestic spermatogonial stem cells (SSCs) is of considerable interest but remains a challenging issue in animal science. In recent years, some progress on the isolation, purification, and genetic manipulation of porcine SSCs has been reported. Here, we summarize the characteristics of porcine SSCs as well current advances in their in vitro culture, potential usage, and genetic manipulation. Furthermore, we discuss the current application of gene editing in pig cloning technology. Collectively, this commentary aims to summarize the progress made and obstacles encountered in porcine SSC research to better serve animal husbandry, improve livestock fecundity, and enhance potential clinical use.

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Reference (1)

[1]

null	Abbasi H , Tahmoorespur M , Hosseini SM , Nasiri Z , Bahadorani M , Hajian M , Nasiri MR , Nasr-Esfahani MH . 2013. THY1 as a reliable marker for enrichment of undifferentiated spermatogonia in the goat. Theriogenology, 80(8): 923–932.
null	Belluzzi A . 2004. Polyunsaturated fatty acids (n-3 PUFAs) and inflammatory bowel disease (IBD): pathogenesis and treatment. European Review for Medical and Pharmacological Sciences, 8(5): 225–229.
null	Bellvé AR , Cavicchia JC , Millette CF , O'brien DA , Bhatnagar YM , Dym M . 1977. Spermatogenic cells of the prepuberal mouse: Isolation and morphological characterization. Journal of Cell Biology, 74(1): 68–85.
null	Borjigin U , Davey R , Hutton K , Herrid M . 2010. Expression of promyelocytic leukaemia zinc-finger in ovine testis and its application in evaluating the enrichment efficiency of differential plating. Reproduction, Fertility and Development, 22(5): 733–742.
null	Brinster RL , Avarbock MR . 1994. Germline transmission of donor haplotype following spermatogonial transplantation. Proceedings of the National Academy of Sciences of the United States of America, 91(24): 11303–11307.
null	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(24): 11298–11302.
null	Buageaw A , Sukhwani M , Ben-Yehudah A , Ehmcke J , Rawe VY , Pholpramool C , Orwig KE, Schlatt S . 2005. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biology of Reproduction, 73(5): 1011–1016.
null	Chiarini-Garcia H , Raymer AM , Russell LD . 2003. Non-random distribution of spermatogonia in rats: evidence of niches in the seminiferous tubules. Reproduction, 126(5): 669–680.
null	Costa GMJ , Avelar GF , Rezende-Neto JV , Campos-Junior PHA , SMSN Lacerda , Andrade BSC , Thomé RG , M-C Hofmann , Franca LR . 2012. Spermatogonial stem cell markers and niche in equids. PLoS One, 7(8): e44091.
null	de Rooij DG . 1998. Stem cells in the testis. International Journal of Experimental Pathology, 79(2): 67–80.
null	de Rooij DG , Russell LD . 2000. All you wanted to know about spermatogonia but were afraid to ask. Journal of Andrology, 21(6): 776–798.
null	de Rooij DG , van Beek MEAB . 2013. Computer simulation of the rodent spermatogonial stem cell niche. Biology of Reproduction, 88(5): 131.
null	Dym M . 1994. Spermatogonial stem cells of the testis. Proceedings of the National Academy of Sciences of the United States of America, 91(24): 11287–11289.
null	Encinas G , Zogbi C , Stumpp T . 2012. Detection of four germ cell markers in rats during testis morphogenesis: Differences and similarities with mice. Cells Tissues Organs, 195(5): 443–455.
null	Ferranti F , Muciaccia B , Ricci G , Dovere L , Canipari R , Magliocca F , Stefanini M , Catizone A , Vicini E . 2012. Glial cell line-derived neurotrophic factor promotes invasive behaviour in testicular seminoma cells. International Journal of Andrology, 35(5): 758–768.
null	Gonen S , Jenko J , Gorjanc G , Mileham AJ , Whitelaw CBA , Hickey JM . 2017. Potential of gene drives with genome editing to increase genetic gain in livestock breeding programs. Genetics Selection Evolution, 49(1): 3.
null	Gori JL , Hsu PD , Maeder ML , Shen S , Welstead GG , Bumcrot D . 2015. Delivery and specificity of CRISPR-Cas9 genome editing technologies for human gene therapy. Human Gene Therapy, 26(7): 443.
null	Hampton T . 2017. Gene editing could help pave the way for pig-to-human transplantations. Circulation, 136(21): 2083–2084.
null	Hofmann MC . 2008. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Molecular and Cellular Endocrinology, 288(1–2): 95–103.
null	Huckins C , Clermont Y . 1968. Evolution of gonocytes in the rat testis during late embryonic and early post-natal life. Archives D'anatomie, D'histologie et D'embryologie Normales et Experimentales, 51(1): 341–354.
null	Hwang WY , Fu Y , Reyon D , Maeder ML , Tsai SQ , Sander JD , Peterson RT , Yeh JR , Joung JK . 2013. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nature Biotechnology, 31(3): 227–229.
null	Kim MS , Park MH , Park JE , Yun JI , Choi JH , Lee E , Lee ST . 2019. Establishment of an electroporation-mediated gene delivery system in porcine spermatogonial stem cells. In Vitro Cellular & Developmental Biology - Animal, 55(3): 177–188.
null	Kubota H , Brinster RL . 2006. Technology Insight: in vitro culture of spermatogonial stem cells and their potential therapeutic uses. Nature Clinical Practice Endocrinology & Metabolism, 2(2): 99–108.
null	Kubota H , Avarbock MR , Brinster RL . 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(11): 6487–6492.
null	Kubota H , Wu X , Goodyear SM , Avarbock MR , Brinster RL . 2011. Glial cell line-derived neurotrophic factor and endothelial cells promote self-renewal of rabbit germ cells with spermatogonial stem cell properties. The FASEB Journal, 25(8): 2604–2614.
null	Kuijk EW , Colenbrander B , Roelen BAJ . 2009. The effects of growth factors on in vitro-cultured porcine testicular cells. Reproduction, 138(4): 721–731.
null	Lee YA , Kim YH , Ha SJ , Kim KJ , Kim BJ , Kim BG , Choi SH , Kim IC , Schmidt JA , Ryu BY . 2014. Cryopreservation of porcine spermatogonial stem cells by slow-freezing testis tissue in trehalose. Journal of Animal Science, 92(3): 984–995.
null	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 . 2017. Long-term propagation of tree shrew spermatogonial stem cells in culture and successful generation of transgenic offspring. Cell Research, 27(2): 241.
null	Li H , Wang G , Hao Z , Zhang G , Qing Y , Liu S , Qing L , Pan W , Chen L , Liu G , Zhao P , Jia B , Zeng L , Guo J , Zhao L , Zhao H , Lv C , Xu K , Cheng W , Li H , Zhao H , Wang W , Wei H . 2016. Generation of biallelic knock-out sheep via gene-editing and somatic cell nuclear transfer. Scientific Reports, 6: 33675.
null	Lin Z , Bao J , Kong Q , Bai Y , Luo F , Zhou S , Wu Y , Huang J . 2017. Effective production of recipient male pigs for spermatogonial stem cell transplantation by intratesticular injection with busulfan. Theriogenology, 89: 365–373.e2.
null	Liu TT , Zhang P , Li TJ , Chen XX , Zhu ZS , Lyu YH , Li XL , Tian X , Zeng WX . 2017. SETDB1 plays an essential role in maintenance of gonocyte survival in pigs. Reproduction, 154(1): 23–34.
null	Luo J , Song Z , Yu S , Cui D , Wang B , Ding F , Li S , Dai Y , Li N . 2014. Efficient generation of myostatin (MSTN) biallelic mutations in cattle using zinc finger nucleases. PLoS One, 9(4): e95225.
null	Ma X , Wong SY , Tam HY , Tsui YK , Chung LS , Feng B . 2018. In vivo genome editing thrives with diversified CRISPR technologies. Zoological Research, 39(2): 58–71.
null	Meachem S , Sch?nfeldt VV , Schlatt S . 2001. Spermatogonia: stem cells with a great perspective. Reproduction, 121(6): 825–834.
null	Meng X , Lindahl M , Hyv?nen ME , Parvinen M , de Rooij DG , Hess MW , Raatikainen-Ahokas A , Sainio K , Rauvala H , Lakso M , Pichel JG , Westphal H , Saarma M , Sariola H . 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science, 287(5457): 1489–1493.
null	Nagano M , Avarbock MR , Leonida EB , Brinster CJ , Brinster RL . 1998. Culture of mouse spermatogonial stem cells. Tissue and Cell, 30(4): 389–397.
null	Park HJ , Lee R , Lee WY , Kim JH , Do JT , Park C , Song H . 2017a. Stage-specific expression of Sal-like protein 4 in boar testicular germ cells. Theriogenology, 101: 44–52.
null	Park JE , Park MH , Kim MS , Park YR , Yun JI , Cheong HT , Kim M , Choi JH , Lee E , Lee ST . 2017b. Porcine spermatogonial stem cells self-renew effectively in a three dimensional culture microenvironment. Cell Biology International, 41(12): 1316–1324.
null	Park K , Kim MS , Kang M , Kang T , Kim B , Lee ST . 2019. Successful genetic modification of porcine spermatogonial stem cells via an electrically responsive Au nanowire injector. Biomaterials, 193: 22–29.
null	Park KE, Kaucher AV , Powell A , Waqas MS , Sandmaier SE , Oatley MJ , Park CH , Tibary A , Donovan DM , Blomberg LA , Lillico SG , Bruce C , Whitelaw A , Mileham A , Telugu BP , Oatley JM . 2017c. Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Scientific Reports, 7: 40176.
null	Polejaeva IA , Chen SH , Vaught TD , Page RL , Mullins J , Ball S , Dai Y , Boone J , Walker S , Ayares DL , Colman A , Campbell KHS . 2000. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature, 407(6800): 86–90.
null	Proudfoot C , Carlson DF , Huddart R , Long CR , Pryor JH , King TJ , Lillico SG , Mileham AJ , Mclaren DG , Whitelaw CBA , Fahrenkrug SC . 2015. Genome edited sheep and cattle. Transgenic Research, 24(1): 147–153.
null	Ran L , Lee WY , Park HJ , Ha WT , Woo JS , Chung HJ , Lee JH , Hong K , Song H . 2018. Stage-specific expression of DDX4 and C-kit at different developmental stages of the porcine testis. Animal Reproduction Science, 190: 18–26.
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Progress in in vitro culture and gene editing of porcine spermatogonial stem cells

doi: 10.24272/j.issn.2095-8137.2019.051

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通讯作者: 陈斌, bchen63@163.com

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