Poised chromatin in the mammalian germ line

Development (Cambridge)

Volumn 141, Issue 19, 2014, Pages 3619-3626

  Lesch, Bluma J ^a   Page, David C ^a,b,c  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Bivalent; Chromatin; Germ cell; Germ line; Pluripotent; Poised

Indexed keywords

ARTICLE; CELL FUNCTION; CHROMATIN; DNA METHYLATION; EPIGENETICS; GERM LINE; HUMAN; INHERITANCE; MAMMAL; NONHUMAN; PLASMA; PROMOTER REGION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; GERM CELL; METABOLISM; MOUSE; PHYSIOLOGY;

CHROMATIN; HISTONE;

ANIMALS; CHROMATIN; DNA METHYLATION; EPIGENESIS, GENETIC; GERM CELLS; HISTONES; HUMANS; MICE; MODELS, BIOLOGICAL; PROMOTER REGIONS, GENETIC;

EID: 84908102194     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.113027     Document Type: Article

References (81)

1. Andreu-Vieyra, C. V., Chen, R., Agno, J. E., Glaser, S., Anastassiadis, K., Stewart, A. F. and Matzuk, M. M. (2010). MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol. 8, e1000453.
2. Aramaki, S., Hayashi, K., Kurimoto, K., Ohta, H., Yabuta, Y., Iwanari, H., Mochizuki, Y., Hamakubo, T., Kato, Y., Shirahige, K. et al. (2013). A mesodermal factor, T, specifies mouse germ cell fate by directly activating germline determinants. Dev. Cell 27, 516-529.
3. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jørgensen, H. F., John, R. M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M. et al. (2006). Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538.
4. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
5. Blobel, G. A., Kadauke, S., Wang, E., Lau, A. W., Zuber, J., Chou, M. M. and Vakoc, C. R. (2009). A reconfigured pattern of MLL occupancy within mitotic chromatin promotes rapid transcriptional reactivation following mitotic exit. Mol. Cell 36, 970-983.
6. Brookes, E., de Santiago, I., Hebenstreit, D., Morris, K. J., Carroll, T., Xie, S. Q., Stock, J. K., Heidemann, M., Eick, D., Nozaki, N. et al. (2012). Polycomb associates genome-wide with a specific RNA polymerase II variant, and regulates metabolic genes in ESCs. Cell Stem Cell 10, 157-170.
7. Brykczynska, U., Hisano, M., Erkek, S., Ramos, L., Oakeley, E. J., Roloff, T. C., Beisel, C., Schübeler, D., Stadler, M. B. and Peters, A. H. F. M. (2010). Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679-687.
8. Carone, B. R., Fauquier, L., Habib, N., Shea, J. M., Hart, C. E., Li, R., Bock, C., Li, C., Gu, H., Zamore, P. D. et al. (2010). Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084-1096.
9. Chen, D., Dundr, M., Wang, C., Leung, A., Lamond, A., Misteli, T. and Huang, S. (2005). Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J. Cell Biol. 168, 41-54.
10. Cohen, N. M., Kenigsberg, E. and Tanay, A. (2011). Primate CpG islands are maintained by heterogeneous evolutionary regimes involving minimal selection. Cell 145, 773-786.
11. Coulondre, C., Miller, J. H., Farabaugh, P. J. and Gilbert, W. (1978). Molecular basis of base substitution hotspots in Escherichia coli. Nature 274, 775-780.
12. Cui, K., Zang, C., Roh, T.-Y., Schones, D. E., Childs, R.W., Peng, W. and Zhao, K. (2009). Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell StemCell 4, 80-93.
13. Denissov, S., Hofemeister, H., Marks, H., Kranz, A., Ciotta, G., Singh, S., Anastassiadis, K., Stunnenberg, H. G. and Stewart, A. F. (2014). Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant. Development 141, 526-537.
14. Erhardt, S., Su, I.-H., Schneider, R., Barton, S., Bannister, A. J., Perez-Burgos, L., Jenuwein, T., Kouzarides, T., Tarakhovsky, A. and Surani, M. A. (2003). Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 130, 4235-4248.
15. Erkek, S., Hisano, M., Liang, C.-Y., Gill, M., Murr, R., Dieker, J., Schübeler, D., van der Vlag, J., Stadler, M. B. and Peters, A. H. F. M. (2013). Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat. Struct. Mol. Biol. 20, 868-875.
16. Extavour, C. G. and Akam, M. (2003). Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130, 5869-5884.
17. Follmer, N. E., Wani, A. H. and Francis, N. J. (2012). A polycomb group protein is retained at specific sites on chromatin in mitosis. PLoS Genet. 8, e1003135.
18. Fonseca, J. P., Steffen, P. A., Muller, S., Lu, J., Sawicka, A., Seiser, C. and Ringrose, L. (2012). In vivo Polycomb kinetics and mitotic chromatin binding distinguish stem cells from differentiated cells. Genes Dev. 26, 857-871.
19. Fouse, S. D., Shen, Y., Pellegrini, M., Cole, S., Meissner, A., Van Neste, L., Jaenisch, R. and Fan, G. (2008). Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3K4/K27 trimethylation. Cell Stem Cell 2, 160-169.
20. Gao, Z., Zhang, J., Bonasio, R., Strino, F., Sawai, A., Parisi, F., Kluger, Y., Reinberg, D. (2012). PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol. Cell 45, 344-356.
21. Gill, M. E., Erkek, S. and Peters, A. H. F. M. (2012). Parental epigenetic control of embryogenesis: a balance between inheritance and reprogramming? Curr. Opin. Cell Biol. 24, 387-396.
22. Guo, H., Zhu, P., Yan, L., Li, R., Hu, B., Lian, Y., Yan, J., Ren, X., Lin, S., Li, J. et al. (2014). The DNA methylation landscape of human early embryos. Nature 511, 606-610.
23. Hammoud, S. S., Nix, D. A., Zhang, H., Purwar, J., Carrell, D. T. and Cairns, B. R. (2009). Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478.
24. Hammoud, S. S., Low, D. H. P., Yi, C., Carrell, D. T., Guccione, E. and Cairns, B. R. (2014). Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis. Cell Stem Cell 15, 239-253.
25. Hattori, N., Niwa, T., Kimura, K., Helin, K. and Ushijima, T. (2013). Visualization of multivalent histone modification in a single cell reveals highly concerted epigenetic changes on differentiation of embryonic stem cells. Nucleic Acids Res. 41, 7231-7239.
26. Hayashi, K. and Surani, M. A. (2009). Resetting the epigenome beyond pluripotency in the germline. Cell Stem Cell 4, 493-498.
27. Kanatsu-Shinohara, M., Inoue, K., Lee, J., Yoshimoto, M., Ogonuki, N., Miki, H., Baba, S., Kato, T., Kazuki, Y., Toyokuni, S. et al. (2004). Generation of pluripotent stem cells from neonatal mouse testis. Cell 119, 1001-1012.
28. Koutsourakis, M., Langeveld, A., Patient, R., Beddington, R. and Grosveld, F. (1999). The transcription factor GATA6 is essential for early extraembryonic development. Development 126, 723-732.
29. Ku, M., Koche, R. P., Rheinbay, E., Mendenhall, E. M., Endoh, M., Mikkelsen, T. S., Presser, A., Nusbaum, C., Xie, X., Chi, A. S. et al. (2008). Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242.
30. Kurimoto, K., Yabuta, Y., Ohinata, Y., Shigeta, M., Yamanaka, K. and Saitou, M. (2008). Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev. 22, 1617-1635.
31. La Salle, S., Mertineit, C., Taketo, T., Moens, P. B., Bestor, T. H. and Trasler, J. M. (2004). Windows for sex-specific methylation marked by DNA methyltransferase
32. expression profiles in mouse germ cells. Dev. Biol. 268, 403-415.
33. Landry, C., Clotman, F., Hioki, T., Oda, H., Picard, J. J., Lemaigre, F. P. and Rousseau, G. G. (1997). HNF-6 is expressed in endoderm derivatives and nervous system of the mouse embryo and participates to the cross-regulatory network of liver-enriched transcription factors. Dev. Biol. 192, 247-257.
34. Leitch, H. G. and Smith, A. (2013). The mammalian germline as a pluripotency cycle. Development 140, 2495-2501.
35. Lesch, B. J., Dokshin, G. A., Young, R. A., McCarrey, J. R. and Page, D. C. (2013). A set of genes critical to development is epigenetically poised in mouse germ cells from fetal stages through completion of meiosis. Proc. Natl. Acad. Sci. USA 110, 16061-16066.
36. Liu, Y. and Rao, M. S. (2004). Olig genes are expressed in a heterogeneous population of precursor cells in the developing spinal cord. Glia 45, 67-74.
37. Lu, Q. R., Yuk, D.-i., Alberta, J. A., Zhu, Z., Pawlitzky, I., Chan, J., McMahon, A. P., Stiles, C. D. and Rowitch, D. H. (2000). Sonic hedgehog–regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317-329.
38. Lucifero, D., La Salle, S., Bourc’his, D., Martel, J., Bestor, T. H. and Trasler, J. M. (2007). Coordinate regulation of DNA methyltransferase expression during oogenesis. BMC Dev. Biol. 7, 36.
39. Maatouk, D. M., Kellam, L. D., Mann, M. R. W., Lei, H., Li, E., Bartolomei, M. S. and Resnick, J. L. (2006). DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development 133, 3411-3418.
40. Mack, S. C., Witt, H., Piro, R. M., Gu, L., Zuyderduyn, S., Stütz, A. M., Wang, X., Gallo, M., Garzia, L., Zayne, K. et al. (2014). Epigenomic alterations define lethal CIMP-positive ependymomas of infancy. Nature 506, 445-450.
41. McLaren, A. (2003). Primordial germ cells in the mouse. Dev. Biol. 262, 1-15.
42. 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. (2008). Genomescale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770.
43. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.-K., Koche, R. P. et al. (2007). Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560.
44. Mochizuki, K., Tachibana, M., Saitou, M., Tokitake, Y. and Matsui, Y. (2012). Implication of DNA demethylation and bivalent histone modification for selective gene regulation in mouse primordial germ cells. PLoS ONE 7, e46036.
45. Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., Bibel, M. and Schübeler, D. (2008). Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30, 755-766.
46. Muramoto, T., Müller, I., Thomas, G., Melvin, A. and Chubb, J. R. (2010). Methylation of H3K4 Is required for inheritance of active transcriptional states. Curr. Biol. 20, 397-406.
47. Ng, R. K. and Gurdon, J. B. (2008). Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat. Cell Biol. 10, 102-109.
48. Ng, S.-F., Lin, R. C. Y., Laybutt, D. R., Barres, R., Owens, J. A. and Morris, M. J. (2010). Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467, 963-966.
49. Ng, J.-H., Kumar, V., Muratani, M., Kraus, P., Yeo, J.-C., Yaw, L.-P., Xue, K., Lufkin, T., Prabhakar, S. and Ng, H.-H. (2013). In vivo epigenomic profiling of germ cells reveals germ cell molecular signatures. Dev. Cell 24, 324-333.
50. Ohinata, Y., Payer, B., O’Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S. C., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A. et al. (2005). Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436, 207-213.
51. Ohm, J. E., McGarvey, K. M., Yu, X., Cheng, L., Schuebel, K. E., Cope, L., Mohammad, H. P., Chen, W., Daniel, V. C., Yu, W. et al. (2007). A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 39, 237-242.
52. Pesce, M., Wang, X., Wolgemuth, D. J. and Schöler, H. (1998). Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech. Dev. 71, 89-98.
53. Posfai, E., Kunzmann, R., Brochard, V., Salvaing, J., Cabuy, E., Roloff, T. C., Liu, Z., Tardat, M., van Lohuizen, M., Vidal, M. et al. (2012). Polycomb function during oogenesis is required for mouse embryonic development. Genes Dev. 26, 920-932.
54. Rakyan, V. K., Down, T. A., Maslau, S., Andrew, T., Yang, T. P., Beyan, H., Whittaker, P., McCann, O. T., Finer, S., Valdes, A. M. et al. (2010). Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res. 20, 434-439.
55. Rosner, M. H., Vigano, M. A., Ozato, K., Timmons, P. M., Poirie, F., Rigby, P.W. J. and Staudt, L. M. (1990). A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 345, 686-692.
56. Rugg-Gunn, P. J., Cox, B. J., Ralston, A. and Rossant, J. (2010). Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Proc. Natl. Acad. Sci. USA 107, 10783-10790.
57. Sachs, M., Onodera, C., Blaschke, K., Ebata, K. T., Song, J. S. and Ramalho-Santos, M. (2013). Bivalent chromatin marks developmental regulatory genes in the mouse embryonic germline in vivo. Cell Rep. 3, 1777-1784.
58. Saitou, M., Barton, S. C. and Surani, M. A. (2002). A molecular programme for the specification of germ cell fate in mice. Nature 418, 293-300.
59. Schmitges, F.W., Prusty, A. B., Faty, M., Stützer, A., Lingaraju, G. M., Aiwazian, J., Sack, R., Hess, D., Li, L., Zhou, S. et al. (2011). Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 42, 330-341.
60. Seisenberger, S., Andrews, S., Krueger, F., Arand, J., Walter, J., Santos, F., Popp, C., Thienpont, B., Dean, W. and Reik, W. (2012). The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 48, 849-862.
61. Shilatifard, A. (2012). The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81, 65-95.
62. Simon, J. A. and Kingston, R. E. (2013). Occupying chromatin: polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol. Cell 49, 808-824.
63. Smallwood, S. A. and Kelsey, G. (2012). De novo DNA methylation: a germ cell perspective. Trends Genet. 28, 33-42.
64. Smallwood, S. A., Tomizawa, S.-i., Krueger, F., Ruf, N., Carli, N., Segonds-Pichon, A., Sato, S., Hata, K., Andrews, S. R. and Kelsey, G. (2011). Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 43, 811-814.
65. Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Gnirke, A., Regev, A. and Meissner, A. (2012). A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344.
66. Smith, Z. D., Chan, M. M., Humm, K. C., Karnik, R., Mekhoubad, S., Regev, A., Eggan, K. and Meissner, A. (2014). DNA methylation dynamics of the human preimplantation embryo. Nature 511, 611-615.
67. Strome, S. and Lehmann, R. (2007). Germ versus soma decisions: lessons from flies and worms. Science 316, 392-393.
68. Tam, P. P. L. and Zhou, S. X. (1996). The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178, 124-132.
69. Tavares, L., Dimitrova, E., Oxley, D., Webster, J., Poot, R., Demmers, J., Bezstarosti, K., Taylor, S., Ura, H., Koide, H. et al. (2012). RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 148, 664-678.
70. Terrenoire, E., McRonald, F., Halsall, J. A., Page, P., Illingworth, R. S., Taylor, A. M. R., Davison, V., O’Neill, L. P. and Turner, B. M. (2010). Immunostaining of modified histones defines high-level features of the human metaphase epigenome. Genome Biol. 11, R110.
71. Vavouri, T. and Lehner, B. (2011). Chromatin organization in sperm may be the major functional consequence of base composition variation in the human genome. PLoS Genet. 7, e1002036.
72. Vincenz, C. and Kerppola, T. K. (2008). Different polycomb group CBX family proteins associate with distinct regions of chromatin using nonhomologous protein sequences. Proc. Natl. Acad. Sci. USA 105, 16572-16577.
73. Voigt, P., LeRoy, G., Drury, W. J.III, Zee, B. M., Son, J., Beck, D. B., Young, N. L., Garcia, B. A. and Reinberg, D. (2012). Asymmetrically modified nucleosomes. Cell 151, 181-193.
74. Voigt, P., Tee, W.-W. and Reinberg, D. (2013). A double take on bivalent promoters. Genes Dev. 27, 1318-1338.
75. Weismann, A. (1893). The Germ-Plasm: A Theory of Heredity. New York: Charles Scribner’s Sons.
76. Woodcock, C. L. and Ghosh, R. P. (2010). Chromatin higher-order structure and dynamics. Cold Spring Harb. Perspect. Biol. 2, a000596.
77. Wu, S.-F., Zhang, H. and Cairns, B. R. (2011). Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm. Genome Res. 21, 578-589.
78. Yabuta, Y., Kurimoto, K., Ohinata, Y., Seki, Y. and Saitou, M. (2006). Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling. Biol. Reprod. 75, 705-716.
79. Yamaguchi, S., Kimura, H., Tada, M., Nakatsuji, N. and Tada, T. (2005). Nanog expression inmousegermcell development. GeneExpr.Patterns 5, 639-646.
80. Yamaguchi, S., Hong, K., Liu, R., Inoue, A., Shen, L., Zhang, K. and Zhang, Y. (2013). Dynamics of 5-methylcytosine and 5-hydroxymethylcytosine during germ cell reprogramming. Cell Res. 23, 329-339.
81. Zhou, Q. and Anderson, D. J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73.