Comparison of epigenetic mediator expression and function in mouse and human embryonic blastomeres

Human Molecular Genetics

Volumn 23, Issue 18, 2014, Pages 4970-4984

  Chavez, Shawn L ^a   McElroy, Sohyun L ^a   Bossert, Nancy L ^b   De Jonge, Christopher J ^b   Rodriguez, Maria Vera ^a,c   Leong, Denise E ^a   Behr, Barry ^a   Westphal, Lynn M ^a   Reijo Pera, Renee A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c IVIOMICS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; METHYLTRANSFERASE; S6 KINASE; SIGNAL PEPTIDE;

ANIMAL; BLASTOMA; COMPARATIVE STUDY; DNA METHYLATION; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HUMAN; MAMMALIAN EMBRYO; METABOLISM; MOUSE; SPECIES DIFFERENCE;

ANIMALS; BLASTOMERES; DNA METHYLATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; METHYLTRANSFERASES; MICE; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SPECIES SPECIFICITY;

EID: 84906832291     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu212     Document Type: Article

References (76)

1. Wong, C.C., Loewke, K.E., Bossert, N.L., Behr, B., De Jonge, C.J., Baer, T.M. and Reijo Pera, R.A. (2010) Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat. Biotechnol., 28, 1115-1121.
2. Wossidlo, M., Nakamura, T., Lepikhov, K., Marques, C.J., Zakhartchenko, V., Boiani, M., Arand, J., Nakano, T., Reik, W. and Walter, J. (2011) 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun., 2, 241.
3. Vassena, R., Boue, S., Gonzalez-Roca, E., Aran, B., Auer, H., Veiga, A. and Izpisua Belmonte, J.C. (2011) Waves of early transcriptional activation and pluripotency program initiation during human preimplantation development. Development, 138, 3699-3709.
4. Plachta, N., Bollenbach, T., Pease, S., Fraser, S.E. and Pantazis, P. (2011) Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nat. Cell Biol., 13, 117-123.
5. Chavez, S.L., Loewke, K.E., Han, J., Moussavi, F., Colls, P., Munne, S., Behr, B. and Reijo Pera, R.A. (2012) Dynamic blastomere behaviour reflects human embryo ploidy by the four-cell stage. Nat. Commun., 3, 1251.
6. Xue, Z., Huang, K., Cai, C., Cai, L., Jiang, C.Y., Feng, Y., Liu, Z., Zeng, Q., Cheng, L., Sun, Y.E. et al. (2013) Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature, 500, 593-597.
7. Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Urven, L., McCarrey, J., Cedar, H. and Razin, A. (1992)Developmental pattern of gene-specificDNA methylation in the mouse embryo and germ line. Genes Dev., 6, 705-714.
8. Reik, W. (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature, 447, 425-432.
9. Lewis, J.D., Meehan, R.R., Henzel, W.J., Maurer-Fogy, I., Jeppesen, P., Klein, F. and Bird, A. (1992) Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell, 69, 905-914.
10. Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N. and Bird, A. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature, 393, 386-389.
11. Jones, P.L., Veenstra, G.J., Wade, P.A., Vermaak, D., Kass, S.U., Landsberger, N., Strouboulis, J. and Wolffe, A.P. (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet., 19, 187-191.
12. Robert, M.F., Morin, S., Beaulieu, N., Gauthier, F., Chute, I.C., Barsalou, A. andMacLeod, A.R. (2003)DNMT1is required to maintainCpGmethylation and aberrant gene silencing in human cancer cells. Nat. Genet., 33, 61-65.
13. May, A., Kirchner, R., Muller, H., Hartmann, P., El Hajj, N., Tresch, A., Zechner, U., Mann, W. and Haaf, T. (2009) Multiplex rt-PCR expression analysis of developmentally important genes in individual mouse preimplantation embryos and blastomeres. Biol. Reprod., 80, 194-202.
14. Golding, M.C. and Westhusin, M.E. (2003) Analysis of DNA (cytosine 5) methyltransferase mRNA sequence and expression in bovine preimplantation embryos, fetal and adult tissues. Gene Expr. Patterns, 3, 551-558.
15. Vassena, R., Dee Schramm, R. and Latham, K.E. (2005) Species-dependent expression patterns ofDNAmethyltransferase genes in mammalian oocytes and preimplantation embryos. Mol. Reprod. Dev., 72, 430-436.
16. Huntriss, J., Hinkins, M., Oliver, B., Harris, S.E., Beazley, J.C., Rutherford, A.J., Gosden, R.G., Lanzendorf, S.E. and Picton, H.M. (2004) Expression of mRNAs for DNA methyltransferases and methyl-CpG-binding proteins in the human female germ line, preimplantation embryos, and embryonic stem cells. Mol. Reprod. Dev., 67, 323-336.
17. Latham, J.A. and Dent, S.Y. (2007) Cross-regulation of histone modifications. Nat. Struct. Mol. Biol., 14, 1017-1024.
18. Liu, H., Kim, J.M. and Aoki, F. (2004) Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development, 131, 2269-2280.
19. Torres-Padilla, M.E., Parfitt, D.E., Kouzarides, T. and Zernicka-Goetz, M. (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature, 445, 214-218.
20. Qiao, J., Chen, Y., Yan, L.Y., Yan, J., Liu, P. and Sun, Q.Y. (2010) Changes in histone methylation during human oocyte maturation and IVF-or ICSI-derived embryo development. Fertil. Steril., 93, 1628-1636.
21. Sarmento, O.F., Digilio, L.C., Wang, Y., Perlin, J., Herr, J.C., Allis, C.D. and Coonrod, S.A. (2004) Dynamic alterations of specific histone modifications during early murine development. J. Cell Sci., 117, 4449-4459.
22. Veeck, L.L., Amundson, C.H., Brothman, L.J., DeScisciolo, C., Maloney, M.K., Muasher, S.J. and Jones, H.W. Jr (1993) Significantly enhanced pregnancy rates per cycle through cryopreservation and thaw of pronuclear stage oocytes. Fertil. Steril., 59, 1202-1207.
23. Miller, K.F. and Goldberg, J.M. (1995) In vitro development and implantation rates of fresh and cryopreserved sibling zygotes. Obstet. Gynecol., 85, 999-1002.
24. El-Toukhy, T., Khalaf, Y., Al-Darazi, K., O'Mahony, F., Wharf, E., Taylor, A. and Braude, P. (2003) Cryo-thawed embryos obtained from conception cycles have double the implantation and pregnancy potential of those from unsuccessful cycles. Hum. Reprod., 18, 1313-1318.
25. Flach, G., Johnson, M.H., Braude, P.R., Taylor, R.A. and Bolton, V.N. (1982)The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J., 1, 681-686.
26. Dobson, A.T., Raja, R., Abeyta, M.J., Taylor, T., Shen, S., Haqq, C. and Pera, R.A. (2004) The unique transcriptome through day 3 of human preimplantation development. Hum. Mol. Genet., 13, 1461-1470.
27. Shi, W., Dirim, F., Wolf, E., Zakhartchenko, V. and Haaf, T. (2004) Methylation reprogramming and chromosomal aneuploidy in in vivo fertilized and cloned rabbit preimplantation embryos. Biol. Reprod., 71, 340-347.
28. Fulka, H., Mrazek, M., Tepla, O. and Fulka, J. Jr (2004) DNA methylation pattern inhumanzygotes and developing embryos. Reproduction, 128, 703-708.
29. Aranyi, T. and Paldi, A. (2006) The constant variation: DNA methylation changes during preimplantation development. FEBS Lett., 580, 6521-6526.
30. Beaujean, N., Hartshorne, G., Cavilla, J., Taylor, J., Gardner, J., Wilmut, I., Meehan, R. and Young, L. (2004) Non-conservation of mammalian preimplantation methylation dynamics. Curr. Biol, 14, R266-R267.
31. Jedrusik, A., Parfitt, D.E., Guo, G., Skamagki, M., Grabarek, J.B., Johnson, M.H., Robson, P. and Zernicka-Goetz, M. (2008) Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev., 22, 2692-2706.
32. Tang, F., Barbacioru, C., Wang, Y., Nordman, E., Lee, C., Xu, N., Wang, X., Bodeau, J., Tuch, B.B., Siddiqui, A. et al. (2009) mRNA-Seq whole-transcriptome analysis of a single cell. Nat. Methods, 6, 377-382.
33. Wang, H., Huang, Z.Q., Xia, L., Feng, Q., Erdjument-Bromage, H., Strahl, B.D., Briggs, S.D., Allis, C.D., Wong, J., Tempst, P. et al. (2001) Methylation of histoneH4at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science, 293, 853-857.
34. Pal, S., Vishwanath, S.N., Erdjument-Bromage, H., Tempst, P. and Sif, S. (2004) Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Mol. Cell Biol., 24, 9630-9645.
35. Goto, H., Yasui, Y., Nigg, E.A. and Inagaki, M. (2002) Aurora-B phosphorylates Histone H3 at serine28 with regard to the mitotic chromosome condensation. Genes Cells, 7, 11-17.
36. Qian, W., Choi, S., Gibson, G.A., Watkins, S.C., Bakkenist, C.J. and Van Houten, B. (2012) Mitochondrial hyperfusion induced by loss of the fission protein Drp1 causes ATM-dependent G2/M arrest and aneuploidy through DNA replication stress. J. Cell Sci., 125, 5745-5757.
37. Crosio, C., Fimia, G.M., Loury, R., Kimura, M., Okano, Y., Zhou, H., Sen, S., Allis, C.D. and Sassone-Corsi, P. (2002) Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol. Cell Biol., 22, 874-885.
38. Cascone, A., Bruelle, C., Lindholm, D., Bernardi, P. and Eriksson, O. (2012) Destabilization of the outer and inner mitochondrial membranes by core and linker histones. PLoS One, 7, e35357.
39. Kim, J.M., Liu, H., Tazaki, M., Nagata, M. and Aoki, F. (2003) Changes in histone acetylation during mouse oocyte meiosis. J. Cell Biol., 162, 37-46.
40. Ribeiro-Mason, K., Boulesteix, C., Fleurot, R., Aguirre-Lavin, T., Adenot, P., Gall, L., Debey, P. and Beaujean, N. (2012) H3S10 phosphorylation marks constitutive heterochromatin during interphase in early mouse embryos until the 4-cell stage. J. Reprod. Dev., 58, 467-475.
41. Srinivasan, M., Sedmak, D. and Jewell, S. (2002) Effect of fixatives and tissue processing on the content and integrity of nucleic acids. Am. J. Pathol., 161, 1961-1971.
42. Schnell, U., Dijk, F., Sjollema, K.A. and Giepmans, B.N. (2012) Immunolabeling artifacts and the need for live-cell imaging. Nat. Methods, 9, 152-158.
43. Summerton, J.E. (2007) Morpholino, siRNA, andS-DNAcompared: impact of structure and mechanism of action on off-target effects and sequence specificity. Curr. Top. Med. Chem., 7, 651-660.
44. Bettencourt-Dias, M., Giet, R., Sinka, R., Mazumdar, A., Lock, W.G., Balloux, F., Zafiropoulos, P.J., Yamaguchi, S., Winter, S., Carthew, R.W. et al. (2004) Genome-wide survey of protein kinases required for cell cycle progression. Nature, 432, 980-987.
45. Leonhardt, H., Page, A.W., Weier, H.U. and Bestor, T.H. (1992) A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell, 71, 865-873.
46. Yang, F., Camp, D.G. 2nd, Gritsenko, M.A., Luo, Q., Kelly, R.T., Clauss, T.R., Brinkley, W.R., Smith, R.D. and Stenoien, D.L. (2007) Identification of a novel mitotic phosphorylation motif associated with protein localization to the mitotic apparatus. J. Cell Sci., 120, 4060-4070.
47. Vakifahmetoglu, H., Olsson, M. and Zhivotovsky, B. (2008) Death through a tragedy: mitotic catastrophe. Cell Death Differ., 15, 1153-1162.
48. Vanneste, E., Voet, T., Le Caignec, C., Ampe, M., Konings, P., Melotte, C., Debrock, S., Amyere, M., Vikkula, M., Schuit, F. et al. (2009) Chromosome instability is common in human cleavage-stage embryos. Nat. Med., 15, 577-583.
49. Johnson, D.S., Gemelos, G., Baner, J., Ryan, A., Cinnioglu, C., Banjevic, M., Ross, R., Alper, M., Barrett, B., Frederick, J. et al. (2010) Preclinical validation of a microarray method for full molecular karyotyping of blastomeres in a 24-h protocol. Hum. Reprod., 25, 1066-1075.
50. Wiggin, G.R., Soloaga, A., Foster, J.M., Murray-Tait, V., Cohen, P. and Arthur, J.S. (2002) MSK1 and MSK2 are required for the mitogen-and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol. Cell Biol., 22, 2871-2881.
51. Soloaga, A., Thomson, S., Wiggin, G.R., Rampersaud, N., Dyson, M.H., Hazzalin, C.A., Mahadevan, L.C. and Arthur, J.S. (2003) MSK2 and MSK1 mediate the mitogen-and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J., 22, 2788-2797.
52. Ikura, T., Ogryzko, V.V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M., Scully, R., Qin, J. and Nakatani, Y. (2000) Involvement of the TIP60 histone acetylase complex inDNArepair and apoptosis. Cell, 102, 463-473.
53. Gehani, S.S., Agrawal-Singh, S., Dietrich, N., Christophersen, N.S., Helin, K. and Hansen, K. (2010) Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol. Cell, 39, 886-900.
54. Anderson, R.A., Bayne, R.A., Gardner, J. and De Sousa, P.A. (2010) Brain-derived neurotrophic factor is a regulator of human oocyte maturation and early embryo development. Fertil. Steril., 93, 1394-1406.
55. Ye, Y., Kawamura, K., Sasaki, M., Kawamura, N., Groenen, P., Sollewijn Gelpke, M.D., Kumagai, J., Fukuda, J. and Tanaka, T. (2009) Leptin and ObRa/MEK signalling in mouse oocyte maturation and preimplantation embryo development. Reprod. Biomed. Online, 19, 181-190.
56. McElroy, S.L., Byrne, J.A., Chavez, S.L., Behr, B., Hsueh, A.J., Westphal, L.M. and Reijo Pera, R.A. (2010) Parthenogenic blastocysts derived from cumulus-free in vitro matured human oocytes. PLoS One, 5, e10979.
57. Bruhat, A., Cherasse, Y., Maurin, A.C., Breitwieser, W., Parry, L., Deval, C., Jones, N., Jousse, C. and Fafournoux, P. (2007) ATF2 is required for amino acid-regulated transcription by orchestrating specific histone acetylation. Nucleic Acids Res., 35, 1312-1321.
58. Rho, J., Choi, S., Seong, Y.R., Cho, W.K., Kim, S.H. and Im, D.S. (2001) Prmt5, which forms distinct homo-oligomers, is a member of the proteinarginine methyltransferase family. J. Biol. Chem., 276, 11393-11401.
59. Kimura, A. and Horikoshi, M. (1998) Tip60 acetylates six lysines of a specific class in core histones in vitro. Genes Cells, 3, 789-800.
60. Schultz, D.C., Ayyanathan, K., Negorev, D., Maul, G.G. and Rauscher, F.J. 3rd (2002) SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev., 16, 919-932.
61. Doherty, A.S., Bartolomei, M.S. and Schultz, R.M. (2002) Regulation of stage-specific nuclear translocation of Dnmt1o during preimplantation mouse development. Dev. Biol., 242, 255-266.
62. Chen, T., Ueda, Y., Xie, S. andLi, E. (2002) A novel Dnmt3a isoform produced from an alternative promoter localizes to euchromatin and its expression correlateswith active de novomethylation. J. Biol. Chem., 277, 38746-38754.
63. Cirio, M.C., Martel, J., Mann, M., Toppings, M., Bartolomei, M., Trasler, J. and Chaillet, J.R. (2008) DNA methyltransferase 1o functions during preimplantation development to preclude a profound level of epigenetic variation. Dev. Biol., 324, 139-150.
64. 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.
65. Sendler, E., Johnson, G.D., Mao, S.H., Goodrich, R.J., Diamond, M.P., Hauser, R. and Krawetz, S.A. (2013) Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res., 41, 4104-4117.
66. Ananieva, O., Darragh, J., Johansen, C., Carr, J.M., McIlrath, J., Park, J.M., Wingate, A., Monk, C.E., Toth, R., Santos, S.G. et al. (2008) The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat. Immunol., 9, 1028-1036.
67. Cui, X., Ji, D., Fisher, D.A., Wu, Y., Briner, D.M. and Weinstein, E.J. (2011) Targeted integration in rat and mouse embryos with zinc-finger nucleases. Nat. Biotechnol., 29, 64-67.
68. Wefers, B., Panda, S.K., Ortiz, O., Brandl, C., Hensler, S., Hansen, J., Wurst, W. and Kuhn, R. (2013) Generation of targeted mouse mutants by embryo microinjection of TALEN mRNA. Nat. Protoc., 8, 2355-2379.
69. Casanova, E., Fehsenfeld, S., Greiner, E., Stewart, A.F. and Schutz, G. (2002) Construction of a conditional allele of RSK-B/MSK2 in the mouse. Genesis, 32, 158-160.
70. Giet, R. and Glover, D.M. (2001) Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol., 152, 669-682.
71. Lightfoot, D.A., Kouznetsova, A., Mahdy, E., Wilbertz, J. and Hoog, C. (2006) The fate of mosaic aneuploid embryos during mouse development. Dev. Biol., 289, 384-394.
72. Wei, Y., Mizzen, C.A., Cook, R.G., Gorovsky, M.A. and Allis, C.D. (1998) Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc. Natl Acad. Sci. USA, 95, 7480-7484.
73. Vigneron, S., Brioudes, E., Burgess, A., Labbe, J.C., Lorca, T. and Castro, A. (2010) RSK2 is a kinetochore-associated protein that participates in the spindle assembly checkpoint. Oncogene, 29, 3566-3574.
74. Kalista, T., Freeman, H.A., Behr, B., Reijo Pera, R.A. and Scott, C.T. (2011) Donation of embryos for human development and stem cell research. Cell Stem Cell, 8, 360-362.
75. Hellemans, J., Mortier, G., DePaepe, A., Speleman, F. and Vandesompele, J. (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol., 8, R19.
76. Foygel, K., Choi, B., Jun, S., Leong, D.E., Lee, A., Wong, C.C., Zuo, E., Eckart, M., Reijo Pera, R.A., Wong, W.H. et al. (2008) A novel and critical role for Oct4 as a regulator of thematernal-embryonic transition. PLoS One, 3, e4109.