1. College of Veterinary Medicine/Shaanxi Centre of Stem Cells Engineering and Technology, Northwest A&F University, Yangling 712100, China 2. Centre for Healthy Brain Ageing, UNSW Medicine, Randwick NSW 2031, Australia
Primordial germ cells (PGCs) are regarded as unipotent cells that can produce only either spermatogonia or oocytes. However, PGCs can be converted into the pluripotent state by first dedifferentiation to embryonic germ cells and then by reprogramming to induce them to become pluripotent stem cells (iPSCs). These two stages can be completely implemented with mouse cells. However, authentic porcine iPSCs have not been established. Here, we discuss recent advances in the stem cell field for obtaining iPSCs from PGCs. This knowledge will provide some clues which will contribute to the regulation of reprogramming to pluripotency in farm species.
Transduction with Oct4, Sox2, Nanog, Klf4, Lin28 and cMyc
Chimera
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Tab.1
Fig.1
1
FBertocchini, S M Chuva de Sousa Lopes. Germline development in amniotes: a paradigm shift in primordial germ cell specification. BioEssays, 2016, 38(8): 791–800 https://doi.org/10.1002/bies.201600025
pmid: 27273724
2
TKimura, Y Kaga, YSekita, KFujikawa, TNakatani, MOdamoto, SFunaki, MIkawa, KAbe, T Nakano. Pluripotent stem cells derived from mouse primordial germ cells by small molecule compounds. Stem Cells, 2015, 33(1): 45–55 https://doi.org/10.1002/stem.1838
pmid: 25186651
3
KTakahashi, K Tanabe, MOhnuki, MNarita, TIchisaka, KTomoda, SYamanaka. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 2007, 131(5): 861–872 https://doi.org/10.1016/j.cell.2007.11.019
pmid: 18035408
4
I HPark, R Zhao, J AWest, AYabuuchi, HHuo, T A Ince, P H Lerou, M W Lensch, G Q Daley. Reprogramming of human somatic cells to pluripotency with defined factors. Nature, 2008, 451(7175): 141–146 https://doi.org/10.1038/nature06534
pmid: 18157115
5
MStadtfeld, M Nagaya, JUtikal, GWeir, K Hochedlinger. Induced pluripotent stem cells generated without viral integration. Science, 2008, 322(5903): 945–949 https://doi.org/10.1126/science.1162494
pmid: 18818365
6
YLi, Q Zhang, XYin, WYang, Y Du, PHou, JGe, C Liu, WZhang, XZhang, YWu, H Li, KLiu, CWu, Z Song, YZhao, YShi, H Deng. Generation of iPSCs from mouse fibroblasts with a single gene, Oct4, and small molecules. Cell Research, 2011, 21(1): 196–204 https://doi.org/10.1038/cr.2010.142
pmid: 20956998
7
TLin, R Ambasudhan, XYuan, WLi, S Hilcove, RAbujarour, XLin, H S Hahm, E Hao, AHayek, SDing. A chemical platform for improved induction of human iPSCs. Nature Methods, 2009, 6(11): 805–808 https://doi.org/10.1038/nmeth.1393
pmid: 19838168
8
YMatsui, K Zsebo, B LHogan. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell, 1992, 70(5): 841–847 https://doi.org/10.1016/0092-8674(92)90317-6
pmid: 1381289
9
F ABazley, C F Liu, X Yuan, HHao, A HAll, ADe Los Angeles, E TZambidis, J DGearhart, C LKerr. Direct reprogramming of human primordial germ cells into induced pluripotent stem cells: efficient generation of genetically engineered germ cells. Stem Cells and Development, 2015, 24(22): 2634–2648 https://doi.org/10.1089/scd.2015.0100
pmid: 26154167
10
TKobayashi, H Zhang, W W CTang, NIrie, S Withey, DKlisch, ASybirna, SDietmann, D AContreras, RWebb, C Allegrucci, RAlberio, M ASurani. Principles of early human development and germ cell program from conserved model systems. Nature, 2017, 546(7658): 416–420 https://doi.org/10.1038/nature22812
pmid: 28607482
YOhinata, B Payer, DO’Carroll, KAncelin, YOno, M Sano, S CBarton, TObukhanych, MNussenzweig, ATarakhovsky, MSaitou, M ASurani. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature, 2005, 436(7048): 207–213 https://doi.org/10.1038/nature03813
pmid: 15937476
13
GNagamatsu, S Saito, KTakubo, TSuda. Integrative analysis of the acquisition of pluripotency in PGCs reveals the mutually exclusive roles of Blimp-1 and AKT signaling. Stem Cell Reports, 2015, 5(1): 111–124 https://doi.org/10.1016/j.stemcr.2015.05.007
pmid: 26050930
14
MYamaji, Y Seki, KKurimoto, YYabuta, MYuasa, MShigeta, KYamanaka, YOhinata, MSaitou. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nature Genetics, 2008, 40(8): 1016–1022 https://doi.org/10.1038/ng.186
pmid: 18622394
15
KKlisch, D A Contreras, X Sun, RBrehm, MBergmann, RAlberio. The Sda/GM2-glycan is a carbohydrate marker of porcine primordial germ cells and of a subpopulation of spermatogonia in cattle, pigs, horses and llama. Reproduction, 2011, 142(5): 667–674 https://doi.org/10.1530/REP-11-0007
pmid: 21896636
16
YZhang, J Ma, HLi, JLv, R Wei, YCong, ZLiu. bFGF signaling-mediated reprogramming of porcine primordial germ cells. Cell and Tissue Research, 2016, 364(2): 429–441 https://doi.org/10.1007/s00441-015-2326-1
pmid: 26613602
17
SGoel, M Sugimoto, NMinami, MYamada, SKume, H Imai. Identification, isolation, and in vitro culture of porcine gonocytes. Biology of Reproduction, 2007, 77(1): 127–137 https://doi.org/10.1095/biolreprod.106.056879
pmid: 17377141
18
S M WHyldig, OOstrup, MVejlsted, P DThomsen. Changes of DNA methylation level and spatial arrangement of primordial germ cells in embryonic day 15 to embryonic day 28 pig embryos. Biology of Reproduction, 2011, 84(6): 1087–1093 https://doi.org/10.1095/biolreprod.110.086082
pmid: 21293033
19
S GPetkov, W A Reh, G B Anderson. Methylation changes in porcine primordial germ cells. Molecular Reproduction & Development, 2009, 76(1): 22
20
Hyldig S M, Croxall N, Contreras D A, Thomsen P D and Alberio R. Epigenetic reprogramming in the porcine germ line. BMC Developmental Biology, 2011, 11(1): 1–11
pmid: 21194500
21
MRuggiu, R Speed, MTaggart, S JMcKay, FKilanowski, PSaunders, JDorin, H JCooke. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature, 1997, 389(6646): 73–77 https://doi.org/10.1038/37987
pmid: 9288969
22
S STanaka, Y Toyooka, RAkasu, YKatoh-Fukui, YNakahara, RSuzuki, MYokoyama, TNoce. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes & Development, 2000, 14(7): 841–853
pmid: 10766740
23
SMasui, Y Nakatake, YToyooka, DShimosato, RYagi, K Takahashi, HOkochi, AOkuda, RMatoba, A ASharov, M SKo, HNiwa. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nature Cell Biology, 2007, 9(6): 625–635 https://doi.org/10.1038/ncb1589
pmid: 17515932
24
JSilva, J Nichols, T WTheunissen, GGuo, A L van Oosten, O Barrandon, JWray, SYamanaka, IChambers, ASmith. Nanog is the gateway to the pluripotent ground state. Cell, 2009, 138(4): 722–737 https://doi.org/10.1016/j.cell.2009.07.039
pmid: 19703398
25
J LResnick, L S Bixler, L Cheng, P JDonovan. Long-term proliferation of mouse primordial germ cells in culture. Nature, 1992, 359(6395): 550–551 https://doi.org/10.1038/359550a0
pmid: 1383830
26
PLopeziglesias, Y Alcaina, NTapia, DSabour, M JArauzobravo, DSainz de la Maza, EBerra, A NO’Mara, MNistal, SOrtega, P JDonovan, H RSchöler, M PDe Miguel, Sainz d l M D, Berra E, Nunezomara A, Nistal M and Ortega S. Hypoxia induces pluripotency in primordial germ cells by HIF1a stabilization and Oct4 deregulation. Antioxidants & Redox Signalling, 2015, 22(3): 205–223 https://doi.org/10.1089/ars.2014.5871
27
L RChen, Y L Shiue, L Bertolini, J FMedrano, R HBonDurant, G BAnderson. Establishment of pluripotent cell lines from porcine preimplantation embryos. Theriogenology, 1999, 52(2): 195–212 https://doi.org/10.1016/S0093-691X(99)00122-3
pmid: 10734388
28
IVassiliev, S Vassilieva, L F SBeebe, S JHarrison, S MMcIlfatrick, M BNottle. In vitro and in vivo characterization of putative porcine embryonic stem cells. Cellular Reprogramming, 2010, 12(2): 223–230 https://doi.org/10.1089/cell.2009.0053
pmid: 20677936
29
HShim, A Gutiérrez-Adán, L RChen, R HBonDurant, EBehboodi, G BAnderson. Isolation of pluripotent stem cells from cultured porcine primordial germ cells. Theriogenology, 1997, 57(5): 1089–1095 https://doi.org/10.1095/biolreprod57.5.1089
pmid: 9369175
30
J APiedrahita, KMoore, BOetama, C KLee, NScales, JRamsoondar, F WBazer, TOtt. Generation of transgenic porcine chimeras using primordial germ cell-derived colonies. Biology of Reproduction, 1998, 58(5): 1321–1329 https://doi.org/10.1095/biolreprod58.5.1321
pmid: 9603271
31
XDong, H Tsung, YMu, LLiu, H Chen, LZhang, HWang, S Feng. Generation of chimeric piglets by injection of embryonic germ cells from inbred Wuzhishan miniature pigs into blastocysts. Xenotransplantation, 2014, 21(2): 140–148 https://doi.org/10.1111/xen.12077
pmid: 24329557
32
F DWest, S L Terlouw, D J Kwon, J L Mumaw, S K Dhara, K Hasneen, J RDobrinsky, S LStice. Porcine induced pluripotent stem cells produce chimeric offspring. Stem Cells and Development, 2010, 19(8): 1211–1220 https://doi.org/10.1089/scd.2009.0458
pmid: 20380514
33
XDu, T Feng, DYu, YWu, H Zou, SMa, CFeng, Y Huang, HOuyang, XHu, D Pan, NLi, SWu. Barriers for deriving transgenefree pig iPS cells with episomal vectors. Stem Cells, 2015, 33(11): 3228–3238 https://doi.org/10.1002/stem.2089
pmid: 26138940
34
WChakritbudsabong, LSariya, SPamonsupornvichit, RPronarkngver, SChaiwattanarungruengpaisan, J NFerreira, PSetthawong, PPhakdeedindan, MTechakumphu, TTharasanit, SRungarunlert. Generation of a pig induced pluripotent stem cell (piPSC) line from embryonic fibroblasts by incorporating LIN28 to the four transcriptional factor-mediated reprogramming: VSMUi001-D. Stem Cell Research, 2017, 24: 21–24 https://doi.org/10.1016/j.scr.2017.08.005
pmid: 29034889
35
NMontserrat, E G Bahima, L Batlle, SHäfner, A MRodrigues, FGonzález, J CIzpisúa Belmonte. Generation of pig iPS cells: a model for cell therapy. Journal of Cardiovascular Translational Research, 2011, 4(2): 121–130 https://doi.org/10.1007/s12265-010-9233-3
pmid: 21088946
36
TEzashi, B P V L Telugu, A P Alexenko, S Sachdev, SSinha, R MRoberts. Derivation of induced pluripotent stem cells from pig somatic cells. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(27): 10993–10998 https://doi.org/10.1073/pnas.0905284106
pmid: 19541600
37
YWu, O Li, CHe, YLi, M Li, X LLiu, YWang, Y He. Generation and characterization of induced pluripotent stem cells from guinea pig fetal fibroblasts. Molecular Medicine Reports, 2017, 15(6): 3690–3698 https://doi.org/10.3892/mmr.2017.6431
pmid: 28393187
AOnishi, M Iwamoto, TAkita, SMikawa, KTakeda, TAwata, HHanada, A CPerry. Pig cloning by microinjection of fetal fibroblast nuclei. Science, 2000, 289(5482): 1188–1190 https://doi.org/10.1126/science.289.5482.1188
pmid: 10947985
40
I APolejaeva, S HChen, T DVaught, R LPage, JMullins, SBall, Y Dai, JBoone, SWalker, D LAyares, AColman, K HCampbell. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature, 2000, 407(6800): 86–90 https://doi.org/10.1038/35024082
pmid: 10993078
41
NMaherali, R Sridharan, WXie, JUtikal, SEminli, KArnold, MStadtfeld, RYachechko, JTchieu, RJaenisch, KPlath, KHochedlinger. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell, 2007, 1(1): 55–70 https://doi.org/10.1016/j.stem.2007.05.014
pmid: 18371336
42
MWernig, A Meissner, RForeman, TBrambrink, MKu, K Hochedlinger, B EBernstein, RJaenisch. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature, 2007, 448(7151): 318–324 https://doi.org/10.1038/nature05944
pmid: 17554336
43
NPashai, H Hao, AAll, SGupta, RChaerkady, ADe Los Angeles, J DGearhart, C LKerr. Genome-wide profiling of pluripotent cells reveals a unique molecular signature of human embryonic germ cells. PLoS One, 2012, 7(6): e39088 https://doi.org/10.1371/journal.pone.0039088
pmid: 22737227
44
MSaitou, S Kagiwada, KKurimoto. Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development, 2012, 139(1): 15–31 https://doi.org/10.1242/dev.050849
pmid: 22147951
45
NMise, T Fuchikami, MSugimoto, SKobayakawa, FIke, T Ogawa, TTada, SKanaya, TNoce, K Abe. Differences and similarities in the developmental status of embryo-derived stem cells and primordial germ cells revealed by global expression profiling. Genes to Cells, 2008, 13(8): 863–877 https://doi.org/10.1111/j.1365-2443.2008.01211.x
pmid: 18782224
46
HNiwa, J Miyazaki, A GSmith. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics, 2000, 24(4): 372–376 https://doi.org/10.1038/74199
pmid: 10742100