Derivation of Pluripotent Stem Cells with In Vivo Embryonic and Extraembryonic Potency

Cell

Volumn 169, Issue 2, 2017, Pages 243-257.e25

  Yang, Yang ^a,b   Liu, Bei ^a,b   Xu, Jun ^a   Wang, Jinlin ^a   Wu, Jun ^c   Shi, Cheng ^d   Xu, Yaxing ^b   Dong, Jiebin ^a   Wang, Chengyan ^a   Lai, Weifeng ^b   Zhu, Jialiang ^a   Xiong, Liang ^b   Zhu, Dicong ^a,b   Li, Xiang ^a   Yang, Weifeng ^e   Yamauchi, Takayoshi ^c   Sugawara, Atsushi ^c   Li, Zhongwei ^c   Sun, Fangyuan ^f   Li, Xiangyun ^f   Li, Chen ^b   He, Aibin ^b   Du, Yaqin ^a   Wang, Ting ^a   Zhao, Chaoran ^a   Li, Haibo ^a   Chi, Xiaochun ^g   Zhang, Hongquan ^g   Liu, Yifang ^h   Li, Cheng ^b   Duo, Shuguang ⁱ   Yin, Ming ^e   Shen, Huan ^d   Belmonte, Juan Carlos Izpisua ^c   Deng, Hongkui ^a,b   more..

^a Peking University   (China)

^b PEKING UNIVERSITY   (China)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

^e Hebei University ^*  (China)

^f HEBEI UNIVERSITY   (China)

^g PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^h TSINGHUA UNIVERSITY   (China)

ⁱ INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

chimeric ability; embryonic and extraembryonic developmental potentials; interspecies chimeric competency; single cell derived chimeras

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; EMBRYO TISSUE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; TETRAPLOIDY; TRANSLATIONAL RESEARCH; ANIMAL; BLASTOCYST; CELL CULTURE TECHNIQUE; CELL LINE; CHEMISTRY; CHIMERA; CYTOLOGY; DRUG EFFECTS; METABOLISM; PROCEDURES;

DIMETINDENE; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; MINOCYCLINE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1;

ANIMALS; BLASTOCYST; CELL CULTURE TECHNIQUES; CELL LINE; CHIMERA; DIMETHINDENE; HUMANS; INDICATORS AND REAGENTS; MICE; MINOCYCLINE; PLURIPOTENT STEM CELLS; POLY (ADP-RIBOSE) POLYMERASE-1;

EID: 85017162810     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.02.005     Document Type: Article

References (64)

1. Abad, M., Mosteiro, L., Pantoja, C., Cañamero, M., Rayon, T., Ors, I., Graña, O., Megías, D., Domínguez, O., Martínez, D., et al. Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502 (2013), 340–345.
2. Alano, C.C., Kauppinen, T.M., Valls, A.V., Swanson, R.A., Minocycline inhibits poly(ADP-ribose) polymerase-1 at nanomolar concentrations. Proc. Natl. Acad. Sci. USA 103 (2006), 9685–9690.
3. Beddington, R.S., Robertson, E.J., An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 105 (1989), 733–737.
4. Brons, I.G., Smithers, L.E., Trotter, M.W., Rugg-Gunn, P., Sun, B., Chuva de Sousa Lopes, S.M., Howlett, S.K., Clarkson, A., Ahrlund-Richter, L., Pedersen, R.A., Vallier, L., Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448 (2007), 191–195.
5. Buehr, M., Meek, S., Blair, K., Yang, J., Ure, J., Silva, J., McLay, R., Hall, J., Ying, Q.L., Smith, A., Capture of authentic embryonic stem cells from rat blastocysts. Cell 135 (2008), 1287–1298.
6. Cantone, I., Fisher, A.G., Epigenetic programming and reprogramming during development. Nat. Struct. Mol. Biol. 20 (2013), 282–289.
7. Chan, Y.S., Göke, J., Ng, J.H., Lu, X., Gonzales, K.A.U., Tan, C.P., Tng, W.Q., Hong, Z.Z., Lim, Y.S., Ng, H.H., Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast. Cell Stem Cell 13 (2013), 663–675.
8. Chen, Y., Niu, Y., Li, Y., Ai, Z., Kang, Y., Shi, H., Xiang, Z., Yang, Z., Tan, T., Si, W., et al. Generation of Cynomolgus Monkey Chimeric Fetuses using Embryonic Stem Cells. Cell Stem Cell 17 (2015), 116–124.
9. Cohen, M.A., Wert, K.J., Goldmann, J., Markoulaki, S., Buganim, Y., Fu, D., Jaenisch, R., Human neural crest cells contribute to coat pigmentation in interspecies chimeras after in utero injection into mouse embryos. Proc. Natl. Acad. Sci. USA 113 (2016), 1570–1575.
10. De Los Angeles, A., Ferrari, F., Xi, R., Fujiwara, Y., Benvenisty, N., Deng, H., Hochedlinger, K., Jaenisch, R., Lee, S., Leitch, H.G., et al. Hallmarks of pluripotency. Nature 525 (2015), 469–478.
11. Evans, M.J., Kaufman, M.H., Establishment in culture of pluripotential cells from mouse embryos. Nature 292 (1981), 154–156.
12. Fang, R., Liu, K., Zhao, Y., Li, H., Zhu, D., Du, Y., Xiang, C., Li, X., Liu, H., Miao, Z., et al. Generation of naive induced pluripotent stem cells from rhesus monkey fibroblasts. Cell Stem Cell 15 (2014), 488–496.
13. Gafni, O., Weinberger, L., Mansour, A.A., Manor, Y.S., Chomsky, E., Ben-Yosef, D., Kalma, Y., Viukov, S., Maza, I., Zviran, A., et al. Derivation of novel human ground state naive pluripotent stem cells. Nature 504 (2013), 282–286.
14. Guo, G., von Meyenn, F., Santos, F., Chen, Y., Reik, W., Bertone, P., Smith, A., Nichols, J., Naive Pluripotent Stem Cells Derived Directly from Isolated Cells of the Human Inner Cell Mass. Stem Cell Reports 6 (2016), 437–446.
15. Hassa, P.O., Hottiger, M.O., The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front. Biosci. 13 (2008), 3046–3082.
16. Hemberger, M., Nozaki, T., Winterhager, E., Yamamoto, H., Nakagama, H., Kamada, N., Suzuki, H., Ohta, T., Ohki, M., Masutani, M., Cross, J.C., Parp1-deficiency induces differentiation of ES cells into trophoblast derivatives. Dev. Biol. 257 (2003), 371–381.
17. Huang, D.W., Sherman, B.T., Lempicki, R.A., Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic acids research 37 (2009), 1–13.
18. Huang, D.W., Sherman, B.T., Lempicki, R.A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols 4 (2009), 44–57.
19. James, D., Noggle, S.A., Swigut, T., Brivanlou, A.H., Contribution of human embryonic stem cells to mouse blastocysts. Dev. Biol. 295 (2006), 90–102.
20. Kolodziejczyk, A.A., Kim, J.K., Tsang, J.C., Ilicic, T., Henriksson, J., Natarajan, K.N., Tuck, A.C., Gao, X., Bühler, M., Liu, P., et al. Single Cell RNA-Sequencing of Pluripotent States Unlocks Modular Transcriptional Variation. Cell Stem Cell 17 (2015), 471–485.
21. Kunath, T., Arnaud, D., Uy, G.D., Okamoto, I., Chureau, C., Yamanaka, Y., Heard, E., Gardner, R.L., Avner, P., Rossant, J., Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development 132 (2005), 1649–1661.
22. Lerdrup, M., Johansen, J.V., Agrawal-Singh, S., Hansen, K., An interactive environment for agile analysis and visualization of ChIP-sequencing data. Nature structural & molecular biology 23 (2016), 349–357.
23. Leung, C.Y., Zernicka-Goetz, M., Mapping the journey from totipotency to lineage specification in the mouse embryo. Curr. Opin. Genet. Dev. 34 (2015), 71–76.
24. Li, H., Durbin, R., Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 (2009), 1754–1760.
25. Li, P., Tong, C., Mehrian-Shai, R., Jia, L., Wu, N., Yan, Y., Maxson, R.E., Schulze, E.N., Song, H., Hsieh, C.L., et al. Germline competent embryonic stem cells derived from rat blastocysts. Cell 135 (2008), 1299–1310.
26. Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biology, 15, 2014, 550.
27. Macfarlan, T.S., Gifford, W.D., Driscoll, S., Lettieri, K., Rowe, H.M., Bonanomi, D., Firth, A., Singer, O., Trono, D., Pfaff, S.L., Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487 (2012), 57–63.
28. 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 78 (1981), 7634–7638.
29. Masaki, H., Kato-Itoh, M., Takahashi, Y., Umino, A., Sato, H., Ito, K., Yanagida, A., Nishimura, T., Yamaguchi, T., Hirabayashi, M., et al. Inhibition of Apoptosis Overcomes Stage-Related Compatibility Barriers to Chimera Formation in Mouse Embryos. Cell Stem Cell 19 (2016), 587–592.
30. Mascetti, V.L., Pedersen, R.A., Contributions of Mammalian Chimeras to Pluripotent Stem Cell Research. Cell Stem Cell 19 (2016), 163–175.
31. Mascetti, V.L., Pedersen, R.A., Human-Mouse Chimerism Validates Human Stem Cell Pluripotency. Cell Stem Cell 18 (2016), 67–72.
32. Morgani, S.M., Canham, M.A., Nichols, J., Sharov, A.A., Migueles, R.P., Ko, M.S., Brickman, J.M., Totipotent embryonic stem cells arise in ground-state culture conditions. Cell Rep. 3 (2013), 1945–1957.
33. Najm, F.J., Chenoweth, J.G., Anderson, P.D., Nadeau, J.H., Redline, R.W., McKay, R.D., Tesar, P.J., Isolation of epiblast stem cells from preimplantation mouse embryos. Cell Stem Cell 8 (2011), 318–325.
34. Nichols, J., Smith, A., Naive and primed pluripotent states. Cell Stem Cell 4 (2009), 487–492.
35. Nozaki, T., Fujimori, H., Wang, J., Suzuki, H., Imai, H., Watanabe, M., Ohura, K., Masutani, M., Parp-1 deficiency in ES cells promotes invasive and metastatic lesions accompanying induction of trophoblast giant cells during tumorigenesis in uterine environment. Pathol. Int. 63 (2013), 408–414.
36. Ockenga, W., Kühne, S., Bocksberger, S., Banning, A., Tikkanen, R., Non-neuronal functions of the m2 muscarinic acetylcholine receptor. Genes (Basel) 4 (2013), 171–197.
37. Ogino, H., Nozaki, T., Gunji, A., Maeda, M., Suzuki, H., Ohta, T., Murakami, Y., Nakagama, H., Sugimura, T., Masutani, M., Loss of Parp-1 affects gene expression profile in a genome-wide manner in ES cells and liver cells. BMC Genomics, 8, 2007, 41.
38. Papaioannou, V.E., Mkandawire, J., Biggers, J.D., Development and phenotypic variability of genetically identical half mouse embryos. Development 106 (1989), 817–827.
39. Pfaff, O., Hildebrandt, C., Waelbroeck, M., Hou, X., Moser, U., Mutschler, E., Lambrecht, G., The (S)-(+)-enantiomer of dimethindene: a novel M2-selective muscarinic receptor antagonist. Eur. J. Pharmacol. 286 (1995), 229–240.
40. Rossant, J., Cross, J.C., Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2 (2001), 538–548.
41. Rossant, J., Tam, P.P., New Insights into Early Human Development: Lessons for Stem Cell Derivation and Differentiation. Cell Stem Cell 20 (2017), 18–28.
42. Shen, L., Shao, N., Liu, X., Nestler, E., ngs. plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC genomics, 15, 2014, 284.
43. Tachibana, M., Sparman, M., Ramsey, C., Ma, H., Lee, H.S., Penedo, M.C., Mitalipov, S., Generation of chimeric rhesus monkeys. Cell 148 (2012), 285–295.
44. Takashima, Y., Guo, G., Loos, R., Nichols, J., Ficz, G., Krueger, F., Oxley, D., Santos, F., Clarke, J., Mansfield, W., et al. Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158 (2014), 1254–1269.
45. Tanaka, S., Kunath, T., Hadjantonakis, A.K., Nagy, A., Rossant, J., Promotion of trophoblast stem cell proliferation by FGF4. Science 282 (1998), 2072–2075.
46. Tang, F., Barbacioru, C., Nordman, E., Bao, S., Lee, C., Wang, X., Tuch, B.B., Heard, E., Lao, K., Surani, M.A., Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLoS ONE, 6, 2011, e21208.
47. Tarkowski, A.K., Experiments on the development of isolated blastomers of mouse eggs. Nature 184 (1959), 1286–1287.
48. Tesar, P.J., Chenoweth, J.G., Brook, F.A., Davies, T.J., Evans, E.P., Mack, D.L., Gardner, R.L., McKay, R.D., New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448 (2007), 196–199.
49. Theunissen, T.W., Powell, B.E., Wang, H., Mitalipova, M., Faddah, D.A., Reddy, J., Fan, Z.P., Maetzel, D., Ganz, K., Shi, L., et al. Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell 15 (2014), 471–487.
50. Theunissen, T.W., Friedli, M., He, Y., Planet, E., O'Neil, R.C., Markoulaki, S., Pontis, J., Wang, H., Iouranova, A., Imbeault, M., et al. Molecular Criteria for Defining the Naive Human Pluripotent State. Cell Stem Cell 19 (2016), 502–515.
51. 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 282 (1998), 1145–1147.
52. Trapnell, C., Pachter, L., Salzberg, S.L., TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 (2009), 1105–1111.
53. Vallier, L., Alexander, M., Pedersen, R.A., Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J. Cell Sci. 118 (2005), 4495–4509.
54. Wang, J., Xie, G., Singh, M., Ghanbarian, A.T., Raskó, T., Szvetnik, A., Cai, H., Besser, D., Prigione, A., Fuchs, N.V., et al. Primate-specific endogenous retrovirus-driven transcription defines naive-like stem cells. Nature 516 (2014), 405–409.
55. Ware, C.B., Nelson, A.M., Mecham, B., Hesson, J., Zhou, W., Jonlin, E.C., Jimenez-Caliani, A.J., Deng, X., Cavanaugh, C., Cook, S., et al. Derivation of naive human embryonic stem cells. Proc. Natl. Acad. Sci. USA 111 (2014), 4484–4489.
56. Wu, J., Izpisua Belmonte, J.C., The Molecular Harbingers of Early Mammalian Embryo Patterning. Cell 165 (2016), 13–15.
57. Wu, J., Okamura, D., Li, M., Suzuki, K., Luo, C., Ma, L., He, Y., Li, Z., Benner, C., Tamura, I., et al. An alternative pluripotent state confers interspecies chimaeric competency. Nature 521 (2015), 316–321.
58. Wu, J., Greely, H.T., Jaenisch, R., Nakauchi, H., Rossant, J., Belmonte, J.C., Stem cells and interspecies chimaeras. Nature 540 (2016), 51–59.
59. Wu, J., Platero-Luengo, A., Sakurai, M., Sugawara, A., Gil, M.A., Yamauchi, T., Suzuki, K., Bogliotti, Y.S., Cuello, C., Morales Valencia, M., et al. Interspecies chimerism with mammalian pluripotent stem cells. Cell 168 (2017), 473–486.e15.
60. Xue, Z., Huang, K., Cai, C., Cai, L., Jiang, C.Y., Feng, Y., Liu, Z., Zeng, Q., Cheng, L., Sun, Y.E., et al. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500 (2013), 593–597.
61. Yan, L., Yang, M., Guo, H., Yang, L., Wu, J., Li, R., Liu, P., Lian, Y., Zheng, X., Yan, J., et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 20 (2013), 1131–1139.
62. Yeom, Y.I., Fuhrmann, G., Ovitt, C.E., Brehm, A., Ohbo, K., Gross, M., Hübner, K., Schöler, H.R., Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122 (1996), 881–894.
63. Ying, Q.L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., Smith, A., The ground state of embryonic stem cell self-renewal. Nature 453 (2008), 519–523.
64. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., Model-based analysis of ChIP-Seq (MACS). Genome biology, 9, 2008, R137.