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SCIENCE CHINA Life Sciences, Volume 59, Issue 6: 576-583(2016) https://doi.org/10.1007/s11427-016-5066-x

Derivation and application of pluripotent stem cells forregenerative medicine

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  • ReceivedMar 30, 2016
  • AcceptedApr 20, 2016

Abstract

Pluripotent stem cells (PSCs) are cells that can differentiate into any type of cells in the body, therefore have valuable promise in regenerative medicine of cell replacement therapies and tissue/organ engineering. PSCs can be derived either from early embryos or directly from somatic cells by epigenetic reprogramming that result in customized cells from patients. Here we summarize the methods of deriving PSCs, the various types of PSCs generated with different status, and their versatile applications in both clinical and embryonic development studies. We also discuss an intriguing potential application of PSCs in constructing tissues/organs in large animals by interspecies chimerism. All these emerging findings are likely to contribute to the breakthroughs in biological research and the prosperous prospects of regenerative medicine.


Funded by

National Natural Science Foundation of China(31471395)


Acknowledgment

Acknowledgements This work was supported by the National Natural Science Foundation of China (31471395).


References

[1] Andrews P.W., Baker D., Benvinisty N., Miranda B., Bruce K., Brustle O., Choi M., Choi Y.M., Crook J.M., de Sousa P.A., Dvorak P., Freund C., Firpo M., Furue M.K., Gokhale P., Ha H.Y., Han E., Haupt S., Healy L., Hei D.J., Hovatta O., Hunt C., Hwang S.M., Inamdar M.S., Isasi R.M., Jaconi M., Jekerle V., Kamthorn P., Kibbey M.C., Knezevic I., Knowles B.B., Koo S.K., Laabi Y., Leopoldo L., Liu P., Lomax G.P., Loring J.F., Ludwig T.E., Montgomery K., Mummery C., Nagy A., Nakamura Y., Nakatsuji N., Oh S., Oh S.K., Otonkoski T., Pera M., Peschanski M., Pranke P., Rajala K.M., Rao M., Ruttachuk R., Reubinoff B., Ricco L., Rooke H., Sipp D., Stacey G.N., Suemori H., Takahashi T.A., Takada K., Talib S., Tannenbaum S., Yuan B.Z., Zeng F., Zhou Q.. Points to consider in the development of seed stocks of pluripotent stem cells for clinical applications: International Stem Cell Banking Initiative (ISCBI). Regen Med, 2015, 10: 1-44. Google Scholar

[2] Baguisi A., Behboodi E., Melican D.T., Pollock J.S., Destrempes M.M., Cammuso C., Williams J.L., Nims S.D., Porter C.A., Midura P., Palacios M.J., Ayres S.L., Denniston R.S., Hayes M.L., Ziomek C.A., Meade H.M., Godke R.A., Gavin W.G., Overstrom E.W., Echelard Y.. Production of goats by somatic cell nuclear transfer. Nat Biotechnol, 1999, 17: 456-461. CrossRef Google Scholar

[3] Betthauser J., Forsberg E., Augenstein M., Childs L., Eilertsen K., Enos J., Forsythe T., Golueke P., Jurgella G., Koppang R., Lesmeister T., Mallon K., Mell G., Misica P., Pace M., Pfister-Genskow M., Strelchenko N., Voelker G., Watt S., Thompson S., Bishop M.. Production of cloned pigs from in vitro systems. Nat Biotechnol, 2000, 18: 1055-1059. CrossRef Google Scholar

[4] Briggs R., King T.J.. Transplantation of living nuclei from blastula cells into enucleated frogs’ eggs. Proc Natl Acad Sci USA, 1952, 38: 455-463. CrossRef Google Scholar

[5] Bui H.T., Wakayama S., Kishigami S., Park K.K., Kim J.H., Thuan N.V., Wakayama T.. Effect of trichostatin A on chromatin remodeling, histone modifications, DNA replication, and transcriptional activity in cloned mouse embryos. Biol Reprod, 2010, 83: 454-463. CrossRef Google Scholar

[6] Carette J.E., Guimaraes C.P., Varadarajan M., Park A.S., Wuethrich I., Godarova A., Kotecki M., Cochran B.H., Spooner E., Ploegh H.L.. Haploid genetic screens in human cells identify host factors used by pathogens. Science, 2009, 326: 1231-1235. CrossRef Google Scholar

[7] Chen J., Lansford R., Stewart V., Young F., Alt F.W.. RAG-2-deficient blastocyst complementation: an assay of gene function in lymphocyte development. Proc Natl Acad Sci USA, 1993, 90: 4528-4532. CrossRef Google Scholar

[8] Chen T., Hao Y., Zhang Y., Li M., Wang M., Han W., Wu Y., Lv Y., Hao J., Wang L., Li A., Yang Y., Jin K., Zhao X., Li Y., Ping X., Lai W., Wu L., Jiang G., Wang H., Sang L., Wang X., Yang Y., Zhou Q.. m(6)A RNA methylation is regulated by microRNAs and promotes reprogramming to pluripotency. Cell Stem Cell, 2015, 16: 289-301. CrossRef Google Scholar

[9] Chen X., Li T., Li X., Xie Y., Guo X., Ji S., Niu Y., Yu Y., Ding C., Yao R., Yang S., Ji W., Zhou Q.. Neural progenitors derived from monkey embryonic stem cells in a simple monoculture system. Reprod Biomed Online, 2009, 19: 426-433. CrossRef Google Scholar

[10] Chesne P., Adenot P.G., Viglietta C., Baratte M., Boulanger L., Renard J.P.. Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat Biotechnol, 2002, 20: 366-369. CrossRef Google Scholar

[11] Cho H.J., Lee C.S., Kwon Y.W., Paek J.S., Lee S.H., Hur J., Lee E.J., Roh T.Y., Chu I.S., Leem S.H., Kim Y., Kang H.J., Park Y.B., Kim H.S.. Induction of pluripotent stem cells from adult somatic cells by protein-based reprogramming without genetic manipulation. Blood, 2010, 116: 386-395. CrossRef Google Scholar

[12] Cibelli J.B., Stice S.L., Golueke P.J., Kane J.J., Jerry J., Blackwell C., Ponce de Leon F.A., Robl J.M.. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science, 1998, 280: 1256-1258. CrossRef Google Scholar

[13] Dai X., Hao J., Hou X., Hai T., Fan Y., Yu Y., Jouneau A., Wang L., Zhou Q.. Somatic nucleus reprogramming is significantly improved by m-carboxycinnamic acid bishydroxamide, a histone deacetylase inhibitor. J Biol Chem, 2010, 285: 31002-31010. CrossRef Google Scholar

[14] Dai X., Hao J., Zhou Q.. A modified culture method significantly improves the development of mouse somatic cell nuclear transfer embryos. Reproduction, 2009, 138: 301-308. CrossRef Google Scholar

[15] Das P.P., Hendrix D.A., Apostolou E., Buchner A.H., Canver M.C., Beyaz S., Ljuboja D., Kuintzle R., Kim W., Karnik R., Shao Z., Xie H., Xu J., De Los Angeles A., Zhang Y., Choe J., Jun D.L., Shen X., Gregory R.I., Daley G.Q., Meissner A., Kellis M., Hochedlinger K., Kim J., Orkin S.H.. PRC2 is required to maintain expression of the maternal Gtl2-Rian-Mirg locus by preventing de novo DNA methylation in mouse embryonic stem cells. Cell Rep, 2015, 12: 1456-1470. CrossRef Google Scholar

[16] Davis R.L., Weintraub H., Lassar A.B.. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell, 1987, 51: 987-1000. CrossRef Google Scholar

[17] Dean W., Santos F., Stojkovic M., Zakhartchenko V., Walter J., Wolf E., Reik W.. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA, 2001, 98: 13734-13738. CrossRef Google Scholar

[18] Ding C., Huang S., Qi Q., Fu R., Zhu W., Cai B., Hong P., Liu Z., Gu T., Zeng Y., Wang J., Xu Y., Zhao X., Zhou Q., Zhou C.. Derivation of a homozygous human androgenetic embryonic stem cell line. Stem Cells Dev, 2015, 24: 2307-2316. CrossRef Google Scholar

[19] Elling U., Taubenschmid J., Wirnsberger G., O’Malley R., Demers S.P., Vanhaelen Q., Shukalyuk A.I., Schmauss G., Schramek D., Schnuetgen F., von Melchner H., Ecker J.R., Stanford W.L., Zuber J., Stark A., Penninger J.M.. Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell, 2011, 9: 563-574. CrossRef Google Scholar

[20] Esteban M.A., Wang T., Qin B., Yang J., Qin D., Cai J., Li W., Weng Z., Chen J., Ni S., Chen K., Li Y., Liu X., Xu J., Zhang S., Li F., He W., Labuda K., Song Y., Peterbauer A., Wolbank S., Redl H., Zhong M., Cai D., Zeng L., Pei D.. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell, 2010, 6: 71-79. CrossRef Google Scholar

[21] Evans M.J., Kaufman M.H.. Establishment in culture of pluripotential cells from mouse embryos. Nature, 1981, 292: 154-156. CrossRef Google Scholar

[22] Galli C., Lagutina I., Crotti G., Colleoni S., Turini P., Ponderato N., Duchi R., Lazzari G.. Pregnancy: a cloned horse born to its dam twin. Nature, 2003, 424: 635. Google Scholar

[23] Germanà M.A.. Gametic embryogenesis and haploid technology as valuable support to plant breeding. Plant Cell Rep, 2011, 30: 839-857. CrossRef Google Scholar

[24] Gu Q., Hao J., Hai T., Wang J., Jia Y., Kong Q., Wang J., Feng C., Xue B., Xie B., Liu S., Li J., He Y., Sun J., Liu L., Wang L., Liu Z., Zhou Q.. Efficient generation of mouse ESCs-like pig induced pluripotent stem cells. Protein Cell, 2014, 5: 338-342. CrossRef Google Scholar

[25] Gu Q., Hao J., Lu Y., Wang L., Wallace G.G., Zhou Q.. Three-dimensional bio-printing. Sci China Life Sci, 2015, 58: 411-419. CrossRef Google Scholar

[26] Gu Q., Hao J., Zhao X., Li W., Liu L., Wang L., Liu Z., Zhou Q.. Rapid conversion of human ESCs into mouse ESC-like pluripotent state by optimizing culture conditions. Protein Cell, 2012, 3: 71-79. CrossRef Google Scholar

[27] Gurdon J.B., Elsdale T.R., Fischberg M.. Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature, 1958, 182: 64-65. CrossRef Google Scholar

[28] Hai T., Hao J., Wang L., Jouneau A., Zhou Q.. Pluripotency maintenance in mouse somatic cell nuclear transfer embryos and its improvement by treatment with the histone deacetylase inhibitor TSA. Cell Reprogram, 2011, 13: 47-56. CrossRef Google Scholar

[29] Hai T., Teng F., Guo R., Li W., Zhou Q.. One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res, 2014, 24: 372-375. CrossRef Google Scholar

[30] Hanna J., Cheng A.W., Saha K., Kim J., Lengner C.J., Soldner F., Cassady J.P., Muffat J., Carey B.W., Jaenisch R.. Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci USA, 2010, 107: 9222-9227. CrossRef Google Scholar

[31] Hao J., Zhu W., Sheng C., Yu Y., Zhou Q.. Human parthenogenetic embryonic stem cells: one potential resource for cell therapy. Sci China C Life Sci, 2009, 52: 599-602. CrossRef Google Scholar

[32] Hemberger M., Dean W., Reik W., 2009. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat Rev Mol Cell Biol 10 526–537... Google Scholar

[33] Herson P.S., Virk M., Rustay N.R., Bond C.T., Crabbe J.C., Adelman J.P., Maylie J.. A mouse model of episodic ataxia type-1. Nat Neurosci, 2003, 6: 378-383. CrossRef Google Scholar

[34] Hou P., Li Y., Zhang X., Liu C., Guan J., Li H., Zhao T., Ye J., Yang W., Liu K., Ge J., Xu J., Zhang Q., Zhao Y., Deng H.. Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science, 2013, 341: 651-654. CrossRef Google Scholar

[35] Huangfu D., Maehr R., Guo W., Eijkelenboom A., Snitow M., Chen A.E., Melton D.A.. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol, 2008, 26: 795-797. CrossRef Google Scholar

[36] Hwang W.S., Ryu Y.J., Park J.H., Park E.S., Lee E.G., Koo J.M., Jeon H.Y., Lee B.C., Kang S.K., Kim S.J., Ahn C., Hwang J.H., Park K.Y., Cibelli J.B., Moon S.Y.. Evidence of a pluripotent human embryonic stem cell line derived from a cloned blastocyst. Science, 2004, 303: 1669-1674. CrossRef Google Scholar

[37] Iannaccone P.M., Taborn G.U., Garton R.L., Caplice M.D., Brenin D.R.. Pluripotent embryonic stem cells from the rat are capable of producing chimeras. Dev Biol, 1994, 163: 288-292. CrossRef Google Scholar

[38] International Stem Cell Banking I.. Consensus guidance for banking and supply of human embryonic stem cell lines for research purposes. Stem Cell Rev, 2009, 5: 301-314. CrossRef Google Scholar

[39] Kang Y.K., Koo D.B., Park J.S., Choi Y.H., Chung A.S., Lee K.K., Han Y.M.. Aberrant methylation of donor genome in cloned bovine embryos. Nat Genet, 2001, 28: 173-177. CrossRef Google Scholar

[40] Kato Y., Tani T., Sotomaru Y., Kurokawa K., Kato J., Doguchi H., Yasue H., Tsunoda Y.. Eight calves cloned from somatic cells of a single adult. Science, 1998, 282: 2095-2098. CrossRef Google Scholar

[41] Kim D., Kim C.H., Moon J.I., Chung Y.G., Chang M.Y., Han B.S., Ko S., Yang E., Cha K.Y., Lanza R., Kim K.S.. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell, 2009, 4: 472-476. CrossRef Google Scholar

[42] Kishigami S., Mizutani E., Ohta H., Hikichi T., Thuan N.V., Wakayama S., Bui H.T., Wakayama T.. Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commun, 2006, 340: 183-189. CrossRef Google Scholar

[43] Kobayashi T., Yamaguchi T., Hamanaka S., Kato-Itoh M., Yamazaki Y., Ibata M., Sato H., Lee Y.S., Usui J., Knisely A.S., Hirabayashi M., Nakauchi H.. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell, 2010, 142: 787-799. CrossRef Google Scholar

[44] Laiosa C.V., Stadtfeld M., Xie H., de Andres-Aguayo L., Graf T.. Reprogramming of committed T cell progenitors to macrophages and dendritic cells by C/EBP alpha and PU. 1 transcription factors. Immunity, 2006, 25: 731-744. Google Scholar

[45] Lee B.C., Kim M.K., Jang G., Oh H.J., Yuda F., Kim H.J., Hossein M.S., Kim J.J., Kang S.K., Schatten G., Hwang W.S.. Dogs cloned from adult somatic cells. Nature, 2005, 436: 641. CrossRef Google Scholar

[46] Lee J., Sayed N., Hunter A., Au K.F., Wong W.H., Mocarski E.S., Pera R.R., Yakubov E., Cooke J.P.. Activation of innate immunity is required for efficient nuclear reprogramming. Cell, 2012, 151: 547-558. CrossRef Google Scholar

[47] Leeb M., Walker R., Mansfield B., Nichols J., Smith A., Wutz A.. Germline potential of parthenogenetic haploid mouse embryonic stem cells. Development, 2012, 139: 3301-3305. CrossRef Google Scholar

[48] Leeb M., Wutz A.. Derivation of haploid embryonic stem cells from mouse embryos. Nature, 2011, 479: U131-U164. CrossRef Google Scholar

[49] Li T., Wang S., Xie Y., Lu Y., Zhang X., Wang L., Yang S., Wolf D., Zhou Q., Ji W.. Homologous feeder cells support undifferentiated growth and pluripotency in monkey embryonic stem cells. Stem Cells, 2005a, 23: 1192-1199. CrossRef Google Scholar

[50] Li T., Zhao X., Teng F., Li X., Jiang M., Li W., Wang X., Wang J., Liu L., Liu Z., Wang L., Zhou Q.. Derivation of germline competent rat embryonic stem cells from DA rats. J Genet Genomics, 2012a, 39: 603-606. CrossRef Google Scholar

[51] Li T., Zheng J., Xie Y., Wang S., Zhang X., Li J., Jin L., Ma Y., Wolf D.P., Zhou Q., Ji W.. Transplantable neural progenitor populations derived from rhesus monkey embryonic stem cells. Stem Cells, 2005, 23: 1295-1303. CrossRef Google Scholar

[52] Li W., Li X., Li T., Jiang M., Wan H., Luo G., Feng C., Cui X., Teng F., Yuan Y., Zhou Q., Gu Q., Shuai L., Sha J., Xiao Y., Wang L., Liu Z., Wang X., Zhao X., Zhou Q.. Genetic modification and screening in rat using haploid embryonic stem cells. Cell Stem Cell, 2014, 14: 404-414. CrossRef Google Scholar

[53] Li W., Shuai L., Wan H., Dong M., Wang M., Sang L., Feng C., Luo G., Li T., Li X., Wang L., Zheng Q., Sheng C., Wu H., Liu Z., Liu L., Wang L., Wang X., Zhao X., Zhou Q.. Androgenetic haploid embryonic stem cells produce live transgenic mice. Nature, 2012b, 490: 407-411. CrossRef Google Scholar

[54] Li W., Teng F., Li T., Zhou Q.. Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat Biotechnol, 2013, 31: 684-686. CrossRef Google Scholar

[55] Li W., Zhao X., Wan H., Zhang Y., Liu L., Lv Z., Wang X., Wang L., Zhou Q.. iPS cells generated without c-Myc have active Dlk1-Dio3 region and are capable of producing full-term mice through tetraploid complementation. Cell Res, 2011, 21: 550-553. CrossRef Google Scholar

[56] Li X., Cui X., Wang J., Wang Y., Li Y., Wang L., Wan H., Li T., Feng G., Shuai L., Li Z., Gu Q., Hao J., Wang L., Zhao X., Liu Z., Wang X., Li W., Zhou Q.. Generation and application of mouse-rat allodiploid embryonic stem cells. Cell, 2016a, 164: 279-292. CrossRef Google Scholar

[57] Li X., Wang J., Wang L., Wan H., Li Y., Li T., Wang Y., Shuai L., Mao Y., Cui X., Wang L., Liu Z., Li W., Zhou Q.. Co-participation of paternal and maternal genomes before the blastocyst stage is not required for full-term development of mouse embryos. J Mol Cell Biol, 2015, 7: 486-488. CrossRef Google Scholar

[58] Li Z., Sun X., Chen J., Liu X., Wisely S.M., Zhou Q., Renard J.P., Leno G.H., Engelhardt J.F.. Cloned ferrets produced by somatic cell nuclear transfer. Dev Biol, 2006, 293: 439-448. CrossRef Google Scholar

[59] Liu H., Chen Y., Niu Y., Zhang K., Kang Y., Ge W., Liu X., Zhao E., Wang C., Lin S., Jing B., Si C., Lin Q., Chen X., Lin H., Pu X., Wang Y., Qin B., Wang F., Wang H., Si W., Zhou J., Tan T., Li T., Ji S., Xue Z., Luo Y., Cheng L., Zhou Q., Li S., Sun Y., Ji W.. TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys. Cell Stem Cell, 2014, 14: 323-328. CrossRef Google Scholar

[60] Liu L., Luo G., Yang W., Zhao X., Zheng Q., Lv Z., Li W., Wu H., Wang L., Wang X., Zhou Q.. Activation of the imprinted Dlk1-Dio3 region correlates with pluripotency levels of mouse stem cells. J Biol Chem, 2010, 285: 19483-19490. CrossRef Google Scholar

[61] Ma M., Guo X., Wang F., Zhao C., Liu Z., Shi Z., Wang Y., Zhang P., Zhang K., Wang N., Lin M., Zhou Z., Liu J., Li Q., Wang L., Huo R., Sha J., Zhou Q.. Protein expression profile of the mouse metaphase-II oocyte. J Proteome Res, 2008, 7: 4821-4830. CrossRef Google Scholar

[62] Martin G.R.. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA, 1981, 78: 7634-7638. CrossRef Google Scholar

[63] Matsunari H., Nagashima H., Watanabe M., Umeyama K., Nakano K., Nagaya M., Kobayashi T., Yamaguchi T., Sumazaki R., Herzenberg L.A., Nakauchi H.. Blastocyst complementation generates exogenic pancreas in vivo in apancreatic cloned pigs. Proc Natl Acad Sci USA, 2013, 110: 4557-4562. CrossRef Google Scholar

[64] Mikkelsen T.S., Hanna J., Zhang X., Ku M., Wernig M., Schorderet P., Bernstein B.E., Jaenisch R., Lander E.S., Meissner A.. Dissecting direct reprogramming through integrative genomic analysis. Nature, 2008, 454: 49-55. CrossRef Google Scholar

[65] Niu Y., Shen B., Cui Y., Chen Y., Wang J., Wang L., Kang Y., Zhao X., Si W., Li W., Xiang A., Zhou J., Guo X., Bi Y., Si C., Hu B., Dong G., Wang H., Zhou Z., Li T., Tan T., Pu X., Wang F., Ji S., Zhou Q., Huang X., Ji W., Sha J.. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell, 2014, 156: 836-843. CrossRef Google Scholar

[66] Ohgane J., Wakayama T., Kogo Y., Senda S., Hattori N., Tanaka S., Yanagimachi R., Shiota K.. DNA methylation variation in cloned mice. Genesis, 2001, 30: 45-50. CrossRef Google Scholar

[67] Ohnuki M., Tanabe K., Sutou K., Teramoto I., Sawamura Y., Narita M., Nakamura M., Tokunaga Y., Nakamura M., Watanabe A., Yamanaka S., Takahashi K.. Dynamic regulation of human endogenous retroviruses mediates factor-induced reprogramming and differentiation potential. Proc Natl Acad Sci USA, 2014, 111: 12426-12431. CrossRef Google Scholar

[68] Onishi A., Iwamoto M., Akita T., Mikawa S., Takeda K., Awata T., Hanada H., Perry A.C.. Pig cloning by microinjection of fetal fibroblast nuclei. Science, 2000, 289: 1188-1190. CrossRef Google Scholar

[69] Polejaeva I.A., Chen S.H., Vaught T.D., Page R.L., Mullins J., Ball S., Dai Y., Boone J., Walker S., Ayares D.L., Colman A., Campbell K.H.. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature, 2000, 407: 86-90. CrossRef Google Scholar

[70] Rashid T., Kobayashi T., Nakauchi H.. Revisiting the flight of icarus: making human organs from PSCs with large animal chimeras. Cell Stem Cell, 2014, 15: 406-409. CrossRef Google Scholar

[71] Riaz A., Javeed A., Zhou Q.. Therapeutic cloning by xenotransplanted oocytes, supplemented with species specific reprogramming factors. Med Hypotheses, 2011, 76: 527-529. CrossRef Google Scholar

[72] Rubin G.M., Spradling A.C.. Genetic transformation of Drosophila with transposable element vectors. Science, 1982, 218: 348-353. CrossRef Google Scholar

[73] Shen C.N., Slack J.M., Tosh D.. Molecular basis of transdifferentiation of pancreas to liver. Nat Cell Biol, 2000, 2: 879-887. CrossRef Google Scholar

[74] Sheng C., Zheng Q., Wu J., Xu Z., Sang L., Wang L., Guo C., Zhu W., Tong M., Liu L., Li W., Liu Z., Zhao X., Wang L., Chen Z., Zhou Q.. Generation of dopaminergic neurons directly from mouse fibroblasts and fibroblast-derived neural progenitors. Cell Res, 2012a, 22: 769-772. CrossRef Google Scholar

[75] Sheng C., Zheng Q., Wu J., Xu Z., Wang L., Li W., Zhang H., Zhao X., Liu L., Wang Z., Guo C., Wu H., Liu Z., Wang L., He S., Wang X., Chen Z., Zhou Q.. Direct reprogramming of Sertoli cells into multipotent neural stem cells by defined factors. Cell Res, 2012b, 22: 208-218. CrossRef Google Scholar

[76] Shi Y., Do J.T., Desponts C., Hahm H.S., Scholer H.R., Ding S.. A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell, 2008, 2: 525-528. CrossRef Google Scholar

[77] Shin T., Kraemer D., Pryor J., Liu L., Rugila J., Howe L., Buck S., Murphy K., Lyons L., Westhusin M.. A cat cloned by nuclear transplantation. Nature, 2002, 415: 859. CrossRef Google Scholar

[78] Shinagawa T., Takagi T., Tsukamoto D., Tomaru C., Huynh L.M., Sivaraman P., Kumarevel T., Inoue K., Nakato R., Katou Y., Sado T., Takahashi S., Ogura A., Shirahige K., Ishii S.. Histone variants enriched in oocytes enhance reprogramming to induced pluripotent stem cells. Cell Stem Cell, 2014, 14: 217-227. CrossRef Google Scholar

[79] Shuai L., Wang Y., Dong M., Wang X., Sang L., Wang M., Wan H., Luo G., Gu T., Yuan Y., Feng C., Teng F., Li W., Liu X., Li T., Wang L., Wang X., Zhao X., Zhou Q.. Durable pluripotency and haploidy in epiblast stem cells derived from haploid embryonic stem cells in vitro. J Mol Cell Biol, 2015, 7: 326-337. CrossRef Google Scholar

[80] Shuai L., Zhou Q.. Haploid embryonic stem cells serve as a new tool for mammalian genetic study. Stem Cell Res Ther, 2014, 5: 20. CrossRef Google Scholar

[81] Solnica-Krezel L., Schier A.F., Driever W.. Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics, 1994, 136: 1401-1420. Google Scholar

[82] Song Y., Hai T., Wang Y., Guo R., Li W., Wang L., Zhou Q.. Epigenetic reprogramming, gene expression and in vitro development of porcine SCNT embryos are significantly improved by a histone deacetylase inhibitor-m-carboxycinnamic acid bishydroxamide (CBHA). Protein Cell, 2014, 5: 382-393. CrossRef Google Scholar

[83] Stadtfeld M., Apostolou E., Akutsu H., Fukuda A., Follett P., Natesan S., Kono T., Shioda T., Hochedlinger K.. Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature, 2010, 465: 175-181. CrossRef Google Scholar

[84] Takahashi K., Yamanaka S.. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 2006, 126: 663-676. CrossRef Google Scholar

[85] Tarkowski A.K., Rossant J.. Haploid mouse blastocysts developed from bisected zygotes. Nature, 1976, 259: 663-665. CrossRef Google Scholar

[86] Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M.. Embryonic stem cell lines derived from human blastocysts. Science, 1998, 282: 1145-1147. CrossRef Google Scholar

[87] Thomson J.A., Kalishman J., Golos T.G., Durning M., Harris C.P., Hearn J.P.. Pluripotent cell lines derived from common marmoset (Callithrix jacchus) blastocysts. Biol Reprod, 1996, 55: 254-259. CrossRef Google Scholar

[88] Tong M., Lv Z., Liu L., Zhu H., Zheng Q., Zhao X., Li W., Wu Y., Zhang H., Wu H., Li Z., Zeng F., Wang L., Wang X., Sha J., Zhou Q.. Mice generated from tetraploid complementation competent iPS cells show similar developmental features as those from ES cells but are prone to tumorigenesis. Cell Res, 2011, 21: 1634-1637. CrossRef Google Scholar

[89] Usui J., Kobayashi T., Yamaguchi T., Knisely A.S., Nishinakamura R., Nakauchi H.. Generation of kidney from pluripotent stem cells via blastocyst complementation. Am J Pathol, 2012, 180: 2417-2426. CrossRef Google Scholar

[90] Vierbuchen T., Ostermeier A., Pang Z.P., Kokubu Y., Sudhof T.C., Wernig M.. Direct conversion of fibroblasts to functional neurons by defined factors. Nature, 2010, 463: 1035-1041. CrossRef Google Scholar

[91] Wakayama T., Perry A.C., Zuccotti M., Johnson K.R., Yanagimachi R.. Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature, 1998, 394: 369-374. CrossRef Google Scholar

[92] Wan H., Feng C., Teng F., Yang S., Hu B., Niu Y., Xiang A., Fang W., Ji W., Li W., Zhao X., Zhou Q.. One-step generation of p53 gene biallelic mutant cynomolgus monkey via the CRISPR/Cas system. Cell Res, 2015, 25: 258-261. CrossRef Google Scholar

[93] Wan H., He Z., Dong M., Gu T., Luo G., Teng F., Xia B., Li W., Feng C., Li X., Li T., Shuai L., Fu R., Wang L., Wang X., Zhao X., Zhou Q.. Parthenogenetic haploid embryonic stem cells produce fertile mice. Cell Res, 2013, 23: 1330-1333. CrossRef Google Scholar

[94] Wang S., Shen Y., Yuan X., Chen K., Guo X., Chen Y., Niu Y., Li J., Xu R., Yan X., Zhou Q., Ji W.. Dissecting signaling pathways that govern self-renewal of rabbit embryonic stem cells. J Biol Chem, 2008, 283: 35929-35940. CrossRef Google Scholar

[95] Wang S., Tang X., Niu Y., Chen H., Li B., Li T., Zhang X., Hu Z., Zhou Q., Ji W.. Generation and characterization of rabbit embryonic stem cells. Stem Cells, 2007, 25: 481-489. CrossRef Google Scholar

[96] Wang X., Yuan Y., Zhou Q., Wan H., Wang M., Zhou Q., Zhao X., Sha J.. RNA guided genome editing in mouse germ-line stem cells. J Genet Genomics, 2014, 41: 409-411. CrossRef Google Scholar

[97] Wang X., Zhou J., Cao C., Huang J., Hai T., Wang Y., Zheng Q., Zhang H., Qin G., Miao X., Wang H., Cao S., Zhou Q., Zhao J.. Efficient CRISPR/Cas9-mediated biallelic gene disruption and site-specific knockin after rapid selection of highly active sgRNAs in pigs. Sci Rep, 2015, 5: 13348. CrossRef Google Scholar

[98] Wang Y., Hai T., Liu Z., Zhou S., Lv Z., Ding C., Liu L., Niu Y., Zhao X., Tong M., Wang L., Jouneau A., Zhang X., Ji W., Zhou Q.. HSPC117 deficiency in cloned embryos causes placental abnormality and fetal death. Biochem Biophys Res Commun, 2010, 397: 407-412. CrossRef Google Scholar

[99] Wani N.A., Wernery U., Hassan F.A., Wernery R., Skidmore J.A.. Production of the first cloned camel by somatic cell nuclear transfer. Biol Reprod, 2010, 82: 373-379. CrossRef Google Scholar

[100] Wei L., Cao X.. The effect of transposable elements on phenotypic variation: insights from plants to humans. Sci China Life Sci, 2016, 59: 24-37. CrossRef Google Scholar

[101] Wilmut I., Schnieke A.E., McWhir J., Kind A.J., Campbell K.H.. Viable offspring derived from fetal and adult mammalian cells. Nature, 1997, 385: 810-813. CrossRef Google Scholar

[102] Woods G.L., White K.L., Vanderwall D.K., Li G.P., Aston K.I., Bunch T.D., Meerdo L.N., Pate B.J.. A mule cloned from fetal cells by nuclear transfer. Science, 2003, 301: 1063. CrossRef Google Scholar

[103] Xie H., Ye M., Feng R., Graf T.. Stepwise reprogramming of B cells into macrophages. Cell, 2004, 117: 663-676. CrossRef Google Scholar

[104] Yamazaki Y., Fujita T.C., Low E.W., Alarcon V.B., Yanagimachi R., Marikawa Y.. Gradual DNA demethylation of the Oct4 promoter in cloned mouse embryos. Mol Reprod Dev, 2006, 73: 180-188. CrossRef Google Scholar

[105] Yang H., Liu Z., Ma Y., Zhong C., Yin Q., Zhou C., Shi L., Cai Y., Zhao H., Wang H., Tang F., Wang Y., Zhang C., Liu X., Lai D., Jin Y., Sun Q., Li J.. Generation of haploid embryonic stem cells from Macaca fascicularis monkey parthenotes. Cell Res, 2013, 23: 1187-1200. CrossRef Google Scholar

[106] Yang H., Shi L., Wang B., Liang D., Zhong C., Liu W., Nie Y., Liu J., Zhao J., Gao X., Li D., Xu G., Li J.. Generation of genetically modified mice by oocyte injection of androgenetic haploid embryonic stem cells. Cell, 2012, 149: 605-617. CrossRef Google Scholar

[107] Yu Y., Mai Q., Chen X., Wang L., Gao L., Zhou C., Zhou Q.. Assessment of the developmental competence of human somatic cell nuclear transfer embryos by oocyte morphology classification. Hum Reprod, 2009, 24: 649-657. Google Scholar

[108] Yuan X., Wan H., Zhao X., Zhu S., Zhou Q., Ding S.. Brief report: combined chemical treatment enables Oct4-induced reprogramming from mouse embryonic fibroblasts. Stem Cells, 2011, 29: 549-553. CrossRef Google Scholar

[109] Yuan Y., Zhou Q., Wan H., Shen B., Wang X., Wang M., Feng C., Xie M., Gu T., Zhou T., Fu R., Huang X., Zhou Q., Sha J., Zhao X.. Generation of fertile offspring from Kitw/Kitwv mice through differentiation of gene corrected nuclear transfer embryonic stem cells. Cell Res, 2015, 25: 851-863. CrossRef Google Scholar

[110] Zhao X., Li W., Lv Z., Liu L., Tong M., Hai T., Hao J., Guo C., Ma Q., Wang L., Zeng F., Zhou Q.. iPS cells produce viable mice through tetraploid complementation. Nature, 2009, 461: 86-90. CrossRef Google Scholar

[111] Zhao X., Li W., Lv Z., Liu L., Tong M., Hai T., Hao J., Guo C., Wang X., Wang L., Zeng F., Zhou Q.. Efficient and rapid generation of induced pluripotent stem cells using an alternative culture medium. Cell Res, 2010a, 20: 383-386. CrossRef Google Scholar

[112] Zhao X., Li W., Lv Z., Liu L., Tong M., Hai T., Hao J., Wang X., Wang L., Zeng F., Zhou Q.. Viable fertile mice generated from fully pluripotent iPS cells derived from adult somatic cells. Stem Cell Rev, 2010b, 6: 390-397. CrossRef Google Scholar

[113] Zhao X., Lv Z., Li W., Zeng F., Zhou Q.. Production of mice using iPS cells and tetraploid complementation. Nat Protoc, 2010c, 5: 963-971. CrossRef Google Scholar

[114] Zhao Y., Zhao T., Guan J., Zhang X., Fu Y., Ye J., Zhu J., Meng G., Ge J., Yang S., Cheng L., Du Y., Zhao C., Wang T., Su L., Yang W., Deng H.. A XEN-like state bridges somatic cells to pluripotency during chemical reprogramming. Cell, 2015, 163: 1678-1691. CrossRef Google Scholar

[115] Zhou H., Wu S., Joo J.Y., Zhu S., Han D.W., Lin T., Trauger S., Bien G., Yao S., Zhu Y., Siuzdak G., Scholer H.R., Duan L., Ding S.. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell, 2009, 4: 381-384. CrossRef Google Scholar

[116] Zhou Q., Brown J., Kanarek A., Rajagopal J., Melton D.A.. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature, 2008, 455: 627-632. CrossRef Google Scholar

[117] Zhou Q., Renard J.P., Le Friec G., Brochard V., Beaujean N., Cherifi Y., Fraichard A., Cozzi J.. Generation of fertile cloned rats by regulating oocyte activation. Science, 2003, 302: 1179. CrossRef Google Scholar

[118] Zhou Q., Wang M., Yuan Y., Wang X., Fu R., Wan H., Xie M., Liu M., Guo X., Zheng Y., Feng G., Shi Q., Zhao X., Sha J., Zhou Q.. Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell, 2016, 18: 330-340. CrossRef Google Scholar

[119] Zhou Q., Yang S., Ding C., He X., Xie Y., Hildebrandt T.B., Mitalipov S.M., Tang X., Wolf D.P., Ji W.. A comparative approach to somatic cell nuclear transfer in the rhesus monkey. Hum Reprod, 2006, 21: 2564-2571. CrossRef Google Scholar

[120] Zhou S., Ding C., Zhao X., Wang E., Dai X., Liu L., Li W., Liu Z., Wan H., Feng C., Hai T., Wang L., Zhou Q.. Successful generation of cloned mice using nuclear transfer from induced pluripotent stem cells. Cell Res, 2010, 20: 850-853. CrossRef Google Scholar

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