Deficiency of microRNA miR-34a expands cell fate potential in pluripotent stem cells

Science

Volumn 355, Issue 6325, 2017, Pages

  Choi, Yong Jin ^a   Lin, Chao Po ^a   Risso, Davide ^a   Chen, Sean ^a   Kim, Thomas Aquinas ^a   Tan, Meng How ^b   Li, Jin Billy ^b   Wu, Yalei ^c   Chen, Caifu ^d   Xuan, Zhenyu ^e   Macfarlan, Todd ^f   Peng, Weiqun ^g   Lloyd, K C Kent ^h   Kim, Sang Yong ⁱ   Speed, Terence P ^a,j,k   He, Lin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c Thermo Fisher Scientific   (United States)

^d INTEGRATED DNA TECHNOLOGIES   (United States)

^e UNIVERSITY OF TEXAS AT DALLAS   (United States)

^f EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^g GEORGE WASHINGTON UNIVERSITY   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^j UNIVERSITY OF MELBOURNE   (Australia)

^k WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; HEPATOCYTE NUCLEAR FACTOR 3BETA; MICRORNA 34A; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BRACHYURY; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; GATA2 PROTEIN, MOUSE; MICRORNA; MIRN34 MICRORNA, MOUSE;

CELLS AND CELL COMPONENTS; EMBRYO; EMBRYONIC DEVELOPMENT; GENE EXPRESSION; PROTEIN; RNA; RODENT; VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYOID BODY; ENDOGENOUS RETROVIRUS; FEMALE; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; INDUCED PLURIPOTENT STEM CELL; MOUSE; MOUSE EMBRYONIC STEM CELL; MUS MUSCULUS; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL EXPANSION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS EXPRESSION; VIRUS INDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; EMBRYONIC STEM CELL; GENETIC TRANSCRIPTION; GENETICS; MALE; METABOLISM; PHYSIOLOGY; VIRUS ACTIVATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; EMBRYONIC STEM CELLS; ENDOGENOUS RETROVIRUSES; FEMALE; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; INDUCED PLURIPOTENT STEM CELLS; MALE; METABOLIC NETWORKS AND PATHWAYS; MICE; MICE, INBRED C57BL; MICRORNAS; TRANSCRIPTION, GENETIC; VIRUS ACTIVATION;

EID: 85009454685     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aag1927     Document Type: Article

References (53)

1. M. J. Evans, M. H. Kaufman, Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156 (1981). doi: 10.1038/292154a0; pmid: 7242681
2. K. Takahashi, S. Yamanaka, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006). doi: 10.1016/j.cell.2006.07.024;pmid: 16904174
3. G. R. Martin, Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U.S.A. 78, 7634-7638 (1981). doi: 10.1073/pnas.78.12.7634; pmid: 6950406
4. R. S. Beddington, E. J. Robertson, An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 105, 733-737 (1989). pmid: 2598811
5. V. E. Papaioannou, J. Mkandawire, J. D. Biggers, Development and phenotypic variability of genetically identical half mouse embryos. Development 106, 817-827 (1989). pmid: 2562672
6. A. K. Tarkowski, Experiments on the development of isolated blastomers of mouse eggs. Nature 184, 1286-1287 (1959). doi: 10.1038/1841286a0; pmid: 13836947
7. T. S. Macfarlan et al., Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487,57-63 (2012). doi: 10.1038/nature11244; pmid:22722858
8. S. M. Morgani et al., Totipotent embryonic stem cells arise in ground-state culture conditions. Cell Rep. 3, 1945-1957 (2013). doi: 10.1016/j.celrep.2013.04.034; pmid: 23746443
9. T. Ishiuchi et al., Early embryonic-like cells are induced by downregulating replication-dependent chromatin assembly. Nat. Struct. Mol. Biol. 22, 662-671 (2015). doi: 10.1038/nsmb.3066; pmid: 26237512
10. M. Abad et al., Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502, 340-345 (2013). doi: 10.1038/nature12586; pmid: 24025773
11. M. Chekulaeva, W. Filipowicz, Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol. 21, 452-460 (2009). doi: 10.1016/j.ceb.2009.04.009; pmid: 19450959
12. S. L. Ameres, P. D. Zamore, Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 14, 475-488 (2013). doi: 10.1038/nrm3611; pmid: 23800994
13. C. Kanellopoulou et al., Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489-501 (2005). doi: 10.1101/gad.1248505; pmid: 15713842
14. R. L. Judson, J. E. Babiarz, M. Venere, R. Blelloch, Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat. Biotechnol. 27, 459-461 (2009). doi: 10.1038/nbt.1535; pmid: 19363475
15. S. R. Viswanathan, G. Q. Daley, Lin28: A microRNA regulator with a macro role. Cell 140, 445-449 (2010). doi: 10.1016/j.cell.2010.02.007; pmid: 20178735
16. S. R. Viswanathan et al., microRNA expression during trophectoderm specification. PLOS ONE 4, e6143 (2009). doi: 10.1371/journal.pone.0006143; pmid: 19582159
17. Y. J. Choi et al., miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat. Cell Biol. 13, 1353-1360 (2011). doi: 10.1038/ncb2366; pmid: 22020437
18. N. Okada et al., A positive feedback between p53 and miR-34 miRNAs mediates tumor suppression. Genes Dev. 28, 438-450 (2014). doi: 10.1101/gad.233585.113; pmid: 24532687
19. T.-C. Chang et al., Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 26, 745-752 (2007). doi: 10.1016/j.molcel.2007.05.010; pmid: 17540599
20. N. Raver-Shapira et al., Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 26, 731-743 (2007). doi: 10.1016/j.molcel.2007.05.017; pmid: 17540598
21. L. He et al., A microRNA component of the p53 tumour suppressor network. Nature 447, 1130-1134 (2007). doi: 10.1038/nature05939; pmid: 17554337
22. H. Tazawa, N. Tsuchiya, M. Izumiya, H. Nakagama, Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc. Natl. Acad. Sci. U.S.A. 104, 15472-15477 (2007). doi: 10.1073/pnas.0707351104; pmid: 17875987
23. H. Niwa et al., Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123, 917-929 (2005). doi: 10.1016/j.cell.2005.08.040; pmid: 16325584
24. M. Giakoumopoulos, T. G. Golos, Embryonic stem cell-derived trophoblast differentiation: A comparative review of the biology, function, and signaling mechanisms. J. Endocrinol. 216, R33-R45 (2013). doi: 10.1530/JOE-12-0433; pmid: 23291503
25. J. Artus, A. Piliszek, A.-K. Hadjantonakis, The primitive endoderm lineage of the mouse blastocyst: Sequential transcription factor activation and regulation of differentiation by Sox17. Dev. Biol. 350, 393-404 (2011). doi: 10.1016/j.ydbio.2010.12.007; pmid: 21146513
26. D. G. Simmons, A. L. Fortier, J. C. Cross, Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 304, 567-578 (2007). doi: 10.1016/j.ydbio.2007.01.009; pmid: 17289015
27. C. Kubaczka et al., Direct induction of trophoblast stem cells from murine fibroblasts. Cell Stem Cell 17, 557-568 (2015). doi: 10.1016/j.stem.2015.08.005; pmid: 26412560
28. H. Benchetrit et al., Extensive nuclear reprogramming underlies lineage conversion into functional trophoblast stem-like cells. Cell Stem Cell 17, 543-556 (2015). doi: 10.1016/j.stem.2015.08.006; pmid: 26412562
29. D. Kigami, N. Minami, H. Takayama, H. Imai, MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol. Reprod. 68, 651-654 (2003). doi: 10.1095/biolreprod.102.007906; pmid: 12533431
30. A. E. Peaston et al., Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell 7, 597-606 (2004). doi: 10.1016/j.devcel.2004.09.004; pmid: 15469847
31. A. V. Evsikov et al., Systems biology of the 2-cell mouse embryo. Cytogenet. Genome Res. 105, 240-250 (2004). doi: 10.1159/000078195; pmid: 15237213
32. L. Bénit, J. B. Lallemand, J. F. Casella, H. Philippe, T. Heidmann, ERV-L elements: A family of endogenous retrovirus-like elements active throughout the evolution of mammals. J. Virol. 73, 3301-3308 (1999). pmid: 10074184
33. J. Nichols et al., Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391 (1998). doi: 10.1016/S0092-8674(00)81769-9; pmid: 9814708
34. T. S. Macfarlan et al., Endogenous retroviruses and neighboring genes are coordinately repressed by LSD1/KDM1A. Genes Dev. 25, 594-607 (2011). doi: 10.1101/gad.2008511; pmid: 21357675
35. Z. Xue et al., Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500, 593-597 (2013). doi: 10.1038/nature12364; pmid: 23892778
36. F. Tang et al., Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLOS ONE 6, e21208 (2011). doi: 10.1371/journal.pone.0021208; pmid: 21731673
37. I. A. Maksakova et al., Distinct roles of KAP1, HP1 and G9a/GLP in silencing of the two-cell-specific retrotransposon MERVL in mouse ES cells. Epigenetics Chromatin 6, 15 (2013). doi: 10.1186/1756-8935-6-15; pmid: 23735015
38. M. Hayashi et al., Chd5 regulates MuERV-L/MERVL expression in mouse embryonic stem cells via H3K27me3 modification and histone H3.1/H3.2. J. Cell. Biochem. 117, 780-792 (2016). doi: 10.1002/jcb.25368; pmid: 26359639
39. P. Loher, I. Rigoutsos, Interactive exploration of RNA22 microRNA target predictions. Bioinformatics 28, 3322-3323 (2012). doi: 10.1093/bioinformatics/bts615; pmid: 23074262
40. C. Zhang, X. Ye, H. Zhang, M. Ding, H. Deng, GATA factors induce mouse embryonic stem cell differentiation toward extraembryonic endoderm. Stem Cells Dev. 16, 605-613 (2007). doi: 10.1089/scd.2006.0077; pmid: 17784834
41. S. H. Orkin, GATA-binding transcription factors in hematopoietic cells. Blood 80, 575-581 (1992). pmid: 1638017
42. M. Suzuki et al., GATA factor switching from GATA2 to GATA1 contributes to erythroid differentiation. Genes Cells 18, 921-933 (2013). doi: 10.1111/gtc.12086; pmid: 23911012
43. K. Piotrowska-Nitsche, A. Perea-Gomez, S. Haraguchi, M. Zernicka-Goetz, Four-cell stage mouse blastomeres have different developmental properties. Development 132, 479-490 (2005). doi: 10.1242/dev.01602; pmid: 15634695
44. I. Tabansky et al., Developmental bias in cleavage-stage mouse blastomeres. Curr. Biol. 23, 21-31 (2013). doi: 10.1016/j.cub.2012.10.054; pmid: 23177476
45. K. Cockburn, J. Rossant, Making the blastocyst: Lessons from the mouse. J. Clin. Invest. 120, 995-1003 (2010). doi: 10.1172/JCI41229; pmid: 20364097
46. I. Wilmut, A. E. Schnieke, J. McWhir, A. J. Kind, K. H. Campbell, Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810-813 (1997). doi: 10.1038/385810a0; pmid: 9039911
47. J. Wang et al., Primate-specific endogenous retrovirus-driven transcription defines naive-like stem cells. Nature 516, 405-409 (2014). doi: 10.1038/nature13804; pmid: 25317556
48. T. W. Theunissen et al., Molecular criteria for defining the naive human pluripotent state. Cell Stem Cell 19, 502-515 (2016). doi: 10.1016/j.stem.2016.06.011; pmid: 27424783
49. -/- embryos. Development 124, 279-287 (1997). pmid: 9053305
50. K.-H. Baek et al., Embryonic demise caused by targeted disruption of a cysteine protease Dub-2. PLOS ONE 7, e44223 (2012). doi: 10.1371/journal.pone.0044223; pmid: 22984479
51. C. P. Concepcion et al., Intact p53-dependent responses in miR-34-deficient mice. PLOS Genet. 8, e1002797 (2012). doi: 10.1371/journal.pgen.1002797; pmid: 22844244
52. P. Svoboda et al., RNAi and expression of retrotransposons MuERV-L and IAP in preimplantation mouse embryos. Dev. Biol. 269, 276-285 (2004). doi: 10.1016/j.ydbio.2004.01.028; pmid: 15081373
53. J. Rossant, Postimplantation development of blastomeres isolated from 4- and 8-cell mouse eggs. J. Embryol. Exp. Morphol. 36, 283-290 (1976). pmid: 1033982 2017