Using of embryonic stem cells (ESCs) could improve production traits and disease resistance by improving the efficiency of somatic cell nuclear transfer (SCNT) technology. However, robust ESCs have not been established from domestic ungulates. In the present study, we generated goat induced pluripotent stem cells (giPSCs) and transgenic cloned dairy goat induced pluripotent stem cells (tgiPSCs) from dairy goat fibroblasts (gFs) and transgenic cloned dairy goat fibroblasts (tgFs), respectively, using lentiviruses that contained hOCT4, hSOX2, hMYC, and hKLF4 without chemical compounds. The giPSCs and tgiPSCs expressed endogenous pluripotent markers, including OCT4, SOX2, MYC, KLF4, and NANOG. Moreover, they were able to maintain a normal karyotype and differentiate into derivatives from all three germ layers in vitro and in vivo. Using SCNT, tgFs and tgiPSCs were used as donor cells to produce embryos, which were named tgF-Embryos and tgiPSC-Embryos. The fusion rates and cleavage rates had no significant differences between tgF-Embryos and tgiPSC-Embryos. However, the expression of IGF-2, which is an important gene associated with embryonic development, was significantly lower in tgiPSC-Embryos than in tgF-Embryos and was not significantly different from vivo-Embryos.
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References
1.
AasenT., RayaA., BarreroM.J., GarretaE., ConsiglioA., GonzalezF., VassenaR., BilićJ., PekarikV., TiscorniaG., EdelM., BouéS., and Izpisúa BelmonteJ.C. (2008). Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat. Biotechnol., 26, 1276–1284.
2.
BalasubramanianS., BabaiN., ChaudhuriA., QiuF., BhattacharyaS., DaveB.J., ParameswaranS., CarsonS.D., ThoresonW.B., SharpJ.G., RaoM., and AhmadI. (2009). Non cell-autonomous reprogramming of adult ocular progenitors: Generation of pluripotent stem cells without exogenous transcription factors. Stem Cells, 27, 3053–3062.
3.
BaoL., HeL., ChenJ., WuZ., LiaoJ., RaoL., RenJ., LiH., ZhuH., QianL., GuY., DaiH., XuX., ZhouJ., WangW., CuiC., and XiaoL. (2011). Reprogramming of ovine adult fibroblasts to pluripotency via drug-inducible expression of defined factors. Cell Res. 21, 600–608.
4.
BavisterB. (2004). The role of animal studies in supporting human assisted reproductive technology. Reprod. Fertil. Dev., 16, 719–728.
5.
BeddingtonR.S., and RobertsonE.J. (1989). An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development, 105, 733–737.
6.
ChenD.Y., JiangM.X., ZhaoZ.J., WangH.L., SunQ.Y., ZhangL.S., LiR.C., CaoH.H., ZhangQ.J., and MaD.L. (2007). Cloning of Asian yellow goat (C. hircus) by somatic cell nuclear transfer: Telophase enucleation combined with whole cell intracytoplasmic injection. Mol. Reprod. Dev., 74, 28–34.
7.
DaliriM., RaoK.B., KaurG., GargS., PatilS., and ToteyS.M. (1994). Expression of growth factor ligand and receptor genes in preimplantation stage water buffalo (Bubalus bubalis) embryos and oviduct epithelial cells. J. Reprod. Fertil., 117, 61–70.
8.
De BemT.H.C., ChiarattiM.R., RochettiR., BressanF.F., SangalliJ.R., MirandaM.S., PiresP.R.L., SchwartzK.R.L., SampaioR.V., Fantinato-NetoP., PimentelJ.R.V., PerecinF, SmithL.C., MeirellesF.V., AdonaP.R., and LealC.L.V. (2011). Viable calves produced by somatic cell nuclear transfer using meiotic-blocked oocytes. Cell. Reprogram., 13, 419–429.
9.
DeanW., SantosF., StojkovicM., ZakhartchenkoV., WalterJ., WolfE., and ReikW. (2001). Conservation of methylation reprogramming in mammalian development: Aberrant reprogramming in cloned embryos. Proc. Natl. Acad. Sci. USA., 98, 13734–13738.
10.
DohertyA.S., TemelesG.L., and SchultzR.M. (1994). Temporal pattern of IGF-I expression during mouse preimplantation embryogenesis. Mol Reprod Dev. 37, 21–26.
EgliD., ChenA.E., SaphierG., IchidaJ., FitzgeraldC., GoK.J., AcevedoN., PatelJ., BaetscherM., KearnsW.G., GolandR., LeibelR.L., MeltonD.A., and EgganK. (2011). Reprogramming within hours following nuclear transfer into mouse but not human zygotes. Nat. Commun., 2, 488.
13.
EstebanM.A., XuJ., YangJ., PengM., QinD., LiW., JiangZ., ChenJ., DengK., ZhongM., CaiJ., LaiL., and PeiD. (2009). Generation of induced pluripotent stem cell lines from Tibetan miniature pig. J. Biol. Chem., 284, 17634–17640.
14.
EzashiT., TeluguB.P., AlexenkoA.P., SachdevS., SinhaS., and RobertsR.M. (2009). Derivation of induced pluripotent stem cells from pig somatic cells. Proc. Natl. Acad. Sci. USA., 106, 10993–10998.
FukudaA., CaoF., MoritaS., YamadaK., JinchoY., TaneS., SotomaruY., and KonoT. (2010). Identification of inappropriately reprogrammed genes by large-scale transcriptome analysis of individual cloned mouse blastocysts. PLoS One, 5, e11274.
17.
HanD.W., SongS.J., UhumS.J., DoJ.T., KimN.H., ChungK.S., and LeeH.T. (2003). Expression of IGF2 and IGF receptor mRNA in bovine nuclear transferred embryos. Zygote, 11, 245–252.
18.
HanX., HanJ., DingF., CaoS., LimS.S., DaiY., ZhangR., ZhangY., LimB., and LiN. (2011). Generation of induced pluripotent stem cells from bovine embryonic fibroblast cells. Cell Res. 21, 1509–1512.
19.
HiratsukaM., UnoN., UedaK., KurosakiH., ImaokaN., KazukiK., UenoE., AkakuraY., KatohM., OsakiM., KazukiY., NakagawaM., YamanakaS., and OshimuraM. (2011). Integration-free iPS cells engineered using human artificial chromosome vectors. PLoS One, 6, e25961.
20.
HolmP., BoothP.J., SchmidtM.H., GreveT., and CallesenH. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology, 52, 683–700.
21.
HuangB., LiT., Alonso-GonzalezL., GorreR., KeatleyS., GreenA., TurnerP., KallingappaP.K., VermaV., and ObackB. (2011). A virus-free poly-promoter vector induces pluripotency in quiescent bovine cells under chemically defined conditions of dual kinase inhibition. PLoS One, 6, e24501.
22.
InoueK., OgonukiN., MikiH., HiroseM., NodaS., KimJ-M., AokiF., MiyoshiH., and OguraA. (2006). Inefficient reprogramming of the hematopoietic stem cell genome following nuclear transfer. J. Cell Sci., 119, 1985–1991.
23.
JaenischR., EgganK., HumpherysD., RideoutW., and HochedlingerK. (2002). Nuclear cloning, stem cells, and genomic reprogramming. Cloning Stem Cells, 4, 389–396.
24.
KaneN.M., NowrouziA., MukherjeeS., BlundellM.P., GreigJ.A., LeeW.K., HouslayM.D., MilliganG., MountfordJ.C., von KalleC., SchmidtM., ThrasherA.J., and BakerA.H. (2010). Lentivirus-mediated reprogramming of somatic cells in the absence of transgenic transcription factors. Mol. Ther., 18, 2139–2145.
25.
KangY.K., KooD.B., ParkJ,S., ChoiY.H., ChungA.S., LeeK.K., and HanY.M. (2001). Aberrant methylation of donor genome in cloned bovine embryos. Nat. Genet., 28, 173–177.
26.
KeeferC.L. (2004). Production of bioproducts through the use of transgenic animal models. Anim. Reprod. Sci., 82–83, 5–12.
27.
KeeferC.L., PantD., BlombergL., and TalbotN.C. (2007). Challenges and prospects for the establishment of embryonic stem cell lines of domesticated ungulates. Anim. Reprod. Sci., 98, 147–168.
28.
KimJ.B., GreberB., Araúzo-BravoM.J., MeyerJ., ParkK.I., ZaehresH., and SchölerH.R. (2009). Direct reprogramming of human neural stem cells by OCT4. Nature. 461, 649–643.
29.
KimS., LeeG.S., LeeS.H., KimH.S., JeongY.W., KimJ.H., KangS.K., LeeB.C., and HwangW.S. (2005). Embryotropic effect of insulin-like growth factor (IGF)-I and its receptor on development of porcine preimplantation embryos produced by in vitro fertilization and somatic cell nuclear transfer. Mol. Reprod. Dev., 72, 88–97.
30.
KimS., LeeS.H., KimJ.H., JeongY.W., HashemM.A., KooO.J., ParkS.M., LeeE.G., HosseinM.S., KangS.K., LeeB.C., and HwangW.S. (2006). Anti-apoptotic effect of insulin-like growth factor (IGF)-I and its receptor in porcine preimplantation embryos derived from in vitro fertilization and somatic cell nuclear transfer. Mol. Reprod. Dev., 73, 1523–1530.
31.
KohdaT., KishigamiS., Kaneko-IshinoT., WakayamaT., and IshinoF. (2012). Gene expression profile normalization in cloned mice by trichostatin A treatment. Cell. Reprogram., 14, 45–55.
32.
InoueK., OgonukiN., MikiH., HiroseM., NodaS., KimJ-M., AokiF., MiyoshiH., and OguraA. (2006). Inefficient reprogramming of the hematopoietic stem cell genome following nuclear transfer. J. Cell Sci., 119, 1985–1991.
33.
KishigamiS., MizutaniE., OhtaH., HikichiT., ThuanN.V., WakayamaS., BuiH.T., and WakayamaT. (2006). Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun., 340, 183–189.
LiW., ZhouH., AbujarourR., ZhuS., Young JooJ., LinT., HaoE., SchölerH.R., HayekA., and DingS. (2009). Generation of human-induced pluripotent stem cells in the absence of exogenous Sox2. Stem Cells, 27, 2992–3000.
36.
LiY., CangM., LeeA.S., ZhangK., and LiuD. (2011). Reprogramming of sheep fibroblasts into pluripotency under a drug-inducible expression of mouse-derived defined factors. PLoS One, 6, e15947.
37.
LightenA.D., HardyK., WinstonR.M., and MooreG.E. (1997). Expression of mRNA for the insulin-like growth factors and their receptors in human preimplantation embryos. Mol. Reprod. Dev., 47, 134–139.
38.
LiuJ., BalehosurD., MurrayB., KellyJ.M., SumerH., and VermaP.J. (2012). Generation and characterization of reprogrammed sheep induced pluripotent stem cells. Theriogenology, 77, 338–346.
39.
LonerganP., Gutiérrez-AdánA., PintadoB., FairT., WardF., FuenteJ.D., and BolandM. (2000). Relationship between time of first cleavage and the expression of IGF-I growth factor, its receptor, and two housekeeping genes in bovine two-cell embryos and blastocysts produced in vitro. Mol. Reprod. Dev., 57, 146–152.
40.
MiyoshiK., MoriH., MizobeY., AkasakaE., OzawaA., YoshidaM., and SatoM. (2010). Valproic acid enhances in vitro development and Oct-3/4 expression of miniature pig somatic cell nuclear transfer embryos. Cell. Reprogram., 12, 67–74.
41.
MizutaniE., YamagataK., OnoT., AkagiS., GeshiM., and WakayamaT. (2012). Abnormal chromosome segregation at early cleavage is a major cause of the full-term developmental failure of mouse clones. Dev. Biol., 364, 56–65.
42.
MontserratN., de OñateL., GarretaE., GonzálezF., AdamoA., EguizábalC., HäfnerS., VassenaR., and Izpisua BelmonteJ.C. (2012). Generation of feeder-free pig induced pluripotent stem cells without Pou5f1. Cell Transplant. 21, 815–825.
43.
NoggleS., FungH.L., GoreA., MartinezH., SatrianiK.C., ProsserR., OumK., PaullD., DruckenmillerS., FreebyM., GreenbergE., ZhangK., GolandR., SauerM.V., LeibelR.L., and EgliD. (2011). Human oocytes reprogram somatic cells to a pluripotent state. Nature, 478, 70–75.
44.
OhganeJ., WakayamaT., SendaS., YamazakiY., InoueK., OguraA., MarhJ., TanakaS., YanagimachiR., and ShiotaK. (2004). The Sall3 locus is an epigenetic hotspot of aberrant DNA methylation associated with placentomegaly of cloned mice. Genes Cells, 9, 253–260.
45.
PandeyA., SinghN., GuptaS.C., RanaJ.S., and GuptaN. (2009). Relative expression of cell growth regulatory genes insulin-like growth factors (IGF-1 and IGF-2) and their receptors (IGF-1R and IGF-2R) in somatic cell nuclear transferred (SCNT) and in vitro fertilized (IVF) pre-implantation buffalo embryos. Cell Biol. Int., 33, 555–564.
46.
QinY., QinJ., ZhouC., LiJ., and GaoW.Q. (2015). Generation of embryonic stem cells from mouse adipose-tissue derived cells via somatic cell nuclear transfer. Cell Cycle, 14, 1282–1290.
47.
RalstonA., and RossantJ. (2005). Genetic regulation of stem cell origins in the mouse embryo. Clin. Genet., 68, 106–112.
48.
RappoleeD.A, SturmK.S., BehrendtsenO., SchultzG.A., PedersenR.A., and WerbZ. (1992). Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. Genes Dev. 6, 939–952.
49.
RenJ., PakY., HeL., QianL., GuY., LiH., RaoL., LiaoJ., CuiC., XuX., ZhouJ., RiH., and XiaoL. (2011). Generation of hircine-induced pluripotent stem cells by somatic cell reprogramming. Cell Res. 21, 849–853.
50.
RideoutW.M.3rd, WakayamaT., WutzA., EgganK., Jackson-GrusbyL., DausmanJ., YanagimachiR., and JaenischR. (2000). Generation of mice from wild-type and targeted ES cells by nuclear cloning. Nat. Genet., 24, 109–110.
51.
SantosF., ZakhartchenkoV., StojkovicM., PetersA., JenuweinT., WolfE., ReikW., and DeanW. (2003). Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr. Biol., 13, 1116–1121.
52.
SchultzG.A., HoganA., WatsonA.J., SmithR.M., and HeynerS. (1992). Insulin, insulin-like growth factors and glucose transporters: Temporal patterns of gene expression in early murine and bovine embryos. Reprod. Fertil. Dev., 4, 361–371.
53.
ShenC.J., LinC.C., ShenP.C., ChengW.T., ChenH.L., ChangT.C., LiuS.S., and ChenC.M. (2013). Imprinted genes and satellite loci are differentially methylated in bovine somatic cell nuclear transfer clones. Cell. Reprogram., 15, 413–424.
TanK.Y., EminliS., HettmerS., HochedlingerK., and WagersA.J. (2011). Efficient generation of iPS cells from skeletal muscle stem cells. PLoS One, 6, e26406.
58.
TakahashiK., and YamanakaS. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663–676.
59.
TakahashiK., TanabeK., OhnukiM., NaritaM., IchisakaT., TomodaK., and YamanakaS. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131, 861–872.
WanY.J., ZhangY.L., ZhouZ.R., JiaR.X., LiM., SongH., WangZ.Y., WangL.Z., ZhangG.M., YouJ.H., and WangF. (2012). Efficiency of donor cell preparation and recipient oocyte source for production of transgenic cloned dairy goats harboring human lactoferrin. Theriogenology, 78, 583–592.
62.
WatsonA.J., HoganA., HahnelA., WiemerK.E., and SchultzG.A. (1992). Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo. Mol. Reprod. Dev., 31, 87–95.
63.
WilmutI., BeaujeanN., de SousaP.A., DinnyesA., KingT.J., PatersonL.A., WellsD.N., and YoungL.E. (2002). Somatic cell nuclear transfer. Nature, 419, 583–586.
64.
WuZ., ChenJ., RenJ., BaoL., LiaoJ., CuiC., RaoL., LiH., GuY., DaiH., ZhuH., TengX., ChengL., and XiaoL. (2009). Generation of pig induced pluripotent stem cells with a drug-inducible system. J. Mol. Cell. Biol., 1, 46–54.
65.
YaseenM.A., WrenzyckiC., HerrmannD., CarnwathJ.W., and NiemannH. (2001). Changes in the relative abundance of mRNA transcripts for insulin-like growth factor (IGF-I and IGF-II) ligands and their receptors (IGF-IR/IGF-IIR) in preimplantation bovine embryos derived from different in vitro systems. Reproduction, 122, 601–610.
66.
YoshidaY., MiyamuraM., HamanoS., and YoshidaM. (1998). Expression of growth factor ligand and their receptor mRNAs in bovine ova during in vitro maturation and after fertilization in vitro. J. Vet. Med. Sci., 60, 549–554.
67.
YuJ., VodyanikM.A., Smuga-OttoK., Antosiewicz-BourgetJ., FraneJ.L., TianS., NieJ., JonsdottirG.A., RuottiV., StewartR., SlukvinI.I., and ThomsonJ.A. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science, 318, 1917–1920.
68.
ZhangX., KidderG.M., WatsonA.J., SchultzG.A., and ArmstrongD.T. (1994). Possible roles of insulin and insulin-like growth factors in rat preimplantation development: Investigation of gene expression by reverse transcription-polymerase chain reaction. J. Reprod. Fertil., 100, 375–380.
69.
ZhouS., DingC., ZhaoX., WangE., DaiX., LiuL., LiW., LiuZ., WanH., FengC., HaiT., WangL., and ZhouQ. (2010). Successful generation of cloned mice using nuclear transfer from induced pluripotent stem cells. Cell Res. 20, 850–853.
