DUSP9 Modulates DNA Hypomethylation in Female Mouse Pluripotent Stem Cells

Cell Stem Cell

Volumn 20, Issue 5, 2017, Pages 706-719.e7

  Choi, Jiho ^a,b,c   Clement, Kendell ^b,c,d   Huebner, Aaron J ^a,b,c   Webster, Jamie ^b,c,d   Rose, Christopher M ^e   Brumbaugh, Justin ^a,b,c   Walsh, Ryan M ^a,b,c   Lee, Soohyun ^e   Savol, Andrej ^a   Etchegaray, Jean Pierre ^a   Gu, Hongcang ^d   Boyle, Patrick ^d   Elling, Ulrich ^f   Mostoslavsky, Raul ^a   Sadreyev, Ruslan ^a   Park, Peter J ^e   Gygi, Steven P ^e   Meissner, Alexander ^b,c,d   Hochedlinger, Konrad ^a,b,c  

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

^c Harvard University   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

cell fusion; DNA methylation; Dusp9; embryonic germ cells; embryonic stem cells; genomic imprinting; inner cell mass; pluripotency; primordial germ cells; X chromosome

Indexed keywords

DUSP9 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; DUAL SPECIFICITY PHOSPHATASE; DUSP9 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; AUTOSOME; BLASTOCYST; CELL FUSION; CONTROLLED STUDY; DNA METHYLATION; EMBRYONIC GERM CELL; EMBRYONIC STEM CELL; EPIGENETICS; FEMALE; GENETIC DIFFERENCE; GENETIC SIMILARITY; HYBRID; MALE; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; UPREGULATION; X CHROMOSOME; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; DRUG EFFECTS; GENETICS; GENOME IMPRINTING; METABOLISM; PHYSIOLOGY;

ANIMALS; BLASTOCYST; DNA METHYLATION; DUAL-SPECIFICITY PHOSPHATASES; EMBRYONIC GERM CELLS; EMBRYONIC STEM CELLS; FEMALE; GENOMIC IMPRINTING; MALE; MICE; MODELS, BIOLOGICAL; PLURIPOTENT STEM CELLS; X CHROMOSOME;

EID: 85016470234     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2017.03.002     Document Type: Article

References (60)

1. Anders, S., McCarthy, D.J., Chen, Y., Okoniewski, M., Smyth, G.K., Huber, W., Robinson, M.D., Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat. Protoc. 8 (2013), 1765–1786.
2. Beard, C., Hochedlinger, K., Plath, K., Wutz, A., Jaenisch, R., Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis 44 (2006), 23–28.
3. Boulard, M., Edwards, J.R., Bestor, T.H., FBXL10 protects Polycomb-bound genes from hypermethylation. Nat. Genet. 47 (2015), 479–485.
4. Burgoyne, P.S., A Y-chromosomal effect on blastocyst cell number in mice. Development 117 (1993), 341–345.
5. Carlone, D.L., Lee, J.-H., Young, S.R.L., Dobrota, E., Butler, J.S., Ruiz, J., Skalnik, D.G., Reduced genomic cytosine methylation and defective cellular differentiation in embryonic stem cells lacking CpG binding protein. Mol. Cell. Biol. 25 (2005), 4881–4891.
6. Caunt, C.J., Keyse, S.M., Dual-specificity MAP kinase phosphatases (MKPs): shaping the outcome of MAP kinase signalling. FEBS J. 280 (2013), 489–504.
7. Chen, A.E., Melton, D.A., Derivation of human embryonic stem cells by immunosurgery. J. Vis. Exp., 10, 2007, 574.
8. Christie, G.R., Williams, D.J., Macisaac, F., Dickinson, R.J., Rosewell, I., Keyse, S.M., The dual-specificity protein phosphatase DUSP9/MKP-4 is essential for placental function but is not required for normal embryonic development. Mol. Cell. Biol. 25 (2005), 8323–8333.
9. Dennis, K., Fan, T., Geiman, T., Yan, Q., Muegge, K., Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev. 15 (2001), 2940–2944.
10. Durcova-Hills, G., Burgoyne, P., McLaren, A., Analysis of sex differences in EGC imprinting. Dev. Biol. 268 (2004), 105–110.
11. Eggan, K., Akutsu, H., Loring, J., Jackson-Grusby, L., Klemm, M., Rideout, W.M. 3rd, Yanagimachi, R., Jaenisch, R., Hybrid vigor, fetal overgrowth, and viability of mice derived by nuclear cloning and tetraploid embryo complementation. Proc. Natl. Acad. Sci. USA 98 (2001), 6209–6214.
12. Elias, J.E., Gygi, S.P., Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4 (2007), 207–214.
13. Elling, U., Taubenschmid, J., Wirnsberger, G., O'Malley, R., Demers, S.-P., Vanhaelen, Q., Shukalyuk, A.I., Schmauss, G., Schramek, D., Schnuetgen, F., et al. Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell 9 (2011), 563–574.
14. Eng, J.K., McCormack, A.L., Yates, J.R., An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5 (1994), 976–989.
15. Erickson, B.K., Jedrychowski, M.P., McAlister, G.C., Everley, R.A., Kunz, R., Gygi, S.P., Evaluating multiplexed quantitative phosphopeptide analysis on a hybrid quadrupole mass filter/linear ion trap/orbitrap mass spectrometer. Anal. Chem. 87 (2015), 1241–1249.
16. Fan, Y., Melhem, M.F., Chaillet, J.R., Forced expression of the homeobox-containing gene Pem blocks differentiation of embryonic stem cells. Dev. Biol. 210 (1999), 481–496.
17. Ficz, G., Hore, T.A., Santos, F., Lee, H.J., Dean, W., Arand, J., Krueger, F., Oxley, D., Paul, Y.-L., Walter, J., et al. FGF signaling inhibition in ESCs drives rapid genome-wide demethylation to the epigenetic ground state of pluripotency. Cell Stem Cell 13 (2013), 351–359.
18. Habibi, E., Brinkman, A.B., Arand, J., Kroeze, L.I., Kerstens, H.H.D., Matarese, F., Lepikhov, K., Gut, M., Brun-Heath, I., Hubner, N.C., et al. Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells. Cell Stem Cell 13 (2013), 360–369.
19. Hackett, J.A., Dietmann, S., Murakami, K., Down, T.A., Leitch, H.G., Surani, M.A., Synergistic mechanisms of DNA demethylation during transition to ground-state pluripotency. Stem Cell Reports 1 (2013), 518–531.
20. Hadjantonakis, A.K., Cox, L.L., Tam, P.P., Nagy, A., An X-linked GFP transgene reveals unexpected paternal X-chromosome activity in trophoblastic giant cells of the mouse placenta. Genesis 29 (2001), 133–140.
21. Hajkova, P., Jeffries, S.J., Lee, C., Miller, N., Jackson, S.P., Surani, M.A., Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329 (2010), 78–82.
22. Hatano, S.-Y., Tada, M., Kimura, H., Yamaguchi, S., Kono, T., Nakano, T., Suemori, H., Nakatsuji, N., Tada, T., Pluripotential competence of cells associated with Nanog activity. Mech. Dev. 122 (2005), 67–79.
23. Huttlin, E.L., Jedrychowski, M.P., Elias, J.E., Goswami, T., Rad, R., Beausoleil, S.A., Villén, J., Haas, W., Sowa, M.E., Gygi, S.P., A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143 (2010), 1174–1189.
24. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., Peterson, R.T., Yeh, J.-R.J., Joung, J.K., Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol. 31 (2013), 227–229.
25. Isasa, M., Rose, C.M., Elsasser, S., Navarrete-Perea, J., Paulo, J.A., Finley, D.J., Gygi, S.P., Multiplexed, proteome-wide protein expression profiling: yeast deubiquitylating enzyme knockout strains. J. Proteome Res. 14 (2015), 5306–5317.
26. Jiang, J., Chan, Y.-S., Loh, Y.-H., Cai, J., Tong, G.-Q., Lim, C.-A., Robson, P., Zhong, S., Ng, H.-H., A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat. Cell Biol. 10 (2008), 353–360.
27. Labosky, P.A., Barlow, D.P., Hogan, B.L., Mouse embryonic germ (EG) cell lines: transmission through the germline and differences in the methylation imprint of insulin-like growth factor 2 receptor (Igf2r) gene compared with embryonic stem (ES) cell lines. Development 120 (1994), 3197–3204.
28. Lee, J.T., Lu, N., Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99 (1999), 47–57.
29. Leitch, H.G., Blair, K., Mansfield, W., Ayetey, H., Humphreys, P., Nichols, J., Surani, M.A., Smith, A., Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state. Development 137 (2010), 2279–2287.
30. Leitch, H.G., McEwen, K.R., Turp, A., Encheva, V., Carroll, T., Grabole, N., Mansfield, W., Nashun, B., Knezovich, J.G., Smith, A., et al. Naive pluripotency is associated with global DNA hypomethylation. Nat. Struct. Mol. Biol. 20 (2013), 311–316.
31. Li, Z., Fei, T., Zhang, J., Zhu, G., Wang, L., Lu, D., Chi, X., Teng, Y., Hou, N., Yang, X., et al. BMP4 signaling acts via dual-specificity phosphatase 9 to control ERK activity in mouse embryonic stem cells. Cell Stem Cell 10 (2012), 171–182.
32. Liao, J., Karnik, R., Gu, H., Ziller, M.J., Clement, K., Tsankov, A.M., Akopian, V., Gifford, C.A., Donaghey, J., Galonska, C., et al. Targeted disruption of DNMT1, DNMT3A and DNMT3B in human embryonic stem cells. Nat. Genet. 47 (2015), 469–478.
33. Matsui, Y., Zsebo, K., Hogan, B.L., Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70 (1992), 841–847.
34. Meissner, A., Gnirke, A., Bell, G.W., Ramsahoye, B., Lander, E.S., Jaenisch, R., Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res. 33 (2005), 5868–5877.
35. Meissner, A., Mikkelsen, T.S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B.E., Nusbaum, C., Jaffe, D.B., et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454 (2008), 766–770.
36. Okashita, N., Kumaki, Y., Ebi, K., Nishi, M., Okamoto, Y., Nakayama, M., Hashimoto, S., Nakamura, T., Sugasawa, K., Kojima, N., et al. PRDM14 promotes active DNA demethylation through the ten-eleven translocation (TET)-mediated base excision repair pathway in embryonic stem cells. Development 141 (2014), 269–280.
37. Oliveros-Etter, M., Li, Z., Nee, K., Hosohama, L., Hargan-Calvopiña, J., Lee, S.A., Joti, P., Yu, J., Clark, A.T., PGC reversion to pluripotency involves erasure of DNA methylation from imprinting control centers followed by locus-specific re-methylation. Stem Cell Reports 5 (2015), 337–349.
38. Ooi, S.K., Wolf, D., Hartung, O., Agarwal, S., Daley, G.Q., Goff, S.P., Bestor, T.H., Dynamic instability of genomic methylation patterns in pluripotent stem cells. Epigenetics Chromatin, 3, 2010, 17.
39. Piccolo, F.M., Bagci, H., Brown, K.E., Landeira, D., Soza-Ried, J., Feytout, A., Mooijman, D., Hajkova, P., Leitch, H.G., Tada, T., et al. Different roles for Tet1 and Tet2 proteins in reprogramming-mediated erasure of imprints induced by EGC fusion. Mol. Cell 49 (2013), 1023–1033.
40. Plath, K., Fang, J., Mlynarczyk-Evans, S.K., Cao, R., Worringer, K.A., Wang, H., de la Cruz, C.C., Otte, A.P., Panning, B., Zhang, Y., Role of histone H3 lysine 27 methylation in X inactivation. Science 300 (2003), 131–135.
41. Popp, C., Dean, W., Feng, S., Cokus, S.J., Andrews, S., Pellegrini, M., Jacobsen, S.E., Reik, W., Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463 (2010), 1101–1105.
42. Reik, W., Surani, M.A., Germline and pluripotent stem cells. Cold Spring Harb. Perspect. Biol., 7, 2015, a019422.
43. Robinson, M.D., McCarthy, D.J., Smyth, G.K., edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 (2010), 139–140.
44. Schulz, E.G., Meisig, J., Nakamura, T., Okamoto, I., Sieber, A., Picard, C., Borensztein, M., Saitou, M., Blüthgen, N., Heard, E., The two active X chromosomes in female ESCs block exit from the pluripotent state by modulating the ESC signaling network. Cell Stem Cell 14 (2014), 203–216.
45. Sharov, A.A., Piao, Y., Matoba, R., Dudekula, D.B., Qian, Y., VanBuren, V., Falco, G., Martin, P.R., Stagg, C.A., Bassey, U.C., et al. Transcriptome analysis of mouse stem cells and early embryos. PLoS Biol., 1, 2003, E74.
46. Sharova, L.V., Sharov, A.A., Piao, Y., Shaik, N., Sullivan, T., Stewart, C.L., Hogan, B.L.M., Ko, M.S.H., Global gene expression profiling reveals similarities and differences among mouse pluripotent stem cells of different origins and strains. Dev. Biol. 307 (2007), 446–459.
47. Shovlin, T.C., Durcova-Hills, G., Surani, A., McLaren, A., Heterogeneity in imprinted methylation patterns of pluripotent embryonic germ cells derived from pre-migratory mouse germ cells. Dev. Biol. 313 (2008), 674–681.
48. Smith, Z.D., Chan, M.M., Humm, K.C., Karnik, R., Mekhoubad, S., Regev, A., Eggan, K., Meissner, A., DNA methylation dynamics of the human preimplantation embryo. Nature 511 (2014), 611–615.
49. Stadtfeld, M., Maherali, N., Breault, D.T., Hochedlinger, K., Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2 (2008), 230–240.
50. Tada, M., Tada, T., Lefebvre, L., Barton, S.C., Surani, M.A., Embryonic germ cells induce epigenetic reprogramming of somatic nucleus in hybrid cells. EMBO J. 16 (1997), 6510–6520.
51. Tada, M., Takahama, Y., Abe, K., Nakatsuji, N., Tada, T., Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr. Biol. 11 (2001), 1553–1558.
52. Tada, T., Tada, M., Hilton, K., Barton, S.C., Sado, T., Takagi, N., Surani, M.A., Epigenotype switching of imprintable loci in embryonic germ cells. Dev. Genes Evol. 207 (1998), 551–561.
53. Takahashi, K., Yamanaka, S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006), 663–676.
54. Takahashi, K., Mitsui, K., Yamanaka, S., Role of ERas in promoting tumour-like properties in mouse embryonic stem cells. Nature 423 (2003), 541–545.
55. Tyanova, S., Temu, T., Sinitcyn, P., Carlson, A., Hein, M.Y., Geiger, T., Mann, M., Cox, J., The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13 (2016), 731–740.
56. von Meyenn, F., Iurlaro, M., Habibi, E., Liu, N.Q., Salehzadeh-Yazdi, A., Santos, F., Petrini, E., Milagre, I., Yu, M., Xie, Z., et al. Impairment of DNA methylation maintenance is the main cause of global demethylation in naive embryonic stem cells. Mol. Cell 62 (2016), 848–861.
57. Yamaji, M., Ueda, J., Hayashi, K., Ohta, H., Yabuta, Y., Kurimoto, K., Nakato, R., Yamada, Y., Shirahige, K., Saitou, M., PRDM14 ensures naive pluripotency through dual regulation of signaling and epigenetic pathways in mouse embryonic stem cells. Cell Stem Cell 12 (2013), 368–382.
58. Yang, L., Kirby, J.E., Sunwoo, H., Lee, J.T., Female mice lacking Xist RNA show partial dosage compensation and survive to term. Genes Dev. 30 (2016), 1747–1760.
59. 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.
60. Zvetkova, I., Apedaile, A., Ramsahoye, B., Mermoud, J.E., Crompton, L.A., John, R., Feil, R., Brockdorff, N., Global hypomethylation of the genome in XX embryonic stem cells. Nat. Genet. 37 (2005), 1274–1279.