Skip to main content
SpringerLink
Log in

Regulation of Zygotic Genome and Cellular Pluripotency

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

An Erratum to this article was published on 01 December 2016

Abstract

Events, manifesting transition from maternal to zygotic period of development are studied for more than 100 years, but underlying mechanisms are not yet clear. We provide a brief historical overview of development of concepts and explain the specific terminology used in the field. We further discuss differences and similarities between the zygotic genome activation and in vitro reprogramming process. Finally, we envision the future research directions within the field, where biochemical methods will play increasingly important role.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ESC :

embryonic stem cells

IPSC :

induced pluripotent stem cells

maternal transcription :

transcription that occurs in the egg and stops in the first meiotic prophase

MBT :

midblastula transition (a particular case of MZT, which occurs in several organisms. MBT is a moment of time, when ZGA, degradation of maternal transcripts, desynchronization of cell cycle, and locomotor activity of the cells start. The definition MBT is mostly applied to amphibians, fish, and Drosophila)

MZT :

maternal to zygotic transition (several events happening after fertilization until establishment of zygotic control over development including ZGA, degradation of maternal transcripts, desynchronization of cell cycle, and acquisition of cell motility. The term MZT can be applied to all metazoans)

pluripotency :

capacity of cells to differentiate along cell lineages contributing to all embryonic but not extraembryonic tissues. Early cells of vertebrate embryos before beginning of gastrulation, ESC, derived from mammals, birds, and fish and IPSC are pluripotent

totipotency :

unrestricted capacity of cells to differentiate along cell lineages contributing to all embryonic and extraembryonic tissues. Zygote is totipotent by definition; early mammalian cells are also totipotent

ZGA :

zygotic genome activation (start of zygotic transcription, which occurs in species-specific interval after fertilization).

References

  1. Adachi, K., and Scholer, H. R. (2012) Directing repro-gramming to pluripotency by transcription factors, Curr. Opin. Gen. Dev., 22, 416–422.

    Article  CAS  Google Scholar 

  2. Chambers, I., and Tomlinson, S. R. (2009) The transcrip-tional foundation of pluripotency, Development, 136, 2311–2322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hanna, J. H., Saha, K., and Jaenisch, R. (2010) Pluripotency and cellular reprogramming: facts, hypothe-ses, unresolved issues, Cell, 143, 508–525.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Sterneckert, J., Hoing, S., and Scholer, H. R. (2012) Concise review: Oct4 and more: the reprogramming expressway, Stem Cells, 30, 15–21.

    Article  CAS  PubMed  Google Scholar 

  5. Young, R. A. (2011) Control of the embryonic stem cell state, Cell, 144, 940–954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Bosch, T. C. (2009) Hydra and the evolution of stem cells, BioEssays, 31, 478–486.

    Article  PubMed  Google Scholar 

  7. Bosch, T. C., Anton-Erxleben, F., Hemmrich, G., and Khalturin, K. (2010) The hydra polyp: nothing but an active stem cell community, Dev. Growth Differ., 52, 15–25.

    Article  CAS  PubMed  Google Scholar 

  8. Tanaka, E. M., and Reddien, P. W. (2011) The cellular basis for animal regeneration, Dev. Cell, 21, 172–185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Conklin, E. G. (1908) The mechanism of heredity, Science, 27, 89–99.

    Article  CAS  PubMed  Google Scholar 

  10. Boveri, T. (1918) Zwei Fehlerquellen bei Merogoniever-suchen und die Entwicklungsfaehigkeit merogonischer und partiellermerogonischer Seeigelbastarde, Arch. Entw. Mech., 44, 417–471.

    Google Scholar 

  11. Godlevski, E. (1906) Untersuchungen ueber die Bastardierung der Echiniden-und Crinoidenfamilie, Arch. Entw. Mech., 20, 579–643.

    Google Scholar 

  12. Moore, J. (1941) Developmental rate of hybrid frogs, J. Exp. Zool., 86, 405–422.

    Article  Google Scholar 

  13. Rugh, R., and Exner, F. (1940) Developmental effects resulting from exposure to X-rays.

  14. Development of leopard frog eggs activated by bullfrog sperm, Proc. Am. Phil. Soc., 83, 607–619.

  15. Neyfakh, A. A. (1959) X-ray inactivation of nuclei as method for studying their function in the early develop-ment of fishes, J. Embryol. Exp. Morphol., 7, 173–192.

    CAS  PubMed  Google Scholar 

  16. Neyfakh, A. A. (1964) Radiation investigation of nucleo–cytoplasmic interrelations in morphogenesis and biochemical differentiation, Nature, 201, 880–884.

    Article  CAS  PubMed  Google Scholar 

  17. Neyfakh, A. A. (1961) Comparative study with the use of radiation of developmental function of nuclei in the devel-opment of animals, Zh. Obshch. Biol., 22, 42–57.

    Google Scholar 

  18. Korzh, V. (2009) Before maternal-zygotic transition… there was morphogenetic function of nuclei, Zebrafish, 6, 295–302.

    Article  PubMed  Google Scholar 

  19. Korzh, V. P., and Minin, A. A. (2010) A short history of loach or why remember morphogenetic function nuclei? The 50th anniversary of A. A. Neyfakh’s discovery of the morpho-genetic function of the nucleus, Ontogenez, 41, 150–158.

    CAS  PubMed  Google Scholar 

  20. Rott, N. N., and Sheveleva, G. A. (1968) Changes in the rate of cell divisions in the course of early development of diploid and haploid loach embryos, J. Embryol. Exp. Morphol., 20, 141–150.

    CAS  PubMed  Google Scholar 

  21. Spirin, A. S. (1966) “Masked” forms of mRNA, Curr. Top Dev. Biol., 1, 1–38.

    Article  CAS  PubMed  Google Scholar 

  22. Spirin, A. S. (1969) Informosomes, Eur. J. Biochem., 10, 20–35.

    Article  CAS  PubMed  Google Scholar 

  23. Voronina, A. S. (2002) Translational regulation in early devel-opment of eukaryotes, Mol. Biol. (Moscow), 36, 956–969.

    Article  CAS  Google Scholar 

  24. Kronja, I., and Orr-Weaver, T. L. (2011) Translational reg-ulation of the cell cycle: when, where, how and why? Phil. Trans. R. Soc., 366, 3638–3652.

    Article  CAS  Google Scholar 

  25. Gerhart, J. (1980) Mechanisms regulating pattern forma-tion in the amphibian egg and early embryo, in: Biological Regulation and Development (Goldberg, R., ed.) Plenum Press, New York, pp. 133-315.

  26. Tadros, W., and Lipshitz, H. D. (2009) The maternal-to-zygotic transition: a play in two acts, Development, 136, 3033–3042.

    Article  CAS  PubMed  Google Scholar 

  27. Yasuda, G. K., and Schubiger, G. (1992) Temporal regula-tion in the early embryo: is MBT too good to be true? Trends Genet., 8, 124–127.

    Article  CAS  PubMed  Google Scholar 

  28. Langley, A. R., Smith, J. C., Stemple, D. L., and Harvey, S. A. (2014) New insights into the maternal to zygotic transi-tion, Development, 141, 3834–3841.

    Article  CAS  PubMed  Google Scholar 

  29. Signoret, J., and Lefresne, J. (1974) Determination, by tri-tiated thymidine incorporation, of the stages of cellular cycle in the axolotl germ in synchronous period of segmen-tation, C. R. Hebd. Seances Acad. Sci., 279, 1189–1191.

    CAS  Google Scholar 

  30. Lefresne, J., Andeol, Y., and Signoret, J. (1998) Evidence for introduction of a variable G1 phase at the midblastula transition during early development in axolotl, Dev. Growth Differ., 40, 497–508.

    Article  CAS  PubMed  Google Scholar 

  31. Newport, J., and Kirschner, M. (1982) A major develop-mental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the mid-blastula stage, Cell, 30, 675–686.

    Article  CAS  PubMed  Google Scholar 

  32. Newport, J., and Kirschner, M. (1982) A major develop-mental transition in early Xenopus embryos: II. Control of the onset of transcription, Cell, 30, 687–696.

    Article  CAS  PubMed  Google Scholar 

  33. Kane, D. A., and Kimmel, C. B. (1993) The zebrafish mid-blastula transition, Development, 119, 447–456.

    CAS  PubMed  Google Scholar 

  34. Trinkaus, J. P. (1992) The midblastula transition, the YSL transition and the onset of gastrulation in Fundulus, Development, Suppl. S, 116, 75–80.

    Google Scholar 

  35. Collart, C., Allen, G. E., Bradshaw, C. R., Smith, J. C., and Zegerman, P. (2013) Titration of four replication fac-tors is essential for the Xenopus laevis midblastula transi-tion, Science, 341, 893–896.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Edgar, B. A., and Schubiger, G. (1986) Parameters control-ling transcriptional activation during early Drosophila development, Cell, 44, 871–877.

    Article  CAS  PubMed  Google Scholar 

  37. Lu, X., Li, J. M., Elemento, O., Tavazoie, S., and Wieschaus, E. F. (2009) Coupling of zygotic transcription to mitotic control at the Drosophila midblastula transition, Development, 136, 2101–2110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Piko, L., and Clegg, K. B. (1982) Quantitative changes in total RNA, total poly(A), and ribosomes in early mouse embryos, Dev. Biol., 89, 362–378.

    Article  CAS  PubMed  Google Scholar 

  39. Alizadeh, Z., Kageyama, S., and Aoki, F. (2005) Degradation of maternal mRNA in mouse embryos: selec-tive degradation of specific mRNAs after fertilization, Mol. Reprod. Dev., 72, 281–290.

    Article  CAS  PubMed  Google Scholar 

  40. Hamatani, T., Carter, M. G., Sharov, A. A., and Ko, M. S. (2004) Dynamics of global gene expression changes during mouse preimplantation development, Dev. Cell, 6, 117–131.

    Article  CAS  PubMed  Google Scholar 

  41. Ferg, M., Sanges, R., Gehrig, J., Kiss, J., Bauer, M., Lovas, A., Szabo, M., Yang, L., Straehle, U., Pankratz, M. J., Olasz, F., Stupka, E., and Muller, F. (2007) The TATA-binding protein regulates maternal mRNA degradation and differential zygotic transcription in zebrafish, EMBO J., 26, 3945–3956.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Aanes, H., Winata, C. L., Lin, C. H., Chen, J. P., Srinivasan, K. G., Lee, S. G., Lim, A. Y., Hajan, H. S., Collas, P., Bourque, G., Gong, Z., Korzh, V., Alestrom, P., and Mathavan, S. (2011) Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition, Genome Res., 21, 1328–1338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Baugh, L. R., Hill, A. A., Slonim, D. K., Brown, E. L., and Hunter, C. P. (2003) Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome, Development, 130, 889–900.

    Article  CAS  PubMed  Google Scholar 

  44. Paillard, L., Omilli, F., Legagneux, V., Bassez, T., Maniey, D., and Osborne, H. B. (1998) EDEN and EDEN-BP, a cis-element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus embryos, EMBO J., 17, 278–287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Audic, Y., Omilli, F., and Osborne, H. B. (1997) Post-fer-tilization deadenylation of mRNAs in Xenopus laevis embryos is sufficient to cause their degradation at the blas-tula stage, Mol. Cell. Biol., 17, 209–218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Voeltz, G. K., and Steitz, J. A. (1998) AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development, Mol. Cell. Biol., 18, 7537–7545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Tadros, W., Westwood, J. T., and Lipshitz, H. D. (2007) Titration of four replication factors is essential for the Xenopus laevis midblastula transition, Dev. Cell, 12, 847–849.

    Article  CAS  PubMed  Google Scholar 

  48. De Renzis, S., Elemento, O., Tavazoie, S., and Wieschaus, E. F. (2007) Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo, PLoS Biol., 5, e117.

  49. Liang, H. L., Nien, C. Y., Liu, H. Y., Metzstein, M. M., Kirov, N., and Rushlow, C. (2008) The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila, Nature, 456, 400–403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Giraldez, A. J., Mishima, Y., Rihel, J., Grocock, R. J., Van Dongen, S., Inoue, K., Enright, A. J., and Schier, A. F. (2006) Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs, Science, 312, 75–79.

    Article  CAS  PubMed  Google Scholar 

  51. Lee, M. T., Bonneau, A. R., Takacs, C. M., Bazzini, A. A., Divito, K. R., Fleming, E. S., and Giraldez, A. J. (2013) Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition, Nature, 503, 360–364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Onichtchouk, D., Geier, F., Polok, B., Messerschmidt, D. M., Mossner, R., Wendik, B., Song, S., Taylor, V., Timmer, J., and Driever, W. (2010) Zebrafish Pou5f1-dependent transcriptional networks in temporal control of early devel-opment, Mol. Syst. Biol., 6, 354.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Farley, E., and Levine, M. (2012) HOT DNAs: a novel class of developmental enhancers, Genes Dev., 26, 873–876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Ten Bosch, J. R., Benavides, J. A., and Cline, T. W. (2006) The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription, Development, 133, 1967–1977.

    Article  CAS  PubMed  Google Scholar 

  55. Kanodia, J. S., Liang, H. L., Kim, Y., Lim, B., Zhan, M., Lu, H., Rushlow, C. A., and Shvartsman, S. Y. (2012) Pattern formation by graded and uniform signals in the early Drosophila embryo, Biophys. J., 102, 427–433.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Nien, C. Y., Liang, H. L., Butcher, S., Sun, Y., Fu, S., Gocha, T., Kirov, N., Manak, J. R., and Rushlow, C. (2011) Temporal coordination of gene networks by Zelda in the early Drosophila embryo, PLoS Genet., 7, e1002339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Satija, R., and Bradley, R. K. (2012) The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo, Genome Res., 22, 656–665.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kvon, E. Z., Stampfel, G., Yanez-Cuna, J. O., Dickson, B. J., and Stark, A. (2012) HOT regions function as patterned developmental enhancers and have a distinct cis-regulatory signature, Genes Dev., 26, 908–913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Nien, C. Y., Liang, H. L., Butcher, S., Sun, Y., Fu, S., Gocha, T., Kirov, N., Manak, J. R., and Rushlow, C. (2011) Temporal coordination of gene networks by Zelda in the early Drosophila embryo, PLoS Genet., 7, e1002339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Leichsenring, M., Maes, J., Mossner, R., Driever, W., and Onichtchouk, D. (2013) Pou5f1 transcription factor con-trols zygotic gene activation in vertebrates, Science, 341, 1005–1009.

    Article  CAS  PubMed  Google Scholar 

  61. Onichtchouk, D. (2012) Pou5f1/oct4 in pluripotency con-trol: insights from zebrafish, Genesis, 50, 75–85.

    Article  CAS  PubMed  Google Scholar 

  62. Bogdanovic, O., Fernandez-Minan, A., Tena, J. J., De la Calle-Mustienes, E., Hidalgo, C., Van Kruysbergen, I., Van Heeringen, S. J., Veenstra, G. J., and Gomez-Skarmeta, J. L. (2012) Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis, Genome Res., 22, 2043–2053.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Kim, J., Chu, J., Shen, X., Wang, J., and Orkin, S. H. (2008) An extended transcriptional network for pluripoten-cy of embryonic stem cells, Cell, 132, 1049–1061.

    Article  CAS  PubMed  Google Scholar 

  64. Foo, S. M., Sun, Y., Lim, B., Ziukaite, R., O’Brien, K., Nien, C. Y., Kirov, N., Shvartsman, S. Y., and Rushlow, C. A. (2014) Zelda potentiates morphogen activity by increasing chromatin accessibility, Curr. Biol., 24, 1341–1346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Li, X. Y., Harrison, M. M., Villalta, J. E., Kaplan, T., and Eisen, M. B. (2014) Establishment of regions of genomic activity during the Drosophila maternal to zygotic transi-tion, eLife, 3, e03737.

  66. Burton, A., and Torres-Padilla, M. E. (2014) Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis, Nat. Rev. Mol. Cell Biol., 15, 723–734.

    Article  CAS  PubMed  Google Scholar 

  67. Lawson, K. A., Meneses, J. J., and Pedersen, R. A. (1991) Clonal analysis of epiblast fate during germ layer formation in the mouse embryo, Development, 113, 891–911.

    CAS  PubMed  Google Scholar 

  68. Garcia-Martinez, V., and Schoenwolf, G. C. (1992) Positional control of mesoderm movement and fate during avian gastrulation and neurulation, Dev. Dyn., 193, 249–256.

    Article  CAS  PubMed  Google Scholar 

  69. Ho, R. K., and Kimmel, C. B. (1993) Commitment of cell fate in the early zebrafish embryo, Science, 261, 109–111.

    Article  CAS  PubMed  Google Scholar 

  70. Domingo, C., and Keller, R. (2000) Cells remain compe-tent to respond to mesoderm-inducing signals present during gastrulation in Xenopus laevis, Dev. Biol., 225, 226–240.

    Article  CAS  PubMed  Google Scholar 

  71. Okabayashi, K., and Asashima, M. (2003) Tissue genera-tion from amphibian animal caps, Curr. Opin. Genet. Dev., 13, 502–507.

    Article  CAS  PubMed  Google Scholar 

  72. Evans, M. J., and Kaufman, M. H. (1981) Establishment in culture of pluripotent cells from mouse embryos, Nature, 292, 154–156.

    Article  CAS  PubMed  Google Scholar 

  73. 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.

    Article  CAS  PubMed  Google Scholar 

  74. Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L., and McKay, R. D. (2007) New cell lines from mouse epiblast share defin-ing features with human embryonic stem cells, Nature, 448, 196–199.

    Article  CAS  PubMed  Google Scholar 

  75. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T. K., Koche, R. P., Lee, W., Mendenhall, E., O’Donovan, A., Presser, A., Russ, C., Xie, X., Meissner, A., Wernig, M., Jaenisch, R., Nusbaum, C., Lander, E. S., and Bernstein, B. E. (2007) Genome-wide maps of chro-matin state in pluripotent and lineage-committed cells, Nature, 448, 553–560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Boyer, L. A., Lee, T. I., Cole, M. F., Johnstone, S. E., Levine, S. S., Zucker, J. P., Guenther, M. G., Kumar, R. M., Murray, H. L., Jenner, R. G., Gifford, D. K., Melton, D. A., Jaenisch, R., and Young, R. A. (2005) Core tran-scriptional regulatory circuitry in human embryonic stem cells, Cell, 122, 947–956.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Loh, Y. H., Wu, Q., Chew, J. L., Vega, V. B., Zhang, W., Chen, X., Bourque, G., George, J., Leong, B., Liu, J., Wong, K. Y., Sung, K. W., Lee, C. W., Zhao, X. D., Chiu, K. P., Lipovich, L., Kuznetsov, V. A., Robson, P., Stanton, L. W., Wei, C. L., Ruan, Y., Lim, B., and Ng, H. H. (2006) The Oct4 and Nanog transcription network regulates pluripoten-cy in mouse embryonic stem cells, Nat. Genet., 38, 431–440.

    Article  CAS  PubMed  Google Scholar 

  78. Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L., and McKay, R. D. (2007) New cell lines from mouse epiblast share defin-ing features with human embryonic stem cells, Nature, 448, 196–199.

    Article  CAS  PubMed  Google Scholar 

  79. Chenoweth, J. G., McKay, R. D., and Tesar, P. J. (2010) Epiblast stem cells contribute new insight into pluripotency and gastrulation, Dev. Growth Differ., 52, 293–301.

    Article  CAS  PubMed  Google Scholar 

  80. Chenoweth, J. G., and Tesar, P. J. (2010) Isolation and maintenance of mouse epiblast stem cells, Methods Mol. Biol., 636, 25–44.

    Article  PubMed  Google Scholar 

  81. Gafni, O., Weinberger, L., Mansour, A. A., Manor, Y. S., Chomsky, E., Ben-Yosef, D., Kalma, Y., Viukov, S., Maza, I., Zviran, A., Rais, Y., Shipony, Z., Mukamel, Z., Krupalnik, V., Zerbib, M., Geula, S., Caspi, I., Schneir, D., Shwartz, T., Gilad, S., Amann-Zalcenstein, D., Benjamin, S., Amit, I., Tanay, A., Massarwa, R., Novershtern, N., and Hanna, J. H. (2013) Derivation of novel human ground state naive pluripotent stem cells, Nature, 504, 282–286.

    Article  CAS  PubMed  Google Scholar 

  82. Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., Vega, V. B., Wong, E., Orlov, Y. L., Zhang, W., Jiang, J., Loh, Y. H., Yeo, H. C., Yeo, Z. X., Narang, V., Govindarajan, K. R., Leong, B., Shahab, A., Ruan, Y., Bourque, G., Sung, W. K., Clarke, N. D., Wei, C. L., and Ng, H. H. (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells, Cell, 133, 1106–1117.

    Article  CAS  PubMed  Google Scholar 

  83. Cole, M. F., Johnstone, S. E., Newman, J. J., Kagey, M. H., and Young, R. A. (2008) Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells, Genes Dev., 22, 746–755.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Frum, T., Halbisen, M. A., Wang, C., Amiri, H., Robson, P., and Ralston, A. (2013) Oct4 cell-autonomously pro-motes primitive endoderm development in the mouse blas-tocyst, Dev. Cell, 25, 610–622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Le Bin, G. C., Munoz-Descalzo, S., Kurowski, A., Leitch, H., Lou, X., Mansfield, W., Etienne-Dumeau, C., Grabole, N., Mulas, C., Niwa, H., Hadjantonakis, A. K., and Nichols, J. (2014) Oct4 is required for lineage priming in the developing inner cell mass of the mouse blastocyst, Development, 141, 1001–1010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wu, G., Han, D., Gong, Y., Sebastiano, V., Gentile, L., Singhal, N., Adachi, K., Fischedick, G., Ortmeier, C., Sinn, M., Radstaak, M., Tomilin, A., and Scholer, H. R. (2013) Establishment of totipotency does not depend on Oct4A, Nat. Cell Biol., 15, 1089–1097.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Pain, B., Clark, M. E., Shen, M., Nakazawa, H., Sakurai, M., Samarut, J., and Etches, R. J. (1996) Long-term in vitro culture and characterization of avian embryonic stem cells with multiple morphogenetic potentialities, Development, 122, 2339–2348.

    CAS  PubMed  Google Scholar 

  88. Hong, N., He, B. P., Schartl, M., and Hong, Y. (2013) Medaka embryonic stem cells are capable of generating entire organs and embryo-like miniatures, Stem Cells Dev., 22, 750–757.

    Article  CAS  PubMed  Google Scholar 

  89. Hong, Y., Winkler, C., and Schartl, M. (1996) Pluripotency and differentiation of embryonic stem cell lines from the medakafish (Oryzias latipes), Mech. Dev., 60, 33–44.

    Article  CAS  PubMed  Google Scholar 

  90. Hong, Y., Winkler, C., and Schartl, M. (1998) Production of medakafish chimeras from a stable embryonic stem cell line, Proc. Natl. Acad. Sci. USA, 95, 3679–3684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. 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.

    Article  CAS  PubMed  Google Scholar 

  92. Maherali, N., Sridharan, R., Xie, W., Utikal, J., Eminli, S., Arnold, K., Stadtfeld, M., Yachechko, R., Tchieu, J., Jaenisch, R., Plath, K., and Hochedlinger, K. (2007) Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution, Cell Stem Cell, 1, 55–70.

    Article  CAS  PubMed  Google Scholar 

  93. Pijnappel, W. W., Esch, D., Baltissen, M. P., Wu, G., Mischerikow, N., Bergsma, A. J., Van der Wal, E., Han, D. W., Bruch, H., Moritz, S., Lijnzaad, P., Altelaar, A. F., Sameith, K., Zaehres, H., Heck, A. J., Holstege, F. C., Scholer, H. R., and Timmers, H. T. (2013) A central role for TFIID in the pluripotent transcription circuitry, Nature, 495, 516–519.

    Article  PubMed  CAS  Google Scholar 

  94. Ichida, J. K., Blanchard, J., Lam, K., Son, E. Y., Chung, J. E., Egli, D., Loh, K. M., Carter, A. C., Di Giorgio, F. P., Koszka, K., Huangfu, D., Akutsu, H., Liu, D. R., Rubin, L. L., and Eggan, K. (2009) A small-molecule inhibitor of tgf-β signaling replaces sox2 in reprogramming by inducing Nanog, Cell Stem Cell, 5, 491–503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. 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., Slukvin, I. I., and Thomson, J. A. (2007) Induced pluripotent stem cell lines derived from human somatic cells, Science, 318, 1917–1920.

    Article  CAS  PubMed  Google Scholar 

  96. Montserrat, N., Nivet, E., Sancho-Martinez, I., Hishida, T., Kumar, S., Miquel, L., Cortina, C., Hishida, Y., Xia, Y., Esteban, C. R., and Izpisua Belmonte, J. C. (2013) Reprogramming of human fibroblasts to pluripotency with lineage specifiers, Cell Stem Cell, 13, 341–350.

    Article  CAS  PubMed  Google Scholar 

  97. Shu, J., Wu, C., Wu, Y., Li, Z., Shao, S., Zhao, W., Tang, X., Yang, H., Shen, L., Zuo, X., Yang, W., Shi, Y., Chi, X., Zhang, H., Gao, G., Shu, Y., Yuan, K., He, W., Tang, C., Zhao, Y., and Deng, H. (2013) Induction of pluripotency in mouse somatic cells with lineage specifiers, Cell, 153, 963–975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Rossello, R. A., Chen, C. C., Dai, R., Howard, J. T., Hochgeschwender, U., and Jarvis, E. D. (2013) Mammalian genes induce partially reprogrammed pluripo-tent stem cells in non-mammalian vertebrate and inverte-brate species, eLife, 2, e00036.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Duboule, D., and Morata, G. (1994) Collinearity and functional hierarchy among genes of the homeotic com-plexes, Trends Genet., 10, 358–364.

    Article  CAS  PubMed  Google Scholar 

  100. Raff, R. A. (1996) The Shape of Life: Genes, Development and the Evolution of Animal Form, Chicago Press.

    Google Scholar 

  101. Sander, K. (1976) Specification of the basic body plan in insect embryogenesis, Adv. Insect Physiol., 12, 125–238.

    Article  Google Scholar 

  102. Domazet-Loso, T., and Tautz, D. (2010) A phylogeneti-cally based transcriptome age index mirrors ontogenetic divergence patterns, Nature, 468, 815–818.

    Article  CAS  PubMed  Google Scholar 

  103. Kalinka, A. T., and Tomancak, P. (2012) The evolution of early animal embryos: conservation or divergence? Trends Ecol. Evol., 27, 385–393.

    Article  PubMed  Google Scholar 

  104. Piasecka, B., Lichocki, P., Moretti, S., Bergmann, S., and Robinson-Rechavi, M. (2013) The hourglass and the early conservation models–co-existing patterns of develop-mental constraints in vertebrates, PLoS Genet., 9, e1003476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Kunarso, G., Chia, N. Y., Jeyakani, J., Hwang, C., Lu, X., Chan, Y. S., Ng, H. H., and Bourque, G. (2010) Transposable elements have rewired the core regulatory network of human embryonic stem cells, Nat. Genet., 42, 631–634.

    Article  CAS  PubMed  Google Scholar 

  106. Xie, D., Chen, C. C., Ptaszek, L. M., Xiao, S., Cao, X., Fang, F., Ng, H. H., Lewin, H. A., Cowan, C., and Zhong, S. (2010) Rewirable gene regulatory networks in the preimplantation embryonic development of three mam-malian species, Genome Res., 20, 804–815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Fernandez-Tresguerres, B., Canon, S., Rayon, T., Pernaute, B., Crespo, M., Torroja, C., and Manzanares, M. (2010) Evolution of the mammalian embryonic pluripotency gene regulatory network, Proc. Natl. Acad. Sci. USA, 107, 19955–19960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Vastenhouw, N. L., Zhang, Y., Woods, I. G., Imam, F., Regev, A., Liu, X. S., Rinn, J., and Schier, A. F. (2010) Chromatin signature of embryonic pluripotency is estab-lished during genome activation, Nature, 464, 922–926.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Lindeman, L. C., Andersen, I. S., Reiner, A. H., Li, N., Aanes, H., Ostrup, O., Winata, C., Mathavan, S., Muller, F., Alestrom, P., and Collas, P. (2011) Prepatterning of developmental gene expression by modified histones before zygotic genome activation, Dev. Cell, 21, 993–1004.

    Article  CAS  PubMed  Google Scholar 

  110. Lunde, K., Belting, H. G., and Driever, W. (2004) Zebrafish pou5f1/pou2, homolog of mammalian Oct4, functions in the endoderm specification cascade, Curr. Biol., 14, 48–55.

    Article  CAS  PubMed  Google Scholar 

  111. Okuda, Y., Ogura, E., Kondoh, H., and Kamachi, Y. (2010) B1 SOX coordinate cell specification with pattern-ing and morphogenesis in the early zebrafish embryo, PLoS Genet., 6, e1000936.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Reim, G., and Brand, M. (2006) Maternal control of ver-tebrate dorsoventral axis formation and epiboly by the POU domain protein Spg/Pou2/Oct4, Development, 133, 2757–2770.

    Article  CAS  PubMed  Google Scholar 

  113. Reim, G., Mizoguchi, T., Stainier, D. Y., Kikuchi, Y., and Brand, M. (2004) The POU domain protein spg (pou2/Oct4) is essential for endoderm formation in coop-eration with the HMG domain protein casanova, Dev. Cell, 6, 91–101.

    Article  CAS  PubMed  Google Scholar 

  114. Xu, C., Fan, Z. P., Muller, P., Fogley, R., Dibiase, A., Trompouki, E., Unternaehrer, J., Xiong, F., Torregroza, I., Evans, T., Megason, S. G., Daley, G. Q., Schier, A. F., Young, R. A., and Zon, L. I. (2012) Nanog-like regulates endoderm formation through the Mxtx2-Nodal pathway, Dev. Cell, 22, 625–638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Morrison, G. M., and Brickman, J. M. (2006) Conserved roles for Oct4 homologues in maintaining multipotency during early vertebrate development, Development, 133, 2011–2022.

    Article  CAS  PubMed  Google Scholar 

  116. Lavial, F., Acloque, H., Bertocchini, F., Macleod, D. J., Boast, S., Bachelard, E., Montillet, G., Thenot, S., Sang, H. M., Stern, C. D., Samarut, J., and Pain, B. (2007) The Oct4 homologue PouV and Nanog regulate pluripotency in chicken embryonic stem cells, Development, 134, 3549–3563.

    Article  CAS  PubMed  Google Scholar 

  117. Dixon, J. E., Allegrucci, C., Redwood, C., Kump, K., Bian, Y., Chatfield, J., Chen, Y. H., Sottile, V., Voss, S. R., Alberio, R., and Johnson, A. D. (2010) Axolotl Nanog activity in mouse embryonic stem cells demon-strates that ground state pluripotency is conserved from urodele amphibians to mammals, Development, 137, 2973–2980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Theunissen, T. W., Costa, Y., Radzisheuskaya, A., Van Oosten, A. L., Lavial, F., Pain, B., Castro, L. F., and Silva, J. C. (2011) Reprogramming capacity of Nanog is func-tionally conserved in vertebrates and resides in a unique homeodomain, Development, 138, 4853–4865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Theunissen, T. W., Van Oosten, A. L., Castelo-Branco, G., Hall, J., Smith, A., and Silva, J. C. (2011) Nanog over-comes reprogramming barriers and induces pluripotency in minimal conditions, Curr. Biol., 21, 65–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Tapia, N., Reinhardt, P., Duemmler, A., Wu, G., Arauzo-Bravo, M. J., Esch, D., Greber, B., Cojocaru, V., Rascon, C. A., Tazaki, A., Kump, K., Voss, R., Tanaka, E. M., and Scholer, H. R. (2012) Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins, Nat. Commun., 3, 1279.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Davidson, E. H., and Erwin, D. H. (2006) Gene regulato-ry networks and the evolution of animal body plans, Science, 311, 796–800.

    Article  CAS  PubMed  Google Scholar 

  122. Ding, J., Xu, H., Faiola, F., Ma’ayan, A., and Wang, J. (2012) Oct4 links multiple epigenetic pathways to the pluripotency network, Cell Res., 22, 155–167.

    Article  CAS  PubMed  Google Scholar 

  123. Van den Berg, D. L., Snoek, T., Mullin, N. P., Yates, A., Bezstarosti, K., Demmers, J., Chambers, I., and Poot, R. A. (2010) An Oct4-centered protein interaction network in embryonic stem cells, Cell Stem Cell, 6, 369–381.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Yanes, O., Clark, J., Wong, D. M., Patti, G. J., Sanchez-Ruiz, A., Benton, H. P., Trauger, S. A., Desponts, C., Ding, S., and Siuzdak, G. (2010) Metabolic oxidation regulates embryonic stem cell differentiation, Nat. Chem. Biol., 6, 411–417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Developmental Biology Unit, University of Freiburg, Biologie 1, 79194, Freiburg, Germany

    D. V. Onichtchouk

  2. Research Center of Biotechnology RAS (Bach Institute of Biochemistry), 119071, Moscow, Russia

    A. S. Voronina

Authors
  1. D. V. Onichtchouk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. S. Voronina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. V. Onichtchouk.

Additional information

Original Russian Text © D. V. Onichtchouk, A. S. Voronina, 2015, published in Uspekhi Biologicheskoi Khimii, 2015, Vol. 55, pp. 197-222.

An erratum to this article is available at http://dx.doi.org/10.1134/S0006297916130137.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Onichtchouk, D.V., Voronina, A.S. Regulation of Zygotic Genome and Cellular Pluripotency. Biochemistry Moscow 80, 1723–1733 (2015). https://doi.org/10.1134/S0006297915130088

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297915130088

Key words

Search

Navigation