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Research Progress of in the Inducers Stimulating in Differentiation of iPS Cells into Male Germ Cells |
Xin LI1,Zhong-li ZHAO1,Xiao-tong LUO2,Yang CAO1,Li-chun ZHANG1,Yong-sheng YU1**(),Hai-guo JIN1**() |
1 Branch of Animal Husbandry, Jilin Academy of Agricultural Sciences, Gongzhuling 136100,China 2 Agricultural College, Yan Bian University, Yanji 133002, China |
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Abstract Induced pluripotent stem cells(iPSCs) refer to stem cells that are artificially produced by cellular reprogramming, which have similar functions to embryonic stem cells. They can differentiate into all cell types, and avoid the ethical controversy of ESCs and immune rejection after transplantation. They have a broad application prospect.The advances in the in vitro differentiation of male germ cells using iPSCs by different inducers was reviewed, the effect was also investigated. Exploring development mechanisms of germ cells is promising to promote future reproductive and developmental engineering technologies.
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Received: 27 September 2018
Published: 08 May 2019
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Corresponding Authors:
Yong-sheng YU,Hai-guo JIN
E-mail: yuyongsheng2002@163.com;khk1962@126.com
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|
[1] |
Wu Y, Li O, He C , et al. Generation and characterization of induced pluripotent stem cells from guinea pig fetal fibroblasts. Molecular Medicine Reports, 2017,15(6) : 3690-3698.
doi: 10.3892/mmr.2017.6431
pmid: 5436227
|
|
|
[2] |
Wernig M, Zhao J P, Pruszak J , et al. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson’ s disease. Proceedings of National Academy of Sciences of the United States of America, 2008,105(15):5856-5861.
doi: 10.1073/pnas.0801677105
|
|
|
[3] |
Takahashi K, Tanabe K, Ohnuki M , et al. Induction of pluripotent stem cells from human fibroblasts by defined factors. Cell, 2007,131(5):861-872.
doi: 10.1016/j.cell.2007.11.019
|
|
|
[4] |
Imamura M, Aoi T, Tokumasu A , et al. Induction of primordial germ cells from mouse induced pluripotent stem cells derived from adult hepatocytes. Molecular Reproduction and Development, 2010,77(9):802-811.
doi: 10.1002/mrd.21223
pmid: 20722049
|
|
|
[5] |
Correia C, Serra M, Espinha N , et al. Combining hypoxia and bioreactor hydrodynamics boosts induced pluripotent stem cell differentiation towards cardiomyocytes. Stem Cell Rev, 2014,10(6):786-801.
doi: 10.1007/s12015-014-9533-0
pmid: 25022569
|
|
|
[6] |
Schenke-Layland K, Rhodes K E, Angelis E , et al. Reprogrammed mouse fibroblasts differentiate into cells of the cardiovascular and hematopoietic lineages. Stem Cells, 2008,26(6):1537-1546.
doi: 10.1634/stemcells.2008-0033
pmid: 18450826
|
|
|
[7] |
Shi Y, Inoue H, Wu J C , et al. Induced pluripotent stem cell technology: a decade of progress. Nat Rev Drug Discov, 2017,16(2):115-130.
doi: 10.1038/nrd.2016.245
pmid: 27980341
|
|
|
[8] |
Hikabe O, Hamazaki N, Nagamatsu G , et al. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature, 2016,539(7628):299-303.
doi: 10.1038/nature20104
pmid: 27750280
|
|
|
[9] |
Cai H, Xia X, Wang L , et al. In vitro and in vivo differentiation of induced pluripotent stem cells into male germ cells. Biochem Biophys Res Commun, 2013,433(3):286-291.
doi: 10.1016/j.bbrc.2013.02.107
pmid: 23524261
|
|
|
[10] |
Eguizabal C, Montserrat N, Vassena R , et al. Complete meiosis from human induced pluripotent stem cells. Stem Cells , 2011,29(8):1186-1195.
doi: 10.1002/stem.672
pmid: 21681858
|
|
|
[11] |
Imamura M, Hikabe O , Lin Z Y C , et al. Generation of germ cells in vitro in the era of induced pluripotent stem cells. Mol Reprod Dev, 2014,81(1):2-19.
doi: 10.1002/mrd.22259
pmid: 23996404
|
|
|
[12] |
Yin X H, Li Y, Li J W , et al. Generation and periodontal differentiation of human gingival fibroblasts-derived integration-free induced pluripotent stem cells. Biochem Biophys Res Commun , 2016,473(3):726-732.
doi: 10.1016/j.bbrc.2015.10.012
pmid: 26456649
|
|
|
[13] |
Yamanaka S . A fresh look at iPS cells. Cell, 2009,137(1):13-17.
doi: 10.1016/j.cell.2009.03.034
|
|
|
[14] |
Liu S P, Fu R H, Huang Y C , et al. Induced pluripotent stem (iPS) cell research overview. Cell Transplant, 2011,20(1):15-19.
doi: 10.3727/096368910X532828
pmid: 20887681
|
|
|
[15] |
Li J, Song W, Pan G , et al. Advances in understanding the cell types and approaches used for generating induced pluripotent stem cells. J Hematol Oncol, 2014,7(50):1-18.
doi: 10.1186/1756-8722-7-1
pmid: 3884022
|
|
|
[16] |
Li Y, Wang X, Feng X , et al. Generation of male germ cells from mouse induced pluripotent stem cells in vitro. Stem Cell Res, 2014,12(2):517-530
doi: 10.1016/j.scr.2013.12.007
pmid: 24463497
|
|
|
[17] |
Tan H, Wang J J, Cheng S F , et al. Retinoic acid promotes the proliferation of primordial germ cell-like cells differentiated from mouse skin-derived stem cells in vitro. Theriogenology, 2016,85(3):408-418.
doi: 10.1016/j.theriogenology.2015.09.002
pmid: 26456183
|
|
|
[18] |
Niederreither K, Dollé P . Retinoic acid in development: towards an integrated view. Nat Rev Genet, 2008,9(7):541-553.
doi: 10.1038/nrg2340
pmid: 18542081
|
|
|
[19] |
Kim J B, Sebastiano V, Wu G , et al. Oct4-induced pluripotency in adult neural stem cells. Cell, 2009,136(3):411-419.
doi: 10.1016/j.cell.2009.01.023
pmid: 19203577
|
|
|
[20] |
Koubova J, Hu Y C, Bhattacharyya T , et al. Retinoic acid activates two pathways required for meiosis in mice. PLoS Genet, 2014,10(8):e1004541.
doi: 10.1371/journal.pgen.1004541
pmid: 4125102
|
|
|
[21] |
Costa J J, Souza G B, Soares M A , et al. In vitro differentiation of primordial germ cells and oocyte-like cells from stem cells. Histol Histopathol, 2018,33(2):121-132
doi: 10.14670/HH-11-917
pmid: 28691729
|
|
|
[22] |
Morita Y, Tilly J L . Segregation of retinoic acid effects on fetal ovarian germ cell mitosis versus apoptosis by requirement for new macromolecular synthesis. Endocrinology, 1999,140(6):2696-2703.
doi: 10.1210/endo.140.6.6826
pmid: 10342860
|
|
|
[23] |
Zhang Y, Wang Y, Zuo Q , et al. Selection of the inducer for the differentiation of chicken embryonic stem cells into male germ cells in vitro. PLoS One, 2016,11(10):e0164664.
doi: 10.1371/journal.pone.0164664
|
|
|
[24] |
Geijsen N, Horoschak M, Kim K , et al. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature, 2004,427(6970):148-154.
|
|
|
[25] |
Li P, Hu H, Yang S , et al. Differentiation of induced pluripotent stem cells into male germ cells in vitro through embryoid body formation and retinoic acid or testosterone induction. Biomed Res Int, 2013,2013(1):608728.
doi: 10.1155/2013/608728
pmid: 23509752
|
|
|
[26] |
Yang S, Yuan Q, Niu M , et al. BMP4 promotes mouse iPS cell differentiation to male germ cells via Smad1/5, Gata4, Id1 and Id2. Reproduction, 2017,153(2):211-220.
doi: 10.1530/REP-16-0292
pmid: 27864336
|
|
|
[27] |
Wozney J M . Overview of bone morphogenetic proteins. Spine, 2002,27(16):2-8.
doi: 10.1097/01.BRS0000020725.01916.7E
pmid: 12205411
|
|
|
[28] |
He Z . Derivation of male germ cells from induced pluripotent stem (iPS) cells: a novel and crucial source for generating male gametes. Asian J Androl, 2012,14(4):516-517.
doi: 10.1038/aja.2012.44
pmid: 22635161
|
|
|
[29] |
Lochab A K, Extavour C G . Bone morphogenetic protein (BMP) signaling in animal reproductive system development and function. Dev Biol, 2017,427(2):258-269.
doi: 10.1016/j.ydbio.2017.03.002
pmid: 28284906
|
|
|
[30] |
Ying Y, Liu X M, Marble A , et al. Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol Endocrinol, 2000,14(7):1053-1063.
doi: 10.1210/me.14.7.1053
pmid: 10894154
|
|
|
[31] |
Ying Y, Qi X, Zhao G Q . Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci USA, 2001,98(14):7858-7862.
doi: 10.1073/pnas.151242798
|
|
|
[32] |
Kee K, Gonsalves J M, Clark A T , et al. Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. Stem Cells Dev, 2006,15(6):831-837.
doi: 10.1089/scd.2006.15.831
pmid: 17253946
|
|
|
[33] |
Panula S, Medrano J V, Kee K , et al. Human germ cell differentiation from fetal-and adult-derived induced pluripotent stem cells. Hum Mol Genet, 2011,20(4):752-762.
doi: 10.1093/hmg/ddq520
|
|
|
[34] |
Bucay N, Yebra M, Cirulli V , et al. A novel approach for the derivation of putative primordial germ cells and sertoli cells from human embryonic stem cells. Stem Cells, 2009,27(1):68-77.
doi: 10.1634/stemcells.2007-1018
pmid: 18845765
|
|
|
[35] |
Park T S, Galic Z, Conway A E , et al. Derivation of primordial germ cells from human embryonic and induced pluripotent stem cells is significantly improved by coculture with human fetal gonadal cells. Stem Cells, 2009,27(4):783-795.
doi: 10.1002/stem.13
pmid: 19350678
|
|
|
[36] |
Yu J, Vodyanik M A, Smuga-Otto K , et al. Induced pluripotent stem cell lines derived from human somatic cells .Science, 2007,31(5858)8:1917-1920.
|
|
|
[37] |
Hikabe O, Hamazaki N, Nagamattsu G , et al. Reconstitution in vitro of the entire cycle of the mouse female gern line. Nature. 2016,539(7628):299-303.
doi: 10.1038/nature20104
pmid: 27750280
|
|
|
[38] |
Hashimoto H, Yuasa S . Testosterone induces cardiomyocyte differentiation from embryonic stem cells. J Mol Cell Cardiol, 2013,62(1):69-71.
doi: 10.1016/j.yjmcc.2013.05.008
pmid: 23711440
|
|
|
[39] |
Silva C, Wood J R, Salvador L , et al. Expression profile of male germ cell-associated genes in mouse embryonic stem cell cultures treated with all-trans retinoic acid and testosterone. Mol Reprod Dev, 2009,76(1):11-21.
doi: 10.1002/mrd.20925
pmid: 18425777
|
|
|
[40] |
Narenji Sani R, Tajik P, Movahedin M , et al. Effect of follicle stimulating hormone and testosterone on viability rate of cryopreserved spermatogonial stem cell after thawing. Iran J Vet Sci Technol, 2013,5:26-34.
|
|
|
[41] |
Tajik P, Sani R N, Moezifar M , et al. Effect of follicle- stimulating hormone and testosterone on colony formation of bovine spermatogonial stem cell. Comp Clin Pathol 2014,23(4):901-906.
doi: 10.1007/s00580-013-1710-z
|
|
|
[42] |
Zanganeh B M, Rastegar T, Roudkenar M H , et al. Co-culture of spermatogonial stem cells with sertoli cells in the presence of testosterone and FSH improved differentiation via up-regulation of post meiotic genes. Acta Med Iran, 2013,51(1):1-11.
pmid: 23456578
|
|
|
[43] |
Silva C, Wood J R, Salvador L , et al. Expression profile of male germ cell-associated genes in mouse embryonic stem cell cultures treated with all-trans retinoic acid and testosterone. Mol Reprod Dev, 2009,76(1):11-21.
doi: 10.1002/mrd.20925
pmid: 18425777
|
|
|
[44] |
Correia S, Alves M R, Cavaco J E , et al. Estrogenic regulation of testicular expression of stem cell factor and c-kit: implications in germ cell survival and male fertility. Fertil Steril, 2014,102(1):299-306.
doi: 10.1016/j.fertnstert.2014.04.009
pmid: 24825426
|
|
|
[45] |
Jeong W, Jung S, Bazer F , et al. Stem cell factor-induced AKT cell signaling pathway:effects on porcine trophectoderm and uterine luminal epithelial cells. Gen Comp Endocrinol, 2017,250(1):113-121.
doi: 10.1016/j.ygcen.2017.05.015
|
|
|
[46] |
Payer B, Saitou M, Barton S C , et al. Stella is a maternal effect gene required for normal early development in mice. Curr Biol, 2003,13(23):2110-2117.
doi: 10.1016/j.cub.2003.11.026
pmid: 14654002
|
|
|
[47] |
Bendall S C, Hughes C, Campbell J L , et al. An enhanced mass spectrometry approach reveals human embryonic stem cell growth factors in culture. Mol Cell Proteomics, 2009,8(3):421-432.
doi: 10.1074/mcp.M800190-MCP200
pmid: 2649806
|
|
|
[48] |
West F D, Machacek D W, Boyd N L , et al. Enrichment and differentiation of human germ-like cells mediated by feeder cells and basic fibroblast growth factor signaling. Stem Cells, 2008,26(11):2768-2776.
doi: 10.1634/stemcells.2008-0124
pmid: 18719225
|
|
|
[49] |
Bahadorani M, Hosseini S M, Abedi P , et al. Glial cell line-derived neurotrophic factor in combination with insulin-like growth factor 1 and basic fibroblast growth factor promote in vitro culture of goat spermatogonial stem cells. Growth Factors, 2015,33(3):181-191.
doi: 10.3109/08977194.2015.1062758
pmid: 26154310
|
|
|
[50] |
Wang H, Xiang J, Zhang W , et al. Induction of germ cell-like cells from porcine induced pluripotent stem cells. Sci Rep, 2016,6(1):27256.
doi: 10.1038/srep27256
pmid: 4893677
|
|
|
[51] |
Boozarpour S, Matin M M, Momeni-Moghaddam M , et al. Glial cell derived neurotrophic factor induces spermatogonial stem cell marker genes in chicken mesenchymal stem cells. Tissue Cell, 2016,48(3):235-241.
doi: 10.1016/j.tice.2016.03.003
pmid: 27026484
|
|
|
[52] |
Kang L, Wang J, Zhang Y , et al. iPS cells can support full-term development of tetraploid blastocyst-complemented embryos. Cell Stem Cell, 2009,5(2):135-138.
doi: 10.1016/j.stem.2009.07.001
pmid: 19631602
|
|
|
[53] |
Nayernia K, Lee J H, Drusenheimer N , et al. Derivation of male germ cells from bone marrow stem cells. Laboratory Investigation, 2006,86(7):654-663.
doi: 10.1038/labinvest.3700429
|
|
|
[54] |
Dyce P W, Wen L, Li J . In vitro germline potential of stem cells derived from fetal porcine skin. Nature Cell Biology, 2006,8(4):384-390.
doi: 10.1038/ncb1388
pmid: 16565707
|
|
|
[55] |
Zhao X Y, Li W, Lü Z , et al. iPS cells produce viable mice through tetraploid complementation. Nature, 2009,461(7260):86-90
doi: 10.1038/nature08267
pmid: 19672241
|
|
|
[56] |
Kerkis A, Fonseca S A, Serafim R C , et al. In vitro differentiation of male mouse embryonic stem cells into both presumptive sperm cells and oocytes. Cloning Stem Cells, 2007,9(4):535-548.
doi: 10.1089/clo.2007.0031
pmid: 18154514
|
|
|
[57] |
Toyooka Y, Tsunekawa N, Akasu R , et al. Embryonic stem cells can form germ cells in vitro. Proceedings of the National Academy of Sciences, 2003,100(20):11457-11462.
doi: 10.1073/pnas.1932826100
|
|
|
[58] |
Bowles J, Koopman P . Retinoci acid, meiosis and germ cell fate in mammals. Development, 2007,134(19):3401-3411.
doi: 10.1242/dev.001107
|
|
|
[59] |
Bowles J, Knight D, Smith C , et al. Retinoid signaling determines germ cell fate in mice. Science, 2006,312(5773):596-600.
doi: 10.1126/science.1125691
|
|
|
[60] |
Pellegrini M, Grimaldi P, Rossi P , et al. Developmental expression of BMP4/ALK3/SAMD5 signalling pathway in the mouse testis: a potential role of BMP4 in spermatogonia differentiation. Journal of Cell Science, 2003,116(16):3363-3372.
doi: 10.1242/jcs.00650
pmid: 12857787
|
|
|
[61] |
West F D , Roche-Rios M I, Abraham S , et al. KIT ligand and bone morphogenetic protein signaling enhances human embryonic stem cell to germ-like cell differentiation. Human Reproduction, 2010,25(1):168-178.
doi: 10.1093/humrep/dep338
pmid: 19840987
|
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|
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