SCNT versus iPSCs: Proteins and small molecules in reprogramming

International Journal of Developmental Biology

Volumn 59, Issue 4-6, 2015, Pages 179-186

  Han, Fei ^a   Li, Xia ^a   Song, Dandan ^a   Jiang, Shaoshuai ^a   Xu, Qun ^a   Zhang, Yunhai ^a  

^a ANHUI AGRICULTURAL UNIVERSITY   (China)

Author keywords

Differentiation; Early embryo; iPSC; Oocyte; Protein; SCNT; Small molecule

Indexed keywords

ASCORBIC ACID; BONE MORPHOGENETIC PROTEIN; GROWTH DIFFERENTIATION FACTOR 9; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR SOX2; KRUPPEL LIKE FACTOR; TRANSCRIPTION FACTOR SOX;

CELL DIFFERENTIATION; CELL FATE; CELL NUCLEUS TRANSPLANTATION; CELL PROLIFERATION; CYTOLOGY; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FIBROBLAST; HIGH THROUGHPUT SEQUENCING; HUMAN; IMMUNOGENICITY; MOLECULE; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEAR REPROGRAMMING; OOCYTE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; REVIEW; SOMATIC CELL; SOMATIC CELL NUCLEAR TRANSPLANTATION; ANIMAL; CELL REPROGRAMMING TECHNIQUE; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PROCEDURES;

ANIMALS; CELLULAR REPROGRAMMING; CELLULAR REPROGRAMMING TECHNIQUES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; NUCLEAR TRANSFER TECHNIQUES; OCTAMER TRANSCRIPTION FACTOR-3; PROTO-ONCOGENE PROTEINS C-MYC; SOXB1 TRANSCRIPTION FACTORS;

EID: 84944216049     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.150042fh     Document Type: Review

References (94)

1. AMIT, M., CARPENTER, M.K., INOKUMA, M.S., CHIU, C.P., HARRIS, C.P., WAKNITZ, M.A., ITSKOVITZ-ELDOR, J. and THOMSON, J.A. (2000). Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 227: 271-278.
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. et al., (1999). Production of goats by somatic cell nuclear transfer. Nat Biotech 17: 456-461.
3. BARRIOS, F., IRIE, N. and SURANI, M.A. (2013). Perceiving signals, building networks, reprogramming germ cell fate. Int J Dev Biol 57: 123-132.
4. BETTHAUSER, J., FORSBERG, E., AUGENSTEIN, M., CHILDS, L., EILERTSEN, K., ENOS, J., FORSYTHE, T., GOLUEKE, P., JURGELLA, G., KOPPANG, R. et al., (2000). Production of cloned pigs from in vitro systems. Nat Biotechnol 18: 1055-1059.
5. BUGANIM, Y., MARKOULAKI, S., VAN WIETMARSCHEN, N., HOKE, H., WU, T., GANZ, K., AKHTAR-ZAIDI, B., HE, Y., ABRAHAM, B.J., PORUBSKY, D. et al., (2014). The developmental potential of iPSCs is greatly influenced by reprogramming factor selection. Cell Stem Cell 15: 295-309.
6. BUI, H.T., KWON, D.N., KANG, M.H., OH, M.H., PARK, M.R., PARK, W.J., PAIK, S.S., VAN THUAN, N. and KIM, J.H. (2012). Epigenetic reprogramming in somatic cells induced by extract from germinal vesicle stage pig oocytes. Development 139: 4330-4340.
7. BUI, H.T., WAKAYAMA, S., KISHIGAMI, S., KIM, J.H., VAN THUAN, N. and WAKAYAMA, T. (2008). The cytoplasm of mouse germinal vesicle stage oocytes can enhance somatic cell nuclear reprogramming. Development 135: 3935-3945.
8. BYRNE, J.A., SIMONSSON, S., WESTERN, P.S. and GURDON, J.B. (2003). Nuclei of adult mammalian somatic cells are directly reprogrammed to oct-4 stem cell gene expression by amphibian oocytes. Curr Biol 13: 1206-1213.
9. CAMPBELL, K.H., FISHER, P., CHEN, W.C., CHOI, I., KELLY, R.D., LEE, J.H. and XHU, J. (2007). Somatic cell nuclear transfer: Past, present and future perspectives. Theriogenology 1: 3.
10. CHEN, J., GUO, L., ZHANG, L., WU, H., YANG, J., LIU, H., WANG, X., HU, X., GU, T., ZHOU, Z. et al., (2013a). Vitamin C modulates TET1 function during somatic cell reprogramming. Nat Genet 45: 1504-1509.
11. CHEN, J., LIU, H., LIU, J., QI, J., WEI, B., YANG, J., LIANG, H., CHEN, Y., WU, Y., GUO, L. et al., (2013b). H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat Genet 45: 34-42.
12. CHEN, J., LIU, J., YANG, J., CHEN, Y., CHEN, J., NI, S., SONG, H., ZENG, L., DING, K. and PEI, D. (2011). BMPs functionally replace Klf4 and support efficient reprogramming of mouse fibroblasts by Oct4 alone. Cell Res 21: 205-212.
13. CHESNE, P., ADENOT, P.G., VIGLIETTA, C., BARATTE, M., BOULANGER, L. and RENARD, J.-P. (2002). Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat Biotech 20: 366-369.
14. 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. et al., (2010). Induction of pluripotent stem cells from adult somatic cells by protein-based reprogramming without genetic manipulation. Blood 116: 386-395.
15. CHUNG, Y.G., EUM, J.H., LEE, J.E., SHIM, S.H., SEPILIAN, V., HONG, S.W., LEE, Y., TREFF, N.R., CHOI, Y.H., KIMBREL, E.A. et al., (2014). Human somatic cell nuclear transfer using adult cells. Cell Stem Cell 14: 777-780.
16. CIBELLI, J.B. (2014). Human somatic cell nuclear transfer is alive and well. Cell Stem Cell 14: 699-701.
17. CIBELLI, J.B., STICE, S.L., GOLUEKE, P.J., KANE, J.J., JERRY, J., BLACKWELL, C., PONCE DE LEON, F.A. and ROBL, J.M. (1998). Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science 280: 1256-1258.
18. EGUCHI, A., LEE, G.O., WAN, F., ERWIN, G.S. and ANSARI, A.Z. (2014). Controlling gene networks and cell fate with precision-targeted DNA-binding proteins and small-molecule-based genome readers. Biochem J 462: 397-413.
19. ESTEBAN, M.A., WANG, T., QIN, B., YANG, J., QIN, D., CAI, J., LI, W., WENG, Z., CHEN, J., NI, S. et al., (2010). Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6: 71-79.
20. ESTEBAN, M.A., XU, J., YANG, J., PENG, M., QIN, D., LI, W., JIANG, Z., CHEN, J., DENG, K., ZHONG, M. et al., (2009). Generation of induced pluripotent stem cell lines from Tibetan miniature pig. J Biol Chem 284: 17634-17640.
21. EVANS, M.J. and KAUFMAN, M.H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156.
22. GALLI, C., LAGUTINA, I., CROTTI, G., COLLEONI, S., TURINI, P., PONDERATO, N., DUCHI, R. and LAZZARI, G. (2003). Pregnancy: A cloned horse born to its dam twin. Nature 424: 635-635.
23. GARDNER, R.L. and BROOK, F.A. (1997). Reflections on the biology of embryonic stem (ES) cells. Int J Dev Biol 41: 235-243.
24. GONZALEZ-MUNOZ, E., ARBOLEDA-ESTUDILLO, Y., OTU, H.H. and CIBELLI, J.B. (2014). Cell reprogramming. Histone chaperone ASF1A is required for maintenance of pluripotency and cellular reprogramming. Science 345: 822-825.
25. GURDON, J.B. (1962). The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J Embryol Exp Morphol 10: 622-640.
26. HAMATANI, T., YAMADA, M., AKUTSU, H., KUJI, N., MOCHIMARU, Y., TAKANO, M., TOYODA, M., MIYADO, K., UMEZAWA, A. and YOSHIMURA, Y. (2008). What can we learn from gene expression profiling of mouse oocytes? Reproduction 135: 581-92.
27. HAN, J., YUAN, P., YANG, H., ZHANG, J., SOH, B.S., LI, P., LIM, S.L., CAO, S., TAY, J., ORLOV, Y.L. et al., (2010). Tbx3 improves the germ-line competency of induced pluripotent stem cells. Nature 463: 1096-1100.
28. HANNA, J., CHENG, A.W., SAHA, K., KIM, J., LENGNER, C.J., SOLDNER, F., CASSADY, J.P., MUFFAT, J., CAREY, B.W. and JAENISCH, R. (2010). Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci USA 107: 9222-9227.
29. HOCKEMEYER, D., SOLDNER, F., BEARD, C., GAO, Q., MITALIPOVA, M., DEKELVER, R.C., KATIBAH, G.E., AMORA, R., BOYDSTON, E.A., ZEITLER, B. et al., (2009). Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol 27: 851-857.
30. HOU, P., LI, Y., ZHANG, X., LIU, C., GUAN, J., LI, H., ZHAO, T., YE, J., YANG, W., LIU, K. et al., (2013). Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341: 651-654.
31. HUMPHREY, R.K., BEATTIE, G.M., LOPEZ, A.D., BUCAY, N., KING, C.C., FIRPO, M.T., ROSE-JOHN, S. and HAYEK, A. (2004). Maintenance of pluripotency in human embryonic stem cells is STAT3 independent. Stem Cells 22: 522-530.
32. ICHIDA, J.K.T.C.W.J., WILLIAMS, L.A., CARTER, A.C., SHI, Y., MOURA, M.T., ZILLER, M., SINGH, S., AMABILE, G., BOCK, C. et al., (2014). Notch inhibition allows oncogene-independent generation of iPS cells. Nat Chem Biol 10: 632-639
33. IRIE, N., WEINBERGER, L., TANG, W.W., KOBAYASHI, T., VIUKOV, S., MANOR, Y.S., DIETMANN, S., HANNA, J.H. and SURANI, M.A. (2015). SOX17 is a critical specifier of human primordial germ cell fate. Cell 160: 253-268.
34. 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. et al., (2009). Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4: 472-476.
35. KIMURA, T., KAGA, Y., SEKITA, Y., FUJIKAWA, K., NAKATANI, T., ODAMOTO, M., FUNAKI, S., IKAWA, M., ABE, K. and NAKANO, T. (2015). Pluripotent stem cells derived from mouse primordial germ cells by small molecule compounds. Stem Cells 33: 45-55.
36. KOCABAS, A.M., CROSBY, J., ROSS, P.J., OTU, H.H., BEYHAN, Z., CAN, H., TAM, W.L., ROSA, G.J., HALGREN, R.G., LIM, B. et al., (2006). The transcriptome of human oocytes. Proc Natl Acad Sci USA 103: 14027-14032.
37. KONG, Q., XIE, B., LI, J., HUAN, Y., HUANG, T., WEI, R., LV, J., LIU, S. and LIU, Z. (2014). Identification and characterization of an oocyte factor required for porcine nuclear reprogramming. J Biol Chem 289: 6960-6968.
38. KRUEGER, W.H., SWANSON, L.C., TANASIJEVIC, B. and RASMUSSEN, T.P. (2010). Natural and artificial routes to pluripotency. Int J Dev Biol 54: 1545-1564.
39. KRUPALNIK, V. and HANNA, J.H. (2014). Stem cells: The quest for the perfect reprogrammed cell. Nature 511: 160-162.
40. KUMAR, R., DIMENNA, L., SCHRODE, N., LIU, T.C., FRANCK, P., MUNOZ-DESCALZO, S., HADJANTONAKIS, A.K., ZARRIN, A.A., CHAUDHURI, J., ELEMENTO, O. et al., (2013). AID stabilizes stem-cell phenotype by removing epigenetic memory of pluripotency genes. Nature 500: 89-92.
41. LEE, B.C., KIM, M.K., JANG, G., OH, H.J., YUDA, F., KIM, H.J., SHAMIM, M.H., KIM, J.J., KANG, S.K., SCHATTEN, G. et al., (2005). Dogs cloned from adult somatic cells. Nature 436: 641-641.
42. LEE, J., SAYED, N., HUNTER, A., AU, K.F., WONG, W.H., MOCARSKI, E.S., PERA, R.R., YAKUBOV, E. and COOKE, J.P. (2012). Activation of innate immunity is required for efficient nuclear reprogramming. Cell 151: 547-558.
43. LEE, J.H., LEE, J.B., SHAPOVALOVA, Z., FIEBIG-COMYN, A., MITCHELL, R.R., LARONDE, S., SZABO, E., BENOIT, Y.D. and BHATIA, M. (2014). Somatic transcriptome priming gates lineage-specific differentiation potential of human-induced pluripotent stem cell states. Nat Commun 5: 5605.
44. LI, X., ZHANG, P., WEI, C. and ZHANG, Y. (2014). Generation of pluripotent stem cells via protein transduction. Int. J. Dev. Biol 58: 21-27.
45. LI, Y., ZHANG, Q., YIN, X., YANG, W., DU, Y., HOU, P., GE, J., LIU, C., ZHANG, W., ZHANG, X. et al., (2011). Generation of iPSCs from mouse fibroblasts with a single gene, Oct4, and small molecules. Cell Res 21: 196-204.
46. LI, Z., SUN, X., CHEN, J., LIU, X., WISELY, S.M., ZHOU, Q., RENARD, J.-P., LENO, G.H. and ENGELHARDT, J.F. (2006). Cloned ferrets produced by somatic cell nuclear transfer. Dev Biol. 293: 439-448.
47. LIANG, P., LAN, F., LEE, A.S., GONG, T., SANCHEZ-FREIRE, V., WANG, Y., DIECKE, S., SALLAM, K., KNOWLES, J.W., WANG, P.J. et al., (2013). Drug screening using a library of human induced pluripotent stem cell-derived cardiomyocytes reveals disease-specific patterns of cardiotoxicity. Circulation 127: 1677-1691.
48. LIN, T., AMBASUDHAN, R., YUAN, X., LI, W., HILCOVE, S., ABUJAROUR, R., LIN, X., HAHM, H.S., HAO, E., HAYEK, A. et al., (2009). A chemical platform for improved induction of human iPSCs. Nat Methods 6: 805-808.
49. LIU, X., SUN, H., QI, J., WANG, L., HE, S., LIU, J., FENG, C., CHEN, C., LI, W., GUO, Y. et al., (2013). Sequential introduction of reprogramming factors reveals a time-sensitive requirement for individual factors and a sequential EMT-MET mechanism for optimal reprogramming. Nat Cell Biol 15: 829-838.
50. MAEKAWA, M., YAMAGUCHI, K., NAKAMURA, T., SHIBUKAWA, R., KODANAKA, I., ICHISAKA, T., KAWAMURA, Y., MOCHIZUKI, H., GOSHIMA, N. and YAMANAKA, S. (2011). Direct reprogramming of somatic cells is promoted by maternal transcription factor Glis1. Nature 474: 225-229.
51. MARTINS-TAYLOR, K. and XU, R.H. (2012). Concise review: Genomic stability of human induced pluripotent stem cells. Stem Cells 30: 22-27.
52. MARUOTTI, J., JOUNEAU, A. and RENARD, J.P. (2010). Faithful reprogramming to pluripotency in mammals - what does nuclear transfer teach us? Int J Dev Biol 54: 1609-1621.
53. MIYAMOTO, K., NAGAI, K., KITAMURA, N., NISHIKAWA, T., IKEGAMI, H., BINH, N.T., TSUKAMOTO, S., MATSUMOTO, M., TSUKIYAMA, T., MINAMI, N. et al., (2011). Identification and characterization of an oocyte factor required for development of porcine nuclear transfer embryos. Proc Natl Acad Sci USA 108: 7040-705.
54. MIYAMOTO, K., TEPEREK, M., YUSA, K., ALLEN, G.E., BRADSHAW, C.R. and GURDON, J.B. (2013). Nuclear Wave1 is required for reprogramming transcription in oocytes and for normal development. Science 341: 1002-1005.
55. MIYOSHI, N., ISHII, H., NAGANO, H., HARAGUCHI, N., DEWI, D.L., KANO, Y., NISHIKAWA, S., TANEMURA, M., MIMORI, K., TANAKA, F. et al., (2011). Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 8: 633-638.
56. NICHOLS, J. and SMITH, A. (2009). Naive and primed pluripotent states. Cell Stem Cell 4: 487-492.
57. OKITA, K., ICHISAKA, T. and YAMANAKA, S. (2007). Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317.
58. OKITA, K., MATSUMURA, Y., SATO, Y., OKADA, A., MORIZANE, A., OKAMOTO, S., HONG, H., NAKAGAWA, M., TANABE, K., TEZUKA, K. et al., (2011). A more efficient method to generate integration-free human iPS cells. Nat Methods 8: 409-412.
59. OKITA, K., NAKAGAWA, M., HYENJONG, H., ICHISAKA, T. and YAMANAKA, S. (2008). Generation of mouse induced pluripotent stem cells without viral vectors. Science 322: 949-953.
60. PARADIS, F., NOVAK, S., MURDOCH, G.K., DYCK, M.K., DIXON, W.T. and FOXCROFT, G.R. (2009). Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction 138: 115-129.
61. PARK, I.-H., ARORA, N., HUO, H., MAHERALI, N., AHFELDT, T., SHIMAMURA, A., LENSCH, M.W., COWAN, C., HOCHEDLINGER, K. and DALEY, G.Q. (2008). Disease-Specific Induced Pluripotent Stem Cells. Cell 134: 877-886.
62. PETERS, A., BURRIDGE, P.W., PRYZHKOVA, M.V., LEVINE, M.A., PARK, T.S., ROXBURY, C., YUAN, X., PEAULT, B. and ZAMBIDIS, E.T. (2010). Challenges and strategies for generating therapeutic patient-specific hemangioblasts and hematopoietic stem cells from human pluripotent stem cells. Int J Dev Biol 54: 965-990.
63. 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. et al., (2000). Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407: 86-90.
64. POLO, J.M., LIU, S., FIGUEROA, M.E., KULALERT, W., EMINLI, S., TAN, K.Y., APOSTOLOU, E., STADTFELD, M., LI, Y., SHIODA, T. et al., (2010). Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotech 28: 848-855.
65. RODRIGUEZ, A., ALLEGRUCCI, C. and ALBERIO, R. (2012). Modulation of pluripotency in the porcine embryo and iPS cells. PLoS One 7: 8
66. SAMAVARCHI-TEHRANI, P., GOLIPOUR, A., DAVID, L., SUNG, H.K., BEYER, T.A., DATTI, A., WOLTJEN, K., NAGY, A. and WRANA, J.L. (2010). Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 7: 64-77.
67. SHI, D., LU, F., WEI, Y., CUI, K., YANG, S., WEI, J. and LIU, Q. (2007). Buffalos (Bubalus bubalis) cloned by nuclear transfer of somatic cells. Biol Reprod 77: 285-91.
68. SHIN, T., KRAEMER, D., PRYOR, J., LIU, L., RUGILA, J., HOWE, L., BUCK, S., MURPHY, K., LYONS, L. and WESTHUSIN, M. (2002). A cat cloned by nuclear transplantation. Nature 415: 859.
69. SHINAGAWA, T., TAKAGI, T., TSUKAMOTO, D., TOMARU, C., HUYNH, L.M., SIVARAMAN, P., KUMAREVEL, T., INOUE, K., NAKATO, R., KATOU, Y. et al., (2013). Histone variants enriched in oocytes enhance reprogramming to induced pluripotent stem cells. Cell Stem Cell 14: 217-227.
70. SHU, J., ZHANG, K., ZHANG, M., YAO, A., SHAO, S., DU, F., YANG, C., CHEN, W., WU, C., YANG, W. et al., (2015). GATA family members as inducers for cellular reprogramming to pluripotency. Cell Res 25: 169-180.
71. SILVA, J., BARRANDON, O., NICHOLS, J., KAWAGUCHI, J., THEUNISSEN, T.W. and SMITH, A. (2008). Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol 6: e253.
72. SONG, Y., HAI, T., WANG, Y., GUO, R., LI, W., WANG, L. and ZHOU, Q. (2013). 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 5: 382-393.
73. STADTFELD, M., NAGAYA, M., UTIKAL, J., WEIR, G. and HOCHEDLINGER, K. (2008). Induced pluripotent stem cells generated without viral integration. Science 322: 945-949.
74. TACHIBANA, M., AMATO, P., SPARMAN, M., GUTIERREZ, N.M., TIPPNER-HEDGES, R., MA, H., KANG, E., FULATI, A., LEE, H.S., SRITANAUDOMCHAI, H. et al., (2013). Human embryonic stem cells derived by somatic cell nuclear transfer. Cell 153: 1228-1238.
75. TAKAHASHI, K., TANABE, K., OHNUKI, M., NARITA, M., ICHISAKA, T., TOMODA, K. and YAMANAKA, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
76. TAKAHASHI, K. and YAMANAKA, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
77. THOMSON, J.A., ITSKOVITZ-ELDOR, J., SHAPIRO, S.S., WAKNITZ, M.A., SWIERGIEL, J.J., MARSHALL, V.S. and JONES, J.M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
78. TSUBOOKA, N., ICHISAKA, T., OKITA, K., TAKAHASHI, K., NAKAGAWA, M. and YAMANAKA, S. (2009). Roles of Sall4 in the generation of pluripotent stem cells from blastocysts and fibroblasts. Genes Cells 14: 683-694.
79. WAKAYAMA, T., PERRY, A.C.F., ZUCCOTTI, M., JOHNSON, K.R. and YANAGIMACHI, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394: 369-374.
80. WANG, J., GU, Q., HAO, J., JIA, Y., XUE, B., JIN, H., MA, J., WEI, R., HAI, T., KONG, Q. et al., (2013). Tbx3 and Nr5alpha2 play important roles in pig pluripotent stem cells. Stem Cell Rev 9: 700-708.
81. WANG, T., CHEN, K., ZENG, X., YANG, J., WU, Y., SHI, X., QIN, B., ZENG, L., ESTEBAN, M.A., PAN, G. et al., (2011). The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell 9: 575-587.
82. 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., (2014). Derivation of naive human embryonic stem cells. Proc Natl Acad Sci USA 111: 4484-4489.
83. WARREN, L., MANOS, P.D., AHFELDT, T., LOH, Y.H., LI, H., LAU, F., EBINA, W., MANDAL, P.K., SMITH, Z.D., MEISSNER, A. et al., (2010). Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7: 618-630.
84. WEN, D., BANASZYNSKI, L.A., LIU, Y., GENG, F., NOH, K.M., XIANG, J., ELEMENTO, O., ROSENWAKS, Z., ALLIS, C.D. and RAFII, S. (2014). Histone variant H3.3 is an essential maternal factor for oocyte reprogramming. Proc Natl Acad Sci USA 111: 7325-30.
85. WILMUT, I., SCHNIEKE, A.E., MCWHIR, J., KIND, A.J. and CAMPBELL, K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385: 810-813.
86. XU, R.H., CHEN, X., LI, D.S., LI, R., ADDICKS, G.C., GLENNON, C., ZWAKA, T.P. and THOMSON, J.A. (2002). BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol. 20: 1261-1264.
87. YAMADA, M., JOHANNESSON, B., SAGI, I., BURNETT, L.C., KORT, D.H., PROSSER, R.W., PAULL, D., NESTOR, M.W., FREEBY, M., GREENBERG, E. et al., (2014). Human oocytes reprogram adult somatic nuclei of a type 1 diabetic to diploid pluripotent stem cells. Nature 510: 533-536.
88. YING, Q.L., NICHOLS, J., CHAMBERS, I. and SMITH, A. (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115: 281-292.
89. YU, C., LIU, Y., MA, T., LIU, K., XU, S., ZHANG, Y., LIU, H., LA RUSSA, M., XIE, M., DING, S. et al., (2015). Small molecules enhance CRISPR genome editing in pluripotent stem cells. Cell Stem Cell 16: 142-147.
90. YU, J., HU, K., SMUGA-OTTO, K., TIAN, S., STEWART, R., SLUKVIN, II and THOMSON, J.A. (2009). Human induced pluripotent stem cells free of vector and transgene sequences. Science 324: 797-801.
91. YU, J., VODYANIK, M.A., SMUGA-OTTO, K., ANTOSIEWICZ-BOURGET, J., FRANE, J.L., TIAN, S., NIE, J., JONSDOTTIR, G.A., RUOTTI, V., STEWART, R. et al., (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
92. ZHANG, Y., WEI, C., ZHANG, P., LI, X., LIU, T., PU, Y., LI, Y., CAO, Z., CAO, H., LIU, Y. et al., (2014). Efficient reprogramming of naive-like induced pluripotent stem cells from porcine adipose-derived stem cells with a feeder-independent and serum-free system. PLoS One 9: e85089.
93. ZHAO, T., ZHANG, Z.N., RONG, Z. and XU, Y. (2011). Immunogenicity of induced pluripotent stem cells. Nature 474: 212-215.
94. ZHOU, Q., RENARD, J.P., LE FRIEC, G., BROCHARD, V., BEAUJEAN, N., CHERIFI, Y., FRAICHARD, A. and COZZI, J. (2003). Generation of fertile cloned rats by regulating oocyte activation. Science 302: 1179.